Quaternary International 389 (2015) 119e130

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How rare was human presence in Europe during the Early ?

* Jesús Rodríguez a, , Ana Mateos a, Jesús Angel Martín-Gonzalez b, 1, Guillermo Rodríguez-Gomez a a CENIEH, Paseo Sierra de Atapuerca, 3, 09002 Burgos, b Dpt. Matematicas y Computacion, Universidad de Burgos, Burgos, Spain article info abstract

Article history: Beneath the hot debate about the tempo and mode of the first human colonization of Europe is the Available online 30 December 2014 perception that the record of human presence in the Early Pleistocene is sparse and fragmented. As a result, it is often implicitly assumed that hominins, if present, were scarce in the Early Pleistocene Eu- Keywords: ropean ecosystems. Here we present a quantitative assessment of the rarity and commonness of the Rarity European large mammal species during the 1.4e0.8 Ma period, including hominins. Considering the Hominin palaeontological record only, Homo was not one of the most common species in Europe, but it may not be Early settlement considered a rare species. In contrast, taking into consideration the archaeological record, hominins Geographical range Occupancy exhibit a wide geographical distribution and a high frequency of occurrence (occupancy) in comparison with other large mammals. It is speculated that hominins were frequent but not abundant in Europe during the late Early Pleistocene. © 2015 Elsevier Ltd and INQUA. All rights reserved.

1. Introduction Mosquera et al., 2013; Martínez et al., 2014). Some theoretical evolutionary scenarios have been proposed including argumen- Timing and nature of the early human colonisation of Europe tations in pro of a continuous settlement (Bermúdez de Castro and has been a hotly debated topic for a long time. Nowadays, there is Martinon-Torres, 2013; Garcia et al., 2013; Martínez et al., 2013) a general consensus in assuming that humans dispersed to and/or supporting a discontinuous and intermittent occupation by Western Europe during the late Early Pleistocene (Carbonell et al., populations constrained by climatic and ecological fluctuations 2010; Made and Mateos, 2010; Moncel, 2010; Palombo, 2010, (Dennell, 2003; Agustí et al., 2009; Dennell et al., 2011; Leroy et al., 2013; Allue et al., 2013). It is generally accepted that humans 2011; MacDonald et al., 2012). These debates reflected the usual occupied Europe as early as 1.4 Ma as evidenced by the fossils and problems derived from the low completeness of the hominin fossil lithic industry recovered at Barranco Leon D (Spain) and Pirro record, which represents a fragmented, poorly-dated set of evi- Nord () (Arzarello et al., 2007; but see Muttoni et al., 2013, dences. Several issues related to the ecological and environmental 2011; but see Rolland, 2013; Toro-Moyano et al., 2013). Beyond context of this dispersal event, or the technological skills of these the debate about the phylogenetic relationships between those populations are still under discussion (Turner, 1992; Arribas and hominin European populations (Stringer, 2012; Gomez-Robles, Palmqvist, 1999; Mosquera et al., 2013). Moreover, recent discov- 2013; Lordkipanidze et al., 2013; Arsuaga et al., 2014), a new eries and critical evaluations of the chronological framework and debate aroused in the last years concerning the continuity or dispersal events related to the first human colonization of Europe discontinuity of this initial settlement (Dennell, 2003; Leroy et al., (Muttoni et al., 2011, 2013; Pares et al., 2013; Rolland, 2013) show 2011; Muttoni et al., 2011; Bermúdez de Castro et al., 2013; that key questions about the tempo and mode of this colonization remain unsolved. Several models have been proposed supporting the idea that * Corresponding author. the first human colonisers were restricted to the Mediterranean E-mail addresses: [email protected] (J. Rodríguez), ana.mateos@cenieh. area because they were unable to survive in mid-latitude Europe es (A. Mateos), [email protected] (J.A. Martín-Gonzalez), guillermo. (Roebroeks and Kolfschoten, 1992; Dennell and Roebroeks, 1996; [email protected] (G. Rodríguez-Gomez). 1 Temporarily assigned to CENIEH. Roebroeks, 2001; Dennell et al., 2010). Although many of the http://dx.doi.org/10.1016/j.quaint.2014.12.016 1040-6182/© 2015 Elsevier Ltd and INQUA. All rights reserved. 120 J. Rodríguez et al. / Quaternary International 389 (2015) 119e130 evolutionary scenarios proposed take into account only the highly constrained opportunities of the settlement for early palaeoanthropological and/or archaeological evidence (Carbonell hominins. et al., 1999; Dennell et al., 2010, 2011; MacDonald et al., 2012; All things considered, human occupation during the Early Barsky et al., 2013; Bermúdez de Castro and Martinon-Torres, Pleistocene is currently represented in Europe by a short list of sites. 2013; Mosquera et al., 2013), it becomes increasingly evident Many authors assume that the fragmentary archaeological and that some complex relationships existed between palaeoclimatic fossil records indicate only sporadic hominin presence or marginal and palaeoecological changes and human dispersals and settling settlement (MacDonald et al., 2012; Barsky et al., 2013; Bermúdez (Turner, 1992; Martínez Navarro and Palmqvist, 1996; Arribas and de Castro et al., 2013). Even a cursory review of the available evi- Jorda, 1999; Arribas and Palmqvist, 1999; O'Regan, 2008; Made dence suggests a “virtual” scarcity of human presence in the Early and Mateos, 2010; Palombo, 2010; Made et al., 2011; O'Regan Pleistocene. According to this argumentation, hominin occupation et al., 2011). Very recently new approaches and hypothesis con- of Europe was occasional, infrequent and intermittent during the cerning the palaeoecological scenario of the human settlement Calabrian (1.4e0.8 Ma). joined the general discussion. Factors like faunal turnover, carni- In summary, beneath the debate summarized above is the im- vore guild structure, dynamics of the Pleistocene food webs and plicit idea that the evidence supporting the human population of resource availability (Arribas and Palmqvist, 1999; Croitor and Europe during the Early Pleistocene is scarce. Moreover, many Brugal, 2010; Palombo, 2010, 2014; Rodríguez et al., 2012, 2013; scholars implicitly assume that, although present, humans were Rodríguez-Gomez et al., 2013; Rodríguez-Gomez et al., 2014) not a common nor abundant component of the European

Fig. 1. Geographical distribution of sites with evidence of hominin presence (top) and local faunas from the time interval 1.4e0.8 Ma (bottom). Detailed information on the sites is provided in Tables 1 and 2. Black dots: reliable Early Pleistocene lithic assemblages or sites with hominin fossils, white dots “dubious” Early Pleistocene lithic assemblages; white squares: sites providing local faunas (see text). J. Rodríguez et al. / Quaternary International 389 (2015) 119e130 121 ecosystems. However, scarcity is a relative concept and, thus, the 2013), only LFs confidently dated to the interval 1.4 Mae0.8 Ma key question is whether Homo sp. was a common species, or not, in (Calabrian, Early Pleistocene) were included in the database. LFs comparison with the other large mammals inhabiting Europe at the were selected according to bio-stratigraphic correlations and nu- end of the Early Pleistocene. merical ages provided by the original sources, although numerical Commonness or rarity of an extinct species, Homo in particular, ages were given priority over bio-stratigraphic correlations. should be evaluated in the context of the palaeontological record. It is A total of 51 LFs from 34 sites met the criteria to be included in universally assumed that the lack of completeness and the spatial and the database (Fig. 1 and Table 1). The inclusion of Huescar 1 in this temporal heterogeneity of the fossil record may make a species tableshouldbebriefly commented on. Luminescence chronology appear to be rarer than it really was. This effect is especially important suggest a Middle Pleistocene age, around 400e500 Kyr, for the when different periods or geographical areas are compared. Here we sediments of the fossil bearing layers (Demuro et al., 2014), present a quantitative measure of the rarity of Homo in the European however it is included here because the fauna strongly suggests a Early Pleistocene communities relative to other species. Moreover, late Early Pleistocene age. It has been repeatedly pointed out that since rarity of a species at continental scale is influenced by the size of taxonomic inconsistency is a potential drawback in this kind of its distribution range, we also compare the size of the area of distri- compiled lists (Palombo, 2010; Rodríguez et al., 2013). To address bution of Homo in Europe during the late Early Pleistocene with the this problem, we reviewed all faunal lists and applied uniform area of the other large mammal species of this period. taxonomic criteria to obtain a taxonomically consistent database. We based our review on systematic revisions of groups by other 2. Material and methods authors (see Rodríguez et al., 2012 and references therein). In case of doubt about the validity of a species we adopted a conservative, A database including georeferenced late Early Pleistocene Local non-splitting criterion, as explained in Rodríguez et al. (2013).As Faunas (LFs) and sites with evidence of human presence was an effect of this decision our results may overestimate the oc- compiled from published sources. Since our focus is on large mam- currences of some species. Several LFs included taxa identified mals, only species in the orders Artiodactyla, Perissodactyla, only at the genus level. We treated these cases as follows. If more Carnivora, Primates and Proboscidea were included. Mustelids were than one species of the genus is recognized in this time period not included in the analyses because of their small size. The records at genus level were not included in the analyses. Other- geographical extent of this database was restricted to longitude be- wise, if a single species of the genus is recognized for this period, tween 10 Wand35 E and latitude between 36 Nand55 N(Fig. 1). records identified at the genus level are assimilated to the species. This extent excludes the high latitude areas of Europe, which are As an example, all records reported as Macaca sp. are included in known to have been colonized only during the Late Pleistocene the analyses as Macaca sp./Macaca sylvanus. Finally, some taxa (Pavlov et al., 2001). Although a small part of Anatolia is included were only recorded at the genus level in the sites included in the inside the extent of our database, data from this Asian peninsula database, e.g. Capra sp. These cases were treated as additional were not collected. Since the oldest evidence of human presence in species. Again, these criteria tend to overestimate the occurrences Europe dates to 1.4 Ma (Arzarello et al., 2007; Toro-Moyano et al., of those taxa affected.

Table 1 Late Early Pleistocene (1.4e0.8 Ma) local faunas included in the analyses.

Locality Longitude Latitude Age Reference

1 Sima del Elefante TE 09 3.52 42.35 1.4e1.2 Ma (Rodríguez et al., 2011) 2 Barranco Leon D 2.43 37.71 1.4e1Ma (Toro-Moyano et al., 2013) 3 Cueva Victoria 1.18 37.85 1.4e0.9 Ma (Gibert, 1993; Gibert et al., 1999) 4 Pirro Nord 13.65 43.28 1.4e1.2 Ma (Palombo et al., 2000e2002; Arzarello et al., 2007) 5 Sandalja-I 13.89 44.90 1.4e1.2 Ma (Kahlke et al., 2011) 6 Ceyssaguet 1 3.90 45.12 1.3e1.2 Ma Paleobiology Database Searched 16-04-2010 7 Saint-Prest 1.50 48.36 1.3e0.8 Ma (Guerin et al., 2003) 8 Sierra de Quibas 0.93 38.20 1.3e1.07 Ma (Montoya et al., 1999; Montoya et al., 2001) 9 Sima del Elefante TE 10 3.52 42.35 1.2e1Ma (Rodríguez et al., 2011) 10 Sima del Elefante TE 11 3.52 42.35 1.2e1Ma (Rodríguez et al., 2011) 11 Sima del Elefante TE 12 3.52 42.35 1.2e1Ma (Rodríguez et al., 2011) 12 Sima del Elefante TE 13 3.52 42.35 1.2e1Ma (Rodríguez et al., 2011) 13 Sima del Elefante TE 14 3.52 42.35 1.2e1Ma (Rodríguez et al., 2011) 14 Apollonia-1 23.44 40.62 1.2e0.8 Ma (Kostopoulus, 1997) 15 Betfia level 3b 22.03 46.97 1.2e0.8 Ma Paleobiology Database Searched 16-04-2010 16 Durfort 3.95 43.98 1.2e1Ma (Palombo and Valli, 2003e2004) 17 Huescar-1 2.50 37.77 1.2e0.8 Ma (Diago et al., 2003) 18 Imola 11.71 44.35 1.2e0.99 Ma (Palombo et al., 2000e2002) 19 11c 22.68 43.63 1.2e0.8 Ma (Guadelli et al., 2005) 20 Kozarnika 11d 22.68 43.63 1.2e0.8 Ma (Guadelli et al., 2005) 21 Kozarnika 12 22.68 43.63 1.2e0.9 Ma (Guadelli et al., 2005) 22 Kozarnika 13 22.68 43.63 1.2e0.78 Ma (Guadelli et al., 2005) 23 Kunino Lower Level 23.96 43.18 1.2e0.99 Ma (Palombo and Mussi, 2006) 24 Marathousa-Megalopolis 22.04 37.51 1.2e0.99 Ma (Palombo and Mussi, 2006) 25 Ravin Voulgarakis 23.50 40.60 1.2e0.99 Ma (Palombo and Mussi, 2006) 26 Rosieres “Usine” 2.25 46.95 1.2e0.99 Ma (Despriee et al., 2007) 27 Torre di Picchio 12.49 42.65 1.2e1Ma (Raia et al., 2009) 28 Redicicoli 12.52 41.93 1.2e0.8 Ma (Raia et al., 2009) 29 Dealul Viilor 24.66 45.15 1.1e0.9 Ma (Palombo and Mussi, 2006) 30 Sainzelles 3.80 45.08 1.1e0.99 Ma (Palombo and Valli, 2003e2004) 31 Colle Curti 12.75 42.95 1.07e0.78 Ma (Palombo et al., 2000e2002) 32 Grotte du Vallonnet BI 7.47 43.77 1.07e1Ma (Lumley et al., 1988b) (continued on next page) 122 J. Rodríguez et al. / Quaternary International 389 (2015) 119e130

Table 1 (continued )

Locality Longitude Latitude Age Reference

33 Grotte du Vallonnet BII 7.47 43.77 1.07e1Ma (Lumley et al., 1988b) 34 Grotte du Vallonnet C 7.47 43.77 1.07e1Ma (Lumley et al., 1988b) 35 Grotte du Vallonnet III 7.47 43.77 1.07e1Ma (Lumley et al., 1988b) 36 Karlich€ Level A 7.47 50.47 1.07e0.9 Ma Paleobiology Database Searched 16-04-2010 37 Soleilhac 4.02 45.02 1.07e0.9 Ma (Alberdi et al., 1997; Palombo and Valli, 2003e2004) 38 Untermassfeld 10.42 50.55 ~1.07 Ma (Koenigswald and Heinrich, 1999) 39 Gran Dolina TD5 3.52 42.35 1e0.8 Ma (Rodríguez et al., 2011) 40 Betfia level 3c 22.03 46.97 1e0.8 Ma Paleobiology Database Searched 16-04-2010 41 Chlum 6 16.76 49.41 1e0.9 Ma (Koenigswald and Heinrich, 1999) 42 Incarcal 1 2.78 42.19 1.4e0.9 Ma (Julia, 1984; Galobart, 2007; Ros-Montoya et al., 2012) 43 Het Gat 3.22 52.40 1e1.2 Ma (Mol et al., 2003) 44 Gran Dolina TD3eTD4 3.52 42.35 0.99e1Ma (Rodríguez et al., 2011) 45 Estrecho de Quipar 1.88 38.04 0.99e0.9 Ma (Scott and Gibert, 2009) 46 Karlich€ Level B 7.47 50.47 0~0.99 Ma Paleobiology Database Searched 16-04-2011 47 Vallparadís 10-10c 2.02 41.56 0.98e0.78 Ma (Martínez et al., 2010; Madurell-Malapeira et al., 2011) 48 Gran Dolina TD6 1-2 3.52 42.35 ~0.9 Ma (Rodríguez et al., 2011) 49 Gran Dolina TD6-3 3.52 42.35 ~0.9 Ma (Rodríguez et al., 2011) 50 Happisburgh Site 3 D-E 1.53 52.82 ~0.8 Ma (Parfitt et al., 2010) 51 Fuente Nueva 3 2.4 37.71 1.19 ± 0.21 (Martínez-Navarro et al., 2010)

Evidence of human presence in Europe during the Early Pleis- is taken as a proxy for the commonness of a species during the Early tocene both in the form of fossils and lithic artifacts was compiled Pleistocene inside the sampled area. The prevalence (P) of a species from published sources. Several of those sites allegedly evidencing is computed as the number of LFs that contain this species. an old human presence in Europe are controversial, thus some of We also compared the amplitude of the geographical distribu- them were flagged as “dubious” on the basis of the criticisms raised tions of Homo and other Early Pleistocene large mammals. Longi- by other authors (Table 2). tudinal amplitude (LgA) was computed as the maximum difference

Table 2 Palaeontological and lithic assemblages providing evidence of the presence of hominins in Europe earlier than 0.8 Ma. Code for dating methods as follows: BS: biostratigraphic correlation, ESR: electron spin resonance, ESR-OB: electron spin resonance of optically bleached grains, CN: cosmogenic nuclides, PM: paleomagnetism, TL: Thermoluminescence.

Site Long. Lat. Technology Hominin Estimated Dating Reference fossils age (Ma) methods

Reliable evidence Kozarnika () 22.68 43.63 Mode 1 1.4e1.6 BS (Sirakov et al., 2010) Pirro Nord P13 (Italy) 13.65 43.28 Mode 1 1.3e1.7 BS (Arzarello et al., 2007) Barranco Leon D (Spain) 2.43 37.71 Mode 1 Homo sp. 1.43 ± 0.38 BS, PM, ESR (Toro-Moyano et al., 2009; Toro-Moyano et al., 2013) Atapuerca Sima del Elefante TE9 (Spain) 3.52 42.35 Mode 1 Homo sp. 1.4e1.2 CN (Pares et al., 2006; Carbonell et al., 2008) Atapuerca Sima del Elefante TE11 (Spain) 3.52 42.35 Mode 1 1.2e0.78 CN, PM (Rodríguez et al., 2011; Olle et al., 2013) Atapuerca Sima del Elefante TE12 (Spain) 3.52 42.35 Mode 1 1.2e0.78 CN, PM (Rodríguez et al., 2011; Olle et al., 2013) Atapuerca Sima del Elefante TE13 (Spain) 3.52 42.35 Mode 1 1.2e0.78 CN, PM (Rodríguez et al., 2011; Olle et al., 2013) Atapuerca Sima del Elefante TE14 (Spain) 3.52 42.35 Mode 1 1.2e0.78 CN, PM (Rodríguez et al., 2011; Olle et al., 2013) Fuente Nueva 3 (Spain) 2.4 37.71 Mode 1 1.19 ± 0.21 PM, BS, ESR (Oms et al., 2000; Toro-Moyano et al., 2009; Duval et al., 2012) Vallparadís EVT8-7 (Spain) 2.02 41.56 Mode 1 0.98e0.95 PM, BS, ESR (Martínez et al., 2010; Duval and Moreno, 2011; Madurell-Malapeira et al., 2012; Martínez et al., 2014) Atapuerca Gran Dolina TD6 (Spain) 3.52 42.35 Mode 1 H. antecessor 0.9 PM, BS, ESR (Rodríguez et al., 2011; Pares et al., 2013) Atapuerca Gran Dolina TD3eTD4 (Spain) 3.52 42.35 Mode 1 0.94 ± 0.1 ESR-OB, (Moreno, 2011; Rodríguez et al., 2011) BS, TL Pont de Lavaud () 1.88 46.25 Mode 1 1.07 ± 0.09 ESR (Bahain et al., 2007) Terre des Sablons 2.26 46.95 Mode 1 1.1 ± 0.18 ESR (Despriee et al., 2010) (Lune Rosiers Unit 3, France) to 930 Le Vallonet (France) 7.46 43.77 Mode 1 >0.9 z 1.0 ESR, PM, BS (Yokoyama et al., 1988; Lumley et al., 1988a; Gagnepain, 1996) Pont de la Hulauderie (France) 1.2 47.92 Mode 1 0.98 ESR (Despriee et al., 2010) Happisburgh (UK) 1.53 52.82 Mode 1 Footprints 0.98e0.78 PM, BS (Parfitt et al., 2010; Ashton et al., 2014) Korolevo VII (Ukraine) 23.13 48.15 Mode 1 0.95 PM (Koulakovska et al., 2010) Monte Poggiolo (Italy) 12.04 44.22 Mode 1 1.06 ± 0.16 ESR (Bahain et al., 2007) “Dubious” evidence Lezignan Le-Cebe (France) 3.43 43.48 Mode 1 1.57 39Ar/40Ar, BS (Crochet et al., 2009) Anagni (Italy) 13 41.77 Mode 1 >0.706 KeAr (Biddittu et al., 1979) Colle Marino-Arce-Fontana Liri (Italy) 13.54 41.62 Mode 1 >0.706 e (Biddittu et al., 1979) Untermassfeld () 10.42 50.55 Mode 1 1.05 BS, PM (Landeck, 2010; Garcia et al., 2013) Dorn-Dürkheim 3 (Germany) 8.26 49.76 Mode 1 >0.78 PM (Haidle and Pawlik, 2010) Karlich€ A (Germany) 7.49 50.39 Mode 1 1.07e0.99 PM (Bosinski et al., 1980; Würges, 1986) Estrecho del Quípar (Spain) 1.88 38.04 Mode 2 c. 0.9 PM (Scott and Gibert, 2009)

Frequency of occurrence in the palaeontological record, or in longitude between two sites where the species is present. prevalence, a measure of occupancy (Gaston and Fangliang, 2010), Similarly, latitudinal amplitude (LtA) is defined as the maximum J. Rodríguez et al. / Quaternary International 389 (2015) 119e130 123 difference in latitude between two sites where the species is pre- contain human fossils are located in the Iberian Peninsula we car- sent. Both variables LgA and LtA are expressed in degrees. Range ried out our analyses at two different extents: the Iberian Peninsula size (Rg) is used as a proxy for the geographical range size of the and the entire sampled area. Although it excludes high latitudes species. It is computed as the maximum distance in km between and the land to the east of 35 E longitude, from here on out we will two sites where the species is present. The distance between each refer to the later area as Europe. pair of sites was computed based on their latitude and longitude. Empirical Cumulative Density Functions (CDF) of P have been The geodesic distance, i.e. the length of the shorter arc of the great computed and used to calculate in which quartile of the distribu- circle passing through both sites, was computed assuming the tion the prevalence of Homo is included. In ecology, species with an Earth is a sphere, instead of using a spheroid to account for the abundance or distribution range below the median are considered flattering of the Earth. to be rare (Yu and Dobson, 2000). Here the quartile is taken as an Carnivore and primary consumers are known to have different index of the rarity or commonness of Homo and other species in the allometric constraints in several parameters related to their dis- Early Pleistocene. Species in the first quartile are considered rare, tribution, like population density (Damuth, 1981) or home range those in the second quartile are considered moderately rare, the size (Martin, 1991). Thus, carnivore and primary consumer species third quartile includes the moderately common species and the were analyzed separately. Moreover, since the three LFs which fourth quartile the common species. A KolmogoroveSmirnov test

Fig. 2. Prevalence of carnivores (top) and other large mammal species (bottom) in Europe during the late Early Pleistocene. Hominin prevalence estimated from the number of sites with fossils attributed to the genus Homo and from the number of lithic assemblages is compared with both distributions. The white part in the bar of lithic assemblages represents dubious assemblages (see text). 124 J. Rodríguez et al. / Quaternary International 389 (2015) 119e130 was used to test for differences in the distribution of geographical chronologies, geological and stratigraphic contexts or collections of range size between carnivores and other large mammals. Statistical uncertain archaeological nature. The precise stratigraphic prove- analyses were carried out using Matlab R2009b. nance of the lithic artifacts from Lezignan Le-Cebe (France) (Crochet et al., 2009) is problematic (Muttoni et al., 2011; Pares 3. Results et al., 2013; Rolland, 2013). The artifacts of the Italian localities of Anagni and those of the Latium area (Colle Marino, Arce, Fontana 3.1. Evidence of human presence in the late Early Pleistocene Liri) (Biddittu et al., 1979) have an imprecise archaeological context and have been dated by regional geological correlations (Rolland, Fossils attributed to the genus Homo have been found only in 2013). The German sites of Untermassfeld (Landeck, 2010; Garcia three Early Pleistocene sites: Sima del Elefante TE9, Gran Dolina et al., 2013), Dorn-Dürkheim 3 and Karlich€ A (Haidle and Pawlik, TD6 and Barranco Leon D, all of them located in the Iberian 2010) are also problematic. The lithic artifacts from Untermass- Peninsula. Though, this restricted distribution of human fossils feld were not found in association with the well-known fauna from contrasts with the wide distribution of the lithic record from the this palaeontological site (Landeck, 2010). Likewise, the strati- same period (Table 2). A total of 26 European lithic assemblages graphic context of the layer Karlich€ A is also doubtful (Roebroeks have been attributed an age older than 0.8 Ma, although 7 of them and van Kolfschoten, 1995; Baales et al., 2000). The nature of the are considered dubious. These later localities contain lithic and artifacts recovered at Dorn-Dürkheim 3 and Karlich€ A is contro- faunal assemblages in an ambiguous status, either imprecise versial (Baales et al., 2000; Haidle and Pawlik, 2010 and references

Fig. 3. Prevalence of carnivores (top) and other large mammal species (bottom) in the Iberian Peninsula during the late Early Pleistocene. Hominin prevalence estimated from the number of sites with fossils attributed to the genus Homo and from the number of lithic assemblages is compared with both distributions. The white part in the bar of lithic assemblages represents dubious assemblages (see text). J. Rodríguez et al. / Quaternary International 389 (2015) 119e130 125 therein; Roebroeks and van Kolfschoten, 1995). In Spain, the mag- primary consumers and carnivores both in Europe and in the Ibe- netostratigraphy and the correlations based on the fauna of Cueva rian Peninsula (Fig. 4c and f). Negra del Estrecho del Quípar (Scott and Gibert, 2009) remain questionable (Jimenez-Arenas et al., 2011; Muttoni et al., 2011). 3.3. Range size

3.2. Prevalence of Homo in the context of the palaeontological The distribution of the range sizes of the late Early Pleistocene record large mammal species is severely skewed to the left (Fig. 5). This is a direct consequence of the distribution of P, since the range of the A total of 83 mammal species, 29 of them carnivores, were species occurring in a single site is 0. At first glance, carnivores included in the database. Prevalence at continental scale ranges seem to exhibit a bimodal distribution of Rg with a tendency to- from 1 to 18 occurrences for the order Carnivora and from 1 to 19 wards larger range size in the species recorded in more than one occurrences for other mammalian orders (Fig. 2). In contrast, P site. In contrast, the distribution of range sizes seems to be more ranges from 1 to 10 for carnivores and from 1 to 12 for other homogeneous in primary consumers (Fig. 5). However, this mammals when only the LFs from the Iberian Peninsula are apparent differences in range size between carnivores and primary considered (Fig. 3). The distribution of P is severely skewed to the consumers are not statistically significant (KeS test ¼ 0.3048, left, as shown in Fig. 4, irrespectively of the taxonomic group or the p ¼ 0.06). geographical extent. Fig. 6 shows the longitudinal and latitudinal amplitudes of the Taking into account only the palaeontological record, Homo late Early Pleistocene large mammals in Europe. Again, a tendency shows a low prevalence (3 sites). Though considering the empiric towards wider geographical ranges is evident for carnivores. distribution of P (Fig. 4c), the prevalence of Homo is included in the Because all hominin fossils from this period have been found in the third quartile of the prevalence of primary consumers in Europe Iberian Peninsula, the latitudinal and longitudinal amplitude of and in the second quartile of the prevalence of carnivores. Homo is very small when computed in this way. However, the Considering only the Iberian Peninsula the prevalence of Homo is amplitude of the distribution of lithic assemblages is one of the also in the third quartile of the prevalence of primary consumers largest for any large mammal in the sample (Fig. 6). The latitudinal and in the second quartile of carnivores (Fig. 4f). and longitudinal amplitude of the lithic record has been obtained In contrast, if the lithic record is taken into consideration, considering reliable assemblages only. humans become one of the most common species in Europe with 15 reliable and 7 dubious occurrences (Fig. 2). In the Iberian 4. Discussion Peninsula the lithic record also places humans among the most common species with 6 reliable and one dubious record (Fig. 3). Commonness and rarity are complex concepts in Ecology that Considering the reliable lithic records only, the prevalence of involve local population density, trophic level, geographical dis- humans would be on the fourth quartile of the distributions of tribution range, and variety of habitats occupied by a species

Fig. 4. Distribution of the prevalence of primary consumers (a), (d) and carnivores (b), (e) in Europe (upper row) and the Iberian Peninsula (lower row). The cumulative density functions (CDFs) of the distributions of prevalence in Europe (c) and the Iberian Peninsula (f) are used to evaluate the commonness or rarity of hominins in the late Early Pleistocene (see text). Continuous line: primary consumers; dashed line: carnivores. The vertical dotted lines show the prevalence of hominins computed on the basis of the fossil record and on the basis of the number of reliable lithic assemblages. 126 J. Rodríguez et al. / Quaternary International 389 (2015) 119e130

(Rabinowitz, 1981; Gaston and Fuller, 2007; Bennett and Provan, of the mammal species with broad habitat distributions occur at 2008; Gaston, 2008). Population density is difficult to estimate on low population densities. The relatively high prevalence of late the basis of palaeontological data, but see Meloro et al. (2007). Early Pleistocene carnivores is likely related to the larger sizes of Thus, we focus our evaluation of rarity in late Early Pleistocene their geographical ranges. It has been widely demonstrated that large mammals on the number of occurrences (prevalence) and the carnivores have lower population density and larger home ranges size of the distribution range. The pattern of rarity observed in our than primary consumers of similar size (Kelt and Van Vuren, 1999; results, either for carnivores or primary consumers, is composed of Jetz et al., 2004). Thus, carnivores must have large geographical a small number of common species and a large number of rare range sizes to sustain populations large enough to avoid extinction species. This pattern is not an artefact of the palaeontological re- (Hernandez Fernandez and Vrba, 2005). Moreover, the relatively cord, as may be thought, since the same pattern is observed in large geographical range of carnivores is also related to their recent faunas (Gaston, 2008). In her classic book on biological di- increased home ranges, marked territoriality and high dispersal versity Magurran (2004, pp. 18) wrote: “In no environment … are abilities. Our results failed to detect statistically significant differ- all species equally common. Instead, it is universally the case that ences in the sizes of the geographical ranges of carnivores and some are abundant, others only moderately common, and the primary consumers, but the distribution of Rg (Fig. 5) and of the remainder-often the majority-rare”. Rarity is not unusual among latitudinal and longitudinal amplitude (Fig. 6) suggest that a ten- recent large mammals. Almost half the species of carnivores in the dency exists in carnivores towards larger geographical ranges. world have relatively small populations and distributions, and mammals as a whole show a high frequency of rare species (Yu and 4.1. Commonness vs. rarity in hominins Dobson, 2000). Although the distribution of prevalence shown by our results is It is apparent from our results that, if the rarity of humans in late coherent with what may be expected on the basis of the frequency Early Pleistocene Europe is judged on the basis of the number of of rarity among recent mammals, it should be acknowledged that sites with hominin fossils, Homo was not one of the most common our results may have been affected by the faunal turnover occurred taxa in the European ecosystems. Homo appears as a moderately inside the time period under consideration. Most of the 1.4e0.8 Ma rare taxon when compared with the prevalence of carnivores, but time interval corresponds to the early Galerian or Epi- not when compared with the prevalence of primary consumers. In Villafranchian Large-Mammal Age (Palombo, 2010; Kahlke et al., contrast, in the Iberian Peninsula, where all sites with Homo re- 2011). Nevertheless, the older LFs included in our database mains are located, the prevalence of humans is above the median of should be considered as late Villafranchian (like Pirro Nord, either carnivores or primary consumers and, thus, it may be Sandalja-1, Ceyssaguet 1, Sainzelles, Beftia or Barranco Leon D). considered a moderately common species. Although the trophic Consequently, some of the species included in the analyses were behaviour of Early Pleistocene hominins is a hotly debated topic not present in Europe along the entire time interval considered. (Binford, 1981; Blumenschine and Madrigal, 1993; Bunn and Ezzo, Likely, some of those species were widely distributed and common, 1993; Bunn, 2001; Pickering, 2001; Bunn and Pickering, 2010; but because of their restricted time distribution they are recorded Domínguez-Rodrigo et al., 2010; Bunn and Gurtov, 2014), they are only in the local faunas of appropriate age. Those species would best described as omnivores that included a high proportion of seem to be rarer than they actually were. In despite of this possible animal food in their diets, and used large mammals as a key trophic bias, restriction of the analyses to the Epi-Villafranchian faunas has resource Indeed, it has been suggested that hominins were skilled little effect on the pattern of prevalence and on the distribution of scavengers, able to successfully compete with such a highly geographical range sizes (results not shown). specialized carnivore as the giant hyaena (Espigares et al., 2013) On average, late Early Pleistocene carnivores exhibit higher Thus, hominins are expected to behave in an intermediate way prevalence than primary consumers (Fig. 4). This result may seem between strict primary and secondary consumers. Taking all this to be odd, because it is a well-established rule that carnivores have together it is apparent that, without being an extremely common lower population densities than primary consumers of the same taxon, Homo sp. was not a rare component of the late Early Pleis- size (Damuth, 1991; Carbone and Gittleman, 2002). However, tocene ecological communities of Europe. prevalence is not related to population density or abundance in a The question of how many hominin species inhabited Europe simple way. A species may be common because it has a large dis- during the Early Pleistocene is beyond the scope of this paper. tribution and it is found in many localities inside its distribution, Though, it is necessary to acknowledge that existence of more than although at low densities. In his analysis of rarity in recent mam- one hominin species in Europe during this period, as proposed by mals Yu and Dobson (Yu and Dobson, 2000) found that almost 25% some authors (Bermúdez de Castro and Martinon-Torres, 2013),

Fig. 5. Distribution of the range size (Rg) in km of large primary consumers (a) and carnivores (b). The empirical cumulative density functions (c) have been used to test for differences between the distributions using a KolmogoroveSmirnov test. J. Rodríguez et al. / Quaternary International 389 (2015) 119e130 127

entire range estimated for them, but this was not the case of hominins. The lithic record show that hominins were present at Happisburgh, Atapuerca and Korolevo VII (Koulakovska et al., 2010; Parfitt et al., 2010; Rodríguez et al., 2011) at roughly the same time. The lithic record suggests that humans had a high occupancy and were widely distributed across Europe during the late Early Pleistocene, but this does not imply that they were abundant. As discussed above, prevalence and geographical range size are not directly related to local population density. Moreover, a low pop- ulation density would explain why hominins show a moderate prevalence in the palaeontological record. We lack reliable proxies to estimate local population densities in the past. Number of ele- ments or minimum number of individuals may serve to assess the relative abundance in the environment of the species in a fossil assemblage (Delpech, 1999; Hertler and Volmer, 2008; Fa et al., 2013), although taphonomic processes may severely affect the es- timates. Comparison of species abundances among different as- Fig. 6. Latitudinal and longitudinal amplitude of the geographical distribution of large semblages, affected by diverse accumulation and diagenetic primary consumers (squares), carnivores (black dots) and hominins (black stars) in processes, is even more problematic using those proxies. Recently, Europe during the late Early Pleistocene. The geographical distribution of hominins has been calculated both on the basis of the fossil record (F) and on the basis of lithic Rodríguez-Gomez et al. (2013) explored resource availability at assemblages (L). The dotted lines indicate the maximum possible latitudinal and Atapuerca TD6 and showed that this southern European ecosystem longitudinal differences between two points inside the sampled area. was able to sustain high hominin population densities. Moreover, Rodríguez et al. (2014) showed that ungulate carrying capacity was high in Mediterranean ecosystems during the late Early Pleisto- would affect our results. If the European Early Pleistocene Homo cene, suggesting abundance of meat resources. Since all hominin fossils actually correspond to several species the prevalence of each fossils have been found in southern Europe, and assuming that the of those hominin species would be markedly lower than estimated probability of being preserved in the fossil record is directly pro- for the genus. Moreover, it would not be possible to match a lithic portional to population density, it may be speculated that hominins assemblage with a particular species, and our analyses of the size of occurred at higher population densities in southern Europe than in the distribution range would not be valid. Analyses of rarity in Early the rest of the continent. An analysis of the spatial variation of Pleistocene mammals at the genus level may be proposed as an resource availability across Europe during the late Early Pleistocene alternative to address this eventuality. However, an analysis at the and its relationship to the distribution of hominin occupancy would genus level would have little ecological meaning, since rare and help to test this hypothesis. common species in the same genus would be merged together. In addition, since not all genera include the same number of species, 5. Conclusions those genera with more species would tend to exhibit higher prevalence. Moreover, as explained in the material and methods The palaeoanthropological record suggests that hominins were section, we adopted a conservative, non-splitting, criterion in not a rare component of the late Early Pleistocene European eco- reviewing the taxonomic consistency of the large mammal LFs. systems, although they were not among the most common ele- Thus, there is no reason to change the criterion in the case of ments. In contrast, the archaeological record suggests that they hominins. Taking into account all these considerations, and given were widely distributed. It may be speculated that hominins were than it is currently not known how many hominin species inhabi- present in many areas but at low densities. On the one hand, if ted Europe, we present our results at the species level as a first humans occurred at low population densities their probability to be quantitative evaluation of the relative rarity of humans in the late preserved as fossils would be low. On the other hand, a small hu- Early Pleistocene. man population would be able to produce several lithic assem- When their prevalence and distribution in late Early Pleistocene blages, some of which might be recovered. Considering Early Europe is estimated from the lithic archaeological record, hominins Pleistocene hominins as a frequent but not abundant species adds a become a common and widely distributed species. However, the new dimension to our understanding of the ecological and de- lithic and the palaeontological records are of different nature, and a mographic constraints of the first colonization of Europe. direct comparison is not warranted. In general, lithic artifacts have higher preservational probabilities than bones. Moreover, a single hominin individual may contribute to the palaeontological record Acknowledgements not only with a single skeleton, composed of several elements, but also with thousands of lithic artefacts produced during its life. Thus, This research was funded by the MINECO project, CGL2012- we must expect lithic evidence always to be more abundant than 38434-C03-02. G. Rodríguez-Gomez was the beneficiary of a pre- palaeontological evidence. In any case, the lithic archaeological doctoral FPI Grant from the Spanish MICINN. We thank L. Arnold, record shows that hominins were one of the most widely distrib- M. Duval, D. Hoffmann and J. M. Pares for having invited J. Rodrí- uted European species in the late Early Pleistocene. More inter- guez to participate in the “The Early-Middle Pleistocene transition: estingly, hominins were one of the few species with a wide Significance of the Jaramillo subchron in the sedimentary record” latitudinal range, may be an indication of a highly carnivorous diet. Workshop and to contribute to this volume. Thanks also to the Certainly, variations in the distribution of species in Europe during workshop participants for their thought provoking discussion and the late Early Pleistocene cannot be assessed with the data pre- suggestions and especially to B. Martínez-Navarro and an anony- sented here. Thus, the geographical ranges estimated here should mous reviewer for their useful comments on the manuscript. An be taken as the maximum distribution of the species in the period anonymous editor from Elsevier's Language services improved the as a whole. Likely, many species never occupied simultaneously the English of the original manuscript. 128 J. Rodríguez et al. / Quaternary International 389 (2015) 119e130

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