Did humans disturb bats? Exploring the hominin-chiropter interactions in the Sierra de Atapuerca sites (early to Middle Pleistocene, Spain)

Quaternary Science Reviews 226 (2019) 106018

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Did humans disturb bats? Exploring the hominin-chiropter interactions in the Sierra de Atapuerca sites (early to Middle Pleistocene, Spain)
n a, *, Carmen Nún ~ ez-Lahuerta a, Juan Manuel Lo
pez-García b, c, Julia Gala a
s Gloria Cuenca-Besco a b c


n, Spain Aragosaurus-IUCA, Ciencias de la Tierra, Facultad de Ciencias, Universidad de Zaragoza, C. Pedro Cerbuna 12, 50009, Zaragoza, Arago ~ a, Spain IPHES, Universidad Rovira i Virgil, Campus Sescelades, Edificio W3, 430007, Tarragona, Catalun  ria, Universitat Rovira i Virgili (URV), Avinguda de Catalunya 35, 43002, Tarragona, Spain Area de Prehisto

a r t i c l e i n f o

a b s t r a c t

Article history: Received 15 May 2019 Received in revised form 5 October 2019 Accepted 16 October 2019 Available online xxx

Fossil bats are common components of Pleistocene palaeontological cave-sites, sometimes appearing in levels with evidence of a human presence. As with other small vertebrates, variations observed in fossil bat palaeocommunities through a stratigraphic sequence may be correlated to palaeoclimatic and palaeoenvironmental fluctuations. As many bat species are typically cave-dwelling animals, however, the bat palaeocommunity may also be affected by hominin presence. The correlation between bat palaeocommunity dynamics and both climatic and anthropic factors is addressed in the present study by analysing their record along the Early and Middle Pleistocene sequence in the Sierra de Atapuerca. A marked deterioration in the Sierra de Atapuerca chiropter faunas occurred from 500 ka on simultaneously with a change in the occupational pattern of the predominant bat species Myotis myotis, which apparently stopped using the shelters as nursery roosts. These changes coincides with a time of extreme cold events succession during glacial periods, but also with evidence of intensive human occupation at some of the sites analysed. Some features of bat assemblages at these levels, such as differences in species composition between synchronous levels, the inability of bat palaeocommunities to recover during intermediate warmer periods, or detected seasonal alternation between hominis and humans, suggest that anthropic disturbance could have play a significant part in the decline of Middle Pleistocene bat palaeocommunities of Atapuerca. © 2019 Published by Elsevier Ltd.

Keywords: Pleistocene Western Europe Palaeoclimatic approach Small mammal palaeontology Chiroptera

1. Introduction Caves used as shelters by prehistoric humans were sometimes shared with bats. There is proof in the Eurasian Pleistocene fossil record of how the human occupation of a cave could negatively influence the bat palaeocommunities roosting there, as described in Denisova Cave (where bat palaeobiodiversity drastically decreased during human occupation of the cave at the Upper Pleistocene, Rossina, 2006) or in Candide Cave (where Lateglacial humans and bats occupied the cave alternately at different times of the year, Salari, 2010). As a rule, this interference is detected as a

* Corresponding author.
n), [email protected] (C. Nún ~ ezE-mail addresses: [email protected] (J. Gala
pez-García), [email protected] (G. CuencaLahuerta), [email protected] (J.M. Lo
s). Besco https://doi.org/10.1016/j.quascirev.2019.106018 0277-3791/© 2019 Published by Elsevier Ltd.

decrease in the amount of bat remains recorded, as well as in their
pez-García et al., 2011b; Rossina, 2006; palaeobiodiversity (Lo Salari, 2010). Noise, and light or smoke (if fire was employed) are factors that could have forced bats to look for new roosts when humans moved into the same cave. The archaeo-palaeontological sites of the Sierra de Atapuerca (Burgos, Northern Spain, Fig. 1A), where hominin and bat remains appear buried together in some layers, provide a good opportunity to analyse the possible interactions between bats and human communities in sharing a cave, using a well-known stratigraphic sequence of about 1 Ma (from the pre-Jaramillo Early Pleistocene to the Middle Pleistocene). On the other hand, there is no previous evidence of this kind of human-bat interaction in such an early period (i.e. involving hominins with technology Mode 1 or 2, who most probably didn’t use fire). This study was conducted with material from several important human fossil localities in

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n et al. / Quaternary Science Reviews 226 (2019) 106018 J. Gala

Fig. 1. Geographical and geological context of the analysed Atapuerca sites. A: location of the Atapuerca sites in the Iberian Peninsula. B: map of the Atapuerca complex, modified from Ortega et al. (2013). C: Schematic stratigraphic profiles of the analysed sites; Sima del Elefante modified from Carbonell et al. (2008); Gran Dolina modified from Berger et al., res et al. (2013); Sima de los Huesos modified from Arsuaga et al. (2014). AGE references: [1] Carbonell et al. (2008); [2] Huguet et al. (2017); [3] (2008); Galería modified from Falgue

pez-García et al. (2011a); [5] Berger et al., (2008); [6] Falgue res et al. (1999); [7] Arnold et al. (2015); [8] Moreno et al. (2015); [9] Alvarez-Posada Arnold and Demuro (2015); [4] Lo res et al. (2013); [11] Arnold et al. (2014); [12] Arsuaga et al. (2014). et al. (2018); [10] Falgue

Atapuerca (Spain) of an Early and Middle Pleistocene age (Fig. 1B): Sima del Elefante Lower Red Unit (Early Pleistocene), Gran Dolina (Early and Middle Pleistocene), Galería (Middle Pleistocene) and Sima de los Huesos (Middle Pleistocene). This all consist of cavefilling sedimentary sequences. The Sierra de Atapuerca has provided hominin fossil remains

from two Early Pleistocene phases (Bermúdez de Castro et al., 1999;
et al., 2013; among others) Carbonell et al., 1999a, 1999b, 2008; Olle through the accumulation of level TE9 of the Sima del Elefante site (dated ca. 1.2 Ma, Carbonell et al., 2008, Fig. 1C) and level TD6 of the Gran Dolina site (age ranging between 0.8 and 0.9 Ma, Arnold et al., 2015; Berger et al., 2008; Moreno et al., 2015, Fig. 1C). The presence


n et al. / Quaternary Science Reviews 226 (2019) 106018 J. Gala

of lithic tools evidences the occurrence of Early Pleistocene hominins over a longer time span, as these have been found at the Sima del Elefante site from levels TE9 up to TE14, and in Gran Dolina from
et al., 2013). The Middle Pleistocene human TD3-4 to TD7 (Olle presence in the Sierra de Atapuerca is apparently ubiquitous (Arsuaga et al., 2014; Carbonell et al., 1995, 2001; García-Medrano, 2011; García-Medrano et al., 2014, 2015; M
arquez et al., 2001;
ndez, 2009; Mosquera, 1995, 1998; Olle
et al., 2013; Rosell, Mene 2001; Rosell et al., 2011; Rodríguez, 2004; Terradillos, 2010; among others). Most human remains have been recorded in lithostratigraphic unit LU6 of Sima de los Huesos (Arsuaga et al., 2014; dated to 0.43 Ma, Arnold et al., 2014, Fig. 1C). Furthermore, two human fossils have been recovered at the Galería complex site: an adult mandible fragment from unit GII (Bermúdez de Castro and Rosas, 1992, Fig. 1C) and a neurocranial fragment at the base of GIII (Arsuaga et al., 1999; top of GIII dated to 0.25 Ma, Berger et al., res et al., 2013, Fig. 1C). Lithic tools have been recov2008; Falgue
et al., 2013; top dated to ered in level TD10 of Gran Dolina (Olle res et al., 1999; Moreno et al., 0.34 Ma, Berger et al., 2008; Falgue 2015, Fig. 1C), lithostratigraphic unit LU6 of Sima de los Huesos (Arsuaga et al., 2014) and levels GII and GIII of the Galería complex
et al., 2013). site (Olle Most of these levels of the Atapuerca sites, both of Early and Middle Pleistocene ages, include fossils from bats. However, the species richness, the particular species represented, and the mortality pattern of the bats differ in each of them. Taking the above into account, the main goals of this work are: (1) to analyse the palaeobiodiversity, the palaeoclimatic and palaeoenvironmental affinities, and the taphonomy of the bat fossil assemblages recorded along the Sierra de Atapuerca Early and Middle Pleistocene sequence, and (2) to explore their possible correlation with both climatic and anthropic factors. 2. Geographical and geological setting The record provided by the many sites that make up the Sierra de Atapuerca complex evidences the presence of the genus Homo in Western Europe over a long period ranging from the Early Pleistocene to the Late Pleistocene and Holocene. However, the materials studied in this work are Early to Middle Pleistocene in age (Arsuaga et al., 1993; Carbonell et al., 2008; Rodríguez et al., 2011;
s et al., 2016). The Atapuerca sites consist of sediCuenca-Besco mentary infillings of karstic cavities, belonging to Las Torcas system (Ortega et al., 2013). This is a three-level system that developed in a mountainous hill of Cretaceous limestones, with a maximum altitude of 1080 m above sea level, located between the Cantabrian and the Iberian Ranges (Fig. 1A). The dissolution that gave rise the karst complex occurred during the Upper Miocene. Las Torcas is divided into two systems (Ortega et al., 2013): Cueva Mayor and Trinchera del Ferrocarril (Fig. 1B). Three of the sites studied in this work, Sima del Elefante, Gran Dolina and Galería, belong to the Trinchera del Ferrocarril system; the other one, Sima de los Huesos, belongs to the Cueva Mayor system.

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s et al., 2001; by allochthonous detrital sediment (Cuenca-Besco Huguet, 2007; Rosas et al., 2006). It is Early Pleistocene in age and includes some of the oldest evidences of human occupation in western Europe, with the presence of Homo remains in level TE9c, dated to 1.22 ± 0.16 Ma (Carbonell et al., 2008). 2.2. Gran Dolina The Gran Dolina site (UTM co-ordinates: 30T 457167 4688915) comprises sedimentary infill of 19 m thickness, which has been divided into 11 lithostratigraphic units from TD1 (TD after Trinchera Dolina) to TD11 (Fig. 1C), mainly allochthonous detrital sed
s et al., 1995, 1999; see the most recently iments (Cuenca Besco ~ a et al., 2015). Levels TD1 to TD6 are updated stratigraphy in Campan Early Pleistocene in age, and levels TD8 to TD11 are Middle Pleistocene. This site has three units with important archaeopalaeontological accumulations, as detailed below. Human remains along with lithic tools were recovered in level TD6 (Early Pleistocene), allowing the description of a new human species:
et al., 2014). In Homo antecessor (Carbonell et al., 1995; Saladie addition, levels TD4 (Early Pleistocene) and TD10 (Middle Pleistocene) yielded large amounts of lithic tools and faunal remains

et al., evidencing human activity (Alvarez-Posada et al., 2018; Olle 2013), and level TD10 has been interpreted as a human campsite
et al., 2013). (Olle 2.3. Galería The Galería complex (UTM co-ordinates: 30T 457168 4688877) is Middle Pleistocene in age and has a 12 m-thick infilling (Fig. 1C), distributed into three sectors or subcavities: a central area called Trinchera Galería; a small chamber to the north, called Trinchera Zarpazos; and a vertical shaft at the southern end called Trinchera Norte (García-Medrano et al., 2017). The infilling of these sectors was approximately simultaneous, so the layers can be laterally correlated, and the following levels are distinguished: GI (Galería I) res et al., 2013; Pe
rez-Gonza
lez et al., 1995). Levels GII to GV (Falgue and GIII contain archaeo-palaeontological deposits and have been interpreted as a home base for humans (García-Medrano et al., 2017). 2.4. Sima de los Huesos The Sima de los Huesos site (UTM co-ordinates: 30T 458819 4688759) is a small cave located in the Cueva Mayor system (Fig. 1B). This Middle Pleistocene site is well known for having yielded the biggest collection of human remains from the Middle Pleistocene, with at least 28 individuals recovered from a single stratigraphic unit, LU6 (Arsuaga et al., 1997, 2014). The deposits were initially divided into two units: clays with human and bear remains (CH&B) and dark clays with bat guano (DCBG), separated by a speleothem (Arsuaga et al., 1997). More recent stratigraphic analyses established a new division into 12 units, LU1 to LU12 (Fig. 1C; Arsuaga et al., 2014).

2.1. Sima del Elefante 3. Material and methods The Sima del Elefante site (UTM co-ordinates: 30T 457195 4688791) is the oldest of the sites analysed. It is formed by a 25 m thick cave infill, divided into 16 stratigraphic levels from TE7 (TE
s et al., after Trinchera Elefante) to TE21 (Fig. 1C; Cuenca-Besco 2001; Huguet, 2007; Rosas et al., 2006). These levels belong to three different sedimentary phases, of which only the first, oldest one is studied in this work. This phase is called TELRU (Trinchera Elefante Lower Red Unit) and it includes levels TE7 to TE14, formed

The samples under study are from the four above-described sites: Sima del Elefante (TELRU, levels TE7 to TE14), Gran Dolina (levels TD3-4 to TD10), Galería (levels GIIIa and GIIIb) and Sima de los Huesos (level LU6). They were recovered during excavation campaigns that took place from 1991 to 2016. The amount of sediment processed differs from one unit to another (see Table 1) due to both the thickness of each layer and the horizontal extension


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Table 1 Processed material by site and lithostratigraphic level, the levels of each site are displayed in stratigraphic order (sites correlation in Fig. 1C). t: estimated tons of processed sediment; NISP: number of identified specimens assigned to order Chiroptera (including Chiroptera indet.); MNI: minimum number of individuals assigned to order Chiroptera. Site

Level

t

NISP

MNI

Galería

GIIIb GIIIa LU6 TD10 TD8-9 TD8 TD7 TD6 TD5 TD3-4 TE14 TE13 TE12 TE11 TE10 TE9 TE8 TE7

1.47 9.80 e 16.18 0.25 0.40 0.35 13.45 22.83 6.14 0.17 0.17 1.42 0.37 2.04 9.58 0.54 1.47

7 75 50 100 19 599 1 1315 336 341 2 0 5 0 44 221 10 64

2 11 7 21 4 51 1 143 60 39 1 0 3 0 5 40 2 14

Sima de los Huesos Gran Dolina

Sima del Elefante

of the excavation performed on each layer. Accordingly, the volume of the samples varied. The small-vertebrate remains were recovered by the screen-washing of the excavated sediment (mesh size from top to bottom of 10, 5 and 0.5 mm). The small fossil remains were picked out under an Olympus SZ61 binocular stereo-microscope. The studied material is stored in the Palaeontology Area of the Earth Science Department of the University of Zaragoza. The identification of the remains, which was based on both cranial and post-cranial diagnostic elements, followed Dodelin
n et al. (2018), (2002), Dupuis (1986), Felten et al. (1973), Gala dulet¸ Menu and Popelard (1987), Pavlini
c and Ðakovi
c (2016), Ra (2003) and Sevilla (1988). The minimum number of individuals (MNI) of each species per layer was obtained in the basis of the body size and life stage of the individuals. The taphonomic analysis includes: (a) calculation of the relative abundance (Ri) of each represented skeletal element per layer, with Ri ¼ (Ni x 100)/(MNI x Ei) where Ni is the number of a specific element in the sample and Ei the number of this element sar, 2010); and per individual (according to Andrews, 1990; Benna (b) scoring of the surface alterations of the remains (following sar, 2010; Ferna
ndez-Jalvo et al., 2016). The Andrews, 1990; Benna life stage groups were distinguished in the most frequent species (Myotis myotis) whenever 10 or more individuals could be determined; these groups were based on the tooth-wear of upper and lower molars (following the three-group classification of Popov and Ivanova, 2002). The following parameters were used to assess palaeobiodiversity from fossil bat asemblages: the total number of species (S) per layer; the evenness (J’) per layer (following Pielou, 1969, 1975); the percentage represented by the predominant species over the total number of individuals per layer (adapted from Medellín et al., 2000); and the number of rare species per layer (counting as rare all those species with less than 10 individuals in all the units of the sequence, adapted from Medellín et al., 2000). The number of thermophilic species per layer was also considered, counting as thermophilic all species belonging to the strictly Mediterranean group of bats described in Hor
a cek et al. (2000).

4. Results and discussion 4.1. Characterization of the fossil bat assemblages Total numbers of remains, MNIs and representative pictures of the bat remains recorded at the Sierra de Atapuerca sites under study are given in Table 2 and Fig. 2. The level that provided the highest richness of bat remains is the Gran Dolina unit TD8, followed by the TELRU units TE7 to TE9 and the Gran Dolina units of TD3-4 to TD6 (Table 1). Myotis myotis is the most frequent and the most abundant species throughout the four studied sites (Table 2). The species composition of the assemblages is based on the almost constant presence of this taxon, which appears throughout the Early and Middle Pleistocene record of Atapuerca (Table 2), together with three other frequent but less abundant species: Rhinolophus ferrumequinum, Rhinolophus mehelyi and Miniopterus schreibersii (Table 2). The remaining associated taxa appear sporadically in some layers, and their remains are scarce (Table 2). The amount of recorded species differs from one level to another. The Gran Dolina units of TD3-4 to TD6 provide the highest species richness (Fig. 3A); the predominance of M. myotis is less evident there and the evenness values of bat assemblages rise (Fig. 3B and C). Evenness values are also high in the Gran Dolina Middle Pleistocene units TD-8 to TD10, and the highest evenness value is recorded at the Sima de los Huesos unit LU6 (Fig. 3C).

4.2. Taphonomic studies and the origin of the accumulation In the sites of the Trinchera system (Sima del Elefante, Gran Dolina and Galería), the abundance of bat remains in every level analysed (Table 1) is relatively low compared to the quantity of other small vertebrate groups. Considering amphibians and reptiles, 39677 elements (MNI ¼ 6162) were recovered from 5.6 t of sediment from a test-borehole in Gran Dolina, comprising TD5 to TD10 (Blain et al., 2008, 2009); the amount of insectivores and rodents recovered from 5.6 t of sediment from the afore mentioned
s et al., 2005, 2011; test-borehole was MNI ¼ 5688 (Cuenca-Besco
pez-Anton ~ anzas and Cuenca-Besco
s, 2002). However, the smallLo vertebrate fossil assemblage recorded in level LU6 of Sima de los Huesos (Cueva Mayor system) shows a similar abundance of flying and non-flying small mammals, if not a slightly higher abundance
s et al., 1997). of bats (Cuenca-Besco The assemblage of recovered and identified fossil bat bones is composed of disarticulated elements from both the cranial and postcranial skeleton. The colours of the remains cover a wide range from white to dark brown. The bones with lighter colours are more frequent in the Gran Dolina and Galería layers whereas the darker ones are in TELRU and Sima de los Huesos. Most of the remains lacks any degree of surface dissolution: only a few isolated specimens display it (less than 0.1% through the TELRU sequence, less than 0.5% through the Gran Dolina sequence, none in the two Galería levels and 2% in the level LU6 of Sima de los Huesos; example of strong dissolution in Fig. 4A). Most of the remains are fragmented, and only a few complete bones (cranial and long bones) were recovered in some levels (Fig. 4B). The relative abundance of different skeletal elements changes along the studied succession. However, mandibles are generally the best represented bone, with an under-representation of postcranial skeleton observed overall, except in level LU6 (Fig. 4C). The age-group pattern for Myotis myotis varies from one layer to another, although all age-groups are represented throughout the sequence. Adults are most numerous along the Gran Dolina sequence (except in TD10) and in the level GIIIa of Galería (Fig. 5). The age-group composition of M. myotis is rather unusual in two levels: in TE9

5 40 2 14 403 44 220 10 64 3100 4 30 4 17 504 4 29 1 8 248 40 187 6 44 2402

1 8 1 4 91

3 3 1 1

5

332 31 41

6 9 1 4 1 4 1 1

1

8

1

16 10 21 5

1 1

2 109

1 20

1 1

1 1 5 3 5 44 14 19

1 2 1 4

7

1

2 1 4 1

1

7 1 15 1 3 5 2 11 7 3 1 2

Sima del Elefante

Sima de los Huesos GranDolina

TD10 TD8-9 TD8 TD7 TD6 TD5 TD3-4 TE14 TE13 TE12 TE11 TE10 TE9 TE8 TE7 TOTAL

1 25

1 4

2

2 2

NISP MNI NISP MNI NISP MNI NISP MNI NISP MNI NISP MNI NISP

GIIIb GIIIa LU6 Galería

2

25

5 2 1

1 2

NISP MNI

14 7 2

MNI

3 2 1

NISP

3 1 1

MNI

8

34

20 3 32 1 72 36 23 1 98 18 529 1 835 266 255 2

1

46 9 6

13

2

5

21 4 51 1 143 60 39 1 100 19 591 1 1258 331 323 2

2 11 7

MNI NISP

7 75 50

MNI NISP MNI

2 11 4

NISP

7 75 38

Total Miniopterus schreibersii Barbastella barbastellus Plecotus austriacus cf. Eptesicus Myotis sp. Myotis nattereri Myotis capaccinii Myotis bechsteinii Myotis myotis Rhinolophus ferrumequinum Rhinolophus mehelyi Level Site

Table 2 Presence/absence of bat species by site and lithostratigraphic unit, the levels of each site are displayed in stratigraphic order (sites correlation in Fig. 1C). NISP: number of identified specimens; MNI: minimum number of individual.


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subadults are clearly predominant and are far more abundant than in the remaining layers studied (Fig. 5); in TD10, subadults represent a relatively high proportion, and old adults become relatively more numerous compared to the older levels of Gran Dolina and to GIIIa (Fig. 5). The bat associations are characterized by a predominance of cave-dwelling species, especially Myotis myotis followed by Miniopterus schreibersii (Table 2), both of which typically live in largecolonies (Dietz et al., 2009; Palomo et al., 2007). Together with the karstic nature of the sites and the scarcity of remains affected by surface dissolution marks (which would indicate digestion,
ndez-Jalvo et al., 2016), this suggests that Andrews, 1990; Ferna these remains most probably result from the natural death of in
n et al., 2016, 2019; Lo
pez-García dividuals living in the caves (Gala et al., 2011b). In the three Trinchera sites (Sima del Elefante, Gran Dolina and Galería), the small quantity of bat remains compared to other groups of small vertebrates (Blain et al., 2008, 2009; Cuenca
s et al., 2005, 2011; Lo
pez-Anton ~ anzas and Cuenca-Besco
s, Besco 2002), as well as the allochthonous origin of the detrital sedi~ a et al., 2015; Rosas et al., ments in all the analysed units (Campan 2006) could indicate that fossil bats underwent different bio
pez-García et al., 2011b) stratinomic processes (Kowalski, 1995; Lo from other small vertebrates. The latter were presumably transported into the inner cave by predators or with the input of sedi
s ments from the outside (Blain et al., 2008, 2009; Cuenca-Besco et al., 2011). The LU6 small-mammal fossil assemblage (Sima de los Huesos, Cueva Mayor system) could also have a multi-factorial origin, and the lower representation of non-flying small mammals might be due to the location of the site within the cavesystem; this is not accessible for owls nor other “common” predators of small mammals. Sima de los Huesos is a deep cavity at a considerable distance from the entrance area, so a lesser amount of exogenous sediment input would be expected. Finally, there is a selective underrepresentation of particular skeletal elements of bats in the various levels of the four sites with mandibles usually showing the highest relative abundance (except for LU6, Fig. 3C), a fact that might be explained by their higher potential durability
pez-García et al., 2011b). The different degrees of destruction (Lo undergone by the various skeletal elements, together with the scarcity of complete bones (Fig. 3B), might be caused by transport or diagenetic processes, although some methodologic bias should also be considered (screen-washing could have caused the destruction of some fragile parts).

4.3. Palaeoclimatic and palaeoenvironmental affinities of the bat assemblages The bat species recorded at these four sites of the Sierra de Atapuerca still inhabit the Iberian Peninsula today. The extant representatives of three of these species currently show strong thermophilic affinities: Rhinolophus mehelyi, Myotis capaccinii and Miniopterus schreibersii (Hor
a cek et al., 2000). Their presence at Atapuerca varies through the levels studied. R. mehelyi and M. schreibersii occur in most of the analysed levels except in TE14, TD8-9 to TD10 and GIIIa to GIIIb (Table 2). The highest abundance of these thermophilic species is recorded in levels TD5 and TD6 (Fig. 3E). The occurrence of higher numbers of rare species in the post-Jaramillo Early Pleistocene units of the sequence (TD3-4, TD5 and TD6, Fig. 3E) than in other, older and younger levels is also noteworthy. These three levels are remarkable for the occurrence of the only bat species in the assemblage currently linked to colderclimate conditions: Barbastella barbastellus (Dietz et al., 2009; Kowalski and Ruprecht, 1981; Palomo et al., 2007; Sevilla, 1988). Most of the recorded species are strictly or preferentially cave-

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Fig. 2. Examples of cranial remains of order Chiroptera from the studied sites in Atapuerca. A: upper canine (Left), Rhinolophus ferrumequinum (TD5); B: mandible (L) with p3 to m3, R. ferrumequinum (TE9); C: maxilla fragment (L) with M2-M3, Rhinolophus mehelyi (TD6); D: rostrum with P3 to M3, Myotis myotis (GIII); E: maxilla fragment (Right) with P4 to M1, M. myotis (TD6); F: mandible (L) with m2 to m3, M. myotis (TD5); G: mandible (L) with m1-m3, Myotis capaccinii (TD6); H: mandible fragment (L) with p2-p3, M. capaccinii (TD6); I: humerus distal epiphysis (R), M. capaccinii (TD6); J: maxilla fragment (R) with M1 to M2, Plecotus austriacus (TD8); K: m1 (L), Barbastella barbastellus (TD5); L: humerus distal epiphysis (R), B. barbastellus (TD6); M: m2 (R), Miniopterus schreibersii (LU6)N: mandible (L) with m2-m3, M. schreibersii (TD6). Scale ¼ 1 mm.

dwellers (R. mehelyi, Rhinolophus ferrumequinum, M. myotis and M. schreibersii), and others among them are occasionally found in caves (the small-sized Myotis, i.e. M. bechsteinii, M. capaccinii, Myotis nattereri and probably Myotis sp., as well as Plecotus austriacus) (Dietz et al., 2009; Palomo et al., 2007). Specifically, the two most frequent bats in the associations, M. myotis and M. schreibersii, are nowadays known to group in large colonies (for example, in the Iberian Peninsula the maternity roosts of M. myotis usually involve about 1000 individuals, exceptionally reaching values as high as 8000; there are extant data for M. schrebersii forming hibernation colonies in the north of Spain of about 70000 individuals; Dietz et al., 2009; Palomo et al., 2007). 4.4. Palaeoenvironmental and palaeoclimatic changes as possible reasons for fluctuations in bat assemblages The main tendency observed through the Early Pleistocene fossil bat record is that the species richness of bats increases at the end of this period, being moderate in the TELRU levels of Sima del Elefante (pre-Jaramillo Early Pleistocene) and reaching the maximum in levels TD5 and TD6 of Gran Dolina (the post-Jaramillo Early

Pleistocene), with at least 10 species (Fig. 3A). The numbers of both thermophilic and rare bat species increase concurrently (Fig. 3D and E). Other palaeoclimate proxies, such as pollen, herpetofauna and small and large mammals, point to warmer and more humid conditions than nowadays for the TELRU levels (Blain et al., 2010;
s and García, 2007; Cuenca-Besco
s and Rofes, 2004; Cuenca-Besco Ll acer et al., 2005; van der Made et al., 2003; Rofes and Cuenca
s, 2006, 2009). As regards units TD5 and TD6, different Besco palaeoclimatic approaches show discrepancies in characterizing
n, 1989) indicates cold and this period. Pollen analysis (García-Anto arid conditions from unit TD5 to the top of TD6, when a change to wetter and warmer conditions is detected, whereas non-pollen
sito et al., 2017) suggest a decrease in local palynomorphs (Expo humidity at the top of TD6. The herpetofauna assemblage (Blain et al., 2008, 2009) indicates wetter conditions for TD5 than the above approaches, with warmer temperatures at the base than at the top of the unit; in unit TD6 it shows an increase in aridity, with temperatures warmer towards the top of the unit. Finally, the non
s et al., 2005, flying small-mammal assemblage (Cuenca-Besco 2011) indicates a change from wet to dry conditions from the base to the top of unit TD5, and the occurrence of a warm, wet climate at


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two cold, arid pulses, in unit TD8-9 and at the top of unit TD10. In the general palaeoclimatic context of the Iberian Peninsula, the Middle Pleistocene is a highly variable period. Between 500 ka and 250 ka, extreme cold events occurred in the Iberian Peninsula mainly during glacial periods, alternating with intervals of warmer temperatures, which during MIS 9 reached higher values than nowadays (Fig. 6A; Rodrigues et al., 2017). The occurrence of three extreme cold events in the Iberian Peninsula at about 450, 350 and 275 ka (Fig. 6; Rodrigues et al., 2017) could explain the impoverishment of fossil bat faunas in the top units of the Gran Dolina sequence and levels GIIIa and GIIIb of Galería. However, it is intriguing why bats would have been unable to recover during the intermediate warmer periods, when other small vertebrates did.

4.5. Anthropic influence as a possible reason for fluctuations in bat assemblages

Fig. 3. Characterization of the fossil bat assemblages through the stratigraphic record of Atapuerca. A: species richness (S, species number). B: relative abundance (%) of the predominant species, Myotis myotis. C: evenness of the associations (J0 , evenness). D: total number (n) of rare (rar) species. E: total number (n) of thermophilic (therm) species.

the top of unit TD6. The only bat species indicating colder conditions in these two units is Barbastella barbastellus (see chapter 4.3). Yet this species is found in exactly the same archaeological levels or “tallas” as the species belonging to the thermophilic group (not only the frequent R. mehelyi and M. schreibersii, but also the rarer Myotis capaccinii; Gal
an et al., 2019). In the palaeoclimatic context of the Iberian Peninsula, the period between 1 Ma and MIS 22 (~900 ka) is characterized by shorter, less severe glacial periods (Fig. 6 A; Rodrigues et al., 2017). This would be approximately contemporaneous with levels TD3-4 and TD5 and could explain the rich and diverse fossil bat assemblages recorded there, although fluctuations detected through these levels with other proxies are not detected on bats. A colder phase started at about 900 ka to 850 ka (Fig. 6A; Rodrigues et al., 2017), approximately contemporaneous with level TD6 (according to age data provided by Arnold et al., 2014; Moreno et al., 2015) or slightly posterior (according to Berger et al., 2008). The rich and diverse fossil bat assemblages recorded at TD6 are in agreement with a general context of favourable climate conditions, though. The main tendency observed through the fossil bat record is a clear decreases of bat species richness from the Middle Pleistocene on. Thermophilic species disappear concomitantly with the decrease in diversity in the Gran Dolina unit TD10 and levels GIIIa and GIIIb of Galería (Fig. 3). Other palaeoclimatic approaches show some discrepancies in characterizing this period. Pollen analysis
n, 1989) suggests a change to cold and arid conditions (García-Anto from the base to the top of unit TD10. Non-pollen palynomorphs
sito et al., 2017) point to arid conditions from unit TD8-9 to (Expo the base of TD10. Herpetofaunal assemblages (Blain et al., 2008, 2009) suggest a change to cold conditions from the base to the top of unit TD10, in agreement with pollen analysis but pointing to drier conditions at the base of unit TD10. Finally, non-flying small
s et al., 2005, 2011) indicate mammal assemblages (Cuenca-Besco

Notwithstanding the climatic fluctuations discussed above, both the difference in response to climate changes recorded between bats and other small vertebrates, and the differences between the fossil bat assemblages in the partially synchronous units LU6 (Sima de los Huesos) and TD10 (Gran Dolina) might also have been a result of anthropic factors. Rhinolophus mehelyii, Myotis myotis and Myotis schreibersii appear in level LU6, an assemblage with a high evenness value (Fig. 3C), Sima de los Huesos being a cave in an inner karst zone that was never occupied by humans (although several corpses were deposited there by other humans according to Arsuaga et al., 1993, 1997, 2014; among others). By contrast, in TD10, where intensive human occupation occurred (García-Medrano,
et al., 2013; among 2011; García-Medrano et al., 2015; Olle others), M. myotis appears as a strongly predominant species accompanied by a few remains of R. ferrumequinum, whereas R. mehelyi and M. schreibersii are absent. Extant M. myotis are frequently known to use human constructions as roosting places (Dietz et al., 2009). This species is probably more tolerant of a human presence since it has been able to adapt, whereas R. mehelyi and M. schreibersii are very sensitive to human disturbance. A further feature that can be used as a tool to explore homininbat interactions is the seasonality inferred from demographic patterns in M. myotis, the predominant bat species along the Early and Middle Pleistocene record of the Sierra de Atapuerca, appearing in almost every level. In the pre-Jaramillo Early Pleistocene level TE9, the age-group pattern observed for this species is largely dominated by subadults (Fig. 5). This suggests that the cave was used as a
pez-García et al., 2011b) during the nursery roost (according to Lo warm season (Dietz et al., 2009; Palomo et al., 2007), a time when colonies are especially vulnerable. The situation is different in the M. myotis assemblages recorded along the Gran Dolina sequence. Here the age-group composition is quite constant through units TD3-4 to TD6, with a largely predominant adults, less frequent subadults and very scarce old adult individuals (Fig. 5). In the Middle Pleistocene level TD8 this pattern varies slightly; although adults remain largely predominant, there is a reduction in the representation of subadults and a slight increase in old adults. These adult-dominated patterns are not consistent with the expected mortality rate for either nursery or hibernation colonies
pez-García et al., 2011a, b). In the absence of pre(according to Lo vious citations of similar cases, we here propose that it could reflect a full-year occupation of the cave including nursery and hibernation periods. The M. myotis assemblages show a clearly distinct pattern in the Middle Pleistocene level TD10. Adults are comparatively rare, whereas subadults dominate and old adults are more abundant than in younger levels (Fig. 5), suggesting the seasonal use of the cave as a hibernation roost during winter (according to

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n et al. / Quaternary Science Reviews 226 (2019) 106018 J. Gala

Fig. 4. Taphonomic remarks. A: example of strong surface dissolution on the distal epiphysis of a humerus of Miniopterus schreibersii, TD6 (Scale ¼ 1 mm). B: Relative frequency of complete and incomplete bones (excluding teeth) recovered by layer. C: Relative abundance (Ri) of bat skeletal elements by site and level, the most abundant element in all the layers shaded in grey; levels TE11, TE13 and TD7 are excluded. Anatomical abbreviations: mx, maxillae; md, mandibles; m, molars; bu, tympanic bullae; clav, clavicles; sca, scapulae; hu, humeri; ra, radiuses; mtcp (IIeV), 2nd to 5th metacarpals; fe, femurs; ti, tibiae.


pez-García et al., 2011b). Finally, in level GIIIa of Galería old Lo adults are not represented and adults are largely predominant. Considering the low abundance of bat remains in this level, this pattern is interpreted here as reflecting the occasional use of the cave, mainly by non-reproductive individuals. There is evidence of a human presence at the Sima del Elefante cave in sublevel TE9C, although these early European hominins probably settled at a nearby location rather than within the cave (Carbonell et al., 2008; Huguet et al., 2017; among others). The occupational pattern of M. myotis in level TE9 (including TE9C,
n et al., 2016), which is presumably indicative of a summer, Gala nursery roost, suggests that hominin activities did not interfere significantly with the bat colonies at this time. Similarly, the high bat palaeobiodiversity and the proposed full-year occupation

pattern of M. myoits for the post-Jaramillo Early Pleistocene units of Gran Dolina suggest that the hominin activity recorded in units
et al., TD3-4 and TD6 (see Fig. 6H and I; Carbonell et al., 1995; Olle
et al., 2014; among others) exerted no notable in2013; Saladie fluence on the bat palaeocommunities roosting there, even though there is evidence of hominin groups occupying Gran Dolina as a home base at least in level TD6-2. These Early Pleistocene, Mode 1 technology bearer hominins from Sima del Elefante and Gran Dolina did not affect significatively the coeval bat communities, according to bat fossil assemblages. A different picture is observed in levels TD10 and GIIIa. There is numerous archaeological evidence of high-intensity use of the Gran Dolina cave as a human campsite at the top of unit TD10, where hominins lived and carried out a multiplicity of domestic activities


n et al. / Quaternary Science Reviews 226 (2019) 106018 J. Gala

Fig. 5. Age-group composition of the Myotis myotis assemblages by level. Percentage (%) represented by each age-group according to tooth-wear: subadults, adults and old adults. Stratigraphic levels with less than 10 individuals available for analysis were excluded.

9

res et al., 1999, 2013; García-Medrano, 2011; García(Falgue
et al., 2013). However, there is only Medrano et al., 2015; Olle sporadic human occupation in the more recent unit GIII (GarcíaMedrano, 2011; García-Medrano et al., 2014, 2015). In both cases the archaeological record shows human populations with Mode 2 technology. The M. myotis occupational pattern recorded in TD10 changes for the first time in the Gran Dolina sequence from a presumed full-year occupation to a winter, hibernation roost (Figs. 5 and 6F). This change in the use M. myotis made of the cave can be interpreted as a response to the human presence; i.e. bats and humans could have occupied the cave alternately at different times of the year (Rossina, 2006). However, this occupational pattern could also reflect a harshening of the climate, as M. myotis is able to endure lower temperatures when hibernating, whereas it chooses warmer roosts for nursery: the current maximum altitude reached by this species in the Iberian Peninsula when hibernating is several hundred metres above the highest recorded nursery colony (Palomo et al., 2007). In this regard, is most interesting to note that there is archaeological evidence of a human seasonal use of Gran Dolina cave, at least in sublevel TE10.2, when hominis did not use the cave in winter (Rodríguez-Hidalgo et al., 2016). The M. myotis occupational pattern recorded in GIIIa, interpreted here as an occasional refuge for non-breeding individuals, could be explained as a result of anthropic influence, as hominis would have use the total internal space of the cave as occasional settlement in this level

Fig. 6. Synthetic overview of the Iberian palaeoclimatic context, bat palaeobiodiversity and human presence at the Sierra de Atapuerca Early and Middle Pleistocene. A: sea-surface temperature of the SW Iberian Margin; in blue, values under 14  C, indicative of mean glacial sea-surface temperature; in red, values above 18.5  C, Holocene sea-surface temperature (from Rodrigues et al., 2017). B: presence of the four most frequent bat species Rhinolophus mehelyi, Rhinolophus ferrumequinum, Myotis myotis and Miniopterus schreibersii. C: total number of species (S) of the bat assemblages. D: evenness (J0 ) of the bat assemblages. E: total number (n) of thermophilic (therm) and rare (rar) bat species. F: lithostratigraphic units displayed in chronological order (sites stratigraphy and correlation in Fig. 1C). F: inferred cave-occupation pattern for M. myotis. G: human cave-occupation pattern, according to Arsuaga et al. (2014), Carbonell et al. (2008), García-Medrano et al. (2017), among others. H: human industry modes recorded in the analysed levels ac
et al. (2013), among others. (For interpretation of the references to colour in this figure legend, the reader is cording to Arsuaga et al. (2014), García-Medrano et al. (2015), Olle referred to the Web version of this article.)

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n et al. / Quaternary Science Reviews 226 (2019) 106018 J. Gala

(García-Medrano et al., 2017). But again, the use of the cave interpreted here from bat mortality pattern could also be explained as an effect of climate harshening, which would have restrained the formation of nursery colonies.

5. Conclusions The bat fossil record from the Early and Middle Pleistocene of the Sierra de Atapuerca has provided fossil assemblages that share some common features. For all the four sites analysed in this work (Sima del Elefante, Gran Dolina, Trinchera-Galería and Sima de los Huesos), the bat accumulation was produced independently of the assemblage of the other, non-flying small vertebrates. The great majority of the preserved bat remains belong to individuals that roosted and died within the karstic cavities where the palaeontological sites were formed. This is in agreement with the fact that the most frequently recorded species at all the sites are four mainly or strictly cave-dwelling bats: Rhinolophus ferrumequinum, Rhinolophus mehelyi, Myotis myotis and Miniopterus schreibersii. These species all inhabit the Iberian Peninsula nowadays and are part of an association with so-called Mediterranean affinities. Along the Early and Middle Pleistocene sequence of the Sierra de Atapuerca, two main sections can be distinguished on the basis of the bat fossil record. The first is characterized by a relatively high abundance of bat remains and high bat palaeobiodiversity, where a maximum of ten species are recorded; this comprises the Early Pleistocene levels of Sima del Elefante and Gran Dolina (especially TD5 and TD6) and level TD8 of this later site, which is Middle Pleistocene in age. The second section is characterized by a general decrease in bat remain richness as well as a pronounced impoverishment of the bat palaeocommunities towards the upper levels of the Gran Dolina site and levels GIIIa and GIIIb of Galería, where the four most frequent species appear barely represented. M. myotis is the only bat species with a constant presence throughout the Atapuerca sequence, including both the less diverse levels and the richer ones. This allowed us to study it from a demographic point of view, analysing the changes in the occupational pattern of the caves according to age-groups. Two different patterns were detected. A seasonal or full-year occupation of the cave, including nursery periods, is inferred for M. myotis concurring with the highpalaeobiodiversity section of the sequence (Early Pleistocene levels plus TD8). On the contrary, a seasonal or occasional use of the cave, excluding nursery periods, is inferred for M. myotis concurring with the low-palaeobiodiversity section (Middle Pleistocene). For the Early Pleistocene plus TD8 section, the bat fossil record indicates favourable environmental conditions. Not climate fluctuations are detected on bat assemblages (as they are by other proxies), neither the hominin presence shows any impact on the bat assemblages in these levels. The use of the sites by humans must be considered non-invasive there. On the other hand, Middle Pleistocene bat fossil record from 500 ka on indicates unfavourable environmental conditions and a change in caves-use. The succession of extreme cold events between 500 and 250 ka could explain the impoverishment of fossil bat faunas as well as the changes in caves-use to some extent. However, some features of bat assemblages at these levels, such as differences in species composition between synchronous levels (Sima de los Huesos level LU6 and Gran Dolina level TD10), the inability of bat palaeocommunities to recover during intermediate warmer periods as other small vertebrates did, or the seasonal alternation between hominis and humans detected at TD10, suggest that anthropic disturbance could have also play a significant part. The use of the sites by humans with a more advanced technology could have determined the decline of Middle Pleistocene bat palaeocommunities of Atapuerca.

Acknowledgments This work has been supported by MINECO Projects CGL201238434-C03-01, CGL2015-65387-C3-2-P (MINECO/FEDER) and
n del CGL2013-46169 C2-1-P, and by Grupos de Investigacio
n E18_17R: GRUPO DE REFERENCIA ARAGOGobierno de Arago
SAURUS: RECURSOS GEOLOGICOS Y PALEOAMBIENTALES. J. G. and C. N.-L were recipients of a Ph. D. fellowship from the Aragon Government, co-financed by the FSE at the early stages of this work.
n y Cajal contract (RYCJ.M. L.-G has been supported by a Ramo 2016-19386), with the financial sponsorship of the Spanish Ministry of Science, Innovation and Universities. We would like to acknowledge R. Glasgow who corrected the English text, as well as the valuable comments and suggestions provided by the reviewers P. Sevilla and L. Maul. References

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