Journal of Archaeological Science 40 (2013) 3105e3116
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Osteophagia and dental wear in herbivores: actualistic data and archaeological evidence Isabel Cáceres a, b, *, Montserrat Esteban-Nadal b, a, Maria Bennàsar a, b, M. Dolores Marín Monfort c, M. Dolores Pesquero c, d, Yolanda Fernández-Jalvo c a
Area de Prehistoria, Universitat Rovira i Virgili (URV), Avinguda de Catalunya 35, 43002 Tarragona, Spain IPHES, Institut Català de Paleoecologia Humana i Evolució Social, C/ Marcel.lí Domingo s/n e Campus Sescelades URV (Edifici W3), 43007 Tarragona, Spain Museo Nacional de Ciencias Naturales (CSIC), José Gutiérrez Abascal, 2, 28006 Madrid, Spain d Fundación Conjunto Paleontológico de Teruel-Dinópolis, Avda. Sagunto s/n, 44002 Teruel, Spain b c
a r t i c l e i n f o
a b s t r a c t
Article history: Received 13 September 2012 Received in revised form 26 March 2013 Accepted 15 April 2013
The ability of herbivores to produce damage in bones and antlers has recently been described by the present authors (Cáceres et al., 2011), showing several cases of modified bones and various stages of bone modification due to osteophagic behavior by herbivores. Herbivores chew and eat bones and antlers to make up for mineral scarcity in their diet. In this paper we describe how the consumption of bone and antlers by herbivore can result in distinct differential tooth wear, breakage and the loss of some dental pieces. This damage has also been identified in fossils. These preliminary results are especially relevant in archaeological contexts, because this marked tooth wear can be mistaken for dental disease or lead to the incorrect assignment of age to the animals. Ó 2013 Elsevier Ltd. All rights reserved.
Keywords: Dental wear Osteophagia Taphonomy Actualistic studies Atapuerca sites Abric Romaní Bosque de Riofrío
1. Introduction The consumption of bone and antler by herbivores is associated with a diet deficient in minerals (calcium and phosphorus, primarily), which are supplied by the ingestion of organic materials (Theiler et al., 1924; Gordon et al., 1954; Barrette, 1985; Denton et al., 1986; Warrick and Kraussman, 1986; Johns and Duquette, 1991; Grasman and Hellgren, 1993; Richard and Juliá, 2001; Mitchell et al., 2005; Bredin, 2006; Bredin et al., 2008). Recently, we published a paper on the ability of herbivores to eat bones and antlers and on the bone modifications that this behavior causes (Cáceres et al., 2011). This study, which was undertaken in the natural reserve of Bosque de Riofrío (Segovia, Spain), based on a total number of 249 chewed bones by red deer (Cervus elaphus) and fallow deer (Dama dama), has allowed us to obtain a deeper
* Corresponding author. Area de Prehistoria, Universitat Rovira i Virgili (URV), Avinguda de Catalunya 35, 43002 Tarragona, Spain. Tel.: þ34 977 943 003x3013. E-mail addresses:
[email protected] (I. Cáceres),
[email protected] (M. Esteban-Nadal),
[email protected] (M. Bennàsar), Maria.Dolores.
[email protected] (M.D. Marín Monfort),
[email protected] (M.D. Pesquero),
[email protected] (Y. Fernández-Jalvo). 0305-4403/$ e see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.jas.2013.04.006
understanding of different forms of bone damage associated with the osteophagic activities of herbivores. Osteophagia is defined as abnormal craving for nonfood items. Sutcliffe (1973) refers that, apart from domestic animals (cow and sheep), osteophagia has been observed in red deer, reindeer, camels, giraffes, wildebeest, kudu, gemsbok and sable antelopes. More exceptional is the case referred by Wald (2011) of osteophagia by a grizzly bear (Ursus arctos horribilis) chewing a shed moose (Alces alces) antler. Sutcliffe (1973, 1977) summarized descriptions by several observers and previous authors that witnessed this phenomenon among domestic and wild artiodactyls. According to these observers, the herbivores introduce bones into their mouth lengthways and sideways, like a cigar, and with the zigzag movements of their jaws produce the fork shape (Sutcliffe, 1977). Traditionally, the osteophagia in herbivores has been identified by the presence of bones and antlers with fork morphology (Fig. 1). This morphology is a fairly advanced stage of damage. However, in the early stages herbivores can also produce grooves, rounded and polished ends, rough surfaces and the irregular disappearance of the epiphyses (Sutcliffe, 1973, 1977; Brothwell, 1976; Johnson, 1985; Justus and Turner, 1990; Kierdorf, 1993, 1994; Cáceres et al., 2007, 2011). These modifications may be similar to those produced by
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Fig. 1. Bones chewed by herbivores from the Bosque de Riofrío (Segovia, Spain), showing the characteristic fork morphology. From top left to bottom right: Tibia, radius, metatarsal, metacarpal, mandible, proximal femur, pelvis, antler, vertebra and rib. These anatomical elements, complete or broken, have a specific format and size/weight suitable for deer to chew (Cáceres et al., 2011).
carnivores, although there are diagnostic criteria for differentiating them (Cáceres et al., 2011). The main difference resides in the state of the bone (fresh or dry) when consumption begins. Carnivores have a nourishing purpose and thus consume fresh bones, whereas herbivores do not have a nutritional intention and therefore consume dry bones. As a result, cracked and weathered surfaces are associated with the grooves produced by herbivores (Cáceres et al., 2011). When monitoring carcasses in the Bosque de Riofrío (Segovia, Spain), we observed that some jaws had a heavy and distinct differential wear. This dental wear did not correspond with the individual ages assigned to the animals by rangers on the basis of antler development. In addition, we observed tumors and other
pathologies in jaws, as well as unusual breaks in the teeth and a loss of teeth in some of the specimens that we studied (Fig. 2). Differential wear and pathologies affected more intensively the middle positions of the tooth row. The way herbivores hold and chew bones ‘like a cigar’ led us to consider the relationship between this unusual differential cheek tooth wear (incisors are free of wear) and the practice of osteophagia so widespread in Riofrío. Consequently, a review has been undertaken on the maxillae and mandibles collected in Riofrío in order to characterize the damage on the teeth associated with the practice of osteophagia. The present study also aims to find criteria for identifying osteophagic practices in the paleontological and archaeological record on the basis of differential dental wear. Therefore, we have
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Fig. 2. Pathological specimens: a) Fallow deer mandible with a tumor on the lingual face, just where lost dentition; b) Fallow deer mandible (vestibular view) with bone and dental pathology.
reviewed the maxillae and mandibles of three archaeological sites in the Iberian Peninsula: Abric Romaní in Capellades (Barcelona), and Gran Dolina site and Galería site both in Atapuerca (Burgos). Similar differential dental wear has been identified in these fossils. In addition, this study also seeks to draw attention to the existence of this phenomenon in order to prevent, as far as possible, errors in age assignment and avoid confusion with other pathologies affecting the health of herbivores. This is relevant in archaeology to establish time periods of human occupations, which are mainly based on the age of death of herbivores.
Fig. 3. Bosque de Riofrío (Segovia, Spain): a) Geographical location of the Nature Reserve of Bosque de Riofrío in the Iberian Peninsula and location of archaeological sites cited in text. b) General view of the Bosque de Riofrío and the Royal Palace.
2. Actualistic study
Camera traps (diurnal and nocturnal vision recording still images and video) have been installed to control animal access to carcasses, as well as, bone dispersal, trampling, and breakage by deer herds. Incidentally, a camera settled in the way to the feeding area as part of a trampling experiment, has confirmed the incidence of osteophagia by a young deer (Fig. 4).
2.1. The Bosque de Riofrío
2.2. Actualistic data
The Bosque de Riofrío is a natural reserve located at the central part of the Iberian Peninsula (Fig. 3), in the foothills of the Northern slope of the Guadarrama Mountain in Segovia (Spain). Several species of herbivores, carnivores and birds inhabit this protected area. The most important taxa are fallow deer (Dama dama) and red deer (C. elaphus) (for further information see Cáceres et al., 2011). Over the last 10 years we have developed a variety of actualistic and experimental studies in the forest, focusing on the disarticulation and dispersal of carcasses and various bone modification processes (Cáceres et al., 2007, 2009, 2011). At present we have 80 skeletons that have been monitored since the death of the animal, located by GPS (Global Positioning System) coordinates. Some skeletons have been collected and are currently being analyzed. Others are found in different stages of disarticulation and scattering in different environments, classified either by features of the terrain (e.g. in closed forest, open areas with no vegetation, on steep sites) or the weather (e.g. suntrap, shady area). Overall, we investigate the involvement of biological agents (vultures, foxes, etc.) in carcass modification and other physical or mechanical processes such as weathering, trampling, transport, soil corrosion or root etching.
In the course of the fieldwork, maxillae and mandibles with bone or dental pathologies as well as those presenting excessive differential tooth wear were collected from monitored carcasses and dispersed specimens across different parts of the Bosque de Riofrío (Fig. 5). The actualistic study focuses mainly on mandibles (30). The maxillae (13) are less abundant, since the skulls are usually removed by the forest rangers in order to prevent access by poachers in search of trophies. For this reason most of the skulls belong to carcasses being monitored. The mandibles and maxillae correspond to similar numbers of red deer (20) and fallow deer (23), showing also a similar ratio between right and left specimens (Table 1). All the specimens whose sex could be determined (9 mandibles and 11 maxillae) are male individuals (Table 2). With regard to the mandibles (Table 2 and Fig. 6), the location of wear is similar for red deer and fallow deer. However, red deer jaws have a greater number of affected dental pieces, with higher percentage representations than in fallow deer jaws. In both taxa, M1 is always modified, followed by P4 in wear intensity and frequency. The other dental pieces are occasionally modified, except M3, which
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Fig. 4. Series of pictures taken with a camera trap (Mod. SG560V 8MPX. Camo) installed near the exit gate of the feeding area in Bosque de Riofrío. The camera has taken a series of pictures of a young individual approaching a metapodial and taking it in the mouth as described by Sutcliffe (1973, 1977) “like a cigar”. The bone was abandoned when other individuals joint this group and disturbed the young individual. We could collect this bone and observe incipient grooves on the bone metaphysis, characteristic of ungulate chewing.
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Fig. 5. Map of the Natural Park of Riofrío (Segovia: N40 520 25.4400 /W4 90 4.0500 ) showing the boundary of the park (red line) and location of finds. Red pins points to monitored skeletons and white pins are isolated specimens collected during survey. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
is the only tooth that does not show wear related to osteophagic practices. However, in pathological jaws, this molar may show a strong wear as seen in Fig. 2b. Wear on M1 usually appears all over the occlusal surface, although at very incipient stages wear primarily affects the anterior lobe (closer to P4). In the case of P4, wear starts when M1 is obviously worn and it is usually the posterior lobe (closer to M1) that starts to be worn down, and at more advanced stages, P4 may also appear completely worn on the entire occlusal surface. Sometimes the wear is so pronounced that the crown of M1 and exceptionally of P4 is a millimeter thick. In certain specimens this causes tooth breakage at the junction of the two lobes. Among the analyzed material we recorded 4.54% of the teeth that were broken among the fallow deer and 23.1% among the red deer. In extreme cases, the breakage of the crown affects several teeth and only the roots are preserved in the alveoli. The 13 maxillae analyzed shows most maxillae are worn in a low degree (Table 2) and wear always appears on M1, mainly in initial stages (Fig. 7a). In a more advanced stage of wear (Fig. 7b), M1 is
Table 1 Maxillae and mandibles collected in the Bosque de Riofrío included in this study. Red deer Right Maxilla (13) Mandible (30) Total (43)
3 8 20
Fallow deer Left 2 7
Right 4 7 23
Left 4 8
severely affected followed by P3 and, occasionally in M2, but the P4 is almost intact. The absence of wear or much milder wear on the P4 contrasts with the severe wear usually present on the P4. In those cases that the same individual preserved both the mandible and the maxilla (RF17, RF75 and RF79) the unusual pattern of P4 having a milder or absent wear degree in between M1 and P3 heavily worn (Fig. 8) appears consistent and it always repeats. This is not then a malocclusion of one individual, it is a wear pattern that repeats amongst several individuals following identical trend (Table 2). We think this pattern may be due to occlusal mechanism modes and movements between mandibles and maxillae in these ungulates (Fig. 8). 3. The fossil data 3.1. The archaeological sites Dental wear has been observed in Pleistocene ungulates, specifically at the sites of Gran Dolina and Galería (Sierra de Atapuerca, Burgos) and Abric Romaní (Capellades, Barcelona), both in Spain (see Fig. 3 for location in the Iberian Peninsula). The Sierra de Atapuerca is located 15 km east of Burgos (Spain). At the beginning of the twentieth century, the construction of a railway exposed the oldest deposits, located in what is nowadays called Trinchera del Ferrocarril (Fig. 9a). Three karstic sites are located in this railway trench, Gran Dolina, Galería and Sima del Elefante (Rodríguelz et al., 2011). The Gran Dolina site (Fig. 9b) is a cave infill 18 m thick with an Early and
3110 Table 2 Maxillae and mandibles with osteophagic dental wear and breakage of deer and fallow deer from Bosque de Riofrío (Segovia, Spain). In brackets the sex of individuals. The age displayed in this table has been provided by the park rangers mainly based on the size and shape of antlers, head, ears, and tooth wear of the individuals (Sáenz de Buruaga et al., 1991). Individual
Age
Identification
Taxon
Wear location
RF17-OTF-257 RF12a RF12b RF2006-1 RF2006-2 RF75a RF75b RF79a RF79b RF2013A-1 RF2013A-2 RF2013B-3 RF2013B-4 RF/HC-OTF-4 RF/HC-OTF-5 RF/HC-OTF-17 RF17-18-OTF-52 RF17-12-OTF-53 RF/HC-OTF-188 RF-OTF-228 RF8-3-OTF-242 RF8-4-OTF-243 RF-OTF-245 RF-OTF-246 RF-OTF-249 RF-OTF-250 RF-OTF-251 RF-OTF-252 RF-OTF-253 RF/HC-OTF-258 RF23 RF/MUA-1 RF/MUA-2 RF/MUB-3 RF/MUB-4 RF/MUC-5 RF/MUD-6 RF-H107 RF-H108 RF75c RF75d RF79c RF79d
RF17 (_) RF12 (_) RF12 (_) RF2006 RF2006 RF75 (_) RF75 (_) RF79 (_) RF79 (_) RF2013A (_) RF2013A (_) RF2013B (_) RF2013B (_)
Adult Adult Adult
Right maxilla (P3-M3) Right maxilla (complete) Left maxilla (complete) Right maxilla (complete) Left maxilla (complete) Right maxilla (complete) Left maxilla (complete) Right maxilla (complete) Left maxilla (complete) Right maxilla (P3-M3) Left maxilla (P3-M3) Right maxilla (complete) Left maxilla (P3-M3) Right mandible (complete) Left mandible (P4-M3) Left mandible (P4-M3) Right mandible (P4-M3) Left mandible (complete) Right mandible (M1-M3) Right mandible (complete) Right mandible (complete) Left mandible (P3-M3) Left mandible (complete) Left mandible (complete) Left mandible (complete) Left mandible (complete) Left mandible (complete) Right mandible (complete) Right mandible (complete) Right mandible (complete) Right mandible (complete) Right mandible (complete) Left mandible (complete) Right mandible (P3-M3) Left mandible (complete) Right mandible (M1-M3) Left mandible (complete) Left mandible (complete) Right mandible (complete) Left mandible (complete) Right mandible (complete) Left mandible (complete) Right mandible (complete)
Red deer Fallow deer Fallow deer Fallow deer Fallow deer Fallow deer Fallow deer Fallow deer Fallow deer Red deer Red deer Red deer Red deer Red deer Red deer Red deer Red deer Red deer Red deer Fallow deer Red deer Red deer Fallow deer Fallow deer Fallow deer Fallow deer Fallow deer Fallow deer Fallow deer Fallow deer Fallow deer Red deer Red deer Red deer Red deer Red deer Fallow deer Red deer Red deer Fallow deer Fallow deer Fallow deer Fallow deer
P3 and M1 M1 M1 M1 M1 Slightly P3 and M1 Slightly P3 and M1 M1 M1 P3, M1, M2 P3, M1, M2 M1 M1 2nd lobe of P4 and M1 2nd lobe of P4 and M1 2nd lobe of P4 and M1 2nd lobe of P4 and M1 and M2 2nd lobe of P4 and M1 M1 2nd lobe of P4 and M1 P3 to M2 P4 and M1 M1 and slightly 2nd lobe of P4 M1 and slightly 2nd lobe of P4 M1 P4 to M2. M1 and slightly 2nd lobe of P4 M1 and slightly 2nd lobe of P4 M1 and M2. M1 slightly 2nd lobe of P4 M1 P2 to M2 P3 to M1 P3 to M1 P3 to M1 M1 2nd lobe of P4 and M1 2nd lobe of P4 and 1st lobe of M1 2nd lobe of P4 and 1st lobe of M1 2nd lobe of P4 and M1 2nd lobe of P4 and M1 2nd lobe of P4 and M1 and 1st lobe M2 2nd lobe of P4 and M1 and 1st lobe M2
RF17 (_) RF17 (_)
RF8 (_) RF8 (_)
4e5 years old 4e5 years old 4e5 years old 4e5 years old 4e5 years old 4e5 years old 3 years old 3 years old
Adult Adult
Adult Adult
RF23 (_) RF/MUA RF/MUA RF/MUB RF/MUB
Young-Adult
RF75 RF75 RF79 RF79
4e5 4e5 4e5 4e5
(_) (_) (_) (_)
years years years years
old old old old
Breakage
M1 and M2 M1
P2 P2 and P3 (roots preserved) 1st lobe of P3
P3 and P4 (roots preserved) M1 (in contact lobes zone)
M1 and M2 (in contact lobes zone)
P3, P4 and M1 P2 and P4 P4 (only roots preserved) M1 (in contact lobes zone) P4 (only roots preserved)
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Specimen
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Fig. 6. Actualistic mandibles with evidence of differential dental wear related to osteophagia from the Bosque de Riofrío. Fallow deer (left column) and red deer (right column). From slight (top) to extreme (bottom) modifications.
Middle Pleistocene stratigraphic sequence divided into 11 stratigraphic units named TD1 to TD11 from bottom to top (Gil and Hoyos, 1987; Pérez-González et al., 2001). The Matuyamae Brunhes boundary has been detected between units TD7 and TD8 (Parés and Pérez-González, 1999). This site has provided abundant remains of macrovertebrates, microvertebrates and stone tools, and a rich collection of human remains assigned to Homo antecessor in unit TD6 (Carbonell et al., 1995, 2005; Bermúdez de Castro et al., 2008). The Galería site (Fig. 9c) is located less than 50 m south-east of Gran Dolina (Fig. 9a). Galería is a cave infill with a stratigraphic succession 7 m thick, which has been divided into six lithostratigraphic units named G I to G VI from bottom to top (Pérez-González et al., 1999). These units have yielded abundant macro- and microvertebrate fossils and a rich collection of stone tools dated to the Middle Pleistocene, from 500 ka
to 250 ka time interval by ESR/UeTh and luminescence techniques (Berger et al., 2008). Two human fossils (cranial and mandibular fragments) attributed to Homo heidelbergensis were found in the middle units (Bermúdez de Castro and Rosas, 1992; Arsuaga et al., 1999). The Abric Romaní site is located on the right bank of the Anoia River as it passes through the village of Capellades (Barcelona, Spain). The site is situated on a travertine platform called Cinglera del Capelló (Fig. 10a). The Abric Romaní (Fig. 10b) shows a stratigraphic sequence of more than 20 m thick within which Middle Paleolithic archaeological levels and sterile travertine platforms occur cyclically (Giralt and Julià, 1996). The Neanderthal occupations have provided a rich archaeological record (Fig. 10c) composed of lithic industry, faunal remains, charcoal from hearths and wood pseudomorphs (Carbonell, 2012).
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3.2. Archaeological evidence
Fig. 7. Maxillae collected at the Bosque de Riofrío, showing differential tooth wear produced by osteophagic practices. a) Fallow deer RF79 with dental wear on right and left M1. b) Right maxillae of red deer RF17 with advanced wear on M1 and P3 and P4 unworn (P2 absent).
Differential dental wear and jaw damage has also been observed in fossils from different archaeological sites and with different chronologies, detailed in Table 3. This type of modification has been observed in different taxa, mainly artiodactyls (Praeovibos cf. priscus, C. elaphus, Dama vallonnetensis, Dama dama clactoniana, Cervidae indet.) and also perissodactyls (Equus ferus). Overall, the damage observed in the fossil samples here studied (Fig. 11aed) occurs in the same teeth as the damage identified in the current samples from the Bosque de Riofrío (Fig. 12). With regard to the fossil mandibles, most of the examples are characterized by progressive and massive wear from M1 e P4. The presence of breakage and the loss of M1 (Fig. 11d) is also usual, as occurs among the actualistic samples (compare with Fig. 6f and h). The only E. ferus mandible shows a different pattern of differential wear (Fig. 11e), in this case being concentrated exclusively in P2. It is for this reason that the percentage of M1 modified in the fossil sample does not reach 100% (Fig. 12), as it does in the modern sample. In this case, it is possible that the difference stems from the difference in mandibular and dental anatomical structure between horses and deer. In the case of the only fossil maxilla (C. elaphus), the wear appears concentrated on the anterior teeth (P2, P3 and M1), but no wear or much milder in P4 (Fig. 13a). This type of damage seen in fossils is similar to that observed in the red deer and fallow deer maxillae from Riofrío, specifically in the individual RF17 (Fig. 13a and b). Thus, it is common to see differential wear on P2, P3 and M1, whereas P4 appears unmodified or only slightly so. 4. Discussion
Fig. 8. Anatomical position of maxilla and mandible of individual RF17 from the Bosque de Riofrío.
Herbivores eat bones and antlers to make up for mineral deficiencies, mainly of phosphorus, in their diet (Sutcliffe, 1973, 1977; Denton et al., 1986; Warrick and Kraussman, 1986; Barnes et al., 1990). The modifications that occur in skeletal remains have been described by several authors (Sutcliffe, 1973, 1977; Brothwell, 1976; Johnson, 1985), and morphological criteria for distinguishing them from those produced by other taphonomic agents have recently been established by Cáceres et al. (2011). However, the damage that this behavior can produce in the dentition of herbivores, which is designed for chewing vegetables and not for the regular consumption of hard materials such as bones and antlers, had not previously been described. The way herbivores hold and chew bones “. lengthways in its mouth with more than half projecting forwards and a little to one side, ‘like a cigar”’ (Sutcliffe, 1973; page 429) is very likely the cause of damages on several jaws of deer observed in Riofrío. These jaws show a heavy and anomalous differential wear on the middle
Fig. 9. The Sierra de Atapuerca: a) Aerial view of Trinchera del Ferrocarril, where the sites of Gran Dolina (1), Galería (2) and Trinchera Elefante (3) are located; b) Excavations at the site of Gran Dolina; c) View of the site of Galería.
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Fig. 10. General view of Cinglera del Capelló, where the site of Abric Romaní is located; b) View of excavations in Abric Romaní; c) Detail of excavation surface of level N, where wood pseudomorphs and hearths have been uncovered.
Table 3 Fossil maxilla and mandibles with damage (dental wear and breakage) identified in ungulates from Pleistocene sites. Preserved teeth showed in parentheses. Site
Specimen
Chronology
Identification
Taxon
Wear location
Gran Dolina Gran Dolina Gran Dolina Gran Dolina Gran Dolina Gran Dolina Galería Abric Romaní Abric Romaní Abric Romaní Abric Romaní
ATA03-TD7-3-F15-1 ATA04-TD7-2-G5-4 ATA07-TD6-2-F13-21 ATA07-TD6-2-F13-443 ATA99-TDE5c-H17-38 ATA87-TD10-I12-4 ATA92-TN5-F25-45 AR-c6 AR09-OeU57-30 AR93-Ja-N47-9 AR94-Ja-M49-21
Lower Pleistocene Lower Pleistocene Lower Pleistocene Lower Pleistocene Lower Pleistocene Middle Pleistocene Middle Pleistocene Middle Palaeolithic Middle Palaeolithic Middle Palaeolithic Middle Palaeolithic
Left Mandible (P2-M3) Right Mandible (P4-M3) Left M1 Left Mandible (M1-M2) Left Mandible (P2-M3) Left Mandible (P2-M3) Right Mandible (P3-M3) Right Mandible P3-M3) Left Mandible (P2-M1) Left Maxilla (P2-M3) Right Mandible (P2-M3)
Praeovibos cf. priscus Dama vallonnetensis Dama vallonnetensis Dama vallonnetensis Dama vallonnetensis Dama dama clactoniana Cervus elaphus Equus ferus Cervus elaphus Cervus elaphus Cervus elaphus
2nd lobe P4 and 2nd lobe P4 and 1st lobe M1 1st lobe M1 P4 and M1 2nd lobe P4 and 2nd lobe P4 and P2 2nd lobe P2 and P2, P3 and M1 2nd lobe P4 and
positions of the cheek teeth following a distinct pattern that we propose here to be result of osteophagia. After analysis of the modern samples, we can define a clear pattern and sequence of wear on the lower and upper dentition to also compare with fossil specimens. The sequence of damage to the mandible teeth is as follows: 1. Most frequently, M1 starts to wear down. Initially, the wear is concentrated on the anterior lobe (Fig. 6a). At this early stage, wear may also affect the posterior lobe of P4 more frequent amongst red deer (Fig. 6b). 2. The two lobes of M1 are worn down to a similar degree (Fig. 6c and d) and the posterior lobe of P4 is more affected than in previous stage 3. The wear extends from M1-P4 to posterior (M2) and anterior teeth, such as P3 (Fig. 6e and f), exceptionally rare to M3 4. The crown of M1 is heavily worn down and also broken (Fig. 6f) other dental pieces may also break (Fig. 6g). This breakage causes the loss of teeth, sometimes leaving all or part of the roots in the alveoli (Fig. 6g and h) and, sometimes, bone resorption or pathological processes at the toothless area. The sequence of differential dental wear observed in maxillae is as follows: 1. Wear on maxillae begins slightly in M1 (Fig. 7a). 2. When wear is more intense in the M1, the P3 has already signs of modification, but the P4 does not appear affected (Fig. 7b) 3. The wear may extend to M2 when, wear is extensive in M1 and P3, but the P4 remains intact or lightly worn. Comparing modern maxillae with the mandibles of the same individuals (RF17, RF75 and, RF79) this pattern of wear could be
Breakage 1st lobe M1 M1
M1 M1
M1 broken M1 broken
2nd lobe P4 M1
M1 broken
caused by the different occlusal mechanism modes and movements between maxilla and mandible (Fig. 8). We propose that maxilla, as part of the face and skull is static and during the process of osteophagia its main function is to hold the bone (using M1 and/or P3). The mandible, capable of performing lateral movements, is actually the responsible of chewing the bone, increasing friction against M1eP4 and, in more extreme stages, extends wear effects to M2 and P3. This may then cause that mandibles appear more extensively damaged than maxillae as observed in both modern and fossil jaws. This differential dental wear and teeth damage has also been identified in fossils from archaeological sites and with different chronologies (Figs. 11 and 13). Some of these specimens come from stratigraphic levels that record the MatuyamaeBrunhes geomagnetic reversal. This, therefore, provides evidence of possible osteophagia as old as Pleistocene times. Osteophagic practices have been identified in several fossil species of herbivores, including horses. Horses are especially relevant because osteophagia has been described by several authors in modern cases mainly amongst ruminants. Modifications due to osteophagia need to be distinguished, since it is possible for the wear to be misinterpreted and be associated with the presence of dental disease when teeth in alveolar position are extremely worn. Also, there is a risk of assigning the incorrect age to the individual, as extreme wear may suggest the presence of senile individuals when in fact the animals in question may be juveniles. Meso- and microwear on the occlusal surface is currently under investigation to obtain further criteria to describe these wear patterns. This is especially relevant if dental pieces that have undergone extreme wear are isolated. In such cases, it may be difficult to distinguish whether the wear is due to osteophagic practices or to the individual’s age, at least at macroscopic level. It is only possible to identify osteophagic wear on isolated teeth if they show differential wear in their lobes (Fig. 14).
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Fig. 11. Fossil mandibles with differential dental wear and breakage associated with herbivore osteophagic practices. a) Praeovibos cf. priscus mandible (ATA03-TD7-3-F15-1) from TD7-3 of Gran Dolina; b) C. elaphus mandible (ATA92-TN5-F25-45) from level TN5 of Galería; c) D. vallonnetensis mandible (ATA04-TD7-2-G5-4) from level TD7-2 of Gran Dolina; d) C. elaphus mandible (AR94-Ja-M49-21) from level J of Abric Romaní; e) E. ferus mandible (AR-c6) from level D of Abric Romaní.
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Fig. 12. Percentage of teeth affected by wear produced by osteophagia in Bosque de Riofrío actulistic samples (red deer and fallow deer) and fossil samples.
The osteophagia is an innate phenomenon amongst herbivores as a response to supply minerals deficiencies. Several authors (Barrette, 1985; Johns and Duquette, 1991; Grasman and Hellgren, 1993; Richard and Juliá, 2001; Mitchell et al., 2005) consider these deficiencies can be related to food stress periods, antler development, and pregnancy or lactation periods. In this study, all
individuals which sex could be assigned were male. This suggests that, in this context, osteophagia is a more habitual practice among males and, therefore, it may be related to antler growth. Hopefully, the cameras we installed in the Bosque de Riofrío will enable us to have a better knowledge of time of the year, rates of temperatures or specific moments in the life of the animals, to test this hypothesis.
Fig. 13. Damage associated with osteophagic practices in maxillae. a) Modern red deer maxilla from the Bosque de Riofrío (RF17-OTF-257) and b) fossil red deer maxilla from Abric Romaní (AR93-Ja-N47-9). The osteophagic differential dental wear is similar in both maxillae and mainly affects M1 and P3, but P4 is slightly altered.
Fig. 14. Left M1 (ATA07-TD6-2-F13-21) with differential wear in each of the lobes produced by bone consumption.
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5. Concluding remarks Results shown here describe a recurrent and characteristic differential dental wear affecting the middle area of the tooth row following a progressive wear pattern. This damage affects several specimens that inhabited a large but confined natural area, where extensive signs of osteophagia in various bones with different stages of chewing intensity (from grooves to fork morphologies) were already described in detail by Cáceres et al. (2011). The differential wear pattern now described in jaws is congruent with the way herbivores hold and chew bones (‘like a cigar’) and the abrasive nature of bone on teeth prepared to ground vegetal fibers using all cheek teeth. The distinct wear pattern observed in mandible teeth differs from the pattern observed in dental wear from maxilla (both in modern and fossil specimens), likely caused by the different movements and occlusal mechanism between maxilla-mandible. This differential dental wear has been identified in Pleistocene fossils which indicate that osteophagia goes back to prehistoric times as old as 780 kya. These fossil evidences suggest that osteophagic activity is related to behavioral patterns of animals in their natural environment and ecological context. Finally, differential dental wear needs to be distinguished from attritional dental wear to prevent mistakes assigning the age of the individual in fossil sites and to recognize oral and dental pathologies. Acknowledgments The authors are grateful to the Patrimonio Nacional for permission to undertake monitoring at the Bosque de Riofrío. We are truly grateful to the Riofrío rangers for their help, assistance and the use of their facilities in the forest. Thanks to our colleague and friend C. Tarazona, for their help with the field work. We want to thank the Atapuerca and Abric Romaní excavation team. The Ministerio de Ciencia y Investigación (CGL2009-12703-C03-02/BTE, CGL2007-66231, CGL2010-19825), Ministerio de Economía y Competitividad (CGL2012-38434-C03-03) and the Generalitat de Catalunya (SGR2009-188) supported this research. References Arsuaga, J.L., Gracia, A., Lorenzo, C., Martínez, I., Pérez, P.J., 1999. Resto craneal humano de Galería/Cueva de los Zarpazos (Sierra de Atapuerca). In: Carbonell, E., Rosas, A., Díez, J.C. (Eds.), Atapuerca: Ocupaciones Humanas y Paleoecología del Yacimiento de Galería. Memorias, vol. 7. Consejería de Educación y Cultura, Zamora, Junta de Castilla y León, pp. 233e236. Barnes, T.G., Varner, L.W., Blankenship, L.I., Fillinger, T.J., Heineman, S.C., 1990. Macro and trace mineral content of selected South Texas deer foragers. Journal of Range Management 43, 220e223. Barrette, C., 1985. Antler eating and antler growth in wild Axis deer. Mammalia 49, 491e499. Berger, G.W., Pérez-González, A., Carbonell, E., Arsuaga, J.L., Bermúdez de Castro, J.M., Ku, T.-L., 2008. Luminescence chronology of cave sediments at the Atapuerca paleoanthropological site, Spain. Journal of Human Evolution 55, 300e311. Bermúdez de Castro, J.M., Rosas, A., 1992. A human mandibular fragment from the Atapuerca Trench (Burgos, Spain). Journal of Human Evolution 22 (1), 41e46. Bermúdez de Castro, J.M., Pérez-González, A., Martinón-Torres, M., GómezRobles, A., Rosell, J., Prado, L., Sarmiento, S., Carbonell, E., 2008. A new early Pleistocene hominin mandible from Atapuerca-TD6, Spain. Journal of Human Evolution 55 (4), 729e735. Bredin, I.P., 2006. Phosphorus and Calcium Extraction from Bone Digestion in the Rumen of Sheep (Ovis Aries). Faculty of Veterinary Science, University of Pretoria, Pretoria, p. 81. Bredin, I.P., Skinner, J.D., Mitchell, G., 2008. Can osteophagia provide giraffes with phosphorus and calcium? Onderstepoort Journal of Veterinary Research 75, 1e 9. Brothwell, D., 1976. Further evidence of bone chewing by ungulates: the sheep of North Ronaldsay, Orkney. Journal of Archaeological Science 3, 179e182. Cáceres, I., Esteban-Nadal, M., Fernández Jalvo, Y., 2007. Mordeduras de herbívoro en el Bosque de Riofrío (Segovia). In: Sainz, M.L.R., Urquijo, J.E.G., Preysler, J.B.
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