Palaeogeography, Palaeoclimatology, Palaeoecology 365–366 (2012) 99–114

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Palaeogeography, Palaeoclimatology, Palaeoecology

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Predator–prey relationships and the role of Homo in Early Pleistocene food webs in Southern Europe

Jesús Rodríguez a,⁎, Guillermo Rodríguez-Gómez a, Jesús Angel Martín-González b,1, Idoia Goikoetxea a, Ana Mateos a a Centro Nacional de Investigación sobre la Evolución Humana (CENIEH), Paseo Sierra de Atapuerca s/n 09002 Burgos, Spain b Dpt. Matemáticas y Computación, Universidad de Burgos, Burgos, Spain article info abstract

Article history: Predator/prey relationships in Mediterranean Europe during the Early Pleistocene are analysed at the local Received 18 June 2012 and regional scales and compared to patterns observed in recent fauna from four regions worldwide (East Received in revised form 10 September 2012 Africa, South Africa, Southeast Asia and North America). Three subregions (South Eastern, Central and Accepted 18 September 2012 South Western Mediterranean) and three time periods (middle Villafranchian, late Villafranchian and Available online 25 September 2012 Galerian) are considered. Our approach focuses on large primary consumers and their potential predators; both are defined as mammals weighing over 10 kg. Early Pleistocene food webs are characterised by a unique Keywords: Predator/prey body size distribution of primary consumers and an extremely rich carnivore guild. These characteristics Food web likely affected ecosystem function in a way not observed in recent communities. The percentage of megafau- Megafauna na species was higher in the middle Villafranchian than in recent fauna, and it increased in the late Pleistocene Villafranchian and early Galerian. The number of predators able to kill megafauna species was high in the late Villafranchian but decreased to modern values in the early Galerian. Competition inside the carnivore guild was similar to recent values in the middle Villafranchian and early Galerian but higher in the late Villafranchian. Hominins likely entered Europe during the late Villafranchian, when survival opportunities for a hunter–gatherer were low and hominins were most likely relegated to a marginal role in the palaeocommunity. This scenario changed in the early Galerian with the extinction of several predators and relatively reduced intraguild competition. © 2012 Elsevier B.V. All rights reserved.

1. Introduction Domínguez-Rodrigo et al., 2010) and Swartkrans (Pickering, 2001) evidencing that primary access to ungulate carcasses in search of Resource availability and competition with carnivores influenced meat, not only marrow, was a common practice and suggesting that survival opportunities for Early Pleistocene hominins and conditioned hunting activities were also important for those Early Pleistocene their ability to spread beyond Africa. Most recent hunter–gatherer human populations. Evidence of primary access to ungulate carcasses populations from temperate regions relied on animal resources as has also been found in Europe, at the lower levels of the Sima del their main energy source (Cordain et al., 2000), and a wide consensus Elefante site (Rodríguez et al., 2011). Moreover, several authors stress of researchers considers that large mammals were key resources for the importance of the carnivore guild composition and food web Palaeolithic foragers (e.g. Binford, 1981; 1985; Marean, 1989; structure, containing large herbivores that weighed over 20 kg and Moigne and Barsky, 1999; Gaudzinski and Roebroeks, 2000; their predators, in conditioning access opportunities for the earliest Roebroeks, 2001; Speth, 2010). The role played by large mammals European hominins to meat resources (Turner, 1992a; Arribas and as a key food resource for early Homo is, however, a more controver- Palmqvist, 1999; Croitor and Brugal, 2010; Palombo, 2010). sial topic. It was initially proposed that Early Pleistocene Homo Studies about food web structures and predator/prey relationships accessed large mammal carcasses mainly through scavenging and in have a long tradition in ecology (Cohen, 1977; Critchlow and Stearns, search of bone marrow (Binford, 1981; Blumenschine et al., 1994). 1982; Pimm et al., 1991; Pascual and Dunne, 2006; Owen-Smith and However, this interpretation has been challenged by several recent Mills, 2008). Several studies have also addressed predator/prey studies at Olduvai Gorge (Bunn, 2001; Bunn and Pickering, 2010; relationships in the Pleistocene both at the regional (Palombo and Mussi, 2006; Raia et al., 2007; Croitor and Brugal, 2010; Palombo, 2010) and local community scales (Stiner, 1992; Palmqvist et al., ⁎ Corresponding author at: CENIEH, Paseo Sierra de Atapuerca s/n 09002 Burgos, Spain. 2008; Perez-Claros and Palmqvist, 2008; Feranec et al., 2010). How- Tel.: +34 947040800; fax: +34 947040810. E-mail address: [email protected] (J. Rodríguez). ever, predator/prey relationships at regional fauna scale are generally 1 Temporarily assigned to CENIEH. described using crude predator/prey species ratios, or even carnivore/

0031-0182/$ – see front matter © 2012 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.palaeo.2012.09.017 100 J. Rodríguez et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 365–366 (2012) 99–114 non-carnivore proportions, considering neither the predators' prefer- Mediterranean region of Europe below 45° N was separated from ences and killing abilities nor the potential prey's characteristics. the rest of Europe by a bio-geographic and climatic frontier of varying Exceptions to these general rules include the description of carnivore intensity throughout the Early Pleistocene (Rodríguez et al., 2011). intra-guild completion in Java during the Pleistocene by Hertler and We here analyse the changes in European food web structures Volmer (2008), based on estimations of carnivore species' prey size below the 45° N parallel throughout the Early Pleistocene to detect preferences, the study of European felids and their prey by Hemmer changes in resource availability for the first human colonisers. As (2004) and the analysis of the effect of predator pressure on prey Kostopoukus et al. (Kostopoulus et al., 2007) discussed, the three abundance in Plio-Pleistocene Italy by Meloro et al. (2007). Works southern peninsulas included in this region have been separated by focusing on local assemblages are usually more refined in their ecological and geographical barriers since the Caenozoic, though approach and provide accurate information on predator preferences connections between Italy and the Balkans occurred during glacial (García et al., 2009; Feranec et al., 2010) and food web function periods allowing some species to migrate from one peninsula to the (Palmqvist et al., 2003; Palmqvist et al., 2008). Nevertheless, studying other (Michaux et al., 2005) We have thus subdivided Mediterranean changes in predator/prey relationships through evolutionary time Europe into three subregions, coinciding with the three peninsulas. and detecting generalised food web patterns are not possible when a study focuses on a single assemblage. We present a new perspective that studies food web patterns and 2. Methods predator prey relationships in Early Pleistocene Southern Europe both at the regional and local scales using a macroecological approach The study area includes southern Europe below latitude 45 °N. This (Brown, 1995). We combine information from studies on local assem- area has been divided into three subregions (Fig. 1), South West (lon- blages, morphofunctional analyses and behavioural information on gitude from −10.00 to 4.00 degrees), Central (longitude from 4.00 to living relatives to assess the prey preferences of Early Pleistocene 18.00 degrees) and South East (longitude from 18.00 to 40.00), basical- large carnivores. This information is eventually used to evaluate ly coinciding with the three southern peninsulas. A dataset of Early predator/prey relationships at the local and regional scales, consider- Pleistocene Local Faunas from this area has been compiled from pub- ing predator preferences and the ecological characteristics of the lished sources (Table 1). Three time periods, corresponding to the mid- potential prey species. Furthermore, the Pleistocene food web dle Villafranchian (2.6–1.8 Ma), late Villafranchian (1.8–1.2 Ma) and characteristics are interpreted using the patterns observed in several early Galerian (1.2–0.78 Ma) (Palombo, 2010) or Epi-Villafranchian selected recent faunas. (Kahlke et al., 2011) were distinguished, and local faunas were Homo likely arrived in Europe during the late Villafranchian, al- assigned to one according to biostratigraphic correlations and numeri- though human populations were unable to cross parallel 45°N until cal ages provided by the original sources. Numerical ages were always 1.2 Ma at the beginning of the Galerian (Rodríguez et al., 2011). The preferred to biostratigraphic correlations for assigning a site to a time

Fig. 1. The study area has been divided into three sub-regions: South Western (SW), South Central (C) and South East (SE) Europe. Middle Villafranchian sites are marked with black dots, late Villafranchian sites are marked with black triangles and early Galerian sites with white dots. J. Rodríguez et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 365–366 (2012) 99–114 101

Table 1 South Mediterranean early Pleistocene Local Faunas used in the present study. PD=The Paleobiology Database searched on 16-04-2010. http://paleodb.org/.

Region Age Locality Longitude Latitude References

SW Mediterranean Galerian Atapuerca Sima del Elefante TE 08 to TE14 −3.52 42.35 Rodríguez et al., 2011 Atapuerca-Dolina TD3-TD4 −3.52 42.35 Rodríguez et al., 2011 Atapuerca-Dolina TD5 −3.52 42.35 Rodríguez et al., 2011 Atapuerca-Dolina TD6 1-2 −3.52 42.35 Rodríguez et al., 2011 Atapuerca-Dolina TD6-3 −3.52 42.35 Rodríguez et al., 2011 Durfort 3.95 43.98 PD Estrecho de Quipar −1.88 38.04 Scott and Gibert, 2009 Huescar-1 −2.50 37.77 PD Sierra de Quibas −0.93 38.20 Montoya et al., 2001; Montoya et al., 1999 Vallparadís 10-10c 2.02 41.56 Martínez et al., 2010 Late Villafranchian Barranco León V −2.43 37.71 Scott and Gibert, 2009 Cueva Victoria −1.18 37.85 Gibert et al., 1999 El Chaparral C1-C2 36.69 −5.39 Giles Pacheco et al., 2011 Fuente Nueva 1 −2.38 37.70 PD Fuente Nueva-3 −2.40 37.71 PD Lézignan-le-Cèbe 3.43 43.48 Crochet et al., 2009 Venta Micena −2.38 37.73 PD Middle Villafranchian Casablanca 1 −0.22 39.76 PD Fonelas P-1 −3.17 37.40 PD Montoussé 5 0.40 43.07 PD Puebla de Valverde −0.91 40.21 Azanza et al., 1997 Valdeganga III −1.68 39.13 Hernández-Fernández, 2004 Central Mediterranean Galerian Colle Curti 12.75 42.95 Palombo et al., 2000–2002 Grotte du Vallonnet III 7.47 43.77 de Lumley et al., 1988 Imola 11.71 44.35 Palombo et al., 2000–2002 Redicicoli 41.93 12.52 Raia et al., 2009 Torre di Picchio 12.49 42.65 Raia et al., 2009 Late Villafranchian Capena 12.55 42.17 Palombo et al., 2000–2002 Casa Frata 11.57 43.55 Palombo et al., 2000–2002 Il Crostolo 10.56 44.63 Palombo et al., 2000–2002 La Sartanette 4.50 43.76 Palombo and Valli, 2003–2004 Pietrafitta 12.21 42.99 PD Pirro Nord Combined 13.65 43.28 PD Selvella 11.76 42.93 PD Val di Chiana sands of the first fluviolacustrine phase 11.73 43.41 Torre et al., 1992 Palombo et al., 2000–2002 Middle Villafranchian Casa Sgherri 10.80 43.77 Marcolini et al., 2000 Casino Lignite mine, Upper lacustrine level 11.33 43.32 PD Collepardo 13.36 41.76 Palombo et al., 2000–2002 Cornillet 6.20 43.91 Palombo and Valli, 2003–2004 Costa San Giacomo 13.36 41.76 Palombo et al., 2000–2002 Saint-Vallier 5.02 44.81 PD Valle Catenaccio 13.36 41.76 Palombo et al., 2000–2002 SE Mediterranean Galerian Kozarnika 11c 22.68 43.63 Guadelli et al., 2005 Kozarnika 11d 22.68 43.63 Guadelli et al., 2005 Kozarnika 12 22.68 43.63 Guadelli et al., 2005 Kozarnika 13 22.68 43.63 Guadelli et al., 2005 Krimni 40.50 23.50 Koufos, 2001 Kunino Lower Level 23.96 43.18 Palombo et al., 2006 Marathousa-Megalopolis 22.04 37.51 Palombo et al., 2006 Ravin Voulgarakis 23.50 40.60 Palombo et al., 2006 Sandalja-I 13.89 44.90 Kahlke et al., 2011 Late Villafranchian Alikes 22.81 39.29 Palombo et al., 2006 Libakos 21.30 40.63 Palombo et al., 2006 Middle Villafranchian Dafnero 1 21.59 40.17 Spassov, 2003 Gerakarou 23.22 40.65 PD Sésklo 22.82 39.63 Athanassiou, 2003 Slatina 2 24.37 44.43 PD Slivnitsa 23.02 42.87 PD Valea Roscai 24.09 44.78 PD Varshets 23.38 43.19 Spassov, 2003 Vassiloudi 23.22 40.65 Palombo et al., 2006 Vatera 26.20 39.02 Palombo et al., 2006 Volakas 24.15 41.24 Palombo et al., 2006

period, and only sites that may be confidently classified into one of obtain a taxonomically consistent database. We based our review on these three time intervals were included. Taxonomic inconsistency is systematic revisions of groups by specialists (Turner, 1992b; Weers, a potential drawback in such compiled lists (Rodríguez, 2006; 1994; Alberdi et al., 1998; Made and Mazo, 2003; Breda and Palombo et al., 2010) for several reasons. Different authors frequently Marchetti, 2005; Croitor, 2005, 2006a, b; Crégut-Bonnoure, 2007; use different names for the same species; conversely, the same name Fostowicz-Frelik, 2008; Turner et al., 2008). This study focuses on may be used for taxa that are actually different. Old publications may large mammals, defined as species weighing more than 10 kg. Carni- also use names currently considered invalid. To address this problem, vore species included in this size category in the studied faunas belong we reviewed all faunal lists and applied uniform taxonomic criteria to to the families Felidae, Canidae, Hyaenidae and Ursidae. This size is 102 J. Rodríguez et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 365–366 (2012) 99–114 slightly below the threshold where predators shift from small to large Table 3 prey, which is set at 21.5 kg (Carbone et al., 1999). We prefer to pro- The 25 recent local assemblages used in the analyses. MAB=Man and the Biosphere Fauna Database. UNESCO. Man and the Biosphere Program (MAB). Information Center ceed in this way to not exclude any medium-sized carnivore species for the Environment (University of California, Davis) http://ice.ucdavis.edu. that includes large prey in its diet. Regional Faunas were composed of all species present in the Local Region Locality Longitude Latitude References Faunas (LFs) of the same age for each region. Combining the three East Amboseli 37.15 −2.39 MAB regions with the three time periods considered, we obtain nine Africa East Usambara 38.20 −4.45 Rodgers and Homewood, Regional Faunas (Table 2). Species recorded at least in one middle 1981 Lake Manyara 35.60 −3.30 MAB Villafranchian and one Galerian LF from the same region are assumed Mount Kenya 37.19 0.10 Young and Evans, 1993 to have also been part of that Regional Fauna during the late Serengeti 35.10 −2.25 Swynnerton, 1958 Villafranchian. Most LFs are obviously incomplete and thus inade- South Turkana 35.37 1.57 Coe, M, 1972. quate for analysing predator–prey relationships at the local scale. Al- North Coram Biosphere −113.79 48.24 MAB West Reserve though it is difficult to establish strong criteria to determine whether America Craters of the Moon −113.10 43.33 MAB a LF is reasonably complete, we have selected a subset of LFs that may Glacier −113.50 48.37 MAB be considered complete or nearly complete. The criterion followed in Grand Teton −110.71 43.81 MAB this selection procedure is to compute the number of carnivore spe- Waterton −113.50 49.60 MAB − cies and prey species for all LFs, including only those LFs in the fourth Yellowstone 110.10 44.58 MAB South Kruger 31.24 −24.35 MAB quartile both for the number of carnivores (>5 species) and the num- Africa Malolotjia Nature 31.30 −26.00 MAB ber of prey (>9 species). Two Galerian LFs (Le Vallonet III and Reserve Kozarnika 13), three late Villafranchian LFs (Pirro Nord, Cueva Victo- Mlawula 32.00 −26.00 MAB ria and Venta Micena) and four middle Villafranchian LFs (Fonelas, Transvaal 38 28.15 −26.20 Rautenbach, 1978 − Puebla de Valverde, Gerakarou and Saint-Vallier) met this criterion. Transvaal 41 29.45 23.15 Rautenbach, 1978 Transvaal 42 27.15 −25.15 Rautenbach, 1978 Completeness of the fossil Regional faunas has been tested using Transvaal 44 30.10 −23.15 Rautenbach, 1978 the CIbda index described in Maas et al. (1995).CIbda is based in the Weenen Game 30.40 −28.70 Bourquin and proportion of genera recorded before and after a time interval but Reserve Mathias, 1995 South Bandhavgarh 80.77 23.39 MAB not in the time interval. Thus, in our case, CIbda can only be computed East Mount Everest 86.72 27.93 MAB for the late Villafranchian faunas. Completeness index is computed Asia (Sagarmatha) as: Royal Chitwan 84.33 27.29 MAB Sanjay 81.37 23.77 MAB ¼ ½=ðÞþ CIbda Nbda Nbda Nrt 100 Simlipal 86.35 21.70 MAB

Where Nbda is the number of genera actually known, before, dur- ing and after the interval and Nrt is the number of genera occurring all the localities where the species has been recorded. Thus, range before and after, but not during the interval. CIbda varies from 0 to maps may predict the presence of a species in places where it is actu- 100. ally absent. On the contrary, compiling the regional Fauna by pooling A set of 25 recent LF from four regions has been selected for com- the species lists from localities inside the region tends to underesti- parison (Table 3 and Fig. 2). These four regions were selected because mate regional species richness, since species living inside the area, they retain a large proportion of medium- and large-sized mammals but not in the sampled localities, are missed. and include a significant number of natural reserves with species Andrews et al. (1979) defined nine body size categories that have lists available for use as local faunas. A 7×7 degree square was used been recurrently used in mammalian palaeoecology with minor mod- to delimit each Regional Fauna, obtaining areas of similar size to the ifications (Andrews et al., 1989; Andrews, 1995; Kay and Madden, three southern European subregions (Table 2). The species lists for 1997; Andrews and O'Brien, 2000; Rodríguez, 2001; Rodríguez et al., the four recent Regional Faunas were compiled from the LF in each re- 2004): A=1–500 g; B=500–1,000 g; C=1–10 kg; D=10–45 kg; gion. This compilation procedure is preferred to using range maps to E=45–90 kg; F=90–180 kg; G=180–360 kg; H=360–1000 kg obtain the species composition of the regional faunas, as it mimics the and I>1,000 kg. We use these body size categories to classify the pri- way that Fossil Regional Faunas have been compiled. Using range mary consumer species present in our dataset of recent and fossil as- maps tends to overestimate the actual number of species in a region, semblages. These intervals have also been used to describe the prey since they are usually drawn as minimum contour curves including preferences of each species of carnivore. Prey preferences for each carnivore have been defined as follows: the “Preferred prey” species (P) is the main prey items of each carnivore species, usually defined Table 2 as the species inside a size interval; and the “Secondary prey” species The nine early Pleistocene and four recent Regional Faunas considered in this study according to geographical region and age. (S) includes species below and above the preferred size interval (see Supplementary Material). Our P and S categories are conceptually Region Area Age Regional Time interval equivalent to the Prey Focus Mass and Prey Mass Spectra of Hertler (km2) Fauna (M.a.) and Volmer (2008). Most predators do not have an absolute lower South Eastern 683,782 Galerian SE Gal 1.2–0.78 limit for the size of their prey (Radloff and Du Toit, 2004). Group Mediterranean late Villafranchian SE lVil 1.8–1.2 hunters usually kill smaller species when they hunt alone (Hayward middle Villafranchian SE mVvil 2.6–1.8 Central 202,761 Galerian C Gal 1.2–0.78 et al., 2006b), and young and small individuals usually kill prey Mediterranean late Villafranchian C lVil 1.8–1.2 below the optimum size for their species (Henschel and Skinner, middle Villafranchian C mVvil 2.6–1.8 1990). All prey species with body sizes below the preferred prey – South Western 514,421 Galerian SW Gal 1.2 0.78 body size interval for a predator have thus been considered “Second- – Mediterranean late Villafranchian SW lVil 1.8 1.2 ” middle Villafranchian SW mVvil 2.6–1.8 ary prey . Prey species above the preferred prey size of a predator, East Africa 604,463 Recent E Afr. – i.e., preferentially weakened individuals, may also be hunted, al- South Africa 545,945 Recent S Afr. – though an upper prey size limit is determined by the ability of a single NW America 550,033 Recent NW A. – individual or a group of individuals to safely subdue and kill a prey. – SE Asia 415,900 Recent SE A. Some species, including porcupines, have not been classified as J. Rodríguez et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 365–366 (2012) 99–114 103

Fig. 2. Recent faunas from four areas have been selected for comparison. Black squares represent the four regions: North West America (MW A.), East Africa (E Afr.), South Africa (S Afr.) and Southeast Asia (SE A.). White dots mark the positions of the National Parks and Reserves sampled in each region.

“preferred prey” for any predator because although several carnivores species are thus assumed to be omnivorous canids that preyed prefer- hunt them, these predators usually prefer other available species with entially on small mammals and consumed carrion opportunistically. similar sizes. Species larger than the maximum prey size for the The arrival of the genus Canis increased the species diversity of the predator have been classified as “No prey” (N). For some species, tribe but did not widen its trophic habits. Three species are recorded e.g., bears, no prey species have been classified as “Preferred”, and in Southern Europe during the Early Pleistocene: C. arnensis, only “Secondary prey” have been marked. We thus try to reflect C. etruscus and C. accitanus. They are small-sized Canini, comparable that meat comprises only a small proportion of a bear's diet to modern coyotes or jackals. Moreover, C. arnensis is considered (Garshelis, 2009). The number of predators per prey size interval (Olive, 2006) closely related to the African jackals, while C. etruscus has been computed as the number of predators with at least one represents a sister species to the clade, including the wolf and coyote. prey (main or secondary) in the size interval. C. accitanus (Garrido and Arribas, 2008) is the smallest species of the We have measured competition for resources among predators genus Canis and an specialised omnivore derived from C. arnensis. based on the number of predator species that share a prey species. The small canid from Venta Micena, first identified as C. etruscus The Total Number of Predators (TNP) for each primary consumer spe- (Palmqvist et al., 1996) and later as C. mosbachensis, has been cies in a fauna has been computed as the number of carnivore species interpreted as an omnivorous species with a diet similar to modern that can kill it. The number of main predators (NMP) for each primary coyotes, based on morphofunctional analyses (Palmqvist et al., consumer has also been computed as the number of carnivore species 1999) and isotopic evidence (Palmqvist et al., 2003). Extant coyotes that have this species as a preferred prey. The mean NMP value for all (C. latrans) are opportunistic social predators that eat invertebrates, primary consumers in a fauna (MNMP) is used to measure the inten- small mammals, ungulates and even some fruits. They consume sity of the competition inside the predatory guild. Primary consumers large mammals, usually as carrion, but they also hunt small ungulates, with NMP=0 are excluded from the MNMP computation, as it seeks especially fawns (Sillero-Zubiri, 2009). We assume a diet similar to to reflect to what degree predators share an average prey. modern coyotes and jackals for the Early Pleistocene species in the genus Canis. Rodents and lagomorphs are assumed be the main 2.1. Predatory behaviour of Early Pleistocene carnivores meat resources, but sporadic ungulate hunting in the 10–45 kg size category is also considered feasible. Carrion would be eaten when Several information sources have been combined to reconstruct available. the prey preferences and predatory behaviour of fossil carnivores. The taxonomy of large wild dogs is a complex and controversial We have combined published data from morphofunctional and topic, but we follow previous research (Martínez-Navarro and Rook, isotopic analyses with information on closely related living species 2003) in considering that all hypercarnivorous forms of the European of similar size, as discussed below. Early Pleistocene belong to the genus Lycaon, with two chronospecies: The first European Canini appeared in the late Miocene and L. falconeri in the middle Villafranchian and L. lycaonoides in the late belonged to the genus Eucyon (Rook, 2009), which is also recorded Villafranchian and early Galerian. Palmqvist et al. (1999) consider in the South Eastern Mediterranean region during the middle Early Pleistocene wild dogs to be hypercarnivorous canids, similar to Villafranchian (Spassov, 2003). Considering the relatively small size the gray wolf, based on their morphofunctional characteristics. Isotopic of Eucyon, we may assume feeding habits similar to those of jackals. analyses at Venta Micena indicate that horses and bovids in open envi- Jackals (Canis aureus and Canis mesomelas) are omnivorous canids ronments were the preferred prey of wild dogs (Palmqvist et al., 2003). with an opportunistic diet, which may include a large amount of veg- In a further analysis, Palmqvist et al. (2008) report the main prey Equus etable food. Small mammals and other vertebrates constitute a major altidens (58%), Hemitragus albus (30%) and Pseudodama sp. (12%). Their part of their diet; small ungulates are opportunistically hunted, and modern relative, the African wild dog (Lycaon pictus), is a social hunter carrion is consumed when available (Sillero-Zubiri, 2009). Eucyon that prefers prey within a bimodal body size range of 16–32 kg and 104 J. Rodríguez et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 365–366 (2012) 99–114

120–140 kg. A single wild dog, weighing 17–36 kg, may kill an adult Pleistocene spotted hyaenas; however, potential prey in the female Tragelaphus strepsiceros weighing more than 120 kg, but the bi- 10–45 kg interval were most likely common prey for solitary hunting modal distribution of preferred prey sizes likely reflects the different individuals. We can also assume that groups of hyaenas regularly abilities of solitary and group hunting individuals. Scavenging has a killed ungulates in the 180–360 kg and 360–1,000 kg weight inter- marginal importance in wild dogs' diets (Hayward et al., 2006b). We vals. Even young individuals of species with more than 1,000 kg of consider Early Pleistocene wild dogs as social hunters with preferred adult body weight were likely opportunistically killed. prey in the range 90–360 kg body weight. However, prey in the smaller Felids are hypercarnivorous mammals and extremely effective size categories (10–45 and 45–90 kg) were likely a significant compo- hunters. Six genera and ten species, ranging in size from 10 kg to nent in the diet of this predator. approximately 200 kg, have been recorded in southern Europe during Hyaenids were represented in Early Pleistocene southern Europe by the Early Pleistocene. The Lynx lineage includes two chronospecies: four genera, differing in body size and feeding habits: the scavengers L. issiodorensis and L. pardinus spealeus. Lynx issiodorensis might be Pliocrocuta and Pachycrocuta and the hunting hyaenids Chasmaporthetes similar in size to a living Eurasian lynx (Lynx lynx), which would be and Crocuta. the best analogue to infer for the predatory behaviour of this felid Pliocrocuta perrieri was a medium-sized hyaenid that Turner et al. (Carotenuto, 2009). Eurasian lynxes prey on small ungulates in the (2008) classifies in his Ecomorph Group 6, “fully developed bone 10–45 kg size interval, (Capreolus sp., Rupicapra sp., and Moschus crackers”. We consider Pliocrocuta a strict scavenger with behaviour sp.), although reindeer and fallow deer are the preferred prey in analogous to the extant brown hyaena (Parahyaena brunnea). some areas (Sunquist and Sunquist, 2009). Although small mammals, Turner and Antón (1996b) consider the giant hyaena a socially active particularly lagomorphs, were likely present in the diet of Lynx scavenger that may also have used cooperative hunting to kill large issiodorensis, its main food items were most likely small ungulates ungulates. However, Pachycrocuta brevirostris is generally considered in the 10–45 kg body size category. Prey in the 45–90 kg category a strict scavenger with high bone-cracking capacities (Arribas and are included as secondary prey for L. issiodorensis, as the Eurasian Palmqvist, 1998; Turner et al., 2008; Croitor and Brugal, 2010). lynx has been reported to sporadically take wild boars and red deer Based on the study of the Venta Micena assemblage, Palmqvist et al. (Sunquist and Sunquist, 2009). The Lynx pardinus spelaeus body size (2011) conclude that Pachycrocuta was a strict scavenger or a is intermediate, falling between the recent Lynx pardinus and Lynx specialised kleptoparasite that stole the prey of sabre-tooths and lynx. For Lynx pardinus spelaeus, we assume a diet similar to its de- other large carnivores. In our opinion Pachycocuta brevirostris was scendant, the Iberian lynx. Lagomorphs were likely the base of lynx likely a strict scavenger, however we also take into consideration diet, while species in the 10–45 kg category were sporadically the alternative scenario with Pachycrocuta as an active scavenger taken, so they are included as "secondary prey". able to hunt large ungulates. In this second scenario Pachycrocuta The European cheetah (Acinonyx pardinensis) was approximately would have a lifestyle similar to that of the European Upper Pleisto- 50% larger than the modern cheetah (O'Regan et al., 2002). Modern chee- cene spotted hyanea (Turner and Antón, 1996b), with preferred tahs weigh near 48 kg and specialise in gazelles and medium-sized ungu- prey in the range 45–180 kg although able to kill prey in the lates as prey, although male coalitions may kill prey up to the size of an 10–1,000 kg interval. adult blue wildebeest (Connochaetes taurinus), weighing approximately The relative gracility and less massive dentition of Chasmaporthetes 140 kg (Sunquist and Sunquist, 2009). A meta-analysis of the cheetah's lunensis suggest reduced scavenging habits (Turner, 1992b). According prey preferences (Hayward et al., 2006a) found that these felids prefer to Antón et al. (2006), it could be a social predator, as a single individ- prey in the 23–56 kg range, with a peak at 36 kg; the researchers ual would be unable to subdue and kill medium- and large-sized prey interpreted this specialisation as a strategy to avoid kleptoparasitism by because of its long muzzle and relatively gracile forelimbs. However, capturing prey that may be quickly eaten. Given its larger size, the Euro- Croitor and Brugal (2010) qualify Chasmaporthetes as a “wolf-like” eco- pean cheetah most likely was able to easily kill prey in the upper range type, retaining strong bone-crushing capabilities, and consider this of modern cheetahs. We thus consider that its preferred prey were in hyaenid a solitary predator. The reconstructed shoulder height is simi- the 45–90 kg range and that it also took prey in the 10–45 kg and lar to a large gray wolf (Agustí and Antón, 2002). We consider the most 90–180 kg ranges. likely scenario Chasmaporthetes lunensis being a solitary cursorial pred- In many areas, the diet of the modern leopard (Panthera pardus) ator similar in size to a large gray wolf. Preferred prey would be in the mainly comprises mammals in the 10–40 kg range, and its most 45–90 kg interval, but species in the 10–45 kg and 90–180 kg intervals preferred prey size is 25 kg. Species over 40 kg are generally avoided are also considered potential secondary prey. In the alternative scenar- (Hayward et al., 2006c), but prey up to 250–400 kg are occasionally io, C. lunensis being a social predator, preferred prey size would be in taken. However, this felid can also survive on small prey in areas the interval 45–180 kg and species in the 10–45 kg and 180–360 kg where ungulates have been extirpated (Sunquist and Sunquist, 2009). would be considered as potential secondary prey. In our analyses, the preferred prey size for the Pleistocene P. pardus Crocuta appeared in Europe during the early Galerian. Living spot- has been set in the 10–45 kg range, and species up to 360 kg have ted hyaenas are extremely efficient cooperative hunters. Although been considered “secondary prey”. carrion is taken when available, between 60 and 95% of the spotted The European jaguar (Panthera gombaszoegensis) is considered an hyaenas prey are killed by themselves (Holekamp and Kolowski, ambush hunter similar to the modern jaguar. Isotopic evidence 2009). There is a high overlap in prey selection with lions suggests that European jaguars preyed on browsing ungulates in (Hayward, 2006): the preferred prey size is in the 56–182 kg range, closed environments, particularly on Praemegaceros verticornis (43%), with a mode at 102 kg. Group hunting allows spotted hyaenas to Pseudodama sp. (38%) and Soergelia minor (19%) (Palmqvist et al., kill large species such as zebra stallions (Tilson and Henschel, 1980) 2008). The European jaguar was larger than the extant P. onca (Turner and even elephant calves defended by adults (Salnicki et al., 2001). and Antón, 1996a), and Hemmer (2004) estimates the Villafranchian Kleptoparasitism is also a common practice, although its success de- jaguar body size in the 70–100 kg range and its younger forms size as pends on the opponents' numbers and strength. Being larger than 70–200 kg. Modern jaguars inhabit a variety of forested habitats, from their modern counterparts, groups of spotted hyaenas were most wooded savannas to montane forests and gallery forests. Jaguars are likely able to hunt large Pleistocene mammals such as horses and often associated with rivers and swampy areas. They are non-selective bison (Turner, 2009). Isotopic analyses of spotted hyaena remains hunters that are able to kill prey 3–4 times their own weight and from the late Pleistocene Valdegoba Cave site suggest that C. crocuta whose diet tends to reflect prey abundance in the area (Sunquist and preyed regularly on cervids, horses and rhinos (Feranec et al., Sunquist, 2009). We consider the European jaguar a solitary ambush 2010). A preferred prey range of 45 to 180 kg is here assumed for predator with a preferred prey size in the 90–360 kg range, but it can J. Rodríguez et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 365–366 (2012) 99–114 105 also kill species in the 360–1,000 kg body weight interval. We assume individual unable to subdue and retain a large prey to give it the killing that small ungulates in the 10–45 kg range were also sporadically bite. Kill defence against giant hyaenas (P. brevirostris) is also argued, hunted. favouring a social behaviour in Homotherium (Anton et al., 2005). Soci- European puma-like fossils were attributed in the past to Panthera ality has also been proposed for other sabre-toothed cats, such as schaubi (Viret, 1954)orViretailurus schaubi (Hemmer, 1964) but the Smilodon sp., on a different basis (Carbone et al., 2009). Homotherium prevalent opinion today classifies them in the species Puma pardoides may have been specialised, or at least better adapted than lions, to kill (Hemmer et al., 2001; Madurell-Malapeira et al., 2010). P. pardoides is Proboscideans. This interpretation is mainly based on evidence from more robust cranially and postcranially than living Puma concolor the North American Friesenhahn Cave (Marean and Ehrhardt, 1995), and close in size to the larger individuals of the later species among other studies (Anton et al., 2005). Isotopic analyses performed (Madurell-Malapeira et al., 2010). Hemmer (2004) estimates the by Palmqvist et al. (2003) on material from Venta Micena suggest body weight of Puma pardoides between 35 and 100 kg while body that juvenile Mammuthus were an important part of the diet of weight of recent P. concolor males is in the range 53–72 kg., and fe- Homotherium at this locality, together with Bison sp. (52%) and Equus males weigh 34–48 kg. Living pumas are solitary ambush hunters altidens (38%) (Palmqvist et al., 2008). We consider Homotherium a that prey on small and medium sized ungulates in the range top predator and likely a group hunter, with a preferred prey size in 10–120 kg (mule deer, white-tailed deer, guanacos, pudu, pampas the 90–360 kg range; it could also kill prey in the 10 to 1,000 kg deer, collared pecaries …) and also take smaller mammals (Sunquist range depending on their availability. Juveniles of species weighing and Sunquist, 2009). Male pumas may kill prey up to the size of a more than one ton are also considered vulnerable to Homotherium at- moose (Knopff et al., 2010). A similar ambush hunting behaviour tack. We also take into consideration the alternative scenario of may be assumed for Puma pardoides although, being stronger than Homotherium being specialised in hunting large and very large prey, its living relative, its preferred prey were probably in the range with a preferred prey size in the interval 180–1,000 kg and able to kill 45–180 kg. Hemmer (2004) estimates Prey Focus mass as 50/20 kg even prey heavier than 1,000 kg. and the range of prey masses as 2–50 kg, though these data are Given the disagreement observed in the literature about the hunt- clear underestimations at the light of the prey range of living ing and/or scavenging behaviour of some Early Pleistocene carni- pumas. We propose that ungulates in the size categories 10–45 kg vores, the analyses have been carried out considering two different and 180–360 kg were probably taken as secondary prey by Pleisto- scenarios. In the first one, considered by us the most likely, cene pumas. Homotherium is considered a social predator with a preferred prey Sabre-toothed cats are represented in the Early Pleistocene South size in the 90–360 kg range; Pachycrocuta brevirostris is considered European faunas by the genera Megantereon and Homotherium. a strict scavenger and Chasmaportetes lunensis a solitary predator Megantereon had teeth and forelimbs well adapted to take with preferred prey in the 45–90 kg body weight interval. In the sec- medium-sized prey. Its strong body, large claws and sharp but fragile ond scenario Homotherium is considered a specialised megafauna canines suggest that it captured prey using a short rush, holding them hunter; Pachycrocuta brevirostris is assumed to be an active scavenger down and killing them with a sudden slashing bite (Turner and and hunter; Chasmaporthetes lunensis is considered a social predator, Antón, 1998). Anton et al. (2005) describe Megantereon as a solitary and the preferred prey size of both hyaenids is assumed to be species specialising in ambush hunting in forest environments, espe- 45–180 kg. cially riparian forests. Isotopic analyses suggest that Megantereon hunted browsing and mixed-feeding cervids in a closed habitat 3. Results (Palmqvist et al., 2003) and that the main prey at Venta Micena were Soergelia minor, Equus altidens and Praemegaceros verticornis Both scenarios of predator preferences produced very similar re- (Palmqvist et al., 2011). The adult mean body weights of these species sults. Thus, for the sake of brevity, only the results of the first scenario, are between 200 kg and 400 kg. Turner and Antón interpret a high considered by us the most likely one, are reported here. Results of the sexual size dimorphism in Meganthereon cultridens, with individuals second scenario are available as supplementary material. varying from the size of a large jaguar to the size of a leopard, and Early Pleistocene European paleocommunities sustained extremely Arribas and Palmqvist (1998) estimated a body weight of 52.9 rich carnivore fauna. Carnivore species richness is similar in the four (46.1–58.1) kg for the Megantereon from Venta Micena. Considering analysed recent Regional Faunas (7–8 species) and remarkably lower how Megantereon killed their prey, it is unlikely that these than in the Early Pleistocene Regional Faunas (9 to 15 species) sabre-tooths were able to kill an adult P. verticornis eight times its (Fig. 3A). For prey species, Early Pleistocene faunas are intermediate own weight. We thus consider that Megantereon preferred prey in richness compared to recent Regional Faunas. Both African Regional body size was in the 90 to 360 kg range, although it also hunted juve- Faunas, E. Afr. and S. Afr., show the highest prey species richness. Inter- nile individuals of species with a mean adult body size between 360 estingly, the same pattern arises when local faunas are considered: the and 1,000 kg. Ungulates in the 45 to 90 kg body size would also be Early Pleistocene communities show an intermediate prey species rich- taken as secondary prey. ness combined with high or very high carnivore species richness The killing behaviour and prey preferences of Homotherium have (Fig. 3B). Interestingly, at the local scale, the NW A. recent faunas are been hotly debated. However, evidence accumulated during the last de- richer in carnivores, although they include a moderate number of cade from different approaches shed light on this controversial topic. non-carnivore species, possibly because they include several omnivo- Anatomical and morphofunctional analyses indicate that Homotherium rous species (Canis latrans, Ursus americanus, and Ursus arctos). killed large prey, the size of a horse or a buffalo, with a canine The high prey species richness observed in the two African Re- shear-bite to the throat of the victim; in this way, it avoided the risk gional Faunas is mainly due to the abundance of medium-sized and, of tooth breakage (Antón and Galobart, 1999; Antón et al., 2004). Its especially, small-sized ungulates weighing between 10 and 45 kg. postcranial skeleton was better adapted to long-distance travel than This abundance of small-sized primary consumers combined with that of pantherines, but their jumping abilities were smaller (Anton et the presence of several megaherbivores (>1,000 kg) in these Region- al., 2005). These features suggest an adaptation to open environments al Faunas gives them a highly distinctive size distribution (Fig. 4). The and a large home range. Accordingly, Turner and Antón (1998) remark other two recent Regional Faunas also exhibit characteristic prey size that Homotherium was less strong and less well equipped for ambush distributions. A low proportion of small-sized ungulates combined hunting than a lion. Antón et al. (Anton et al., 2005) infer group killing with a moderate presence of megaherbivores characterise the SE behaviour based on the clear adaptations of the head and neck to kill Asia Regional fauna, while a high proportion of medium-sized ungu- large prey as well as the relatively weak forelimbs, which made a single lates and the lack of megaherbivores (body size category I) are unique 106 J. Rodríguez et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 365–366 (2012) 99–114

Fig. 3. Total number of carnivores (Nc) and primary consumers (Np) in recent and fossil faunas. Only mammals weighing over 10 kg have been included. A. Regional Faunas. Black dots: fossil Regional faunas; white dots recent Regional faunas. Codes as in Table 2. B. Local Faunas. Recent localities are grouped according to region: S. Afr.: South Africa; E. Afr.: East Africa; SE.A.: Southeast Asia and NW.A.: North West America (see Table 2 and Fig. 2). Middle Villafranchian LFs: black dots; Late Villafranchian LFs: black triangles and Early Galerian LFs: white dots.

to the NW A. Fauna (Fig. 4). This pattern is a direct consequence of the Concerning the number of predators able to kill megafauna, the pattern late Pleistocene Megafaunal extinction, which extirpated 72% of the is similar to that observed in the SW and Central Mediterranean Faunas. North American mammal genera weighing more than 45 kg (Koch Competition inside the predatory guild, as measured by the and Barnosky, 2006). In contrast to recent Regional faunas, all Early MNMP index, also shows different patterns in the SE Mediterranean, Pleistocene Regional faunas are rich in large-sized ungulates and on the one hand, and in the SW and Central regions, on the other. megaherbivores and relatively poor in small-sized ungulates. The In the South East region, the MNMP was always similar to recent scarcity of ungulates weighing between 10 and 45 kg in the fossil values, with a slight decrease in the late Villafranchian. During the Regional Faunas might be partially due to a bias in the fossil record, middle Villafranchian, the MNMP values in the SW and Central Re- especially in the late Villafranchian faunas from the Central and gional faunas were similar to those observed in recent faunas. South East Regions and possibly also in the Galerian faunas. Neverthe- MNMP increased markedly in the late Villafranchian and decreased less, the combination of a high abundance of mammals weighing over in the Galerian to reach modern values (Fig. 5). The same pattern is 360 kg and a low presence of small-sized ungulates seems to consti- observed when data are analysed at a local scale, pooling LFs from tute a distinctive pattern of the Early Pleistocene Regional Faunas the entire Mediterranean region (Fig. 6). The different pattern from southern Europe considered as a whole. The abundance of pred- observed in the SE Mediterranean might be explained by the ators able to kill large and very large prey (>360 kg) in the Early abovementioned incompleteness of the late Villafranchian record in Pleistocene Faunas is coherent with their prey size distributions this area. (Fig. 4). A tendency towards increased body sizes of primary con- sumers is visible in the middle Villafranchian and Galerian Regional 4. Discussion Faunas (Fig. 5). In contrast, the number of predator species able to kill megafauna species increased in the late Villafranchian but decreased 4.1. Characteristics of Early Pleistocene food webs in the early Galerian, both in the SW and Central Mediterranean regions. The SE Mediterranean regional fauna shows a different pattern, with a Early Pleistocene food webs exhibit unique features not observed decrease in the number of predators able to kill megafauna during the in any recent food webs used for comparison. Some features were late Villafranchian coincident with an increase in the proportion of present in the Southern European mammalian faunas for a period megafauna species. This apparent contradiction may be due to the in- lasting 1.8 million years, while other characteristics show variations completeness of the record in this region and time. The late in time. The body size distribution of primary consumers has a dis- Villafranchian SE Mediterranean fauna is represented only by two LFs tinctive pattern of the Early Pleistocene faunas already highlighted (the Greek sites of Alikes and Libakos), and it includes the lower num- in previous studies (Rodríguez et al., 2004). Pleistocene faunas, at ber of species (Fig. 3A). In addition, the value of CIbda for the late both the regional and local scales, show a high relative abundance Villafranchian SE Mediterranean fauna is only 44.4, while the values of of megafauna species compared to recent faunas. The body size this index for the late Villafranchian NW Mediterranean (CIbda =100) composition of current mammalian faunas shows a high variation and Central Mediterranean (CIbda =93.3) regions indicate these two from one biogeographical region to another, with no relationship to Regional Faunas are complete or nearly complete. environmental factors (Nieto et al., 2005), but influenced by the late The prey size distribution and predator killing ability patterns ob- Pleistocene megafauna extinction . Three of the four regions selected served in the recent and fossil Regional Faunas are confirmed by for comparison are among the areas currently richer in large herbi- analysing local faunas (Fig. 6). The Early Pleistocene local faunas are vore species (Eastern and Southern Africa and Southeast Asia), but characterised by a high number of predators able to kill megafauna spe- the megafauna comprises a small proportion of the entire mammal cies (body weight >360 kg) and a large proportion of megaherbivores fauna in these areas. The abundance of large herbivores in the Early (Fig. 6). At the local fauna scale, the proportion of megaherbivores in Pleistocene faunas had deep effects on food web architecture and the communities seems to increase during the late Villafranchian and functioning, as prey body size strongly conditions the ability of a decrease in the early Galerian. However, the small number of LFs in- predator to kill prey (Levinton, 1982; Carbone et al., 1999). The cluded in this analysis requires caution in interpreting this result. evolution of a larger body size is recognised as a good strategy to J. Rodríguez et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 365–366 (2012) 99–114 107

Fig. 4. Predator–prey relationships in recent and fossil Regional Faunas. White bars represent the number of primary consumer species per body size interval, and black bars indicate the number of predators able to kill species in that size interval. A single predator may be able to prey in several body size categories. D=10–45 kg; E=45–90 kg; F=90–180 kg; G=180–360 kg; H=360–1000 kg; I>1000 kg.

avoid predation (Stanley, 1973; Yoshida, 2006), and it may explain but carnivore body size is limited by the balance between energy in- the increase in the number of megafauna species and the body size take and expenditure (Carbone et al., 2007). Consequently, such a of many lineages (Prado et al., 2004) throughout the Pleistocene “megapredator” would be energetically inefficient, and their (Fig. 5), as suggested in a previous study (Croitor and Brugal, 2010). populations prone to extinction if prey availability fluctuated. Early The number of predators able to kill megaherbivores (>360 kg) in- Pleistocene carnivores may have evolved social behaviour as a strate- creased in the late Villafranchian and eventually decreased in the gy to kill larger prey (Croitor and Brugal, 2010), which may certainly early Galerian to values similar to those found in the middle be the case for Homotherium, which would likely be the only predator Villafranchian and recent African faunas. Although megaherbivores able to effectively kill megaherbivores with a coordinated attack. were part of several carnivores' diets, there were likely no predators An apparent paradox is observed in the transition to the early with extremely large herbivores as their main prey. Extrapolating Galerian, when the percentage of megafauna increased but the num- the relationship between predator body mass and mean prey body ber of megafauna hunters decreased. Several factors may have mass observed in African savannahs (Radloff and Du Toit, 2004) indi- influenced this trend. Environmental change (Croitor and Brugal, cates that a carnivore with a mean prey body mass of 700 kg would 2010) may have played a role in the decrease of carnivore diversity have to weigh 400 kg on average. A carnivore specialising in mega- from the Late Villafranchian to the early Galerian. Competition inside fauna would have to be extremely large to be able to subdue and the carnivore guild, as measured by the NMP index, was extremely kill their prey (500 kg, if the mean prey body mass were 1,000 kg), high in the late Villafranchian (Fig. 5), which may explain the general 108 .Rdíuze l aaoegah,Pleciaooy aaoclg 365 Palaeoecology Palaeoclimatology, Palaeogeography, / al. et Rodríguez J. – 6 21)99 (2012) 366 – 114

Fig. 5. Changes in food web structures during the Early Pleistocene at the Regional Fauna scale (South Western, Central and South East Mediterranean). The total number of predators (TNP) is computed as the number of carnivore species able to kill megaherbivores (>360 kg) or a small- or medium-sized primary consumer (b360 kg). The whiskers represent the maximum and minimum numbers of predators for a prey, while the lines connect the means. The percentage of megafauna (% MF) is computed as the proportion of primary consumers weighing over 360 kg, and the number of predators able to kill them is indicated as the MFP (Megafauna Predators). The number of main predators (NMP) represents the number of predators that share a prey that they all prefer. The line connects the mean number of main predators (MNMP) values, which is an index of competition inside the predatory guild. The whiskers represent the maximum and minimum NMP values for a primary consumer in that fauna. The values of these indexes in the four recent Regional Faunas are indicated for reference. J. Rodríguez et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 365–366 (2012) 99–114 109

Fig. 6. Changes in food web structures during the Early Pleistocene at the Local Fauna scale. The percentage of megafauna (% MF) is computed as the proportion of primary consumers weighing over 360 kg, and the number of predators able to kill them is indicated as the MFP (Megafauna Predators). The mean number of main predators (MNMP) represents the average number of predators sharing a prey that they all prefer. The mean (square), maximum and minimum (whiskers) values of these indexes observed in recent local faunas, grouped by region, are shown on the upper part of the graph for reference.

decrease in carnivore richness observed in the early Galerian. As and Lézignan Le-Cébe (Crochetetal.,2009). Survival opportunities for discussed above, megafauna predators relied mainly on smaller those hominin populations during the late Villafranchian seem to prey, and energetic constraints prevented them from evolving to larg- have been low if they entered Europe as new members of an already er sizes and becoming specialised megafauna predators. Competition overcrowded predatory guild. Given the versatility of hominins, a mark- inside the large carnivore guild thus occurred mainly for medium- edly omnivorous behaviour not dependent on meat resources seems sized prey, the carnivores' main resource, not for megafauna prey. more likely for these earlier settlers, as suggested by Croitor and With the change at the end of the Villafranchian, intra-guild competi- Brugal (2010), following the model proposed by Ungar et al. (2006) tion, as measured by the mean number of main predators, fell to the for African early hominins. Conversely, data on recent hunter–gatherer value observed in recent food webs. diets worldwide, taken with subsistence models based on macronutri- ent plant and animal food content, suggest that meat is a key resource 4.2. The role of Homo in Early Pleistocene food webs for any human hunter–gatherer (Leonard and Robertson, 1994; Cordain et al., 2000; Jenike, 2001). Furthermore, the meat proportion Homo dispersed into Southern Europe at the end of the late in the recent hunter–gatherer diets increases at higher latitudes, from Villafranchian or the beginning of the Galerian (Bosinski, 2006; approximately 50% in the tropics to approximately 70% in the band be- Carbonell et al., 2010). As our results show, this arrival coincided with tween parallels 41 and 50, likely because of different macronutrient remarkable changes in carnivore guild structure and food web architec- availability from plant foods (Cordain et al., 2000). Unfortunately, ture. Several authors suggest a relationship between the changes in the there is no archaeological evidence of the subsistence strategies of carnivore guild at the end of the Villafranchian and the arrival of Homo Homo during the late Villafranchian in Southern Europe. The scarcity (Turner, 1992a; Martínez-Navarro and Palmiqvist, 1996; Arribas and of archaeological sites from the late Villafranchian suggests that Palmqvist, 1999; Palombo, 2010). The high intraguild competition in hominins, if present, played a marginal role in the food webs during the late Villafranchian, suggested by the high MNMP values, supports this period. Some of the oldest evidence about these early settlers' be- the hypothesis that the European fauna composition precluded the ex- haviour comes from the TE9 level of the Sima del Elefante Site, at pansion of Homo during this period. However, this interpretation is Atapuerca, dated to approximately 1.2 Ma. The bone and lithic assem- challenged by the artefacts found in the Late Villafranchian localities blage from TE9 suggest highly opportunistic behaviour, consuming a of Kozarnika (Sirakov et al., 2010), Pirro Nord (Azzarello et al., 2007), wide variety of animal foods, including medium-sized mammals as 110 J. Rodríguez et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 365–366 (2012) 99–114 well as rabbits, birds and tortoises (Blasco et al., 2011; Rodríguez et al., of the fossil record. Several authors have previously stressed the ade- 2011). quate degree of completeness of the Pleistocene large mammal record With the faunal turnover at the end of the Villafranchian, competi- in Europe as a whole (Croitor and Brugal, 2010; Palombo et al., 2010). tion inside the predatory guild decreased and evidence of human activ- Considering the data analysed here, only faunas from the South East ities increased. Considering the food web structure, it is tempting to Mediterranean region seem to have been affected by significant biases, think that an empty niche, if one existed at all, was for a specialised especially in late Villafranchian fauna, which is only represented by two megafauna predator. The social behaviour and high planning capacities sites (Alikes and Libakos). Accounting for this data scarcity, it is not pos- of hominins make them apriorigood candidates to fill that empty sible to determine whether the different patterns detected in the South niche. Archaeological evidence of hominin prey preferences at the Eastern Mediterranean are due to a different evolutionary trajectory of end of the Early Pleistocene are scarce and do not fit this expectation. this regional fauna or the incompleteness of the fossil record. In the ab- Zooarchaeological analyses of the Atapuerca TD6-2 assemblage, accu- sence of additional information, it is advisable to take a conservative po- mulated by Homo antecessor and dated to approximately 0.8 M.a. sition and assume that the different pattern detected for the South (Falguères et al., 1999; Moreno, 2011), show a body size spectrum Eastern Mediterranean Fauna may be an artefact due to biases and lim- dominated by medium- and small-sized herbivores (Saladié et al., itations of the fossil record. 2011). Although hunting activities cannot be definitively concluded, In the Local Fauna scale, accumulation and preservation biases are primary access to carcasses has been demonstrated for most of the potentially even more disrupting than in the regional fauna scale. sample. Although the TD6-2 assemblage may under-represent the im- Most LFs analysed here show evident signs of incompleteness. To portance of very large mammals (>1,000 kg) in the human diet, as minimise this effect, we selected only those LFs with a high number large mammals' remains are usually not transported, these data of species in the fourth quartile for our analyses. Interestingly, the suggest that H. antecessor was not a specialised megafauna predator. patterns detected at the regional scale are confirmed for the LF scale. Conversely, a preferred prey size in the 90–360 kg interval seems Taking apart the South Eastern Mediterranean region, the robust- more feasible for the Early Pleistocene hunter–gatherers. Including ness of the patterns detected throughout the Early Pleistocene should H. antecessor as an additional large predator in the early Galerian be stressed. The high carnivore richness and high MNMP in the late regional fauna undoubtedly increases the intra-guild competition Villafranchian is exactly the opposite of what can be expected from a level estimated here, but not beyond the reference values from recent bias in the fossil record. Carnivores usually occur at population food webs. densities much lower than primary consumers of a similar size (Robinson and Redford, 1986; Damuth, 1993); the fossilisation proba- 4.3. Ecological implications of food web structures bility is thus smaller for a carnivore than a primary consumer. Space averaging might also be claimed as an explanation for the high The peculiar body size distribution of primary consumers, com- carnivore richness of the Pleistocene Faunas at the regional scale. The bined with the structure of the predatory guild in Early Pleistocene three Southern European peninsulas are today topographically and en- communities, not only determined the predator–prey relationships vironmentally heterogeneous areas. If environmental heterogeneity but also conditioned food web dynamics and ecosystem functioning. was also high in the Mediterranean Area during the Early Pleistocene Studies on food web dynamics in African savannas suggest that the regional faunas would sample different biomes with different top-down mechanisms regulate small- and medium-sized herbivore carnivore guild compositions. However, the recent Regional faunas populations, while bottom-up controls do so for large herbivores used for comparison belong to areas of similar size, which are also (Sinclair, 2003; Fritz et al., 2011). The increased proportion of environmentally heterogeneous. Thus, space averaging cannot explain megaherbivores in the late Villafranchian and early Galerian means the differences in richness observed between fossil and recent regional that bottom-up controls became the main regulatory mechanisms in faunas. Moreover, most carnivore species co-occur at the local scale late Early Pleistocene communities, an idea mentioned by Raia et al. and the LFs show the same extremely rich carnivore guild pattern. (2007) for the Italian peninsula. Time averaging should also be considered as a possible explanation A strong relationship exists in recent communities between to the high carnivore richness observed in the Pleistocene faunas. If time population density of carnivores and prey biomass density averaging exists at the scale of fossil Regional faunas it should be low. (Carbone and Gittleman, 2002); prey biomass density is strongly Definition of the Regional faunas is based on widely recognised large related to ecosystem net primary productivity (McNaughton et al., mammal biochronological units of different length. Thus, a significant 1989) and species richness (Fritz and Duncan, 1994). The species amount of time averaging would inflate the species richness of the lon- richness of primary consumers was low in the European Early Pleis- gest period (the middle Villafranchian). However, by definition, tocene compared to recent African communities (Fig. 3B), and it is biochronological units should be periods of faunal stasis, without unlikely that the net primary productivities were higher in south- significant turnovers inside the unit (Palombo and Sardella, 2007). ern Europe during the Early Pleistocene than in East or South Africa Thus, species composition of the Regional fauna do not changes during at present. We may thus assume that prey biomass density was a biochronological unit and we can discard time averaging as a signifi- much lower in the Early Pleistocene that in recent African commu- cant influence on our results at the scale of Regional faunas. The situa- nities. Low prey biomass density makes the high predator/prey ra- tion is more complex at the scale of local faunas. We excluded from tios observed in the Pleistocene food webs, especially during the our database all fossil assemblages with evidence of time-averaging, middle Villafranchian, even more striking. The total carnivore bio- and those assemblages that were pooled faunal lists from several mass was likely much lower in the late Villafranchian in southern stratigraphic levels. However, we lack detailed sedimentary and Europe than in current African communities, but predator richness taphonomical information for all the LFs included in the analyses. was markedly higher. A credible explanation to this apparent para- Thus, with the evidence at hand, it is not possible to assert that none dox, as suggested elsewhere (Rodríguez-Gómez et al., in press)is of the LFs analysed is time-averaged. All the above notwithstanding, that carnivores occurred in European communities with low popu- time-averaging can be discarded as the main cause of the high lation densities. carnivore richness and intraguild competence detected in the Early Pleistocene local faunas based on two well studied sites: Venta Micena 4.4. Possible biases and feasibility of the results (late Villafranchian) and Fonelas (middle Villafranchian). Fonelas P1 is interpreted as a hyaena den in the distal part of a fluvial drainage sys- We have analysed our data at two different spatial scales: Local and tem, near its connection to a shallow lake, where bones were accumu- Regional Faunas. Analyses on both scales depend on the completeness lated during a very short period(Viseras et al., 2006; Arribas et al., J. Rodríguez et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 365–366 (2012) 99–114 111

2009; Pla-Pueyo et al., 2011). Thus, the Fonelas assemblage may be Role of funding source considered representative of a living community, with extremely high carnivore species richness (Fig. 3b), a high number of megafauna The Funding source had no involvement neither in study design, predators and very high intra-guild competition (Fig. 6), in comparison nor in the collection, analysis and interpretation of data. with recent local faunas. Venta Micena was also a hyaena den in the margins of a lake (Arribas and Palmqvist, 1998; Palmqvist and Arribas, Appendix A. Supplementary data 2001). This fossil assemblage is also unaffected by time-averaging pro- cesses and may be taken as representative of a living community Supplementary data to this article can be found online at http:// (Palmqvist et al., 1996; Palmqvist et al., 2008). 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