Beavers (Castoridae, Rodentia, Mammalia) from the Quaternary sites of the Sierra de Atapuerca, in Burgos, Spain

Quaternary International xxx (2015) 1e15

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Beavers (Castoridae, Rodentia, Mammalia) from the Quaternary sites of the Sierra de Atapuerca, in Burgos, Spain

s a, *, Jordi Rossel Ardevol b, c, Alvaro Gloria Cuenca-Besco Morcillo-Amo a,
María Angeles Galindo-Pellicena d, Elena Santos d, Raquel Moya Costa a a

Aragosaurus-IUCA, Departamento de Ciencias de la Tierra, Facultad de Ciencias, Universidad de Zaragoza, c. Pedro Cerbuna 12, 50009 Zaragoza, Spain  de Paleoecologia Humana i Evolucio
Social, Campus Sescelades URV (Edifici W3), 43007 Tarragona, Spain IPHES, Institut Catala  ria, Universitat Rovira i Virgili (URV), Avinguda de Catalunya 35, 43002 Tarragona, Spain Area de Prehisto d
n y Comportamiento Humanos, C/Monforte de Lemos 5, pab. 14, 28029 Madrid, Spain Centro Mixto UCM-ISCIII de Evolucio b c

a r t i c l e i n f o

a b s t r a c t

Article history: Available online xxx

The Eurasian beaver, Castor fiber is known from the Pleistocene in Europe, although there are references to the presence of the genus Castor since the Miocene, ca. 10 Ma. Beavers are present in the Iberian Peninsula since the Pliocene, though the first appearance of Castor fiber took place in the Early Pleistocene levels of the localities of the Sierra de Atapuerca, where the fossil beaver remains are found in the lower levels of Sima del Elefante and Gran Dolina (Early Pleistocene), Galería de las Estatuas (Late
n (Holocene). The presence of fossil beavers suggests humid and mild climatic Pleistocene) and Portalo conditions in the Early Pleistocene levels of Gran Dolina and Sima del Elefante. During the Middle Pleistocene, although conditions for beavers seemed favourable, they disappeared from Atapuerca, appearing again during the Late Pleistocene and the Holocene. © 2015 Elsevier Ltd and INQUA. All rights reserved.

Keywords: Sierra de Atapuerca Spain Quaternary beavers Castor fiber

1. Introduction The Family of the Castoridae, commonly known as beavers, comprehends the most aquatic and large rodents from Eurasia (Crusafont and Villalta, 1948; Freye, 1978; Antunes, 1989; Hugueney, 1999; Barisone et al., 2006). The Castoridae appeared during the Late Eocene in North America (Korth, 2008; Rybczynski et al., 2010) and the Oligocene in France (Hugueney, 1999). Since their origin, the beavers have being restricted to the Northern Hemisphere. Today, beavers are represented by the genus Castor only, although in the Eurasian Miocene and up to the late Pleistocene, the group had a higher taxonomic diversity (Crusafont and Villalta, 1948; Aldana Carrasco, 1992; Hugueney, 1999, 2004; €rs et al., 1998; Lopatin, 2003; Barisone et al., 2006; CasanovasMo € rs, 2008; Vilar et al., 2008; García-Alix et al., 2007; Stefen and Mo € rs and Stefen, 2010; Erbajeva and AlexRekovets et al., 2009; Mo eeva, 2013; Rook and Angelone, 2013). The extant beaver, genus Castor is present in Eurasia (Germany) since the late Miocene, ca.

* Corresponding author.
s). E-mail address: [email protected] (G. Cuenca-Besco

10 Ma (Hugueney, 1999; Rekovets et al., 2009). During the Quaternary there were two beaver species in Europe, Castor plicidens and C. fiber, both morphologically related. Additionally, the beavers are specialized mammals with concrete ecological preferences; usually related to aquatic environments surrounded by abundant arboreal vegetation, and so seems too happened in the past, such as C. plicidens from the lignites of the Early Pleistocene from Pietrafitta in Italy (Barisone et al., 2006), the Pliocene of the lacustrine sediments of the Baikalian Region (Erbajeva and Alexeeva, 2013), and the Pleistocene of Saint Vallier in France (Hugueney, 2004). The extant beaver from Eurasia, Castor fiber, needs a mix of running and still waters, of about 2 m in depth or more, never completely dry, nor completely frozen, and sur~ a et al., 2004; Campbell-Palmer et al., 2012; rounded by forests (Cen Perfect et al., 2015). This made these aquatic mammals of great interest for paleoecological reconstructions. The aim of this paper is characterize and allocate the beavers from Atapuerca to the Castor fiber species. The status of C. plicidens as a valid taxon is maintained, and an overview of the taxonomy and paleogeography of C. fiber in the Iberian Peninsula will be displayed. Its paleoecological significance will be weighed with further paleoecological proxies in Atapuerca. It is important to

http://dx.doi.org/10.1016/j.quaint.2015.10.072 1040-6182/© 2015 Elsevier Ltd and INQUA. All rights reserved.


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remark, as Hugueney (1999) asserts that beavers are usually found in monospecific assemblages, with determination of age difficult. Also, she remarks that beavers are rarely found in karst localities. Consequently, our goal here is presenting the first well dated and stratigraphically situated cranial material of the Pleistocene beavers recovered during the field excavations from the archaeological and paleontological cave sites from the Quaternary from the Sierra de Atapuerca, Burgos, Spain. 2. The fossil record of Castoridae in the Iberian Peninsula Beavers are present, though scarce, during the Miocene in Spain
and Lo
pez(Crusafont and Villalta, 1948; Weerd, 1976; Sese
and Soto, 1981; Sese
, 1989; Aldana Carrasco, Martínez, 1981; Sese 1992; Garcia-Alix et al., 2007; Casanovas-Vilar et al., 2008; Casanovas-Vilar and Alba, 2011). During the Pliocene the extant genus Castor appears, and its oldest record is from the sites of
lago 5 (Friant, 1964; Sese
, 1989). Castor appeared Villarroya and Hue probably when the wet conditions increased after the aridity maximum of the Turolian (García-Alix et al., 2007). Then, it vanishes during the end of the Pliocene. Probably its disappearance was related with several aridity peaks such as recorded in the Zújar section. Beavers only return during the Holocene in Southern Spain. The extant species C. fiber appeared in the north of the Iberian Peninsula, during the Early Pleistocene, in the localities of Sima del Elefante and Gran Dolina in the Sierra de Atapuerca. The Early Pleistocene levels from Atapuerca, with beaver remains, are the lower red unit of Sima del Elefante (TELRU, level TE9), and the lower
s levels of Gran Dolina levels TD5, TD6 (Gil, 1988; Cuenca-Besco et al., 1999a, 2005, 2010b, 2013, 2014, 2015a, b). The age of TELRU
s et al., 2013, 2015a, b). The is around 1.2e1.4 Ma (Cuenca-Besco youngest age provided for the level TD6 from Gran Dolina is 846 ± 57 ka (Arnold et al., 2014). When Gil (1988) described the first

fossil remains of beavers from Gran Dolina, the geological age of TD6 was younger than it is considered today. Noteworthy is the absence of the beavers in Atapuerca during the Middle Pleistocene, absent from Galería-Zarpazos, the upper levels of Gran Dolina TD10 and the upper levels of Sima del Elefante TE18-19. We have demonstrated in previous works that these levels
s may correspond to drier and less forested periods (Cuenca-Besco
pez-García et al., 2005, 2010b; Blain et al., 2009, 2010, 2013; Lo et al., 2011). Therefore, we interpret the local disappearance of the beavers from Atapuerca during the Middle Pleistocene as a matter of habitat loss, probably due to degradation of forests and water environments twisted by harsh climatic conditions. We do not perceive biases in the fossil record of the middle Pleistocene levels from Gran Dolina, Sima del Elefante or Galería-Zarpazos sites
s et al., 1999a, 2005, 2011; Rodriguez et al., 2011, (Cuenca-Besco 2014). Later, the beaver appear once more in the Late Pleistocene from Atapuerca, in the site of Galeria de las Estatuas (GE II), and in
n. Modern and comprehensive the Holocene levels from Portalo reviews of some of the Atapuerca sites are Carretero et al. (2008), res et al. (2013), Arnold et al. (2014), and Cuenca-Besco
s Falgue et al. (2015a,b). Beavers are present in the Middle Pleistocene of the Iberian Peninsula, in the locality of Aridos 1 (Arganda, Madrid), the only
pez-Martínez, 1980, this record of beavers of this age in Spain (Lo work). The late Pleistocene beaver populations seem to rise again in the Iberian Peninsula, where in addition to the above quote from GEII, it appears in several localities such as Caldeirao (Portugal), Cova Negra (Valencia), Los Casares (Guadalajara), Lezetxiki (Alava), Las Hienas (Las Caldas, Cantabria), among others. Beavers seem to recover and expand during the Holocene in the Iberian Peninsula, being last recorded in archaeological sites of
n in Atapuerca and Gava
, in Catalunya Roman age, such as Portalo (Fig. 1, Table 1).

Fig. 1. Situation of the localities from the Iberian Peninsula with fossil remains of Castor fiber. The white figures correspond to Early Pleistocene; black, Middle Pleistocene; dark grey, Late Pleistocene, and light grey, Holocene.


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Table 1 The fossil record of Castor fiber in the Iberian Peninsula. The Castor species from Villarroya, Huelago and Tortosa remain uncertain. Data from Liesau von Lettow-Vorbeck (1998), authors in table, and this work. Age Holocene

Late Pleistocene

Middle Pleistocene Early Pleistocene

Locality

Author(s)

Roman, IVeVI century Roman Roman/Iron Iberic

Gav
a Bilbilis Portalon 1/2 Ronda

Nadal Lorenzo, 2000 Liesau von Lettow-Vorbeck 1998 this work Riquelme, 1995

Iron Iron Iron Bronze

Soto Medinilla Ucero Era Alta Portalon 3/4

Liesau von Lettow-Vorbeck, 1998

Bronze Bronze Bronze Neolithic Neolithic Meso-Neolithic Upper Paleolithic

B. del Negro Perales del Rio Sima del Ruidor V.N. S. Pedro ~a La Pen C.B. Fondo Olazagutia, Coscovilo

Liesau von Lettow-Vorbeck 1998

Azilien Azilien Magdalenien? Solutrean Aurignacien Aurignacien Mousterian Mousterian Mousterian Mousterian Mousterian Mousterian Mousterian Mousterian Mousterian Acheulian 0,9 1,2

Dufaure Zatoya C. Blanca Caldeirao Gatzarria Lezetxiki C. Hienas C. Figuras Los Casares C. Negra GEII C. Millan Muricecs Olha Pinilla Aridos 1 TD 6 TE 9 Tortosa
lago Hue Villarroya

Liesau von Lettow-Vorbeck 1998

Pliocene

this work

Antunes 1989 Liesau von Lettow-Vorbeck 1998 Liesau von Lettow-Vorbeck 1998 Crusafont and Villalta 1948

Liesau von Lettow-Vorbeck 1998 Antunes 1989 Liesau von Lettow-Vorbeck 1998 Altuna 1972
and Soto 1981 Sese Liesau von Lettow-Vorbeck 1998 Altuna 1972 Villaverde Bonilla and Martí Oliver, 1984 this work Liesau von Lettow-Vorbeck 1998 Liesau von Lettow-Vorbeck 1998 Altuna 1972 Liesau von Lettow-Vorbeck 1998
pez-Martínez, 1980 Lo Gil 1988, this work this work Aldana Carrasco 1992
and Soto 1981 Sese Friant 1964

Nonetheless, in several regions of Europe it survives until the present day. There are references to the presence of beavers in the Ebro River today (La Rioja, Navarra, and Zaragoza), though they ~ a et al., were purportedly introduced by modern humans (Cen 2004). 3. Material and methods Given their meso-size, beavers are found during the archaeological digging as well as during the washingesieving of the sediments from the excavations of Atapuerca (Figs. 2e13). The terms used in the descriptions of the teeth and mandibles of Castoridae (Figs. 4e8, and text) are partially extracted from Hugueney (1999), €rs and Stefen (2010). Korth, 2008, Barisone et al. (2006), and Mo Following Crusafont and Villalta (1948) and Weerd (1976) in the Castoridae premolars and molars, the folds at the lingual and labial sides are named striidae for lower, and striae for upper cheek-teeth; while in the occlusal surface these are named flexids for the lower and flexae for the upper cheek-teeth. Isolated enamel islands on the occlusal surface are fossettids in the lower and fossettes in the upper cheek-teeth. In the present work we use the term digastric eminence (DE), the insertion crest for the muscle digastricus, for the small flange immediately posterior to the distal end of the mental symphysis (Figs. 6 and 7); being the symphyseal eminence
s et al. (2010a). This term is used in Repenning (1968), Cuenca-Besco instead of the deep mandibular break of the ventral margin of the €rs and mandible of Barisone et al. (2006), or the chin process of Mo Stefen (2010). Also in the description of the mandible, we use the

Fig. 2. The Quaternary sites from the Sierra de Atapuerca (Burgos, Spain) with Castor fiber.


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Fig. 3. Stratigraphy of the site of Portalon (Atapuerca, Burgos) with Castor fiber fossil remains: a left P4 (CMI-A8-25-2) and a left hemimandible (Ata00ATPLimpExcW). The asterisk (*) point to the stratigraphic position of the left hemimandible, HLUBU.

terms: boundaries of the masseteric fossa (fma), the upper masseteric crest (uefma), and the lower (lefma). Notes on the differences among Hystricidae (porcupines) and Castoridae are based on the works of Sulimsky (1960), Hugueney (1999), Sen (2001), and Vekua et al. (2010). The measurements are given in mm. The measurements of the mandible have been taken, the high from the tip of the DE to the most mesial alveolar limit of the chewing teeth, the total alveolar length, and the length of the diastema. The Length and Width of the incisor and the cheek teeth (LxW) have been taken in the occlusal surface with a precision calliper. Some measurements were taken with a Mitutoyo digital calliper model No. CD-8’’CX, and they are given in millimetres. Because of the large size of some specimens, they have been photographed with a digital camera Nikon Coolpix 3100 and then measured again. Later, we photographed and measured the teeth, both isolated and in mandible, with the Image Acquisition Software LCmicro (Windows system), with a LC20 camera attached to an SZ61 Olympus microscope. Some of the specimens are kept in the Museo de Ciencias Naturales de la Universidad de Zaragoza (MPZ). Nomenclature of the anatomical terms and measurements are figured in Figs. 4e8.

3.1. Abbreviations Anatomical e Md, Mandible; fma, masseteric fossa; the boundaries of the fma are formed by two crests, uefma, upper masseteric crest; lefma, lower masseteric crest; DE, digastric eminence; Mx, maxilar; I, P, M, in capital letters are for the upper dentition, incisor, premolar and molar respectively. Lower case letters, i, p, m are for the lower dentition. The anatomical terms of the mandible and dentition are a compilation of terms used by €rs and Stefen 2010 (See Repenning (1968), Hugueney (1999), Mo Figs. 4e8). Institutional and field labels e MPZ, Museo Paleontologico y de Ciencias Naturales de la Universidad de Zaragoza; HLUBU (Human laboratory of University of Burgos).

4. Results Systematic Paleontology. Order Rodentia Bowdich, 1821 Family Castoridae Hemprich, 1820 Note on the differences between Castoridae and Hystricidae.


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Fig. 4. Castor fiber from Portalon (Atapuerca, Burgos). The left P4 (CMI-A8-25-2) recovered from historic Level 1e2 of Iron/Roman Age.

Even though the rodent families of beavers (Castoridae) and porcupines (Hystricidae) are not phylogenetically related, their size and dentition are similar. In some cases, the isolated fossil teeth may be difficult to attribute to family (Lopatin, 2003). Moreover, they are usually found in the same localities, while not necessary in the same levels, such as it is the case in the Atapuerca sites. Hence, we present here a short report on the differences and similarities of the largest rodents from Atapuerca, the genus Castor and Hystrix because they have similar size, and the premolars and molars have

a similar occlusal surface, especially in specimens of intermediate to senile state of wear. The differences between the mandibles of the rodents from both families are: the Hystricidae have stronger, deeper, and wider lower masseteric fossa, a single deep and large mental foramen that is situated more dorsally than in the Castoridae mandible; which in turns may have two foramina instead of a single one (compare the mandibles of both taxa in Hugueney, 2004; Rook and Sardella, 2005). See the strong mental foramen of Hystrix from i.e. the

Fig. 5. Castor fiber from the Early Pleistocene layers of Gran Dolina and Sima del Elefante (Atapuerca, Burgos). A. Right M3 from Gran Dolina level TD6 (Ata95td6t40th17, MPZ 2015/ 1542). B. Right M3 from Sima del Elefante level TE9 (Ata02TE9bl30z580-590, MPZ 2015/1544).


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Fig. 6. Nomenclature of the mandible of Castor fiber from the Early Pleistocene layers of Gran Dolina. Right mandible in medial view. TD6 08.

Fig. 7. Nomenclature of the mandible of Castor fiber from the Early Pleistocene layers of Gran Dolina. Right mandible in medial view. TD6 08.

Pliocene of Chaingzauk, Myanmar (Nishioka et al., 2011); or from the Early Pleistocene of Dmanisi (Vekua et al., 2010). The DE is situated in the ventral margin of the mandible as described above: it is larger and more ventral projected in Castoridae, though it turns out to be stronger with the age (Frahnert, 2000) than in Hystricidae (see Figs. 6, 7, 10 and 11, this work, and the X-ray images in Stefen et al., 2011). Moreover, the lefma, well-marked in the lateral side of the mandible, is more ventrally protruded in Hystrix than in Castor. This character made the ventral border of the mandibular corpus of the Hystrix species shorter and with a ventrally emarginated shape, whereas in the species of Castor the ventral border is nearly straight and horizontal (except for the digastric eminence). The incisors or gnawing teeth of Hystrix have a round enamel surface (Sulimsky, 1960) (anterior or labial side of the incisor) in occlusal view, whereas in Castor fiber it is flat to nearly flat. Yellow to orange in colour, the enamel covers the mesial part of the tooth and expands a bit toward the sides in Hystricidae whereas in

Castoridae it covers the incisor all along its mesial length and do not expands e or only slightly in the lateral side d (see X-ray images in Stefen et al., 2011). Finally, we can differentiate the premolars and molars (cheekteeth or chewing teeth) of Hystrix and Castor for the following characters: Hystrix has more braquiodont chewing teeth, and roots are developing in early stages of ontogeny. Isolated enamel islands on the occlusal surface are fossettids in the lower and fossettes in the upper cheek-teeth (enamel islets in Sulimsky, 1960), and are formed early in the ontogeny of the porcupines (Vekua et al., 2010). In the Castoridae, the striae and striidae usually reach the base of the crown, while in the Hystricidae these are shorter. In Castoridae the striae and striidae are formed in late ontogenetic stages in primitive taxa (Stefen, 2010), whereas in Castor they are seldom developed (Wessels et al., 2011) or in late, strongly wear molars (the circular enamel island in Barisone et al., 2006).


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Fig. 8. Nomenclature of the mandible and dentition of Castor fiber from the Early Pleistocene layers of Gran Dolina. Right mandible in medial view. Ata95TD6t42g16 (MPZ 2015/1539).

4.1. Description The small differences between the fossil remains of beavers from the Holocene and the Early Pleistocene from Atapuerca are sparse criteria to separate two species. Therefore, we classify the fossil beaver remains from the Sierra de Atapuerca sites, Portalon, Galeria de las Estatuas, Gran Dolina and Sima del Elefante, as Castor fiber (Tables 1 and 2, Figs. 3e15). 4.1.1. Mandible Figs. 6e11, 13, Table 1. Castor fiber Linnaeus 1758 4.1.1.1. Portalon. The mandible (Ata00ATPLimpExcW) was recovered during the process of cleaning of the “ancient excavation”,
niz's excavation area, during the field situated to the west of Apella campaign from 2000 (Figs. 3 and 7). The differences with the mandibles from Gran Dolina level TD6 are the larger mental foramen and the stronger uefma in lateral view (Fig. 9A in comparison with Fig. 10). In medial view it lacks the ventral border, and the alveolus for the lower incisor can be seen all along the length of the fragment (Fig 9B. It is interesting to note the roots of the p4 visible through the small window opened mesially in the alveolar wall. In occlusal view it is visible a larger retromandibular diastema in the mandible from Portalon in relation to the mandibles from TD6 (Figs. 9C and 13). The premolar is slightly shorter than in the mandibles of TD6.

Fig. 9. Castor fiber from Portalon (Atapuerca, Burgos). Left hemimandible from Level 3 of Middle Bronze Age, dated in 3.330 ± 30 BP (according to Carretero et al., 2008). In A, lateral, B, medial, and C, occlusal views. Ata00ATPLimpExcW.

4.1.1.2. Gran Dolina level TD6. The mandibular material from Gran Dolina level TD6 differs slightly from the mandibular material from Portalon. Also their measurements show small differences (Fig. 14). The material from TD6 consist of four, nearly complete, mandibular fragments, three rights and one left, with complete to incomplete dentition. They were quarried during the field campaigns of 1994, 1995, 2008 and 2009 [Ata95TD6t42g16 (MPZ 2015/1539); Ata94TD6t37j18-12zi479 (MPZ 2015/1540); Ata09td6-2g4zi489-73 (MPZ 2015/1543); Ata08TD6-2 (no MPZ)]. These mandibles represent four individuals of different stratigraphic layer and ontogenetic age, from the youngest with a dp4, to the oldest. The alveolar septa between the teeth are well preserved


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C. fiber

Castor sp.

C. plicidens

C. fiber

Label

Wessels et al., 2011 Aldana Carrasco, 1992

€ rs et al., 1998 Mo

Hugueney, 2004

Freye, 1978 present work

md

85

Hambach Reuver Clay, Germany The Netherlands Tarragona, Spain

Tortosa (IPS)

Guadix-Baza, Spain Drome, France

Valdarno, Italy Pietrafitta, Italy

Navarra, Spain

md md md

m2

I M3 md p4 I 38.3

37 32.9

36.9 21.4 23.9 25 24.5 19.2 25

27.4 23 25.1 29 29.1 28.2 27.9

22.5

7.5

8.04

10

9.8 7.8 7.7 8.4

8.8

10.7

9.57 9.22

9.1

8.2

11 12.2 10

8.3 11.3 8 7.7 9.3 8.5 10.6 11.6

8.5

8.3

9.05

9.2 11.2 9.5

8.3 6.7 9.6 7 11 7.4

8.5 8.9 8.4

8.2 9.3 8.2 8.4 8.8 8.3 9.3 8

7.9 9 8.5 8.9

7.4 8.3 8.6

7.4 7.6

7.5 8

8.1

7.4 9.3

7.1 7.7 8.5

8.5

9.6 8.1 7.9 8.8

8.7 9.3 9.4

7.8

7.6

7.8

6.7

8.5

7.9

7 7.6 8

6.9

8.8

9.1

8.8 7.8

8.8 8.4 8.9

8.7

7.3

7.6

9.3

7.5

7.1 7.6 8.1

6.7

9.8

8.8

9.4 8

8.5 8.4 8.9

7.4

7.4

6.7

6.8

7.5

7.2 8.6

7.2

8.2

7.1 8.2

6.3 6.3

6.2

4.2

6.6 6.8

6.8 7.5 8.1

8.7 7.4

8.5 9.2

7 7.3 7.8

8.2

7 6.5

7.5 7

6.4 6.5 6.8

9.6 11 8.7 9.2

9.9 8.1 9.9 8

8.5 8.9

8.8 8.7

7.6 6.7

9.1 8.4

9.7

8.4

7.4

6 6.4 6.8 6.4 6.7

6.6

6.2

8.5

6.7 7.8 7.6 7.1 6.3

6.15

6.09

6.5

Pliocene?

Pliocene

Villanyan/ Villafranchian

Epivillafranchian

Mousterian Biharian

Extant Iron/Roman Middle Bronze Solutrean

Extant

WI LP4 WP4 LM3 WM3 Age

6.5

md md mx P4 I I I I M3 M3 M3 M3 M3 md md md md md md md md p4 inf

31

24

9 9

6.7 10.1

7.9

7.7 7.9

wp4 Lm1 Wm1 Lm2 Wm2 Lm3 Wm3 LI

M3

35

22.5 26.3

5.7

8.62

Lp4

6.3

33.5

34.2 35.46

21.38

31.7

Wi

M3

33.12

84

md I

38.04 40

89

md

md

14.9

Hmdantp4 Ldiastema Li

33e33.1 32 27.32

33.57

39

45.3

Element ims-alvi-li p4-m3 alv

lower d mx P4 md Caldeirao, Portugal I, m3 Lezetxiki m1 Cova Negra Atapuerca md J 80

Pretzsch, Elbe Atapuerca

NA

Site

Saint-Vallier 161944 Saint-Vallier 161945 Saint-Vallier 161946 Saint-Vallier 161948 GPIBO-Har 5505-5506 MAB 4600, Langenboom

extant C. canadensis MPZ 2015/1549 ZFMK 39.40219 ATPNS3/4. CMI-A8-25-2 Ata00ATPLimpExcW HLUBU Antunes, 1989 Isup, CAL-P14-P15 Altuna, 1972 Lezetxiki IIIa Perez Ripoll, 1977 Cova Negra present work Ata09TD6-2g4zi489-73 MPZ 2015/1543 Ata94TD6t37z479j18-12 MPZ 2015/1540 Ata95TD6t42g16 MPZ 2015/ 1539 Ata08TD6-2 ata96td6t43h16#338 MPZ 2015/1541 Ata95td6t40h17#110 MPZ 2015/1542 ata02TE9bl30z580-590 MPZ 2015/1544 Crusafont and Olazagutía Villalta, 1948 Olazagutía Olazagutía Antunes, 1989 Vale de Arno IGF 943 Barisone et al., sample no. 1744 2006 sample no. 1744 Sample no. 1819 Sample no. 460/3 Sample no. 461/10 Sample no. 461/13 Sample no. 1083 Sample no. 1829 Sample no. 457 sample no. 458 sample no. 459 sample no. 1095 sample no. 1095 Sample no. 1222 Sample no. 1222 Sample no. 1223
, 1989 Sese Huelago 5

Author

C. canadensis present work

Castor species

Table 2 Measurements of selected fossil and extant beavers from the localities of the Sierra de Atapuerca and, with the exception of the extant C. canadensis, the rest of Europe. Measurements are in mm.

Pliocene

Early Pleistocene

Late Pleistocene

Holocene

Extant

8
s et al. / Quaternary International xxx (2015) 1e15 G. Cuenca-Besco


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Fig. 10. Mandibles of Castor fiber from the Early Pleistocene of Gran Dolina level TD6 (Atapuerca, Burgos, Spain) in lateral view. A, B, D right; C, left mandibles. MPZ labels in brackets. A) Ata95TD6t42g16 (MPZ 2015/1539); B) Ata94TD6t37j18-12zi479 (MPZ 2015/1540); C) Ata09td6-2g4zi489-73 (MPZ 2015/1543); D) Ata08TD6-2 (no MPZ). 10D corresponds to the juvenile individual. MPZ labels in brackets.

in the adult specimens, this together with the size and occlusal stage of the molars; indicate that the three mandibles were adult individuals. The horizontal ramus of the mandible of Castor fiber from the level TD6 of Gran Dolina is strong, massive, and high. The juvenile is slightly lower in height. Also in the juvenile, the DE is less

robust than in the adults. The four mandibles preserve the symphyseal area and part of the horizontal ramus. The vertical or ascending ramus of the mandible is incompletely preserved, in MPZ 2015/1539 is lacking. The mandible Ata08TD6-2 has the ascending ramus with a high coronoid process that is almost complete, while the mandibles MPZ 2015/1540 and the juvenile

Fig. 11. Mandibles of Castor fiber from the Early Pleistocene of Gran Dolina level TD6 (Atapuerca, Burgos, Spain) in medial view. A, B, adult, right; 11C, juvenile left. Numbers and letters indicate field labels (MPZ labels in brackets). A) Ata95TD6t42g16 (MPZ 2015/1539); B) Ata08TD6-2 (no MPZ); C) Ata09td6-2g4zi489-73 (MPZ 2015/1543).


s, G., et al., Beavers (Castoridae, Rodentia, Mammalia) from the Quaternary sites of the Sierra de Please cite this article in press as: Cuenca-Besco Atapuerca, in Burgos, Spain, Quaternary International (2015), http://dx.doi.org/10.1016/j.quaint.2015.10.072

10


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Fig. 12. Details of the lower incisors of the mandibles of Castor fiber from the Early Pleistocene of Gran Dolina level TD6 (Atapuerca, Burgos, Spain) in A, C, E, lateral view, and B, D, F, medial view.

specimen MPZ 2015/1543 preserve only part of the coronoid and angular processes (the beginning of the angular shelf). The horizontal ramus exhibits a prominent DE in its anterior part and a relatively straight ventral rim of the ramus between the DE and the angular shelf. The masseteric fossa (fma) in lateral view shows a triangular shape, the uefma and the lefma forming a triangle, where its anterior vortex is situated below the p4-m1 junction. The mental foramen is arranged in a line with the vertex of the fma, below the diastema. It is larger in the adult specimens than in the juvenile (Fig. 10). In medial view the prominent symphysis runs from the incisor to the DE. The mandibular or sublingual fossa (fsm, Fig. 11) is large

and elongated. It is limited posteriorly by the crista ramus mandibulae (CRM). Posterior to it, a deep fossa for the pterygoid muscle is present, best visible in Ata08TD6-2 (Fig. 10B). The mandibular foramen is large, elongated and situated above the CRM, which is prominent and elongated posteriorly. The occlusal surface of the tooth row is plane to slightly concave €rs and (by comparison with i.e. Steneofiber depereti described by Mo Stefen, 2010). 4.1.2. Dentition Gran Dolina level TD6 and Portalon. Figs. 4, 5, 8, 9, 12, 13

Fig. 13. Mandible of Castor fiber from the Early Pleistocene of Gran Dolina level TD6 (Atapuerca, Burgos, Spain) in occlusal view. Ata08TD6-2 (no MPZ). A. The whole mandible. B. detail of the p4-m2.


s, G., et al., Beavers (Castoridae, Rodentia, Mammalia) from the Quaternary sites of the Sierra de Please cite this article in press as: Cuenca-Besco Atapuerca, in Burgos, Spain, Quaternary International (2015), http://dx.doi.org/10.1016/j.quaint.2015.10.072


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Fig. 14. Bivariate analysis, Length and Width (LxW), of the lower dentition (i, p4, m1, m2, m3) of selected Castor species specimens from the Pleistocene of Europe (see Table 1 for more information). The measurements are taken from the literature. The dimensions of the specimens from the Atapuerca sites were taken in the occlusal surface. Measurements are in mm.

4.1.2.1. Incisors. As described by Freye (1978) the incisors of Castor fiber, both upper and lower incisors (I, i) are large, strong, chisel-shaped and diprotodont or procumbent. The lower incisors of C. fiber from TD6 are robust as well. The size of the incisor of the juvenile mandible is to some extent lesser than the incisor in the adult (Table 1, Figs. 10e12). The anterior face is slightly convex and the enamel surface is smooth and orange-red to maroon coloured (due to iron mineralization as in most rodent incisors and in Soricines, Gordon et al., 2015), and it is best visible in anterior and lateral views (Figs. 10 and 12). There is only one upper incisor, one fragment of an Id (Ata96TD6t43h16#338, MPZ 2015/1541). The wear planes of both, upper and lower incisors differ in shape. The wear facet of the lower incisors is elongated and extends in a constant angle from the tip to the lingual side. The facet of the upper incisor is shorter and consists of two parts: a very steep part at the very tip with nearly only the enamel band, and a posterior, more sloping part. These features are already present in the Cas€ rs and Stefen, 2010). torids of the Miocene (Mo €rs et al. (1998) describe the castorids from the Hambach Mo Reuver Clay fauna (Germany), where they are represented by two incisors with a smooth enamel surface and slightly-arched medial side. The width is similar to that in C. fiber. 4.1.2.2. Cheek teeth: premolar and molars (chewing teeth). The premolar and molars of extant beavers are hypsodont and lophodont and do not grow unlimited. They display a four-loph pattern in the occlusal surface with four lophs and four valleys or flexus (Hugueney, 1999; Barisone et al., 2006; Korth, 2008). Except for the labial fold of the paraflexid in the m1 and m2 of the mandible (Ata95TD6t42g16 (MPZ 2015/1539, Fig. 8), there are no crenulations on their occlusal surface. The striae and striidae are filled with cement and are reaching nearly the base of the crown. In the lateral view of the skull of an extant beaver, such as i.e. the American beaver Castor canadensis,

the striidae in the lower and the striae in the upper chewing teeth are also evident as it occurs in the premolars and molars of Castor fiber from the localities of Atapuerca.

4.1.2.3. Upper cheek teeth. Figs. 4 and 5 We describe here the three elements of the upper chewing teeth of Castoridae recovered until now in Atapuerca, one P4 from the
n (Fig. 4, AtaATPNS3/4, CMIRoman/Iron cultural levels of El Portalo A8-25-2), one isolated M3d from Gran Dolina level TD6 (Fig. 5A, Ata95td6t40th17, MPZ 2015/1542) and one isolated M3s from Sima del Elefante level TE9 (Fig. 5B, Ata02TE9bl30z580-590, MPZ 2015/ 1544). P4
n, AtaATPNS3/4, CMI-A8-25-2) is still attached The P4 (El Portalo to the maxilar bone. The beginning of the zygomatic arch is visible in occlusal view (Fig. 4B). In occlusal view the premolar presents four lophs: anteroloph, protoloph þ mesoloph, metaloph and posteroloph (Fig. 4C), differing from the pentalophodont pattern of the Miocene Castorids (Hugueney, 1999). The hypostria is filled up with cement, another typical character in Castor fiber (Crusafont and Villalta, 1948). The degree of wear and the length of the hypostria, reaching the base of the molar in lingual view (Fig. 4A) indicate an individual of mature age. M3 Two isolated M3, one from TD6 (Fig. 5A) and the other from TE9 (Fig. 5B), differ in size and shape. The M3 from TD6 is trapezoid whereas the M3 from TE9 is rectangular in shape. The trapezoid shape is usual in extant C. fiber, contrasting from the rectangular shape of the M3 of C. plicidens from i.e. Pietrafitta (Barisone et al., 2006). Both M3 from Atapuerca have no crenulations.


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Fig. 15. Matrix of the Presence (1)dAbsence (0) of Castor fiber, and other relevant taxa in the Quaternary sequence from Atapuerca. The presence of C. fiber is signaled with the drawing of a beaver: white corresponds to Early Pleistocene; dark grey, Late Pleistocene, and light grey, Holocene.

TD6 The M3 from TD6 is trapezoid in the occlusal plane. It has four lophs, anteroloph, protoloph þ mesoloph, metaloph and posteroloph. There are four flexii, three in the labial side, paraflexus, mesoflexus and metaflexus, and the hypoflexus in the lingual side. The paraflexus is in contact with the end or the side of the hypoflexus. The mesoflexus is proportionally long and curved towards the back. The metaflexus is short and seems a Tdinverted shape. The enamel wall is thick. The striae do not reach the base of the tooth. There is also a large attrition facet in the mesial side. This indicates an individual of an old age. The roots are also formed.

metaflexus. The enamel wall is thin. The striae reach the base of the crown. The roots are not formed. The morphology as it is seen at the root surface shows the paraflexus and hypoflexus separated, and the rectangular shape is maintained though it is longer and wider than in the occlusal side. We classify it as an M3 because an attritional facet is present in the anterior side, while it is absent in the posterior side.

4.1.2.4. Lower dentition. We describe the premolar and molars from the mandibles of TD6 and Portalon. Despite of the small differences such as the stronger upper masseteric crest in the mandible of El Portalon, the dentition is similar; being thus described together here (Figs. 9, 13 and 14).

TE9 p4 The M3 from TE9b is nearly rectangular in the occlusal surface. There are the same lophs and flexii than in the tooth from TD6. It belongs to a juvenile individual. Consequently the morphology of the occlusal surface differs from that in the M3 from TD6. The paraflexus is in contact with the hypoflexus forming a single flexus. The long mexoflexus is running along from the labial to the lingual side. The two distal lophs have a Udshape limiting a nearly round

The p4 is rectangular shape with a convex mesial side. It is the larger tooth of the lower cheek teeth. It has four lophs, anterolophid, metalophid, mesolophid and posterolophid, three flexid in the lingual side, paraflexid, mesoflexid and metaflexid, and one in the labial side, the hypoflexid. The p4 is slightly shorter in the Castor fiber from Portalon (Fig. 9) than in TD6 (Figs. 8, 10e14).


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m1 and m2 The first two lower molars are similar to the p4 although they are more quadrangular in shape and both, the mesial and posterior sides are planar. The length and width are similar in both, Portalon and TD6 m1, m2 (Figs. 8B, C, 9, 13, 14). m3 It is similar to the m1, m2, although slightly smaller and with the posterior side convex. The m3 from Portalon is shorter than the m3 from TD6, though wider (Fig. 14). 4.2. Taxonomic remarks and discussion The species Castor fiber is well differentiated from the species of Castoridae from the Miocene by its larger size and the retaining of
and Lopez Martinez, 1981). the striidae even with strong wear (Sese Moreover, the flexus and flexid are filled up with cement, distinguishing C. fiber from Trogontherium and other Castorid species
and Villalta, 1948; Sese
, 1989; from the Miocene (Crusafont Pairo Aldana Carrasco, 1992; Hugueney, 1999; Casanovas-Vilar et al., € rs and Stefen, 2010). 2008; Mo During the Quaternary, the variation in the size of the C. fiber
and Villalta, 1948; Antunes, 1989; teeth is large (Crusafont Pairo Frahnert, 2000; Barisone et al., 2006; Wessels et al., 2011). Nevertheless, as we show in the present study, the variation in width is lesser than in length (Fig. 14, Table 2). Barisone et al. (2006) gives recognition to C. plicidens from Pietrafitta as a subspecies of C. fiber for its crenulated enamel walls in the occlusal surface. Nevertheless, following Forsyth Major (1875) and Friant (1964) here we consider C. fiber and C. plicidens two different species, being both similar in size, and differing in morphology, as i.e. the broader m1, m2, and m3 in C. plicidens (see Fig. 14). Important differences between both species are seen in the occlusal surface of the yugal teeth: in C. plicidens the enamel of the molars appears strongly folded, while this character is absent or only appears partially in older specimens of C. fiber such as in the two first molars of the mandible from TD6 (MPZ 2015/1539). Antunes (1989) also remarks that the incisor in C. fiber is smaller than in C. plicidens. See also the discussion about the status of C. plicidens in Barisone et al. (2006) and Rook and Angelone (2013). The beaver specimens from the different stratigraphic levels from Atapuerca fit in the morphologic and biometric variability of
lago 5 has nearly the same size as one Castor fiber. The p4 from Hue
individual from TD6 (Fig. 14). This specimen is classified by Sese (1989) in open nomenclature, Castor sp.; therefore we tentatively
lago 5 as C. fiber. On the other hand, the classify the p4 from Hue absence of crenulations distinguishes the species from Atapuerca from Castor plicidens, although note the folds in the first two lower molars of the mentioned mandible, Ata95TD6t42g16 (MPZ 2015/ 1539, see Fig. 8. In our opinion these folds show that there are morphological relationships between both species. The molars of C. plicidens from Pietrafitta are also larger than these in C. fiber from Atapuerca except for the incisors which are nearly of the same size in both species (Table 2, Fig. 14). The C. fiber individuals from SaintVallier are similar to slightly larger than the Spanish beavers. 5. Biostratigraphy The species Castor fiber first appears in Spain the Early Pleistocene from Atapuerca; it disappears during the Middle Pleistocene in Atapuerca, though it is present in only one locality from the Iberian Peninsula, Aridos 1. It returns once more at the end of the Late Pleistocene and in the Holocene it disappears during the

13

roman period (Tables 1 and 2, Fig. 15). There are rare mentions of beaver discoveries in the Pleistocene/Holocene of the Iberian Peninsula (see Fig. 1 and Tables 1 and 2). The populations of this species probably were at no time abundant (Antunes, 1989; Liesau von Lettow-Vorbeck, 1998; this work). From our data and the bibliographic compilation it is evident that they disappeared during the Middle Pleistocene in Atapuerca and nearly in the Iberian Peninsula, if not for the remains of Aridos 1, we could say they locally disappeared. The tremendous amount of excavated material in the archaeological/paleontological sites of Atapuerca exclude a bias of selectivity in the samples from Atapuerca which influences its distribution (we analysed 25 t of sediments each year, during the field campaign, for the search of small vertebrates with the sieving
s et al., washing techniques described elsewhere, Cuenca-Besco
s, 2013). 1999b, 2005; Rofes and Cuenca-Besco 6. Human paleoecology and the beavers from the cave-sites from Atapuerca From the paleontological study of the Castor species from the Atapuerca sites we can reconstruct the sceneries were the hominids from Atapuerca once thrived. Different authors, Ortega et al. (2013); Benito-Calvo and Perez-Gonzalez (2015) have shown that the caves from the Sierra de Atapuerca have been surrounded by three Rivers
n, Pico and Vena. During during the Pleistocene, the rivers Arlanzo the first stages of fluvial downcutting, the phreatic influence of the
n River generated an endokarst system in the Cretaceous Arlanzo limestones of the Sierra de Atapuerca, excavating three phreatic
n River galleries (Ortega et al., 2013). The incision of the Arlanzo changed progressively the condition of the galleries from phreatic to vadose conditions, starting the allochthonous infilling of the caves, and generating a series of available dry caves whose entrances were used by hominids from the Early Pleistocene to the Holocene
rez-Gonzalez, 2015). (Ortega et al., 2013; Benito-Calvo and Pe Being that the rivers propitiated the freshwater habitats, forests and water edge or riparian habitats are present throughout the Atapuerca fossil record (Blain et al., 2010; Rodriguez et al., 2011). The beavers undoubtedly have lived near the caves, in the forest galleries in the river valley, during the Early Pleistocene and Late Pleistocene/ Holocene. The beavers from the Early Pleistocene (TE9 and TD6) have surely coexisted with Homo species that were living in the Sierra while there are no traces of have been eaten by humans. Rivergallery forest habitats were surely dominating the landscape. The analysis of the small mammal assemblages have shown that the Early Pleistocene levels of Gran Dolina and Sima del Elefante rep
s et al., resented forested and humid environments (Cuenca-Besco
s, 2009; Blain 1999b, 2005, 2010b, 2013; Rofes and Cuenca-Besco et al., 2010, 2013; Rodríguez et al., 2011). Desmanines (aquatic moles) represented by Galemys spp., are present, though scarce, throughout the whole diachronous sequence of the sites of Atapuerca though nearly disappear also during the Middle Pleistocene, and the same may be said of Neomys, the water shrew (Fig. 15). The beavers live in the riverbanks, they are the aquatic elements of the landscape in the present times and also during the Quaternary as we have shown in Atapuerca, and other localities, such as Pietrafitta Lake in Italy (Barisone et al., 2006). Another instance is that the only beavers found in the localities of the Alpes-Maritimes in South East France are these from the fluvial plains of the thermoMediterranean stage from the Late Pleistocene of Pie Lombard (Desclaux, 2013). 7. Conclusions The fossil beaver remains found in Atapuerca are attributed to the species Castor fiber. We show in the present work that the Early


s, G., et al., Beavers (Castoridae, Rodentia, Mammalia) from the Quaternary sites of the Sierra de Please cite this article in press as: Cuenca-Besco Atapuerca, in Burgos, Spain, Quaternary International (2015), http://dx.doi.org/10.1016/j.quaint.2015.10.072

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s et al. / Quaternary International xxx (2015) 1e15 G. Cuenca-Besco

Pleistocene beavers from Atapuerca TE, TD are biometrically similar among them and to the beavers from the Holocene levels of El Portalon. Moreover, the Castor fiber fossil remains from the Sierra de Atapuerca sites are similar to the fossil and extant record of C. fiber from Europe since the Early Pleistocene (Fig. 14). The specimens of C. fiber studied in the localities of Atapuerca reveal the presence of beavers near the caves of Atapuerca during the Early Pleistocene (Lower levels of both localities, Sima del Elefante and Gran Dolina), and during the Upper Pleistocene
n). (Galería de las Estatuas) to the Holocene (Portalo Surprisingly, they do not appear in the Middle Pleistocene layers of the sites such as TD10 in Gran Dolina, the site of Galería-Zarpazos, or in the upper red unit of the Sima del Elefante (TEURU). We discard a bias in the fossil record because we have analysed tons of sediments and determined thousands of large and small vertebrates from the different sites of Atapuerca (Fig. 15). We can conclude that the Eurasian beaver is present in Spain since the Early Pleistocene, nearly 1.4 million years ago. They were living in the aquatic environments provided by the rivers near the Sierra de Atapuerca, as their extant relatives do. Other proxies such as the stratigraphy and sedimentology, other fossil rodents, insectivores, anurans, and birds, show that the early Pleistocene levels of Sima del Elefante and Gran Dolina indicate humid and forested conditions, and that running water or ponds were near the entrances of the caves. The humans that visited Atapuerca during the Early Pleistocene, the late Pleistocene and the Holocene, always had a source of water near the caves. The absence of beavers during the Middle Pleistocene, when the human presence was intense (Arsuaga et al., 2014, 2015; García-Medrano et al., 2015), indicates that suitable habitats for beavers were probably more scarce in the vicinity of the caves. Acknowledgements € rs, Clara Stefen, Carlos Lastanao, To Stefan Ramme, Sebastien Mo Roisin Campbell-Palmer, Miguel Telles Antunes, that share their knowledge and papers about beavers with us. Jordi Mestre and Javier Rubio made some of the field photographs. J.J. Negro and Ismael help with the identification of iron in some incisors of extant rodents. The Guest Editor, Jesús Rodríguez and one referee greatly improved the first draft of the MS. Thanks must be offered to the team of Atapuerca during the field campaigns each year since 1990, nearly 150 researchers and technicians, for their work during the excavations. We also would like to thank the Museum of Burgos for
n providing access to archaeological samples from the prior Portalo excavations. M. Galindo-Pellicena is being supported by a post
n Atapuerca. The financial support doctoral grant from the Fundacio for the Atapuerca project has been provided by the research projects MICICINN CGL2012-38434-C03-01, CGL2012-38434-C03-03, CGL2012-38358, from Generalitat de Catalunya 2014/100573 and
NeCa Foundation project 19434/PI/14; 2014 SGR 900, and the Se
n Atapuerca, and Grupos ConJunta de Castilla y Leon, Fundacio
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