Journal of Mammalian Evolution https://doi.org/10.1007/s10914-022-09600-0 ORIGINAL PAPER Middle Pleistocene Steppe Lion Remains from Grotte de la Carrière (Têt Valley, Eastern Pyrenees) Maria Prat‑Vericat1 · Adrian Marciszak2 · Isaac Rufí3 · Leonardo Sorbelli1 · Manel Llenas1,4,5 · Saverio Bartolini Lucenti6,7 · Joan Madurell‑Malapeira1,4,5 Accepted: 7 January 2022 © The Author(s) 2022 Abstract Late Pleistocene cave lions are one of the most iconic species of Northern Hemisphere Quaternary taphocoenoses. Despite their often-scarce record in cave environments, their ubiquitous distribution across Eurasia and North America assemblages attests to their position as top ice-age predators. Nevertheless, the origins of these former large felids, their distribution during the Middle Pleistocene, and their paleoecology during co-existence with the scimitar- toothed cat Homotherium remain debated. Here we describe for the first time an abundant collection of large-sized and stout felid remains from the recently discovered site of Grotte de la Carrière in Eastern Pyrenees, with an estimated age corresponding to MIS 9. Our results highlight the larger size of Middle Pleistocene lions compared to Late Pleistocene ones as well as a trend of decreasing in size, which has been previously stated by other authors. Grotte de la Carrière steppe lions have similar morphological and biometrical parameters to those of other samples from MIS 11–9, being larger and stouter than younger latest Middle Pleistocene-Late Pleistocene forms and slightly smaller than older MIS 15–12 forms. Keywords Pleistocene · Quaternary · Pyrenees · Carnivore · Felidae · Panthera fossilis Introduction The Earliest Lions and their European Record * Joan Madurell‑Malapeira Nowadays, the African lion (Panthera leo) lives mainly in joan.madurell@icp.cat scattered populations across Sub-Saharan Africa (Stuart 1 Institut Català de Paleontologia Miquel Crusafont, and Lister 2011; Bellani 2020). However, Middle to Late Universitat Autònoma de Barcelona, Edifici ICTA-ICP, C/ Pleistocene lions were one of the most widely distributed de Les Columnes S/N Campus de La UAB, Cerdanyola del terrestrial carnivores (Kahlke 1999; Barnett et al. 2009; Vallès, 08193 Barcelona, Spain Stuart and Lister 2011; Bellani 2020), being recorded in 2 Department of Paleozoology, Faculty of Biological Sciences, Europe, Asia, and North America in the Late Pleistocene University of Wrocław, Sienkiewicza 21, 50‑335 Wrocław, under different Panthera specific attributions, such as Pan- Poland thera spelaea, P. fossilis, P. intermedia, and P. atrox. Since 3 Departament d’Història i Història de l’Art, Universitat de the split of their ancestors in eastern Africa, which has Girona, Pl. Ferrater Mora, 1, 17004 Girona, Spain been dated to the earliest Early Pleistocene (ca. 2.5 Ma) 4 Secció Villalta, Federació Catalana d’Espeleologia, c\ del (Werdelin and Lewis 2005; Argant et al. 2007; Sabol Mas Casanovas 66, 08025 Barcelona, Spain 2011), lions spread over the Holarctic domain, where they 5 Conflent Spéléo Club, 4, Traverse Des Fabriques, became one of the top predators of the European carnivore 66500 Prades de Conflent, France guild (Turner 2009; Lewis et al. 2010; Bocherens et al. 6 Dipartimento Di Scienze Della Terra, Università Di Firenze, 2011). They survived until the early Holocene, when the Via G. La Pira 4, 50121 Firenze, Italy last cave lion lineage went extinct ca. 12 ka (Stuart and 7 Museo Di Storia Naturale, Università Degli Studi Di Firenze, Lister 2011). Via la Pira, 50121 Firenze, Italy 13 Vol.:(0123456789) Journal of Mammalian Evolution Historically, the Middle Pleistocene lion fossil record is of two valid chronospecies: Panthera fossilis (von Reichenau, not as well-known as the Late Pleistocene one due to the 1906) and Panthera spelaea (Goldfuss, 1810) (Sotnikova and scarcity of Middle Pleistocene sites. Sites have mainly been Nikolskiy 2006; Sabol 2014; Barnett et al. 2016). Other schol- known in Southern and Central Europe (Fig. 1) such as ars regard both of these species as subspecies of P. spelaea Breccia de Château (Argant 1988) and Mauer and Mosbach (Argant et al. 2007; Barycka 2008; Marciszak and Stefaniak (Schütt and Hemmer 1978). This scantiness does not help 2010). Recent DNA studies reveal that the cave lion putatively clarify the evolutionary history of Pleistocene lions. The first dispersed over Europe ca. 600 ka after becoming isolated from documented Eurasian lions come from Pakefield (ca. 750 ka; Asian and African populations (Burger et al. 2004; Barnett Lewis et al. 2010), Kozi Grzbiet (ca. 750 ka; Marciszak et al. et al. 2009) and diverged from modern lions around 1.89 Ma 2021), and Isernia la Pineta (ca. 650 ka; Sala 1990). Recent (Barnett et al. 2016), becoming a clear monophyletic outgroup paleontological works have pointed to eastern Africa as (Barnett et al. 2016; deManuel et al. 2020). Other more recent the origin of lion dispersion around 800 ka (Argant 1991; studies have supported the existence of three different clades Burger et al. 2004; Argant et al. 2007; Sabol 2011). How- of cave lions that diverged from extant species ca. 1.85 Ma. ever, the presence of lions in the latest Early Pleistocene of One of these clades was putatively restricted to Beringia, Iberia (i.e., Vallparadís Section and Cueva Victoria, Spain) while others were prevalent in Eurasia (Stanton et al. 2021). suggests that the complex history of European lions may Despite everything, it seems to be clear that P. fossilis have started earlier (Madurell-Malapeira et al. 2014, 2017). spread to Central and Eastern Europe and dispersed across Furthermore, an entrance from Western Siberia should not mountain areas during marine isotopic stages (MIS) 17–12 be ruled out, as Sotnikova and Foronova (2014) recently (Sabol 2011), dominating them until MIS 10–9. Then, P. described P. fossilis in the Kuznetsk Basin (Russia) at ca. fossilis was progressively replaced by P. spelaea (Argant 1.0 Ma. 2010; Baryshnikov and Tsoukala 2010; Marciszak et al. Unfortunately, the taxonomy of the cave lion lineage still 2014). According to Marciszak and Stefaniak (2010), the generates debate in the scientific community (Sabol 2011; replacement occurred around MIS 7-5e. However, fossil Marciszak et al. 2014). According to some authors, skull specimens of lions belonging to MIS 9–6 present inter- similarities with modern lions indicate that the Pleistocene mediate characteristics (Marciszak et al. 2014; Argant and forms are a large extinct subspecies of P. leo (Ballesio 1975, Brugal 2017). Argant and Brugal (2017) identify the fossil 1980; Turner 1984). In contrast, others support the existence record from Igue-de-Rameaux (MIS 9–7) as P. l. intermedia. Fig. 1  Grotte de la Carrière geographical location and European distribution of Middle and Late Pleistocene fossiliferous sites mentioned in the text 13 Journal of Mammalian Evolution Nevertheless, as indicated by European regional differences, addition to sexual dimorphism and the scantiness of fos- the replacement probably occurred during a different span sil record, constrain attempts to correctly resolve phylo- of time. genetic relationships (Schütt 1969; Turner 1984; Argant All these phylogenetic problems are partly a con- et al. 2007; Diedrich 2011; Christiansen and Harris 2012; sequence of the high adaptability of European lions to Marciszak et al. 2014, 2017; Sabol et al. 2018). diverse environmental conditions and biomes (Sabol The field surveys performed the last five years in the et al. 2018). Following this interpretation, it seems plau- newly discovered site of Grotte de la Carrière inside the sible that P. fossilis was distributed throughout European Reséau Lachambre (Têt Valley, Eastern Pyrenees) have lands (Fig. 1), inhabiting a great variety of biotopes, from provided new Middle Pleistocene lion material chrono- open lowlands and woodlands to mountainous boreal for- logically constrained to MIS 9 (Fig. 2) and previously ten- est (Turner 2009; Baryshnikov 2011; Sabol et al. 2018). tatively attributed to P. fossilis (Madurell-Malapeira and Their large size qualifies them to be predators of a wide Llenas 2018, 2019; Prat-Vericat et al. 2019, 2020). The prey spectrum, including large-sized herbivores and occa- aim of the present paper is to provide a detailed descrip- sionally cave bears (Hemmer 2004; Baryshnikov 2011; tion of all unearthed specimens, determine their morpho- Bocherens et al. 2011; Diedrich 2011; Stuart and Lister logical and taxonomical position close to the latest known 2011; van Valkenburgh et al. 2016). In general, regional occurrences of P. fossilis, and report new knowledge about differences attributed to habitat and prey availability, in the paleobiology of this European Lion. Fig. 2  Grotte de la Carrière topography, stratigraphy, and chronology of Sondage 1 and 2. Below on the right shows a picture of Sondage 1 layer 4 squares C6 and C5 in the 2020 field season 13 Journal of Mammalian Evolution Les Gorges de Villefranche and the Réseau according to Alps glacial stages (Fig. 3): Günz (MIS 15–12), Lachambre Mindel (MIS 11–9), Riss (MIS 8–6), and Würm (MIS 5e-2). This classification follows Marciszak et al. (2021) and has Les Gorges de Villefranche are an important karst system been done to minimize the influence of climatic events and in the Têt Valley (Eastern Pyrenees, France) composed of the imprecise dating of old publications on phylogenetic three large cave networks located in the surroundings of interpretations. The most significant division is MIS 11–9, the Villefranche-de-Conflent village: R. d’en Gorner, R. de which spans the mid-Brunhes transition (MBT; ca. 430 ka), Fullà-Canaletes, and R. Lachambre (Madurell-Malapeira when climatic fluctuations could have impacted middle Mid- et al. 2019). Since 2011, the paleontological richness from dle Pleistocene lions’ evolutionary trends. Similarly, the the three karstic systems was highlighted by Federació Cata- Late Pleistocene sample includes several phases of climatic lana d’Espeologia (FCE) and Institut Català de Paleontolo- oscillations. Unfortunately, we cannot divide the interval gia Miquel Crusafont (ICP) in a project led by M. Ll. and J. from MIS 5 to MIS 2 because of the lack of fossil records. M.-M., also members of the Conflent Spéléo Club de Prades. The sample includes metric data from the fossil sites listed The surveys provided an exceptional quantity of paleonto- below, which are grouped by age. To avoid confusion, P. l. logical material from different caves that is chronologi- intermedia from Igue-de-Rameaux have been placed with cally constrained from the Middle to the Late Pleistocene the “spelaea” group. (Madurell-Malapeira et al. 2015). The Reséau Lachambre, located in the surroundings of Middle Middle Pleistocene (MIS 15–12; 712–424 ka) P. Villefranche-de-Conflent village, is a karstic system with fossilis: Tunnel Wielki (Marciszak et al. 2019), Mosbach more than 25 km of galleries and several accessory cavi- (Hemmer and Schütt 1970), Breccia de Château (Argant ties (Madurell-Malapeira and Llenas 2018). In one of its 1991; Argant et al. 2007), Westbury (Bishop 1982), Caune accessory caves, namely Grotte de la Carrière, five system- de l’Arago (Testu 2006), Mauer (Hemmer and Schütt 1970), atic excavations recovered more than 8,000 well-preserved Scharzfeld (= Unicorn cave; Schütt 1969; Hemmer and large mammal remains in two distinct stratigraphic Sondages Schütt 1970) and Stránská Skala (Thenius 1972), Moggaster (Prat-Vericat et al. 2019, 2020). (Groiss 1992). The cavity located at 540 m of altitude and 75 m above the Lachambre main cave is a Middle to Late Pleistocene Late Middle Pleistocene Steppe Lion (MIS 11–9; 424– cave that was inhabited by the cave bear Ursus deningeri in 300 ka) P. fossilis: Moggaster (Groiss 1992), Scharzfeld the lower layers (Sondage 1) and Ursus spelaeus in Sondage (= Unicorn cave; Schütt 1969; Hemmer and Schütt 1970), 2 (Madurell-Malapeira and Llenas 2019; Prat-Vericat et al. Lunel-Viel (Bonifay 1971), Petralona (Baryshnikov and 2020). According to preliminary data, the lion remains have Tsoukala 2010), Zernavá (Musil 1969), Vértesszölös II been found in the lower layers of Sondage 1 (Fig. 2) in asso- (Hankó 2007), Aldène (Testu 2006), Trinchera Dolina ciation with Middle Pleistocene assemblage (ca. 0.3 Ma; TD10-11 (Garcia 2003), Za Hajovnou cave (Sabol 2014), MIS 9; López-García et al. 2016; Madurell-Malapeira and Biśnik Cave (layers 19ad-19) Marciszak and Stefaniak Llenas 2018). 2010); P. spelaea: Orgnac (Testu 2006), Sima de los Huesos (Garcia 2003), Kent’s Cavern (Proctor et al. 2005), Torre in Pietra (lower layers; Caloi and Palombo 1978). Material and Methods Late Middle Pleistocene (MIS 8–6; 300–130 ka) P. spelaea: Material Wierzchowska (Marciszak et al. 2019), Verzé (Bonifay 1971; Testu 2006), Igue-de-Rameaux (= P. l. intermedia, Argant and All the specimens described herein were restored by the Brugal 2017), Paks (Hankó 2007), Abimes de la Fage (Ballesio preparation lab team of the Institut Català de Paleontologia 1975), Azé I-3 (Argant 1991), Solymar (Hankó 2007), Lherm Miquel Crusafont (ICP, Spain) and are under supervision of (Filhol and Filhol 1871; Testu 2006), Romain-la-Roche (Argant the Direction Regionalle des Affaires Culturelles (DRAC) 2010; Guérin et al. 2010), Santenay (Argant 1991). of Occitanie (Montpellier, France) and the Conflent Spéléo Club de Prades and housed in Prades-de-Conflent (Occitaine, Late Pleistocene (MIS 5e‑2; 130–14 ka) P. spelaea: Baume France). Longue (Bonifay 1971), Jaurens (Ballesio 1980), Rübeland The material has been compared to several lion spe- (Baryshnikov 2016), Chlum (Baryshnikov 2016), Willendorf cies from Eurasia (Panthera leo, P. spelaea, P. fossilis, and (Thenius 1959), Slöuperhöhle (Zapfe 1966), Baia de Fier P. intermedia) on the basis of published descriptions and (Terzea 1965), Kudaro 1–3 (Baryshnikov and Tsoukala measurements (Online Resource 1, Tables S1–S4). The fos- 2010), Zoolithen (Ghezzo 2014; Testu 2006), Equi and sil sample has been classified into four paleoclimatic ages Grotta Poccala (Ghezzo 2014), Vindja (Testu 2006), Balve 13 Journal of Mammalian Evolution Fig. 3  Biochronological position of the European sites mentioned in the text and the chronological record of Panthera fossilis and Panthera spe- laea. The orange squares mark the relevant Middle Pleistocene interglacials and Bilstein cave (Diedrich 2011), Torca del Léon (Álvarez- Methods Lao et al. 2020), Lezetxiki VI (Altuna 1972), Arrikrutz (Altuna 1972), Reclau Viver (Crusafont-Pairó and The statistical approach for the systematic classification of Casajuana 1950). Grotte de la Carrière (GDC) individuals was based on clas- sic morphometric analyses performed from dental mor- In addition, measurements of North American Late phology and represented by bivariate graphs and boxplot Pleistocene P. atrox from Rancho La Brea (ca. 0.4 ka) performed in PAST v. 3 (Hemmer et al. 2001). We follow housed at the George C. Page Museum (La Brea Tar Pits, Schmid (1940) for terminology (dental and osteological) Los Angeles, USA) and extant Panthera leo from Royal and the measurements taken with a digital caliper to the Museum for Central Africa (Tervuren, Belgium) were nearest 0.1 mm (Fig. 4; Table 1). To test the normal distri- used for the analysis (Tables S3–S4). bution of the analyzed variables such as the homogeneity 13 Journal of Mammalian Evolution Fig. 4  Morphological param- eters for the lower dentition mentioned in the text of variance across the groups, a Shapiro–Wilk test was The Mann–Whitney test was run to determinate the sta- carried out on data sets including at least two specimens. tistical relevance for the astragalus (n = 3). Additionally, Finally, we test the variables that showed significant inter- we tested how several dimensions are affected by sexual group differences in a one-way ANOVA (for parametric dimorphism in various skeletal elements throughout a one- groups of dental specimens) or Mann–Whitney pairwise way ANOVA for parametric groups. Finally, we tested the (for non-parametric groups of post-cranial specimens). putative climatic and regional differences throughout time Table 1  Cranial and postcranial Element Record number L W Lpr Lpa Hpr measurements in mm of Panthera fossilis from Grotte p3 GDC2016-D6-225-Nv6 22.7 12.4 12.2 de la Carrière S1. See text for GDC2016-B5-29-Nv1 22 12.6 anatomical and measurement abbreviations p4 GDC2016-B4-Nv1 32.5 16.7 14.6 GDC2015-Pou-268 16.8 16.9 m1 GDC2015-Pou-176 30.6 16.3 17.7 16.6 GDC2016-D6-64-Nv6 31.7 17.1 18.5 17.4 18.1 Element Record number TL PDap PDtr MDap MDtr DDap DDtr Mtc II GDC-D5-545-Nv4 124.5 37.3 29.5 21.3 20.1 27.5 28.2 GDC-D6-216-Nv6 117.4 36.9 27.7 21.3 20.7 25.2 25.9 GDC-D6-137-Nv8 111.3 27.7 20.7 19.7 Mtc III GDC-D7-21-Nv4 133.4 34.1 31.3 19.8 18.9 29.1 GDC-D6-277-Nv6 131.5 19.3 18.2 27.7 28.3 GDC-D6-276-Nv8 131.9 34.7 20.7 18.7 27.7 28.3 GDC-C6-17-Nv4 138.6 35.5 32.0 19 20.8 28.4 28.8 Mtc IV GDC-D6-79-Nv6 127 26.7 GDC2019-C7-147-Nv4 124.5 30.9 25.4 17.2 19.4 Mtc V GDC-D6-283-Nv8 106.3 29.6 30.1 18.1 14.8 Mtt II GDC-D6-80-Nv4 144.6 39.4 31.6 18.8 24.4 26.8 GDC2020-C5-11-Nv4 151.7 42.4 31.6 22.5 26.1 27.5 30.0 GDCD2020-C5-484-Nv4 44 33.1 27.4 Element Record TL MD Astragalus GDC2015-Pou-63 71.9 56.9 GDC-D6-122-Nv8 72.1 62.8 GDC-B7-579-Nv4 76.5 67.4 Calcaneum GDC-D6-318-Nv6 137.9 87.6 13 Journal of Mammalian Evolution in all the available fossil sample; however, the number of Maximum transversal diameter; MDap, middle diaphy- complete fossil bones coming from each locality is nor- sis anterior–posterior diameter; MDtr, middle diaphysis mally low. If we separate in glacial/interglacial stages or transversal diameter; PDap, anterior–posterior proximal by latitude, the sample size is short to assess the results or diameter; PDtr, transversal proximal diameter; TL, Total to be statistically significative. Furthermore, to realize an length. accurate latitudinal distinction, we must take into consid- eration also the differences among biomes. Systematic Paleontology Institutional Abbreviations ICP, Institut Català de Paleontologia Order Carnivora Bowdich (1821) Miquel Crusafont, Universitat Autònoma de Barcelona, Catalo- Family Felidae Gray (1821) nia, Spain; RMCA, Royal Museum for Central Africa, Tervuren, Subfamily Felinae Simpson (1945) Belgium. Genus Panthera Oken (1816) Panthera fossilis von Reichenau (1906) Anatomical Abbreviations c, lower canine; L, length; M/n, Figures 5, 6, 7 and 8 upper and lower molar, respectively; Mtc, metacarpal; Mtt, metatarsal; Pa, paraconid; Ph, Phalanx; P/p, upper and Referred Material 63 cranial and postcranial elements lower premolar, respectively; Pr, protoconid; W, width. representing at least three Individuals. See detailed list in Table S5. Measurement Abbreviations DDap, anterior–posterior distal diameter; DDtr, transversal distal diameter; MD, Measurements See Table 1 Fig. 5  Grotte de la Carrière lion dentognathic specimens from Sondage e. GDC2015-Pou-176, left m1. f. GDC2016-D6-64-Nv6, right m1. g. 1 in occlusal, buccal, and lingual views (from left to right). a. GDC2016- GDC2016-D6-37-Nv6, left c1 in buccal (left) and lingual (right) views. D5-29-Nv1, left p3. b. GDC2016-D67-255-Nv6, right p3. c. GDC2016- Scale bar equals 2 cm B4-Nv1, right p4. d. GDC2015-Pou-168, left distally fragmented p4. 13 Journal of Mammalian Evolution Fig. 6  Grotte de la Carrière metacarpal bones from lower layers of D5-545-Nv4, right Mtc II. c. GDC2015-D6-276-Nv8, left Mtc III. d. Sondage 1 in proximal, dorsal, medial, ventral and lateral views (from GDC2015-D7-21-Nv4, left Mtc III. e. GDC2016-D6-79-Nv6, left Mtc left to right). a. GDC2016-D6-216-Nv6, right Mtc II. b. GDC2019- IV. f. GDC2019-C7-147-Nv4, right Mtc IV. Scale bar equals 2 cm Description displays a moderate degree of wear. The apical part is par- tially fragmented, which prevent us from taking measure- Dental Remains Only one left c1 (GDC2016-D6-37-Nv6) ments (Fig. 5a). Nevertheless, two clear longitudinal ridges was recovered. It belongs to an adult specimen. The tooth can be seen on the buccal side seen. 13 Journal of Mammalian Evolution Fig. 7  Grotte de la Carrière metatarsal and metacarpal bones from physis of right Mtt IV. d. GDC2015-D6-283-Nv8, right MtcV. e. lower layers of Sondage 1 in proximal, dorsal, medial, ventral, and GDC2015-B6-98-Nv8, right Mtt V in dorsal, lateral and ventral view. lateral views. a. GDC2020-C5-11-Nv4, right Mtt III. b. GDC2016- f. GDC2020-D6-638-Nv4c, right MtcI in dorsal, medial, ventral and D6-80-Nv4, left Mtt III. c. GDC2020-C5-314a-Nv4, proximal epi- lateral view. Scale bar equals 2 cm One left (GDC2016-D5-29-Nv1) and one right (GDC2016- accessory cusp is characterized by a rounded morphology. D6-225-Nv6) p3 were studied (Fig. 5b–c). The shape of the Finally, a very incipient distal cingulum is visible, especially buccal margin is slightly convex on its whole mesiodistal in GDC16-B5-29-Nv6 (Fig. 5b). length. Both p3 protoconids are low and asymmetric in Regarding lower forth premolars, only right GDC16- buccal view. Mesiolingually, a small and rounded paraco- B4-r-Nv6 (Fig. 5d) is complete. In the middle of the crown nid is visible in occlusal view. Distally, a well-developed in buccal view, a high protoconid is well-separated from 13 Journal of Mammalian Evolution Fig. 8  Grotte de la Carrière lion tarsal bones from Sondage 1. a. (left) and distal articulation facet (right) views. f. GDC2020-C5- GDC2015-Pou-63, right astragalus in dorsal (left) and ventral (right) 393-Nv4, left navicular in proximal articulation facet (left) and distal views. b. GDC2019-B7-579-Nv4, right astragalus in dorsal (left) and articulation facet (right) views. g. GDC2020-C5-313-Nv4, right navic- ventral (right) views. c. GDC2015-D6-318-Nv4, calcaneus in dorsal, ular in proximal articulation facet (left) and distal articulation facet medial, ventral and lateral views (from left to right). d. GDC2016-D6- (right) views. h. GDC2020-C5-548-Nv4, cuneiform III in proximal 122-Nv8, right astragalus in dorsal (upper) and ventral (down) views. articulation facet (left) and distal articulation facet (right) views e. GDC2020-C5-312-Nv4, right cuboid in proximal articulation facet 13 Journal of Mammalian Evolution mesiobuccally placed paraconid and distal metaconid. Both proximal view, displaying an elliptical longitudinally devel- are much smaller than the protoconid and relatively equally oped facet on the lateral proximal side for Mtc III articu- developed. A second tiny distal accessory cusp is visible lation. On the anterior side, a diagonal depression crosses attached to a distinct distal thin cingulum (Fig. 5d). The the proximal epiphysis (strongly marked in GDC16-D6- mesial margin is slender and uniform without any visible 216-Nv6; Fig. 6a). cingulum. The two well-preserved isolated m1s were studied Four Mtc III are preserved including two that are almost (Tables S6–S7; Fig. 5f–g). The protoconid is higher than complete (right GDC-C6-17-Nv4 and left GDC-D7-21-Nv4; the stouter paraconid, being comparable in mesiodistal Fig. 6c–d) and one that is partially fragmented on the lateral length. Distally to the protoconid there is a small slightly side of proximal epiphysis (GDC-D6-276-Nv8; Fig. 6c). The developed talonid, both cusps are separated by a rela- two well-preserved proximal epiphyses (Fig. 6d) display a tively deep notch. In occlusal view, this valley forms a V deep central depression in proximal view for the capitate shape. In the middle of the lingual side, a tiny tubercle can carpal joint. The lateral articular facets for the Mtc IV articu- be observed at the base of the crown. Distally, both m1s lation consist of one circular surface on the lateral anterior display a developed cingulum without any accessory cusp side and another one, elliptical and longitudinally expanded, (Fig. 5f–g). In occlusal view, the crown is convexly curved. on the lateral posterior side, similar to Mtc II. All the three Its enamel presents a zigzag structure. Biometrically, p4 is metacarpals display a strongly marked depression on the practically equal in size to both studied m1s, being slightly anterior side of the proximal epiphysis. Contrary to Mtc larger (32.5 mm vs. 30.6 and 31.7 mm in GDC16-B4-r-Nv1, II and Mtc III, the diaphyses of the two recovered Mtc IV GDC15-Pou-176, and GDC16-D6-64-Nv6, respectively). are slender (Fig. 6e–f). The proximal epiphysis has a stout morphology. The single recovered Mtc V is well-preserved, Axial Skeleton Two complete and well-preserved caudal the shaft is distally curved, and both epiphyses are stout vertebrae were recovered. The systematic description of (Fig. 7e). The medial side of the proximal epiphysis presents caudal vertebrae (or the vertebral column in general) does a large surface with a wide circular facet for the Mtc IV not report any taxonomic information at the species level. articulation (Fig. 6e). However, the large size of both specimens suggests a large Concerning the hindlimb skeleton, the bones recov- lion (Fig. S1b–c). ered are represented by a fragmented fibula, one calcaneus (Fig. 8c), three right astragali (Fig. 8a, b, d), three cuneiform Appendicular Skeleton The lion forelimb skeleton speci- III (Fig. 8h), one cuboid (Fig. 8e), two naviculars (Fig. 8f–g), mens come from the lowest layers of Grotte de la Carrière and five metatarsal bones: three Mtt III, one Mtt IV, and one and are represented by a right ulna and eleven metacarpals Mtt V (Fig. 7). from at least two individuals: one Mtc I, three Mtc II, four Mtc III, two Mtc IV and one Mtc V (Table S5; Figs. 6 and 7). Fibula The single right fibula (GDC2015-D6-182-Nv6) is partially fragmented on the proximal epiphysis. Only the Ulna The well-preserved fragment of a proximal right ulna distal epiphysis is relatively well-preserved. It shows an includes the sigmoid cavity and the olecranon. The sigmoid irregular rectangular shape with great relief in the distal cavity is concave and deep and forms a C shape in lateral tibiofibular joint, suggesting a powerful muscle insertion. view. An especially robust and elongated olecranon is proxi- mal to the sigmoid cavity (75.4 mm and 30.4 mm anter- Calcaneus The posterior part of the calcaneus is fragmented oposterior and transverse diameter, respectively; Table 1), (Fig. 8c). The calcaneal tubercle measures 87.63 mm in which displays clear scoring marks (Binford 1981) and pits length, and on the superior surface, a strongly marked cal- (Online Resource 1, Fig. S1a). On the cranial surface of the caneal tuberosity is present. On the inferior surface of this proximal epiphysis is observed a significant depression for calcaneal tubercle, the sustentaculum tali emerges promi- the triceps muscle insertion. The anterior part is broken. In nently from the anteromedial portion of calcaneus body. In general terms, GDC15-D6-37-Nv4 is anteroposteriorly stout. general terms, the calcaneus is large and slender. Metacarpals A stout and short right Mtc I was recovered Astragalus All three preserved astragali display rounded (GDC-D6-638-Nv4c; Fig. 7F). Two almost complete stoutly borders in the neck and the body (Fig. 8a, b, d); the malleolar built right Mtc II (Fig. 6a–b) from distinct individual from articulation, visible on the medial side of lateral trochlea, is that of the Mtc I (GDC-D6-638-4c) were preserved. The dia- partially fragmented (except in GDC-B7-579-Nv4), which physis of Mtc II is comparatively less straight and proximo- prevents the measurement of maximal transverse diameter distally large. The medial side of the proximal epiphysis is (Fig. 8). Between the lateral and the medial trochlear crests, rectilinear. The shape of proximal epiphysis is triangular in there is an accentuated depth depression for the superior 13 Journal of Mammalian Evolution tibia facet. The lateral trochlear crest is relatively distally For further information on the studied specimens oriented, towards the medial one, and is significantly larger. unearthed from the Middle Pleistocene layers of Grotte de On the posterior part of astragalus body, the wide articular la Carrière, the reader is referred to Online Resource 1. facets for the calcaneus insertion minimizes the calcaneal sulcus space. On the distal part, an especially stout neck and a large surface for the insertion of the navicular are visible Results (Fig. 8). Morphological Comparisons with Middle and Late Cuneiform III Three cuneiforms III were recovered, all of Pleistocene Lions them belonging to adults (Fig. 8h). GDC-C5-583-Nv4c is associated with a right third metatarsal GDC-S1-C5- The European Pleistocene lions are similar to one another 11-Nv4, right cuboid GDC-C5-312-Nv4, and right navicular both morphologically and metrically (Argant et al. 2007). GDC-C5-313-Nv4. Notwithstanding, the large size of Middle Pleistocene lions has been noted by numerous authors (Schütt 1969; Schütt Navicular Two almost complete oval naviculars were recov- and Hemmer 1978; Argant 1988, 1991; Argant et al. 2007; ered from the same layer (L4) and square (C5) (Fig. 8f, g). Marciszak et al. 2019, 2021). Historically, the phylogenetic Both conserve the wide surface for the astragalar insertion position and taxonomy of fossil lion species was mainly superiorly and for the cuneiform III posteriorly and are based on dentognathic morphology (Schütt 1969; Schütt partially fragmented on the posterior side. Specimen GDC- and Hemmer 1978; Argant 1988, 1991; Sotnikova and C5-313-Nv4 belongs to the same individual as right Mtt Nikolskiy 2006; Hankó, 2007; Marciszak and Stefaniak III GDC-s1-C5-11-Nv4, right cuneiform III GDC-C5-583- 2010, Sabol 2014). Accordingly, the premolars of P. fossilis Nv4c, and right cuboid GDC-C5-312-Nv4. differ from those of P. spelaea in the following aspects: more robust p3 crown (Marciszak et al. 2021); slightly Cuboid GDC-C5-312-Nv4 is a well-preserved cuboid of convex buccal margin on the whole p3 (Marciszak and an adult individual without any traces of damage (Fig. 8e). Stefaniak 2010); elongated and high protoconid in p3 The tarsal bone articulates with Mtt IV GDC-C5-314-Nv4 (Marciszak et al. 2021); presence of well-developed ante- and belongs to the same individual as right Mtt III rior and posterior cusps, namely paraconid and hypoconid GDC-C5-11-Nv4. (= metaconid; Baycka 2008), respectively, in p4 (Schütt and Hemmer 1978; Ballesio 1980; Hankó 2007; Barycka 2008); Metatarsal Three almost complete large and stoutly-built shorter and higher protoconid in p4 (Schütt and Hemmer Mtt III were recovered (Fig. S7a, b). The asymmetrical “T” 1978); premolars, especially p4, proportionally larger than shape of the proximal epiphysis for the third cuneiform m1 (Schütt and Hemmer 1978; Argant 1988, 1991; Barycka articulation is well-preserved in two of them (Fig. 7a, b). 2008); elongated p4 with respect to total length of m1 On the proximolateral side (Fig. 7a, b), the proximal epi- within the same mandibular fragment (Schütt 1969; Schütt physis displays a deep fossa for the Mtt IV articulation. The and Hemmer 1978; Sabol 2014; Marciszak et al. 2017; fragmented right Mtt IV GDC-s1-C5-314-Nv4 (Fig. 7d) pre- Fig. 5). P. fossilis is also distinguishable from P. spelaea serves only the proximal epiphysis. In proximal view, the in the following m1 characters: wider m1 crown (Schütt proximal epiphyseal surface for the cuboid bone insertion and Hemmer 1978; Ballesio 1980); higher and sharper is asymmetrically quadrangular (Fig. 7c). This Mtt IV is protoconid and rounded robust lower portion of the para- associated with Mtt III GDC-C5-11-Nv4 and cuboid GDC- conid (Thenius 1972); mesially oriented protoconid edge C5-312-Nv4. Finally, the only recovered Mtt V (Fig. 7d) is (Fig. 5; Hankó, 2007); more developed posterior talonid distally fragmented and presents strong traces of weather- in m1 (Schütt 1969; Schütt and Hemmer 1978; Argant ing and corrosion on the bone surface along the diaphysis, et al. 2007; Hankó 2007; Argant and Brugal 2017); pres- precluding accurate morphological description (This issue is ence of mediolingual protuberance or bulge at the base of present in all the bones recovered but is especially prominent the crown (Schütt 1969; Schütt and Hemmer 1978; Hankó in Mtt V). 2007; Argant and Brugal 2017; Marciszak et al. 2021); presence of zig-zag enamel structures (Schütt and Hemmer Phalanges Twenty-five phalanges from the anterior and pos- 1978; Barycka 2008); and well-developed abrupt curve of terior paws were recovered, thirteen Ph I (Fig. S2) and twelve the enamel, on the buccal side, in occlusal direction, that Ph II (Fig. S2). All of them are almost complete and belong to rises below the protoconid and produces a convex shape adult or subadult individuals. The right Ph I GDC-C5-394a- margin of the whole m1 (Hankó 2007). Lastly, as a conse- Nv4 (Fig. S2i) and Ph II GDC-s1-C5-314b-Nv4 (Fig. S3d) quence of a wider m1 crown, the teeth have a higher B/T associate with the right Mtt III GDC-s1-C5-11-Nv4 (Fig. 7b). ratio (Schütt 1969; Hemmer and Schütt, 1970; Schütt and 13 Journal of Mammalian Evolution Hemmer 1978; Ballesio, 1980); according to Marciszak and in the dental remains and of the tendency of postcranial Stefaniak (2010), this ratio has an average value of 0.54 for remains such as tarsal and metapodial bones to be stouter, P. fossilis (range from 0.47–0.58) and 0.5 for P. spelaea as in P. fossilis, further suggest the presence of intermediate (range from 0.36–0.57). features towards late Pleistocene European lions. Despite the high reliability of teeth for taxonomic purposes, the postcranial skeleton may help when the dentognathic Biometrical Comparisons with European Pleistocene remains are scarce (Barycka 2008; Sotnikova and Foronova Lions 2014; Marciszak et al. 2019). The interspecific differences of limb bones have been observed both dimensionally and The morphometric differences between European lion proportionally. According to Argant and Brugal (2017) and groups over geological time normally follow the diagnos- Marciszak et al. (2019, 2021), the chronologically older P. tic features related to dentognathic remains (Schütt 1969; fossilis showed an increase in size until MIS11-9, when the Argant 1991, 2010; Hankó 2007; Sabol, 2014). Alterna- largest individuals are recorded. From this moment on, size tively, several researchers have also included the propor- in fossil lions decreased until they reached a size similar to tions of postcranial in statistical analyses (Dietrich 1968; that of extant African lions. The main problem in considering Ballesio 1980; Bona and Sardella 2012; Baryshnikov 2016; this simplified size-reduction trend is that it does not seem to Sotnikova and Foronova 2014; Marciszak et al. 2019). In respond only to chronological proxies. Indeed, it is neces- the present study, biometrical comparisons are focused on sary to consider the different biotope inhabited, which lower dental remains and several morphometric characters of depends on the climate, the faunal communities, and postcranial bones, such as tarsals and metapodials. To maxi- intraspecific differences, especially sexual dimorphism (see mize intergroup differences and to avoid intraspecific vari- Table S8 for our analysis on the sexual dimorphism of extant ation, we chose those variables with significant intergroup lions). differences supported by statistical tests have been observed: Focusing our attention in the morphological characters, one-way ANOVA (p < 0.05) for parametric variables and the specimens described in this study share the diagnostic Mann–Whitney pairwise (p < 0.05) for non-parametric. The features reported for P. fossilis, namely (Schütt 1969; Schütt complete measurements are shown in Table 1 and the statis- and Hemmer 1978; Argant 1988, 1991; Argant et al. 2007; tically significant comparisons in Table S11. Hankó 2007; Barycka 2008; Marciszak and Stefaniak 2010; Marciszak et al. 2019, 2021): markedly wide m1 at the base Dental Remains of the crown, larger premolars (Tables S9 and S10), high and sharp protoconid edge and short rounded paraconid edge in In general terms, European lions display a trend of m1, mesially oriented edge of the protoconid of m1, small decreasing size over time from the Middle Pleistocene lingual protuberance in the medial part of m1 crown, the zig- forms to their most recent relatives (Marciszak and zag structure in the m1 crown’s enamel - taxonomically used Stefaniak 2010; Marciszak et al. 2019). Nevertheless, by some authors who considered that a common character the decrease of middle Middle Pleistocene lions to the related to Middle Pleistocene lions (Marciszak and Stefaniak two younger groups of Late Pleistocene and the extant 2010) but questioned by others (Sabol 2014), proportionally African lions is not always observed in the geologically short paraconid and oval and slightly convex buccal margin older group from MIS 15–12. These forms usually show in both p3, presence of abrupt curve in the buccal enamel smaller values compared with those from MIS 11–9 in m1 that rises below the protoconid, B/T ratio close to P. (Marciszak et al. 2019). Notwithstanding, the extant rela- fossilis average (Table S1), stoutly-built astragalus (Fig. 8), tives and the MIS 5e-2 lions were significantly smaller large calcaneus, anteroposteriorly stout ulna, robust proximal than the massive, large lions from the early and middle and distal epiphyses of third and fourth metacarpals and third Middle Pleistocene (Fig. 9a). metatarsal (Figs. 6 and 7). On the other hand, the analyzed The above-mentioned chronological decreasing trend specimens differ from previously reported P. fossilis in: the of size was firstly observed in the lower dental remains slightly developed posterior talonid in m1, absence of the (Fig. 9a). In the lower m1 B/TL ratio (Fig. 9a), this trend groove at the top of the medial lingual protuberance of the m1 is easily followed from MIS 15 to latest Pleistocene ones, (Schütt 1969; Schütt and Hemmer 1978; Argant and Brugal with the GDC specimens better grouped with MIS 11–9 2017), slender calcaneum, and proportionally proximodistally forms, as expected. The box plots depicted from the premo- short metatarsus and metacarpus. lars (Fig. 9a) show that the smaller specimens are the ones In summary, based on morphological characteristics of the MIS 15–12 group. Moreover, MIS 5e-2 is larger than described and compared above, the specimens from Grotte MIS 8–6 in the p4 B/TL (Fig. 9a). GDC values fit in the de la Carrière can be referred here to Panthera fossilis. The middle Middle Pleistocene box, much closer to the median combination of morphological similarities with P. spelaea point of MIS 11–9 box (Fig. 9a). 13 Journal of Mammalian Evolution Fig. 9  a. Boxplots of total breadth to total length B/TL ratio of lower dental remains from Grotte de la Carrière, Middle to Late Pleistocene localities and extant relatives showing the chronological trend. b. bivariate graphs of total width against total length of lower dental remains Concerning interspecific differences, the studied speci- measurements of Grotte de la Carrière specimens can be mens were compared to both European lions, P. fossilis and found in Table 1. In Fig. 9b are represented the scatter plot P. spelaea, as well as extant P. leo. We included the P. inter- diagrams for maximum breadth against total length for m1, media m1 values from Igue de Rameaux in the P. spelaea p4, and p3. The one-way ANOVA corroborates the statistical group, as they are biometrically indistinguishable. Complete significance of results (see Table S11). 13 Journal of Mammalian Evolution In the scatter diagrams for p3 and p4 are observed some are perfectly separated into two clouds of points (Fig. 10b). clear intergroup differences (Fig. 9b). The set of P. fossilis In the uppermost part of the graph, where GDC specimens p3 variables are in the uppermost part of the plot, separated fit, are located the P. fossilis individuals. GDC-s1-Pou-63, in from P. spelaea and P. leo values (Fig. 9b). Concerning which the partially rounded bone affected the measurement the p4 bivariate graph, P. fossilis values are located in the of maximum transversal diameter, is located outside the P. uppermost part (Fig. 9b). In this case, overlapping groups fossilis range, near one specimen from Zá Hájovnou Cave. of species can be observed in the lowermost part of the con- vex hull. In both premolars, the GDC specimens overlap the Calcaneus In the MD/TL ratio for calcaneus, the trend is not uppermost part of P. fossilis variance (Fig. 9b). As regards as clear as the one for the astragalus (Fig. 10a). The differ- the m1 (Fig. 9b), GDC m1 fits within the P. fossilis cloud, ences are also not statistically significant. Nevertheless, the near the uppermost P. spelaea area (population from Lherm P. fossilis groups from middle Middle Pleistocene differ sta- and Azé I-3), in the fringe between both species. In detail, tistically in the total length of calcaneus from P. spelaea and GDC values are located closest to P. fossilis from Westbury, P. intermedia from MIS 8–6 and MIS 5e-2 (Fig. 10a). In the Petralona, Aragó, and Vértesszȍlȍs II and P. spelaea from bivariate graph, the uppermost part corresponds to P. fossilis Lherm and Azé I-3. values and the lowermost part to P. spelaea (Fig. 10b). The According to some authors (Schütt 1969; Hemmer and single GDC specimen fits within the P. fossilis variability, Schütt, 1970; Schütt and Hemmer 1978; Ballesio 1980), near the edge of the P. spelaea cloud where the highest values the m1 B/TL coefficient can be used to separate P. fos- are located, for Lezetxiki VI and within the Château range. silis from P. spelaea. In the former, this ratio is normally above 0.47–0.58, whereas in the latter, the ratio normally is 0.36–0.57 (Marciszak and Stefaniak 2010). The GDC sam- Metapodial Bones ple matches better with P. fossilis (0.54) (Table S6). The taxonomic reliability of the metacarpus and metatarsus Tarsal Bones is rather poor. These features present an intraspecific varia- tion related generally to the locomotor apparatus in relation- Among the postcranial elements, the tarsal and metapodial ship with the habitat (Turner 2009). In general, autopodial bones have significant results for interspecific correlations bones are practically indistinguishable from one to another. (Sabol 2014). In tarsal bones, the chronological trend of In the comparison below, we included European and North decreasing size over time seen in dental remains is also nor- American fossil lions from MIS 15–2 to recent lions and mally displayed (Fig. 10a). However, lions from MIS 5e-2 focused only on variables in which the intergroup differ- experienced an increase in size compared to the chrono- ences were supported by statistical tests (Mann–Whitney logically older MIS 8–6 group, a tendency also observed test, p > 0.05; Tables S1, S2, S7 and S11). In Figs. 11 and between MIS 11–9 and MIS 15–12 for the calcaneus values 12 are represented in boxplots the significant interspecific (Fig. 10a). The tarsal bones were compared to both classi- indices. cal Pleistocene European lions: P. spelaea and P. fossilis. In general terms, the P. spelaea from MIS 5e-2 and the Complete measurements are in Table 1. In Fig. 10b are extant lions are less stoutly-built than the ancient P. fos- represented the bivariate graphs for astragalus/calcaneus, silis and North American P. atrox. The recent lions differ plotting the maximum mediolateral diameter against total from the rest of the groups in the slenderness of both epi- proximodistal length, with the graphical representation of physis and the shorter diaphysis. In P. fossilis from Poland MD/L and TL ratio in boxplots. MIS 9–10 and P. spelaea from MIS 6 of Lherm (France), relatively larger values have been noticed in comparison to Astragalus The statistically significant results for the maxi- others of their own groups in the maximum anteroposterior mum mediolateral diameter to the total length ratio MD/ diameter of the proximal epiphysis and the proximodistaly TL for the astragalus point out a clear division between the larger diaphysis. two species and reflect how Late Pleistocene P. spelaea dif- The intergroup differences that are statistically signifi- fers from the Middle Pleistocene ones based on smaller size cant for the Mtc III include total length and maximum (Fig. 10a). Contrary to the observed analysis for the dental anteroposterior diameter of proximal and distal epiphysis remains, the set of variables from MIS 11–9 shows a decreas- (Fig. 11). For Mtc IV, they are total length, maximum ing size tendency with respect to the older MIS 15–12. The anteroposterior diameter of proximal epiphysis, maxi- MIS 8–6 group instead, has significantly reduced size com- mum transverse middle shaft diameter and maximum pared to the most recent group, MIS5e-2. GDC values are transversal diameter of distal epiphysis (Fig. 11). For located at the top level of the MIS 11–9 box and at the upper- Mtt III, they are: total length, maximum anteroposte- most MIS 5e-2. In the resulting bivariate graph, the values rior and transversal diameter of proximal epiphysis, 13 Journal of Mammalian Evolution Fig. 10  a. Boxplots of select ratios of tarsal bones from Grotte de la Carrière, Middle to Late Pleistocene localities showing the chronological trend. b. bivariate graphs of total width against total length of astragalus (left) and calcaneus (right) and maximum transversal diameter of distal epiphysis in proportions from Late Pleistocene European and North (Fig. 12). Checking the resulting boxplots for the ratio American lions and their extant African relatives. Generally, between Dpap/TL and Ddap/TL of Mtc III and Mtc IV the studied specimens differ from Middle Pleistocene lions (Fig. 11), the midpoint of the GDC data is closer to the P. fossilis in total length but are similar to them in anteropos- top or midpoint of the P. fossilis box, except Ddap/TL of terior and mediolateral diameter of the proximal epiphyses, Mtc IV, which are near the bottom (Fig. 11). a feature especially prominent in Mtt III (Fig. 12). According to the performed analyses, the GDC specimens are significantly distinct from P. spelaea in maximum anter- oposterior diameter of the proximal epiphysis of metacarpals III Discussion and IV (Fig. 11) and maximum anteroposterior and mediolateral diameter of the proximal epiphysis of metatarsal III (Fig. 12). Grotte de la Carrière Lions in the Context of Middle None of the metacarpals nor metatarsals from GDC shows a Pleistocene European Lions statistically significant distinction compared with P. fossilis. In summary, the trend observed shows that middle Mid- As discussed in the biometrical comparisons section, the fossil dle Pleistocene P. fossilis are significantly distinguishable remains of P. fossilis from Grotte de la Carrière reveal stout 13 Journal of Mammalian Evolution Fig. 11  Boxplots of select ratios and measurements of Grotte de la Carrière metacarpal bones (marked in red) compared to Panthera fossilis, Panthera spelaea, Panthera atrox and values for extant relatives and relatively large specimens, fitting within the size range Torre in Pietra (Italian Peninsula), Kent’s Cavern (Great Brit- and morphology of this species from coeval sites (middle ain), and Lunel-Viel and Orgnac (France) samples. In con- Middle Pleistocene, MIS 11–9). The specimens from Sima de trast, those individuals from the Polish localities of Biśnik los Huesos from the Atapuerca complex (Iberian Peninsula), and Wierzchowska, predominantly from steppe-tundra and Vértesszȍlȍs 2 (Hungary), and Zá Hájovnou from Moravia boreal forest landscape, are especially large. The harsh and (Czech Republic) are the similar to Grotte de la Carrière indi- cold ecosystems in which they lived could explain their larger viduals and also proportionally larger than Petralona (Greece), size following Bergmann's Rule (Bergmann 1847). 13 Journal of Mammalian Evolution Fig. 12  Boxplots of select ratios and measurements of Grotte de la Carrière metatarsal bones (marked in red) compared to Panthera fossilis, Panthera spelaea, Panthera atrox and values for extant relatives Bergman’s Rule proposes a heat balance explanation de los Huesos, and Petralona) and steppe/tundra (Biśnik and for the differences in body size depending on the latitudi- Wierzchowska) or alpine boreal forest (Zá Hájovnou) may nal distribution of species (Bergmann 1847). In general, the affect the biocenosis. gradient of body size increase with the latitude (in accord- Traditionally in the paleontological literature, the steppe ance with increasingly cold conditions). Not all species fit lion has been considered a predator adapted to wide vari- Bergman’s Rule because there are other factors to take into ety of ecosystems (Hemmer 2004; Turner 2009). Bearing in consideration. In this case, the differences in the biomes such mind that each biotic community is naturally adjusted accord- as the Mediterranean vegetation (e.g., Torre in Pietra, Sima ing to its local climate and that the locomotor apparatus is 13 Journal of Mammalian Evolution linked to predatory strategies (Moore and Biewener 2015), general larger than major part of chronologically older lions species adaptations to distinct biomes may reflect regional from MIS 15–12. This implicit trend is fulfilled by most differences in the skeleton. For example, European terrestrial fossiliferous sites, except the northeastern France locality biomes usually encompassed grassland, forest, and tundra. of Breccia de Château and the Central European sites of Consequently, the prey spectrum available and hunting strat- Moggaster and Poludniowa, in which they are larger and egies are distinct for each one. In particular, for ambushing stouter. The studied specimens from Westbury and Caune prey hunters wait for the prey and launch one quick strike de l’ Arago share similar characteristics with GDC lions. (Moore and Biewener 2015), so this type of predatory behav- The intraspecific distinctions between the larger speci- ior strategy has specific skeletal requirements. To illustrate, mens from Central Europe could be a response to climatic recent studies report that extant male lions use the savanna dynamics and geographical settings, as has been seen with vegetation for ambushing prey instead of pursuit in open the coeval sites. Traditionally, climatic events strongly grasslands like female lions (Loarie et al. 2013). influenced the biogeographical distributions of mammalian According to the last assertions, the inhabitants of steppe- species and influenced the faunal associations of regional tundra would prey on woolly mammoth (Mammuthus primi- biomes (Rodríguez et al. 2004). The earliest glaciation genius) and rhinoceros (Coelodonta antiquitatis), giant deer period (MIS 16–13) from the Middle Pleistocene occurred (Megaloceros giganteus) or elks (Alces alces) beyond the at the same time for all European regions (Head and Gibbard northern boundary of boreal or deciduous forest (Kahlke 2005). It is characterized by non-glacial cooling during cold 2014). Those lions from Western Europe, which inhabited stages (Candy et al. 2010, 2014; Lindner et al. 2013), suc- deciduous/mixed or mountainous forests with steep cliffs, far ceeded by less interglacial warming compared to MIS 11–9 from the ice sheet cover during glacial periods (Fig. 1), prob- (Szymanek and Julien 2018). The Mid-Brunhes Transition ably preyed on large red deer (Cervus elaphus), the fallow (ca. 430 ka) marks the increase in the amplitude of the cli- deer (Dama dama), the steppe bison (Bison priscus), the rhi- mate cycles to 100 kyr (Jansen et al. 1986; Elderfield et al. noceros (Stephanorhinus hemitoechus), and cave bear (Ursus 2012). So, the strong glacial dynamics and the development deningeri or U. spelaeus s.l.) and occasionally on relatively of regular icesheet covering during cold stages started in smaller roe deer (Capreolus capreolus), ibex (Capra Ibex), MIS 12–10 (Böse et al. 2012) with the arrival of the so- and chamois (Rupicapra rupicapra). called Elster glaciation across northern Europe (Kahlke Regarding the case of Biśnik Cave, the fossil remains et al. 2011; Ehlers et al. 2011), also known as Mindel in the were deposited on the cavity during the Odra Glaciation, Alpine region and Anglian in Great Britain. Consequently, when the typical steppe tundra dominated these habitats, the increase in body size may be related to these climatic a landscape dominated by wooly rhinoceros (Coelodonta fluctuations, as an adaptation to the resulting new cold con- antiquitatis) and steppe bison (Bison priscus). These condi- ditions and the latitudinal changes in the biomes (Rodríguez tions favored long proportions, especially in the metapodi- et al. 2004). Indeed, that could explain the coincidence als, whereas the proportions of Grotte de la Carrière lions among the large and stout lions' occurrence with the strong resemble those from the inhabitants of forest biomes. The climatic events of MIS 12–10. presence of species well adapted to rocky environments such In Central and Northern Europe, the cold-adapted as the genus Hemitragus or the roe deer (Capreolus capreo- large mammals of the Mammuthus-Coelodonta steppe lus) (Demay et el. 2020 and references therein) suggest a complex were established then for the first time (Kahlke mountainous forest, probably with steep cliffs. The mam- et al. 2011; Szymanek and Julien 2018). Some stud- mal assemblage from MIS 9 layers of Caune de l’ Arago ies have revealed that the increase in body size may be (50 km northeast of Grotte de la Carrière), formed by Cervus related to the expansion of this so-called ‘Mammuthus- elaphus, Bison priscus, Equus ferus, and Stephanorhinus Coelodonta steppe’ as an adaptation to the resulting (Moigne et al. 2006), spans a wider spectrum of species new biome. The mammal assemblage of Mosbach and adapted to more open grasslands, the same conditions as in other localities from the Great European Plains suggest Moravian localities. To sum up, the lions from the above- a sequence of changes in ecological conditions usu- mentioned Polish localities and surrounding areas probably ally dominated by dry steppe-tundra landscapes occa- tended to be stouter and larger, conditioned by the surround- sionally interrupted by the extension of deciduous and ing biome. mixed forest during warmer and wet climatic episodes (Kahlke et al. 2011). Instead, in southwestern Mediter- Comparisons with the Earliest Lions from Middle ranean regions, including southern France and the Great Middle Pleistocene MIS 15–12 Britain site of Westbury, the climate during MIS 13–7 intervals was generally temperate (Szymanek and Julien, Following the size trend observed by Marciszak et al. (2019), 2018; López-García et al. 2021), less cold than in Cen- the studied material from Grotte de la Carrière should be in tral Europe. That favored the expansion of deciduous 13 Journal of Mammalian Evolution areas. Precisely, the largest individuals from Moggaster Conclusions and Poludniowa come from the steppe-tundra, areas in which extreme climatic conditions, prey availability (and On the basis of the morphological and morphometric analy- thus the hunting strategies), and interspecific competi- sis performed in the present study, the Grotte de la Carrière tion forced individuals to be stouter. large felid remains are included in the hypodigm of the spe- Unfortunately, all the factors that affect the body size cies Panthera fossilis (von Reichenau, 1906). The studied structure of large mammals are difficult to analyze due to lion from the Réseau Lachambre karstic complex, with an the lack of available specimens in the known fossiliferous estimated chronology corresponding to the MIS 9 inter- sites. glacial, shares several dental diagnostic features and body proportions related to previously recorded Middle Pleisto- Comparisons with Transitional Forms from Late cene forms from the interval MIS 11–9. Nevertheless, some Middle Pleistocene MIS 8–6 minor features more closely resemble later P. spelaea Euro- pean forms from MIS 8–6. Such later forms have also been According to Marciszak and Stefaniak (2010), the forms called ‘intermediate forms’ by previous authors, between between MIS 9–6 normally possesses intermediate charac- the two species of the European lion lineage. The reported teristics, especially those around MIS 7-5e. The specimens data can shed new light on the still scarcely recorded North- from GDC presents some intermediate features, especially ern Hemisphere lions and their size trends over the Pleisto- in the biometric dimensions the of metapodial bones and the cene putatively related to climatic shifts and environmental proportions of m1, which resemble the ones of P. spelaea. parameters. Argant and Brugal (2017) describe the lion from Igue-de- Rameaux as a distinct species with intermediate features, Supplementary Information The online version contains supplemen- namely Panthera intermedia, and include in its hypodigm tary material available at https://d​ oi.o​ rg/1​ 0.1​ 007/s​ 10914-0​ 22-0​ 9600-0. individuals from the French localities of Abimes de la Fage Acknowledgements The authors want to express their gratitude to (MIS 7, France), Romain la Roche (MIS 6), and Orgnac III Philippe Galant, Jean Louis-Perez, Michel Gomez and Jêrome Durbet (MIS 9). Compared to them, the Grotte de la Carrière sam- for their help and availability during the field work at the Têt Valley ple has some morphometrical resemblances including the and to Darin Croft, the associate editors and two anonymous reviewers reduced talonid and the absence of a tiny groove at the top for improve an early version of this manuscript. of the medial lingual protuberance of m1 and the proximo- Authors Contributions All authors contributed to the study concep- distally shorter metacarpals and metatarsals in the case of tion and design. Material preparation, data collection and analysis Romain la-Roche and Orgnac III specimens. However, the were performed by Maria Prat-Vericat, Adrian Marciszak and Joan size of dental remains is proportionally larger than in the Madurell-Malapeira. The first draft of the manuscript was written by Abimes de la Fage and Romain la Roche samples and similar Maria Prat-Vericat and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript. to large-sized specimens from Igue de Rameaux. The lion remains from the rest of the fossiliferous sites of Central- Funding Open Access Funding provided by Universitat Autonoma de Eastern Europe MIS 8–6 are attributed to P. fossilis, whereas Barcelona. This work has been funded by the Direction Regionalle in the western France localities of Lherm, Santenay, and des Affaires Culturelles of the French Government (DRAC Occitaine) Azé I-3, the lions are referred to the P. spelaea group. This and the Agencia Estatal de Investigación-European Regional Develop- ment Fund of the European Union (CGL2017-82654-P, AEI/FEDER- complexity in the characters of populations, considering the UE) and the Generalitat de Catalunya (CERCA Program). J.M.-M. is chronology of the studied sites, is expected. Notwithstand- member of the consolidated research group 2017 SGR 116 (AGAUR, ing, the lions from Lherm differ substantially from the rest Generalitat de Catalunya). LS is supported by the FI AGAUR fellow- by their larger dimensions, similar to the P. fossilis of the ship (ref. 2020 FI_B1 00131) funded by the Secretaria d’Universitats i Recerca de la Generalitat de Catalunya and the European Social Fund. Middle Pleistocene, almost equal to Grotte de la Carrière lions. As seen above, geography is not the only factor that Availability of Data and Material The datasets generated during and/or influences species variability. Considering the chronology of analyzed during the current study are available in the Online Resource 1. Lherm, those lions lived in glacial conditions. In this case, Bergman’s rule should not be ruled out, for which the mam- Open Access This article is licensed under a Creative Commons Attri- mals in cold regions have the trend to be stouter and larger bution 4.0 International License, which permits use, sharing, adapta- tion, distribution and reproduction in any medium or format, as long than the individuals of the same species living in warmer as you give appropriate credit to the original author(s) and the source, sites. Finally, it should not be forgotten that due to European provide a link to the Creative Commons licence, and indicate if changes regional differences, the replacement P. fossilis-P. spelaea were made. The images or other third party material in this article are probably occurred at different times (Marciszak et al. 2014). included in the article's Creative Commons licence, unless indicated 13 Journal of Mammalian Evolution otherwise in a credit line to the material. 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