Journal of Human Evolution 123 (2018) 141E147

Journal of Human Evolution 123 (2018) 141e147

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Journal of Human Evolution

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Macaque remains from the early Pliocene of the Iberian Peninsula

* David M. Alba a, , Eric Delson b, c, d, e, a, Jorge Morales f, Plini Montoya g, Gregorio Romero h, i 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 PhD Program in Anthropology, The Graduate Center of the City University of New York, 365 Fifth Avenue, New York, NY 10016, USA e New York Consortium in Evolutionary Primatology, New York, NY, USA f Departamento de Paleobiología, Museo Nacional de Ciencias Naturales (CSIC), Jose Gutierrez Abascal 2, 28006 Madrid, Spain g Departament de Botanica i Geologia, Universitat de Valencia, Doctor Moliner 50, 46100 Burjassot, Spain h Direccion General de Bienes Culturales de la CARM, Casa Díaz Cassou, C/ Santa Teresa 21, 30071 Murcia, Spain i Grupo de Investigacion de Geología, Facultad de Química, Universidad de Murcia, 30100 Murcia, Spain article info abstract

Article history: Macaques dispersed out of Africa into Eurasia in the framework of a broader intercontinental faunal Received 28 March 2018 exchange that coincided in time with the sea level drop associated with the Messinian Salinity Crisis. Accepted 16 July 2018 They are first recorded in Europe (Italy and Spain) by the latest Miocene, being subsequently recorded all Available online 20 August 2018 over Europe, albeit sparsely, throughout the Pliocene and Pleistocene. These fossil European macaques are attributed to several (sub)species of the extant Barbary macaque (Macaca sylvanus). In Iberia, fossil Keywords: macaques are best documented by Macaca sylvanus florentina from various Early Pleistocene sites, Macaca whereas their published Pliocene record is very scarce. Here we report the oldest post-Messinian Messinian Turolian occurrence of macaques in the Iberian Peninsula, based on the description and metrical comparisons Puerto de la Cadena of two upper teeth (a male canine and a third molar of two different individuals) from the early Pliocene 1 Murcia (MN14, 5.0e4.9 Ma) site of Puerto de la Cadena (Murcia, SE Spain). The male C is fully comparable in 3 Spain morphology with those of extant and fossil M. sylvanus, and larger than those of Mesopithecus. The M ,in turn, displays the typical papionin morphology that characterizes the dentally-conservative genus Macacadthereby discounting an alternate assignment to either the extinct colobine monkey Meso- pithecus or the more dentally-derived papionin Theropithecus. Dental size and proportions of the M3 further support an attribution to an extinct subspecies of M. sylvanus instead of the larger papionin Paradolichopithecus. Mostly on biochronologic grounds, the two macaque teeth from Puerto de la Cadena are here assigned to Macaca sylvanus cf. prisca, albeit tentatively, given the lack of clear-cut criteria to distinguish this subspecies from the younger Macaca sylvanus florentina. The described material repre- sents the oldest well-dated Pliocene record of macaques in Iberia, predating the record of Para- dolichopithecus by almost 1.5 million years. © 2018 Elsevier Ltd. All rights reserved.

1. Introduction Peninsula) have been known for many decades, particularly on the basis of two sites (La Alberca and La Paloma) correlated to the latest 1.1. Puerto de la Cadena Miocene Mammal Neogene (MN) unit MN13 (Montenat and Crusafont, 1970; Mein et al., 1973; Aguirre et al., 1974; de Bruijn Continental fossil vertebrates from the late Neogene fossili- et al., 1975; Morales, 1984; Lopez Martínez, 1989; Freudenthal ferous outcrops of the Puerto de la Cadena area (Murcia, SE Iberian et al., 1998; Mancheno~ Jimenez and Fierro Bandera, 2011; Perez- García et al., 2011; Morales et al., 2013). The location in 2008 of a new site, due to the construction of highway MU-31 in the area of Puerto de la Cadena, led to the discovery of more than 2000 fossil * Corresponding author. E-mail address: [email protected] (D.M. Alba). remains during successive emergency paleontological works in the https://doi.org/10.1016/j.jhevol.2018.07.005 0047-2484/© 2018 Elsevier Ltd. All rights reserved. 142 D.M. Alba et al. / Journal of Human Evolution 123 (2018) 141e147 following three years (Mancheno~ Jimenez and Fierro Bandera, 2. Age and geological background 2011; Pinero~ et al., 2017). This fossil vertebrate assemblage from Puerto de la Cadena was recently described by Pinero~ et al. (2017). The site of Puerto de la Cadena is located 8 km SW of the city of Although preliminary accounts suggested a latest Miocene age for Murcia (Fig. 1), close to the towns of La Alberca and El Palmar, on this site (Mancheno~ et al., 2013), Pinero~ et al. (2017) conclusively the northern flank of the Sierra de Carrascoy y el Valle. From a correlated it to the early Pliocene. Among the 26 reported species, geological viewpoint, the fossiliferous outcrops of Puerto de la Pinero~ et al. (2017) noted the presence of a cercopithecine, which Cadena (Murcia-Carrascoy Basin) belong to the Cigarron Unit, on the basis of the two available teeth was assigned to Macaca sp. whose sediments were deposited under shallow marine conditions towards the bottom and within a continental setting towards the top (Pinero~ et al., 2017). The lower boundary of this unit consists of 1.2. The fossil macaques from the Iberian Peninsula an erosional surface that has been correlated to the end-Messinian discontinuity, thus being interpreted as a post-Messinian regressive Macaques are first recorded in Eurasia by the latest Miocene sequence (Pinero~ et al., 2017). The site of Puerto de la Cadena is (MN13), based on fossil remains from Almenara-Casablanca M, located in the upper portion of the Cigarron Unit, being composed Spain (Kohler€ et al., 2000) and Moncucco Torinese, Italy (Alba et al., of alternating sandstones and mudstones with some conglomeratic 2014), all assigned to cf. Macaca sp. The remains from Moncucco layers, indicative of a fluvial depositional environment with chan- Torinese are confidently dated to 5.41e5.33 Ma (Colombero et al., nels and floodplain development (Mancheno~ Jimenez and Fierro 2017), whereas those from Almenara-Casablanca M are roughly Bandera, 2011; Pinero~ et al., 2017). contemporaneous with the Messinian Salinity Crisis (ca. 5.9e5.3 Magnetostratigraphic analyses (Pinero~ et al., 2017) indicate that Ma; Agustí et al., 2006; Minwer-Barakat et al., 2009; Alba et al., the short section from Puerto de la Cadena records a reverse 2014). Coupled with the lack of papionin remains from older lo- magnetozone, which is also recorded in the upper portion of the calities in Eurasia as a whole, this evidence suggests that macaques nearby Barranco del Cigarron section, being correlated to either probably did not disperse out of Africa until the sea level drop C3n.3r (4.997e4.896 Ma; Ogg, 2012) or C3n.2r (4.799e4.631 Ma; associated with the Messinian Salinity Crisis (Agustí et al., 2006; Ogg, 2012). Correlation with the former has been favored on Alba et al., 2014, 2015; Colombero et al., 2017). biostratigraphic grounds by Pinero~ et al. (2017:112), who further It is uncertain whether macaques dispersed into Europe through considered the fauna from Puerto de la Cadena to be “earliest southern Iberia or followed the Middle East route that was already MN14”. These authors advocated for the placement of the MN13/ available from pre-Messinian times (Alba et al., 2015). In any case, MN14 boundary within C3n.3r (i.e., about 0.3 million years younger the dispersal of macaques coincides with a major mammalian than the Miocene/Pliocene boundary at 5.33 Ma), in agreement turnover that took place ca. 5.5e5.3 Ma and involved multiple with previous proposals by some authors (Opdyke et al., 1997; intercontinental dispersals between Africa and Europedthe so- Agustí et al., 2001). However, such a proposal is at odds with the called ‘Gerbil Event’ (Agustí et al., 2006)or‘Third African-Iberian most common, recently strongly supported view that the MN13/ Dispersal’ (Gibert et al., 2013). Subsequently, during the Plio- MN14 boundary is somewhat older and might even roughly coin- Pleistocene, European fossil macaques are represented by several cide with the Miocene/Pliocene boundary (García-Alix et al., 2008; taxa that belong to the lineage of Macaca sylvanus (Linnaeus, 1758), Minwer-Barakat et al., 2012b; Pinero~ and Agustí, 2017; Pinero~ et al., the extant Barbary macaque from northern Africa (Delson, 1974, 2018). 1980; Szalay and Delson, 1979; Alba et al., 2011, 2014, 2016), Pinero~ et al. (2017) did not provide positive evidence for their which on phylogenetic evidence is considered the basal-most interpretation of Puerto de la Cadena as earliest MN14. They member of the genus (e.g., Springer et al., 2012). The Plio- correctly indicated that it appears to be ca. 200 kyr younger than Pleistocene remains of European macaques are customarily Sifon 413, which occurs just above the local end-Messinian erosion attributed to chronologically successive subspecies of M. sylvanus, and thus must be within the Pliocene, at ca. 5.3 Ma, but they did not which due to the lack of cranial remains are not particularly well correlate Sifon 413 to a MN unit. Pinero~ and Agustí (2017) revised characterized (Szalay and Delson, 1979; Delson, 1980; Alba et al., the rodent assemblages from the Sifon de Librilla section (Fortuna 2008, 2011, 2016; Marigo et al., 2014). Only the endemic macaque Basin) and made a good case that Sifon 413 yielded several taxa from Sardinia, Macaca majori Azzaroli, 1946, is customarily indicative of MN14, especially Occitanomys brailloni, which they considered distinct enough from extant M. sylvanus to be consid- suggested is the best marker for the beginning of MN14 in southern ered a separate species (Zanaga, 1998; Rook and O'Higgins, 2005; Spain. Therefore, Puerto de la Cadena does not represent the Smith et al., 2014). Early Pliocene macaques from Europe are customarily assigned to M. sylvanus prisca Gervais, 1859, which ranges from the earliest Ruscinian to the early Villafranchian (MN14eMN16; Szalay and Delson, 1979; Delson, 1980). The oldest record corre- sponds to the site of Montpellier, France (type locality; MN14, ~5 Ma), followed by Csarnota 2, Hungary (late MN15, ~3.6e3.2 Ma; Minwer-Barakat et al., 2012a) and several MN16 localities, such as Fornace RDB, Italy (early MN16, ~3.2e3.0 Ma; see Rook et al., 2001, and references therein). Although M. s. prisca was considered to be somewhat smaller than more recent and extant subspecies (Szalay and Delson, 1979; Delson, 1980), subsequent works have failed to substantiate such claims (Delson et al., 2000; Rook et al., 2001). Here we figure and describe in detail the fossil macaque remains from Puerto de la Cadena, which represent the oldest securely dated record of Macaca from the Iberian Pliocene, and tentatively one of the oldest occurrences of M. s. prisca in Figure 1. Location map of Puerto de la Cadena within the Iberian Peninsula (left) and Europe. within the province of Murcia (inset, right). D.M. Alba et al. / Journal of Human Evolution 123 (2018) 141e147 143 earliest part of MN14, although with an age of 5.0e4.9 Ma, it can be displays some degree of rounding and erosion overall (most conclusively correlated to both MN14 and the early Pliocene. evident at the crown and root preserved apices), which suggests some transport before burial. It also shows marked abrasion 3. Material and methods throughout the surface of the root and the crowndnot only are some superficial flakes of enamel and cement missing, but the The macaque fossil remains from Puerto de la Cadena described remaining portions of the root and crown are abraded, probably here consist of a left C1 (MAM VLP3-62) and a left M3 (MAM VLP2- indicating soil acid corrosion. 715). Although these remains were originally studied by the senior On the basis of its large dimensions, extension of the mesio- author of this paper in 2013 at the Museo Paleontologico de Elche lingual groove onto the root and overall dagger-like morphology, (MUPE; Elche, Spain), they are currently housed at the Museo this canine can be attributed to a male individual. Both the root and Arqueologico de Murcia (MAM; Murcia, Spain). These teeth corre- the preserved portion of the crown display a labiolingually com- spond to two different individuals, since they were recovered from pressed (crown breadth/length index 77%), subtriangular cross- two different outcropping slopes of the site (no. 3 in the case of the section. The root is somewhat tilted distally, displaying in buccal C1, and no. 2 in the case of the M3). The acronym (VLP) of the catalog and lingual views a rather straight distal contour, but a more numbers stands for ‘Venta La Paloma,’ which is the informal name markedly convex mesial profile. There is a broad and marked originally given to the site that is currently known as Puerto de la mesiolingual sulcus that runs along the root and the crown through Cadena (Pinero~ et al., 2017). the cervix, as well as a shallower and more diffuse lingual sulcus. Measurements of mesiodistal crown length (MD) and bucco- These sulci result in biconvex lingual and, especially, mesial pro- lingual crown breadths (BL), taken to the nearest 0.1 mm with a files, which contrast with the flat or even slightly convex buccal digital caliper, were used to compare the Puerto de la Cadena sides of the root and the crown, respectively. The crown is broken specimens with other available samples of extant M. sylvanus, fossil away obliquely to a large extent, so that only its basal portion is Macaca and Paradolichopithecus (and for canines, Mesopithecus preserved (especially on the mesial and buccal sides), thereby species and Dolichopithecus ruscinensis) from Europe. In the case of exposing the pulp cavity. The cementoenamel junction on the upper canines, MD was defined as the maximum crown diameter, buccal side shapes a shallow inverted ‘V’. Distally, the basal-most and BL as the maximum crown diameter perpendicular to MD. portion of the honing facet against the P3, which extends basally Bivariate dental plots of BL vs. MD were employed to visually assess beyond the cervix, is preserved. the size and proportions of the dental remains from Puerto de la Cadena with regard to the comparative sample. Given that canines Upper molar Only the crown of this tooth is preserved (Fig. 2aee). are generally not diagnostic to distinguish between cercopithecid Although small portions of enamel are missing at some points close subfamilies (e.g., Delson, 1973; Hill and Gundling, 1999; Delson to the cervix, the overall dimensions of the crown can be reliably et al., 2005), and the fact that Macaca is known to co-occur with taken (MD ¼ 10.2 mm, mesial BL ¼ 10.2 mm, distal BL ¼ 8.5 mm; the colobines Mesopithecus and/or Dolichopithecus in some Pliocene see also SOM Table S1). This tooth displays only a slight degree of localities (Delson, 1974; Szalay and Delson, 1979; Delson et al., wear, with very minimal dentine exposure at the apices of all 2005), upper canine measurements for the latter genera were main cusps except the paracone. There is a small contact facet on also included in the comparisons. Dental measurements for the the mesial crown wall, but no distal contact facet; in combination Puerto de la Cadena specimens and the comparative sample are with the marked distal tapering and the presence of an accessory reported in Supplementary Online Material (SOM) Table S1. They cusp on the distal margin (frequent in papionin last molars, were taken from NYCEP's PRIMO (PRImate Morphometrics Online) although usually being situated more buccally; Delson, 1973), database (http://primo.nycep.org) or the literature (Alba et al., these features point to the tooth being an M3. 2011; Bona et al., 2016), or measured by one of the authors of this This molar is as broad as long (breadth/length index 100%) and paper (D.M.A.) at the American Museum of Natural History displays a suboval contour that markedly tapers distally, since the Department of Mammalogy (AMNH-M) in New York, USA. mesial lobe is much broader than the distal one. The crown is slightly longer buccally than lingually, due to the more mesial po- 4. Systematic paleontology sition of the paracone compared to the protocone. The crown is moderately waisted, with biconvex lingual and buccal occlusal Order Primates Linnaeus, 1758 profiles. The mesial and distal lobes are separated by a moderately- Infraorder Catarrhini E. Geoffroy Saint-Hilaire, 1812 developed median lingual cleft, which is located well above the Superfamily Cercopithecoidea Gray, 1821 cervix and displays no interconule, as well as a groove-like median Family Cercopithecidae Gray, 1821 buccal cleft that does not reach the crown base either. The mesial Subfamily Cercopithecinae Gray, 1821 lingual and buccal clefts are narrow and groove-like, whereas no Tribe Papionini Burnett, 1828 distinct distal clefts can be discerned. The shallow median buccal Subtribe Macacina Owen, 1843 and lingual notches do not surpass one-third of crown height. The Genus Macaca Lacep ede, 1799 occlusal surface displays the typical cercopithecid bilophodont Macaca sylvanus (Linnaeus, 1758) pattern, with four main cusps that are not particularly compressed Macaca sylvanus cf. prisca Gervais, 1859 buccolingually. The paracone is slightly larger and higher than the (Fig. 2) protocone, and the distal cusps are shorter, less extensive and more closely packed than the mesial ones. The degree of lingual flare is slightly more marked than the buccal. The mesial fovea is crescent- 4.1. Description shaped and extends to some extent above the mesial shelf. The distal fovea is intermediate in size between the mesial and the Upper canine This specimen (Fig. 2fej) preserves the root (buccal central ones. The hypocone has a twinned appearance, due to the height ¼ 20.6 mm) and the basal-most portion of the crown development of the posthypocrista into an accessory cuspule (preserved buccal crown height ¼ 11.9 mm), thus enabling (distoconule), which is separated from the hypocone by subtle reliable measurements of the relevant dimensions buccal and lingual grooves and is smaller than the four main cusps. (MD ¼ 11.2 mm, BL ¼ 8.6 mm; see also SOM Table S1). This tooth There are no discernible cingula. 144 D.M. Alba et al. / Journal of Human Evolution 123 (2018) 141e147

Figure 2. Dental remains of Macaca sylvanus cf. prisca from Puerto de la Cadena. aee) Left M3 (MAM VLP2-715), in occlusal (a), mesial (b), lingual (c), distal (d), and buccal (e) views. fej) Left C1 (MAM VLP3-62), in occlusal (f), mesial (g), lingual (h), distal (i) and buccal (j) views.

4.2. Morphometric comparisons between those of M. majori and those of extant M. sylvanus; Fig. 3a)dbut not so confidently in the case of Dolichopithecus. The dental size and proportions of the two macaque teeth from More taxonomically-informative comparisons can be made Puerto de la Cadena (SOM Table S1) are compared with those of regarding the M3 from Puerto de la Cadena due to the larger sample other fossil macaques in Figure 3. The male C1 (Fig. 3a), like those of available for fossil macaques (Fig. 3b). A referral to the larger Plio-Pleistocene European subspecies of M. sylvanus for which this papionin Paradolichopithecus, which is recorded in the late Pliocene tooth is known, overlaps in size with those of the extant Barbary of Iberia (Delson et al., 2014; Marigo et al., 2014), can be confidently macaque, from which only M. majori markedly differs by its smaller discounted based on its much larger occlusal dimensions (Fig. 3b). occlusal dimensions. Given the variability of the extant subspecies, In contrast, the dimensions of the M3 from Puerto de la Cadena and the very limited sample available for extinct M. sylvanus sub- (Fig. 4a) only minimally exceed those of M. sylvanus sylvanus species, no taxonomic conclusions can be drawn from this tooth, (Fig. 4feh), and fit well with those of some extinct subspecies other than concluding that its dimensions are compatible with an (Figs. 3b and 4bee; see also Alba et al., 2011), including a male assignment to this species. An attribution to a colobine can be specimen of M. s. prisca from Fornace RDB (Fig. 4c; see also Rook discounted on size grounds in the case of Mesopithecusdsince the et al., 2001:Fig. 3). Male and female specimens of the extant Bar- male canines of this genus are much smaller (intermediate in size bary macaque largely overlap, although males tend to display larger

Figure 3. Bivariate dental plots of mesial buccolingual (BL) breadth vs. mesiodistal (MD) length (in mm) for the two teeth of Macaca sylvanus cf. prisca from Puerto de la Cadena, compared to those of other fossil European and African macaques, Paradolichopithecus, Mesopithecus and Dolichopithecus, as well as extant Macaca sylvanus. a) Male upper canine (C1_). b) Upper ﬁrst molar (M1). The measurements for the comparative sample are reported in SOM Table S1. D.M. Alba et al. / Journal of Human Evolution 123 (2018) 141e147 145

Figure 4. Macaca sylvanus cf. prisca from Puerto de la Cadena (a) compared to extinct Macaca sylvanus prisca from Montpellier (b) and Fornace RDB (c), Macaca sylvanus florentina from Quibas (dee), and extant Macaca sylvanus sylvanus from North Africa (feh). All specimens are depicted in occlusal view. a) Left M3 (MAM VLP2-715). b) Left M3 (FSL 40136). c) Left M3 (NMB VJ 88). d) Left M3 (UM Q03-E-155b). e) Right (reversed) M3 (UM Q05-Ec-87). f) Right (reversed) M3 (AMNH-M 19014, female). g) Left M3 (AMNH-M 2060/5484, female). h) Left M3 (AMNH-M 185277, female). Specimens identified as UM were formerly housed at the Universidad de Murcia (Spain; Alba et al., 2011), but currently they are housed in the MAM collections. The specimens labeled as FSL and NMB are respectively housed in Lyon and Basel (for further details on institutional acronyms, see SOM Table S1). dimensions on average. The extinct taxa also overlap with the crown (more markedly biconvex buccal and lingual contours), an extant subspecies to a large degree, although M. majori mostly asymmetrical distal margin, and a less developed buccal flare of the overlaps with female specimens, whereas both M. libyca (Stromer, crown (Delson, 1973, 1975; Szalay and Delson, 1979), as well as 1920) from the late Miocene of north Africa and extinct subspe- smaller size. Several of these features further discount an attribu- cies of M. sylvanus mostly overlap with male specimens of the tion to the papionin Theropithecus, which is characterized by higher Barbary macaque, and show in all instances larger dimensions than cusps, more deeply excavated foveae, and better-developed M. majori. Unlike Macaca sylvanus pliocena Owen, 1846 and the notches, among other features (Delson, 1973, 1975; Szalay and single specimen of M. libyca, the M3 from Puerto de la Cadena re- Delson, 1979). Finally, an attribution to the dentally-generalized sembles some specimens of the early Pliocene M. s. prisca and the papionin Paradolichopithecus can be discounted on the basis of size. younger Macaca sylvanus florentina (Cocchi, 1872) in having larger An attribution of the material from Puerto de la Cadena to the dimensions than the extant subspecies. As such, the size of the genus Macaca, and in particular to M. sylvanus, is further supported described M3 is compatible with an attribution of the Puerto de la by the dental size and proportions of the described remains. In fact, Cadena macaque to either of these two extinct subspecies of the teeth are compatible with an assignment to M. s. prisca, which M. sylvanus. would seem logical on biochronologic (and paleobiogeographic) grounds. The teeth of specimens assigned to the various extinct 5. Discussion and conclusions subspecies of M. sylvanus overlap to a large extent with those of extant M. sylvanus (e.g., Alba et al., 2011). Thus, although M. s. prisca The male C1 from Puerto de la Cadena is fully comparable in was considered to be smaller than the Barbary macaque and other morphology with those of both extant and fossil M. sylvanus (e.g., extinct subspecies (Szalay and Delson, 1979; Delson, 1980; see Alba et al., 2011). Although it should be taken into account that Jablonski, 2002), in fact there is a considerable overlap (Rook this tooth is less informative from a taxonomic viewpoint than et al., 2001). Our comparisons indicate that the M3 from Puerto cheek teeth (Delson, 1973), an alternate assignment to the colobine de la Cadena is somewhat larger than those of the extant Barbary Mesopithecus can be discounted on size grounds. In turn, the upper macaque, as is also the case for some specimens of both M. s. prisca molar from Puerto de la Cadena is identified as an M3 and displays and M. s. florentina (see Alba et al., 2011). Given the lack of clear the typical papionin morphology that characterizes the dentally- dental metric criteria to distinguish between these two subspecies conservative genus Macaca (Fig. 4). This fact allows us to rule out of M. sylvanus, our attribution to the former largely relies on bio- an attribution to the colobine monkeys Mesopithecus or Dolichopi- chronological criteria and, as such, it must be considered tentative thecus, which would be characterized by a more marked occlusal (M. sylvanus cf. prisca), at least until more complete macaque re- relief, deeper median notches, a deeper lingual cleft, more bucco- mains from similarly-aged European localities enable a more lingually compressed cusps, a larger mesial fovea, a more waisted complete taxonomic assessment. 146 D.M. Alba et al. / Journal of Human Evolution 123 (2018) 141e147

Before going extinct during the Late Pleistocene, European Supplementary Online Material macaques attained a wide geographical distribution throughout the Plio-Pleistocenedeven if their sparse record suggests that, due to Supplementary online material related to this article can be suboptimal ecological conditions, they were not a common faunal found at https://doi.org/10.1016/j.jhevol.2018.07.005. element (Meloro and Elton, 2012; Elton and O'Reagan, 2014). Most of the macaque records from the Iberian Peninsula are based on fragmentary remains that have not been assigned to (sub)species References and/or described in detail (Marigo et al., 2014, and references therein; see also Elton and O'Reagan, 2014:Appendix A). There are, Aguirre, E., Alberdi, M.T., Thaler, L., Lopez, N., Ruiz Bustos, A., 1974. Coloquio Internacional sobre Biostratigrafía Continental del Neogeno superior y Cua- however, some exceptions, including Late Pleistocene remains ternario inferior, 1974.e Guía 6.10. MurciaeGranada. In: Aguirre Enríquez, E., assigned to M. s. pliocena (Castanos~ et al., 2011) and, especially, the Morales Romero, J. (Eds.), Coloquio Internacional sobre Biostratigrafía Conti- fl nental del Neogeno Superior y Cuaternario Inferior. MontpelliereMadrid, more abundant Early Pleistocene material of M. s. (cf.) orentina e e e 25.9 11.10, 1974. Libro-Guía. Adosa, Madrid, pp. 155 171. from sites such as Incarcal (ca. 1.5 1.2 Ma; Alba et al., 2016), Quibas Agustí, J., Cabrera, L., Garces, M., Krijgsman, W., Oms, O., Pares, J.M., 2001. (ca. 1.3e1.0 Ma; Alba et al., 2011), and Vallparadís and Cal Guardiola A calibrated mammal scale for the Neogene of Western Europe. State of the art. (ca. 1.2e0.8 Ma; Alba et al., 2008). Earth-Science Reviews 52, 247e260. Agustí, J., Garces, M., Krijgsman, W., 2006. Evidence for AfricaneIberian exchanges The published Pliocene record of Iberian macaques is, in during the Messinian in the Spanish mammalian record. Palaeogeography, contrast, very scarce, being restricted to the late Pliocene sites of Palaeoclimatology, Palaeoecology 238, 5e14. Orrios 7 (MN15; Mein et al., 1990) and Cova Bonica (MN16, 3.2e2.6 Alba, D.M., Moya-Sola, S., Madurell, J., Aurell, J., 2008. Dentognathic remains of Macaca (Primates, Cercopithecidae) from the late early Pleistocene of Terrassa Ma; Delson, 1971; Crusafont-Pairo and Golpe-Posse, 1984), attrib- (Catalonia, Spain). Journal of Human Evolution 55, 1160e1163. uted to Macaca sp. by Marigo et al. (2014) and M. s. prisca by Alba, D.M., Carlos Calero, J.A., Mancheno,~ M.A., Montoya, P., Morales, J., Rook, L., Crusafont-Pairo and Golpe-Posse (1984). Guillen Castejon (2010) 2011. Fossil remains of Macaca sylvanus florentina (Cocchi, 1872) (Primates, Cercopithecidae) from the Early Pleistocene of Quibas (Murcia, Spain). Journal further reported the presence of both M. cf. sylvanus prisca and of Human Evolution 61, 703e718. M. s. florentina from the karstic infills of Canal Negre 1. However, Alba, D.M., Delson, E., Carnevale, G., Colombero, S., Delfino, M., Giuntelli, P., given dating uncertainties (Miocene-Pleistocene), and pending a Pavia, M., Pavia, G., 2014. First joint record of Mesopithecus and cf. Macaca in the e more detailed study, Marigo et al. (2014) left these remains unas- Miocene of Europe. Journal of Human Evolution 67, 1 18. Alba, D.M., Montoya, P., Pina, M., Rook, L., Abella, J., Morales, J., Delson, E., 2015. First signed to subspecies rank. Additional remains of M. s. prisca might record of Mesopithecus (Cercopithecidae, Colobinae) from the Miocene of the be available from an unpublished collection of papionin fossils from Iberian Peninsula. Journal of Human Evolution 88, 1e14. Cova Bonica, where macaques coexisted with a small-sized Para- Alba, D.M., Madurell-Malapeira, J., Delson, E., Vinuesa, V., Susanna, I., Espigares, M.P., Ros-Montoya, S., Martínez-Navarro, B., 2016. First record of dolichopithecus species (Delson, 1971; Moya Sola et al., 1990; Delson macaques from the early Pleistocene of Incarcal (NE Iberian Peninsula). Journal et al., 2014; Marigo et al., 2014). The ongoing study of these re- of Human Evolution 96, 139e144. mains, together with those from the slightly older site of Moreda 1a Azzaroli, A., 1946. La scimmia fossile della Sardegna. Rivista di Scienze Preistoriche e e 1, 68 76. (late MN15, 3.5 3.2 Ma), should clarify whether Para- Burnett, G.T., 1828. Illustrations of the Manupeda or apes and their allies: being the dolichopithecus sp. further coexisted with Macaca in the latter lo- arrangements of the Quadrumana or Anthropomorphous beasts indicated in cality (Marigo et al., 2014). In any case, with a much older (early the outline. Quarterly Journal of Science, Literature, and Art 26, 300e307. e Bona, F., Bellucci, L., Casali, D., Schirolli, P., Sardella, R., 2016. Macaca sylvanus Lin- MN14) age of ca. 5.0 4.9 Ma, the two macaque teeth from Puerto naeus 1758 from the Middle Pleistocene of Quecchia quarry (Brescia, Northern de la Cadena, attributed here to M. s. cf. prisca, clearly attest the Italy). Hystrix 27. https://doi.org/10.4404/hystrix-27.2-11503. presence of macaques in the earliest Pliocene of the Iberian Castanos,~ P., Murelaga, X., Arrizabalaga, A., Iriarte, M.-J., 2011. First evidence of Macaca sylvanus (Primates, Cercopithecidae) from the Late Pleistocene of Peninsula, thereby predating by almost 1.5 million years the record Lezetxiki II cave (Basque Country, Spain). Journal of Human Evolution 60, of the larger terrestrial papionin Paradolichopithecus. 816e820. Cocchi, I., 1872. Su di due Scimmie fossili italiane. Bolletino del Regio Comitato Geologico d'Italia 3, 59e71. Colombero, S., Alba, D.M., D'Amico, C., Delfino, M., Esu, D., Giuntelli, P., Acknowledgments Harzhauser, M., Mazza, P., Mosca, M., Neubauer, T.A., Pavia, G., Pavia, M., Villa, A., Carnevale, G., 2017. Late Messinian mollusks and vertebrates from Moncucco This work has been funded by the Generalitat de Catalunya Torinese, north-western Italy. Paleoecological and paleoclimatological implications. Palaeontologia Electronica 20, 10A. (CERCA Program), and the Agencia Estatal de Investigacion Crusafont-Pairo, M., Golpe-Posse, J.M., 1984. Nuevo hallazgo de macaco en Cova (Ministerio de Economía, Industria y Competitividad)eEuropean Bonica (Gava). Acta Geologica Hispanica 19, 29e32. Regional Development Fund of the European Union (CGL2015- de Bruijn, H., Mein, P., Montenat, C., van de Weerd, A., 1975. Correlations entre les gisements de rongeurs et les formations marines du Miocene terminal 68333-P, MINECO/FEDER-UE; and CGL2016-76431-P and CGL2017- d'Espagne meridionale (provinces d'Alicante et de Murcia). Proceedings of the 82654-P, AEI/FEDER-UE). Fieldwork at Puerto de la Cadena was Koninklijke Nederlandse Akademie van Wetenschappen 78(4), 1e31. e Delson, E., 1971. Estudio preliminar de unos restos de simios pliocenicos proce- carried out with funding from the Fundacion Seneca Agencia de dentes de “Cova Bonica” (Gava) (Prov. Barcelona). Acta Geologica Hispanica 6, Ciencia y Tecnología de la Region de Murcia (11891/PHCS/09), and it 54e57. was possible thanks to the collaboration of the Demarcacion de Delson, E., 1973. Fossil colobine monkeys of the circum-Mediterranean region and Carreteras del Estado in Murcia (Ministerio de Fomento) and the the evolutionary history of the Cercopithecidae (Primates, Mammalia). Ph.D. Dissertation, Columbia University. Direccion General de Bienes Culturales of the Comunidad Delson, E., 1974. Preliminary review of cercopithecid distribution in the circum Autonoma de la Region de Murcia, and the Asociacion Cultural Mediterranean region. Memoires du Bureau de Recherches Geologiques et Paleontologica Murciana. D.M.A. further thanks the Museo Minieres (France) 78, 131e135. Delson, E., 1975. Evolutionary history of the Cercopithecidae. Contributions to Pri- Arqueologico de Murcia (Murcia, Spain) for permission to study the e matology 5, 167 217. material, the Museo Paleontologico de Elche (Elche, Spain) for the Delson, E., 1980. Fossil macaques, phyletic relationships and a scenario of deploy- facilities given, Eileen Westwig (Mammalogy Department, Amer- ment. In: Lindburg, D.E. (Ed.), The Macaques. Studies in Ecology, Behavior and e ican Museum of Natural History) for access to extant primate Evolution. Van Nostrand, New York, pp. 10 30. Delson, E., Terranova, C.J., Jungers, W.L., Sargis, E.J., Jablonski, N.G., Dechow, P.C., comparative material, and Raef Minwer-Barakat for discussion on 2000. Body mass in Cercopithecidae (Primates, Mammalia): estimation and Messinian biochronology. Finally, we thank Mike Plavcan (Editor), scaling in extinct and extant taxa. Anthropological Papers of the American Sarah Elton, Chris Gilbert, and an additional anonymous reviewer Museum of Natural History 83, 1e159. Delson, E., Thomas, H., Spassov, N., 2005. Fossil Old World monkeys (Primates, for helpful comments and suggestions that improved a previous Cercopithecoidae) from the Pliocene of Dorkovo, Bulgaria. Geodiversitas 27, version of this paper. 159e166. D.M. Alba et al. / Journal of Human Evolution 123 (2018) 141e147 147

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