To catch a chameleon, or actualism vs. natural history in the taphonomy of the microvertebrate fraction at Qesem Cave, Israel

Journal of Archaeological Science 40 (2013) 3326e3339

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To catch a chameleon, or actualism vs. natural history in the taphonomy of the microvertebrate fraction at Qesem Cave, Israel K.T. Smith a, *, L.C. Maul b, R. Barkai c, A. Gopher c a

Department of Palaeoanthropology and Messel Research, Senckenberg Research Institute, Senckenberganlage 25, 60325 Frankfurt am Main, Germany Senckenberg Research Station of Quaternary Palaeontology, Am Jakobskirchhof 4, 99423 Weimar, Germany c Institute of Archaeology, Tel Aviv University, Tel Aviv 69978, Israel b

a r t i c l e i n f o

a b s t r a c t

Article history: Received 29 October 2012 Received in revised form 12 February 2013 Accepted 22 February 2013

Qesem Cave is a unique Middle Pleistocene, hominin-bearing site in Israel that contains a rich microvertebrate accumulation. The microvertebrates are highly unusual in that half of them are from small reptiles, and most of the reptiles are chameleons, which are otherwise rare in the fossil record. Analysis of the lower vertebrate component shows uniform taphonomic characteristics: on average 17.6% of specimens show evidence of corrosion (the vast majority light), and specimen breakage is between 4.9 and 12.0%, depending on metric. Charring is negligible. Most species are small (body mass <60 g). These taphonomic attributes do not vary in the studied portion of the stratigraphic profile, nor do they systematically vary between taxa. Thorough study of all skeletal parts suggests that most individuals probably entered the cave as whole animals; the only exception is the large glass lizard, Pseudopus, which is represented mostly by the tail. These taphonomic data suggest a Barn Owl as the predominant accumulator. However, natural history observations on Barn Owls and chameleons are strongly at odds with this actualistic inference: Barn Owls are nowhere recorded as a major predator on chameleons. We argue that a focus on extant, especially European, populations could distort our understanding of their feeding biology and is vulnerable to counterexample. We propose a scenario that harmonizes actualism and natural history. We further identify a possible owl roost in Qesem Cave, the first time such a roost has been identified in a collapsed cave setting. These conclusions may have conservation implications for chameleons. They also suggest that the hearth adjacent to the microvertebrate concentration was situated in the twilight zone. Ó 2013 Elsevier Ltd. All rights reserved.

Keywords: Taphonomy Microvertebrates Reptiles Barn Owl Actualism Qesem Cave

1. Introduction William Buckland (1824) concluded that collections of larger “ante-diluvial” bones in caves could be attributed to macropredators, especially hyenas. Microvertebrates also occur in caves, often in great numbers, and Buckland (1824: 35e36) was at a loss to explain them. After owl pellet analysis was introduced in the 19th century to study the food spectrum of birds of prey (e.g., Altum, 1863), the paleontologist Liebe (1878) was one of the first to recognize that many such fossil assemblages may be attributed to owls. Intact fossilized pellets are only rarely found (see Tobien, 1977), for they quickly disintegrate, leaving numerous isolated bones wherever owls roost or nest (Terry, 2004). Other biological agents for the perimortem or postmortem concentration of microvertebrate remains are also recognized, including diurnal

* Corresponding author. Tel.: þ49 69 75421218. E-mail address: [email protected] (K.T. Smith). 0305-4403/$ e see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.jas.2013.02.022

birds of prey (Mayhew, 1977), mammalian carnivores (Andrews and Evans, 1983; Mellett, 1974), fossorial rodents (e.g., Brain, 1981; Hoffman and Hays, 1987; Thomas, 1971; Vaughan, 1990), and modern harvester ants, Myrmicinae (Hatcher, 1896; Matthias and Carpenter, 2004; McKenna, 1994; Shipman and Walker, 1980). Considerable effort has been devoted to identifying predator accumulations on the basis of observable characteristics of fossil remains (e.g., Andrews, 1990; Brain, 1981; Buckland, 1824; Stahl, 1996) and to distinguishing them from non-biological enrichments. In order to infer the mode of accumulation, rich and well-documented samples are required. This is the case for Qesem Cave. Qesem Cave (Fig. 1) is a late Lower Paleolithic (400e200 ka) archeological site in Israel (Barkai et al., 2003; Gopher et al., 2005, 2010) whose importance lies in its uniquely detailed record of late middle Pleistocene hominin behavior (Boaretto et al., 2009; Shimelmitz et al., 2011; Stiner et al., 2009, 2011; Verri et al., 2005), including rich Acheulo-Yabrudian lithic industries (Barkai et al., 2005, 2010; Gopher et al., 2005; Lemorini et al., 2006) and the

K.T. Smith et al. / Journal of Archaeological Science 40 (2013) 3326e3339

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2. Setting and fossil occurrence

36°

34°

32°

30°

28° 26°

28°

30°

32°

34°

36°

38°

Fig. 1. Map showing the location of Qesem Cave (star) in the Levant.

tool-makers themselves (Hershkovitz et al., 2011). Of special relevance to its investigation are copious accumulations of wellpreserved microvertebrate remains. One of them was recently uncovered at a deep stratigraphic level near the center of the cave. The other, the focus of this paper, was discovered in 2006 in the eastern part of the cave and systematically excavated since 2008 (Maul et al., 2011). These assemblages offers an unparalleled opportunity to explore human ecology at Qesem Cave and its relation to environmental circumstance. The microfaunal spectrum of the eastern accumulation, at least, is highly unusual for a cave site. In particular, it contains a very high proportion of lower vertebrates (mainly reptiles, with one fish and rare amphibians), 49% of identified specimens in the sample studied here. In itself this is extra-ordinary, for no described microvertebrate accumulation in the circum-Mediterranean region (e.g., Belmaker and Hovers, 2011; Marder et al., 2011; Salotti et al., 2008; Stoetzel et al., 2012; Tchernov, 1996, 1998) is reported to contain such a high proportion of lower vertebrates. More unusual still is that most of the reptile remains represent a species of chameleon. Even in areas where chameleons are common, their cryptic coloration (Cooper and Greenberg, 1992) and behavior (Greene, 1988) protect them from major visual predators. It is therefore no surprise that chameleons, although they have been reported in some deposits, are not so abundant (Hooijer, 1961). The Qesem microvertebrate assemblage is thus an interesting case. In order to achieve their potential to elucidate hominin ecology, it is necessary to understand the mode of accumulation of the microvertebrates. In this paper we present a taphonomic analysis of the eastern microvertebrate assemblage, with special reference to the lower vertebrates, in an attempt to infer the mode of accumulation in the most parsimonious manner. We draw on actualistic data (corrosion, breakage, etc.) and also on a wealth of natural history observations. As will be seen, some of these data are starkly contradictory. This first look at microvertebrate taphonomy in Qesem Cave focuses on the lower vertebrates, because they constitute half the assemblage, and because the high incidence of chameleons is one of its most salient features. Later work will treat the taphonomy of the micromammals.

The Qesem Cave sequence is divisible into a lower and an upper sequence (Karkanas et al., 2007). The lower sequence is characterized by fine-grained sediment, probably derived from terra rossa soil outside the cave and deposited by mud slurries across the cave floor, which was studded with limestone blocks derived from roof spalling. When the lower sequence was deposited, the cave was closed to light, apart from the entrance zone (Frumkin et al., 2009). The upper sequence was deposited after a cave-in and is dominated by anthropogenic sediment (ash); root-casts indicate the cave was open to light (Karkanas et al., 2007) following several phases of roof collapse (Frumkin et al., 2009). The microfauna of the eastern accumulation was briefly presented by Maul et al. (2011). Collections up through the year 2008 contain 3283 specimens identified at least to class level (Amphibia, Aves, Reptilia, or Mammalia). Fossils first occur at 320 cm below datum, but they are very rare until 360 cm, and only become abundant below 460 cm (see Maul et al., 2011: Fig. 2). Thus, most specimens were extracted from the upper-most part of the lower sequence, but some come from the lower part of the upper sequence. Calling it the microvertebrate “fraction” could suggest that the microvertebrates were part of a more complete collection and were arbitrarily segregated based on size. In fact, the microvertebrates form a natural spatial unit, for they are highly restricted in distribution (see Maul et al., 2011: Fig. 5). Large mammal bones and lithics were also found in the sediment of this part of the cave, but we have excluded them from consideration here. 3. Materials and methods Taphonomic data were collected on all 1622 lower vertebrate specimens collected in the year 2006 from the eastern microvertebrate accumulation, i.e., the majority of the identifiable lower vertebrates reported in Maul et al. (2011). The specimens all come from the interval 495e545 cm below datum. The lower vertebrates were all sorted by the first author. For the purpose of analysis, the assemblage was treated as a whole, and divided taxonomically, and binned into analytical units 10 cm in thickness. 3.1. Relative abundance Number of identified specimens (NISP) and minimum number of individuals (MNI; White, 1953) were tallied per element type. Elemental representation Ri (“MNI per skeletal portion” of Lyman, 1994) was calculated in the usual way (Andrews, 1990) as NISP per element i O (Ei  MNI), where Ei is the number of element i in an organism (except for serially homologous elements like vertebrae, 1 or 2). MNI per element type is based solely on the highest number of left/right specimens of an element. Other attributes, such as extent of wear of teeth or ontogenetic stage, could not be evaluated with sufficient rigor to refine this estimate. Maximum MNI per element type gives MNI (with respect to organisms). For the purpose of these tallies, cervical and sacral vertebrae were counted among the “dorsals.” The braincase was treated as a single unit. Fusion of its components during the course of postembryonic ontogeny makes its treatment difficult. Basisphenoids, prootics, basioccipitals, otoccipitals, and supraoccipitals are sometimes found isolated, sometimes partially fused, and sometimes completely united; in one case, the otoccipital was inseparably fused to the basal elements only unilaterally. Treating the endocranial elements together makes little difference for the purpose of these analyses.

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3.2. Corrosion Corrosion was determined by examining bone surfaces under a binocular microscope for characteristic fine-scale pocking and roughening (Fig. 2B) of the normally smooth bone (Fig. 2A), which removes the surficial shine. Corrosion is accompanied by discoloration: the beige-colored bone surface becomes cream-colored to white (see Inline Supplementary Fig. S1). Nearly all specimens were examined for corrosion, excepting a few completely encrusted by carbonate. Inline Supplementary Fig. S1 can be found online at http://dx. doi.org/10.1016/j.jas.2013.02.022. 3.3. Breakage Original breaks were distinguished from postdepositional breaks (especially those generated during excavation) in several ways. First, original breaks often do not have such sharp edges, because the breaks may not have been so clean to begin with and can subsequently have been corroded. Second, original break surfaces show some evidence of precipitation (calcite, manganese

dioxide, etc.). An original distal break in a maxilla is show in Fig. 2C; a recent break is shown in Fig. 2D. Postdepositional breaks are present on nearly all specimens to some extent, and when a specimen represents only half a bone, it cannot be determined how complete the specimen originally was. These specimens were scored ?. A scoring system similar to Hoffman’s (1988) for recording completeness was used, whereby a bone is divided into quadrants designated A, B, C and D. For elongate bones (maxilla, pterygoid, prefrontal, jugal, postorbit(ofront)al, squamosal, quadrate, dentary, angular, surangular, articular, girdle bones, limb bones, and, for Chamaeleo, parietal) these were considered a serial arrangement (Fig. 2E). For other bones (ectopterygoid, frontal, parietal, vertebrae) they were stacked. In scoring the vertebrae, the neural spine was ignored, as it was missing in the vast majority of specimens from this collection, usually as a result of recent breaks. (In more recent collections, in which the vertebrae were picked from sediment before screenwashing, these processes are usually intact.) A quadrant was counted as present when a majority of it was complete. The quadrants were used as quantile estimates of completeness, taking a value of 25 (A, B, C, D), 50 (AeB, BeC, CeD), 75 (AeC, BeD) or 100 (AeD) for

Fig. 2. Corrosion on bones preserved in the microvertebrate accumulation. (A) Uncorroded bone surface on dorsal vertebra of Chamaeleo (M/14b, 505e510, box 161-d5). (B) Light corrosion visible on dorsal vertebra of Chamaeleo (M/14b, 505e510, box 161-b10); light carbonate precipitation covers the bone surface in some areas, but pocking is particularly clear on the right and left sides of the micrograph at mid-height. Because of the directionality of the electron beam, pocks or depressions (corrosion) can be distinguished from bumps or prominences (precipitation). (C) Original distal break (arrow) in left maxilla of Chamaeleo (M/14b, 500e505, box 157-c1). (D) Recent break (arrow) in right maxilla of Chamaeleo (M/14b, 535e540, box 187-b4). (E) Whole right maxilla of (M/14b, 510e515, box 168-a1), showing quadrants used for breakage analysis.

K.T. Smith et al. / Journal of Archaeological Science 40 (2013) 3326e3339

each specimen. Thus, every specimen is necessarily at least 25% complete in this system. Completeness was also calculated for cranial and postcranial bones separately. Additionally, the cranial bones were divided into posterior (occipital bones, parietal, squamosal, quadrate, surangular, articular/compound bone) and anterior elements for separate analysis. Mean completeness was calculated as the average of all specimens in a set. This quadrant system will tend to generate higher completeness estimates than a simple binary scoring system. If every bone necessarily receives a score of at least 0.25, the average will rise. If every broken bone is broken only once and all fragments are recognized, then mean completeness values for a collection of bones will vary between 0.5 and 1.0. If the smaller of two broken parts is less likely to be recognized, then the value will rise still further. Thus, a traditional binary scoring system, whereby each specimen is considered broken or not broken, was also used, and results are analyzed separately. 3.4. Discoloration & other surface modification Small black flecks are present on almost all specimens, similar to those usually identified as manganese oxides (e.g., Stoetzel et al., 2012), presumably manganese dioxide (Oakley, 1956). Although the difference between charring and discoloration by mineral deposition is not always obvious (Shahack-Gross et al., 1997), the highly localized nature of these flecks clearly indicates that they are mineral precipitates. Most of the microvertebrate bones at Qesem Cave are beige in color, although the color can also vary to reddish-brown. Rarely, the bone is noticeably darkened, taking on a deep brown or black tone. This discoloration is tentatively interpreted, in the absence of histological, chemical or microstructural evidence (Brain and Sillen, 1988; Hanson and Cain, 2007), as evidence of strong heating or burning (Shipman et al., 1984), leading to the carbonization of the organic compounds (Brain, 1981). Root traces are recognized on specimens from the microvertebrate accumulation as linear, sometimes branching channels (Andrews, 1990) of nearly uniform width. Because most bone surfaces are so smooth, it is relatively easy to recognize these channels. 4. Results 4.1. Relative abundance and element representation The single species of Chamaeleo is the most abundant species of lower vertebrate at Qesem Cave (Maul et al., 2011). Specimens of Chamaeleo constitute 65% of the total number of lower vertebrate specimens (NISP) (Table 1); the second and third most abundant taxa are Pseudopus (20%) and Stellagama (13%) (on the name, see Baig et al., 2012). Relative fossil abundance attempts to be a Table 1 Relative abundance of lower vertebrate specimens based on NISP in the Qesem Cave microvertebrate accumulation. Taxon

NISP

Rel. Ab. (%)

NISP cranial

Rel. Ab. (%)

Testudines Chamaeleo Stellagama Pseudopus Lacertidae Gekkonidae Scincidae Colubroidea Anura TOTAL

11 1039 211 313 8 3 1 6 9 1601

0.7 64.9 13.2 19.6 0.5 0.2 0.1 0.4 0.6

3 358 70 4 3 3 1 0 0 442

0.7 81.0 15.8 0.9 0.7 0.7 0.2 0.0 0.0

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measure of relative organismal abundance, and because species with elongated bodies (i.e., Pseudopus, snakes) often have many more vertebrae than typical lizards (see below), and because osteoderms vastly outnumber all other bones when they are present (as in Pseudopus), it is more useful to compare only the cranial elements (Smith, 2006), which are approximately equally abundant among lizard and snake species. By this measure, Chamaeleo forms 81% of the assemblage, followed by Stellagama (16%) (Table 1). All other species are individually <1% of the assemblage. Note that the tentative identification of Varanus sp. based on a specimen from the 2006 collection (Smith in Maul et al., 2011) was in error. The minimum number of individuals (MNI) paints a similar portrait, albeit one with reduced numbers (Table 2, which excludes podial and metapodial elements and phalanges). A minimum of 44 individuals of Chamaeleo are represented (77.2%, considering only squamates); there are 7 of Stellagama (12.3%), 2 of Colubroidea indet. (2 species, together 3.5%) and 1 each of Pseudopus, Gekkonidae indet., Lacertidae indet., and Scincidae indet. (1.8% each). Element representation provides further insight. Expected proportions of the various cranial elements are standard. “Dorsal” count in Chamaeleo (see Section 3.1) may have been 24 (based on Chamaeleo chamaeleon SMF 33202 and Klaver, 1981). In Chamaeleo africanus, in contrast, dorsal count is 25 (UMMZ 181145, ZFMK 5151). Although there is no inevitable relation between dorsal and caudal vertebral counts (e.g., Polly et al., 2001), the dorsal counts given above may suggest slightly lower caudal vertebral number in C. chamaeleon than in C. africanus. In the latter (ZFMK 5151), this number is about 64. Dorsal count in Stellagama stellio CM 39115 and 39116, from the same locality, is 26 and 27, respectively. Caudal vertebral number in the latter was poorly constrained, but in the former it was about 36. Pseudopus apodus CM 38478, finally, had 55 dorsal and about 115 caudal vertebrae (within the ranges given by Obst, 1981). As a whole, dentigerous elements (maxillae and dentaries in Chamaeleo, dentaries in Stellagama) are the most abundant (Table 2). In both species, a dentigerous element gives the highest estimate of MNI (maxilla for Chamaeleo, dentary for Stellagama). In Chamaeleo, prefrontal and jugal were also represented by proportions of nearly 50%; postorbitofrontals, parietals, and dorsal vertebrae by proportions of about 30%. All other elements were rarer. The particularly low proportion of caudal vertebrae may be due to oversight during picking, which was not conducted under a microscope. The tail in chameleons is not fragile (Etheridge, 1967), but distal caudal vertebrae are especially small. In Stellagama, ectopterygoid, frontal, parietal, and endocranium were all represented by proportions of 50e60%, and the coronoid and compound bone by >40%. The dorsal vertebrae in this taxon show a proportion similar to caudal vertebrae and also to dorsal vertebrae of Chamaeleo. The tail in Stellagama does not have intravertebral fracture planes (Etheridge, 1967); however, the tail is found to have broken intervertebrally with high frequency (about 50%) in large samples of the species (Arnold, 1984). This suggests that Ri for Stellagama caudal vertebrae may be an underestimate. The most obvious similarity between the relative elemental abundances of Chamaeleo and Stellagama are in the dentigerous elements (Table 2), but this is not enough to sway the general lack of correspondence. Using least-squares regression, there is no significant relationship between the relative elemental abundances of the two taxa, whether the most fragile and rarest bones e premaxilla, nasal, and palatine e are excluded (slope ¼ 0.05, P ¼ 0.88) or not (slope ¼ 0.33, P ¼ 0.23). Similar results obtain for Spearman rank correlation, as conducted by Hoffman (1988) (r ¼ 0.10, P ¼ 0.73; and r ¼ 0.32, P ¼ 0.20, respectively). In Pseudopus the caudal vertebrae appear to be unusually abundant. The ratio of dorsal to total vertebrae in P. apodus CM

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Table 2 Abundance of lower vertebrates in the Qesem Cave microvertebrate accumulation. NISP and MNI are given per element type, as is elemental representation Ri for the two most abundant taxa, Chamaeleo and Stellagama. NISP here differs from the values in Table 1 because this table does not include phalanges or metapodial elements. Chamaeleo

Premaxilla Maxilla Nasal Palatine Pterygoid Ectopterygoid Prefrontal Jugal Frontal Postorbit(ofront)al Parietal Squamosal Quadrate Endocranium Dentary Coronoid Angular Compound bone Dorsal vertebrae Caudal vertebrae Scapula Coracoid Interclavicle Humerus Ilium Ischium Pubis Femur Osteoderms Total/max Cranial

Lacertidae

Gekkonidae

Scincidae

MNI

NISP

Actual (%)

MNI

Stellagama NISP

Actual (%)

MNI

Pseudopus NISP

MNI

NISP

MNI

NISP

MNI

NISP

0 44 0 1 0 7 25 24 10 14 14 9 9 4 35 4 n.a. 8 14 (14.0) 5 (4.4) 4 0 n.a. 1 0 1 0 0 n.a. 44 44

0 82 0 1 0 11 41 51 10 25 14 18 16 8 60 8 n.a. 12 335 281 7 0 n.a. 1 0 2 0 0 n.a. 983 357

0.0 93.2 0.0 1.1 0.0 12.5 46.6 58.0 22.7 28.4 31.8 20.5 18.2 18.2 68.2 9.1 n.a. 13.6 31.7 10.0 8.0 0.0 n.a. 1.1 0.0 2.3 0.0 0.0 n.a.

0 3 1 1 3 5 3 1 4 2 4 1 2 3 7 3 1 4 3 (2.2) 2 (1.9) 0 0 1 1 1 0 2 0 n.a. 7 7

0 4 1 1 4 7 4 1 4 4 4 2 4 4 13 6 1 6 56 67 0 0 1 2 1 0 2 0 n.a. 199 70

0.0 28.6 7.1 7.1 28.6 50.0 28.6 7.1 57.1 28.6 57.1 14.3 28.6 57.1 92.9 42.9 7.1 42.9 30.8 26.6 0.0 0.0 14.3 14.3 7.1 0.0 14.3 0.0 n.a.

0 0 0 0 0 0 0 1 0 1 0 1 0 0 0 0 0 0 1 (0.02) 1 (0.14) 0 0 0 n.a. 0 n.a. n.a. 0 n.a. 1 1

0 0 0 0 0 0 0 2 0 1 0 1 0 0 0 0 0 0 1 17 0 0 0 n.a. 0 n.a. n.a. 0 291 313 4

0 0 0 0 0 0 0 0 1 0 0 0 1 0 0 0 0 1 1 0 0 0 0 1 0 0 0 0 0 1 1

0 0 0 0 0 0 0 0 1 0 0 0 1 0 0 0 0 1 4 0 0 0 0 1 0 0 0 0 0 8 3

0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 1 0 0 0 0 0 0 0 0 0 0 n.a. 1 1

0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 2 0 0 0 0 0 0 0 0 0 0 n.a. 3 3

0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 1

0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 1

38478 is w0.32, whereas in the fossil material the ratio is much lower, 0.06 (Table 2). Assuming dorsal and caudal vertebrae have the same detection probability, the probability of drawing so low a number of dorsal vertebrae given this ratio and a simple binomial model is 0.01. If there is a size bias working against distal caudal vertebrae, this would serve to magnify the discrepancy. Thus, the ratio of dorsal to caudal vertebrae in the deposit is significantly different from the ratio in the living animals, with caudal vertebrae much more common. The tail in Pseudopus, like in Stellagama, is not fragile in the normal manner for lizards, and fracture planes are absent on caudal vertebrae (Etheridge, 1967; Fig. 4A). However, Obst (1981) notes that the tail can be detached. 4.2. Size The majority of the squamate taxa are small. Comparisons with living species (to which the fossils are highly similar, if not conspecific) are useful. Adult C. chamaeleon (at least 1 year old) in northern Israel have a mean snout-vent length (SVL) of about 10 cm and a mean mass of 35 g (Keren-Rotem et al., 2006). Adult male S. stellio in the Levant have a snout-vent length of 8e13 cm (Daan, 1967); Hertz et al. (1983) reported mean mass in lowland populations to be 36 g (range up to 39 g). The lacertids and gekkonids are smaller than this, and the scincid is much smaller still. The only exception among the “lizards” is P. apodus, whose SVL may reach 53 cm (Meiri, 2008); a 42-cm (SVL) specimen was reported by Gans and Gasc (1990) to have a total body mass of 510 g. As noted in the previous section, however, the tail can break in Pseudopus, and the overrepresentation of caudal vertebrae suggests that the tail most frequently entered the cave separated from the body. Thus, Pseudopus need not represent an exception to the generalization that all squamate specimens represent animal (parts) <60 g in mass.

The turtles, identified as Testudo cf. graeca by Stiner et al. (2009, 2011), are also generally very small, not just the material listed here but also all other collected material in the microvertebrate area. The two humeri in the present sample are representative with regard to size, measuring just 10.2 and 13.1 mm in length. A set of eight specimens of Testudo graeca (Hebrew University of Jerusalem, Natural History Collection, HUJ Z-81, 125, 126 and two uncataloged specimens; and SMF 58700, 67583, 69733) suggest a nearly isometric relationship between humerus length in mm (H) and plastron length in mm (P), P ¼ 3.6H (almost identical, if the intercept is not constrained to be 0). Extrapolating this equation for the two humeri (from 505 to 515 cm below datum), it is clear that the tortoises were very small, with estimated plastron lengths of 37 and 47 mm, respectively. The former corresponds to a mass of about 13 g (reviewed in Buskirk et al., 2001). One unit e 505e510 cm below datum in subsquare M/14b e contains a relatively large number of turtle specimens (five), of which two (cervical vertebra and ungual phalanx) are quite large. The ungual, in particular, suggests a large animal. For reasons of size also, it is not clear that the ungual and cervical pertain to the same individual. 4.3. Corrosion Overall, most specimens are unaffected by corrosion (Fig. 2A). Only 282 (17.6%) of the 1598 specimens that could be examined for corrosion showed any evidence of it. When only those specimens are included which could be identified to the taxonomic level used here, the fraction of corroded specimens (278/1578) is unchanged (Table 3), indicating that it is not influenced by the destruction of specimens. Corrosion is usually light (Fig. 2B): only 26 (9.2%) of those cases (or 1.6% overall) were judged to be more severe. When

K.T. Smith et al. / Journal of Archaeological Science 40 (2013) 3326e3339 Table 3 Corrosion frequencies on specimens in the microvertebrate accumulation, divided by taxon. Taxon

N

Percent corroded

Testudines Chamaeleo Stellagama Pseudopus Lacertidae Gekkonidae Scincidae Colubroidea Anura TOTAL

8 1024 209 311 8 3 1 6 8 1578

12.5 19.2 13.9 14.5 0.0 0.0 0.0 66.7 12.5 17.6

the sample is partitioned by taxon, it is seen that the proportion of corroded specimens varies only slightly (for the more abundant species). At 19.2%, it is highest in Chamaeleo; it is lower in Stellagama (13.9%) and Pseudopus (14.5%). A cause for this discrepancy is not immediately apparent, but only 1 of every 20 specimens differs in this respect between Chamaeleo and the others. Colubroid snakes (represented by a couple of species) are possibly the only divergent taxon: two-thirds of specimens showed corrosion. However, the proportion is based on only 6 specimens. Corrosion proportions are also nearly constant throughout the profile (Fig. 3A), generally varying from 16.3 to 19.4%. The only weak departure is in the uppermost level, where only 12.1% of specimens were corroded. This level also has the lowest number of observations (107, vs. 299 or more in all other levels). 4.4. Breakage Averaged over the entire assemblage, breakage based on the quantile system is 4.9% (Table 4). Where sample size is high, a difference is apparent between Pseudopus on the one hand (0.3%) and Chamaeleo (6.6%) and Stellagama (4.2%) on the other. This difference reflects differences in the average completeness of cranial vs. postcranial (chiefly vertebrae, for Pseudopus also osteoderms) elements. The Pseudopus fraction is dominated by osteoderms, which are nearly without exception complete. Stellagama and Chamaeleo share a similar pattern in which the postcranial specimens are almost always complete (1.4 and 1.3% breakage, respectively) but the cranial specimens are distinctly less complete (10.8 and 20.0% breakage, respectively). Using a binary scoring system (see Section 3.3), average breakage of the total assemblage is higher, 12.0% (Table 5). As with the quadrant system, a notable difference is observed between cranial and postcranial bones, which have average breakage proportions of 44.6 and 2.5%, respectively. Vertebrae are more

495 - 505

A

505 - 515

B

Fraction corroded

Fraction broken

C

Fraction burned

Table 4 Breakage of specimens in the microvertebrate accumulation, divided by taxon and body part. For proportions of cranial bones only (right three columns), “all” is the weighted average of anterior and posterior cranial bones. Breakage is calculated using the quadrant system described in Section 3.3. Taxon

Testudines Chamaeleo Stellagama Pseudopus Lacertidae Gekkonidae Scincidae Colubroidea Anura TOTAL

525 - 535 535 - 545 0.0

0.4

0.8

0.0

0.4

0.8

0.0

0.4

0.8

Fig. 3. Stratigraphic distribution of taphonomic attributes of specimens recovered in the microvertebrate accumulation from 495 to 545 cm below datum. (A) Fraction of specimens showing corrosion (>90% of it light). (B) Fraction of specimens showing breakage, quantified using the quadrant system. (C) Fraction of specimens showing marked darkening, interpreted as burning.

N

10 880 280 298 7 3 1 5 7 1491

Total breakage

Cranial

Body

All

Anterior cranial

Posterior cranial

17.5 6.6 4.2 0.3 0.0 0.0 25.0 0.0 0.0 4.9

25.0 20.0 10.8 0.0 0.0 0.0 25.0 e e 14.8

25.0 19.7 9.7 0.0 0.0 e 25.0 e e

e 20.9 16.7 0.0 0.0 0.0 e e e

14.4 1.3 1.4 0.2 0.0 e e 0.0 0.0

geometrically compact than typical cranial bones, which may partly account for their completeness (quadrates are also notably usually complete), but it is also worth noting that all seven Chamaeleo scapulae were whole. Some predatory birds will destroy the posterior portion of the skull in feeding (see, for example, Chitty, 1938; Dodson and Wexlar, 1979), so it is useful to inquire whether posterior bones were more subject to breakage than anterior bones. In Chamaeleo, both posterior and anterior cranial bones showed similar breakage proportions (Table 4), whereas in Stellagama the posterior cranial bones tended to be more frequently broken (16.7%) than anterior ones (9.3%). Mean element breakage is similar throughout the stratigraphic profile (Fig. 3B). The proportion of broken bones varies from 5.6 to 3.4% using the quadrant system. The only slight departure is in the uppermost level, where average breakage was 8.1%. This level also has the lowest number of observations (80, vs. 276 or more in all other levels).

4.5. Burning Dark discoloration, equated here with burning, affects only a tiny percentage of specimens, on average 1.9% (Table 6). In one case only a part of a specimen was blackened: a caudal vertebra of Pseudopus, where the neural spine is strongly affected, but not the body (Fig. 4A). There do not appear to be major divergences between taxa. Lacertids have a higher percentage (12.5%) but a low specimen number, so this figure (1/8) is probably a sampling artifact. It may be noteworthy that Pseudopus showed a higher percentage of darkened specimens (2.4%) than either Chamaeleo (1.6%) or Stellagama (0.96%). The fraction of burned specimens is low throughout the profile (Fig. 3C), generally varying from 0.2 to 2.0%. However, the level Table 5 Breakage of specimens in the microvertebrate accumulation, divided by taxon and body part. Breakage is calculated using the binary system described in Section 3.3. Taxon

515 - 525

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Testudines Chamaeleo Stellagama Pseudopus Lacertidae Gekkonidae Scincidae Colubroidea Anura TOTAL

Cranial

Postcranial

N

Breakage (%)

N

Breakage (%)

3 246 53 4 3 3 1 0 0 313

67.0 49.8 30.1 0.0 0.0 0.0 100.0 e e 44.6

7 629 127 293 3 0 0 5 7 1071

28.6 3.0 3.9 0.3 0.0 e e 0.0 0.0 2.5

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Table 6 Frequencies of noticeably darkened specimens in the microvertebrate accumulation, suggestive of burning, divided by taxon. Taxon

N

Percent burned

Testudines Chamaeleo Stellagama Pseudopus Lacertidae Gekkonidae Scincidae Colubroidea Anura TOTAL

11 1031 313 211 8 3 1 6 8 1606

0.0 1.6 1.0 2.4 12.5 0.0 0.0 0.0 0.0 1.9

515e525 cm below datum stands out has having an elevated (but still not high) percentage (6.1%), which are evenly distributed between level 515e520 cm and 520e525 cm below datum. This percentage cannot be explained as an artifact of small sample size, because it is on par with other levels. The specimens interpreted as burned are not usually Pseudopus; in fact, Stellagama is represented by more specimens at this level than any other taxon. 4.6. Other post-depositional modification Most specimens show some calcite encrustation (Fig. 2D). In a small minority of cases, specimens are severely encrusted, rarely so completely that the bone surface cannot be inspected. Nearly all specimens showed small black flecks of manganese dioxide on the surface, which in a few specimens were extensive. Flecks occur on the bone itself (Fig. 2C) as well as on the calcite sinter (Fig. 2D). The crystal growth habit was not studied more closely. On a few specimens are apparent root traces (Fig. 4B). These are not extensive, a parietal of Chamaeleo (163-b8) showing one of the most extensive networks. Often, tiny fractures are present at the base of the channels, possibly associated with mineral leaching. The traces are relatively large, on the order of 102 mm in width. 5. Discussion 5.1. Elemental representation Partial skulls of micromammals are not uncommon in the microvertebrate accumulation. Unlike mammals, lizards have loosely constructed skulls (Jollie, 1960); individual elements are

united syndesmodically and lack major interdigitations, in some places forming joints for intracranial kinesis (see Evans, 2008). This results in a flexibility that culminated in the skull of advanced snakes (Cundall and Irish, 2008) but also ensures that lizard skull bones are nearly always found isolated. Therefore, the fact that lizard skull bones are all disarticulated in Qesem Cave does not imply a different taphonomic history for this component of the assemblage. Element representation of the lizards is similar to that for micromammals in that the dentigerous elements (dentary and/or maxilla) are always among the most completely represented (high  ski and Ri: Andrews, 1990; Dodson and Wexlar, 1979; Raczyn Ruprecht, 1974). There is a large amount of intra- and interspecific variation in element representation among predators on small mammals when feeding is not strictly controlled (op. cit.). In contrast, Hoffman (1988) found high rank-order correlations of element representation between nearly all pairs of hawks and owls in his study; in other words, relative element representation did not vary much between predator species. This result contrasts markedly with our comparison of prey species and with variation in the aforementioned studies. However, Hoffman used only a single prey item. This suggests that differences in element constitution among prey species could be responsible for poor interspecific correspondence observed at Qesem Cave. For instance, the ectopterygoid of Stellagama, which has a high Ri, is extremely robust. Higher breakage of cranial than postcranial elements is consistent with destruction during prey capture and killing. Some predators are also known to sever and selectively swallow (Strix aluco) or discard (Asio otus, Solenodon) the heads of prey (Andrews, 1990; Cramp, 1985; Dodson and Wexlar, 1979). In Chamaeleo and Stellagama, underrepresentation of vertebrae (Ri z 0.3), which stand for the body, is on par with pellet analyses of extant owls (including the Barn Owl), diurnal raptors and mammalian predators (Andrews, 1990: 46e48). Numerous cranial elements are even more poorly represented than the vertebrae are. Thus, low Ri for vertebrae does not necessarily suggest that these species did not enter the accumulation as wholes. On the other hand, the underrepresentation of the limb elements in the sample remains unexplained. It is possible that damage to the ends of bones due to screenwashing, prey immaturity (lack of fusion of epiphyses), and atypical morphology (in Chamaeleo) led to underrecognition of these elements during initial sorting. More recently sorted collections have more common limb elements. Pseudopus caudal vertebrae are greatly overrepresented by comparison with the dorsal vertebrae. A plausible explanation for

Fig. 4. Other surface modification observed on bones in the microvertebrate accumulation. (A) Burning affecting only neural spine of a caudal vertebra of Pseudopus (M/14a, 525e 530, box 179-a1). (B) Linear, branching grooves suggestive of root traces, on an otherwise clean (but broken) parietal of Chamaeleo (M/14a, 505e510, box 163-b8).

K.T. Smith et al. / Journal of Archaeological Science 40 (2013) 3326e3339

this discrepancy is that most specimens of this taxon came from severed tails. That is, they derive from partially successful acts of predation, in which the predator came away with only the tail. Tortoises were often consumed by Pleistocene hominins (e.g., Blasco et al., 2011; Stiner et al., 2009). Brain (1981) considered them an item “gathered” rather than hunted because they are so slowmoving. Unlike in some of the sites Brain examined, where he thought that neck and skull may have been consumed, both cranial and postcranial material is present here, including shell fragments. [It should be emphasized that specimens of Testudo cf. graeca occur elsewhere in the cave, where they are usually larger, and like the macromammals bear extensive evidence of human manipulation for dietary purposes (Ben-Dor et al., 2011; Stiner et al., 2009, 2011).] Although the present sample size is small, our preliminary data suggest that the small tortoises entered the microvertebrate accumulation as wholes. 5.2. Size spectrum & activity patterns Chamaeleo and Stellagama are diurnal species and together account for 93% of the MNI of lizards in the microvertebrate assemblage. Of the rarer taxa, only the gekkonid (depending on identity) is plausibly nocturnal. Thus, at least 98% of the lizards (by MNI) are probably diurnal individuals. Assuming that the ratio of lizard to mammal MNI in the accumulation equals the ratio of lizard to mammal NISP, then some 48% of the animals in the accumulation are diurnal. Nearly all of the lower vertebrates in the accumulation are also small animals, less than 60 g in mass. The only possible exception in the examined material is Pseudopus. Large individuals (80% of maximum body SVL given in Meiri, 2008) had mass of 510 g (Gans and Gasc, 1990). If, however, this taxon is represented mostly by the tail (see above), then a mass considerably less than this value may be indicated. 5.3. Abiotic processes and postdepositional modification The lack of corrosion on most specimens might suggest that many of them arrived in the accumulation without entering a predator’s stomach. Data on hydraulic behavior or structural density are not available for lizard bones. However, there is no evidence of abrasion or rounding due to exposure to moving water, nor does surface splitting indicate preburial weathering of specimens (see Pinto Llona and Andrews, 1999). The existence of a strong spatial concentration is also inconsistent with the mode of deposition of the sediment (Karkanas et al., 2007) if the mud slurries had brought the specimens into the cave. Furthermore, the dip of the sediments is toward the center of the cave, rather than toward the wall, where specimens are concentrated. Falling is also implausible, because of the preponderance of arboreal lizards (Chamaeleo) and the fact that not only small but also mid-sized and larger terrestrial animals should have been affected. For instance, almost all the tortoise specimens in the microvertebrate concentration e unlike the rest of the cave (M. Stiner, pers. comm. 2012; pers. obs.) e are of very small individuals. Finally, spatial aggregation implies that all the animals would have had to die immediately upon falling. The sediment in this portion of the Qesem Cave profile (>495 cm below datum in M/14) belongs to the lower sequence (Maul et al., 2011: Fig. 2) and so should lack obvious evidence of roots (Karkanas et al., 2007). The very rare occurrence of root marks on the fossils is thus of some interest. Although some fungi, like plants, are known to exude oxalic acid that functions in weathering (Cromack et al., 1979; Hoffland et al., 2004), fungal hyphae appear to be too small (e.g., Cromack et al., 1979: Fig. 2B) to be the cause of the root marks observed on fossils.

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The concentration of manganese associated with manganese dioxide precipitation is attributed, in some cases, to bacteria (Dorn and Oberlander, 1981). Relations with oxalate, which plays a role in manganese chelation (Dutton and Evans, 1996), are uncertain. Manganese oxides are not typically identified as authigenic precipitates in studies of cave sediment mineralogy (Karkanas et al., 2000). Even if all specimens identified as “burned” were in fact subjected to high heating, the fraction is still a very small one. The colors also suggest only low levels of heating (Shipman et al., 1984), except perhaps in one or two cases. In many archaeological sites incidental charring associated with wild-fires may affect a small proportion of specimens (reviewed in Alperson-Afil and GorenInbar, 2010). In the case of Qesem Cave, a wild-fire is implausible, but a major man-made hearth was constructed 2e3 m to the westnorthwest of the microvertebrate accumulation (Maul et al., 2011: Fig. 5; Shahak-Gross et al., In prep.). Although the hearth is distinctly lower than the microvertebrate accumulation in absolute terms, the dip of the strata indicates that it could have been contemporaneous. Regardless, since all species show similarly low proportions of burning, there is no reason to think that any species experienced a different taphonomic history from the others. 5.4. Predator digestive categories e actualism The co-occurrence of so many species in the assemblage, particularly non-hibernating forms (the micromammals), rules out such a natural death accumulation (see Andrews, 1990). The exclusion of abiotic processes leaves only predators as a plausible mode of accumulation. Actualistic data on the corrosion and breakage caused by various extant predators then provides a means for identifying the predator(s) involved (Andrews, 1990). Corrosion and breakage to the lower vertebrate remains is uniformly low in the profile. Pinto Llona and Andrews (1999) studied patterns of corrosion and breakage in postcranial bones of amphibians preyed upon by various mammalian carnivores and owls. They found that the Barn Owl was distinct from all other examined predators in showing low levels of both corrosion and breakage (Fig. 5). Mammalian carnivores usually showed higher rates of corrosion and much higher rates of bone breakage, whereas other owls showed somewhat higher rates of breakage (Dodson and Wexlar, 1979) and much higher rates of corrosion. Pinto Llona and Andrews (1999) treated only the appendicular skeleton, which was poorly represented in the sample. Thus, our data cannot be taken as strictly comparable to theirs. On the other hand, most of the postcranial skeleton is comparably buried beneath soft tissue, so there is no reason to suspect that the frequency of postcranial corrosion in our data set is unduly influenced by this discrepancy. It is also unlikely that breakage to vertebrae (which has not been studied actualistically) should differ so much from appendicular elements. With this in mind, we added the Qesem Cave accumulation (with breakage calculated using the quadrant or binary system) to Fig. 5. Qesem Cave plots strikingly close to pellet assemblages of the Barn Owl, Tyto alba, and far away from other owls and mammalian predators (Fig. 5). Another way to put this is: the Qesem Cave accumulator may be placed in digestion category 1 and breakage category 1 (Andrews, 1990; Pinto Llona and Andrews, 1999), and only the Barn Owl occupies this position among examined mammals and birds of prey. Pinto Llona and Andrews (1999) did not specifically study diurnal raptors, but these are also more destructive of bone than Barn Owls. In Hoffman’s (1988) experiments, not a single whole bone was recovered in pellets from the three species of hawks he studied.  ski et al. (1998) noted a high proportion of bone breakage in Bochen pellets of Falco rusticolis. Andrews (1990: Table 3.3) found that two

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this and other reasons, they are highly implausible accumulators. Thus, available actualistic taphonomic data on corrosion and breakage suggest that the bones were accumulated largely or solely by Barn Owls, a conclusion also consistent with the more recently excavated partial skulls. 5.5. Natural history and actualism

Fig. 5. Summary of modification to amphibian bones caused by extant predators (data from Pinto Llona and Andrews, 1999). The Qesem Cave assemblage is plotted on this graph using open circles (with breakage calculated using both quadrant and binary systems). The specimens examined here, like those of Pinto Llona and Andrews, are largely postcranial elements but differ in being axial rather than appendicular.

European eagles showed frequencies of breakage of postcrania comparable to most owls (other than the Barn Owl), and other accipitrids and a falconid showed even higher breakage frequencies. Corrosion is also more significant, as has been noted for a number of species (Hockett, 1996; Mayhew, 1977). This is presumably related to the lower pH (compared to owls) of typical gastric fluid in diurnal raptors (e.g., Duke et al., 1975; Leprince et al., 1979). Particularly noteworthy is the Kestrel, Falco tinnunculus, which, when it ingests bone, causes strong corrosion (Mayhew, 1977). This is consistent with observations that Kestrels leave very little bone in pellets (Duke et al., 1976; Uttendörfer, 1939; Yalden and Warburton, 1979; Yalden and Yalden, 1985). However, it is inconsistent with the single report (Mennega, 1938; Farner, 1960) of Barn Owlelike pH in the Kestrel. Stomach pH is known to rise during the digestive process, especially in birds of prey (Duke et al., 1975); thus, variation in sampling time might explain this single apparent anomaly. Hominins are the one predator whose occurrence in the cave is indisputable. Human agency in the accumulation of animals can be manifold, and one can hardly test for it without specifying the particular process involved. Here, we evaluate the proposition that hominins collected these lower vertebrates for food. The pH of the human stomach is sufficiently low, pH ¼ 1.1, as to cause moderate to severe etching or destruction (Crandall and Stahl, 1995). The microfaunal accumulation cannot consist of fecal remains, because the bones are neither comminuted nor strongly etched. Moreover, there is no evidence of frequent charring, or of high frequency for particular species (cf. Weissbrod et al., 2005). Therefore, there is no evidence that hominins accumulated microvertebrates for consumption. Furthermore, natural history observations of humans suggest that, when they prey on reptiles, it is usually large-bodied species for food (Klemens and Thorbjarnarson, 1995). On the other hand, consumption of large Testudo cf. graeca by hominins (Stiner et al., 2011) means that this is the only species they are known to have shared with the microvertebrate accumulator. Other predators could include snakes, but snakes leave behind only an amorphous mass as feces (Blain and Campbell, 1942). For

Since the early 19th century and the demise of curiosity cabinets, natural history has increasingly been sidelined in the biological sciences, losing prestige to a proliferation of new, laboratory- or experiment-based disciplines: physiology, experimental embryology, ecology, genetics, ethology, and molecular biology (Mayr, 1982). Similarly in taphonomy, the early observation-based program of Weigelt (1989 [1927]) (and his antecedents: Lyman, 1994) was superseded by the experimental program advocated by Efremov (1940). This so-called nomothetic enterprise now commonly goes by the name actualism (Gifford, 1981), or more specifically actualistic paleontology (neotaphonomy of Hill, 1978; cf. Richter, 1928). It seeks “laws,” or transferable generalizations (Gifford, 1981), in the processes of fossilization through the study of these processes as they act today under controlled conditions. The actualistic approach has been highly successful in interpreting fossil data (e.g., Andrews, 1990). Yet natural history is a wellspring of ideas, not merely a dry catalog of facts. It highlights what is possible. Even in a hard, hypothetico-deductive framework, hypotheses must come from somewhere (Popper, 1965). Indeed, the idea of natural selection itself evolved out of just such observations (Mayr, 1982). Still today, natural history is commonly used alongside actualistic concepts in order to evaluate taphonomic hypotheses. For instance, Weissbrod et al. (2005) used the markedly elevated frequency of Mole Rat (Spalax) bones in a fossil assemblage with respect to known owl diets to support their contention, based otherwise on breakage and charring, that the Spalax were eaten by humans rather than owls. Andrews and Fernandez-Jalvo (2012) used information on nesting and prey behavior as secondary sources of support for their predator inferences. The observational rather than cause-seeking basis of natural history, however, leaves its conclusions vulnerable to counterexample when they are not properly circumscribed. Natural history observations do not necessarily describe “immanent properties” (Simpson,1970) of the organisms in question, which is why behavior has frequently been excluded. Actualistic studies are designed to test particular assertions under controlled conditions (Hill, 1978). They seek causal relationships that map product (effect) onto process (cause) [which does not necessarily imply a unique mapping of product to process e i.e., the problem of equifinality (reviewed in Lyman, 1994)]. To put this another way: natural history observations are potential actualistic principles that have not yet achieved causal understanding, i.e., where the link between process and product is still tenuous and the set of background assumptions necessary for establishing generality unknown. Our conclusions drawn from breakage and corrosion are the direct result of actualistic studies, particularly those initiated by Andrews (1990). The low frequency and extent of corrosion on specimens implies relatively low stomach acidity. The causal relationship between acid and corrosion is clear enough (e.g., Fisher, 1981), and the exact relation between “low” acidity and corrosion can be calibrated experimentally. In this case, there is also a unique mapping of product onto predator: the only species in which individuals with such high pH are encountered is the Barn Owl. Although intraspecific variation (Lowe, 1980), as always, means that more data are desirable, it seems unlikely that stomach acidity will vary greatly under normal conditions (Smith and Richmond, 1972).

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After all, enzymes like pepsin have an optimal pH range (Withers, 1992) that relates to their structure, which in turn is under genetic control. Furthermore, it is a testable assumption that the properties of the digestive apparatus do not differ markedly from one individual to another or over time in the same individual. Breakage patterns are less clearly deterministic, because it is not well understood why certain predators comminute their prey to a greater extent than others. It has simply been observed that they do; perhaps observations under different circumstances will produce different results (Saavedra and Simonetti, 1998). Size, of course, may play a role. In the case of Qesem Cave, some natural history observations e particularly on nesting behavior and prey size spectrum e are consistent with the conclusions given above. For instance, most diurnal raptors do not nest in caves (F. tinnunculus may be an exception). The spatial concentration of microvertebrate remains, and their virtual absence outside the accumulation, implies that if the remains derived from diurnal raptors sitting on a perch near a cave opening (cf. Brain, 1981), that opening must have been a chute leading directly downward to the accumulation. There is no evidence of such a chute, nor is there evidence that the bones were subject to weathering (Pinto Llona and Andrews, 1999), as would be expected of bones that accumulated outside and fell in sporadically. The following members of the strigiform avifauna occur in the Levant today: Barn Owl, European and Pallid Scops Owls, Eurasian and Pharaoh Eagle Owls, Little Owl, Tawny and Hume’s Tawny Owls, and Long-eared and Short-eared Owls (Porter et al., 1996). (1) Barn Owl, T. alba (33e35 cm tall; Cramp, 1985). It frequents caves and such cavities (e.g., Andrews, 1990; Brain, 1981; Cramp, 1985). It seems limited in its ability to occupy available habitat because of its restrictive nesting/roosting requirements (Cramp, 1985). Today, these are frequently better met on the outskirts of human habitations, where Barn Owls can take advantage of abandoned or disused buildings. [Thus, ironically, some modern population declines (e.g., de Bruijn, 1994) are conceivably returns toward a more natural state.] Additionally, most of the prey species are well within the range of Barn Owls, which most commonly eat food items with a mass of 20e60 g (Brain, 1981: 125e126). The size distribution of specimens collected beneath a roost in South Africa included prey up to 140 g (Brain, 1981, based on Dean, 1973). Pseudopus does not pose a problem here if known specimens came from severed tails. Rare hyraxes (unpubl.) and a sciurid are known in the microvertebrate accumulation (Maul et al., 2011) and could be an exception. (2) European Scops Owl, Otus scops (19e20 cm; Cramp, 1985). The most common elements in this small owl’s diet are insects and other invertebrates (reviewed in Cramp, 1985). (3) Pallid Scops Owl, Otus brucei (20e21 cm; Cramp, 1985). This small owl will eat some small vertebrates in addition to large quantities of insects, and it sometimes hunts during the day (Cramp, 1985). Its small size probably means that it has to reduce larger items, leading to breakage. Additionally, it usually nests in trees (Cramp, 1985; Porter et al., 1996). (4) Eagle Owl, Bubo bubo (60e75 cm; Cramp, 1985). Like B. africanus (Brain, 1981), B. bubo nests or roosts in caves from time to time (A. Frumkin, pers. comm., 2012). However, the most common species in the microvertebrate accumulation (Maul et al., 2011; this paper), are probably too small to form a dietary staple. The desert form, B. ascalaphus, is similar but slightly smaller. (5) Little Owl, Athene noctua (21e23 cm; Cramp, 1985). The most common elements in this small owl’s diet are insects and other invertebrates, but it will also take small vertebrate prey, such as

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mice, gerbils (Sekour et al., 2011) or even (very) juvenile tortoises (Cramp, 1985). (6) Tawny Owl, S. aluco (37e39 cm; Cramp, 1985). This owl is known to take prey of the right size. However, it usually breeds in holes in trees or cliffs (Cramp, 1985). An form more common in arid environments, S. butleri is similar in size (Cramp, 1985). (7) Long-eared Owl, Asio otus (35e37 cm; Cramp, 1985). This owl is known to take prey of the right size. However, it usually breeds in holes in trees or cliffs or even on the ground (Cramp, 1985). The similar-sized A. flammeus often nests and roosts on the ground (Cramp, 1985). Thus, the foregoing natural history data on prey size and nesting behavior also support the Barn Owl as the more likely predator of the Qesem Cave microvertebrates. On the other hand, several additional (interrelated) aspects of natural history present a challenge to the idea that the Barn Owls were the accumulator at Qesem Cave. Most obviously, nearly all the lower vertebrates are diurnal, whereas owls are generally nocturnal. Barn Owls also usually prey on terrestrial organisms, not arboreal ones. Furthermore, Barn Owls are not considered to be major predators on chameleons, nor do chameleons feature prominently in Barn Owl dietary studies. Barn Owls co-occur with chameleons, on a coarse scale, not only in Israel but also elsewhere in the circum-Mediterranean region (see distribution maps in Klaver, 1981; Svensson, 2009), and thus opportunity for predation exists. Barn Owls have been recorded (Brosset, 1956; Tores and Yom-Tov, 2003) or noted anecdotally (Schleich et al., 1996) as predators on C. chamaeleon, but the numbers taken are always very low. Rather, the most serious predators on C. chamaeleon are thought to be snakes (e.g., Malpolon monspessulanus; Lin and Nelson, 1980; Schleich et al., 1996) and falcons (T. Keren-Rotem, pers. comm., 2011; Lin and Nelson, 1980; Schleich et al., 1996). Nor are owls known to prey on chameleons in other environments where these lizards are abundant, as on Madagascar (Goodman et al., 1993; Jenkins et al., 2009). In fact, reptiles in general are apparently rare in Barn Owl pellets in most areas (e.g., Buden, 1974; Coetzee, 1963; Cramp, 1985; Cunningham and Aspinall, 2001; de Graaff, 1960; Dean, 1974, 1975; Lovari et al., 1976; MacFarlane and Garrett, 1989; Mahmood-ulHassan et al., 2007; Nel and Nolte, 1965; Pezzo and Morimando, 1995; Schnurre and Bethge, 1973; Uttendörfer, 1939; Vernon, 1972; Wilson, 1987), including the circum-Mediterranean region (Boukhamza, 1989; Goutner and Alivizatos, 2003; Obuch and Benda, 2009; Rihane, 2003; Sekour et al., 2010; Tores and Yom-Tov, 2003; Tores et al., 2005; Veiga, 1978 [1980]), even if Herrera (1974) found the prey spectrum to be relatively more variegated in southern than northern Europe. Some of the aforecited works, especially Cramp (1985), Martín and López (1990), and Uttendörfer (1939), are extensive in their treatment of European populations. Instead, if Barn Owls are not exactly non-selective predators (Mikkola, 1983), then they are thought to specialize on the so-called microtinemurid-soricid fraction (Andrews, 1990; Tores et al., 2005). Yet at Qesem Cave, small reptiles form half of the accumulating predator’s diet. It seems implausible that reptiles should be collected at such high frequency by Barn Owls, particularly chameleons, which have never been recorded as a notable constituent in any dietary study of these birds. 5.6. Synthesis e an explanation for the Qesem Cave accumulation One possible way to harmonize these data is to hypothesize that the Qesem Cave microfauna was collected by an extinct species, particularly another species of the T. alba complex, which has been diversifying over the last 1e2 million years (Wink et al., 2008). On

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the one hand, this could resolve the problematic observations of natural history (diet data), perhaps without contradicting actualistic data on breakage and especially corrosion (assuming stomach pH was similar). Extinct species of Tyto are known (e.g., Pregill et al., 1988). On the other hand, most newly recognized lineages of the T. alba complex are island endemics (Wink et al., 2009). Furthermore, the hypothesis still does not conform with the conclusion that no owl is known to be a serious predator on chameleons. Identification of fossil remains of owls in the cave could help test this hypothesis. A simpler ad hoc hypothesis, however, can be derived from natural history. The claim that Barn Owls are mammal specialists is a generalization that does not hold everywhere without qualification. In fact, Barn Owls are known to specialize locally or at times on other prey, including lizards. For instance, nocturnal geckos were more abundant than small mammals in pellets of T. alba on Vanuatu (Ineich et al., 2012). Around the city of Berkane in Morocco, Barn Owls were recorded as taking nearly 90% pigeons (Brosset, 1956). In a sample of Barn Owl pellets from Madagascar, collected throughout the year, three species of amphibians made up nearly half of MNI, and one of those species alone accounted for 35% of the total individuals (Goodman et al., 1993). Amphibians, especially Pelobates, formed a large portion of the diet of some Hungarian Barn Owls (Marián and Marián, 1973). Brain and Brain (1977) found that prey composition at the Mirabib Rock Shelter (Brain, 1974) contained nearly 50% Pachydactylus (a large, saxicolous gecko) at certain levels; since the rock shelter is currently used as a Barn Owl roost, it is assumed that they also used it in the past (Brain, 1981). Vernon (1972) cites an example of high proportions (up to w50%) of lizards in the vertebrate prey of Barn Owls in the Namib. Clearly, prey items other than small mammals are available to Barn Owls in other areas, but local conditions are not conducive to specialization. Other owls do not appear to specialize (except perhaps seasonally) to such an extent as Barn Owls (Boukhamza, 1989; Cramp, 1985). Chameleons are possibly different from other lizards in being cryptically colored and so presumably less apparent to visual predators like owls, and especially the Barn Owl, with its relatively poor eyesight (Mikkola, 1983). However, Barn Owls, unlike many other owls at most times, may be active well before dusk (Cramp, 1985), especially in winter or during breeding (Glutz von Blotzheim, 1980; Mikkola, 1983), and thus can take primarily diurnal prey (e.g., Lovari et al., 1976). Dusk is the time when C. chamaeleon, like other warm-adapted chameleons (Reilly, 1982), seeks out the distal ends of branches (i.e., twigs) for the night, perhaps in order to minimize predation risk by snakes or terrestrial mammals (T. Keren-Rotem, pers. comm., 2011). As the animal becomes torpid, its normally cryptic coloring lightens, part of a circadian rhythm under hormonal control (Okelo, 1986). When they turn pale, their camouflage is finally disrupted. Thus, dusk and dawn may be precisely the times when owls, even (or especially) T. alba, can find cryptically colored chameleons. Indeed, herpetologists frequently find chameleons in a similar way: by shining flashlights at branches after dusk (e.g., Keren-Rotem et al., 2006). There is some precedent for this conclusion. Pregill et al. (1988) reasoned that large accumulations of arboreal anoles (>50% of NISP in the microvertebrate fauna) were collected by Barn Owls. They did so without a formal taphonomic analysis, even though Barn Owl diets on Caribbean islands, according to contemporary reports, included few reptiles (Buden, 1974). Anoles also show similar crepuscular behavior and some ability to change color, hence a colloquial name for Anolis carolinensis: the American Chameleon. Barn Owls are reported to take prey at times from trees and bushes (Andrews, 1990: 178). (If the trees were furthermore deciduous, then the probability of discovery might be increased after the leaves had fallen.)

An abundance of chameleons in the fossil fauna suggests a vegetation that was at least locally lush. A candidate area exists. One of the headwaters of the Yarkon River, which flows from the Judean hills into the Mediterranean near Tel Aviv, is in a spring near Rosh Ha’ayin, merely 5.3 km from Qesem Cave (see historical map from the year 1880, available here: http://amudanan.co.il). The same valley continues into the Judean hills as the Wadi Rabah, which passes by Qesem Cave. Perhaps the conditions around Qesem Cave in the Middle Pleistocene e in particular the vegetation associated with Rosh Ha’ayin e led to a specialization on the part of the Qesem Barn Owls which has not (yet) been recognized in the Levant today. However, it may be worth noting that Haas (1952) described seemingly co-abundant remains of Chamaeleo, Stellagama and Pseudopus in the Natufian of Abu Usba. Further work there may prove fruitful. If the accumulator was a Barn Owl, then it must have had a roost or more probably a nest in Qesem Cave. T. alba is almost everywhere “limited by [its] exceptional requirements for more floor-space and easier access than often associated with hole-sites for nests” (Cramp, 1985: 433). We have identified one possible nesting area adjacent to the accumulation. This area is located along the contemporary eastern wall of the cave, which is covered in places by thick flowstone (Fig. 6; see also Maul et al., 2011: Fig. 5). Above the accumulation, a ledge once projected from the wall into the interior, as indicated by refitting its broken margins (Fig. 6). It had fallen, but not far, more or less rotating downward along the axis formed by the broken margin. The fact that it broke and fell downward indicates that the space beneath it e about 40 cm from its base to level where it came to rest e was empty at the time of collapse. Along the same wall are additional prominences and niches that also could have served as nesting sites. The level where the broken ledge came to rest not only roughly marks the change from closed to open conditions (Karkanas et al., 2007), which was caused by a cave-in, but also the termination of the richest portion of the accumulation. de Bruijn (1994) tested a series of box-sizes for conservation purposes in Belgium and concluded that the optimal size was 40 cm wide by 75 cm deep by 50 cm tall. The Qesem ledge has dimensions similar to those preferred by the Belgian Barn Owls, about 75 cm wide by 65 cm deep. Finally, it was located immediately above the microvertebrate accumulation. Thus, spatial proximity, dimensions,

Fig. 6. Photograph of the corner of the Qesem Cave containing the eastern microvertebrate accumulation. The broken margins of the fallen, flowstone-covered ledge are marked with short-dashed lines. The accumulation is located below the ledge (highlighted area). The thick, long-dashed line shows the approximate boundary between the lower and upper sequences (see Maul et al., 2011: Fig. 2). The large blocks to the left (highlighted) are associated with the roof collapse approximately coincident with said boundary (see Karkanas et al., 2007).

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and reconstructed relation to the contemporary wall suggest that this may have been the nesting area. Additional niches higher on the wall could have served the same purpose. 6. Conclusions The taphonomic and natural history data we have collected and analyzed here suggests the following scenario, a working hypothesis to explain this microvertebrate accumulation at Qesem Cave. The cave was initially dark enough, away from the entrance, that (nearly) all plant growth was strangled (Karkanas et al., 2007). Inside the cave, on the eastern wall, was a ledge that projected some 65 cm into the interior; other ledges and a niche were present higher up on the wall. Barn Owls used this space as a nesting area. While there, they hunted in the heterogeneous environment around the entrance (Maul et al., 2011), particularly in open spaces (Microtus guentheri) and woods (Chamaeleo), perhaps associated with the spring at Rosh Ha’ayin. Eventually the ledge collapsed, possibly coincident with a roof collapse that further opened the cave to light (Karkanas et al., 2007). Accumulation of microvertebrates in this area was then highly curtailed. Buckland’s (1824: 170) view that human remains had not and would never be found in “diluvial” deposits with ancient animals has long since been dashed. The penecontemporaneous occupation of Qesem Cave by hominins and Barn Owls has bequeathed us with a rich microvertebrate record that illuminates ancient hominin ecology. Not only does the superabundance of chameleons e highly unusual in a microvertebrate assemblage e suggest a lush vegetation, at least locally, in the vicinity of the cave (possibly Rosh Ha’ayin), but it also makes a first contribution to hominin ecology within the cave. To our knowledge we have pinpointed for the first time, if only tentatively, an ancient nesting site in a collapsed cave setting. Brain (1981) diagramed three extant Barn Owl roosts in dolomitic caves in the Sterkfontein valley, each located in the twilight zone of the cave, and noted that this was the preference for Barn Owls. Reed (2005) also found that “cavity-roosting” Barn Owls, where present in rock fissures, were found in the twilight zone. These natural history observations suggest that the opening of the cave was not located far from the identified roost. They further suggest that the adjacent hearth may also have been bathed in twilight. Acknowledgments We are grateful to O. Comay, O. Kolodny, T. Dayan and Y. Leshem (Tel Aviv University), A. Frumkin, R. Rabinovich and R. Biton (Hebrew University, Jerusalem), G. Shenbrot (University of the Negev, Mizpe Ramon), M. Stiner (University of Arizona), J. A. Gauthier (Yale University), and N. Munro and G. Hartman (University of Connecticut) for discussion. S. Rogers (CM), R. Rabinovich (HUJ), G. Schneider and R. Nussbaum (UMMZ), G. Köhler and L. Acker (SMF), and W. Böhme (ZMFK) provided access to modern specimens. K. Krohmann (SMF) was instrumental in production of the SEMs, and A. Vogel (SMF) helped with the figures. Financial support was provided by the Fritz Thyssen Foundation, the Israel Science Foundation, the Leakey Foundation, the Wenner Gren Foundation and the CARE Archaeological Foundation. Two anonymous colleagues carefully read the manuscript and provided constructive criticism. References Alperson-Afil, N., Goren-Inbar, N., 2010. The Acheulian Site of Gesher Benot Ya’aqov. In: Ancient Flames and Controlled Use of Fire, vol. II. Springer, New York. Altum, B., 1863. Die Nahrung unserer Eulen. Journal für Ornithologie 11, 41e46. Andrews, P., 1990. Owls, Caves and Fossils. University of Chicago Press, Chicago. Andrews, P., Evans, E.M.N., 1983. Small mammal bone accumulations produced by mammalian carnivores. Paleobiology 9, 289e307.

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