First Record of Macaques from the Early Pleistocene of Incarcal (NE Iberian Peninsula)

Journal of Human Evolution 96 (2016) 139e144

Contents lists available at ScienceDirect

Journal of Human Evolution

journal homepage: www.elsevier.com/locate/jhevol

News and views First record of macaques from the Early Pleistocene of Incarcal (NE Iberian Peninsula)

* David M. Alba a, , Joan Madurell-Malapeira a, Eric Delson b, c, d, a, Víctor Vinuesa a, Ivette Susanna a, María Patrocinio Espigares e, Sergio Ros-Montoya e, Bienvenido Martínez-Navarro f, g, h a Institut Catala de Paleontologia Miquel Crusafont, Universitat Autonoma de Barcelona, Ediﬁci ICTA-ICP, Carrer de les Columnes s/n, Campus de la UAB, 08193 Cerdanyola del Valles, Barcelona, Spain b Department of Anthropology, Lehman College of the City University of New York, 250 Bedford Park Boulevard West, Bronx NY 10468, USA c Department of Vertebrate Paleontology, American Museum of Natural History, 200 Central Park West, New York, NY 10024, USA d New York Consortium in Evolutionary Primatology, New York, NY, USA e Departamento de Ecología y Geología, Universidad de Malaga, Campus Teatinos, 29071 Malaga, Spain f ICREA, Barcelona, Spain g Institut Catala de Paleoecologia Humana i Evolucio Social, Campus Sescelades, Ediﬁci W3, 43007 Tarragona, Spain h Area de Prehistoria, Universitat Rovira i Virgili, Avda. Catalunya 35, 43002 Tarragona, Spain article info

Article history: papionins during the Late Miocene, with M. sylvanus being its Received 3 March 2016 basal-most extant species (Springer et al., 2012). Fossil evidence Accepted 12 May 2016 suggests in turn that early members of the macaque lineage Available online 11 June 2016 dispersed into Eurasia by the latest Miocene, roughly coinciding with the sea level drop associated with the Messinian Salinity Crisis Keywords: (Alba et al., 2014, 2015). Old World monkeys Cercopithecidae Although macaques were widely distributed across Eurasia Papionini during the Plio-Pleistocene, unlike in Asia they did not experience Macaca an impressive species radiation. There is consensus (e.g., Szalay and Pleistocene Delson, 1979; Delson, 1980; Alba et al., 2011, 2014) that all the Eu- ropean fossil macaques belong to the lineage of the extant M. sylvanus. The two earliest (latest Miocene) European macaque records (Kohler€ et al., 2000; Alba et al., 2014) are attributed to cf. Macaca sp., while the macaque fossil remains from Sardinia are recognized as an extinct, endemic insular species, Macaca majori Azzaroli, 1946 (Zanaga, 1998; Rook and O'Higgins, 2005). The remaining fossil macaque remains from Europe, following Szalay 1. Introduction and Delson (1979) and Delson (1980), are customarily attributed to various extinct subspecies of M. sylvanus (e.g., Alba et al., 2008, 1.1. Fossil European macaques 2011; Marigo et al., 2014). Due to the lack of complete cranial remains, these extinct subspecies are not particularly well charac- Macaques belong to the speciose and widely-distributed genus terized, being largely delimited on biochronological grounds Macaca Lacep ede, 1799 (Cercopithecidae: Papionini), which (Delson, 1980; Alba et al., 2008, 2011; Marigo et al., 2014): currently includes twenty one Asian species and a single North M. sylvanus prisca Gervais, 1859, Early Pliocene; M. sylvanus ﬂor- African species, the Barbary macaque or Macaca sylvanus (Linnaeus, entina Cocchi, 1872, Late Pliocene to Early Pleistocene; and 1758), which was also introduced into Gibraltar in historical times M. sylvanus pliocena Owen, 1846, Middle and perhaps Late Pleis- (Fooden, 1976, 2007; Modolo et al., 2005; Masseti and Bruner, tocene. The local extinction of M. sylvanus in Europe during the Late 2009; Majolo et al., 2013; Roos and Zinner, 2015). According to Pleistocene may be attributable to a combination of different molecular analyses, macaques diverged from other extant ecological factors, such as climatic ﬂuctuations, concomitant vegetation changes, and small population sizes, although human pressure and direct predation might have played major roles as * Corresponding author. E-mail address: [email protected] (D.M. Alba). well (Meloro and Elton, 2012; Elton and O'Regan, 2014). http://dx.doi.org/10.1016/j.jhevol.2016.05.005 0047-2484/© 2016 Elsevier Ltd. All rights reserved. 140 D.M. Alba et al. / Journal of Human Evolution 96 (2016) 139e144

Despite the wide geographical and temporal distribution of 1999; Anton et al., 2005; Ros-Montoya et al., 2012). To date, no macaques during the European Plio-Pleistocene, their fossil record primate remains have been found in any of the more than fifteen is quite sparse, thereby suggesting that they were not very abun- fossiliferous infills discovered (Madurell-Malapeira and Martínez- dant, probably due to suboptimal ecological conditions (Meloro and Navarro, in press). Elton, 2012; Elton and O'Regan, 2014). Here we report the first The Early Pleistocene limestones of Crespia have yielded abun- primate find from the Early Pleistocene site complex of Incarcal (NE dant plant but only a few vertebrate remains (Ros et al., 2003; Iberian Peninsula): an upper molar identified as a macaque that Galobart et al., 2010). Most of the vertebrate fossils come from was found during the 2015 field season. the karstic infills of the Incarcal site complex, which consists of a series of funnel-shaped dolines filled with fossiliferous clays that 1.2. The Incarcal site complex originated due to the karstification (by dissolution and collapse) of the limestones (Ros and Palomar, 2003; Galobart et al., 2010). The The fossiliferous deposits from Incarcal (Crespia, NE Iberian fossil reported here comes from the most-extensively excavated Peninsula; Fig. 1) were discovered shortly after the Cal Taco car- site, Incarcal I, which has provided 1576 large mammal remains bonate quarry began to be exploited in 1967, and take their name (Table 1). The overrepresentation of carnivorans and the frequent from the acronym of the former excavation company (Industrias de recovery of bones in anatomical connection suggest that these Carbonato de Cal; Maroto et al., 2003a; Galobart et al., 2010). Initial karstic cavities functioned as vertebrate traps (Galobart, 2003a), in surveys resulted in the publication of plant macroremains from the agreement with the very short transportation distance inferred limestones of Crespia( Villalta and Vicente, 1972; Roiron, 1983), from the abundance of unfragmented long bones and the excellent from the lacustrine Incarcal Formation (Banyoles-Besalú Basin), as state of preservation of the fossils (Galobart, 2003b). However, well as the publication of abundant late Villafranchian vertebrate sedimentological evidence suggests that bones were transported fossils from the karstic infills developed in these limestones (Julia by water flow into the dolines (Canals and Galobart, 2003). This is and Villalta, 1984). Subsequent surveys and excavations between further supported by current natural ponds from nearby areas, 1984 and 1990 (Maroto and Galobart, 1991; Maroto et al., 2003b; which act as sinkholes that eventually collect animal remains from Galobart et al., 2010) and 1999e2005 (Galobart et al., 2010)were the surroundings after rainy episodes (Madurell-Malapeira and particularly focused on Incarcal I and V. Excavations were resumed Martínez-Navarro, in press). in 2009 by a team led by the Institut Catala de Paleontologia Miquel There are no known age differences among the various karst Crusafont and have continued to the present (Madurell-Malapeira infills (Galobart et al., 2010), although no chronometric dates are and Martínez-Navarro, in press). The fauna from Incarcal has available yet (Madurell-Malapeira and Martínez-Navarro, in been treated in a doctoral dissertation (Galobart, 1996), a journal press). On biochronological grounds, several studies suggested special issue (Galobart and Maroto, 2003), and several scattered an estimated age of ca. 1.5e1.4 Ma (millions of years ago) for the papers (Pons-Moya and Moya-Sol a, 1992; Anton and Galobart, Incarcal sites (Ros-Montoya et al., 2012; Madurell-Malapeira et al.,

Figure 1. Location map of the site of Incarcal (dot), close to the town of Crespia, and its surroundings; rivers and lakes are indicated in light gray, urban areas in dark gray, and roads in black. The inset in bottom left shows the situation of the depicted area (square) relative to the city of Barcelona (black dot) within the Iberian Peninsula. D.M. Alba et al. / Journal of Human Evolution 96 (2016) 139e144 141

Table 1 2. Description and comparisons Large mammal species from Incarcal I. Updated from Madurell-Malapeira and Martínez-Navarro (in press). The primate upper molar IN-I 1960 (Fig. 2) is temporarily Order Proboscidea housed at the Institut Catala de Paleontologia Miquel Crusafont Mammuthus meridionalis and later will be deposited at the Museu Arqueologic Comarcal de Order Perissodactyla Banyoles. The crown and the mesiobuccal root are completely Stephanorhinus hundsheimensis Equus altidens preserved, whereas the tip of the single lingual root and most of Order Artiodactyla the distobuccal root are missing. The crown shows a moderate Hippopotamus antiquus degree of wear (with very slight dentine exposure at the apices of Bison sp. the buccal cusps, but more extensive dentine exposure on the Bovidae indet. Megacerini indet. lingual ones) and two (mesial and distal) contact facets. It dis- Metacervocerus rhenanus plays a bilophodont and typically papionin occlusal pattern (e.g., Caproleus sp. Delson, 1973, 1975), as indicated by such features as the relatively Order Carnivora well developed median lingual cleft that ends well before the Homotherium latidens cervix and the moderate cusp relief with a shallow median buccal Pachycrocuta brevirostris Lycaon sp. notch relative to crown height. The crown displays some degree Canis mosbachensis of lingual flare, with buccal cusps being much more peripheral Carnivora indet. than the lingual ones, and occlusal foveae mainly buccal. The Order Primates mesial fovea is more restricted and shallower than the trigon Macaca sylvanus florentina basin, but better developed than the distal fovea and, together with the well-developed mesial marginal ridge, it constitutes a 2014), although the younger boundary of this estimate has been ledge-like mesial enamel extension. No distal accessory cuspules most recently revised down to 1.2 Ma, due to the identification of seem to have been present originally, although due to wear this Metacervocerus rhenanus and Capreolus sp. (Madurell-Malapeira cannot be determined definitively. There are no cingular rem- and Martínez-Navarro, in press;seealsoTable 1), and in further nants, except for a small enamel indentation on the shallow agreement with the lack of Sus ex gr. scrofa (Martínez-Navarro mesial lingual cleft, and a short vertical groove on the corre- et al., 2015). sponding buccal side of the crown.

Figure 2. Left M2 of Macaca sylvanus ﬂorentina from Incarcal IN-I 1960, in occlusal (a), mesial (b), buccal (c), distal (d) and lingual (e) views. In occlusal view (a), mesial is to the left. 142 D.M. Alba et al. / Journal of Human Evolution 96 (2016) 139e144

Overall, the generalized papionin occlusal pattern displayed by also true of the Incarcal specimen. The identification of the latter as the Incarcal molar is fully compatible with an assignment to Macaca an M2 further agrees with the distinct but moderate distal tapering (Fig. 3). The crown measurements of the Incarcal molar (mesio- of the crown (buccolingual breadth in the distal lobe 9.3 mm), since distal length 10.1 mm; maximum buccolingual breadth 10.4 mm, tapering is usually less marked in M1 and more accentuated in M3. taken on the mesial lobe) are beyond the metrical variability of M1 Moreover, the latter generally display a more oval occlusal contour in both extant and fossil M. sylvanus, and in contrast fit well with with a convex distal margin, and identification as an M3 is in any the size range and proportions of M2 in M. s. florentina (Fig. 4; see case ruled out by the presence of a distal contact facet. A taxonomic also Fig. 3deg). In spite of considerable overlap in dental size with assignment to Paradolichopithecus, the other papionin recorded in extant M. s. sylvanus, it has been argued that M. s. florentina differs the Early Pleistocene of Iberia (Delson et al., 2014; Marigo et al., metrically in some respects (Alba et al., 2011), such as larger and 2014), can be also confidently discounted based on the larger size relatively wider upper molars on average (as seen in Fig. 4), as is of Paradolichopithecus (Fig. 4).

Figure 3. Left M2 of Macaca sylvanus florentina from Incarcal (a) compared to the same tooth locus in extant M. s. sylvanus (b, c), M. s. cf. florentina from Vallparadís (d, e; see Alba et al., 2008), and M. s. florentina from Quibas (f, g; see Alba et al., 2011): a, IN-I 1960; b, AMNH2060/5484; c, AMNH19014 (reversed); d, IPS64216 (EVT22372, reversed); e, IPS64217 (EVT24036); f, Q05-Ec-88 (reversed); g, GCP-CV4054 (reversed). All specimens are depicted in occlusal view as if from the left side; mesial is to the left.

Figure 4. Bivariate plot of maximum buccolingual breadth (in mm) versus mesiodistal length (in mm) in the M2 of Macaca sylvanus ﬂorentina from Incarcal, compared to extant M. s. sylvanus and fossil European papionins (M. sylvanus sspp. and Paradolichopithecus arvernensis). Data for the comparative sample were measured by the authors, taken from NYCEP's PRIMO (PRImate Morphometrics Online) database (http://primo.nycep.org), or taken from the literature (Zanaga, 1998; Rook et al., 2001; Alba et al., 2008, 2011). D.M. Alba et al. / Journal of Human Evolution 96 (2016) 139e144 143

3. Discussion and conclusions with herbaceous vegetation (Hanya et al., 2011). The Barbary macaque further shows a preference for seeds (when available) 3.1. Taxonomic attribution over leaves (Hanya et al., 2011). In this regard, the recovery of abundant fossilized walnuts at Incarcal I (Buxo, 2003) suggests Based on morphological, metrical and biochronological grounds, that the depositional environment might have been a suitable the Incarcal molar is here assigned to M. s. florentina. Although feeding site for macaques, with a humid riparian forest probably fossil macaques are relatively well recorded in the Iberian Penin- developed around the ponds (Buxo, 2003). Overall, the Incarcal sula (Marigo et al., 2014) and elsewhere in Europe (Elton and paleoenvironment would not have been optimal for macaques O'Regan, 2014), their presence in Early Pleistocene Iberian sites is (which might explain the scarcity of their remains), but is likely to quite limited. For example, this subspecies had been previously have been an area they regularly visited for drinking, feeding, and reported from the roughly coeval Iberian site of Quibas (ca. sheltering from predators. 1.3e1.0 Ma; Alba et al., 2011; Fig. 3f,g) and, tentatively, from the somewhat younger section of Vallparadís (1.0e0.8 Ma; Alba et al., Acknowledgments 2008; Fig. 3d,e). Macaca sp. was also reported from Sima del Ele- fante in Atapuerca (1.2 Ma; Carbonell et al., 2008; Huguet et al., The research reported in this work has been funded by the 2013), but the material is unpublished and most recently Huguet Spanish Ministerio de Economía y Competitividad (CGL2014- et al. (2015) merely attributed it to Cercopithecidae. In any case, 54373-P) and the Generalitat de Catalunya (2014 SGR 416 GRC and macaques have not been reported from other well-sampled and 2014 SGR 901, and predoctoral grant 2015FI-B00088 to VV), while roughly coeval Iberian sites, such as Venta Micena (ca. 1.6e1.5 Ma), recent fieldwork at Incarcal has been further supported by the Barranco Leon (ca. 1.4 Ma) and Fuente Nueva 3 (ca. 1.3 Ma), which Generalitat de Catalunya (2014/100589). We acknowledge the otherwise show strong faunal similarities to Incarcal (Palmqvist collaboration of the Servei d'Arqueologia and Paleontologia of the et al., 2003; Martínez-Navarro et al., 2010; Toro-Moyano et al., Generalitat de Catalunya, the company Yesos Ibericos (which 2013; Madurell-Malapeira et al., 2014). currently exploits the Cal Taco quarry), and the staff of the Museu Arqueologic Comarcal de Banyoles. We are also grateful to Eileen 3.2. Paleoenvironmental implications Westwig for access to extant comparative material in the American Museum of Natural History Department of Mammalogy; to Josep The presence of Hippopotamus antiquus at Incarcal is particularly Manel Mendez, for finding the macaque molar reported in this informative from a paleoenvironmental viewpoint, since it in- paper; to Salvador Moya-Sol a, for discussions about the fossil ma- dicates unambiguously that the climate was quite warm. This terial; to all the volunteers that, over the years, participated in the agrees with the presence of macaques, since extant M. sylvanus excavations at Incarcal; and to two anonymous reviewers, the habitats are characterized by a Mediterranean climate with warm Associate Editor (Melissa Tallman) and the Editor (Sarah Elton), for summers (Fooden, 2007), and cold temperatures represent a helpful comments and suggestions on a previous version of this serious threat to their survival (by restricting access to trophic re- paper. sources; McFarland and Majolo, 2013). Paleontological data further suggest that the past distribution of M. sylvanus in Europe was References largely determined by climatic factors, as the species expanded northward during the interglacials and retreated into Mediterra- Alba, D.M., Moya-Sol a, S., Madurell, J., Aurell, J., 2008. Dentognathic remains of Macaca (Primates, Cercopithecidae) from the late early Pleistocene of Terrassa nean areas during the glacials (Fooden, 2007; Elton and O'Regan, (Catalonia, Spain). J. Hum. Evol. 55, 1160e1163. 2014). Evergreen forests with a nearby water supply appear to be Alba, D.M., Carlos Calero, J.A., Mancheno,~ M.A., Montoya, P., Morales, J., Rook, L., the optimal biotope of extant M. sylvanus, since these monkeys 2011. Fossil remains of Macaca sylvanus florentina (Cocchi, 1872) (Primates, need to be near water and, in spite of being largely terrestrial, still Cercopithecidae) from the Early Pleistocene of Quibas (Murcia, Spain). J. Hum. Evol. 61, 703e718. require trees for sleeping, feeding and avoiding predators (Fooden, Alba, D.M., Delson, E., Carnevale, G., Colombero, S., Delfino, M., Giuntelli, P., 2007; Masseti and Bruner, 2009). The abundance of H. antiquus, Pavia, M., Pavia, G., 2014. First joint record of Mesopithecus and cf. Macaca in the e which fed on aquatic vegetation and was tightly linked to water Miocene of Europe. J. Hum. Evol. 67, 1 18. fi Alba, D.M., Montoya, P., Pina, M., Rook, L., Abella, J., Morales, J., Delson, E., 2015. First (Palmqvist et al., 2003; Martínez-Navarro et al., 2010), con rms the record of Mesopithecus (Cercopithecidae, Colobinae) from the Miocene of the presence of nearby permanent water, most likely in the very same Iberian Peninsula. J. Hum. Evol. 88, 1e14. depositional environment, as suggested by permanent ponds of Anton,M.,Galobart,A.,1999.Neckfunctionandpredatorybehaviorinthe scimitar toothed cat Homotherium latidens (Owen). J. Vert. Paleontol. 19, karstic origin currently established in the same area (Madurell- 771e784. Malapeira and Martínez-Navarro, in press). Anton, M., Galobart, A., Turner, A., 2005. Co-existence of scimitar-toothed cats, lions With regard to vegetation, although the macroflora and pollen and hominins in the European Pleistocene. Implications of the post-cranial anatomy of Homotherium latidens (Owen) for comparative palaeoecology. from the limestones of Crespia indicate a well-developed decid- Quaternary Sci. Rev. 24, 1287e1301. uous forest and a mild climate with Mediterranean influence Azzaroli, A., 1946. La scimmia fossile della Sardegna. Riv. Sci. Preist. 1, 68e76. (Roiron, 1983), the somewhat younger mammalian fauna from Buxo, R., 2003. Presencia de semillas y frutos de nogal en el yacimiento de Incarcal I (Girona, NE de la Península Iberica). Paleontol. Evol. 34, 43e46. Incarcal suggests more open (woodland) habitats (Galobart and Canals, A., Galobart, A., 2003. Arqueoestratigrafía y reconstruccion de la dinamica Agustí, 2003). Although open biotopes are not optimal for sedimentaria en los yacimientos del Pleistoceno inferior de Incarcal I e Incarcal extant M. sylvanus, they are not at odds with the presence of this V. Paleontol. Evol. 34, 221e232. taxon at Incarcal, since this species currently inhabits a wide va- Carbonell, E., Bermúdez de Castro, J.M., Pares, J.M., Perez-Gonzalez, A., Cuenca- Bescos, G., Olle, A., Mosquera, M., Huguet, R., van der Made, J., Rosas, A., Sala, R., riety of biotopes, including not only forests of conifers (cedar and Vallverdú, J., García, N., Granger, D.E., Martinon-Torres, M., Rodríguez, X.P., fir) and oaks (both deciduous and evergreen), but also more open Stock, G.M., Verges, J.M., Allue, E., Burjachs, F., Caceres, I., Canals, A., Benito, A., areas dominated by herbaceous vegetation (such as scrub, grass- Díez, C., Lozano, M., Mateos, A., Navazo, M., Rodríguez, J., Rosell, J., Arsuaga, J.L., 2008. The first hominin of Europe. Nature 452, 465e469. lands and rocky ridges; Fooden, 2007). In fact, the diet of extant Cocchi, I., 1872. Su di due Scimmie fossili italiane. Boll. R. Comit. Geol. Ital. 3, 59e71. M. sylvanus (and probably that of fossil European macaques as Delson, E., 1973. Fossil colobine monkeys of the circum - Mediterranean region and well; Elton and O'Regan, 2014), besides being more folivorous the evolutionary history of the Cercopithecidae (Primates, Mammalia). Ph.D. Dissertation, Columbia University. than that of tropical macaques (allowing them to cope with sea- Delson, E., 1975. Evolutionary history of the Cercopithecidae. Contrib. Primatol. 5, sonal variation in fruit availability), is regularly complemented 167e217. 144 D.M. Alba et al. / Journal of Human Evolution 96 (2016) 139e144

Delson, E., 1980. Fossil macaques, phyletic relationships and a scenario of deploy- Maroto, J., Galobart, A., 1991. Incarcal (Crespia, Pla de l'Estany): un jaciment re- ment. In: Lindburg, D.E. (Ed.), The Macaques. Studies in Ecology, Behavior and presentatiu de la fauna de grans mamífers del plistoce inferior. Trib. Arqueol. Evolution. Van Nostrand, New York, pp. 10e30. 1990, 7e15. Delson, E., Alba, D.M., Frost, S.R., Harcourt-Smith, W.E., Martín Suarez, E., Maroto, J., Sanz, E., Galobart, A., 2003a. Antecedentes de las excavaciones en los Mazelis, E.J., Morales, J., Moya-Sol a, S., Shearer, B.M., 2014. Paradolichopithecus,a yacimientos pleistocenos de Incarcal (Girona, NE de la Península Iberica). large terrestrial Pliocene cercopithecine from Europe: New remains and an Paleontol. Evol. 34, 25e30. update. In: Delfino, M., Carnevale, G., Pavia, M. (Eds.), Abstract Book and Field Maroto, J., Galobart, A., Menendez, E., Ros, X., Soler, N., Moya-Sol a, S., Marín, M., Trip Guide, XII Annual Meeting of the European Association of Vertebrate Agustí, J., Sanz, E., Gibert, J., 2003b. Las excavaciones en los yacimientos pleis- Palaeontologists, Torino - Italy 24e28 June 2014. Museo Regionale di Scienze tocenos de Incarcal (Girona, NE de la Península Iberica). Campanas~ 1984-1990. Naturali, Regione Piemonte, Torino, p. 50. Paleontol. Evol. 34, 31e41. Elton, S., O'Regan, H.J., 2014. Macaques at the margins: the biogeography and Martínez-Navarro, B., Palmqvist, P., Madurell-Malapeira, J., Ros-Montoya, S., extinction of Macaca sylvanus in Europe. Quaternary Sci. Rev. 96, 117e130. Espigares, M.P., Torregrosa, V., Perez-Claros, J.A., 2010. La fauna de grandes Fooden, J., 1976. Provisional classification and key to living species of macaques mamíferos de Fuente Nueva-3 y Barranco Leon-5: Estado de la cuestion. In: (Primates: Macaca). Folia Primatol. 25, 225e236. Toro, I., Martínez-Navarro, B., Agustí, J. (Eds.), Ocupaciones Humanas en el Fooden, J., 2007. Systematic review of the Barbary macaque, Macaca sylvanus Pleistoceno Inferior y Medio de la Cuenca de Guadix-Baza. Junta de Andalucía, (Linnaeus, 1758). Fieldiana Zool. 113, 1e60. Consejería de Cultura, pp. 197e236. Galobart, A., 1996. Estudi de la fauna de mamífers dels jaciments del Plistoce Martínez-Navarro, B., Madurell-Malapeira, J., Ros-Montoya, S., Espigares, M.P., inferior d’Incarcal (Crespia, Pla de l'Estany): sistematica, tafonomia i paleo- Medin, T., Hortola, P., Palmqvist, P., 2015. The Epivillafranchian and the arrival of ecologia. Ph.D. Dissertation, Universitat Autonoma de Barcelona. pigs into Europe. Quatern. Int. 389, 131e138. Galobart, A., 2003a. Origen de las acumulaciones, diversidad y reconstruccion de los Masseti, M., Bruner, E., 2009. The primates of the western Palaearctic: a biogeo- yacimientos Incarcal I e Incarcal V. Paleontol. Evol. 34, 233e244. graphical, historical, and archaeozoological review. J. Anthropol. Sci. 87, 33e91. Galobart, A., 2003b. Aspectos tafonomicos de los yacimientos del Pleistoceno McFarland, R., Majolo, B., 2013. Coping with the cold: predictors of survival in wild inferior de Incarcal (Crespia, NE de la Península Iberica). Paleontol. Evol. 34, Barbary macaques, Macaca sylvanus. Biol. Lett. 9, 20130428. 211e220. Meloro, C., Elton, S., 2012. The evolutionary history and palaeo-ecology of primate Galobart, A., Agustí, J., 2003. Paleoecología de los yacimientos del Pleistoceno predation: Macaca sylvanus from Plio-Pleistocene Europe as a case study. Folia inferior de Incarcal (Girona, NE de la Península Iberica). Paleontol. Evol. 34, Primatol. 83, 216e235. 245e266. Modolo, L., Salzburger, W., Martin, R.D., 2005. Phylogeography of Barbary macaques Galobart, A., Maroto, J. (Eds.), 2003. Los yacimientos paleontologicos de Incarcal (Macaca sylvanus) and the origin of the Gibraltar colony. Proc. Natl. Acad. Sci. (Crespia). Paleontol. Evol. 34, 1e299. 102, 7392e7397. Galobart, A., Blaya, E., Madurell, J., Ros, X., Maroto, J., 2010. Resultats de la segona Owen, R., 1846. A History of British Fossil Mammals and Birds. John Van Voorst, fase d'actuacions (1999-2005) als jaciments paleontologics del Plistoce Inferior London. d'Incarcal (Crespia, Pla de l'Estany). Treb. Paleontol. 1, 59e98. Palmqvist, P., Grocke,€ D.R., Arribas, A., Farina,~ R.A., 2003. Paleoecological recon- Gervais, P., 1859. Zoologie et Paleontologie Françaises, second ed. Bertrand, Paris. struction of a lower Pleistocene large mammal community using biogeo- Hanya, G., Menard, N., Qarro, M., Tattou, M.I., Fuse, M., Vallet, D., Yamada, A., Go, M., chemical (v13C, v15N, v18O, Sr:Zn) and ecomorphological approaches. Takafumi, H., Tsujino, R., Agetsuma, N., Wada, K., 2011. Dietary adaptations of Paleobiology 29, 205e229. temperate primates: comparisons of Japanese and Barbary macaques. Primates Pons-Moya, J., Moya-Sol a, S., 1992. Observacions sobre l'evolucio i biologia del 52, 187e198. genere Homotherium Fabrini, 1890 (Mammalia, Carnivora). Boll. Soc. Hist. Nat. Huguet, R., Saladie, P., Caceres, I., Díez, C., Rosell, J., Bennasar, M., Blasco, R., Esteban- Bal. 35, 88e92. Nadal, M., Gabucio, M.J., Rodríguez-Hidalgo, A., Carbonell, E., 2013. Successful Roiron, P., 1983. Nouvelle etude de la macroflore Plio-Pleistocene de Crespia (Cat- subsistence strategies of the first humans in south-western Europe. Quatern. alogne, Espagne). Geobios 16, 687e715. Int. 295, 168e182. Rook, L., O'Higgins, P., 2005. A comparative study of adult facial morphology and its Huguet, R., Vallverdú, J., Rodríguez-Alvarez, X.P., Terradillos-Bernal, M., Bargallo, A., ontogeny in the fossil macaque Macaca majori from Capo Figari, Sardinia, Italy. Lombera-Hermida, A., Menendez, L., Modesto-Mata, M., Van der Made, J., Folia Primatol. 76, 151e171. Soto, M., Blain, H.-A., García, N., Cuenca-Bescos, G., Gomez-Merino, G., Perez- Rook, L., Mottura, A., Gentili, S., 2001. Fossil Macaca remains from RDB quarry Martínez, R., Exposito, I., Allue, E., Rofes, J., Burjachs, F., Canals, A., Bennasar, M., (Villafranca d'Asti, Italy): new data and overview. J. Hum. Evol. 40, 187e202. Nunez-Lahuerta,~ C., Bermúdez de Castro, J.M., Carbonell, E., 2015. Level TE9c of Roos, C., Zinner, D., 2015. Diversity and evolutionary history of macaques with Sima del Elefante (Sierra de Atapuerca, Spain): a comprehensive approach. special focus on Macaca mulatta and Macaca fascicularis. In: Bluemel, J., Quatern. Int. http://dx.doi.org/10.1016/j.quaint.2015.11.030. Korte, S., Schenck, E., Weinbauer, G. (Eds.), The Nonhuman Primate in Julia, R., de Villalta, J.F., 1984. El yacimiento de vertebrados del Pleistoceno inferior Nonclinical Drug Development and Safety Assessment. Elsevier, Amsterdam, de Crespia (Girona, NE de la Península Iberica). Acta Geol. Hisp. 19, 129e139. pp. 3e16. Kohler,€ M., Moya-Sol a, S., Alba, D.M., 2000. Macaca (Primates, Cercopithecidae) Ros, X., Palomar, J., 2003. Contexto geografico y geologico de los yacimientos plio- from the Late Miocene of Spain. J. Hum. Evol. 38, 447e452. pleistocenos de Incarcal (Girona, NE de la Península Iberica). Paleontol. Evol. 34, Lacep ede, B.G.E. de la V., 1799. Tableau des divisions, sous-divisions, ordres et 13e22. genres des mammiferes. In: Discours d'Ouverture et de Cloture^ du Cours Ros, X., Galobart, A., Maroto, J., Gaete, R., Ortega-Cobos, D., Sintes, X., 2003. d'Histoire Naturelle, Donne dans le Museum National d'Histoire Naturelle, l'An Excavacion de un Stephanorhinus etruscus en las calizas de Crespia (Girona, NE VII de la Republique, et Tableaux Methodiques des Mammiferes et des Oiseaux. de la Península Iberica). Paleontol. Evol. 34, 269e277. Plassan, Paris. Ros-Montoya, S., Madurell-Malapeira, J., Martínez-Navarro, B., Espigares, M.P., Linnaeus, C., 1758. Systema Naturae per Regna Tria Naturae, secundum Classes, Palmqvist, P., 2012. Late Villafranchian Mammuthus meridionalis (Nesti, 1825) Ordines, Genera, Species, cum Characteribus, Differentiis, Synonymis, Locis. In: from the Iberian Peninsula: Dentognathic remains from Incarcal-I (Crespia, vol. I: Regnum Animale. Editio Decima, Reformata. Laurentii Salvii, Stockholm. Girona) and Venta Micena (Orce, Granada). Quatern. Int. 276e277, 17e22. Madurell-Malapeira, J., Ros-Montoya, S., Espigares, M.P., Alba, D.M., Aurell- Springer, M.S., Meredith, R.W., Gatesy, J., Emerling, C.A., Park, J., Rabosky, D.L., Garrido, J., 2014. Villafranchian large mammals from the Iberian Peninsula: Stadler, T., Steiner, C., Ryder, O.A., Janecka, J.E., Fisher, C.A., Murphy, W.J., 2012. paleobiogeography, paleoecology and dispersal events. J. Iber. Geol. 40, Macroevolutionary dynamics and historical biogeography of primate diversifi- 167e178. cation inferred from a species supermatrix. PLoS One 7, e49521. Madurell-Malapeira, J., Martínez-Navarro, B., in press. Reinici dels treballs als jaci- Szalay, F., Delson, E., 1979. Evolutionary History of the Primates. Academic Press, ments del Pleistoce inferior del complex d'Incarcal (Crespia, Pla de l'Estany): New York. campanyes 2009e2013. Trib. Arqueol. Toro-Moyano, I., Martínez-Navarro, B., Agustí, J., Souday, C., Bermúdez de Majolo, B., van Lavieren, E., Marechal, L., MacLarnon, A., Marvin, G., Qarro, M., Castro, J.M., Martinon-Torres, M., Fajardo, B., Duval, M., Falgueres, C., Oms, O., Semple, S., 2013. Out of Asia: The singular case of the Barbary macaque. In: Pares, J.M., Anadon, P., Julia, R., García-Aguilar, J.M., Moigne, A.-M., Radhakrishna, S., Huffman, M.A., Sinha, A. (Eds.), The Macaque Connection. Espigares, M.P., Ros-Montoya, S., Palmqvist, P., 2013. The oldest human fossil in Cooperation and Conflict between Humans and Macaques. Springer, New York, Europe, from Orce (Spain). J. Hum. Evol. 65, 1e9. pp. 167e183. de Villalta, J.F., Vicente, J., 1972. Una flora del Cuaternario antiguo en las cercanías de Marigo, J., Susanna, I., Minwer-Barakat, R., Madurell-Malapeira, J., Moya-Sol a, S., Crespia. Acta Geol. Hisp. 7, 120e128. Casanovas-Vilar, I., Robles, J.M., Alba, D.M., 2014. The primate fossil record in the Zanaga, M., 1998. Macaca majori Azzaroli 1946, primate endemico del Pleistocene Iberian Peninsula. J. Iber. Geol. 40, 179e211. della Sardegna. Unpublished thesis, Universita degli Studi di Firenze.