First occurrence of Panthera atrox (Felidae, Pantherinae) in the Mexican state of Hidalgo and a review of the record of felids from the Pleistocene of Mexico Author Bravo-Cuevas, Victor Manuel Jaime Priego-Vargas & Marco Antonio Pineda Maldonado & Museo de Paleontología,`rea AcadØmica de Biología, Universidad Autónoma del Estado de Hidalgo, Ciudad del Conocimiento, Carretera Pachuca-Tulancingo km 4.5, CP 42184, Pachuca, Hidalgo, Mexico Author Priego-Vargas, Jaime Miguel`ngel Cabral-Perdomo & AcadØmica de Biología, Doctorado en Biodiversidad y Conservación, Universidad Autónoma del Estado de Hidalgo, Ciudad del Conocimiento, Carretera Pachuca-Tulancingo km 4.5, CP 42184, Pachuca, Hidalgo, Mexico Author Cabral-Perdomo, Miguel`ngel Jaime Priego-Vargas & Marco Antonio Pineda Maldonado & Museo de Paleontología,`rea AcadØmica de Biología, Universidad Autónoma del Estado de Hidalgo, Ciudad del Conocimiento, Carretera Pachuca-Tulancingo km 4.5, CP 42184, Pachuca, Hidalgo, Mexico Author Maldonado, Marco Antonio Pineda AcadØmica de Biología, Maestría en Biodiversidad y Conservación, Universidad Autónoma del Estado de Hidalgo, Ciudad del Conocimiento, Carretera Pachuca-Tulancingo km 4.5, CP 42184, Pachuca, Hidalgo, Mexico text Fossil Record 2016 2016-07-20 19 2 131 141 http://dx.doi.org/10.5194/fr-19-131-2016 journal article 298390 10.5194/fr-19-131-2016 31edc4a0-986a-4bf9-ab81-60803deeb386 2193-0074 11588541 – Panthera atrox Leidy, 1853 Referred material. El Barrio locality: UAHMP-4221, left lower canine; UAHMP-4222, left fifth metacarpal. Distribution and age. The American lion was widely distributed across North America from Alaska ( Whitmore and Foster, 1967 ) to southern Mexico ( Montellano-Ballesteros and Carbot-Chanona, 2009 ; Carbot-Chanona and Gómez-PØrez, 2014 ); some records from Alaska and western Canada maybe represent members that are more closely related to the cave lion ( P. spelaea ) ( Barnett et al., 2009 ). It is a taxon limited to the Rancholabrean NALMA (Kurten and Anderson, 1980; Lange, 2002 ). 4.1 Description The canine UAHMP-4221 is large and robust ( Table 1 ). A thin layer of enamel (< 1 mm thick) covers the first third of the tooth. The tip has broken anterolaterally after death (given that it does not show wear) and is subacute in shape. The specimen is moderately curved, and in cross section it is oval to oval-elongate toward to the base. The lateral surface of the tooth is slightly convex, whereas the medial surface is flattened ( Fig. 2 ). The metacarpal UAHMP-4222 is slender and long, showing a relatively gracile appearance ( Table 2 , Fig. 3 ). The shaft is oval in cross section and without sharply defined borders between the dorsal and palmar surfaces. At the proximal end, the articular surface for the unciform is narrow. The medial face presents the articular surface for metacarpal IV, formed by a large projection (“ear-shaped projection” of Merriam and Stock, 1932 ) and a narrow notch placed on the palmar side. The lateral surface presents a convex tuberosity. At the distal end, the lateral tuberosity is more prominent than the medial tuberosity. The distal articulation surface is situated at a 10 ◦ angle from the axis of the shaft and a prominent palmar keel is apparent. 4.2 Taxonomic assessment The deciduous lower canine of felids is distinguished by having an accessory cusp situated on the anterolingual side of the tooth ( Salles, 1992 ). The specimen UAHMP-4221 does not show this condition, indicating that it is a permanent tooth; furthermore, it resembles the lower canine of pantherines in the absence of a lingual cavity (a widespread condition among felids), and differs from an upper canine in the absence of a lingual ridge ( Salles, 1992 ) and in being more robust. By contrast, the lower canine of Smilodon is smaller and slender, strongly curved, and shows a median lateral ridge ( Merriam and Stock, 1932 ). Table 1. Comparison of measurements (in mm) in UAHMP-4221 and lower canine specimens of Panthera atrox (a–d) and the extant species P. tigris (e) and P. leo (f). Rancholabrean localities: (a) El Barrio, southeastern Hidalgo, central Mexico (present study); (b) Lost Chicken Creek, Alaska, United States ( Whitmore and Foster, 1967 : table 1, p. 250); (c) Rancho La Brea, California, United States ( Merriam and Stock, 1932 : table 94, p. 177); and (d) La Tejería, Chiapas, southern Mexico ( Montellano-Ballesteros and Carbot-Chanona, 2009 : table 1, p. 219). Abbreviations: AD, anteroposterior diameter; TD, transverse diameter.

(a)	(b)	(c)	(d)	(e)	(f)
UAHMP-4221	USNM-23619	Rancho La Brea	IHNFG-2678	OCMP-077	OCMP-080
Left	Right	( N = 11)	Right	Left	Right/left
AD	30.1	30.0	21.8–30.4	21.9	20.8	21.0/20.7
TD	21.6	21.5	15.1–21.6	15.6	14.2	13.9/13.7

Table 2. Comparison of measurements (in mm) between UAHMP-4222 and fifth metacarpal specimens of Panthera atrox from Rancho La Brea (RLB), late Pleistocene of California, United States ( Merriam and Stock, 1932 : table 62, p. 134). The observed range in the specimens from Rancho La Brea is in parentheses.

UAHMP-4222	RLB	RLB
Left	Right	Left
Greatest length	105.9	x = 105	x = 106.6
(90.6–115.3)	(91.7–113.0)
Greatest transverse diameter of proximal end	28.4	28.7	x = 27.8
(25.1–27.7)	(24.9–30.0)
Greatest dorsoventral diameter of proximal end	26.8	x = 31.3	x = 29.8
(27.0–30.8)	(27.3–33.2)
Transverse diameter at middle of shaft	17.0	x = 17.0	x = 16.3
(14.2–15.8)	(14.2–17.6)
Dorsoventral diameter at middle of shaft	13.9	x = 15.0	x = 14.1
(13.2–15.2)	(12.2–15.8)
Greatest transverse diameter at distal end of shaft	23.5	x = 24.9	x = 24.8
(21.2–25.2)	(22.2–25.2)

The size of the tooth is comparable to that observed for lower canines belonging to Panthera atrox , including USNM 23619 (right lower jaw with c, p3–m1) from Lost Chicken Creek , Rancholabrean of Fairbanks , Alaska; it falls in the upper limit of the observed range in specimens from Rancho La Brea , California, United States; and it is nearly 25 % larger than the specimen IHNFG-2678 (isolated lower canine) from Chiapas , southern Mexico ( Table 1 ). The difference in size between the specimens from Hidalgo and Chiapas could be explained by intraspecific variation (related to age and/or sex), considering that UAHMP-4221 shows dimensions comparable to the larger lower canines from Rancho La Brea , whereas the dimensions of IHNFG-2678 correspond to those of the smaller ones ( Table 1 ). It should be stated that the specimen UAHMP-4221 is significantly larger (ca. 33 %) than lower canines of Panthera leo and P. tigris ; however, the size of this tooth between those extant species is similar ( Table 1 ). Figure 2. Isolated left lower canine (UAHMP-4221) of Panthera atrox from the late Pleistocene of southeastern Hidalgo, central Mexico. (a) Labial and (b) lingual views. Scale bar equals 2 cm. Figure 3. Left fifth metacarpal (UAHMP-4222) of Panthera atrox from the late Pleistocene of southeastern Hidalgo, central Mexico. (a) Ventral, (b) dorsal, (c) medial, (d) lateral, (e) proximal, and (f) distal views. Scale bar equals 2 cm. Among felids, the morphology of the limb elements is somewhat homogeneous, including the metacarpals. In general, the metacarpal bones of felids are characterized by being short and robust with a broad and curved diaphysis as well as broad proximal and narrow distal ends ( Morales-Mejía and Arroyo-Cabrales, 2012 ). All these features are observed in the specimen UAHMP-4222, indicating its felid condition. In particular, the fifth metacarpal from Hidalgo resembles those of Panthera atrox in the following characters: (1) well-developed projection on the palmar side at the proximal end; (2) the articulating surface for the unciform is narrow; (3) the diaphysis is relatively slender; (4) the notch on the articulating surface for the fourth metacarpal is narrow; and (5) the diaphysis at the middle is oval in cross section ( Merriam and Stock, 1932 ). Furthermore, the size of UAHMP-4222 (greatest length = 105.9 mm) is within the observed range of fifth metacarpals of P. atrox from Rancho La Brea, California , United States ( Table 2 ); however, it is about 25 % larger than the fifth metacarpal of OCMP-077 belonging to P. tigris (greatest length = 80.3 mm). It should be noted that the fifth metacarpal of Smilodon is distinguished in having a poorly developed projection on the palmar side at the proximal end, a broad articulating surface for the unciform, and a relatively stout diaphysis ( Merriam and Stock, 1932 ). The comparative study indicates that the size and morphology of dental and postcranial remains from Hidalgo are closely comparable to those observed in specimens belonging to Panthera atrox . Hence, the studied sample is formally assigned to that large-sized cat species. 5 Paleobiological significance 5.1 Paleoecology The American lion was one of the largest cats that inhabited North America during the late Pleistocene ( KurtØn and Anderson, 1980 ; Lange, 2002 ). Body size estimations indicate that this felid had a mean body mass of 300 kg , ranging from 200 to 400 kg ( Van Valkenburgh et al., 2016 ). It has been observed that prey body size tends to increase with the predator size ( Sinclair et al., 2003 ). Therefore, it should be expected that large mammalian herbivores were common prey of Panthera atrox . Van Valkenburgh et al. (2016 : fig. 2, p. 865) predicted a typical prey size ranging from 60 to 900 kg for the American lion, and the maximum prey size could have been about 1000 kg . Figure 4. Potential common prey-size range for Panthera atrox from the late Pleistocene of southeastern Hidalgo, including the herbivores that have been reported at the El Barrio locality (HGO-47). Diamond and line indicate the mean and observed range of body mass (from Van Valkenburgh et al., 2016 ). Given the above and considering the taxonomic mammalian composition known at the El Barrio locality, it seems that potential prey for Panthera atrox in that site could include adult individuals of llamas ( Hemiauchenia gracilis and Camelops sp. ), deer ( Odocoileus cf. virginianus ), horses ( Equus conversidens ), and even bison ( Bison sp. ); the body mass among these herbivores is estimated to have been 200 to 900 kg ( Fig. 4 ). Hunting in groups increases the upper range of available prey size; consequently, it has been suggested that large-sized Pleistocene cats (such as Panthera atrox ) were able to kill prey with a body mass of about 6000 kg ( Van Valkenburgh et al., 2016 ). Assuming a hunting group behavior and potential presence of other individuals belonging to Panthera atrox at southeastern Hidalgo during the late Pleistocene, it is also probable that adult individuals of glyptodonts ( Glyptotherium floridanum ) and ground sloths ( Paramylodon cf. harlani ), as well as young and/or subadult individuals of proboscideans ( Cuvieronius sp. and Mammuthus sp. ), could represent other, perhaps occasional prey. The American lion was the second largest carnivore in the late Pleistocene ecosystems of North America, exceeded by only the short-faced bear Arctodus simus ( KurtØn and Anderson, 1980 ) . The large size and restricted dietary behavior of Panthera atrox (a carnivore that feeds mostly on meat, i.e., a hypercarnivore) suggest that this extinct cat occupied the top of the trophic chain, considering that both conditions are typical of extant top predators ( Ritchie and Johnson, 2009 ). At the El Barrio locality, it is probable that the individual of P. atrox described here had the ecological role of the top predator, displacing other carnivores of small to medium size, such as the dire wolf ( Canis dirus ) to the mesopredator guild. 5.2 Geographic distribution By the late Pleistocene, the American lion was widely distributed from Alaska to southern Mexico . The earliest known occurrences are from the Sangamonian interglacial stage, including localities in the western of the United States , as well as northern and central Mexico ( KurtØn and Anderson, 1980 ; Van Devender et al., 1985 ), indicating that this large-sized cat reached regions of southern temperate North America in a relatively short time. Subsequently, the American lion spread its distribution to the Great Plains, the Great Basin, the California Coast, the Gulf Coast, and Mexico during the Wisconsinan ( KurtØn and Anderson, 1980 ; Lange, 2002 ). Based on the known geographic distribution of Panthera atrox , it seems that it was a common inhabitant of temperate areas of central-western North America, although it was able to reach tropical areas that now are part of southern Mexico ( Fig. 5 ). Figure 5. Geographic distribution of Panthera atrox in North America during the late Pleistocene (main source: KurtØn and Anderson, 1980 ). The gray silhouette indicates the record from southeastern Hidalgo, central Mexico. Previous to this study, the American lion Panthera atrox has been reported from nine Mexican localities in northern ( La Brisca ( Sonora ); Arroyo-Cabrales et al., 2005), central ( San Josecito ( Nuevo León ), El Cedral ( San Luis Potosí ), El Cedazo ( Aguascalientes ), Chapala–Zacoalco ( Jalisco ), Tequixquiac ( State of Mexico ); Freudenberg, 1910 ; Mooser and Dalquest, 1975 ; Lorenzo and Mirambell, 1981 ; Arroyo-Cabrales and Polaco, 2003 ; Arroyo-Cabrales et al., 2005; Lucas, 2008 ), and southern ( La Simpatía , La Tejería y Villa Corzo ( Chiapas ); Aviaea, 1969 ; Montellano-Ballesteros and Carbot-Chanona, 2009 ; Carbot-Chanona and Gómez-PØrez, 2014 ) areas of the country. The record reported here supplements its presence in central Mexico , specifically in areas that now are part of southeastern Hidalgo . It is noted that most of the localities where Panthera atrox has been reported are located in central Mexico , between 19 and 24 ◦ N at an altitude from 1500 to 2250 m a.s.l. (including El Barrio locality at 2184 m a.s.l. , Hidalgo (present study)), whereas the occurrences in northern ( La Brisca , Sonora ) and southern (Chiapasan localities) Mexico are located at a mean altitude of 750 m a.s.l. ( Fig. 6a ). Figure 6. Mexican Pleistocene localities with records of Panthera atrox , considering (a) a hypsometric base and (b) the Mexican biogeographic corridors (sensu Ceballos et al., 2010 ). Diamond indicates the record from southeastern Hidalgo, central Mexico. Biogeographic corridors: 1, eastern US–Sierra Madre Oriental; 2, western US–Baja California; 3, Rocky Mountains–Sierra Madre Occidental; 4, central US–northern Mexico; 5, Transvolcanic Belt– Sierra Madre del Sur; 6, Tamaulipas–Central America Gulf Lowlands; and 7, Sonora–Central America Pacific Lowlands. According to the major biogeographic corridors of Ceballos et al. (2010) , the records of Panthera atrox from northwestern and central Mexico (including the Hidalgoan record considered in the present study) indicate that this felid used the corridors of the Rocky Mountains– Sierra Madre Occidental and/or central US –northern Mexico , which correspond to the southern Rocky Mountains– Sierra Madre Occidental branch and to the Great Plains– western Chihuahua /Central Plateau corridors, respectively (after Ferrusquía-Villafranca et al., 2010 ). Furthermore, it used the corridor of the Tamaulipas – Central America Gulf Lowlands (i.e., Gulf Coastal Plain corridor (after Ferrusquía-Villafranca et al., 2010 )) for reaching southern tropical areas of the Mexican territory ( Fig. 6b ). 6 Review of the felid record from the Pleistocene of Mexico In Mexico , Pleistocene felid fossils are uncommon and fragmentary. Nevertheless, this group of carnivores was relatively diverse, including seven genera ( Felis , Miracinonyx , Panthera , Puma , Lynx , Leopardus , and Smilodon ) and 11 species ( Felis rexroadensis , Miracinonyx inexpectatus , Panthera atrox , Panthera onca , Puma concolor , Puma yagouaroundi , Lynx rufus , Leopardus pardalis , Leopardus wiedii , Smilodon fatalis , and Smilodon gracilis ) ( Table 3 ). The Mexican record of Pleistocene felids includes 87.5 % and 73.3 % of generic and specific diversity known for North America, respectively. Table 3. The record of felids from the Pleistocene of Mexico. The morphotectonic provinces are those of Ferrusquía-Villafranca (1993). Morphotectonic provinces: NW, Northwestern Plains and Sierras; CH-CO, Chihuahua–Coahuila Plateaus and Ranges; SMOr, Sierra Madre Oriental; CeP, Central Plateau; TMVB, Trans-Mexican Volcanic Belt; GCP, Gulf Coastal Plain; SMS, Sierra Madre del Sur; CHI, Sierra Madre de Chiapas; YPL, Yucatan Platform. Localities: 1, El Golfo (Sonora); 2, La Brisca (Sonora); 3, Terapa (Sonora); 4, Cuatro CiØnegas (Coahuila); 5, Cueva de JimØnez (Chihuahua); 6, Cueva de San Josecito (Nuevo León); 7, El Cedral (San Luis Potosí); 8, Mina San Antonio (San Luis Potosí); 9, El Cedazo (Aguascalientes); 10, Chapala–Zacoalco (Jalisco); 11, Tequixquiac (State of Mexico); 12, Tlapacoya (State of Mexico); 13, Tlailotlacan (State of Mexico); 14, El Barrio (Hidalgo, present study); 15, Valsequillo (Puebla); 16, Mixtequilla (Veracruz); 17, San Agustín (Oaxaca); 18, La Simpatía (Chiapas); 19, La Tejería (Chiapas); 20, Villa Corzo (Chiapas); 21, Cueva de Loltoen (YucatAEn); 22, Hoyo Negro (Quintana Roo).

NW	CH-CO		SMOr			CeP	TMVB		GCP	SMS	CHI	YPL
Taxa	1	2	3	4	5	6	7	8	9	10	11	12	13	14	15	16	17	18	19	20	21	22
Panthera atrox	X	X	X	X	X	X	X	X	X	X
Panthera onca	X	X	X	X	X	X
Panthera cf. P. onca	X
Puma concolor	X	X	X	X	X	X	X	X
Puma yagouaroundi	X	X
Lynx rufus	X	X	X	X	X	X	X	X
Leopardus pardalis	X
Leopardus wiedii	X
Smilodon fatalis	X	X	X	X	X
Smilodon sp.	X
Felis rexroadensis	X
Miracinonyx inexpectatus	X

As far as we know, the only record of felids from the early Pleistocene of Mexico consists of three species ( Felis rexroadensis , Miracinonyx inexpectatus , and Panthera cf. P. onca ) from El Golfo , State of Sonora , in the Northwestern Plains and Sierras morphotectonic province ( Lindsay, 1984 ; Croxen III et al., 2007 ). By contrast, the late Pleistocene record of Mexican felids is represented by at least eight species whose material has been recovered from several localities across the country ( Fig. 7 ). Fossil material that has been referred to Panthera atrox (the American lion), P. onca (jaguar), Lynx rufus (bobcat), Puma concolor (cougar), and Smilodon fatalis (sabertoothed cat) is somewhat numerous. These species are known from several late Pleistocene localities in the following morphotectonic provinces: Northwestern Plains and Sierras ( P. atrox and P. onca ; Arroyo-Cabrales et al., 2005; Ferrusquía-Villafranca et al., 2010 ), Chihuahua – Coahuila Plateaus and Ranges ( P. onca , L. rufus , and P. concolor ; Gilmore, 1947 ; Messing, 1986 ), Sierra Madre Oriental ( P. atrox , P. onca , L. rufus , P. concolor , and S. fatalis ; Lorenzo and Mirambell, 1981 ; Arroyo-Cabrales and`lvarez, 2003; Arroyo-Cabrales et al., 2005, 2010; Ferrusquía-Villafranca et al., 2010 ), Central Plateau ( P. atrox , P. onca , L. rufus , and S. fatalis ; Mooser, 1959 ; Mooser and Dalquest, 1975 ), Trans-Mexican Volcanic Belt ( P. atrox , P. onca , P. concolor , and S. fatalis ; Freudenberg, 1910 ; Aviaea, 1969 ; Rufolo, 1998 ; Lucas, 2008 ; Ferrusquía-Villafranca et al., 2010 ), Gulf Coastal Plain ( P. concolor ; Arroyo-Cabrales et al., 2005; Ferrusquía-Villafranca et al., 2010 ), Sierra Madre del Sur ( P. concolor ; Arroyo-Cabrales et al., 2005; Ferrusquía-Villafranca et al., 2010 ), Sierra Madre de Chiapas ( P. atrox ; Montellano-Ballesteros and Carbot-Chanona, 2009 ; Carbot-Chanona and Gómez-PØrez, 2014 ), and Yucatan Platform ( P. concolor and S. fatalis ;`lvarez and Polaco, 1982; Collins et al., 2015 ). The present study adds an occurrence of Panthera atrox from a late Pleistocene locality in southeastern Hidalgo , central Mexico , within the Trans-Mexican Volcanic Belt morphotectonic province. The species Puma yagouaroundi (jaguarondi) is known from the Sierra Madre Oriental and Yucatan Platform morphotectonic provinces ( Arroyo-Cabrales and Johnson, 1998 ; Arroyo-Cabrales and`lvarez, 2003). By the same token, the species Leopardus pardalis (ocelot) and a saber-tooth cat with an uncertain specific identity (referred to as Smilodon cf. S. gracilis ) have single occurrences from localities in the Yucatan Platform and Trans-Mexican Volcanic Belt morphotectonic provinces, respectively ( KurtØn, 1967 ; Arroyo-Cabrales and`lvarez, 2003; Ferrusquía-Villafranca et al., 2010 ). There is a report of Leopardus wiedii from a site known as Tlailotlacan, late Pleistocene of the State of Mexico (Arroyo-Cabrales et al., 2005, 2010). Furthermore, there are mentions of Smilodon sp. , Panthera sp. , and Lynx sp. from localities in the Sierra Madre Oriental ( Smilodon sp. ; Arroyo-Cabrales et al., 2005) and Trans-Mexican Volcanic Belt morphotectonic provinces ( Smilodon sp. , Panthera sp. , and Lynx sp. ; Arroyo-Cabrales et al., 2005; Bravo-Cuevas et al., 2009 ). Figure 7. Mexican Pleistocene localities with records of felids. The map is regionalized in the morphotectonic provinces of Ferrusquía-Villafranca (1993). Abbreviations of the morphotectonic provinces as in Table 3. Squares indicate the early Pleistocene localities and circles the late Pleistocene localities. The felid record includes the following species: A: Panthera atrox ; B: Panthera onca ; C: Puma concolor ; D: Puma yagouaroundi ; E: Lynx rufus ; F: Leopardus pardalis ; G: Leopardus wiedii ; H: Smilodon fatalis ; I: Smilodon cf. S. gracilis ; J: Felis rexroadensis ; K: Miracinonyx inexpectatus . Clearly, felids were more diverse and widespread in their geographic distribution across the Mexican territory during the late Pleistocene. There are several areas in northern, central, and southern Mexico that testify to the presence of three to four species of felids, including Cuatro CiØnegas, Coahuila ( P. onca , P. concolor , and L. rufus ); El Cedazo , Aguascalientes ( P. atrox , P. onca , L. rufus , and S. fatalis ); Chapala–Zacoalco, Jalisco ( P. atrox , P. onca , P. concolor , and S. fatalis ), Tequixquiac, State of Mexico ( P. atrox , L. rufus , and S. fatalis ); and Cueva de Loltoen , YucatAEn, ( P. concolor , P. yagouaroundi , and L. pardalis ). The San Josecito Cave locality testifies to the presence of six species of felids. It is probable that the high diversity recorded there should be related to the nature of the site, which functioned as a shelter for maternity, resting, and/or feeding of several carnivore groups, including felids (Arroyo-Cabrales and`lvarez, 2003).