Resource availability and competition intensity in the carnivore guild of the Early Pleistocene site of Venta Micena (Orce, Baza Basin, SE Spain)

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Resource availability and competition intensity in the carnivore guild of the Early Pleistocene site of Venta Micena (Orce, Baza Basin, SE Spain)

Guillermo Rodríguez-G omez

^a^,^b

, Paul Palmqvist

^b^,^*

, Sergio Ros-Montoya

^b

, M. Patrocinio Espigares

^b

, Bienvenido Martínez-Navarro

^c^,^d^,^e

aCentro Nacional de Investigacion Sobre la Evolucion Humana (CENIEH), Paseo Sierra de Atapuerca 3, 09002 Burgos, Spain

bDepartamento de Ecología y Geología, Universidad de Malaga, Campus de Teatinos, 29071 Malaga, Spain

cIPHES, Institut Catala de Paleoecologia Humana i Evolucio Social, C/ Marcel.lí Domingo S/n, Campus Sescelades, Ediﬁci W3, 43007 Tarragona, Spain

dArea de Prehistoria, Universitat Rovira i Virgili (URV), Avda. Catalunya 35, 43002 Tarragona, Spain

eICREA, Pg. Lluís Companys 23, 08010 Barcelona, Spain

a r t i c l e i n f o

Article history:

Received 17 October 2016 Received in revised form 1 March 2017

Accepted 1 April 2017

Keywords:

Leslie matrices Paleoecology Large mammals Early pleistocene Orce

a b s t r a c t

With an age of ~1.6e1.5 Ma, the Early Pleistocene site of Venta Micena (Orce, Baza Basin, SE Spain) has provided the large mammals assemblage of Late Villafranchian age with higher preservational completeness in Western Europe and offers a unique opportunity to analyze the food webs of the mammalian paleocommunity before theﬁrst human arrival in this continent. Taphonomic analysis of the fossil assemblage has shown evidence of carnivore involvement, particularly hyenas, in the bone accu- mulating process. In this study we use a mathematical approach based on Leslie matrices to quantify the biomass of ungulates available to the members of the carnivore guild as well as the pattern of resource partitioning and competition intensity among them. The results obtained show that although the biomass of primary consumers available to the secondary consumers was lower than the value expected under optimal conditions, more than half the individuals and biomass of carnivores expected would be reached, which allowed a viable ecosystem in Venta Micena. In fact, the biomass available for the members of the carnivore guild is 25e30% greater than the estimates obtained for two nearby sites, Barranco Leon-D and Fuente Nueva-3, which are somewhat younger (~1.4 Ma) and preserve the oldest evidence on human presence in this region. Given that the competition intensity estimated in the carnivore guild of Venta Micena was lower than in the latter sites, this suggests that the timing of theﬁrst human dispersal in Western Europe was probably not a matter of ecological opportunity.

1. Introduction

The Early Pleistocene (Late Villafranchian) site of Venta Micena (VM) (Martínez-Navarro et al., 2015) is located near the village of Orce in the eastern sector of the Baza Basin (Guadix-Baza Depres- sion, SE Spain;Fig. 1). This sedimentary basin was endorheic (i.e., characterized by interior drainage) from the end of the Miocene epoch to late Pleistocene times, which resulted in wide swampy and lacustrine systems subject to hydrothermal feeding (García- Aguilar and Palmqvist, 2011; García-Aguilar et al., 2014).

Compared to present day conditions (mean annual temperature

and rainfall: 12.0C, 370 mm), the presence of the lakes prompted a warmer, wetter and more stable (i.e., less continental) climate in the region during the Late Villafranchian (16.5C, 750 mm;Blain et al., 2011). In addition, the moderately saline character of the lake waters resulted in a high organic productivity, which favored the growth of aquatic macrophytes (García-Aguilar et al., 2015).

This allowed the development of a rich and well-diversiﬁed mammalian paleocommunity in the surroundings of the lacustrine environments, which facilitated an exceptional record of the Plio-Quaternary species that inhabited the basin (Moya-Sola et al., 1987; Martínez-Navarro, 1991; Palmqvist et al., 1996; Arribas and Palmqvist, 1999; Espigares, 2010).

The excavated surface of the VM stratum (quarry III, ~380 m²; quarry IV, ~27 m²) outcrops along>2.5 km in the basin and has

*Corresponding author.

E-mail address:[email protected](P. Palmqvist).

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provided a large mammals assemblage with high preservational completeness, which includes ~12,000 identiﬁable skeletal remains from 395 individuals belonging to 21 taxa of large (>10 kg) mammals, and ~10,000 bone fragments not determined anatomically such as diaphyseal shafts and cranial fragments (Espigares, 2010).

Complete elements and bone fragments range in size from isolated teeth and phalanges of small carnivores to elephant mandibles.

Herbivore species dominate the assemblage in both number of identiﬁable specimens (NISP) and estimates of minimal number of individuals (MNI). The age estimated for individuals preserved in the assemblage includes juveniles with deciduous teeth and adults with fully erupted permanent dentition. More common herbivores such as horse, bison and megacerine deer are all represented by

>45% of juveniles. Among carnivores, only adult individuals are recovered with the exception of hyena and bear (see details in Espigares, 2010; Medin et al., 2017).

Two nearby sites that are slightly younger (~1.4 Ma) than VM, Barranco Leon-D (BL-D) and Fuente Nueva-3 (FN-3), provide un- equivocal evidence of human presence in the Baza Basin during the Late Villafranchian. They preserve: (1)>3000 Oldowan (i.e., Mode 1) tools made of allochtonousﬂint and limestone, includingﬂakes,

cores, and modified cobbles, as well as two sets of refitted pieces in BL-D and abundant unmodified limestone manuports in FN-3; (2) cut marks on large mammal bones at both sites; and (3) a human deciduous tooth in BL-D (Espigares et al., 2013; Toro-Moyano et al., 2013). In the case of VM, a cranial fragment from VM attributed to Homo sp. (specimen VM-0) was subject to intense debate and controversy during the mid nineties, but now it is not accepted as human (for review and references, see Palmqvist et al., 2005).

Therefore, all evidence currently available indicates that BL-D and FN-3 are the oldest sites in Western Europe with human presence.

Competition intensity between humans and other species of secondary consumers recorded at BL-D and FN-3 has been estimated recently with a mathematical model that allows evaluating resource partitioning among the members of the carnivore guild (Rodríguez-Gomez et al., 2016a). For this reason, the main objective of this study is to test with the model if: (1) the absence of hominins from the assemblage preserved at VM resulted from increased competition among carnivores compared to BL-D/FN-3; or (2) this absence merely indicates that the human population dispersing in Western Europe from the East had not reached the Baza Basin by the times the VM assemblage was being formed.

Fig. 1.Geographic location of Venta Micena (VM) in the eastern sector of the Baza Basin (SE Spain). The photographs at the bottom show the location of the main two excavation quarries of this site, VM-III and VM-IV (left), and the density of skeletal elements unearthed from one square meter of VM-IV (right).

omez et al. / Quaternary Science Reviews 164 (2017) 154e167 155

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2. Material and methods 2.1. The faunal assemblage of VM

Our analysis was restricted to those mammal species weighing

>10 kg, as these include the ungulates that contributed the main sources of meat and fat for the carnivore guild of the VM paleocommunity (Binford, 1981, 1985; Gaudzinski and Roebroeks, 2000;

Marean, 1989; Owen-Smith and Mills, 2008; Roebroeks, 2001;

Speth, 2010) and, eventually, also for the hunter-gatherer human population that inhabited the Baza Basin during Early Pleistocene times (which evidence has not been detected by the moment at the VM site, as noted before).

Thirteen species of primary consumers with body masses ranging between 25 and 6000 kg have been recorded in the faunal assemblage (Table 1): one proboscidean (elephant Mammuthus meridionalis), two perissodactyls (horseEquus altidens and rhino Stephanorhinusaff.hundsheimensis) and ten artiodactyls, including one hippo (Hippopotamus antiquus), six bovids (bison Bison sp., water buffaloHemibosaff.gracilis,muskoxPraeovibossp., ovibovine caprine Soergelia minor, goat Hemitragus cf. albus and Bovidae indet., chamois-sized) and three cervids (megacerine deer Prae- megaceroscf.verticornis,fallow deerMetacervocerus rhenanusand Cervidae indet., roe deer-sized).

Eight species of secondary consumers, which distribute over a size range of 12e300 kg, were also identiﬁed (Table 1): one ursid (Ursus etruscus), two canids (jackalCanis mosbachensisand painted dogLycaon lycaonoides), four felids (lynxLynxcf.pardinus,jaguar Pantheracf.gombaszoegensis, and saber-toothsHomotherium lat- idensandMegantereon whitei) and one hyaenid (Pachycrocuta brevirostris) (Pons-Moya, 1987; Martínez-Navarro, 1991; Martínez- Navarro and Palmqvist, 1995; Martínez-Navarro and Rook, 2003;

Boscaini et al., 2015). Of these species, the bear shows craniodental morphology indicative of an omnivorous behavior (Medin et al., 2017) and its diet was assumed to include only 10% meat based on data from modern and ancient populations of European brown bears (Ursus arctos) (Bocherens et al., 2004; Parde and Camarra, 1992), with a substantial contribution of ﬁsh as suggested by isotopic biogeochemistry (Palmqvist et al., 2008a,

2008b). Similarly, C. mosbachensis has a craniodental anatomy that suggests a mesocarnivore diet (Palmqvist et al., 1999, 2002), which is confirmed by itsd¹⁵N values of bone collagen, lower than in other carnivores (Palmqvist et al., 2003, 2008a, 2008b; however, see also Flower and Schreve, 2014). Given that extant African jackals of similar body size and craniodental shape occasionally prey upon ungulate calves and have secondary access to carrion (Palmqvist et al., 1996),C. mosbachensiswas included in the model as a scavenger with access to all ungulate size categories. Among the hypercarnivores (i.e., those species whose diet consists exclu- sively offlesh), the three large felids (H. latidens, M. whiteiand Panthera cf. gombaszoegensis) and the pack-hunting canid (L. lycaonoides) were interpreted as obligate predators, a behavior unequivocally deduced for them from ecomorphology and biogeochemistry (Palmqvist et al., 1999, 2002, 2003, 2007, 2008a, 2008b). In contrast, the giant, short-faced hyena P. brevirostris was considered as a strict scavenger, as deduced from taphonomic analysis in VM (Arribas and Palmqvist, 1998; Palmqvist and Arribas, 2001) as well as from skull biomechanics and ecomorphology of the postcranial skeleton of this bone-cracking hyena, which showed massive limbs with shortened distal bones and a heavy, powerfully built mandible with robust, well-developed premolars (Turner and Anton, 1996; Palmqvist et al., 1996, 2011). The lynx, a small to medium-sized felid, was also considered in the model as a predator because modern lynxes prey on small ungulates. Finally, a number of small-sized carnivores (<10 kg) preserved in the site (e.g.,Vulpescf.praeglacialisandMeles meles) were excluded from the analysis because they presumably had a hypocarnivorous diet, with a consumption offlesh basically derived from small verte- brates (see review inRodríguez-Gomez et al., 2016b).

The large mammals assemblage from VM shows close afﬁnities to the one preserved at the Caucasian site of Dmanisi, a locality dated at 1.85e1.77 Ma (Lordkipanidze et al., 2007, 2013), although the absence of some species (e.g., girafﬁdPalaeotragussp.) and the presence of others (e.g.,L. lycaonoides) indicates that VM is somewhat younger (~1.6e1.5 Ma) than Dmanisi (Martínez-Navarro and Rook, 2003; Martínez-Navarro, 2004, 2010; Rook and Martínez- Navarro, 2010; Martínez-Navarro et al., 2015).

The longitudinal axes of major limb bones in the assemblage

Table 1

Faunal list and body masses estimated byPalmqvist et al. (1996)using allometric equations (see chapters inDamuth and MacFadden, 1990) for the large mammals species identiﬁed in the fossil assemblage of Venta Micena (VM).

Trophic level, family/subfamily Species Body mass (kg)

Primary consumers

Elephantidae Mammuthus meridionalis 6000

Rhinocerotidae Stephanorhinusaff.hundsheimensis 1000

Equidae Equus altidens 350

Hippopotamidae Hippopotamus antiquus 3200

Bovinae Bisonsp. 450

Bovinae Hemibosaff.gracilis 300

Caprinae Bovidae indet., small size 25

Caprinae Hemitragus albus 75

Caprinae Praeovibossp. 315

Caprinae Soergelia minor 225

Cervidae Cervidae indet., small size 25

Cervidae Metacervocerus rhenanus 95

Cervidae Praemegaceroscf.verticornis 385

Secondary consumers

Ursidae Ursus etruscus 300

Canidae Canis mosbachensis 12

Canidae Lycaon lycaonoides 30

Felinae Lynxcf. pardinus 18

Machairodontinae Homotherium latidens 200

Machairodontinae Megantereon whitei 100

Pantherinae Pantheracf.gombaszoegensis 105

Hyaenidae Pachycrocuta brevirostris 110

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unearthed from VM quarry III show no preferred orientation, which suggests that the currents did not align them. Moreover, the ratio of isolated teeth to vertebrae (0.94:1) is close to the value expected in the absence of hydrodynamic sorting (1:1) and the frequencies of bones grouped according to their potential for dispersal by water (i.e., Voorhies groups) are similar to those in the mammalian skeleton, which rules outﬂuvial transport (Arribas and Palmqvist, 1998; Espigares, 2010). Analysis of weathering stages indicates exposure to the elements for a very short time, less than one year in most cases (~90% of the bones show weathering stage 0;Palmqvist et al., 1996), and the scarcity of root-marks helps to discard the possibility of delayed burial in a moist environment where the bones would be protected from weathering by the vegetation (Palmqvist and Arribas, 2001).

Taphonomic analyses of the assemblage have shown that the hyenaP. brevirostrisaccumulated the skeletal remains preserved at VM quarry III and that most losses of paleobiological information were a consequence of the selective destruction of bones by the hyenas during the time elapsed on the surface until their permanent burial (Arribas and Palmqvist, 1998; Espigares, 2010;

Palmqvist et al., 2011). Speciﬁcally, mortality patterns deduced for ungulate species from tooth wearing show U-shaped attritional proﬁles. Similarly, juvenile/adult proportions in these species correlate with their estimated masses, which indicates a strong selection of prey by predators (Palmqvist et al., 1996). This has been interpreted as evidencing that most skeletal remains were scavenged by the hyenas from carcasses of animals previously hunted by hypercarnivores such asH. latidens, M. whiteiandL. lycaonoides.

Patterns of skeletal representation for ungulate taxa show that the hyenas selectively transported herbivore carcasses and body parts to the vicinity of their maternity dens as a function of the mass of the ungulates scavenged (Palmqvist and Arribas, 2001). The frac- turing of major limb bones in the denning area was also highly selective, because the frequencies of major limb bones preserved complete correlates well with their estimated marrow contents and mineral densities (Palmqvist et al., 2011). As a result, important differences of preservational completeness are recorded among the skeletal elements of each ungulate species as well as among taxa (Arribas and Palmqvist, 1998; Espigares, 2010).

However, it should be noted that the interpretation depicted above is not generalizable to the whole fertile stratum of VM, because a new excavation area (VM quarry IV) located some hun- dred meters distant from VM quarry III shows signiﬁcant differences in the abundance of cranial, axial and appendicular elements, as well as quite distinct taphonomic attributes. Speciﬁcally, major limb bones are more abundantly preserved complete in quarry IV than in quarry III, where they are systematically fractured by the hyenas for consuming their marrow (Palmqvist et al., 2011), and the elements of the axial skeleton (vertebrae and ribs) and pelves are also more abundant, being often preserved in anatomical connec- tion, which suggests a different bone-collecting agency for this assemblage (García-Aguilar et al., 2015).

Paleoautecological inferences for the large mammal species have been obtained from combined biogeochemical and ecomor- phological approaches (Palmqvist et al., 1999, 2002, 2003, 2008a, 2008b). Speciﬁcally, analysis of the proportions of stable isotopes (d¹³^C,d¹⁵^N,d¹⁸O) and trace elements (Sr, Zn) from bone collagen and tooth enamel allowed estimation of the dietary niches and habitat preferences of ungulate and carnivore species, providing clues on predator-prey relationships within this paleocommunity.

For example,H. latidensandM. whiteishow quite distinct isotopic signatures, which indicates that both saber-tooths preyed on different ungulate prey. This is also suggested by the anatomy of their postcranial skeletons, which suggests that Homotherium pursued grazing ruminants and juveniles of megaherbivores in

open plains, while Megantereon ambushed browsing and mix- feeding ungulates in bushland and forest (Turner and Anton, 1998; Arribas and Palmqvist, 1999). Of interest to this study, the hyena P. brevirostris shows isotopic values that match those expected from isotopic enrichment from prey to predator for a carnivore consuming all ungulate species preserved in the faunal assemblage. This suggests that the hyenas specialized in scavenging the kills of these hypercarnivores in the proportions in which they were available (Palmqvist et al., 2008b), which is in agreement with the taphonomic evidence.

2.2. Methodology applied

Resource partitioning among the members of the carnivore guild of VM was analyzed using a mathematical model (Fig. 2) that takes into account: (1) the abundance of ungulate resources in the paleocommunity, which depends on the population density and demographic structure of the species of primary consumers; (2) the ability of each predator to obtain and process these resources, which results from differences in hunting success (e.g., between ambushers in forest and coursers in open plains) and in carcass processing (e.g., between ﬂesh eating and bone-cracking carnivores); and (3) the level of competition intensity among the secondary consumers (e.g., competitive displacement, interference predation and kleptoparasitism). The model determines: (1) the age structure that would make stable the population of each primary consumer; (2) the distribution of individuals among body mass categories; and (3) the average biomass that could be extracted in the long term from this population. This provides the values of total available biomass (TAB) of primary consumers, which are derived for maximum and minimum mortality rates of subadults (TAB-m and TAB-M, respectively), and the total demanded biomass (TDB) required by the secondary consumers in ideal conditions (Fig. 2). Later, the distribution of ungulate resources among the secondary consumers is modeled and sustainable densities for each carnivore species are estimated. For an in-depth description of this model, see Rodríguez-Gomez et al. (2013, 2014a, 2016a, 2016b).

The model assumes that variations in population size and age structure tend to remain stationary. Age profiles are obtained using Leslie matrices (Leslie, 1945, 1948), which allows to model population dynamics under conditions of stability. Species-specific estimates of life history traits for the large mammals species (e.g., adult and neonate body masses, litter size, breeding interval, age at reproductive maturity, growth rate and potential lifespan) are used as input data. This provides population and mortality profiles for each primary consumer, from which estimates of average sustainable biomass outputs by age classes are derived (Fig. 2). However, given that the model solutions do not depend on population size, the population density of each ungulate species is estimated with the equation of Damuth (1981) for European mixed temperate forest ecosystems using the body mass values that appear in Table 1. Damuth's equation was used instead ofSilva and Downing's equation (1995)because a chi-squared test showed that the estimates derived from the former were in greater agreement with the density values of extant primary consumers reported in the Pan- Theria database (Jones et al., 2009). It could be argued that the MNIs and/or NISPs of the ungulate species in the assemblage would represent a more direct approach to estimating their population densities. However, it is worth noting that taphonomic analyses (Palmqvist and Arribas, 2001; Palmqvist et al., 2011) have shown that the frequencies of the ungulate species recorded in the fossil assemblage are highly biased compared to their original abun- dances in the paleocommunity (see discussion inRodríguez-Gomez et al., 2014b).

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Each ungulate carcass was assigned to one of six size classes (Table 2) and estimates of annual biomass available for carnivores from each ungulate population were computed taking into account, for each age class, the mortality rate and the average mass of those individuals from this age class. This provided estimates of sustainable total biomass outputs (TBO) for each primary consumer.

Given that TBO includes non-edible tissues (e.g., horns, bones and hide), a size-specific“wastage factor”(modified fromViljoen,1993) was used to subtract them and obtain the total available biomass (TAB), which was subsequently distributed among the six size classes. It should be noted, however, that although the model considers constant mortality rates during the subadult and adult phases, this assumption is not correct in real populations of ungulates. Assuming a constant mortality rate during adulthood does not affect the estimates of biomass output, since the same average body mass is assigned all individuals in the adult age classes. In the case of subadults, the higher mortality typically occurs during the first year of life and decreases as the calf grows (Gaillard et al., 2000), which leads to a slight (5e10%) overestimation of the biomass output (seeRodríguez-Gomez et al., 2013).

Values of total demanded biomass (TDB) for each carnivore species are derived from the equation ofFarlow (1976). Following

Rodríguez-Gomez et al. (2016b), the contribution of ungulateﬂesh to the diet of the VM carnivores was estimated as 10% for U. etruscus,20% forC. mosbachensis,10% forLynxcf.pardinus,100%

forL. lycaonoides, H. latidens, M. whiteiand Pantheracf.gombaszoegensis,and 98% forP. brevirostris.Population densities for each carnivore species are derived from the equation ofDamuth (1993) for Africanﬂesh-eaters in open environments. As in the case of ungulates, the equation ofDamuth (1993)is used instead of the one derived bySilva and Downing (1995)because the former provides estimates for extant carnivores that are in better agreement with data available in PanTheria (Jones et al., 2009). It is worth noting here that the sustainable population densities obtained with the model for the Pleistocene carnivores agree well with the values observed in nature for their living relatives (see discussion in Rodríguez-Gomez et al., 2013).

The distribution of the total demanded biomass of each predator over the ungulate size categories (Table 2) was based on: (1) the prey size preferences of its living analogues (Palmqvist et al., 1996;

Rodríguez et al., 2012; Treves and Palmqvist, 2007); and (2) the inferences on predator-prey interactions obtained for VM from isotopic data (Palmqvist et al., 2008a, 2008b). In this way, the percentage of predation of a carnivore on an ungulate size category Fig. 2. Flowchart diagram showing the components of the model used to evaluate trophic resource availability of carnivores and intraguild competition in Venta Micena (modiﬁed fromRodríguez-Gomez et al., 2014a).

Table 2

Carnivore guild of Venta Micena, with indication of the body masses estimated for the species (BM, in kg; values taken fromTable 1) and their nutritional requirements (NR, kcal/km²per year). The NR values of each secondary consumer were corrected according to their kind of diet with a correction factor (CF) that multiplies the total species requirements. CFﬂuctuates between 0.10 and 0.20 (omnivores) and 1.00 (ﬂesh-eating hypercarnivores that don't consume bone marrow). For each secondary consumer, the last six columns represent the preferences of size categories of primary consumers (see text) expressed in percentages (a null percentage indicates that an ungulate body class category is not consumed by a secondary consumer).

Species BM NR CF Class-1

(10e45 kg)

Class-2 (45e90 kg)

Class-3 (90e180 kg)

Class-4 (180e360 kg)

Class-5 (360e1000 kg)

Class-6 (>1000 kg)

Canis mosbachensis 12 40,062 0.20 16.67 16.67 16.67 16.67 16.67 16.67

Lycaon lycaonoides 30 211,024 1.00 13.00 37.00 25.00 25.00 0.00 0.00

Lynxcf.pardinus 18 20,498 0.10 75.00 25.00 0.00 0.00 0.00 0.00

Homotherium latidens 200 235,060 1.00 0.00 11.00 21.00 26.00 31.00 11.00

Megantereon whitei 100 225,976 1.00 6.00 19.00 25.00 31.00 19.00 0.00

Pantheracf. gombaszoegensis 105 226,604 1.00 11,11 11,11 33,33 22,22 22,22 0,00

Pachycrocuta brevirostris 110 222,660 0.98 16.67 16.67 16.67 16.67 16.67 16.67

Ursus etruscus 300 24,054 0.10 16.67 16.67 16.67 16.67 16.67 16.67

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represents the contribution of this size category to the predator's diet, although theﬁnal contribution of a prey category to the diet of a given predator is an output of the model (as it results from prey availability and competition with other carnivores). Rodríguez- Gomez et al. (2013) provide a detailed description of resource distribution computation.

Finally, three indexes were used for measuring in the secondary consumers the amount of requirements unsatisﬁed both at the species level and at the guild level (Fig. 2): (1) the species competition index (SCI), which compares the densities expected and estimated for each carnivore species (thus measuring the degree to which they fulﬁll their dietary requirements in a given environment); (2) the global competition index (GCI), which measures competition intensity at the level of the whole carnivore guild; and (3) the global competition index biomass (GCIB), which estimates the degree to which the members of the guild of secondary consumers reach their optimal biomass. These indexes provide information on the degree of competition intensity in the ecosystem compared to an ideal condition in which all species would reach optimal densities and/or levels of population biomass. The closer the value of an index is to 1, the higher is the competition among the secondary consumers. In contrast, index values close to 0 indicate a low degree of competition for dietary resources (for details on the mathematical calculation of these indexes, seeRodríguez- Gomez et al., 2016a, 2016b).

3. Results

3.1. Total available biomass

The model estimates the total available biomass (TAB) produced by the primary consumers of VM. The minimum value of TAB (TAB- m), which corresponds to the maximum rate of subadult mortality, is 584,030 kcal/km²per year. In contrast, the maximum value of TAB (TAB-M), which corresponds to the minimum rate of subadult mortality, is 779,118 kcal/km² per year. Therefore, TAB-m is 25%

lower than TAB-M. Both estimates show that the biomass of primary consumers available for the secondary consumers was lower than the value expected under optimal conditions (i.e., those in which the requirements of all carnivore populations with maximum densities are satisﬁed), which is represented by the total demanded biomass (TDB), 1,205,940 kcal/km²per year. A comparison of the TDB, based on the proportional predation pressure (PPP), with TAB, taking into account the interval between TAB-m and TAB-M, provides an estimate of the population densities of secondary consumers that could be fed by the primary consumers of VM: an area of 100 km²could support during a year 3e4 individuals of U. etruscus, 23e30 of C. mosbachensis, 12e14 of L. lycaonoides, 29e28 ofLynxcf.pardinus, 3e5 ofH. latidens, 5e6 of M. whitei, 5e6 of Panthera cf. gombaszoegensis and 6e7 of P. brevirostris(Table 3). According to the values of minimum viable population density (MVPD) of Silva and Downing (1994), these sustainable densities would allow a viable ecosystem for VM (Table 3).

Fig. 3shows the percentages of the total available biomass (TAB) consumed by the VM carnivores. These data indicate that resource distribution among the members of the carnivore guild was similar for both TAB-m and TAB-M, withP. brevirostrisas the species that would consume a greater fraction of the available biomass. Spe- ciﬁcally,P. brevirostriswould consume ~125,000 kcal/km²per year in the scenario of maximum rate of subadult mortality (Table 3), which represents 21.3% of TAB-m. The percentage of consumption in descending order for the other species would be 19.4% for L. lycaonoides,17.3% for M. whitei,17.0% for Pantheracf. gombaszoegensis,15.6% forH. latidens, 3.8% forC. mosbachensis,3.1% for

Lynxcf. pardinusand 2.3% forU. etruscus.In the scenario of minimum rate of subadult mortality,P. brevirostriswould increase its consume to ~160,000 kcal/km²per year, which represents 20.6% of TAB-M. The next species would beH. latidens,with a yearly consumption of ~157,000 kcal/km² (20.2% of TAB-M), followed by M. whitei(17.4%),Pantheracf. gombaszoegensisandL. lycaonoides (16.8% in both cases), C. mosbachensis (3.7%), Lynx cf. pardinus (2.3%), andU. etruscus(2.2%). According to these results, the species of secondary consumers could be divided in two groups, those that consumed >15% of the total available biomass supplied by the primary consumers (the scavengingP. brevirostrisand the hypercarnivores) and those that consumed <4% (the meso- and hypocarnivores).

3.2. Species competition indexes

The species competition index (SCI), which measures the percentage of satisfaction of the requirements for each carnivore species (Table 3,Fig. 4A), shows similar patterns for the scenarios of maximum and minimum rates of subadult mortality (TAB-M and TAB-m), although it should be noted that the values are consistently lower for TAB-M than for TAB-m. The only exception is Lynxcf.

pardinus,in which the SCI-m value is slightly lower than the SCI-M one (0.11 and 0.12, respectively). The low species competition indexes of the lynx indicate that its energetic requirements would be covered to a large extent in the scenarios of TAB-m and TAB-M.

Apart from the lynx, there are two groups of species according to their SCI-m values: on the one hand,C. mosbachensis,L. lycaonoides, P. brevirostrisandU. etruscushave values below 0.46; on the other, H. latidens,M. whiteiandPantheracf.gombaszoegensisshow values in excess of 0.55. To a certain extent, both groups can be also distinguished for TAB-M, although there is a change in the values of H. latidensandL. lycaonoides(Table 3,Fig. 4A). The species more affected by the differences between TAB-m and TAB-M is H. latidens,which gets a SCI-m value (0.61) that nearly doubles the one obtained for SCI-M (0.33). Apart fromLynxcf. pardinus,the species less affected by the differences between TAB-m and TAB-M isL. lycaonoides,followed byPantheracf.gombaszoegensis, M. whitei and those that had scavenging habits (C. mosbachensis, P. brevirostrisandU. etruscus) (Fig. 4A).

The indexes that measure competition intensity at the level of the whole carnivore guild of VM, the global competition index (GCI) and the global competition index biomass (GCIB), show values lower than 0.50 in both cases (Table 4). This indicates that more than half the individuals and biomass of secondary consumers expected under optimal conditions were reached in the scenarios of total available biomass with maximum and minimum rates of subadult mortality (TAB-m and TAB-M, respectively). However, given that the amount of biomass available depends on the mortality rate of subadult individuals in the community of primary consumers, some interesting differences emerge when both scenarios are compared. Speciﬁcally, in the TAB-m scenario the mortality rate is displaced towards the juveniles, whose carcasses provide less biomass, which results in a decrease of the total biomass available to the secondary consumers. In contrast, in the TAB-M scenario the biomass is displaced towards the largest size categories, which are not available to the small sized carnivores that do not scavenge, for example the lynx and the painted dog (see Rodríguez-Gomez et al., 2016a, 2016b). This results in higher values of GCI and GCIB for TAB-m than for TAB-M, because with a minimum rate of subadult mortality more biomass is available, which results in lesser competition intensity.

The difference observed between the global competition indexes GCI and GCIB for TAB-m and TAB-M is due to the pattern of consumption of these resources by the carnivore guild. GCIB-m is

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greater than GCI-M because when the rate of subadult mortality is maximal (TAB-m) the biomass of secondary consumers is displaced towards the species of smaller size (e.g., the lynx), which reach their higher densities. In contrast, when the rate of subadult mortality is minimal (TAB-M) the consumption of the biomass of primary consumers is displaced towards the species of larger size (e.g., the saber-toothH. latidens) and the values of GCI-M and GCIB-M get closer (Figs. 3 and 4A,Table 4).

4. Discussion

4.1. Theﬁrst human arrival in Western Europe

A number of issues related to the ﬁrst peopling of Western

Europe have been subject to intense debate during the last decades, including: (1) the chronology of their dispersal out of Africa; (2) the anatomical afﬁnities, taxonomic status, populational variability and techno-cultural developments of the dispersing population; (2) the possible dispersal routes; and (4) the ecological context and cli- matic conditions of the human settlements (Arribas and Palmqvist, 1999; Anton and Swisher, 2004; Nikitas and Nikita, 2005;

Palmqvist et al., 2005; Agustí et al., 2009; Agustí and Lordkipanidze, 2011; Jimenez-Arenas et al., 2011; Martínez- Navarro et al., 2014; Carotenuto et al., 2016; Perez-Claros et al., 2015; Palmqvist et al., 2016). For this reason, the Early Pleistocene sites of Orce are key for approaching the faunal and environmental circumstances faced by the hominins thatﬁrst dispersed out of Africa (Martínez-Navarro and Palmqvist, 1995, 1996; Martínez- Table 3

Sustainable densities of the Venta Micena secondary consumers estimated for the scenarios of maximum and minimum“Total Available Biomass”(TAB-M and TAB-m, respectively). Expected densities (Dx, individuals per km²) of carnivores were calculated using Damuth's allometric equations (see text). Nutritional requirements (NR), total intake (TI) and unsatisﬁed requirements (UR) of carnivoran species were measured in kcal per km². TI is deﬁned as the biomass (in kcal) consumed by each member of the carnivore guild after dividing TAB among the secondary consumers, taking into account the distribution of TAB by ungulate size categories and the dietary preferences of each carnivore species (data fromTable 2). This table includes also the values of sustainable densities (Ds, individuals per km²) calculated with the model for each secondary consumer, the values of minimum viable population densities (MVPD, individuals per km²) estimated as 10% of their expected densities (Silva and Downing, 1994) and the values of the species competition index (SCI) obtained with the model.

Dx NR TI UR Ds MVPD SCI

TAB-m

Canis mosbachensis 0.42 40,062 22,402 17,660 0.23 0.04 0.44

Lycaon lycaonoides 0.23 211,024 113,459 97,565 0.12 0.02 0.46

Lynx cf. pardinus 0.32 20,498 18,342 2156 0.29 0.03 0.11

Homotherium latidens 0.07 235,060 91,352 143,709 0.03 0.01 0.61

Megantereon whitei 0.11 225,976 101,273 124,703 0.05 0.01 0.55

Panthera cf. gombaszoegensis 0.10 226,604 99,242 127,362 0.05 0.01 0.56

Pachycrocuta brevirostris 0.10 222,660 124,509 98,151 0.06 0.01 0.44

Ursus etruscus 0.05 24,054 13,451 10,603 0.03 0.01 0.44

TAB-M

Canis mosbachensis 0.42 40,062 28,891 11,171 0.30 0.04 0.28

Lycaon lycaonoides 0.23 211,024 130,578 80,446 0.14 0.02 0.38

Lynx cf. pardinus 0.32 20,498 17,983 2516 0.28 0.03 0.12

Homotherium latidens 0.07 235,060 157,191 77,869 0.05 0.01 0.33

Megantereon whitei 0.11 225,976 135,902 90,074 0.06 0.01 0.40

Panthera cf. gombaszoegensis 0.10 226,604 130,656 95,948 0.06 0.01 0.42

Pachycrocuta brevirostris 0.10 222,660 160,571 62,090 0.07 0.01 0.28

Ursus etruscus 0.05 24,054 17,347 6708 0.04 0.01 0.28

Fig. 3.Distribution of the percentages of meat consumed by the secondary consumers identiﬁed in the faunal assemblage of Venta Micena (VM) according to the minimum (TAB-m, left) and maximum (TAB-M, right) values of total available biomass estimated for these sites.

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Navarro, 2004, 2010; Martínez-Navarro et al., 2015; Rodríguez- Gomez et al., 2016b).

With an age of 1.6e1.5 Ma, the fossil assemblage unearthed from Venta Micena (VM) offers a unique opportunity for analyzing the food webs of the large mammals community before theﬁrst human arrival in Western Europe. It should be taken into account, however, that during the last decades there has been intense debate and controversy on human presence at VM based on the anatomical afﬁnities of a cranial vault fragment (VM-0) and, to a lesser extent, of two humeral diaphyses (for review and discussion, seeMoya- Sola and Kohler, 1997; Palmqvist, 1997; Gibert et al., 1998;

Palmqvist et al., 2005). The last comparative study of VM- 0 concluded that it was part of the frontal bones of a female

ruminant without cranial appendages (Martínez-Navarro, 2002).

Moreover,Arribas and Palmqvist (2002)estimated as negligible the probability that a taxon the size of earlyHomo(~50 kg) could be represented in the assemblage of VM (which includes >20,000 bones and teeth) by three bones and no tooth remains. In contrast, evidence of human presence is well documented in two nearby sites that are somewhat younger than VM, Barranco Leon-D (BL-D) and Fuente Nueva-3 (FN-3). These sites have been dated by the U/

ESR method in 1.43±0.38 and 1.19±0.21 Ma, respectively (Duval et al., 2012; Toro-Moyano et al., 2013), and there is also an age estimate of 1.50 ± 0.31 Ma for FN-3 obtained from cosmogenic nuclides (Alvarez et al., 2015). For this reason, Carotenuto et al.

(2016)consider that BL-D and FN-3 mark the end of the dispersal route of a second out of Africa event, which took place between 1.4 and 0.9 Ma.

Therefore, the rich and well-preserved assemblage of VM opens the possibility of studying the paleoecosystems of Mediterranean Europe before theﬁrst human arrival in this continent. Given the high diversity and preservational completeness of the fossil assemblage (Arribas and Palmqvist, 1998; Palmqvist et al., 1999;

Palmqvist and Arribas, 2001), which records 13 species of primary consumers and eight species of secondary consumers, it is Fig. 4.Distribution of the values of the species competition index (SCI) among the secondary consumers of VM (A) and BL-D y FN-3 (B) (modiﬁed fromRodríguez-Gomez et al., 2016b) for two scenarios: minimum (TAB-m, blue diamonds) and maximum (TAB-M, red squares) estimates of total available biomass. (For interpretation of the references to colour in thisﬁgure legend, the reader is referred to the web version of this article.)

Table 4

“Global Competition Index” (GCI) and“Global Competition Index Biomass”

(GCIB) for the Venta Micena (VM) assemblage. TAB-m: minimum Total Available Biomass; TAB-M: maximum Total Available Biomass.

Index TAB-m TAB-M

GCI 0.39 0.28

GCIB 0.48 0.32

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essential for analyzing the ecological interactions in the large mammals community and deciphering the behavior of the members of the carnivore guild (Palmqvist et al., 1996, 2011, 2003, 2008a, 2008b).

4.2. The ecological context of the earliest human settlements

We have used in this study the methodology recently applied to the analysis of the large mammals communities of BL-D and FN-3 (Rodríguez-Gomez et al., 2016b), which is based on mathematical tools widely used in population dynamics (Caswell, 2000; Keyﬁtz and Caswell, 2005; Owen-Smith, 2010) that allow evaluating the sustainability of the carnivore guild through the biomass poten- tially available of primary consumers. In this way, the results of this study are fully comparable with those obtained for BL-D/FN-3 (Rodríguez-Gomez et al., 2016b).

The estimates of total available biomass (TAB) for the members of the carnivore guild of VM are greater than those obtained in the case of BL-D/FN-3, both in the sceneries of maximum and minimum rates of subadult mortality (TAB-m and TAB-M, 30% and 26%

greater, respectively). It should be noted, however, that the herbivore guild of VM shows a number of differences with the one unearthed from BL-D and FN-3. Speciﬁcally, it includes three bovids (Hemibosaff.gracilis, Praeovibossp., andS. minor) and two small- sized ruminants that are currently under study (Bovidae indet., chamois-sized, and Cervidae indet., roe deer-sized), which are all absent from BL-D and FN-3. Similarly, two ungulate species present at BL-D and FN-3 (Equus suessenbornensisandAmmotragus euro- paeus) have not been identiﬁed in VM. There are also differences in the carnivore guild of these sites, asPantheracf.gombaszoegensisis recorded in VM whileHomosp. is present in BL-D and FN-3. As a result, the total demanded biomass (TDB) of the secondary consumers is 13% greater for VM than for BL-D/FN-3.

The differences in the values of total available biomass and total demanded biomass together with the competition intensity indexes estimated for these sites indicate a less hostile ecosystem for the carnivore guild of VM compared to BL-D and FN-3. Speciﬁcally, the values of the global competition index (GCI) for TAB-m and TAB-M conditions (GCI-m ¼ 0.39 and GCI-M ¼ 0.28; Table 4) indicate that the carnivores of VM would reach densities that are above half the value expected for optimal conditions (i.e., those in which they would reach their maximum ecological densities).

These estimates are clearly lower than those of BL-D/FN-3 (GCI- m¼0.58, GCI-M¼0.50). In which concerns the global competition index biomass (GCIB), the values obtained (GCIB-m¼0.48 for TAB- m and GCIB-M¼0.32 for TAB-M) indicate that more than half the biomass expected under optimal conditions was reached in VM.

The high GCIB-m value compared to the GCI-m estimate indicates that a greater percentage of the biomass of primary consumers would be consumed by the carnivore species of smaller size if the rates of subadult mortality were maximum for ungulates. In the TAB-M scenario, however, the GCIB and GCI values are closer, which suggests that in these conditions the consumption of ungulate resources was displaced towards the largest carnivores (Rodríguez- Gomez et al., 2016a, 2016b). In the case of GCIB, the differences between VM and BL-D/FN-3 (GCIB-m¼0.59, GCIB-M¼0.45) are slightly lower (Table 4andRodríguez-Gomez et al., 2016b: Table 4).

These results show that more than half of the resources demanded under optimal conditions by the carnivore guild of VM could be satisﬁed with the total available biomass of ungulates, while this is only met for BL-D/FN-3 under the TAB-M scenario.

Accordingly, an area of 100 km²of the Baza Basin could hold in the paleoecosystem of VM, under the most favorable scenario for the availability of meat resources (TAB-M), 30 individuals of C. mosbachensis,28 ofLynxcf.pardinus,14 ofL. lycaonoides,seven of

P. brevirostris,six of bothM. whiteiandPantheracf.gombaszoegensis, ﬁve ofH. latidensand four ofU. etruscus(Table 3). These values were obtained considering the biomass available in the paleoecosystem from those ungulate species weighing>10 kg. However, the population densities of the scavenging carnivores (P. brevirostris), omnivores (C. mosbachensisandU. etruscus) and hypercarnivores in which a signiﬁcant part of their diet was based on prey of<10 kg (Lynx cf. pardinus) would be greater, as these species would consume other resources not considered in the model. If these sustainable densities are compared with those of BL-D/FN-3 (Rodríguez-Gomez et al., 2016b: Table 3), it is clear that all carnivore species reach higher values in VM. The most striking difference is found in the case ofLynxcf.pardinus, which density in VM triples the one estimated in BL-D/FN-3 (nine individuals per 100 km²).

According to the studies ofSilva and Downing (1994)on the minimum viable population densities of carnivores, the estimates for the members of the carnivore guild of VM would allow a viable ecosystem, and this would be also the case in FN3/BL-D. However, Rodríguez-Gomez et al. (2016b) indicated that the study ofSilva and Downing (1994)analyzed populations classiﬁed by the Inter- national Union for the Conservation of Nature Red List (Thornback and Jenkins, 1982) as “endangered”, “vulnerable”, or “close to extinction”. Even in the case ofH. latidens, the species of VM that shows the highest value of the species competition index (Fig. 4, Table 3), the estimate for TAB-m (SCI-m¼0.61) is distant from the MVPD value (which, translated into a SCI value, would be of ~0.90).

In the case of BL-D/FN-3, however, the species competition index of Lynxcf.pardinusfor TAB- M (SCI-M ¼0.71) is near the value in which the population would not be viable (Fig. 4).

Five members of the carnivore guild of VM (L. lycaonoides, H.

latidens, M. whitei, Pantheracf.gombaszoegensisandP. brevirostris) show greater demands of consumption of the total available biomass (TAB), while the other three (C. mosbachensis, Lynx cf.

pardinusandU. etruscus) played a more secondary role (Fig. 3). In spite of the differences of composition between the faunal assem- blages of VM and BL-D/FN-3, similar results were also found in the two latter sites (Rodríguez-Gomez et al., 2016b). In VM, the percentages of TAB consumed by most carnivore species are similar in the TAB-m and TAB-M scenarios, withH. latidensandL. lycaonoides showing the most important differences. Speciﬁcally,H. latidens increases the percentage of meat consumed in the TAB-M scenario (20.2%) compared with the conditions for TAB-m (15.6%). In contrast, there is a decrease in the percentage of consumption of L. lycaonoidesfrom TAB-m (19.4%) to TAB-M (16.8%). These results are in agreement with the prey preferences deduced for both predators from a combined approach based on biogeochemistry and ecomorphology analyses (Palmqvist et al., 1999, 2003, 2008a, 2008b), because the saber-tooth would focus on adult ungulates of medium-to-large size while the pack-hunting canid would mainly prey on small ungulates and juveniles of medium-sized species. The only species with access to megaherbivore carcasses in excess of 1000 kg would be H. latidens and the scavengers (Table 2). The abundance of this ungulate size category is greater with TAB-M, because under these circumstances the proportion of adult individuals is greater, which beneﬁts H. latidens and the scavengers. In fact, isotopic analyses of the VM species (Palmqvist et al., 2003, 2008b) have shown that very large prey were relatively minor components of the diet of all hypercarnivores except H. latidens(in which juvenile proboscideans would represent up to 10% of its diet) and the scavengingP. brevirostris.

Concerning the values of the species competition index (Fig. 4A, Table 3),Lynxcf.pardinusis the carnivore that would satisfy to a greater degree its requirements, showing the lowest TAB-m and TAB-M values, in spite of the fact that it consumed a lower omez et al. / Quaternary Science Reviews 164 (2017) 154e167

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percentage of the total available biomass than all other species exceptU. etruscus.This is so because in the analysis we considered that the lynx population would cover 90% of its requirements with prey of<10 kg (e.g., small mammals and birds), which are outside the range of the model. In addition, this species is the one that suffers least with the difference between TAB-m and TAB-M, followed byL. lycaonoides, because both hypercarnivores would have mostly preyed on those ungulates of smaller body size. It is worth noting that under TAB-M conditions the proportion of adult herbivores would be greater than for TAB-m, which would mean that these individuals reached their maximum weight. In spite of this, the biomass supplied by the four taxa that belong to theﬁrst two size classes (i.e., Bovidae indet. small size, Cervidae indet. small size,H. albus, andM. rhenanus) would be relatively stable. Although L.lycaonoidesdecreases its percentage of consumption of the total available biomass when the abundance of adult individuals is greater in the prey species (Fig. 3), this carnivore reaches its lowest value of the species competition index (SCI) for TAB-M conditions (i.e., considering a maximum rate of subadult mortality). This indicates a greater degree of satisfaction for the population of wild dogs, which increases its annual consumption of meat from TAB-m to TAB-M conditions. To a lesser extent, this would also apply to the lynx, which consumes nearly the same amount of meat in both scenarios (Table 3). The difference of the SCI value forH. latidens between TAB-m and TAB-M shows the weight of the ﬁrst size category on TAB-m, which is the one not consumed by this species (Table 2).

A different pattern emerges for the TAB-m scenario (i.e., if a minimum rate of subadult mortality is considered) when the results of VM are compared with those obtained for BL-D/FN-3 (Fig. 4B). In the latter sites, Rodríguez-Gomez et al (2016b:

Fig. 3B, Table 3) noted a ceiling effect in which most species obtained values of the species competition index close to 0.60, as happens in VM forH. latidensbut not for the other members of the carnivore guild, which all show SCI values<0.56 (Fig. 4,Table 3).

The most relevant data for TAB-M is that the lynx continues to show the lowest SCI value. This was not the case for BL-D/FN-3, in which the SCI of the lynx was the highest among carnivores. This indicates that the pressure on the prey categories of smaller body size would be lower in VM than in BL-D/FN-3. In the latter sites, this could result from a decrease in the total available biomass for these categories and also from the presence ofHomosp., because the human population would probably exert a signiﬁcant pressure on them.

Therefore, a number of changes in the composition of the large mammals assemblage of BL-D/FN-3 with respect to VM seem to be behind the differences in the results obtained for both paleocommunities. Such differences in community structure can provide information on the changes in their trophic webs. Although there is a reduction in the values of total available biomass (TAB) and total demanded biomass (TDB) from VM to BL-D/FN-3, this reduction is greater for TAB, as discussed before, which indicates an increase in competition in the carnivore guild from VM to FN-3/BL-D. The reduction in TAB results from a change in the composition of the guild of primary consumers, which are less diverse in FN-3/BL-D (10 spp.) than in VM (13 spp.). Of these species,A. europaeusand E. suessenbornensisare present in FN-3/BL-D, but not in VM. How- ever,Hemibosaff. gracilis, Praeovibossp.,S. minor,Bovidae indet.

(small size) and Cervidae indet. (small size) are all present in VM and absent from the other two sites. These ungulates would represent an important fraction of the biomass provided by theﬁrst three prey size categories (i.e., 10e45 kg, 45e90 kg and 90e180 kg), which would translate into better conditions for the small-sized secondary consumers that focused on them, as noted before.

The differences in the composition of the carnivore guild between VM and FN-3/BL-D consist of the presence of the European

jaguar,Pantheracf.gombaszoegensis,and the absence ofHomosp. in VM, while the opposite holds for FN-3/BL-D. The values of the species competition index (SCI) in VM show that the presence of the jaguar under TAB-m conditions shifts saber-toothsH. latidens andM. whiteitowards higher SCI values, dissociating them from the rest of carnivore species. This is not evidenced in the case ofHomo sp. at BL-D/FN-3, because the SCI values of both saber-toothed predators in these sites are more similar to those of other members of the carnivore guild (Fig. 4). Suchﬁnding suggests that the jaguar would be competing with the other two large felids to a larger extent thanHomosp. Therefore, the presence of the jaguar would have consequences on the availability of large-sized ungulates for both saber-tooths, which would only prey on the juveniles of megafauna (Palmqvist et al., 2008a, 2008b). However, this does not apply to the presence ofHomo sp., a scavenger of the carcasses of megafauna (Espigares et al., 2013), which would also prey occasionally on the smallest size categories. In fact,Rodríguez- Gomez et al. (2014b)tested with the model used here three pro- curement strategies in the access to ungulate carcasses forHomosp.

at BL-D/FN-3: (1) a strict scavenging behavior with no preferences for any size category; (2) a mixed strategy that combined hunting and scavenging; and (3) a strict hunting strategy of small-to- medium ungulate prey. The results obtained in this study suggested that the hominin populations that inhabited Southeast Spain during the Early Pleistocene behaved more as opportunistic scavengers than as active predators.

In a study on the presence of hominins in the Atapuerca karstic complex (Burgos, NW Spain),Rodríguez-Gomez et al. (2014a,b) also noted that Homo antecessor and Panthera cf. gombaszoegensis seemed to be in conﬂict. For this reason, they proposed that the presence of one of these species was linked to the absence of the other. This opens two alternative scenarios (Rodríguez-Gomez et al., 2014a,b): (1) human dispersal in the Baza Basin resulted in the ecological displacement ofPantheracf.gombaszoegensis; or (2) the jaguar disappeared from this basin, which allowed human arrival in it. Under theﬁrst hypothesis, the change in the composition of the guild of primary consumers of BL-D/FN-3 with respect to VM would be linked to top-down forces (sensuRipple and Van Valkenburgh, 2010). This would mean that the populations of some ungulate species of VM were subject to a severe pressure by the secondary consumers, which led them to low population densities. The arrival of Homo sp. would destabilize these relationships, which would perhaps result in the local extinction at the basin ofHemibosaff.gracilis, Praeovibossp.,S. minorand the two small-sized ruminants of the VM assemblage. IfHomosp. behaved more as a hunter than as a scavenger, it would impact mainly on the size categories of these species, although it should be noted that a scavenging behavior has been proposed for these early human populations in BL-D/FN-3 (Arribas and Palmqvist, 1999; Espigares et al., 2013; Rodríguez-Gomez et al., 2016b).

According to their values of the species competition index, the carnivore species at greater disadvantage for satisfying their requirements in VM would beH. latidensandPantheracf.gombaszoegensis, which show the highest TAB-m and TAB-M values, respectively (Fig. 4A). This means that the jaguar would be the species more sensitive to any ecological change under a minimum rate of subadult mortality for ungulates. However, the human presence would not have had a severe impact on this predator, because the consumption proﬁle ofHomosp. both as a scavenger or as a hunter does not coincide with the one of the jaguar, which means that they would not compete directly. This seems to support the second hypothesis, as it suggests that the absence ofPantheracf.

gombaszoegensiswas the cause of the presence ofHomosp. and not its consequence. In any case, we must take into account that both species have been recorded in a number of sites, for example the

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level TD3-TD4 of Atapuerca Gran Dolina (Rodríguez et al., 2011) and the site of Vallonnet in France (Moulle et al., 2006), which means that if an ecological displacement between humans and jaguars took place at Orce this would not reﬂect a general scenario of competitive displacement.

4.3. Comparison with other early pleistocene sites

A comparison of the results of this study with those obtained by Rodríguez-Gomez et al. (2017: Table 5) for the sites of Atapuerca Gran Dolina (TD3-TD4, TD6-2, TD8, TD10-1) and Galería (GIIb and GIIIa) shows that the degree of competition in VM is slightly higher than in all these sites, with the only exception of TD6-2, in which the degree of competition is minimum. Speciﬁcally, VM shows a value of the global competition index for the scenary of maximum rate of subadult mortality (GCI-m¼0.39) that is close to the one obtained in level GIIIa of Galería (0.36) and its value for the scenary of minimum rate of subadult mortality (GCI-M ¼ 0.28) is also similar to those of GIIb and GIIIa (0.26 in both cases). However, the estimates of the global competition index biomass (GCIB) are higher in VM (GCIB-m: 0.48; GCIB-M: 0.32;Table 4) than in the Atapuerca sites, of which TD3-TD4 shows the closest values (GCIB- m: 0.38; GCIB-M: 0.22; Rodríguez-Gomez et al., 2017: Table 5).

These differences in competition intensity result from differences in the composition of the carnivore guild between both sets of paleocommunities, because the diversity of carnivores in VM (eight species) is greater than in any of the Atapuerca sites (in which a maximum of six species have been recorded).

A study at a European scale for sites dated between 1.1 and 0.8 Ma (Rodríguez-Gomez, 2015) showed that the global competition indexes estimated for Atapuerca are the most similar to those of VM, although the levels Wa1-Wa3 of Wannenk€opfe (Germany) (Koenigswald and Heinrich, 1999), which show GCI-m and GCI-M values of 0.43 and 0.26, respectively, are also close to the VM estimates (0.39 and 0.28, respectively;Table 4). Concerning the values of the global competition index biomass, the faunal set that comes closest to VM is the Lower Unit of Vallparadís (Spain) (García et al., 2011; Madurell-Malapeira et al., 2014), which shows GCIB-m and GCIB-M values of 0.49 and 0.31, respectively, similar to those of VM (0.48 and 0.32, respectively;Table 4). According to the values obtained byRodríguez-Gomez (2015), VM is placed among the sites that show competition levels that are situated slightly above the mean.

A study of predator:prey ratios (Meloro et al., 2007;Raia et al., 2007;Croitor and Brugal, 2010;Palombo, 2010) show that these ratios tended to decrease during the Epivillafranchian. However, the analyses of the Orce sites suggest that this decrease started earlier, during the Late Villafranchian, as suggested by the comparison between the values of VM (8:13) and BL-D/FN-3 (8:10). This trend can be interpreted as an increase of competition intensity in the carnivore guild, because less species of primary consumers would support the same diversity of secondary consumers, although it must be borne in mind that the meat requirements of Homosp. in BL-D/FN-3 would be lower than those ofPantheracf.

gombaszoegensisin VM.

Trophic network analysis represents a different approach to the study of paleo-food webs (Dunne et al., 2002, 2008, 2014, 2016;

Pires et al., 2014; Yeakel et al., 2013; Yeakel and Dunne, 2015).

Lozano et al. (2016)used this methodology for analyzing ecosystem dynamics in the late Early Pleistocene to Middle Pleistocene of Europe, with emphasis on the changes in the ecological interactions among large mammals during the Mid-Pleistocene Revolution (~1.0e0.8 Ma) and the trophic position of Homo. They found a decreasing trend in the connectance (i.e., the average number of feeding links per species) of the paleo-food webs from the

Villafranchian to the Galerian, which would result from the disappearance of a number hypercarnivore species and the arrival of more versatile social predators that were unable to kill the megafauna. Such change was evidenced in the comparison of the paleo-food webs of VM and Atapuerca GIIa (Lozano et al., 2016:

Fig. 3), which showed that VM had a higher degree of connectance.

This implied that bottom up regulatory mechanisms gained more relevance in the Mid-Pleistocene ecosystems and the food webs were simpliﬁed, as previously noted byRaia et al. (2007). Of interest to our study,Lozano et al. (2016)found that the values of connectance of BL-D and FN-3 were similar to those of other Late Villafranchian sites of Europe. For this reason, they concluded that the arrival of hominins had a minimal effect on the food webs, as they were likely opportunistic omnivores that integrated in the existing ecosystems without inducing signiﬁcant structural changes on them. This is in agreement with the relatively marginal role considered forHomosp. in Europe during the Early Pleistocene (Rodríguez et al., 2012; Espigares et al., 2013; Rodríguez-Gomez et al., 2016b).

4.4. Theﬁrst human dispersal in Europe: a matter of ecological opportunity?

Theﬁnding of hominin remains and Mode 1 lithic artifacts at the Caucasian site of Dmanisi (Agustí and Lordkipanidze, 2011;

Lordkipanidze et al., 2013) points to an age of ~1.8 Ma for theﬁrst human settlements at the gates of Europe, while the oldest evidence of human presence in Western Europe can be traced back to

~1.4 Ma, the age of BL-D and FN-3 in Orce (Martínez-Navarro et al., 1997; Toro-Moyano et al., 2013; Palmqvist et al., 2016), followed at

~1.2 Ma by Sima del Elefante and Gran Dolina in Atapuerca (Bermúdez de Castro et al., 1997; Carbonell et al., 2008). In this context, the absence of evidence of human presence at VM could be interpreted as evidencing that: (1) this Early Pleistocene site marks the earliest chronology (~1.6e1.5 Ma) in which hominins were still absent from Western Europe; and (2) thefirst human arrival in this area took place slightly later, as documented in FN-3 and BL-D. The second possibility should be taken with caution, however, because there is a preliminary report on thefinding of lithic artifacts and cut marks on bones in a karstic locality placed in the eastern region of the Iberian Peninsula, the site of Alto de las Picarazas, which pre- serves an assemblage withS. minorand the arvicolidAllophaiomys ruffoi(Vicente-Gabarda et al., 2016). Both species are present at VM but not at FN-3/BL-D. For this reason, given that humans could have been present at other sites of the Iberian Peninsula of similar chronology to VM, the absence by the moment of a hominin record at this site could be perhaps a deficiency of its record. However, the recovery of>22,000 fossils of large mammals at VM, which allow calculating a minimal number of ~400 individuals, argues against this interpretation, because it is difficult to conceive that no human tooth or bone remain was preserved at VM ifHomosp. was present in the Baza Basin during the time this assemblage was being formed.

In any case, given that there were no considerable barriers for the dispersal into Mediterranean Europe of the pioneering population of Dmanisi, the most reasonable scenario for explaining a delay in the colonization of the Baza basin at SE Spain would be to consider that the ecological conditions at Venta Micena didn't allow a human population to inhabit these ecosystems. However, our results contradict this hypothesis, because the competition intensity estimated in the carnivore guild of this site was lower than the one of FN-3/BL-D (Fig. 4AeB), which suggests that the timing of theﬁrst human dispersal in Western Europe was probably not a matter of ecological opportunity.