New human burials from northern Jordan provide important insights into the appearance of cemeteries and the nature of human-animal relationships within mortuary contexts during the Epipalaeolithic period (c. 23,000–11,600 cal BP) in the Levant, reinforcing a socio-ideological relationship that goes beyond predator-prey. Previous work suggests that archaeological features indicative of social complexity occur suddenly during the latest Epipalaeolithic phase, the Natufian (c. 14,500–11,600 cal BP). These features include sedentism, cemeteries, architecture, food production, including animal domestication, and burials with elaborate mortuary treatments. Our findings from the pre-Natufian (Middle Epipalaeolithic) cemetery of ‘Uyun al-Hammam demonstrate that joint human-animal mortuary practices appear earlier in the Epipalaeolithic. We describe the earliest human-fox burial in the Near East, where the remains of dogs have been found associated with human burials at a number of Natufian sites. This is the first time that a fox has been documented in association with human interments pre-dating the Natufian and with a particular suite of grave goods. Analysis of the human and animal bones and their associated artefacts provides critical data on the nature and timing of these newly-developing relationships between people and animals prior to the appearance of domesticated dogs in the Natufian.

Funding: This research is funded by a Social Sciences and Humanities Research Council of Canada Research Grant to L. A. Maher and E.B. Banning (410-2007-1269; http://www.sshrc-crsh.gc.ca/ ), a National Geographic Society Committee for Research and Exploration Fieldwork Grant to L. A. Maher (8495-08; http://www.nationalgeographic.com/field/grants-programs/cre-fund.html ), and an Arts and Humanities Research Council Research Grant to J. T. Stock (AH/E009484/1; http://www.ahrc.ac.uk/Pages/default.aspx ). The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Copyright: © 2011 Maher et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

‘Uyun al-Hammam is a pre-Natufian burial ground, with elaborate human burials that include evidence for unique human-animal relationships, demonstrating that these features are not unique to the Natufian. The remains of at least eleven individuals, interred in eight graves, represent the earliest known cemetery in the southern Levant and more than double the number of human burials for the entire Early and Middle Epipalaeolithic periods [14] . Recent discoveries at ‘Uyun al-Hammam demonstrate a unique collection (in abundance and diversity) of grave goods and varied patterns of interment associated with the human remains. Two adjacent graves contain the articulated remains of several individuals, and include the following elements: 1) the earliest human-fox burial, 2) the movement of human and animal (fox) body parts between graves and, 3) the presence of red ochre, worked bone implements, chipped and ground stone tools, and the remains of deer, gazelle, aurochs and tortoise – grave goods that together became common among later Natufian and Neolithic burials. The ‘Uyun al-Hammam burials thus demonstrate intriguing human-animal relationships earlier than the first domesticated animal in the region. In light of the significance recently given to the Natufian “shaman” of Hilazon Tachtit [7] , our findings provide strong evidence that key aspects of these complex mortuary traditions occurred earlier in the Epipalaeolithic of the Near East than previously thought.

Despite early work that seemed to indicate a behavioural break between Early/Middle Epipalaeolithic and later, socially-complex Natufian sites (e.g., [2] ), new excavations suggest an earlier emergence of some of the features characteristic of the Natufian period [14] – [17] . Key features used to differentiate Natufian from preceding Epipalaeolithic groups include the appearance of formalized burial grounds and the origin of mortuary traditions that become characteristic of Neolithic symbolic and ideological life [6] . Two key mortuary practices demonstrate ideological continuity between the Natufian and Neolithic, while highlighting a break between the Natufian and earlier EP groups (e.g., [18] ): a) the movement or removal of skulls and, b) special human-animal relationships. For example, the burial of an adult female with a juvenile domestic dog is well-known from ‘Ain Mallaha (‘Eynan) [10] , while another human-dog burial comes from Hayonim Terrace [12] . Also, a unique burial from the Late Natufian site of Hilazon Tachtit features an elderly female buried with over 50 tortoise carapaces, several articulated raptor wings, the pelvis of a leopard, and the mandible of a wolf [7] . These unmodified animal parts could be viewed as evidence for changing human-animal interactions or domestication yet-to-come.

The archaeological record of the Epipalaeolithic period in the southern Levant (ca. 23–11.6 ka cal BP) exhibits considerable variability across time and space. A wealth of archaeological investigations suggest dramatic disparities in material culture between earlier and later phases [1] – [4] , explained in terms of pre-adaptive thresholds necessary for the development of subsequent Neolithic farming communities. The Late Epipalaeolithic Natufian culture is well-known for its stone architecture, organized site structures, portable art and decoration, and human burials, some of which display grave goods and personal ornaments. Formalized cemeteries, totalling more than 400 interments, appear for the first time [5] – [9] . These burials document a wide variety of mortuary practices, with treatments of the dead including stone and organic burial containers and installations, worked stone and bone grave goods and, notably, animal inclusions such as early domesticated dog ( [10] – [12] , although see [13] ). Elucidating the social meanings of these variable burial customs is challenging due to limitations of the material culture record and limitations of ethnographic comparisons. However, contextual examination of items accompanying human remains permits preliminary interpretations of this mortuary behaviour. For example, Grossman et al. [7] interpret an elderly female Natufian burial containing a unique array of grave goods as the first shaman burial.

Analysis

The Human Remains Grave I included two groupings of bones that we interpret as separate interment episodes identified as Burials A and B (Figure 3). In addition, a variety of miscellaneous bones are consistent with the interpretation of a minimum of two individuals for this grave (Table 2). Burial A includes a fragmentary adult pelvis articulated with lower limb elements, including a left and right femur, a left tibia and articulated bones of a left foot. Burial B includes an articulated but very fragmentary adult thorax, with thoracic vertebrae from T1 to T7, and associated right and left ribs. Among the miscellaneous elements were two adult femora, a left humerus, left scapula, left clavicle, left radius and ulna, which were articulated in situ, and all of which are consistent with a single adult individual. Isolated teeth and two mandibular fragments, one relatively robust and one gracile, were discovered in 2000 [21]. The reconstructed size, age and condition of these bones and teeth are also consistent with the other human remains in the grave. We inferred the distinction between Burials A and B on the basis that both appear to be articulated primary interments, with Burial A superimposed upon (and causing the partial disarticulation of) Burial B. The two adult femora that we associate with Burial B are clearly bilaterally paired, and thus belong to a single adult individual. PPT PowerPoint slide

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larger image TIFF original image Download: Figure 3. Grave I and VIII showing (A) the distribution of human remains and grave goods in each grave, and (B) blown-up photographs of select grave features. https://doi.org/10.1371/journal.pone.0015815.g003 PPT PowerPoint slide

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larger image TIFF original image Download: Table 2. Human remains and inferred burial associations from ‘Uyun al-Hammam graves discussed in the text. https://doi.org/10.1371/journal.pone.0015815.t002 Among the skeletal elements preserved, the pelvis from Burial A provides the only reliable sexually dimorphic traits, and is identified as a probable female on the basis of having broad sciatic notches (category 1, [22]). Discriminant function analysis of osteometric data collected from long-bones, including bone lengths, and diaphyseal and articular dimensions was used to further attempt sex determination (Supporting Information S1). Comparative samples included Levantine Epipalaeolithic skeletons where sex had been determined from pelvic morphology. The discriminant analysis provided ambiguous and male classifications of the two femora of Burial A, while all long bones in Grave I were classified as male. While this is not a conclusive sex determination, given the evidence from the Burial A pelvis, the results suggests that Grave I likely contains interments of one adult female (Burial A) and one adult male (Burial B). Grave I is taphonomically complex. Subsequent to interment, Burial B appears to have been partially re-opened and another adult individual (Burial A) was interred in the same general area. This burial is represented by a pelvis and articulated lower limbs, which overlie the humerus and vertebral column of Burial B. The thorax, upper limbs and skull of Burial A may have been removed during road construction and subsequent erosion at the terrace edge. Burial A was found with a few small chunks of red ochre (that may have originated from Burial B), and a large limestone pounder lay adjacent to the individual's right femur. Burial B consists of an adult buried together with an articulated fox skull and humerus, a worked bone dagger, chipped and ground stone tools, and unmodified animal bones all lying on a continuous layer of red ochre (see below). The location of disarticulated remains in Grave I suggests that their movement occurred relatively soon after death or initial interment. During decomposition, joints of the limb generally disarticulate from proximal to distal, while the thorax and spine remain articulated with connective tissue much longer [23]. Excavation of the articulated ribs and vertebrae of Burial B revealed no scapulae underneath. Therefore, if the burial was disturbed after partial decomposition it is plausible that the upper limbs, scapula, clavicle and skull were detached and moved, while the ribs and vertebrae remained intact and ulna and radius articulated. Only upper limb elements from the left side are represented from Burial B, and most extend to the north-east of the thorax. Red ochre underlay the bones in a relatively continuous manner around the rib cage, but occurred more as infrequent chunks around the other isolated bones. Movement of the remains of Burial B after partial decomposition may also explain the missing skull, cervical vertebrae and right arm elements (see below). Grave VIII is immediately adjacent to Grave I; approximately 10 cm separates objects associated with each grave (excavated in subsequent years, Figure 3). Grave VIII includes both articulated and disarticulated human remains along with a bone spoon or spatula, chipped and ground stone implements, and several unmodified animal bones, including deer antler and a fox skeleton missing only its skull and right humerus (Figure 3). Human remains included a fragmentary cranium and mandible of an adult with erupted third molars and considerable tooth wear on all molars. The skull featured a prominent glabella and robust left supraorbital margin (categories 5 and 4 respectively, [22]), with prominent superciliary arches. While these suggest the possibility that the skull represents a male, this determination cannot be made with confidence on the current evidence. A large, flat, water-worn stone was brought from the nearby wadi and placed over the skull, while another similar stone was found ∼20 cm to the southwest, adjacent to a wild goat horn core (Capra sp.) and several articulated tortoise carapaces (Figure 3). All seven cervical vertebrae were articulated with the base of the skull, but there was 180 degree rotation between atlas and axis, so that the vertebral spines face towards the left, anterior and inferior side of the skull. No other skeletal elements were articulated, suggesting that the skull and cervical vertebrae had been disarticulated from a body and placed here, or moved from another burial (possibly Grave I). While there is no positive evidence that this skull has been moved from Grave I, there is no duplication of cranial or vertebral elements between the graves and many skeletal elements from Burial B (also male) in Grave I are co-mingled, so we cannot rule this possibility out. Grave VIII also included very fragmentary tibia and fibula, in articulation, and a left humerus, scapula, radius and ulna, representing an articulated arm of an adult. Discriminant analysis of humeral metrics suggests that these elements represent an adult female. While the upper limb is situated near the skull, the orientations, different sex determinations, and lack of elements articulating these remains mean that they cannot conclusively be identified as representing the same individual.

The Earliest Fox-Human Burial Grave I included an articulated fox skull, lying on its right side, underneath the articulated human ribs of Burial B (Figure 3). Although distorted by post-depositional crushing, the skull is remarkably intact (Figure 4). The complete right humerus of a fox was found directly below and adhering to the right side of the mandible. Large pieces of red ochre were found adhering to the underside of the human ribs on both left and right sides, while ochre fragments adhered to the nasal bones, mandible and right side of the fox cranium, as well as in the sediment within the skull cavity. The red ochre here is dense and continuous, suggesting that fox skull and human rib cage were placed on top of a layer of red ochre (Figure 3) as part of the primary interment episode of Burial B. PPT PowerPoint slide

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larger image TIFF original image Download: Figure 4. The red fox skull from Grave I after conservation and reconstruction. https://doi.org/10.1371/journal.pone.0015815.g004 A morphological comparison was made between the fox skull and 30 skulls representing various canid species, including Pleistocene specimens of Near Eastern canids, archaeological specimens of wolves, foxes and jackals from sites in the Near East, as well as domesticated dogs from Jericho. The closest match based on size and morphology was the Red Fox (Vulpes vulpes), a species known to inhabit the area in the late Pleistocene. A nearly complete fox skeleton, missing its skull and right humerus, was discovered in Grave VIII (Figure 3) adjacent to a bone ‘spoon’, red deer antler, several large flint blades and flakes and several flat unmodified cobbles (see below). The fox skeleton is located 50 cm northwest of the fox skull in Grave I (Figure 3). The size and morphology of the skeleton is consistent with that of the nearby skull. The skeleton has only a left humerus (length = 117.2 mm) while a right humerus (length = 117.0 mm) was found adhering to the skull in Grave I. Considering their proximity, adult status, and the complementary representativeness of elements, we suggest that the skull from Grave I and the post-cranial skeleton from Grave VIII belong to the same animal. The metric similarity of the humeri strongly supports this interpretation.