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Quaternary Science Reviews 30 (2011) 3196e3209
Contents lists available at ScienceDirect
Quaternary Science Reviews
journal homepage: www.elsevier.com/locate/quascirev
Ecological change and the extinction of the Levantine Neanderthals: implications
from a diachronic study of micromammals from Amud Cave, Israel
Miriam Belmaker a, b, *, Erella Hovers c
a
Department of Anthropology, Harvard University, 11 Divinity Ave., Cambridge, 02138 MA, USA
Department of Anthropology, The College of William and Mary, 241 Jamestown Rd. Williamsburg, VA 23185, USA
c
Institute of Archaeology, The Hebrew University of Jerusalem, Mt. Scopus, Jerusalem 91905, Israel
b
a r t i c l e i n f o
a b s t r a c t
Article history:
Received 5 January 2011
Received in revised form
9 July 2011
Accepted 2 August 2011
Available online 24 August 2011
It has been hypothesized that the climate shift associated with the Heinrich 5 event (H5) and the
decrease in productivity throughout MIS 4 contributed to the demise of Neanderthals from the Levant.
The Middle Paleolithic stratigraphic sequence of Amud Cave (Israel) spans MIS 4 and the transition to MIS
3 and contains Neanderthal skeletal remains as well as microfaunal assemblages, often used in the
literature as reliable paleoecological proxies. This combination offers a unique case study to address the
question of the effects of climate on Neanderthal population dynamics. Here we present a diachronic
study of the rodent assemblages from Amud Cave, Israel, using taphonomic and nested hierarchical
paleoecological models to test the hypothesis of a decrease in environmental productivity throughout
the Amud sequence. Results suggest that there is no change in high-level presenceeabsence and rank
abundance of rodent species throughout the sequence of Amud Cave, but there is change in low-level
relative abundance of four taxa. Paleoecological analysis suggests that while all the stratigraphic subunits of Amud Cave can be assigned to a Mediterranean biome, an apparent trend of decrease in
grasslands proportions throughout the sequence is discordant with other regional paleoecological
proxies. Taphonomic analysis reveals that this may be attributed to specific predator preferences of
rodent prey, and thus does not reflect the true shift in paleoecology throughout the temporal sequence
represented in the cave. The high-level overall stability in rodent community suggests that climatic shifts
during the MIS 4e3 transition were of a magnitude that did not have a major impact on small mammals
in the region. Such results are consistent with evidence from analysis of large mammal community and
vegetal remains in Amud and contemporaneous Middle Paleolithic cave sites, and suggest that climate
change may not have had the hypothesized effect on Neanderthal extinction in the Levant.
Ó 2011 Elsevier Ltd. All rights reserved.
Keywords:
Micromammals
Neanderthals
Paleoecology
Last Glacial
Levant
Amud Cave
1. Introduction
The past years have seen a growing interest in the effect of
climate change on European Neanderthal population dynamics
(Gamble et al., 2004; Stewart, 2005; Finlayson et al., 2006;
Finlayson and Carrion, 2007; Tzedakis et al., 2007). The bulk of
skeletal remains that exhibit Neanderthal features in the cranium
as well as in the face date from ca 300 ka to 28 ka in Europe
(Millard, 2008), encompassing a number of climatic cycles (Zachos
et el, 2001). The most recent of these cycles (MIS 4 and 3) are
characterized by instability and unpredictability of climate systems
(Van Andel and Davies, 2003; Finlayson and Carrion, 2007), and are
* Corresponding author. Dept. of Anthropology, Harvard University, 11 Divinity
Ave., Cambridge, 02138 MA, USA.
E-mail
addresses:
[email protected],
[email protected]
(M. Belmaker), [email protected] (E. Hovers).
0277-3791/$ e see front matter Ó 2011 Elsevier Ltd. All rights reserved.
doi:10.1016/j.quascirev.2011.08.001
suggested to have played a significant role in the fragmentation of
habitats and subsequently the extinction of the European Neanderthals (Finlayson et al., 2006; Finlayson and Carrion , 2007 but
see Tzedakis et al., 2007).
In the Levant, Neanderthal remains are confined to cave sites in
Syria and northern Israel. Kebara Cave on Mt. Carmel is currently the
southernmost occurrence of skeletal remains of these hominins.
Most of the Neanderthal remains are dated to MIS 4 and early MIS 3
(70e55 ka), whereas those of modern humans are assigned to MIS
5e and 5c (see Hovers, 2009, pp. 233e234 for details of alternative
age estimates and Appendix 6 for references). Shea (2008) identified two turnover events in human populations in the Levant during
the later part (130e50 ka) of the Middle Paleolithic. He suggested
that climatic forcing was the main trigger for the disappearance of
Levantine Middle Paleolithic modern humans ca 80 ka as well as the
cause for the dispersal of Neanderthals into the region at that time.
Following the model presented for the European Neanderthals
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M. Belmaker, E. Hovers / Quaternary Science Reviews 30 (2011) 3196e3209
(Finlayson et al., 2006; Finlayson and Carrion, 2007, 2008)), Shea
(2007, 2008) also suggested that climatic forcing was the main
trigger for the extinction of the Levantine Neanderthals. He inferred
a gradual trend of decrease in terrestrial productivity in the Mediterranean zone of the Levant throughout the Last Glacial (Shea,
2008) and an overall decrease in precipitation throughout MIS 4,
culminating in the MIS 4/3 transition as identified from a number of
paleoecological proxies (e.g., Bar-Matthews et al., 1997, 1999;
Langgut, 2008). One the of main lines of evidence used to support
the hypothesis of climatic forcing (Shea, 2008) is the faunal turnover observed in the micromammal community of the Levant
during the Last Glacial and specifically that observed between MIS 4
and 3 (Tchernov, 1988a,b, 1989, 1992a,b, 1994, 1998).
The presence of diagnostically-meaningful, dated hominin
remains renders the site of Amud Cave (eastern Upper Galilee,
Israel) (Fig. 1) an appropriate case study for evaluating the
hypothesis that climatic changes in the Levant were sufficiently
severe to cause a turnover of human taxa in the region. Here we use
the micromammal assemblage from Amud Cave to evaluate this
hypothesis by addressing three main questions about the environments of the Upper Galilee of Israel during MIS 4e3:
1. Can we detect an environmental shift throughout the sequence
of Amud Cave? i.e., can we observe a trend throughout the
sequence between stratigraphic sub-units B4 (dated to ca
70 ka) and B2/B1 (dated to ca 55 ka).
2. How does the climate in the Upper Galilee during MIS 4e3,
compare to modern day environment in the same area, based
on the micromammal assemblages?
3. How representative is the environment of the Upper Galilee in
comparison to other regions of the region where Neanderthal
remains are found during MIS 4e3, specifically the Mount
Carmel region?
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The answers to these questions will be used to evaluate two
arguments of the climatic hypothesis for population turnover in the
Levant. First, we ask whether the notion of an overall decrease in
productivity during MIS 4e3 is supported by our data. Second, we
ask whether the magnitude of such changes as reflected in the data
might have had an appreciable effect on Neanderthal population
dynamics, to the degree that may have led to their extinction in the
region during MIS 4/3.
1.1. The site
Amud Cave is situated in the eastern Upper Galilee of Israel, in
what today is the Mesic Mediterranean phytogeographic zone
(Danin, 1988). The climate is Mediterranean, with a dry, hot
summer and a cool, wet and short winter. The rainy season lasts
from the mid-October to early May, with the majority of rainfall
between December and February. Mean annual precipitation is
550 mm and the mean temperatures are 28 C and 11 C for the
hottest and coldest months, respectively (Goldriech, 1998). The
Mediterranean C3 vegetation is comprised of oak (Quercus) and
pistachio (Pistacia) forest with open areas dominated by various
Germianae (Zohary, 1982).
All the archaeological stratigraphic units in the site (designated
B4, B2 and B1 from bottom to top; Chinzei, 1970; Suzuki and Takai,
1970; Hovers et al., 1991) contain abundant lithic and faunal
assemblages, associated with hearth remains (Hovers, 2004, 2007;
Rabinovich and Hovers, 2004; Alperson-Afil and Hovers, 2005).
Hominin skeletal remains were found in the two topmost stratigraphic sub-units of Amud, designated B2 and B1. Of the 18 hominin specimens recorded in these sub-units, two bear diagnostic
characteristics sufficient for their identification as Neanderthals
(Hovers et al., 1995 and references therein). The age estimates of
sub-units B2 and B1 (56.5 3.5, 57.6 3.7, respectively) are
statistically undistinguishable and range between 65.0e49.5
within 2 sigma, thus spanning the later part of the MIS 4/3 transition that is crucial to Shea’s hypothesis. The mean TL age estimate
for the lowest Middle Paleolithic stratigraphic sub-unit B4 is
68.5 3.4 ka (Valladas et al., 1999). Within the range of 2 sigma
(75.3e61.7 ka), this age estimate spans the MIS 5/4 transition. No
diagnostic hominin remains are known from this stratigraphic subunit. While age estimates within 95% statistical certainty suggest
temporal continuity, a gap in Middle Paleolithic human occupation
of the cave is represented by the accumulation of the
archaeologically-sterile sub-unit B3, stratigraphically encountered
between sub-units B4 and B2 (Hovers et al., 1991; Valladas et al.,
1999; Rink et al., 2001).
1.2. Micromammals and paleoenvironmental reconstruction
Fig. 1. Location of Amud in the Levant. Sites mentioned in the text are shown.
Mammals have been widely used for both for paleoecological
reconstructions and for studies of communities and environment
changes through time (e.g., Bate, 1937; Andrews et al., 1979;
Andrews, 1995; Reed, 1998; Bobe and Eck, 2001). The main
premise underlying paleoecological reconstruction based on
fauna is the unique niche requirements of a species. Paleoecological interpretations derived from faunal data are based on
analyses of community composition. However, persistence (i.e.
stability or stasis) vs. change over time is examined at three
hierarchical numerical scales (Rahel, 1990): species’ presenceeabsence, rank abundance, and species proportional abundance. The hierarchy is nested such that a community can be
stable at a low level (presenceeabsence) but show change at
a higher level (proportional abundance). Community-wide
diversity is captured by indices that measure the number of
species (e.g., richness), those that express the uniformity of the
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abundance of species (e.g., evenness, dominance and the ShannoneWiener indices) (Magurran, 2003).
Micromammals, defined as mammals of less than <500 g live
weight (Reed, 2005), include members of the orders Rodentia,
Insectivora and Chiroptera that fall within this criterion (e.g., Hystrix or Erinaceus are excluded). Micromammals have been used as
paleoecological indictors due to their rapid evolution, small home
range size and unique niche requirements (Chaline, 1977) as well as
their frequent preservation in the archaeological record. They are
excellent indicators of vegetation type and provide a highresolution proxy for environmental changes, in particular when
used in tandem with proxies derived from large and medium-size
mammals.
The taxonomic composition of rodent communities differs
across biomes (Hernádez-Fernádez, 2007). Specifically, members
of the Subfamily Gerbillinae (gerbils and jirds) inhabit open, hot
and arid environment, members of the Subfamily Murinae (Old
world mice and rats) inhabit closed, wooded and more humid
environments, and members of the Subfamily Arvicolinae
(lemmings and voles) inhabit open, temperate to cool humid
environments. These subfamily-level adaptations can be used as
general indicators of paleoecological change through time using
changes both in presenceeabsence of species and relative abundances (MNI, number of individuals). The ratio between Gerbillinae and Muridae, calculated as MNI as well as number of species
and number of genera has been shown to distinguish between
biome types in Africa (Denys, 1999). Similarly, the number of
Arvicolines shows a negative correlation with mean annual
temperature (Montuire et al., 1997).
Precipitation has been shown to be a reliable proxy for environmental productivity (Rosenzweig, 1968). Because rodent diversity is altered by levels of precipitation, it reflects environmental
productivity (Spevak, 1983; Ernest et al., 2000). There is a positive
correlation between precipitation and species richness as well as
between precipitation and rodent species diversity (Avery, 1982,
1988; Ernest et al., 2000).
1.3. Effects of taphonomic biases on paleoecological analyses
Micromammal fossil assemblages are susceptible to taphonomic
biases that need to be considered prior to any paleoecological
analyses (Andrews and Evans, 1983; Andrews, 1990; Denys, 1990;
Fernández-Jalvo and Andrews, 1992; Matthews, 1995, 2002;
Dauphin et al., 1999). A major source of error in paleoecological
and paleoenvironmental reconstructions lies in the varied levels of
fidelity of the fossil assemblage when compared to the living
community from which it was derived (Behrensmeyer, 1991;
Lyman, 1994; Behrensmeyer et al., 2000; Flessa, 2000). Before
asking if rodent paleo-communities differed over time due to
paleoenvironmental changes, we must consider the effects of
taphonomic processes and how similar such processes might have
been across a set of sampled sites.
Important taphonomic biases of paleoecological and paleoenvironmental reconstructions include the predator responsible for
the accumulation of the assemblage (Andrews and Evans, 1983;
Andrews, 1990; Reed, 2003, 2005). All predators exert some level
of selectivity, although their hunting preferences differ. The Barn
Owl (Tyto alba) and Eagle Owl (Bubo bubo), two of the most
common accumulators of rodent fossil assemblages, create
assemblages that correspond to abundances in the live community
(Andrews, 1990; see Reed, 2005 on Bubo africanus). This is reflected
in parameters of presenceeabsence, species diversity (e.g., richness
and evenness), and even relative abundance (Avenant, 2005; Terry,
2010). In contrast, other predators are highly selective and consume
specific species in greater abundance than available in the
environment. In these cases, the taxonomic composition, diversity
indices and abundance measurements of the fossil assemblages
produced are not consistent with the live community. For example,
the tawny owl (Strix aluco) takes a higher proportion of Microtus
spp. in fragmented woodlands and grassland patches than other
taxa that are present in the same habitats, such as bank voles and
wood mice, even when those are more common in these environments (Andrews, 1990; Petty, 1999). Fossil assemblages created by
such predators will be highly biased and have a low fidelity with
the biocoenosis from which they are derived. Therefore, prior to any
paleoecological analysis, it is necessary to identify the predator(s)
responsible for the observed taxonomic composition of the rodent
assemblages.
Other processes that reduce our ability to correctly identify the
fossil remains to taxa include differential patterns of postdepositional breakage (Andrews, 1990; Wilson, 2008) and transport (Voorhies, 1969; Wolff, 1973; Korth, 1979). The common
protocol for micromammal taxonomic identification is based on
molars (Avery, 1982). Since paleoecological analysis is based on
taxonomic composition, any post-depositional processes that
differentially affect the representation of molars, such as trampling
and fluvial transport, may reduce the fidelity of paleoecological
reconstruction. For example, it has been shown by Wolff (1973) that
due to their flat shape and bone mineral density, microtine teeth
tend to be over-represented in fluvially-transported assemblages
relative to murid teeth.
2. Methods and materials
2.1. Materials
This study uses rodent material from the 1991e1994 excavations at Amud Cave (Hovers et al., 1991; Hovers, 2004). Lagomorphs
and larger sized Rodentia and Insectivora are being studied as part
of the anthropogenic accumulation at the site that pertains to
hominin choice and consumption of faunal resources, and are not
included in the current analysis. Furthermore, while birds,
amphibians, reptiles and fish may also be deposited in raptor
pellets, their paleoecological interpretation relies on a different
ecological model and their analysis will be presented elsewhere.
Bats, rarely preserved in the archaeological record, are also not
included in micromammal studies.
All the excavated sediments were wet sieved through a 5 mm
and 1 mm stacked mesh. Wet-sieved material was sorted on-site
and further in the lab for micromammal material. Three wellpreserved assemblages of micromammals were derived from the
three archaeological sub-units and were analyzed in this study. All
the material is housed in the National Natural Collections, Hebrew
University of Jerusalem (Jerusalem, Israel). A small sample originally identified by the late Eitan Tchernov is included in the
analysis.
2.2. Methods
2.2.1. Taxonomy
Taxonomic identifications were made by comparisons with the
mammal and paleontological comparative collections held at the
National Natural Collections, Hebrew University of Jerusalem (Jerusalem, Israel) and at the Museum of Comparative of Zoology,
Harvard University (Cambridge, MA). Following common protocol
used in micromammal studies (Avery, 1982; Andrews, 1990;
Fernández-Jalvo et al., 1998), determinations were based on
dental morphology and measurements.
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2.2.2. Taphonomy
A sub-sample of the assemblage retrieved from each stratigraphic sub-unit was subjected to a taphonomic study in order to
determine the post-depositional history of the assemblages. Postcranial and cranial elements and molars were observed using
a stereoscopic microscope as well as a Dino-Lite Pro2 Digital
microscope AD 413TÓ up to 200 magnification. Comparative data
for predator-derived micromammal assemblage were retrieved
from the literature (Andrews, 1990; Fernández-Jalvo, 1996;
Fernández-Jalvo et al., 1998; Matthews, 1999, 2002; Reed, 2003,
2005; Matthews et al., 2005; Weissbrod et al., 2005).
The taphonomic methodology followed Andrews (1990) and
Fernández-Jalvo and Andrews (1992), later developed and standardized in several studies (e.g., Matthews, 1999, 2002, 2006;
Matthews et al., 2005; Dewar and Jerardino, 2007). This method
identifies five levels of modification (little, moderate, intermediate,
great and extreme). Different predators can be identified with
a high level of probability by the degree of modification they exert
on different body elements (molars, incisors and post-cranial
elements).
Two types of indices in particular have been shown to differ
between predators: breakage patterns (i.e., postcranial-to-cranial
proportions, distal element loss, differential breakage of cranial,
dental and post-cranial elements, and maxillary, mandibular and
isolated tooth loss) and digestion levels (i.e., the intensity and
degree of digestion of molars, incisors and post-cranial elements)
(Andrews and Evans, 1983; Andrews, 1990; Laudet et al., 2002;
Matthews, 2002).
The standard micromammal taphonomic method developed by
Andrews (1990) was based on modern pellet assemblages, which
were not subjected to post-depositional taphonomic processes.
Such assemblages most often included all elements of the skeleton
(skulls, mandibles and complete post-cranial elements) used to
deduce the predator responsible for the accumulation of the
assemblage. In archaeological material, substantial breakage may
result from post-depositional processes (e.g., soil compaction,
trampling and fluvial transport) in addition to modification
resulting from predator activities. Therefore, breakage indices,
while extremely useful in predator identification from pristine
pellet assemblages, produce equivocal results in the analysis of
archaeological assemblages (Andrews, 1990; Fernández-Jalvo et al.,
1998; Belmaker et al., 2001). In cases where trampling is suspected
to have been a major post-depositional factor, the most reliable and
unequivocal means to identify the taxon of the accumulating
predator are only the intensity and degree of digested teeth and
possibly the analysis of post-crania (complete elements only;
Fernández-Jalvo et al., 1998).
The micromammal assemblage of Amud is extremely fragmented, a pattern shared with the assemblages of large mammal
bones due in part to post-depositional trampling (Rabinovich and
Hovers, 2004). The high fragmentation rate of the rodent bones
resulted in the absence of complete skeletal elements, which
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precluded identification of post-cranial elements. Specifically, most
post-crania are present in the form of shafts and the incisors are
highly fragmented. The identified elements in the assemblage are
mostly loose molars. Hence measurements of digestion were conducted only on molars. To avoid the complications of potential
equifinality, the taphonomic indices used in the study included
only intensity and degree of digested loose molars.
Predators (owl, diurnal raptors and mammalian carnivores) can
be classified into one of five groups based on the degree of modification they exert on skeletal assemblages of their prey (Andrews,
1990). While there is considerable overlap in modification levels of
taxa for each of the taphonomic categories, they are not identical,
and there are slight differences in the assignment of taxa to each of
the categories for each taphonomic factor. Thus, the final classifications are based on the composition and averaging of the modification intensities of all the taphonomic parameters. As this study
used only molar digestion as an indicator of predator-induced
modifications, we rely on the classifications for these elements to
identify the accumulating agent. Table 1 presents Andrews’ (1990)
modification categories for molars by digestion. Loose molars were
assigned to one of five categories of digestion intensity: none, light,
moderate, heavy, extreme. For molars, there is a differential
digestion based on taxon i.e., voles, mice and shrews. Microtines,
murids, and shrews undergo digestion by predators at different
rates (e.g., Weissbrod et al., 2005) and therefore the taphonomic
analysis of each taxon was performed separately. As voles (Microtus
guentheri) comprise 80e90% of each assemblage in this study, we
confined the taphonomic analysis of digestion to Microtus molars in
order to obtained robust results.
Since many of the molars were also fragmented, we sampled
randomly from each of the sub-units for the taphonomic study. The
sample size for each sub-unit (n ¼ 68; n ¼ 33; n ¼ 132 for B1, B2 and
B4 respectively) is above sample sizes needed to estimate the
parameters of a normal distribution with a 95% confidence interval,
usually set at n ¼ 25 (Legendre and Legendre, 1998).
To determine if the distribution of the degree of digestion of
molars and the frequencies of teeth varied between strata we used
a c2 contingency r x c test of association with bootstrapping (see
details in the Supplementary data).
To identify the predator(s) that contributed to the accumulation
of the assemblage of each sub-unit, we compared the distribution
of the levels of intensity of the digested molars to those of known
predators (Andrews, 1990). These distributions were then analyzed
by using a cluster analysis, which applied the BrayeCurtis similarity
index (see details in Supplementary data).
2.2.3. Biodiversity
The ecological diversity for each of Amud’s stratigraphic subunits was measured using four parameters across the analytical
and taxonomic hierarchical scales. The first analysis was aimed at
whole community biodiversity and included diversity indices such
as species richness, dominance, and ShannoneWiener. The second
Table 1
Classification of predator groups (After Andrews, 1990) based on degree of molar digestion.
Predator Category
Molar digestion
Taxon examples for molar digestion
I (Little modification)
<3% of molars digested, digestion is limited to the
occlusal corners of the salient angles of the teeth.
4e6% of molar digested, digestion is limited to the
occlusal corners of the salient angles of the teeth.
18e22% molar digested, molars have strongly rounded
corners and the dentine exposed from projecting angle.
50e70% of molars digested with edges of microtine teeth
denuded of enamel
50e100% digested molars, digestion of enamel and dentine.
Barn owl, Long-eared Owl and Short-eared owl
II (Intermediate modification)
III (Moderate modification)
IV (Great modification)
V (Extreme modification)
Snowy Owl,
European owl and Tawny Owl
Little Owl, Kestrel and Peregrine
Buzzard and red kite
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analysis was aimed at the distribution of taxonomic composition
through time at three levels: presenceeabsence, rank abundance
and proportional abundance. Comparison of the four parameters
across all the hierarchical numerical scales in the community
(Rahel, 1990) was used to test change in biodiversity throughout
the Amud sequence and as a proxy for environmental productivity.
2.2.3.1. Diversity indices. Species richness (S) was calculated as the
number of species identified in each sample (Magurran, 2003).
Because samples from the various sub-units differed in size
(measured as NISP [Number of Identified Specimens]), species
richness might be attributed to sample size as opposed to ecological
differences (Magurran, 2003). To compare species richness from
unequal sample sizes, we conducted a rarefaction analysis using the
freeware Analytic Rarefaction 1.3 (http://www.uga.edu/strata/
software/). Rarefaction curves were based on the NISP quantification method.
Communities that have equal species richness may differ in
abundances. Where one community may have a high abundance of
a single or several species (i.e., low evenness or high dominance), in
another community all species may occur in a near equal abundance (i.e., high evenness or low dominance). In addition, informational diversity indices (e.g., the ShannoneWiener index (H0 ),
the SHE analysis and the Brillouin Index; see Magurran (2003) for
details) are based on the rationale that diversity in a natural system
is a proxy for the entropy or information of a system and can be
measured as the average amount of diversity conveyed by the
probability (i.e. the abundance) of discrete random variables (i.e.
species). Thus, indices that include taxa abundance are more
informative of community ecological diversity than those that
include only species richness, though the former may be more
susceptible to taphonomic processes. Nonetheless, both forms of
diversity estimates are given for comparison value. We compared
community diversity among Amud sub-units using: the ShannoneWiener index of diversity (H0 ) and the Simpson’s Dominance
index (D). The significance of each index across the stratigraphic
units was obtained by bootstrapping (see Supplementary data).
2.2.3.2. Taxonomic composition. Species distributions at the presenceeabsence and proportional abundance scale (Bennington and
Bambach, 1996) were compared using a c2 contingency r x c test of
association (Sokal and Rohlf, 1995) with P values estimated by
bootstrapping.
The first method, which was applied both to presenceeabsence
and proportion abundance data, is commonly used in paleoecological studies to test for the association between stratigraphic
units and species distribution. A c2 contingency r x c test of association was used to test for the association between the relative
abundance of taxa and the three stratigraphic sub-units of Amud
Cave. The test statistic was compared across the three different
assemblages (i.e., populations) to test if they derived from the same
underlying presenceeabsence and/or abundance distributions,
which would suggest that there was no change in the community
throughout the sequence (see Supplementary data). To determine
which taxon changed in abundance throughout the sequence of
Amud cave, we compared the proportion of each taxon (using NISP)
across the sub-units using the 95% binomial distribution, which
was calculated for each taxon separately (Wolda, 1978).
The second method, Q mode analysis, aims to address the high
variability in fossil species distribution in space, time and the
unknown effects of taphonomy which may hinder a statistically
rigorous test based on abundance data. We used the Bray Curtis
index for abundance data and the Jaccard index for presenceeabsence data. In order to determine if the difference in
taxonomic composition between the two sub-units signifies
a turnover or shift in community membership, we applied two
cluster analyses using the similarity indices defined above (see
Supplementary data).
2.2.3.3. Rank abundance. It has been shown that live-death
agreement studies tend to preserve rank order (Reed, 2007;
Terry, 2008, 2010). To assess the correlation in rank abundance
between two assemblages, we used a one-tailed Kendal’s Tau nonparametric correlation. Statistical analysis was performed using
SPSS 18.0.
2.3. Paleoecological reconstruction along the Amud sequence
Several methods for reconstructing paleoecology and habitats
based on micromamalian remains have been described in the
literature (Andrews and Evans, 1979; Andrews et al., 1979; Avery,
1988; Montuire et al., 1997; Fernández-Jalvo et al., 1998).
Different methods focus on different aspects of the environment.
Some will provide aspects of climate (i.e. temperature), while
others will focus on vegetation type, microhabitats ecotones. When
choosing the appropriate method, we considered several aspects
and chose the most appropriate for the question at hand. As the aim
of the study was to address the question of aridification throughout
the sequence, we opted to focus on a woodland/grassland classification, which has been shown correlate with precipitation levels
(Danin and Orshan, 1990).
Paleoecological reconstruction based on rodent taxa was based
on two methods. The first was based upon inferences about environmental preferences based on modern taxa (Tchernov, 1982,
1986). The second method was based on a multivariate analysis
of modern communities (Andrews, 1990; Reed, 2005).
In southwestern Asia, there are in general a north-to-south and
a west-to-east gradient in precipitation, associated with a number
of phytogeographic zones: mesic Mediterranean, xeric Mediterranean, semi-arid and arid phytogeographic zones (Danin and
Orshan, 1990; Kadmon and Danin, 1999). To the north, the region
is bound by the Hyper-mesic Mediterranean and the Pontic biomes,
whereas to the south it borders the dry Arabian biome (Zohary,
1982). There is a positive correlation between precipitation and
percent of woody vegetation in a given region. Hence the relative
proportions between woody and grass vegetation forms within
each region may serve as a proxy for the different phytogeographic
zones in the Southern Levant (Danin and Orshan, 1990; Kadmon
and Danin, 1999; Kutiel et al., 2000).
Since all micromammal species found in Amud exist today
(albeit not necessarily in the study area) we assumed that the
ecological preferences of the Middle Paleolithic taxa were the same
as those extant species (Belmaker et al., 2001; Belmaker, 2002).
Each species found in the Amud assemblages was assigned a woody
or grass vegetation form based on the preferred vegetation form of
its extant relative (Table 2) (Harrison and Bates, 1991; Mendelssohn
and Yom-Tov, 1999). The change over time based on relative
abundance of NISP assigned to each habitat was used to track
changes in paleoenvironments.
Rodent assemblages derived from modern barn owl pellets
shown high fidelity in presenceeabsence of species to the living
community from which they are derived (Reed, 2005; Terry, 2010)
and therefore are a good source for reconstructing modern habitats.
We scanned the literature on micromammal species distributions
as derived from barn owl pellets in different localities representative of the climatic regions (Table 3). Urban and agricultural
settings, which may be biased toward an increase in anthropogenic
habitats and commensal species, were omitted from the database.
Also included are data of fossil micromammal assemblages from
contemporaneous MIS 4e3 sites: Kebara VIeXII (Tchernov, 1998),
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M. Belmaker, E. Hovers / Quaternary Science Reviews 30 (2011) 3196e3209
Table 2
Distribution of micromammal taxa in different phytogeographic zones and vegetation types in the Southern Levant.
Species
Preferred vegetation Biome present in
type
Apodemus cf. mystacinus Woody vegetation
Cricetulus migratorius
Grass vegetation
Crocidura leucodon
Crocidura russula
Meriones tristrami
Woody vegetation
Woody vegetation
Grass vegetation
Microtus guentheri
Grass vegetation
Myomimus roachi
Woody vegetation
Mus macedonicus
Sciurus anomalus
Woody vegetation
Woody vegetation
Spalax ehrenbergi
Grass vegetation
Mesic Mediterraean
Mesic Mediterranean,
Xeric Mediterranean
Mesic Mediterraean
Mesic Mediterraean
Mesic Mediterranean,
Xeric Mediterranean
Mesic Mediterranean,
Xeric Mediterranean
Hyper-mesic Mediterranean,
Pontic
Ubiquitous
Hyper-mesic Mediterranean,
Pontic
Mesic Mediterranean,
Xeric Mediterranean, Semi Arid
Geula (Heller, 1970), Tabun B (Bate, 1937) and Douara (Payne, 1983).
The micromammals from these sites were accumulated by barn
owls (Payne, 1983; Belmaker, 2008). Therefore, ecological reconstructions derived from either modern or fossil assemblages should
provide comparable results.
In order to determine if the difference in taxonomic composition
between the sites signifies differences in community membership
and thus a different local ecology, we applied a neighbor joining
clustering using the Jaccard similarity index (defined above) (see
Supplementary data).
3. Results
Five hundred and fifty-four molars were retrieved from the
three samples, representing a minimum of 90 individuals distributed nearly equally across the stratigraphic sub-units. Taxonomic
distribution of rodents and insectivores at the site comprises ten
species (Table 4).
3.1. Taphonomy
3.1.1. Molar digestion
Table 5 shows the results of molar digestion intensity for the
three Amud sub-units. Results of the bootstrap chi-square test
indicate that the three sub-units do not differ in intensity of
digestion (c2 ¼ 3.79, estimated P value for 1000 iterations ¼ 0.97).
Results indicate that the distribution of digestion categories among
the micromammal assemblages from Amud included a high
proportion of undigested or only lightly digested molars (Fig. 2).
Table 3
Species distributions as derived from Barn Owl pellets in different localities representative of the climatic regions in Southwest Asia.
Site
Phytogeographic
zone
Reference
Be’erotayim, Israel
Sapir, Israel
Nizzana, Israel
Kharabow, Syria
Khrab al Shaham, Syria
Cliff Cave, Turkey
18 sites raging from Beer
Tuvia to Tel Hai, Israel
Carmel, Isah Cave, Israel
Arid
Arid
Arid
Semi Arid
Xeric Mediterranean
Pontic
Mesic Med
Rekasi and Hovel (1997)
Pokines (1997)
Tores and Yom-Tov (2003)
Shehab (2005)
Shehab (2005)
Corbet and Morris (1967)
Dor (1947)
Mesic Med
Weissbrod et al. (2005)
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Table 4
Taxonomic distribution of Amud micromammals by sub-units. Data in percentages
(absolute numbers given in parentheses).
Species
A. NISP
Apodemus cf. mystacinus
Cricetulus migratorius
Crocidura leucodon
Crocidura russula
Meriones tristrami
Microtus guentheri
Myomimus roachi
Mus macedonicus
Sciurus anomalus
Spalax ehrenbergi
Total
B. MNI
Apodemus cf. mystacinus
Cricetulus migratorius
Crocidura leucodon
Crocidura russula
Meriones tristrami
Microtus guentheri
Myomimus roachi
Mus macedonicus
Sciurus anomalus
Spalax ehrenbergi
Total
C. MNI without Microtus
Apodemus cf. mystacinus
Cricetulus migratorius
Crocidura leucodon
Crocidura russula
Meriones tristrami
Myomimus roachi
Mus macedonicus
Sciurus anomalus
Spalax ehrenbergi
Total
B1
B2
B4
9.74 (19)
1.03 (2)
0.51 (1)
0 (0)
1.54 (3)
68.21 (133)
6.67 (13)
9.23 (18)
0.51 (1)
2.56 (5)
100 (195)
7.27 (12)
0 (0)
0.61 (1)
0 (0)
20 (33)
55.15 (91)
1.82 (3)
12.12 (20)
0 (0)
3.03 (5)
100 (165)
0.63 (1)
0 (0)
0 (0)
1.26 (2)
3.77 (6)
89.94 (143)
1.26 (2)
1.26 (2)
0.63 (1)
1.26 (2)
100 (159)
12.90 (4)
3.23 (1)
3.23 (1)
0 (0)
3.23 (1)
41.94 (13)
6.45 (2)
22.58 (7)
3.23 (1)
3.23 (1)
100 (31)
16.13 (5)
0 (0)
3.23 (1)
0 (0)
16.13 (5)
32.26 (10)
3.23 (1)
25.81 (8)
0.00 (0)
3.23 (1)
100 (31)
3.33 (1)
0 (0)
0 (0)
3.33 (1)
6.67 (2)
73.33 (22)
3.33 (1)
3.33 (1)
3.33 (1)
3.33 (1)
100 (30)
22.22 (4)
5.88 (1)
5.88 (0)
0 (0)
5.56 (1)
11.11 (2)
38.89 (7)
5.56 (1)
5.56 (1)
100 (18)
25 (5)
0 (0)
5 (1)
0 (0)
23.81 (5)
4.76 (1)
38.1 (8)
0 (0)
4.76 (1)
100 (21)
14.29
0
14.29
12.5
25
12.5
12.5
12.5
12.5
100
(1)
(0)
(0)
(1)
(2)
(1)
(1)
(1)
(1)
(8)
3.1.2. Predator type
To test for predator type we compared the patter of molar
digestion with those of known predators. Since results of the chisquare test indicated that there is no difference between Amud
sub-units, we combined the data to obtain a single sample to
increase the robusticity of the results. Results of the cluster analysis
(Fig. 3) suggest that the Amud assemblage is equally consistent
with either predator type 1 or 2. The most common representative
of predator types 1 and 2 in the region are the barn owl (T. alba)
and, respectively the European eagle owl (Bubo bubo).
3.2. Biodiversity
3.2.1. Diversity indices
Fig. 4 presents the species richness (S) across the Amud subunits with 95% confidence intervals. B1 is the richest unit with 8
species followed by B2 and B4 with 7 species each. However, subunit B1 also has the largest sample size of all sub-units (195, 165
Table 5
Breakdown of levels of digestion in Microtus guentheri molars in the various subunits of Amud Cave. Data in percentages (absolute numbers given in parentheses).
Variable
Molar digestion
None
Light
Moderate
Heavy
Extreme
B1
B2
B4
23.53 (16)
58.82 (40)
11.76 (8)
5.88 (4)
0 (0)
27.27 (9)
60.61 (20)
12.12 (4)
0 (0)
0 (0)
25.76 (34)
54.55 (72)
10.61 (14)
9.09 (12)
0 (0)
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Fig. 4. Species richness for the three Amud sub-units with 95% confidence intervals.
Fig. 2. Percent digested Microtus molars in Amud compared to selected predators.
Data for predators retrieved from Andrews (1990).
and 159 in B1, B2 and B4 respectively). Therefore, the difference in
species richness may correlate only to sample size.
Fig. 5 shows the results for the point-by-point rarefaction of the
three Amud sub-units with 95% confidence intervals. Since the
rarefaction curves for all three sub-units overlap, the species richness is not due to difference in the ecology of the sub-units but due
to the differences in sampling between the sub-units. This is further
supported by evidence using 95% confidence intervals (Fig. 4),
where the 95% confidence intervals for species richness overlap for
all three samples. Moreover, there is no directional decrease or
increase in species richness between the samples, which would
have been expected in a scenario of a directional change in environmental productivity.
Fig. 3. Dendrogram assigning Amud sub-units to predator category (Andrews, 1990)
using BrayeCurtis Similarity index.
Fig. 6 presents the differences in the biodiversity indices
(Dominance D and ShannoneWeiner H0 ) across the three sub-units
after bootstrapping. Results indicate that the samples do not differ
at the 95% confidence interval for either index.
3.2.2. Taxonomic composition
The result of the c2 contingency r x c test of association indicates
that there is a significant association between species composition
and stratigraphic sub-unit. This relationship is not significant for
presenceeabsence data (presenceeabsence c2 ¼ 5.04, estimated P
value for 1000 iterations ¼ 0.734). However, it is significant for the
relative abundance data (c2 ¼ 105.039, estimated P value for 1000
iterations ¼ 0.001). Following this result, we tested which individual taxon abundances changed through time. Fig. 7 presents the
shift in relative abundances of all species, with a 95% confidence
interval calculated based on the binomial distribution using NISP.
Four species show significant shifts in abundance through time: M.
guentheri, Apodemus cf. mystacinus, Meriones tristrami and Mus
macedonicus. All other changes of species relative abundances are
contained within the 95% confidence interval. The proportion of
Microtus is highest in B4 and decreases in B2 and B1. Within the 95%
Fig. 5. Point-by-point rarefaction curves for the three Amud sub-units.
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confidence interval, there is no change between B2 and B1 in the
proportion of Microtus. This pattern is mirrored in the distributions
of Mus and Apodemus that are lowest in B4 but increase in B2 and
B1. Again, there is no significant difference between B2 and B1 in
the distributions of these two taxa. The abundance trend of M.
tristrami differs in that it is lowest in B4, increases in B2 and
decreases again in B1.
Fig. 8 presents the dendrograms for the three Amud sub-units
based on the Jaccard similarity index and the BrayeCurtis similarity index. For presenceeabsence, sub-units B1 and B2 cluster
together with B4 forming an outgroup, while based on relative
abundance B1 and B4 cluster together and B2 forms the outgroup.
Results of the rank data for one-tailed non-parametric correlation indicate that all three pair-wise correlations were significantly
different at the 0.1 significance level or less (B1eB2: Spearman’s
rho ¼ 0.861, P value ¼ 0.001; B1eB4: Spearman’s rho ¼ 0.508, P
value ¼ 0.081; B2eB4: Spearman’s rho ¼ 0.706, P value ¼ 0.017).
These results suggest that there is a shift in relative abundance
but not in rank order or presenceeabsence. The results emphasize
the nested hierarchical changes over time in the composition of the
micromammal community in Amud Cave.
3.3. The paleoecology of Amud Cave
Results of the habitat distribution are presented in Fig. 9 and
indicate a decrease in distribution of grassland vegetation forms
and an increase of woodlands from sub-unit B4 to sub-units B2 and
B1. There is no significant change between sub-units B2 and B1.
In order to test if rodent communities can distinguish between
biomes in the southern Levant, we first performed a neighborjoining cluster using only modern data. These results are shown
in Fig. 10a. Two clear clusters are observed. One comprises of
assemblages from the mesic Mediterranean, xeric Mediterranean
and Pontic phytogeographic zones, which have an average annual
rainfall of over 350 mm; the other cluster consists of assemblages
from the semi-arid and arid zones (i.e., less that 350 mm/year).
Fig. 10b shows the results of the cluster analysis that includes both
the archaeological and the modern samples. Since there was no
difference in presenceeabsence in micromammal taxa between the
Fig. 6. Dominance and ShannoneWiener indices for the three Amud sub-units with
95% confidence intervals.
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Amud sub-units, we opted to combine them into a single assemblage to increase the assemblage size. Here, Amud, together with
other Middle Paleolithic sites (Kebara, Geula, Tabun and Douara)
cluster together. All the fossil assemblages are more similar to the
Mediterranean and Pontic habitats than to the arid ones. Notably,
the Middle Paleolithic assemblages differ from modern mesic and
xeric Mediterranean samples in the presence of two taxa, the
mouse-tailed dormouse (Myomimus roachi) and the Persian
squirrel (Sciurus anomalus), known today from the Pontic region.
4. Discussion
The taphonomic analyses conducted on the three assemblages
of rodent bones from Amud Cave suggest that the three assemblages are isotaphonomic, i.e., were subjected to similar predator
taphonomic processes. Specifically, the predators responsible for
the accumulation of all three sub-units belonged to type 1 or 2
(Andrews, 1990), most probably the European Eagle owl (Bubo
bubo) and/or Barn owl (T. alba). It has been claimed that the
paleoecological comparison among isotaphonomic assemblages
(such as among the three sub-units of Amud Cave) should reflect
ecological changes rather than changes in predator preferences
(e.g., Fernández-Jalvo et al., 1998; Reed, 2005).
The micromammal remains from Amud Cave comprise 10
species across three stratigraphic units. There is no change in the
diversity indices throughout the 15 kyr of the site’s sequence. None
of the diversity indices indicate shifts throughout the sequence.
When testing for diachronic changes in taxonomic composition at
the presenceeabsence level or at the rank abundance level, no
significant changes are observed. Furthermore, presenceeabsence
paleoecological analysis shows that all three assemblages are
indistinguishable from those formed in Mediterranean wet habitats
(mesic, xeric and Pontic), and can be qualified as falling within this
group of phtyogeographic zones.
In contrast, there is a significant change over time at the level of
relative abundance through time of the four most common species:
M. guentheri, Apodemus cf. mystacinus, M. tristrami and M. macedonicus. Given the preferred habitats of these taxa, this apparently
reflects a diachronic change of paleo-habitats around the cave.
Specifically, there seems to be a decrease in grassland habitats from
sub-unit B4 to sub-unit B1 and a concomitant increase in woodland
Fig. 7. Changes in individual taxa through the Amud sequence with 95% confidence
intervals based on NISP.
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Fig. 8. Dendrogram of similarity between the Amud sub-units: A) based on presenceeabsence; B) based on relative abundance.
habitats. The pattern observed along the Amud sequence is
consistent with the model described for nested hierarchical
communities (Rahel, 1990), such that the Amud micromammal
communities appear stable at a high-level response (presenceeabsence, rank) yet undergo change at the low-level
response (proportional abundance), to environmental change.
These trends in the rodent community of Amud Cave seem
discordant with other contemporaneous paleoenvironmental
proxies in the Levant. Phytolith analysis in Amud Cave suggested
a change to a generally more xeric environment at the time of subunits B2 and B1 compared to B4 (Madella et al., 2002). On a regional
scale, climate change recorded in the isotopic record from Peqi’in
Cave (Upper Galilee, Israel) is interpreted to indicate a shift from
wet to dry climate (Bar-Matthews et al., 2003) and a decrease in
productivity during the time period corresponding to the Amud
sequence (Shea, 2008). This pattern is consistent with the trend
inferred from stable isotope data from foraminifera in East Mediterranean sediment cores (Bar-Matthews et al., 2003), and pollen in
marine sediment cores in the Eastern Mediterranean (Almogi-Labin
et al., 2004). Palynological analysis of core 95-09 in the Eastern
Mediterranean (75.5e56.3 ka) indicates a low proportion of arboreal pollen along the entire sequence (<8%). Deciduous oak is more
prevalent in the lower part of the core, supporting a trend of drying
throughout the Last Glacial in general, and a decline in regional
productivity throughout the MIS 4 in particular (Langgut, 2008). It
is worth noting, however, that this core is located in the southern
part of the Eastern Mediterranean and may not reflect conditions in
the northern part, where Amud is situated. All these proxies
suggest increasing aridification during the time span 70e55 ka.
The differences in inferences drawn from the micromammal
data compared to other paleoecological proxies seem difficult to
reconcile. One possibility of resolving the discordance is that presenceeabsence analyses of raptor-derived micromammal assemblages have higher paleoecological fidelity than relative abundance
analyses. If this is true, the presenceeabsence results from Amud
Cave do not indicate a significant environmental change
throughout the sequence. On the other hand, the relative abundance data may be biased.
Barn and Eagle owls are considered small-mammal specialists in
terms of diet (Love et al., 2000). It has been argued that owls in
general exhibit a high degree of opportunism within a certain size
group of mammals and thus micromammal assemblages derived
from owl accumulations accurately represent the environment.
Furthermore, owls tend to sample a wider range of habitats, and it
may be assumed that the relative abundance of prey taxa reflects
the environment accurately (Tchernov, 1991; Yom-Tov and Wool,
1997). Analysis of the diet of Barn Owl in Argentina suggested that
it hunts prey in accordance to the proportion of taxa along
a gradient (Traviani et al., 1997). However, other studies have
indicated that the Barn Owl pellets are only good representatives of
Fig. 9. Habitat reconstruction for the three Amud sub-units based on taxon preference
based on NISP.
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Fig. 10. Dendrogram representation of Amud sub-units compared to modern ecosystems, based on rodent assemblages derived from pellet material using neighbor joining
clustering and Jaccard similarity index. A) modern assemblages; B) fossil and modern assemblages.
species presenceeabsence in the living community (Avenant,
2005). For example, several studies found that Barn Owls were
highly selective predators, such that no correlation existed between
the abundance of preyed taxa in the owl pellets and their abundances in the immediate environment (Jorgensen et al., 1998). Thus,
the question of the fidelity of relative abundance of owl prey to
their environments remains an open question.
The above examples derive from ecological analyses of modern
pellet-trap. Thus, they do not include time and space averaging or
taphonomic considerations. Terry (2010) noted that the fidelity in
relative abundance of live-death studies dropped noticeably for
assemblages that were time-averaged from ca 20 to ca 300 years.
For assemblages such as those from Amud or other Levantine
Middle Paleolithic sites, which are averaged over a much longer
period, the fidelity of relative abundance measures may be much
lower..
Another confounding factor in the study of Amud’s rodent
assemblages is the high selectivity of Barn Owl and Eagle owl to
microtines, which typically comprise over 80% of the diet (Andrews,
1990), and ca 55e90% in Amud (based on NISP). Tchernov (1991)
pointed out that although owls show selectivity toward microtines, it would be averaged out in the fossil record, and that
ecological shifts would be picked up despite this preference. Most
of the community structure changes between the sub-units of
Amud Cave (diversity, richness, habitat assignment) may be
attributed to the high proportion of Microtus in the assemblages.
This begs the question whether the increased abundance of
Microtus (in all sub-units) is by itself a taphonomic bias, and does
not reflect the species’ prevalence in the environment. The difference observed in relative abundances when using raw abundance
data may be due to taphonomic or sampling bias previously not
addressed. The results of an estimated Jaccard similarity index
based on abundances (Chao et al., 2005), which accounts for species
missing due to sampling bias, suggest that all sub-units are in fact
similar, supports this hypothesis.
Other taphonomic processes such as geogenic or anthropogenic
transport may alter the relative proportion of taxa in the fossil
record. Specifically, Microtus teeth tend to be more easily transported via fluvial processes than murid teeth (Wolff, 1973). In this
study, sub-unit B4 was excavated in the center of the cave (a
topographic low) while samples from sub-units B2 and B1 were
taken from topographically elevated area near the cave wall
(Alperson-Afil and Hovers, 2005: Fig. 3). We assume that the pellets
were originally dropped near the walls of the cave. The higher
proportion of microtine molars in sub-unit B4 may be the result of
increased transport from areas near the wall. Given the nature of
the cave’s sediments (Chinzei, 1970; Hovers et al., 1991; Valladas
et al., 1999) this would be due mostly to colluvial processes.
While this hypothesis requires further testing, it is supported by the
higher fragmentation level of micromammal dentition in sub-unit
B4. This would suggest that the high proportion of microtine
teeth in the assemblage and the change in their relative distribution
throughout the sequence of Amud cave is not related to climatic
changes but rather to variation in Barn owl diet and/or syn- and
post-depositional movement within the cave.
The Amud micromammal communities are stable at a high level
(presenceeabsence, rank) of Rahel’s (1990) nested hierarchical
model. Results of the presenceeabsence, rank and community level
analysis indicate that all three sub-units were similar and that there
is no change in diversity or community composition throughout the
sequence. Taphonomic factors preclude definitive conclusions
regarding persistence or change at the low-level response of
proportional abundance. Thus there is still a discrepancy between
the climatic stability as inferred from the presenceeabsence of
Amud’s micromammals and the shifts observed by other proxies
(stable isotopes, pollen).
This discrepancy is more apparent than real. The question to
focus on is the multi-faceted response of faunal communities to
levels and amplitudes of climate changes. The responses of taxa to
climate shifts cannot be modeled as merely linear responses to
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vegetation shifts. Vegetation forms may change (e.g., from woody
to grasslands), but the response of micromammalian communities
lags behind (Montuire and Girard, 1998). The interval of 15 kyr
between the deposition of sub-unit B4 and of B2 and B1 may not
have been sufficiently long to resolve a significant community level
change.
In fact, in the Eastern Mediterranean Levant, the correlation
between vegetation forms e woody, herbaceous and annuals e is
not linear but a logarithmic one (Kutiel et al., 2000). There is
a linear relationship between percent of woody vegetation and
annual rainfall in the semi-arid and arid phytogeographic zones.
This relationship disappears when the annual rainfall crosses the
threshold value of 300 mm annual rainfall, which separates the
semi-arid and from the xeric Mediterranean, i.e., in the xeric and
mesic Mediterranean zones this relationship does not hold.
In the paleoclimatic record, the isotopic shift observed in the
speleothem record 76e50 ka is less than 1&. This shift is equivalent
to 200 mm rain (Bar-Matthews et al., 2003). Therefore, even if the
average annual rainfall during this time span decreased enough to
leave an isotopic signature (Bar-Matthews et al., 2003), the decrease
may not have been sufficient to have led to a change in the micromammal communities of the xeric and mesic Mediterranean zones.
The results obtained from the study of Amud’s micromammal
assemblages are consistent with results obtained from other faunal
analyses within Middle Paleolithic sites. Analysis of the large
mammals at the site does not indicate changes in the faunal
composition over time (Rabinovich and Hovers, 2004). The taxonomic distributions of the large mammals are consistent with
a mesic-xeric Mediterranean fauna, including Gazella gazella, Dama
mesopotamica, Cervus elaphus and Capreolus capreolus. The Amud
assemblages do not include taxa that are typical of semi-arid environments such as Camelus sp. and Struthio camelus (Griggo, 2004).
Comparison between the micromammal assemblages of Amud
Cave and other contemporaneous sites reveals that they are similar,
and that all the assemblages are associated with humid Mediterranean (mesic, xeric and Pontic) zones. Differences between Amud
and the Mount Carmel Middle Paleolithic assemblages are
restricted to the cricetid Mesocricetus auratus. This taxon is present
in Kebara, Geula and Douara Caves and is missing from the Amud
and Tabun samples.
Today, the Carmel and eastern Upper Galilee where Amud is
situated are two different geomorphological districts that receive
slightly different amounts of rainfall (Danin and Orshan, 1990),
which would suggest that they might have slightly different rodent
communities. Still, given that sample sizes from Amud (NISP ¼ 554)
and Tabun (Bate, 1937) are low compared to Kebara (NISP ¼ 2374),
the absence of M. auratus from Amud and Tabun may be an artifact
of sample size rather a reflection of an ecotonal shift between the
Mount Carmel region in the west and Upper Galilee in the east.
With the exception of four taxa, micromammal species
composition in Amud cave and those in other contemporaneous
Middle Paleolithic sites are similar to those seen today in the
respective regions, with the exception of the presence of two taxa
not present today in the Carmel, Upper Galilee and the Palmyra
Basin, M. roachi (mouse-tailed dormouse) and Sciurus anomalus
(Syrian squirrel), and two species, Gerbillus dasyurus and Acomys
cahirinius, which are present in the region today but absent from
the Carmel and Upper Galilee (Shalmon et al., 1993).
M. roachi is a rare species with a unique taxonomic history.
Today its modern counterpart is known as Myomimus personatus
(Corbet and Morris, 1967) with a patchy distribution that includes
Bulgaria, Thrace, western Turkey (Ognev, 1963; Daams and De
Bruijn, 1994). Fossil specimens identified as M. roachi in level B in
Tabun Cave (Bate, 1937) were shown to be the same species as
M. personatus. Subsequent analyses have identified two extant
species, the western M. bulgaricus (Rossolimo, 1976a,b) and an
eastern M. setzeri, which is found in extreme southwestern
Turkmenistan, and perhaps Afghanistan. The fossil species present
in the Levant e M. roachi, M. personatus and M. bulgaricus e are
synonymous with M. roachi, the senior taxonomic name and thus
the one applied to the taxon in this paper. The taxon present in
Amud can be traced to the extant species present in Bulgaria,
Thrace and Western Turkey, which was prevalent in the Southern
Levant as early as ca 400 ka (Tabun E). The modern habitat of
M. roachi is terrestrial; it lives in small bushes and underground.
The preferred climate in the taxon’s modern day distribution
includes an average annual rainfall between 700 and 1000 mm,
higher than the present-day annual mean in the Lower Galilee.
The Persian squirrel, Scirius anomalus, includes four subspecies
that differ in pelage appearance: S. a. pallescens, known from Iraq;
S. a. anomalus, known from the Caucasus, and S. a syriacus that is
known from the northern regions of the Southern Levant (Lebanon,
The Hermon Mt. Golan Heights and Northern Jordan). The Amud
Cave specimens cannot be assigned to subspecies. Specimens
attributed to Sciurus anomalus have been present in the southern
Levant since MIS 6. Today the taxon is arboreal and requires dense
oak and pine forests. Annual precipitation in its distribution areas is
in the range of 750e1000 mm.
Two taxa, G. dasyurus and A. cahirinius, are present in the region
today and are absent from Amud and the Mt. Carmel caves. These
taxa are indicative of more arid environment and rocky habitats
and appear in the region during MIS 3 in the Upper Paleolithic
layers (IVeIII) of Kebara and Hayonim (layer D) Caves, as well as at
the Upper Paleolithic levels in the Carmel caves of Sefunim and
Rakefet.
The presence in Middle Paleolithic horizons dated to MIS 4 of
M. roachi and S. anomalus is indicative of cooler and more humid
climates than are present in the region today (Harrison and Bates,
1991). When combined with the absence of G. dasyurus and
A. cahirinius, this supports a reconstruction of cooler and wetter
climate for these sites.
Using other paleoecological proxies, the Mt. Carmel sites have
been shown to be situated in Oak woodland and a Mediterranean
climate (Alberts et al., 1999, 2000, 2003). Douara Cave is an
exception in that its Middle Paleolithic environment appears to
have been similar to that of today (Payne, 1983). This is consistent
with its relative distance from the other Israeli Middle Paleolithic
sites that cluster together. Still, Douara and the Mt. Carmel sites and
Amud Cave do share some taxa, which suggests shared Middle
Paleolithic climatic characteristics. Specifically, they all cluster most
closely with the rodent assemblages from the Pontic zone (Fig. 10b),
which today receives higher annual precipitation levels (ca
1000e1200 mm of precipitation annually) than any of the sites. In
Douara this is consistent with the vegetal evidence for Celtis australis (Matsutani, 1987).
A major drying trend characterizes the later part of the Last
Glacial, 56.3e16.2 ka (Langgut, 2008). The appearance of G.
dasyurus and Acomys cahirinus in the southern Levant in the Upper
Paleolithic may be associated with this post-MIS 4 aridification.
This has been associated with other arid indicators in the faunal
assemblages, such as an increase in the proportion of gazelle over
fallow deer (see review in Rabinovich, 2003). Nonetheless, both the
dormouse and squirrel became extinct from the Levant only during
the warmer and much drier mid-Holocene (Tchernov, 1988b). Were
one to invoke a climatic explanation for this extinction, it would be
expected to happen at the MIS 4/3 transition. The extended postMIS 4 survival of the dormouse suggests that its extinction may
not have been entirely related to severe Heinrich 5 climatic event.
It is important that interpretations of paleoclimatic proxies
are not always concordant. Bar-Matthews et al. (1999, 2003)
Author's personal copy
M. Belmaker, E. Hovers / Quaternary Science Reviews 30 (2011) 3196e3209
interpret the speleothem data as indicative of cooler and drier
conditions during the Last Glacial, a reconstruction supported by
pollen (Langgut, 2008) and foraminifera spectra (Schilman et al.,
2002). Enzel et al. (2008) and Frumkin et al. (2011) argue that
speleothems cannot be used to reconstruct paleo-rainfall. Based on
Lake Lisan levels, they suggest that the Last Glacial of the southern
Mediterranean was wetter and more humid than today (e.g., Lisker
et al., 2009). A pollen core from Lake Hula similarly suggests that
the Last Glacial was cold and more humid than today (WeinsteinEvron, 1983, 1990), with arboreal pollen remaining relatively
common throughout MIS 4e3. The paleoecological analysis of the
micromammal assemblages from Amud Cave speaks to a relatively
cool and wet environment 70e55 ka, a characteristic that is shared
with other contemporaneous sites across the southern Levant.
Given the time averaging inherent to the various paleoclimatic
proxies as well as paleoecological studies, this pattern cannot be
used to differentiate between a hypothesis arguing for a Last Glacial
that was wetter than today (Frumkin et al., 2011) or an alternative
scenario of intermittent periods of increased humidity within
a cold and dry Last Glacial (Bar-Matthews et al., 2003).
Shea (2008) raised the question of the extinction of the Levantine Neanderthals due to increased aridity throughout the MIS 4
and the climatic crisis that occurred during the Heinrich 5 (H5)
event of 50e45 ka. The assertion that climate shifts were responsible for hominin extinction in the region is based on the underlying hypotheses that the climatic change was severe enough to
cause depletion in resources. The important question is not
whether climate changes occurred but rather if climate change was
significant enough to warrant a response from large mammals,
including hominin populations?
While the Amud sequence does not span the H5, our results do
allow us to test the question of increasing aridity throughout the
Last Glacial. The results reported here do not depict a dramatic
response of the micromammal community to the climatic changes
documented in the region between 70 and 55 ka. We infer that any
climate changes were below the threshold needed to effect the
micromammal community, and therefore only of small amplitudes.
Changes of the magnitude implied by our results would probably
not have a devastating effect on Neanderthal populations so as to
cause their complete local extinction, as hypothesized in the
climatic turnover scenario.
5. Conclusions
The results of this study suggest that changes in relative abundance of micromammal species throughout the Amud Cave
sequence are likely the result of taphonomic biases. Once such
biases are addressed, there is no shift in the presenceeabsence;
rank abundance and diversity measures of these communities in
the time span 70e55 ka. The persistence of the micromammal
community is consistent with low amplitude climate change. There
is no indication for a decrease in productivity and aridification
throughout the sequence of the cave, specifically toward the end of
the sequence at 55 ka. The species present are suggestive of a mesic
humid Oak woodland environment in Amud Cave and most of the
contemporaneous Middle Paleolithic sites in northern Israel.
Consequently, climate change may not have had a cause-and-effect
relationship with the disappearance of the local Neanderthal
populations from the southern Levant.
Acknowledgments
This study would not have taken place without the inspiration
and guidance of the late Eitan Tchernov, which began the identification of the micromammals sample of the Amud micromammals
3207
but passed away before completing the study. Funding for this
research was provided by the Israel Science Foundation (grants
#803/03, 514/04, 63/08), the Wenner-Gren Foundation (#6291)
and Irene Levy Sala CARE Foundation. MB is supported by the
American School for Prehistoric Research (ASPR), Harvard University. We thank Alon Barash, Navot Morag and Anna Schwartz for
their assistance in sample curation and sorting. Rivka Rabinovich
provided access to the mammalian and paleontological comparative collection, National Natural Collections, Hebrew University of
Jerusalem and Judy Chupasko enabled the use of the Mammalian
Collections at the Museum of Comparative Zoology, Cambridge,
MA. We are indebted to Pnina Shor, Judith Ben-Michael and Hava
Katz of the Israel Antiquity Authority for facilitating logistical
aspects of this research.
We thank Larry Flynn and two anonymous reviewers for their
critical reading and helpful comments on earlier drafts of this
paper.
Appendix. Supplementary material
Supplementary data associated with this article can be found, in
the online version, at doi:10.1016/j.quascirev.2011.08.001.
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