Taphonomic decoding of the paleobiological information locked in a Lower Pleistocene assemblage of large mammals

Abstract

The processes of fossilization have usually been perceived by paleontologists as destruc- tive ones, leading to consecutive (and in most cases irretrievable) losses of paleobiological infor- mation. However, recent developments of conceptual issues and methodological approaches have revealed that the decrease in paleobiological information runs parallel to the gain of taphonomic information. This taphonomic imprinting often makes it possible to decode the fraction of paleo- biological information that was lost during fossilization, and may also contribute new data for de- ciphering paleobiological information that was not originally preserved in the assemblage, such as paleoethology. A good example is the study of the macrovertebrate assemblage from the lower Pleistocene site at Venta Micena (Orce, southeastern Spain). Taphonomic analysis showed that the giant, short-faced hyenas (Pachycrocuta brevirostris) selectively transported ungulate carcasses and body parts to their maternity dens as a function of the mass of the ungulates scavenged. The frac- turing of major limb bones in the dens was also highly selective, correlating with marrow content and mineral density. Important differences in bone-cracking intensity were related to which species the bones came from, which in turn biased the composition of the bone assemblage. The analysis of mortality patterns deduced for ungulate species from juvenile/adult proportions revealed that most skeletal remains were scavenged by the hyenas from carcasses of animals hunted by hyper- carnivores, such as saber-tooths and wild dogs. Analytical study of the Venta Micena assemblage has unlocked paleobiological information that was lost during its taphonomic history, and has even provided paleobiological information that was not preserved in the original bone assemblage, such as the paleoethology of P. brevirostris, which differed substantially from modern hyenas in being a strict scavenger of the prey hunted by other carnivores.

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2001 The Paleontological Society. All rights reserved. 0094-8373/01/2703-0007/$1.00
Paleobiology, 27(3), 2001, pp. 512–530
Taphonomic decoding of the paleobiological information locked
in a lower Pleistocene assemblage of large mammals
Paul Palmqvist and Alfonso Arribas
Abstract.—The processes of fossilization have usually been perceived by paleontologists as destruc-
tive ones, leading to consecutive (and in most cases irretrievable) losses of paleobiological infor-
mation. However, recent developments of conceptual issues and methodological approaches have
revealed that the decrease in paleobiological information runs parallel to the gain of taphonomic
information. This taphonomic imprinting often makes it possible to decode the fraction of paleo-
biological information that was lost during fossilization, and may also contribute new data for de-
ciphering paleobiological information that was not originally preserved in the assemblage, such as
paleoethology. A good example is the study of the macrovertebrate assemblage from the lower
Pleistocene site at Venta Micena (Orce, southeastern Spain). Taphonomic analysis showed that the
giant, short-faced hyenas (Pachycrocuta brevirostris) selectively transported ungulate carcasses and
body parts to their maternity dens as a function of the mass of the ungulates scavenged. The frac-
turing of major limb bones in the dens was also highly selective, correlating with marrow content
and mineral density. Important differences in bone-cracking intensity were related to which species
the bones came from, which in turn biased the composition of the bone assemblage. The analysis
of mortality patterns deduced for ungulate species from juvenile/adult proportions revealed that
most skeletal remains were scavenged by the hyenas from carcasses of animals hunted by hyper-
carnivores, such as saber-tooths and wild dogs. Analytical study of the Venta Micena assemblage
has unlocked paleobiological information that was lost during its taphonomic history, and has even
provided paleobiological information that was not preserved in the original bone assemblage, such
as the paleoethology of P. brevirostris, which differed substantially from modern hyenas in being a
strict scavenger of the prey hunted by other carnivores.
Paul Palmqvist. Departamento de Geologı´a y Ecologı´a (A
´rea de Paleontologı´a), Facultad de Ciencias, Uni-
versidad de Ma´laga. 29071 Ma´laga, Spain. E-mail: Paul.Palmqvist@uma.es
Alfonso Arribas. Museo Geominero, Instituto Geolo´gico y Minero (I.G.M.E.), c/ Rı´os Rosas, 23. 28003
Madrid, Spain. E-mail: A.Arribas@igme.es
Accepted: 13 March 2001
Introduction
Prior to the 1980s most vertebrate taphon-
omists emphasized the incompleteness of the
fossil record, because the processes of fossil-
ization were envisioned as destructive, lead-
ing to loss of paleobiological information. As
a result, taphonomy came to be associated
with the documentation of information loss
and bias in the transition of organic remains
from the biosphere to the lithosphere. How-
ever, in their important paper Behrensmeyer
and Kidwell (1985) envisioned taphonomy as
‘‘the study of processes of preservation and
how they affect information in the fossil rec-
ord.’’ They were following the approach of nu-
merous invertebrate paleontologists who were
engaged since the mid-1980s in more ‘‘posi-
tive’’ aspects of comparative taphonomic re-
search intended to establish that postmortem
processes (e.g., weathering, transport, and
sorting) leave signatures that are useful and
diagnostic of various paleoenvironmental and
sedimentary conditions (Kidwell and Bosence
1991; Kidwell and Flessa 1995). Additionally,
time-averaging—viewed negatively by most
paleontologists in the past—is widely recog-
nized as advantageous, because short-term
ecological ‘‘noise’’ is dampened and longer-
term signals from a biological community are
preserved. In fact, bone assemblagesfrom sur-
face environments are considered comparable
in some respects to repeated ecological sur-
veys in assessing the long-term dynamics of
the potentially preservable fraction of terres-
trial communities (for review and references,
see Behrensmeyer and Hook 1992; Cutler et al.
1999; Martin 1999).
Our analysis of large mammals preserved
at Venta Micena shows that it is possible to re-
cover significant paleobiological information
from a taphonomically altered assemblage.

513BEHAVIOR OF AN EXTINCT HYENA
Such information is obtainable from quanti-
tative study of the preservational bias intro-
duced by the behavior of the large, extinct hy-
ena Pachycrocuta brevirostris, the bone-collect-
ing agent at this site (Palmqvist et al. 1996; Ar-
ribas and Palmqvist 1998). Until now little has
been known about the relative importance of
hunting and scavenging for this extinct bone-
cracking carnivore, its role as a bone-accu-
mulating agent during the lower Pleistocene,
and the bias it introduced in the composition
of the assemblages of large mammals. Here
we evaluate the nature and consequences of
such bias for the composition of the Venta Mi-
cena assemblage, paying special attention to
several aspects not reported in detail before,
such as the transport by hyenas of carcasses
and bone remains to their maternity dens and
the differential breakage of limb bones from
various ungulate species.
The Venta Micena Site
Venta Micena (Orce, Granada, southeastern
Spain) is located in the eastern sector of the
Guadix-Baza intramontane basin. The basin
was endorheic (i.e., characterized by interior
drainage) until late Pleistocene times, thus fa-
cilitating an exceptional record of Plio-Qua-
ternary taphocenoses of large mammals pre-
served in swampy and lacustrine sediments
(Fig. 1A). This site is dated by biostratigraphy
to the early Pleistocene, with an estimated age
of 1.3
6
0.1 Ma (Arribas and Palmqvist 1999).
The 80–120-cm-thick Venta Micena stratum
(VM-2, Fig. 1A) is one of the various fossilif-
erous units in the Plio-Pleistocene sedimen-
tary sequence of Orce, whose surface can be
followed along
;
2.5 km and stands out to-
pographically in the ravines of the region.
This stratum has the following vertical struc-
ture from bottom to top (Arribas and Palm-
qvist 1998: Fig. 2):
1. A basal unit (first lacustrine stage) that is
one-third to one-half the total thickness,
formed by homogeneous micrite with some
carbonate nodules (5–20 cm thick) and
small mud banks. The sediment preserves
abundant shells of freshwater mollusks and
is sterile in vertebrate fossils, thus attesting
to a first generalized lacustrine stage in the
region, in which the micrite was precipitat-
ed in water of variable depth; the absence
of pyrite and carbonate facies rich in organ-
ic matter are evidence that the lake was not
eutrophic.
2. A 4–15-mm-thick calcrete paleosol (hard-
pan) developed on the surface of the mi-
crite sediments deposited during the pre-
vious lacustrine stage. The calcrete forms
an irregular surface, subparallel to the bed-
ding plane, following the preexisting limn-
ic microtopography, and is thicker at to-
pographic highs. This surface defines a
stratigraphic unconformity, indicating a
major drop of the Pleistocene lake level and
thus the emergence of an extensive plain
around the lake.
3. An upper unit of micrite (second lacustrine
stage) deposited in a subsequent rise of the
lake level, which continues up to the top of
the stratum, showing root marks, mud
cracks, and a high density of fossil bones of
large mammals resting on the paleosol.
The sedimentary environment of the fossil
assemblage was characterized by wide
emerged zones (
;
4 km width) around the
lake, with small shallow ponds (
,
1 m depth,
2–20 m diameter) (Arribas 1999). The bones
are embedded in a porous micrite matrix (98–
99% CaCO
3
) with mud cracks and root marks,
which precipitated during a period of partial
expansion of the ponds (i.e., restricted
swampy biotope of carbonate facies, with
plants colonizing the border of the ponds). It
is capped by a massive micritic limestone,
produced during a subsequent phase of water
level rise (i.e., second lacustrine stage) that
was rather slow, as indicated by the absence of
terrigenous, erosive structures and of any ev-
idence of sediment traction.
The Venta Micena quarry has an area of
;
300 m
2
(Fig. 1B,C). This surface was divided
in square meters and excavated systematically
from 1979 to 1995, providing a rich collection
composed of 5798 identifiable skeletal re-
mains from 225 individuals belonging to 19
taxa of large (
$
5 kg) mammals, 655 anatom-
ically identifiable bones of mammals that
could not be determined taxonomically (e.g.,
diaphyses and small cranial fragments), and

514 PAUL PALMQVIST AND ALFONSO ARRIBAS
F
IGURE
1. A, Geographic location of the paleontological site at Venta Micena (Orce, Granada, southeastern Spain)
in the intramontane basin of Guadix-Baza, and stratigraphic section of the lower Pleistocene deposits in the Venta
Micena (VM) sector. The location of two other paleontological and archaeological sites (BL
5
Barranco Leo´n, FN
5
Fuente Nueva) is also indicated. B, Bones outcropping at high density in one grid of the surface excavated at
Venta Micena. C, Density plot for the abundance of skeletal remains per square meter (z-axis) in the quarry.
;
10,000 unidentifiable bone shafts. Complete
elements and bone fragments range in size
from isolated premolars and third phalanges
of Vulpes to complete mandibles of Mammu-
thus. Fossil remains of micromammals, includ-
ing teeth and elements from the axial skeleton,
are also present in small numbers and were
not included in the taphonomic study; they
were probably deposited as fecal droppings of
small carnivores. Table 1 summarizes the raw
data on the abundances of large-mammal
taxa.
The longitudinal axes of major longbones
show no preferred orientation, which suggests
that the bones were not aligned by current.
The stratigraphy also indicates the absence of
channeled currents in the area in which fossils
were accumulated. The bones lie horizontally
on the paleosurface, and there is no evidence
of trampling, as no skeletal element was found
in vertical or diagonal position (Arribas 1999).
Surfaces of the bones are well preserved; no
signs of abrasion or polish are present and
only four elements show evidence of slight
dissolution. The concentration of fossils on the
excavated surface is very high, with a mean
density of elements of
;
60 bones/m
2
(Fig.
1C), and
.
90% of skeletal elements are in con-
tact with other bones. Two areas had 80–90
bones/m
2
of up to 50 cm in length, such as tib-

515BEHAVIOR OF AN EXTINCT HYENA
T
ABLE
1. Abundance of taxa of large mammals (
$
5 kg) identified in the Venta Micena assemblage (data from Ar-
ribas and Palmqvist 1998). MNI
5
minimum number of individuals (juveniles/adults), based on counts of decid-
uous and permanent teeth. NISP
5
number of identifiable specimens (teeth/bones). C
5
carnivore (Hy
5
hyper-
carnivore,
.
70% vertebrate flesh in diet; Co
5
carnivore/omnivore,
,
70% flesh in diet; Bc
5
bone cracker). H
5
herbivore (Br
5
browser,
,
10% grass in diet; Mf
5
mixed-feeder, 10–90% grass; Gr
5
grazer,
.
90% grass). O
5
omnivore.
Species
Trophic
habits
MNI
(juv./adults)
%
Juv.
NISP
total
(teeth/bones)
%
Total
NISP
sample
(teeth/bones)
%
Sam-
ples
Mass of
adults
(kg)
Mammuthus meridionalis
Hippopotamus antiquus
Bovini cf. Dmanisibos
Soergelia minor
Praeovibos sp.
Hemitragus alba
Caprini gen. et sp. indet.
Eucladoceros giulii
Dama sp.
Stephanorhinus etruscus
Equus altidens
Vulpes praeglacialis
Canis falconeri
Canis etruscus
Lynx aff. issiodorensis
Megantereon whitei
Homotherium latidens
Pachycrocuta brevirostris
Ursus etruscus
H (Mf)
H (Gr)
H (Gr)
H (Mf)
H (Gr)
H (Gr)
H (Mf)
H (Br)
H (Mf)
H (Br)
H (Gr)
C(Co)
C (Hy)
C(Co)
C (Hy)
C (Hy)
C (Hy)
C (Bc)
O
5 (4/1)
5 (3/2)
27 (16/11)
13 (3/10)
1 (0/1)
14 (2/12)
1 (0/1)
36 (15/21)
20 (3/17)
6 (2/4)
70 (32/38)
1 (0/1)
3 (0/3)
4 (0/4)
1 (0/1)
3 (0/3)
2 (0/2)
10 (4/6)
3 (1/2)
80.0
60.0
59.3
23.1
0.0
14.3
0.0
41.7
15.0
33.3
45.7
0.0
0.0
0.0
0.0
0.0
0.0
40.0
33.3
48 (16/32)
58 (19/39)
775 (382/393)
334 (215/129)
6 (3/3)
305 (209/96)
1 (0/1)
962 (557/405)
417 (231/186)
90 (55/35)
2562 (1183/1379)
24 (19/5)
65 (40/25)
33 (20/13)
6 (2/4)
16 (7/9)
7 (6/1)
62 (34/28)
27 (15/12)
0.8
1.0
13.4
5.8
0.1
5.3
0.0
16.6
7.2
1.6
44.2
0.4
1.1
0.6
0.1
0.3
0.1
1.1
0.5
21 (4/17)
14 (0/14)
97 (48/49)
74 (51/23)
3 (2/1)
30 (12/18)
1 (0/1)
121 (70/51)
55 (30/25)
27 (16/11)
457 (210/247)
12 (10/2)
33 (21/12)
16 (10/6)
3 (1/2)
8 (3/5)
3 (2/1)
31 (17/14)
14 (8/6)
2.1
1.4
9.5
7.3
0.3
2.9
0.1
11.9
5.4
2.6
44.8
1.2
3.2
1.6
0.3
0.8
0.3
3.0
1.4
6000
3000
450
225
320
75
10
380
95
1500
350
5
30
10
10
100
250
100
375
iae of Equus and metapodials of Eucladoceros
(Arribas and Palmqvist 1998: Figs. 7, 8). Ar-
ticulated bones are relatively scarce, repre-
senting less than 20% of all elements in the
sample; however, there is a low degree of hor-
izontal dispersion, with abundant groups of
disarticulated but associated elements, such as
skulls with mandibles and metapodials with
phalanges. The most frequently preserved ar-
ticulations are those formed by tibiae-tarsal-
metatarsal-phalanges, humerus-radius/ulna,
radius-carpal-metacarpal-phalanges, and ver-
tebrae.
The age estimated for individuals pre-
served in the assemblage included two major
groups: immature or juvenile individuals
with deciduous teeth, and adults with fully
erupted permanent dentition (Table 1). Body
mass estimates for adults were obtained from
Palmqvist et al. (1996), who used ‘‘taxon-free’’
regression equations of mass on craniodental/
postcranial measurements from modern spe-
cies (Damuth and MacFadden 1990).
Inspection of data in Table 1 shows that her-
bivore taxa dominate the assemblage in both
number of identifiable specimens (NISP) and
estimates of minimum number of individuals
(MNI). More common herbivorous species
(those with higher NISP and MNI values),
such as the horse Equus altidens and the large
deer Eucladoceros giulii, have high percentages
of juveniles,
.
40% in both cases (32/70 and
15/36, respectively). Among carnivores, only
adult individuals are recovered, with the ex-
ception of the hyaenid and the ursid. Forty
percent (4/10) of the individuals of P. breviros-
tris are juveniles, represented by deciduous
teeth contained within the maxilla or mandi-
ble, indicating that these cranial elements
were produced not by tooth replacement but
as a consequence of the death of immature in-
dividuals.
An Overview of the Taphonomy of Venta
Micena
Previous research on the taphonomy of Ven-
ta Micena (Palmqvist et al. 1996; Arribas and
Palmqvist 1998; Arribas 1999; Palmqvist and
Arribas 2001) focused on the analysis of size/
abundance patterns in ungulate species using
the model of Damuth (1982), and on the abun-
dance of preserved epiphyses and complete

516 PAUL PALMQVIST AND ALFONSO ARRIBAS
T
ABLE
2. Abundance of skeletal elements of large mammals grouped according to their potential for water dis-
persal (Voorhies’ groups) in the subset used for taphonomic analysis (n
5
1231), and in the three better-represented
taxa in the assemblage, the horse (Equus altidens;n
5
488), the buffalo (Bovini cf. Damanisibos;n
5
95), and the
megacerine deer (Eucladoceros giulii;n
5
138).
Voorhies’
groups Skeletal element n
total
%n
horse
%n
buffalo
%n
deer
%
Group I Isolated teeth
Fragments of deer antlers
Vertebrae
Ribs
Scapulae
Ulnae
Calcanei
Astragali
Phalanges
168
19
178
36
31
8
36
51
72
13.7
1.5
14.5
2.9
2.5
0.6
2.9
4.1
5.9
47
—
51
16
12
3
14
23
38
9.6
—
10.5
3.3
2.5
0.6
2.9
4.7
7.8
3
—
21
0
2
0
8
10
7
3.2
—
22.1
0.0
2.1
0.0
8.4
10.5
7.4
13
14
13
0
11
0
8
8
5
9.4
10.1
9.4
0.0
8.0
0.0
5.8
5.8
3.6
Group II Humeri
Radii
Pelvis fragments
Femora
Tibiae
Metapodials
78
34
23
32
87
258
6.3
2.8
1.9
2.6
7.1
21.0
24
7
12
25
47
145
4.9
1.4
2.5
5.1
9.6
29.7
12
2
2
0
7
11
12.6
2.1
2.1
0.0
7.4
11.6
9
7
2
0
12
25
6.5
5.1
1.5
0.0
8.7
18.1
Group III Cranial elements 120 9.7 24 4.9 10 10.5 11 8.0
limb bones of ruminants. The resultsobtained
indicated that most losses of paleobiological
information during the taphonomic history of
the assemblage were a consequence of the se-
lective destruction of skeletal remains during
the period when the bones were exposed on
the surface before burial, and that the effect of
this preservational bias was more pronounced
in those species of smaller body size (Arribas
and Palmqvist 1998; Arribas 1999).
The role of hyenas in the bone accumulation
process at Venta Micena was determined by
comparing the frequencies of different types
of postcranial bones in this assemblage (e.g.,
vertebrae, ribs, limb and girdle bones, phalan-
ges) with the corresponding figures for sev-
eral recent and archaeological deposits accu-
mulated by carnivores, rodents and hominids
(Arribas and Palmqvist 1998: Table 2). Results
indicated that P. brevirostris was the main
agent responsible for the bone accumulation
at Venta Micena, because the composition of
the fossil assemblage is strikingly similar to
bone accumulations produced by modern hy-
enas in which major limb bones predominate
whereas ribs and vertebrae are comparatively
scarce. Specifically, the relative abundances of
limb bones and vertebrae/ribs in Venta Mi-
cena (79.3% and 14.3%, respectively) are sim-
ilar to the frequencies of these elements in as-
semblages collected by spotted hyenas (Cro-
cuta crocuta), 69.4–76.2% and 12.2–24.2%, re-
spectively (Behrensmeyer and Dechant Boaz
1980; Brain 1981; Skinner and Van Aarde 1981;
Bunn 1982; Skinner et al. 1986), but different
from those accumulated by striped hyenas
(Hyaena hyaena) and brown hyenas (Parahyaena
brunnea), in which higher frequencies of limb
bones (90.8–93.2%) and lower frequencies of
vertebrae/ribs (4.2–7%) are found (Maguire et
al. 1980; Skinner et al. 1980, 1995; Skinner and
Van Aarde 1981, 1991; Kerbis Petherhans and
Kolska-Horwitz 1992). However, Venta Mi-
cena resembles assemblages from dens of
brown and striped hyenas in its high density
of bones (Leakey et al. 1999). Spotted hyenas
are efficient hunters, owing to their greater
body size and strong social behavior, and pro-
duce a highly enriched milk; thus, they do not
regularly carry carrion to their maternity dens
to feed their cubs (Kruuk 1972; Ewer 1973;
Mills 1989). Nonetheless, there are some re-
ported cases of spotted hyenas accumulating
huge amounts of skeletal remains (e.g., see
Hill 1981 for a dense accumulation of bones
within a breeding den in Amboseli National
Park, Kenya), and this was certainly the case
with the cave hyena (Crocuta crocuta spelaea)in
the late Pleistocene of Europe (Fosse 1996).
The differences in composition between the

517BEHAVIOR OF AN EXTINCT HYENA
assemblage accumulated by Pachycrocuta at
Venta Micena and those collected by other
species suggest that the life habits of the short-
faced hyenas were not identical to those of any
living hyaenid.
The quantitative study of differential pres-
ervation of major limb bones of ruminants in
the assemblage (Palmqvist et al. 1996; Arribas
and Palmqvist 1998) showed that bone-gnaw-
ing and -crushing behavior by hyenas of those
ruminant carcasses transported to the mater-
nity den resulted in the preferential consump-
tion of longbone epiphyses with high fat con-
tents, and thus the differential breakage of
major limb bones according to their marrow
yields. Such a selective pattern rules out the
possibility that other processes (e.g., ungulate
trampling) were responsible for bone fractur-
ing.
The recovery of several deciduous teeth of P.
brevirostris belonging to four individuals also
suggests that the assemblage originated
through accumulation of skeletal parts near
shallow breeding dens excavated by the hye-
nas in the plains surrounding the Pleistocene
lake (Arribas and Palmqvist 1998). The abun-
dance of unworn deciduous hyena teeth rules
out the possibility that bones were accumu-
lated in open feeding places located at hunt-
ing sites distant from maternity dens, if we
presume that, like modern hyenas, the cubs
did not accompany adults on their search for
ungulate carcasses.
A comparison of the Venta Micena assem-
blage with those from other Plio-Pleistocene
lacustrine sites from the Guadix-Baza Basin
(Arribas 1999) revealed that Venta Micena
shows the highest diversity of large mam-
mals, mainly because of the high diversity of
carnivores, from opportunistic scavengers to
large predators. The taxonomic richness of
large mammals at Venta Micena (19 taxa) is
similar to that recorded from a modern spot-
ted hyena den developed on a calcrete paleo-
sol in Amboseli (18 taxa) (Hill 1981). Similarly,
Leakey et al. (1999) identified 15 species of
mammals from skeletal remains collected by
striped hyenas in Lothagam, Kenya, and Skin-
ner et al. (1991, 1998) identified 11 mammali-
an taxa at two maternity den sites of brown
hyenas from the west coast of Namibia. These
counts of taxonomic richness from hyena ac-
cumulations accurately reflect the composi-
tion of the available vertebrate prey commu-
nity in these areas.
Biostratinomic Analysis of the Assemblage
We have used here several biostratinomic
variables to further characterize the bone as-
semblage from Venta Micena, following in
part the procedure described by Behrensmey-
er (1991) for studying vertebrate assemblages.
Descriptive analysis was based on a subset of
1339 specimens, which includes 1020 identi-
fiable skeletal remains (distributed among
taxa in Table 1) as well as 211 bones and 108
bone shafts that could not be determined tax-
onomically. This sample comprises the well-
restored specimens housed at the Museum of
Paleontology of Orce (Palmqvist et al. 1996).
The high value obtained for the Pearson prod-
uct-moment correlation between the relative
frequencies of taxa in the whole assemblage
and in the subset (Table 1; r
5
0.985; p
,
0.0001) indicates that the latter represents a
random sample of the entire assemblage.
Table 2 shows the abundances of different
skeletal elements in the subset of large mam-
mals and in the three most abundant taxa, the
horse (E. altidens), the buffalo (Bovini cf.
Dmanisibos), and the megacerine deer (E. giu-
lii).
The ratio of isolated teeth to vertebrae (0.94:
1) is close to the value expected in the absence
of hydrodynamic sorting (1:1), indicating that
the skeletal remains were not transported by
fluvial processes prior to deposition (Behrens-
meyer and Dechant Boaz 1980; Shipman
1981). The frequencies of bones grouped ac-
cording to their potential for dispersal by wa-
ter (i.e., Voorhies’ groups) are as follows:
48.6% for Group I (isolated teeth, deer antlers,
vertebrae, ribs, scapulae, ulnae, calcanei, as-
tragali, phalanges), 41.7% for Group II (fem-
ora, tibiae, humeri, metapodials, pelvis, radii),
and 9.7% for Group III (cranial elements);
such a degree of skeletal completeness rules
out the possibility of hydraulic sorting (Voor-
hies 1969).
Limb elements clearly dominate (57.7%) the
sample, followed by vertebrae, cranial ele-
ments (cranial vaults, maxillae, and mandi-

518 PAUL PALMQVIST AND ALFONSO ARRIBAS
bles; Fig. 2G–I), and ribs. Scapulae are mostly
represented by proximal fragments. Diaphy-
ses and distal epiphyses predominate among
humeri (Fig. 2A). Femora are mainly pre-
served as fragments of diaphyses, and tibiae
as distal epiphyses (Fig. 2B). The pelvis is rep-
resented only by fragments that preserve the
acetabulum.
Analysis of weathering stages for the bones
in the subset indicates exposure to the ele-
ments for only a relatively short time: 89.3%
(784/878) of the skeletal elements show
weathering stage 0 (Behrensmeyer 1978) and
only 10.7% of the bones (of which two-thirds
are metapodials) show weathering stage 1,
with a few, shallow, small split-line cracks due
to insolation (Fig. 2C) and without flaking of
the outer surface (Arribas and Palmqvist 1998;
Arribas 1999). Although low degrees of phys-
ico-chemical weathering could reflect protec-
tion by vegetation in moist conditions until
burial, this was not the case here becausemost
bones show no evidence of root marks. On the
other hand, bones that were preserved com-
plete lack sedimentary infilling, even in areas
of the medullary cavity that are close to nu-
trient foramina, indicating that they were bur-
ied in fresh condition, with the periosteum in-
tact (Arribas and Palmqvist 1998). Thus, these
results suggest a very short period of subaer-
ial exposure before burial (less than one year
in most cases).
The detailed study of horse remains has
shown that biostratinomic fractures are very
abundant (Fig. 2), as only 29.1% of major limb
bones are complete; metapodials are the most
abundant bones preserved as complete ele-
ments, 82.2%. Among the fractured elements,
type II spiral fractures (Shipman 1981; Lyman
1994) predominate (100% of fragmented hu-
meri, femora, and radii; 74.4% of tibiae). Other
types are longitudinal fractures in tibiae, un-
differentiated fractures (all ribs and vertebrae,
with the exception of some vertebrae that lack
only apophyses), and maxillary bones with
both cheek-tooth rows (33.3% of cranial ele-
ments). Gnaw-marks are very frequent on the
horse remains: all cranial fragments,scapulae,
humeri, radii, pelves, femora, and tibiae show
striations and gnaw-marks produced by car-
nivores; the preserved epiphyses have fur-
rows and punctures; and the diaphyses, as
well as the skull bones, show scoring and pit-
ting. These marks are also observed in all oth-
er taxa identified at Venta Micena. Coprolites
(3–6 cm thick) are relatively common.
Evaluation of Taphonomic Bias in the
Assemblage
The taphonomic analysis of the large-mam-
mal assemblage preserved at Venta Micena
has revealed the existence of the following
preservational biases, which took place con-
secutively during the biostratinomic stage and
affected its original composition (Palmqvist et
al. 1996; Arribas and Palmqvist 1998; Palm-
qvist and Arribas 2001): (1) scavenging by hy-
enas of ungulate prey hunted by hypercarni-
vores; (2) selective transport of carcasses and
bone remains to their maternity dens; and (3)
differential breakage of major limb bones
within the dens. In the following sections we
evaluate the importance of these biases and
their consequences for the composition of the
assemblage, with a special focus on the trans-
port of carcasses and the breakage of bones
from horse (E. altidens) and buffalo (Bovini cf.
Dmanisibos), which are two of the better-rep-
resented ungulate taxa in the assemblage.
Bias I: Scavenging of Ungulate Prey Selectively
Hunted by other Predators. Previous research
on the composition of the bone assemblage
(Palmqvist et al. 1996; Arribas and Palmqvist
1998) has shown that the overwhelming ma-
jority of skeletal remains preserved in Venta
Micena were scavenged by hyenas from car-
casses of ungulates preyed upon by hypercar-
nivores (i.e., species in which vertebrate flesh
represented
.
70% of diet). The selection by
hypercarnivores of specific ungulates was ba-
sically a function of differences in the body
mass of the prey—between juveniles and
adults as well as between the sexes.
The evidence of prey selection at Venta Mi-
cena is the following: (1) U-shaped (i.e., bi-
modal) attritional mortality profiles deduced
from crown height measurements for those
herbivore species that are well represented in
the assemblage, indicating a strong selection
by predators of very young and old individ-
uals (Palmqvist et al. 1996: Fig. 8); (2) the in-
terspecific analysis of the relative abundance

519BEHAVIOR OF AN EXTINCT HYENA
of juveniles with deciduous teeth, and adults
with permanent dentition, which shows that
juveniles represent 16.7% (8/48) of all indi-
viduals in ungulate species
,
300 kg, yet the
proportion of juveniles increases to 48.0%
(72/150) in those species
.
300 kg (these per-
centages are significantly different according
to a one-tailed t-test: t
5
4.63; p
,
0.0001); (3)
the presence of many metapodials with severe
osteopathologies (Palmqvist et al. 1996: Fig.
11A,B), such as arthrosis, which limited the
locomotor capabilities of the ungulates and
therefore their ability to escape from preda-
tors; and (4) the sex ratio deduced from the
size distribution of metapodials in large prey
species, such as horse and buffalo, which is bi-
ased in favor of females in both cases (ap-
proximately 1 male : 3–4 females [Palmqvistet
al. 1996: Fig. 11C]). This sex ratio suggests that
females were more vulnerable to predation
because of their smaller body size.
Given that most carnivores usually hunt
herbivores within a narrow range of body
mass around the same size as that of the pred-
ator (Kruuk 1972; Schaller 1972 and references
therein), the wide range of body mass repre-
sented by the ungulate taxa preserved in the
assemblage (10–6000 kg) suggests that in most
cases these animals were preyed upon by dif-
ferent carnivore species (Palmqvist et al.
1996).
Hypercarnivores are represented in the as-
semblage by four species—two saber-tooths
(Homotherium latidens and Megantereon whitei),
a felid (Lynx aff. issiodorensis), and a wild dog
(Canis falconeri).
M. whitei (Fig. 3) had an intermediate body
size (
;
100 kg), similar to that of a jaguar,
Panthera onca (Martı´nez-Navarro and Palm-
qvist 1995, 1996). Judging from the low value
estimated for the brachial index (i.e., radius
length : humerus length,
;
80%) it was an am-
bush predator, hunting in closed, forested
habitats and presumably preying on browsing
and mixed-feeding ungulates of intermediate
to large body mass (Lewis 1997). This recon-
struction of its predatory behavior is corrob-
orated by the fact that the metapodials were
comparatively shorter than those of large
modern felids and other saber-tooths. This
dirk-toothed machairodont had a strong body
with a short back, powerfully developed fore-
limbs with large claws, and extremely long,
sharp, laterally compressed (and inherently
fragile) upper canine teeth. The brain was
small in relation toHomotherium‘s, showing ol-
factory lobes that were well developed. All
these features give the strong impression of an
animal built for capturing prey using a short
rush and then using its considerable strength
to bring down and hold prey with the fore-
limbs, before killing with a slashing bite to the
throat (Turner and Anto´n 1998; Arribas and
Palmqvist 1999). A similar hunting behavior
was inferred by Anyonge (1996) for the closely
related genus Smilodon, a possible descendant
of Megantereon in the New World.
Homotherium (Fig. 3) was a scimitar-toothed
machairodont with relatively long and slender
limbs, which provided considerable leverage
(Turner and Anto´n 1998; Martin et al. 2000).
According to regressions of body mass
against postcranial measurements in modern
carnivores (Anyonge 1993), it was similar in
size to a modern male lion, Panthera leo (150–
220 kg). The regression of body mass on lower
carnassial length in modern felids (Van Val-
kenburgh 1990), however, provides a larger
size estimate for the Venta Micena H. latidens
(Palmqvist et al. 1996), 250 kg. The upper ca-
nines were comparatively shorter and broader
than those of Megantereon, bearing coarse ser-
rations in the enamel of the posterior margin.
The forelimb was more elongated than the
hindlimb, indicating that the animal probably
had a sloping back. The claws of Homotherium
appear to have been small, with the exception
of a well-developed dewclaw in the first digit
of the forefoot. The elongated forelimb and
smaller claws suggest increased cursoriality
and less prey-grappling capability than other
saber-tooths (Rawn-Schatzinger 1992; Turner
and Anto´ n 1998; Arribas and Palmqvist 1999).
Both the comparatively high brachial index
(
$
100% [Lewis 1997]) and the results ob-
tained by Anyonge (1996) in a multivariate
analysis of the postcranial skeleton of extant
and extinct felids, indicate that Homotherium
was a pursuit predator, which presumably
hunted very large grazing and mixed-feeding
ungulates in open habitats. Homotherium had a
large brain relative to other saber-tooths, with

520 PAUL PALMQVIST AND ALFONSO ARRIBAS
F
IGURE
2. Selected examples of equid bones from Venta Micena, with evidence of modification by hyenas: A, B,
Humeri and tibiae, respectively, showing gnawing of epiphyses, spiral and longitudinal fractures. C, Third meta-
tarsals, complete and fractured, showing longitudinal and spiral fractures made by hyaenid crushing, and orthog-

521BEHAVIOR OF AN EXTINCT HYENA
F
IGURE
3. Skulls and reconstructions of the life appearance of the threelargest carnivore species preserved atVenta
Micena, the dirk-tooth Megantereon whitei, the scimitar-tooth Homotherium latidens, and the giant hyena Pachycrocuta
brevirostris. All drawn to scale, with a typical height at shoulder of 110 cm for Homotherium. Specific coat patterns
are unknown but typical of those seen across the range of living felids and hyaenids. Drawings by Mauricio Anto´n.
←
onal diagenetic fractures in the diaphyses due to sediment compaction. D, Astragali. E, Calcanei; one calcaneum
shows marks made by insect larvae. F, Third phalanges; one phalanx is partially gnawed by hyenas. G, Maxillae
gnawed by hyenas, indicating an extreme destruction of the splancnocranium. H, I, Mandibles gnawed and frag-
mented by hyenas. Typical sequences of bone modification by hyenas for postcranial elements of Equus (Arribas
1999; Arribas and Palmqvist 1998) are also indicated.

522 PAUL PALMQVIST AND ALFONSO ARRIBAS
an enlargement of the optic center, a condition
similar to that of the cheetah, Acinonyx jubatus
(Rawn-Schatzinger 1992). Turner and Anto´n
(1998) suggest that such a cursorial lifestyle
and hunting strategy would imply some de-
gree of group activity to bring down and re-
strain prey. In addition, given that a pursuit
strategy for hunting can be deployed only in
relatively open terrain, group behavior may be
needed to repel the inevitable attention of
scavengers. The likelihood of group activity is
suggested by the similarly proportioned
American species, H. serum, which is known
in some numbers (NISP
.
250, MNI
5
33)
from the late Pleistocene site of Friesenhahn
cave, Texas. At this site, H. serum is associated
with numerous remains (NISP
.
900 [Rawn-
Schatzinger 1992: Table 38]; MNI
5
34 [Ma-
rean and Ehrhardt 1995: Fig. 1]) of mam-
moths—one adult and the remainder juve-
niles—and it has been suggested that success-
ful predation of mammoths most likely would
require group hunting.
C. falconeri was a hypercarnivorous canid of
;
30 kg, according to the results of multivar-
iate analysis and multiple regression of body
mass on craniodental measurements in mod-
ern canids (Palmqvist et al. 1999). The second
metacarpal has a very reduced articular facet
with the first metacarpal, which indicates that
the latter bone was vestigial if not absent, a
condition similar to that of African painted
dogs (Lycaon pictus); this suggests increased
cursoriality for C. falconeri. This predator
probably hunted small to medium-sized graz-
ing ungulates (50–300 kg) in open to inter-
mediate forested country.
Pachycrocuta brevirostris (Fig. 3) was a bone-
cracking carnivore with a body 10–20% larger
than the modern spotted hyena and was well
adapted for dismembering carcasses and con-
suming bone (Palmqvist et al. 1996; Turner
and Anto´ n 1996; Arribas and Palmqvist 1998;
Saunders and Dawson 1998). Apart from its
size, this short-faced hyena differed from oth-
er species in the relative shortening of its dis-
tal limb segments (Turner and Anto´n 1996):
the brachial index is close to 88%, whereas in
modern hyaenids the values range between
99% and 106%; the crural index (i.e., tibia
length : femur length) is 74%, whereas the cor-
responding figures for modern species range
between 80% and 89%. These differences sug-
gest a less cursorial lifestyle for P. brevirostris.
It is also possible that the shortening of the
distal limb segments could provide greater
power and more stability to dismember and
carry large pieces of carcasses, which perhaps
could be obtained from aggressive scavenging
(i.e., kleptoparasitism).
The proportion of juveniles in a population
of a given species depends on two factors
(Palmqvist et al. 1996): the reproduction rate
(i.e., the annual birthrate) and the duration of
infancy (i.e., the time spent as a juvenile in-
dividual). Rates of birth and death scale to the
2
0.3 power of adult body mass (M), whereas
generation time (measured by life expectancy
at birth, duration of infancy, or age at death)
is interspecifically related to body mass by a
power of 0.3 (Damuth 1982; Peters 1983; Cal-
der 1984). As a result, larger species have low-
er birth and mortality rates per unit of abso-
lute time but not per unit of biological time
(i.e., relative to maximum life span), because
rates of birth and death per generation are size
independent. A third factor, differences in
age-specific mortality rate, could be relevant
here, as high adult mortality would increase
the proportion of juveniles in the population
and vice versa. However, data on cohort anal-
ysis and survivorship curves for African her-
bivores ranging in adult body mass between
,
50 kg and
.
3500 kg (Western 1979, 1980)
show no differences among species in the age-
specific mortality rate (e.g., the life expectancy
at birth fluctuates around 30% of total life
span, with small variations not related to
body size). Moreover, several studies on the
timing of ontogeny in eutherian mammals
(summarized in Peters 1983) indicate that, re-
gardless of size, a given developmental phase
requires a constant proportion of the mam-
mal’s life; thus, the relative time spent as a ju-
venile individual does not scale with body
mass.
The ratio of juvenile to adult individuals in
a population would be the product of annual
birthrate (B
r
) and duration of infancy (D
i
):
20.3 0.3 0
% juveniles
;
BD
5
MM
5
M.
ri
This relationship implies that the proportion

523BEHAVIOR OF AN EXTINCT HYENA
T
ABLE
3. Differences between primary bone assemblages collected by predators, such as leopards, and non-pri-
mary, secondary assemblages accumulated by scavenger carnivores, such as hyenas (Maguire et al. 1980; Richardson
1980; Skinner et al. 1980, 1986, 1995; Skinner and Van Aarde 1981, 1991; Vrba 1980; Brain 1980, 1981; Hill 1981;
Shipman 1981; Klein and Cruz-Uribe 1984; Behrensmeyer 1991; Kerbis Petherhans and Kolska-Horwitz 1992;
Palmqvist et al. 1996; Arribas and Palmqvist 1998). Data for Venta Micena also shown (a
5
estimated from the
whole collection, b
5
estimated from the subset used for taphonomic analysis).
Characteristics of the
bone assemblage
Primary assemblage,
collected by predators
Secondary assemblage,
collected by scavengers
Venta Micena
assemblage
Proportion of vertebrae and
ribs in relation to girdle and
limb bones
High, 1:4 (range
5
1:
3–5)
Low, 1:9 (range
5
1:4.5–25) 16.9% (429/2544)
a
Abundance of articulated
bones, in anatomical connec-
tion
Articulated elements
are quite abundant
Articulated bones are scarce
(exceptions: metapodials
and phalanges, vertebrae)
20.0% (204/1020)
b
Abundance of major longbones
preserved complete
High and not related
to their marrow
content
Low, inversely related to
marrow yield; spiral and
longitudinal fractures are
abundant
27.6% (137/497)
b
Abundance of limb bone
epiphyses in relation to di-
aphyses
High (2:1), without
preferential destruc-
tion of skeletal parts
of low structural
density
Comparatively low (1.5–1:
1), with evidence of pref-
erential consumption of
low-density epiphyses
139.4% (693/497)
b
Carnivore/ungulate index, cal-
culated from MNI counts
High (25–50%) or very
high (
.
50%, in
death traps)
Low (5–15%), similar to that
found in modern commu-
nities
13.6% (27/198)
a
Relative abundance of juvenile
ungulates, with deciduous
teeth
High proportion
(
.
25%)
Low proportion (
,
25%) 40.4% (80/198)
a
Proportion of young/adult in-
dividuals for ungulate spe-
cies
Increases as a function
of species body
mass
Not related with the size of
species
Positively corre-
lated with spe-
cies mass
Range of body mass covered
by the species preserved in
the assemblage
Narrow, usually
around the same
size as that of the
predator
Wide, in general more than
two orders of magnitude
(from
,
10 kg to
.
1000
kg)
5–6000 kg
a
Richness of species (large
mammals)
Comparatively low
(only prey species)
High diversity (all scav-
enged species)
19
a
F
IGURE
4. Least-squares regression analysis of the pro-
portion of juvenile individuals (estimated from MNI
counts) on adult body mass (in kg) for ungulate species
(n
5
9) of the Venta Micena assemblage (data from Table
1). Separate analyses were conducted for two groups of
prey species, the first of which (
,
1000 kg of estimated
mass for the adult individuals) were presumably hunt-
ed by Megantereon whitei and Canis (Xenocyon)falconeri,
and the second one (
.
1000 kg) by the large saber-tooth
Homotherium latidens.
of juveniles in any ungulate population is ap-
proximately constant (30–40%) and indepen-
dent of species body size (Palmqvist et al.
1996).
As previously indicated, in the Venta Mi-
cena assemblage the juvenile/adult ratios of
ungulates (estimated from MNI counts based
on deciduous and permanent teeth) as a func-
tion of adult body mass suggests that mortal-
ity age profiles differed depending on the size
of the prey. This would be the consequence of
selection by predators, which increased the
proportion of young and more vulnerable in-
dividuals of those ungulate species of larger
size. This interpretation is in accordance with
available data on prey selection by Recent car-
nivores as a function of size and age of their
preferred prey (Palmqvist et al. 1996: Fig. 7;
Arribas and Palmqvist 1998: Table 3). Figure 4

524 PAUL PALMQVIST AND ALFONSO ARRIBAS
F
IGURE
5. Comparison between the relative abundanc-
es of ungulate size classes in the prey hunted and scav-
enged by modern spotted hyenas (Crocuta crocuta)inthe
Serengeti National Park (data from Kruuk 1972) and the
frequencies of such categories in the ungulate assem-
blage preserved at Venta Micena (data from Table 1,
MNI counts).
shows the increase in the value of the juve-
nile/adult ratio in relation to the mass esti-
mated for the ungulate species from Venta Mi-
cena.
Therefore, the positive slope for the rela-
tionship between the proportion of juveniles
and the mass estimated for the adults indi-
cates that the Venta Micena assemblage was
not formed through catastrophic mortality
events during droughts (in such case the
abundance of juveniles of different species
would be approximately constant and size-in-
dependent). We can conclude that the vast ma-
jority of skeletal elements accumulated by hy-
enas came from attritional mortality in un-
gulate populations, caused by selective choice
of carnivores.
Bias II: Selective Transport of Carcasses and
Skeletal Parts. According to field data collect-
ed by Kruuk (1972) in the Serengeti and Ngo-
rongoro National Parks (Tanzania), modern
spotted hyenas are efficient hunters that hunt
their prey in 58.3% of cases and scavenge un-
gulate carcasses in the remaining 41.7% of cas-
es. Of those ungulates scavenged, individuals
dead by illness or accident represent 19.4%,
whereas the rest are carcasses of prey hunted
and partially defleshed by lions and painted
dogs. The relative abundances of ungulate
prey of different body size classes hunted by
lions and painted dogs correlate well with the
frequencies of ungulate populations (Kruuk
1972; Schaller 1972).
The distribution of specimens among size
classes in the ungulate assemblage from Venta
Micena (Fig. 5; frequencies estimated from
MNI counts in Table 1) is different from the
frequencies of ungulates hunted by spotted
hyenas according to a
x
2
test for the cumula-
tive differences (
x
2
5
148.2; df
5
4; p
,
0.0001), but remarkably similar to those in
which spotted hyenas scavenge carcasses of
animals killed by lions and wild dogs (
x
2
5
17.8; p
,
0.01 for all size classes;
x
2
5
4.3; df
5
3; p
.
0.1 for ungulates weighing
.
50 kg).
The only significant difference between the
distribution of ungulate size classes in Venta
Micena and in the prey scavenged by spotted
hyenas is the proportion of small species (
,
50
kg), which are underrepresented in the fossil
assemblage (one individual of Caprini indet.,
1/198, Table 1) but represent 14.5% (80/551
[Kruuk 1972: Table 26]) of the carcasses scav-
enged by spotted hyenas (one-tailed t-test: t
5
9.68; p
,
0.0001). This indicates that short-
faced hyenas preferentially consumed small
ungulates in situ and selectively transported
carcasses and body parts of larger species to
their maternity dens.
These results suggest that the predatory be-
havior of Pachycrocuta differed from that of
Crocuta, because modern spotted hyenas both
hunt and scavenge ungulates, whereas the
short-faced hyenas seem to have relied more
heavily on prey hunted by other predators;
therefore, the behavior of Pachycrocuta was
probably more similar to that of modern
brown and striped hyenas, which are predom-
inantly scavengers (Mills 1989). This trophic
dependence was facilitated by the fact that un-
gulate carcasses left by machairodonts and
hypercarnivorous canids would retain vari-
able amounts of flesh and all nutrients within
the bones, given that the slicing dentition of
these carnivores made them incapable of bone

525BEHAVIOR OF AN EXTINCT HYENA
F
IGURE
6. Abundance of ungulate species in Venta Mi-
cena, according to minimum number of adult individ-
uals (MNI), calculated from craniodental elements (per-
manent teeth and antlers or horn bases) and from min-
imum number of elements (MNE) of postcranial bones
(independent estimates for forelimb and hindlimb
bones). Caprini indet., Praeovibos sp., and species
.
1000
kg were excluded from this analysis owing to their low
sample sizes. Species ordered by decreasing values in
the ratio MNI
(teeth)
: MNI
(bones)
.
cracking (Marean 1989; Arribas and Palm-
qvist 1999).
The bone assemblage of Venta Micena can
thus be considered as mixed, showing some
features typical of primary assemblages, col-
lected by predators, and others that are char-
acteristic of non-primary, secondary assem-
blages accumulated by scavenger carnivores
(Table 3).
The bias produced by the selectivetransport
of ungulate remains is particularly evidenced
by the differential representation of preserved
skeletal parts. The abundance of each taxon
can be estimated by MNI counts obtained
from teeth and cranial elements (i.e., antlers
and horn bases in the case of ruminants), as
well as from MNI counts based on minimum
number of elements (MNE) estimated from
postcranial remains (i.e., forelimb and hin-
dlimb bones, complete elements or those rep-
resented by isolated epiphyses). Figure 6
shows that for small ungulates, such as the
goat (Hemitragus alba; 75 kg of estimated mass
for adult individuals) or the fallowdeer (Dama
sp.; 95 kg), MNI
(teeth)
gives a higher estimate of
abundance than MNI
(bones)
(
x
2
-test:
x
2
5
5.33
and 5.88; p
,
0.05 in both cases; MNI
teeth
counts used as expected frequencies). For Soer-
gelia minor, a bovine of intermediate mass (225
kg), the two MNI counts are similar (
x
2
5
0.10;
p
.
0.5). Finally, ungulate taxa of larger size,
such as the horse (E. altidens; 350 kg) and the
buffalo (Bovini cf. Dmanisibos; 450 kg), are bet-
ter represented by postcranial elements (
x
2
5
30.42 and 20.45, respectively, p
,
0.0001 in
both cases).
These differences are in large part an indi-
cation of how the hyenas handled the carcass-
es they scavenged. In the case of species that
were preferentially transported as complete
carcasses, the original abundances, estimated
from MNI counts based on teeth and bones,
would be approximately the same as the abun-
dances in the accumulated assemblage. How-
ever, because hyenas selectively fracture major
longbones and destroy limb bone epiphyses to
get at the marrow and fat, MNI estimates for
the assemblage that are based on teeth should
be higher than those based on postcranial el-
ements. Therefore small ungulate species
(
,
100 kg), which are represented by an
MNI
(teeth)
: MNI
(bones)
ratio of approximately 2:
1 in the Venta Micena assemblage (H. alba and
Dama sp.), were probably transported in most
cases as complete carcasses. In the case of
larger species (
.
300 kg), selective transport of
marrow-rich body parts (i.e., the forelimb in
buffalo and the hindlimb in horse) is suggest-
ed by the reverse ratio (MNI
teeth
: MNI
bones
5
1:
2). Finally, for ungulate species of intermedi-
ate size (100–300 kg), such as S. minor, post-
cranial elements were transported by hyenas
with a somewhat higher frequency than heads
(after preferential consumption of major long-
bones, MNI counts calculated from teeth and
bones are similar, 1:1).
The only exception to this trend is the large
megacerine deer E. giulii. Although its body
mass is estimated at 380 kg for adult individ-
uals, MNI counts from teeth and bones are
quite similar (Fig. 6;
x
2
5
0.05; p
.
0.5). This
may be due to two reasons: (1) major limb
bones are relatively slender in this species and

526 PAUL PALMQVIST AND ALFONSO ARRIBAS
T
ABLE
4. Number of forelimbs and hindlimbs (calculated from MNE counts for each major limb bone) of Equus
altidens and Bovini cf. Dmanisibos from Venta Micena. Total marrow yields and flesh weights of forelegs and hind
legs estimated from values for modern Equus caballus (Outram and Rowley-Conwy 1998) and Bison bison (Brink
1997).
Equus altidens
Forelimbs Hindlimbs
Bovini cf. Dmanisibos
Forelimbs Hindlimbs
Number of legs (right/left)
Total marrow yields (g)
Flesh content (kg)
118 (59/59)
77.1
14.0
141 (72/69)
115.4
46.2
44 (18/26)
622.0
13.0
41 (24/17)
558.4
43.9
were presumably more easily fractured by hy-
enas; and (2) the antlers of the males were par-
ticularly large (
;
1.5 m in width), and the hy-
enas might have transported the heads to their
dens to exploit mineral phases and hemopoi-
etic tissues supplied by the antlers; interest-
ingly, fragments of deer antlers are well rep-
resented in the assemblage (Table 2).
The evidence that hyenas selectively trans-
ported certain parts from the carcasses of
large ungulate species suggests that each
short-faced hyena foraged alone in search of
scavengeable carcasses, as do modern brown
hyenas (Mills 1989). If they had foraged in
groups, as spotted hyenas often do (Kruuk
1972; Mills 1989), the members of the hyena
clan would have transported all the anatomi-
cal regions of each carcass scavenged to their
maternity den; large ungulate taxa would then
be represented in the assemblage by similar
numbers of postcranial bones and cranioden-
tal elements, rather than the skewed ratio we
observed.
Table 4 shows the number of forelimbs and
hindlimbs calculated from MNE counts for
each limb bone in two taxa well represented
in the assemblage, the equid E. altidens and the
buffalo Bovini cf. Dmanisibos. The correspond-
ing values for flesh and marrow contents, es-
timated from data for major longbones in two
modern, similarly sized herbivores—the
horse, Equus caballus (Outram and Rowley-
Conwy 1998) and the North American plain
bison, Bison bison (Brink 1997), are also pro-
vided. The ratio of forelimbs to hindlimbs is
0.837 in the Venta Micena horse, which is
clearly different from that of flesh yields pro-
vided by forelimbs and hindlimbs, 0.303, and
closer to the corresponding ratio estimated for
marrow contents, 0.668. In the case of the buf-
falo, the ratio of forelimbs to hindlimbs is
1.073, again a value different from that esti-
mated for flesh contents, 0.296, but very close
to the value obtained for marrow, 1.114. This
suggests that marrow content was the main
reason hyenas transported limb bones to their
maternity dens.
Bias III: Consumption of Epiphyses and the Re-
duction of Major Limb Bones. Typical bone-
consuming sequences for each postcranial el-
ement of Equus were described recently for
Venta Micena by Arribas and Palmqvist (1998)
and Arribas (1999). Three distinct types of
bone-consuming activities by hyenas were es-
tablished (Fig. 2), depending on the position
of the bone in the horse skeleton (which is re-
lated to the hyenas’ pattern of disarticulation),
as well as on the amount of within-bone nu-
trients (i.e., grease and marrow content) and
mineral density:
1. Humerus, radius, tibia, ulna, and calca-
neum: these are consumed following an in-
variant proximodistal pattern. The reduction
of these bones by hyenas starts with gnawing
the proximal epiphysis, then is followed by
fracturing the diaphysis, and is finished by
gnawing of the distal epiphysis, which usu-
ally shows abundant tooth marks.
2. Femur: this is the only element in which
the sequence of consumption follows a vari-
able direction (i.e., from the proximal epiph-
ysis to the distal epiphysis or vice versa) and
both epiphyses are lost.
3. Third metacarpal and metatarsal: these
bones are modified by crushing, with a vari-
able direction of activity, and they tend to be
more abundantly preserved as complete ele-
ments than other major limb bones, owing to
their higher mineral density and lower mar-
row yields.

527BEHAVIOR OF AN EXTINCT HYENA
F
IGURE
7. Least-squares regression analysis of the raw
abundance at Venta Micena of preserved major limb
bone epiphyses of horse (Equus altidens) (A) and buffalo
(Bovini cf. Dmanisibos) (B) on their mean marrow con-
tent, estimated from data for modern horse (Equus ca-
ballus) by Outram and Rowley-Conwy (1998) and bison
(Bison bison) by Brink (1997) (variables log-trans-
formed).
Therefore, these results indicate that the
skeletal elements preserved in the fossil as-
semblage are those remaining once all within-
bone nutrients were consumed by hyenas. To
evaluate quantitatively this taphonomic bias
on the preservational completeness of the
bone assemblage, we performed a compara-
tive analysis of the preservational state and
abundance of postcranial elements in E. alti-
dens and Bovini cf. Dmanisibos. We hypothe-
sized that there would be differences in the
abundance of postcranial elements because
there are differences in their within-bone nu-
trients (Emerson 1990; Brink 1997; Arribas
and Palmqvist 1998; Outram and Rowley-
Conwy 1998). Figure 7A shows the raw abun-
dance in which major limb bone epiphyses of
horse are preserved in the assemblage, as a
function of their mean marrow content (esti-
mated from values for E. caballus in Outram
and Rowley-Conwy 1998). A least-squares re-
gression revealed an inverse relationship be-
tween both variables, which is statistically sig-
nificant (r
52
0.60; p
,
0.05). This indicates
that hyenas selectively consumed the epiphy-
ses of bones having higher within-bone nutri-
ent content (e.g., proximal and distal femur,
proximal tibia), and acted less intensely on
those yielding lower marrow values (e.g., me-
tapodials, distal tibia).
The raw abundance of major longbone
epiphyses of buffalo in relation to their mar-
row weight is shown in Figure 7B (data for B.
bison in Brink 1997). The regression line also
shows a negative slope (r
52
0.85, p
,
0.0001), which indicates that the skeletal parts
better represented among the surviving
epiphyses are those with lower marrow
yields. However, the regression obtained for
this species is statistically more significant
than in the case of E. altidens, owing to the
higher marrow contents of bovine epiphyses
(six-fold on average). This suggests a great se-
lectivity in the bone-cracking behavior of hy-
enas, which was in turn translated into a dif-
ferential preservation of the skeletal elements
of both taxa in the bone assemblage.
Three major factors therefore appear to
have biased the composition of the Venta Mi-
cena assemblage: the scavenging by adult hy-
enas of ungulate prey hunted by hypercarni-
vores (bias I); the selective transport of whole
carcasses or certain anatomical parts, depend-
ing on the size of the ungulate species scav-
enged (bias II); and the preferential breakage
in the dens of bones with higher marrow con-
tent (bias III). Although these biasesdecreased
the amount of paleobiological information
preserved in the assemblage, the representa-
tion of the original mammalian community is
valid, thanks to the scavenging behavior of hy-
enas. A collection of bones from the prey of a
single predator may differentially sample par-
ticular species because of the predator’s prey
preferences, and such accumulation would
provide a poor estimate of standing diversity

528 PAUL PALMQVIST AND ALFONSO ARRIBAS
in the paleocommunity (Vrba 1980; Brain
1981; Shipman 1981; Behrensmeyer 1991).
This is not the case at Venta Micena, however,
where the skeletal remains of a wide spectrum
of ungulate prey hunted by several species of
hypercarnivores in different habitats were col-
lected by hyenas, thus providing a detailed
picture of the diversity of large mammals that
inhabited southern Spain during early Pleis-
tocene times. This is corroborated by several
studies of recent bone assemblages collected
by hyenas (Maguire et al. 1980; Skinner et al.
1980; Hill 1981; Skinner and Van Aarde 1981,
1991; Skinner et al. 1980, 1986, 1995, 1998; Ker-
bis-Petherhans and Kolska-Horwitz 1992;
Leakey et al. 1999), which indicate that the as-
semblages accurately reflect the composition
of the mammalian fauna in areas adjacent to
the maternity dens.
The assemblage from Venta Micena was
probably accumulated over a very short time
span; thus it is evidently not time-averaged
and retains a relatively high degree of envi-
ronmental resolution. The fact that most skel-
etal elements are unweathered suggests this,
as do inferences on hyaenid mortality pat-
terns. According to data on population den-
sities of modern spotted hyenas obtained by
Kruuk (1972), the mean numbers of adult and
juvenile spotted hyenas per den in Serengeti
are 55 and 12, respectively. With Kruuk’s es-
timate of mean annual mortality at 16.7%, ap-
proximately 11 individuals of the hyena clan
die each year, a figure remarkably similar to
the MNI calculated for P. brevirostris in the fos-
sil assemblage (10 individuals, 6 adults and 4
juveniles; Table 1). In fact, the juvenile short-
faced hyenas from Venta Micena can be clas-
sified within two age groups: two newborn in-
dividuals, with unworn milk teeth, and an-
other two that show deciduous dentition se-
verely worn and being replaced by permanent
teeth, indicating that they were at the end of
their first year of life. This suggests that dur-
ing a single season, probably summer, all four
of these individuals died.
Conclusions
Taphonomic processes have previously
been interpreted as solely destructive forces.
Information loss in terrestrial and fluvial bio-
tas results largely from such processes as
transport, disarticulation, sorting, and break-
age of skeletal parts by water, predators, scav-
engers, and trampling. However, such biostra-
tinomic processes imprint a taphonomic sig-
nature that often provides new data useful for
decoding paleobiological information (Wilson
1988; Ferna´ndez-Lo´pez 1991; De Renzi 1997).
The assemblage of large mammals fromVenta
Micena constitutes a good example of how an-
alytical studies can contribute toward re-cre-
ating a significant fraction of paleobiological
information lost during the taphonomic his-
tory.
As we have discussed here, it is even pos-
sible to infer information that was not origi-
nally preserved in the bone assemblage, such
as the behavior of the extinct hyena P. breviros-
tris, a species that differed from the modern
spotted hyena in being a strict scavenger of
ungulate carcasses selectively preyed upon by
hypercarnivores. This inference was based on
the quantitative study of the preservational
bias introduced by the scavenging behavior of
this giant hyena, which is shown to have been
highly specialized.
However, similar paleobiological inferences
may be obtained only in assemblages that
were collected during the biostratinomic stage
by biological agents, like hyenas, hominids, or
porcupines. Other types of terrestrial accu-
mulations, where the bones were accumulated
exclusively by physical agents (e.g., fluvial as-
semblages), would reveal useful sedimento-
logical and paleoenvironmental data (e.g.,
strength and direction of water currents), but
because the skeletal remains of such assem-
blages are frequently mixed, hydrodynami-
cally sorted, and even reworked, decoding the
taphonomic information locked in these as-
semblages would contribute little reliable pa-
leobiological information about the structure
and composition of the original paleocom-
munity from which they were derived. In this
context, the macrovertebrate assemblage from
Venta Micena constitutes an exceptional win-
dow for the detailed study of the mammalian
communities that inhabited Western Europe
during the early Pleistocene and the relation-
ships among the species that lived within
them.

529BEHAVIOR OF AN EXTINCT HYENA
Acknowledgments
Thanks to M. De Renzi, M. Foote, A. Miller,
R. A. Reyment, and L. Spencer for suggestions
that led to significant improvements in this
contribution. We gratefully acknowledge M.
Anto´ n for providing us the reconstructions of
carnivores used in Figure 3. R. Bobe, J. Saun-
ders, S. L. Wing, and an anonymous reviewer
provided insightful comments and helpful
criticism of the manuscript. And, last but not
least, N. Atkins improved the style of this ar-
ticle.
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