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q 2001 The Paleontological Society. All rights reserved.
0094-8373/01/2703-0007/$1.00
Paleobiology, 27(3), 2001, pp. 512530
Taphonomic decoding of the paleobiological information lockedin
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 haverevealed that
the decrease in paleobiological information runs parallel to the
gain of taphonomicinformation. 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
aspaleoethology. A good example is the study of the macrovertebrate
assemblage from the lowerPleistocene site at Venta Micena (Orce,
southeastern Spain). Taphonomic analysis showed that thegiant,
short-faced hyenas (Pachycrocuta brevirostris) selectively
transported ungulate carcasses andbody 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 contentand mineral density.
Important differences in bone-cracking intensity were related to
which speciesthe bones came from, which in turn biased the
composition of the bone assemblage. The analysisof mortality
patterns deduced for ungulate species from juvenile/adult
proportions revealed thatmost 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 assemblagehas unlocked paleobiological information that was
lost during its taphonomic history, and has evenprovided
paleobiological information that was not preserved in the original
bone assemblage, suchas the paleoethology of P. brevirostris, which
differed substantially from modern hyenas in being astrict
scavenger of the prey hunted by other carnivores.
Paul Palmqvist. Departamento de Geologa y Ecologa (Area de
Paleontologa), Facultad de Ciencias, Uni-versidad de Malaga. 29071
Malaga, Spain. E-mail: [email protected]
Alfonso Arribas. Museo Geominero, Instituto Geologico y Minero
(I.G.M.E.), c/ Ros Rosas, 23. 28003Madrid, Spain. E-mail:
[email protected]
Accepted: 13 March 2001
Introduction
Prior to the 1980s most vertebrate taphon-omists emphasized the
incompleteness of thefossil record, because the processes of
fossil-ization were envisioned as destructive, lead-ing to loss of
paleobiological information. Asa result, taphonomy came to be
associatedwith the documentation of information lossand bias in the
transition of organic remainsfrom the biosphere to the lithosphere.
How-ever, in their important paper Behrensmeyerand Kidwell (1985)
envisioned taphonomy asthe study of processes of preservation
andhow they affect information in the fossil rec-ord. They were
following the approach of nu-merous invertebrate paleontologists
who wereengaged since the mid-1980s in more posi-tive aspects of
comparative taphonomic re-search intended to establish that
postmortemprocesses (e.g., weathering, transport, and
sorting) leave signatures that are useful anddiagnostic of
various paleoenvironmental andsedimentary conditions (Kidwell and
Bosence1991; Kidwell and Flessa 1995).
Additionally,time-averagingviewed negatively by mostpaleontologists
in the pastis widely recog-nized as advantageous, because
short-termecological noise is dampened and longer-term signals from
a biological community arepreserved. In fact, bone assemblages from
sur-face environments are considered comparablein some respects to
repeated ecological sur-veys in assessing the long-term dynamics
ofthe 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 preservedat Venta Micena shows
that it is possible to re-cover significant paleobiological
informationfrom a taphonomically altered assemblage.
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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 hasbeen known about the relative importance
ofhunting 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 compositionof the
assemblages of large mammals. Herewe evaluate the nature and
consequences ofsuch bias for the composition of the Venta Mi-cena
assemblage, paying special attention toseveral aspects not reported
in detail before,such as the transport by hyenas of carcassesand
bone remains to their maternity dens andthe differential breakage
of limb bones fromvarious ungulate species.
The Venta Micena Site
Venta Micena (Orce, Granada, southeasternSpain) is located in
the eastern sector of theGuadix-Baza intramontane basin. The
basinwas endorheic (i.e., characterized by interiordrainage) 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
biostratigraphyto the early Pleistocene, with an estimated ageof
1.3 6 0.1 Ma (Arribas and Palmqvist 1999).The 80120-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 befollowed 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 isone-third to
one-half the total thickness,formed by homogeneous micrite with
somecarbonate nodules (520 cm thick) andsmall mud banks. The
sediment preservesabundant shells of freshwater mollusks andis
sterile in vertebrate fossils, thus attestingto a first generalized
lacustrine stage in the
region, in which the micrite was precipitat-ed in water of
variable depth; the absenceof pyrite and carbonate facies rich in
organ-ic matter are evidence that the lake was noteutrophic.
2. A 415-mm-thick calcrete paleosol (hard-pan) developed on the
surface of the mi-crite sediments deposited during the pre-vious
lacustrine stage. The calcrete formsan irregular surface,
subparallel to the bed-ding plane, following the preexisting
limn-ic microtopography, and is thicker at to-pographic highs. This
surface defines astratigraphic unconformity, indicating amajor drop
of the Pleistocene lake level andthus the emergence of an extensive
plainaround the lake.
3. An upper unit of micrite (second lacustrinestage) deposited
in a subsequent rise of thelake level, which continues up to the
top ofthe stratum, showing root marks, mudcracks, and a high
density of fossil bones oflarge mammals resting on the
paleosol.
The sedimentary environment of the fossilassemblage was
characterized by wideemerged zones (;4 km width) around thelake,
with small shallow ponds (,1 m depth,220 m diameter) (Arribas
1999). The bonesare embedded in a porous micrite matrix (9899%
CaCO3) with mud cracks and root marks,which precipitated during a
period of partialexpansion of the ponds (i.e., restrictedswampy
biotope of carbonate facies, withplants colonizing the border of
the ponds). Itis capped by a massive micritic limestone,produced
during a subsequent phase of waterlevel rise (i.e., second
lacustrine stage) thatwas rather slow, as indicated by the absence
ofterrigenous, erosive structures and of any ev-idence of sediment
traction.
The Venta Micena quarry has an area of;300 m2 (Fig. 1B,C). This
surface was dividedin square meters and excavated
systematicallyfrom 1979 to 1995, providing a rich
collectioncomposed of 5798 identifiable skeletal re-mains from 225
individuals belonging to 19taxa of large ($5 kg) mammals, 655
anatom-ically identifiable bones of mammals thatcould not be
determined taxonomically (e.g.,diaphyses and small cranial
fragments), and
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514 PAUL PALMQVIST AND ALFONSO ARRIBAS
FIGURE 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 VentaMicena (VM) sector. The location
of two other paleontological and archaeological sites (BL 5
Barranco Leon, FN5 Fuente Nueva) is also indicated. B, Bones
outcropping at high density in one grid of the surface excavated
atVenta Micena. C, Density plot for the abundance of skeletal
remains per square meter (z-axis) in the quarry.
;10,000 unidentifiable bone shafts. Completeelements and bone
fragments range in sizefrom isolated premolars and third
phalangesof 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 werenot
included in the taphonomic study; theywere probably deposited as
fecal droppings ofsmall carnivores. Table 1 summarizes the rawdata
on the abundances of large-mammaltaxa.
The longitudinal axes of major longbonesshow no preferred
orientation, which suggeststhat the bones were not aligned by
current.
The stratigraphy also indicates the absence ofchanneled currents
in the area in which fossilswere accumulated. The bones lie
horizontallyon the paleosurface, and there is no evidenceof
trampling, as no skeletal element was foundin vertical or diagonal
position (Arribas 1999).Surfaces of the bones are well preserved;
nosigns of abrasion or polish are present andonly four elements
show evidence of slightdissolution. The concentration of fossils on
theexcavated surface is very high, with a meandensity of elements
of ;60 bones/m2 (Fig.1C), and .90% of skeletal elements are in
con-tact with other bones. Two areas had 8090bones/m2 of up to 50
cm in length, such as tib-
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515BEHAVIOR OF AN EXTINCT HYENA
TABLE 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
5herbivore (Br 5 browser, ,10% grass in diet; Mf 5 mixed-feeder,
1090% grass; Gr 5 grazer, .90% grass). O 5omnivore.
SpeciesTrophichabits
MNI(juv./adults)
%Juv.
NISPtotal(teeth/bones)
%Total
NISPsample(teeth/bones)
%Sam-ples
Mass ofadults(kg)
Mammuthus meridionalisHippopotamus antiquusBovini cf.
DmanisibosSoergelia minorPraeovibos sp.Hemitragus albaCaprini gen.
et sp. indet.Eucladoceros giuliiDama sp.Stephanorhinus
etruscusEquus altidensVulpes praeglacialisCanis falconeriCanis
etruscusLynx aff. issiodorensisMegantereon whiteiHomotherium
latidensPachycrocuta brevirostrisUrsus 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)
80.060.059.323.1
0.014.3
0.041.715.033.345.7
0.00.00.00.00.00.0
40.033.3
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)
0.81.0
13.45.80.15.30.0
16.67.21.6
44.20.41.10.60.10.30.11.10.5
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)
2.11.49.57.30.32.90.1
11.95.42.6
44.81.23.21.60.30.80.33.01.4
60003000
450225320
7510
38095
1500350
5301010
100250100375
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 thesample;
however, there is a low degree of hor-izontal dispersion, with
abundant groups ofdisarticulated but associated elements, such
asskulls with mandibles and metapodials withphalanges. 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 majorgroups: immature or juvenile individualswith
deciduous teeth, and adults with fullyerupted permanent dentition
(Table 1). Bodymass estimates for adults were obtained
fromPalmqvist et al. (1996), who used taxon-freeregression
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 bothnumber 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 largedeer Eucladoceros giulii,
have high percentagesof juveniles, .40% in both cases (32/70
and15/36, respectively). Among carnivores, onlyadult individuals
are recovered, with the ex-ception of the hyaenid and the ursid.
Fortypercent (4/10) of the individuals of P. breviros-tris are
juveniles, represented by deciduousteeth contained within the
maxilla or mandi-ble, indicating that these cranial elementswere
produced not by tooth replacement butas a consequence of the death
of immature in-dividuals.
An Overview of the Taphonomy of VentaMicena
Previous research on the taphonomy of Ven-ta Micena (Palmqvist
et al. 1996; Arribas andPalmqvist 1998; Arribas 1999; Palmqvist
andArribas 2001) focused on the analysis of size/abundance patterns
in ungulate species usingthe model of Damuth (1982), and on the
abun-dance of preserved epiphyses and complete
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516 PAUL PALMQVIST AND ALFONSO ARRIBAS
TABLE 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-representedtaxa in the assemblage, the horse (Equus
altidens; n 5 488), the buffalo (Bovini cf. Damanisibos; n 5 95),
and themegacerine deer (Eucladoceros giulii; n 5 138).
Voorhiesgroups Skeletal element ntotal % nhorse % nbuffalo %
ndeer %
Group I Isolated teethFragments of deer
antlersVertebraeRibsScapulaeUlnaeCalcaneiAstragaliPhalanges
16819
1783631
8365172
13.71.5
14.52.92.50.62.94.15.9
47511612
3142338
9.6
10.53.32.50.62.94.77.8
321
0208
107
3.2
22.10.02.10.08.4
10.57.4
131413
011
0885
9.410.1
9.40.08.00.05.85.83.6
Group II HumeriRadiiPelvis fragmentsFemoraTibiaeMetapodials
7834233287
258
6.32.81.92.67.1
21.0
247
122547
145
4.91.42.55.19.6
29.7
122207
11
12.62.12.10.07.4
11.6
9720
1225
6.55.11.50.08.7
18.1
Group III Cranial elements 120 9.7 24 4.9 10 10.5 11 8.0
limb bones of ruminants. The results obtainedindicated that most
losses of paleobiologicalinformation during the taphonomic history
ofthe assemblage were a consequence of the se-lective destruction
of skeletal remains duringthe period when the bones were exposed
onthe surface before burial, and that the effect ofthis
preservational bias was more pronouncedin those species of smaller
body size (Arribasand Palmqvist 1998; Arribas 1999).
The role of hyenas in the bone accumulationprocess at Venta
Micena was determined bycomparing the frequencies of different
typesof 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). Resultsindicated that P. brevirostris was the mainagent
responsible for the bone accumulationat Venta Micena, because the
composition ofthe fossil assemblage is strikingly similar tobone
accumulations produced by modern hy-enas in which major limb bones
predominatewhereas ribs and vertebrae are comparativelyscarce.
Specifically, the relative abundances oflimb 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),
69.476.2% and 12.224.2%, re-spectively (Behrensmeyer and Dechant
Boaz1980; Brain 1981; Skinner and Van Aarde 1981;Bunn 1982; Skinner
et al. 1986), but differentfrom those accumulated by striped
hyenas(Hyaena hyaena) and brown hyenas (Parahyaenabrunnea), in
which higher frequencies of limbbones (90.893.2%) and lower
frequencies ofvertebrae/ribs (4.27%) are found (Maguire etal. 1980;
Skinner et al. 1980, 1995; Skinner andVan Aarde 1981, 1991; Kerbis
Petherhans andKolska-Horwitz 1992). However, Venta Mi-cena
resembles assemblages from dens ofbrown and striped hyenas in its
high densityof bones (Leakey et al. 1999). Spotted hyenasare
efficient hunters, owing to their greaterbody size and strong
social behavior, and pro-duce a highly enriched milk; thus, they do
notregularly carry carrion to their maternity densto feed their
cubs (Kruuk 1972; Ewer 1973;Mills 1989). Nonetheless, there are
some re-ported cases of spotted hyenas accumulatinghuge amounts of
skeletal remains (e.g., seeHill 1981 for a dense accumulation of
boneswithin a breeding den in Amboseli NationalPark, Kenya), and
this was certainly the casewith the cave hyena (Crocuta crocuta
spelaea) inthe late Pleistocene of Europe (Fosse 1996).The
differences in composition between the
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517BEHAVIOR OF AN EXTINCT HYENA
assemblage accumulated by Pachycrocuta atVenta Micena and those
collected by otherspecies suggest that the life habits of the
short-faced hyenas were not identical to those of anyliving
hyaenid.
The quantitative study of differential pres-ervation of major
limb bones of ruminants inthe assemblage (Palmqvist et al. 1996;
Arribasand Palmqvist 1998) showed that bone-gnaw-ing and -crushing
behavior by hyenas of thoseruminant 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 ofmajor limb bones according to their
marrowyields. Such a selective pattern rules out thepossibility
that other processes (e.g., ungulatetrampling) were responsible for
bone fractur-ing.
The recovery of several deciduous teeth of P.brevirostris
belonging to four individuals alsosuggests that the assemblage
originatedthrough accumulation of skeletal parts nearshallow
breeding dens excavated by the hye-nas in the plains surrounding
the Pleistocenelake (Arribas and Palmqvist 1998). The abun-dance of
unworn deciduous hyena teeth rulesout the possibility that bones
were accumu-lated in open feeding places located at hunt-ing sites
distant from maternity dens, if wepresume that, like modern hyenas,
the cubsdid not accompany adults on their search forungulate
carcasses.
A comparison of the Venta Micena assem-blage with those from
other Plio-Pleistocenelacustrine sites from the Guadix-Baza
Basin(Arribas 1999) revealed that Venta Micenashows the highest
diversity of large mam-mals, mainly because of the high diversity
ofcarnivores, from opportunistic scavengers tolarge predators. The
taxonomic richness oflarge mammals at Venta Micena (19 taxa)
issimilar 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
ofmammals from skeletal remains collected bystriped hyenas in
Lothagam, Kenya, and Skin-ner et al. (1991, 1998) identified 11
mammali-an taxa at two maternity den sites of brownhyenas 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 biostratinomicvariables to further
characterize the bone as-semblage from Venta Micena, following
inpart the procedure described by Behrensmey-er (1991) for studying
vertebrate assemblages.Descriptive analysis was based on a subset
of1339 specimens, which includes 1020 identi-fiable skeletal
remains (distributed amongtaxa in Table 1) as well as 211 bones and
108bone shafts that could not be determined tax-onomically. This
sample comprises the well-restored specimens housed at the Museum
ofPaleontology of Orce (Palmqvist et al. 1996).The high value
obtained for the Pearson prod-uct-moment correlation between the
relativefrequencies of taxa in the whole assemblageand in the
subset (Table 1; r 5 0.985; p ,0.0001) indicates that the latter
represents arandom sample of the entire assemblage.
Table 2 shows the abundances of differentskeletal elements in
the subset of large mam-mals and in the three most abundant taxa,
thehorse (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 absenceof hydrodynamic sorting (1:1),
indicating thatthe skeletal remains were not transported byfluvial
processes prior to deposition (Behrens-meyer and Dechant Boaz 1980;
Shipman1981). 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 rulesout the possibility of hydraulic sorting
(Voor-hies 1969).
Limb elements clearly dominate (57.7%) thesample, followed by
vertebrae, cranial ele-ments (cranial vaults, maxillae, and
mandi-
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518 PAUL PALMQVIST AND ALFONSO ARRIBAS
bles; Fig. 2GI), and ribs. Scapulae are mostlyrepresented by
proximal fragments. Diaphy-ses and distal epiphyses predominate
amonghumeri (Fig. 2A). Femora are mainly pre-served as fragments of
diaphyses, and tibiaeas distal epiphyses (Fig. 2B). The pelvis is
rep-resented only by fragments that preserve theacetabulum.
Analysis of weathering stages for the bonesin the subset
indicates exposure to the ele-ments for only a relatively short
time: 89.3%(784/878) of the skeletal elements showweathering stage
0 (Behrensmeyer 1978) andonly 10.7% of the bones (of which
two-thirdsare metapodials) show weathering stage 1,with a few,
shallow, small split-line cracks dueto insolation (Fig. 2C) and
without flaking ofthe 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 untilburial, this was not the case here because
mostbones show no evidence of root marks. On theother hand, bones
that were preserved com-plete lack sedimentary infilling, even in
areasof 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, theseresults
suggest a very short period of subaer-ial exposure before burial
(less than one yearin most cases).
The detailed study of horse remains hasshown that biostratinomic
fractures are veryabundant (Fig. 2), as only 29.1% of major
limbbones are complete; metapodials are the mostabundant bones
preserved as complete ele-ments, 82.2%. Among the fractured
elements,type II spiral fractures (Shipman 1981; Lyman1994)
predominate (100% of fragmented hu-meri, femora, and radii; 74.4%
of tibiae). Othertypes are longitudinal fractures in tibiae,
un-differentiated fractures (all ribs and vertebrae,with the
exception of some vertebrae that lackonly apophyses), and maxillary
bones withboth cheek-tooth rows (33.3% of cranial ele-ments).
Gnaw-marks are very frequent on thehorse remains: all cranial
fragments, scapulae,humeri, radii, pelves, femora, and tibiae
showstriations and gnaw-marks produced by car-nivores; the
preserved epiphyses have fur-
rows and punctures; and the diaphyses, aswell as the skull
bones, show scoring and pit-ting. These marks are also observed in
all oth-er taxa identified at Venta Micena. Coprolites(36 cm thick)
are relatively common.
Evaluation of Taphonomic Bias in theAssemblage
The taphonomic analysis of the large-mam-mal assemblage
preserved at Venta Micenahas revealed the existence of the
followingpreservational biases, which took place con-secutively
during the biostratinomic stage andaffected its original
composition (Palmqvist etal. 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 andbone remains to their maternity dens; and
(3)differential breakage of major limb boneswithin the dens. In the
following sections weevaluate the importance of these biases
andtheir consequences for the composition of theassemblage, with a
special focus on the trans-port of carcasses and the breakage of
bonesfrom 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 SelectivelyHunted by other
Predators. Previous researchon the composition of the bone
assemblage(Palmqvist et al. 1996; Arribas and Palmqvist1998) has
shown that the overwhelming ma-jority of skeletal remains preserved
in VentaMicena were scavenged by hyenas from car-casses of
ungulates preyed upon by hypercar-nivores (i.e., species in which
vertebrate fleshrepresented .70% of diet). The selection
byhypercarnivores of specific ungulates was ba-sically a function
of differences in the bodymass of the preybetween juveniles
andadults 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 deducedfrom crown height measurements for thoseherbivore
species that are well represented inthe assemblage, indicating a
strong selectionby predators of very young and old individ-uals
(Palmqvist et al. 1996: Fig. 8); (2) the in-terspecific analysis of
the relative abundance
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519BEHAVIOR OF AN EXTINCT HYENA
of juveniles with deciduous teeth, and adultswith permanent
dentition, which shows thatjuveniles represent 16.7% (8/48) of all
indi-viduals in ungulate species ,300 kg, yet theproportion of
juveniles increases to 48.0%(72/150) in those species .300 kg
(these per-centages are significantly different accordingto a
one-tailed t-test: t 5 4.63; p , 0.0001); (3)the presence of many
metapodials with severeosteopathologies (Palmqvist et al. 1996:
Fig.11A,B), such as arthrosis, which limited thelocomotor
capabilities of the ungulates andtherefore their ability to escape
from preda-tors; and (4) the sex ratio deduced from thesize
distribution of metapodials in large preyspecies, such as horse and
buffalo, which is bi-ased in favor of females in both cases
(ap-proximately 1 male : 34 females [Palmqvist etal. 1996: Fig.
11C]). This sex ratio suggests thatfemales were more vulnerable to
predationbecause of their smaller body size.
Given that most carnivores usually huntherbivores within a
narrow range of bodymass around the same size as that of the
pred-ator (Kruuk 1972; Schaller 1972 and referencestherein), the
wide range of body mass repre-sented by the ungulate taxa preserved
in theassemblage (106000 kg) suggests that in mostcases these
animals were preyed upon by dif-ferent carnivore species (Palmqvist
et al.1996).
Hypercarnivores are represented in the as-semblage by four
speciestwo 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 bodysize (;100 kg),
similar to that of a jaguar,Panthera onca (Martnez-Navarro and
Palm-qvist 1995, 1996). Judging from the low valueestimated for the
brachial index (i.e., radiuslength : humerus length, ;80%) it was
an am-bush predator, hunting in closed, forestedhabitats and
presumably preying on browsingand mixed-feeding ungulates of
intermediateto large body mass (Lewis 1997). This recon-struction
of its predatory behavior is corrob-orated by the fact that the
metapodials werecomparatively shorter than those of largemodern
felids and other saber-tooths. Thisdirk-toothed machairodont had a
strong body
with a short back, powerfully developed fore-limbs with large
claws, and extremely long,sharp, laterally compressed (and
inherentlyfragile) upper canine teeth. The brain wassmall in
relation to Homotheriums, showing ol-factory lobes that were well
developed. Allthese features give the strong impression of ananimal
built for capturing prey using a shortrush and then using its
considerable strengthto bring down and hold prey with the
fore-limbs, before killing with a slashing bite to thethroat
(Turner and Anton 1998; Arribas andPalmqvist 1999). A similar
hunting behaviorwas inferred by Anyonge (1996) for the
closelyrelated genus Smilodon, a possible descendantof Megantereon
in the New World.
Homotherium (Fig. 3) was a scimitar-toothedmachairodont with
relatively long and slenderlimbs, which provided considerable
leverage(Turner and Anton 1998; Martin et al. 2000).According to
regressions of body massagainst postcranial measurements in
moderncarnivores (Anyonge 1993), it was similar insize to a modern
male lion, Panthera leo (150220 kg). The regression of body mass on
lowercarnassial length in modern felids (Van Val-kenburgh 1990),
however, provides a largersize estimate for the Venta Micena H.
latidens(Palmqvist et al. 1996), 250 kg. The upper ca-nines were
comparatively shorter and broaderthan those of Megantereon, bearing
coarse ser-rations in the enamel of the posterior margin.The
forelimb was more elongated than thehindlimb, indicating that the
animal probablyhad a sloping back. The claws of Homotheriumappear
to have been small, with the exceptionof a well-developed dewclaw
in the first digitof the forefoot. The elongated forelimb
andsmaller claws suggest increased cursorialityand less
prey-grappling capability than othersaber-tooths (Rawn-Schatzinger
1992; Turnerand Anton 1998; Arribas and Palmqvist 1999).Both the
comparatively high brachial index($100% [Lewis 1997]) and the
results ob-tained by Anyonge (1996) in a multivariateanalysis of
the postcranial skeleton of extantand extinct felids, indicate that
Homotheriumwas a pursuit predator, which presumablyhunted very
large grazing and mixed-feedingungulates in open habitats.
Homotherium had alarge brain relative to other saber-tooths,
with
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520 PAUL PALMQVIST AND ALFONSO ARRIBAS
FIGURE 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-
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521BEHAVIOR OF AN EXTINCT HYENA
FIGURE 3. Skulls and reconstructions of the life appearance of
the three largest carnivore species preserved at VentaMicena, the
dirk-tooth Megantereon whitei, the scimitar-tooth Homotherium
latidens, and the giant hyena Pachycrocutabrevirostris. All drawn
to scale, with a typical height at shoulder of 110 cm for
Homotherium. Specific coat patternsare unknown but typical of those
seen across the range of living felids and hyaenids. Drawings by
Mauricio Anton.
onal diagenetic fractures in the diaphyses due to sediment
compaction. D, Astragali. E, Calcanei; one calcaneumshows marks
made by insect larvae. F, Third phalanges; one phalanx is partially
gnawed by hyenas. G, Maxillaegnawed 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 (Arribas1999; Arribas
and Palmqvist 1998) are also indicated.
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522 PAUL PALMQVIST AND ALFONSO ARRIBAS
an enlargement of the optic center, a conditionsimilar to that
of the cheetah, Acinonyx jubatus(Rawn-Schatzinger 1992). Turner and
Anton(1998) suggest that such a cursorial lifestyleand hunting
strategy would imply some de-gree of group activity to bring down
and re-strain prey. In addition, given that a pursuitstrategy for
hunting can be deployed only inrelatively open terrain, group
behavior may beneeded to repel the inevitable attention
ofscavengers. The likelihood of group activity issuggested by the
similarly proportionedAmerican species, H. serum, which is knownin
some numbers (NISP .250, MNI 5 33)from the late Pleistocene site of
Friesenhahncave, Texas. At this site, H. serum is associatedwith
numerous remains (NISP .900 [Rawn-Schatzinger 1992: Table 38]; MNI
5 34 [Ma-rean and Ehrhardt 1995: Fig. 1]) of mam-mothsone adult and
the remainder juve-nilesand it has been suggested that success-ful
predation of mammoths most likely wouldrequire group hunting.
C. falconeri was a hypercarnivorous canid of;30 kg, according to
the results of multivar-iate analysis and multiple regression of
bodymass on craniodental measurements in mod-ern canids (Palmqvist
et al. 1999). The secondmetacarpal has a very reduced articular
facetwith the first metacarpal, which indicates thatthe latter bone
was vestigial if not absent, acondition similar to that of African
painteddogs (Lycaon pictus); this suggests increasedcursoriality
for C. falconeri. This predatorprobably hunted small to
medium-sized graz-ing ungulates (50300 kg) in open to inter-mediate
forested country.
Pachycrocuta brevirostris (Fig. 3) was a bone-cracking carnivore
with a body 1020% largerthan the modern spotted hyena and was
welladapted for dismembering carcasses and con-suming bone
(Palmqvist et al. 1996; Turnerand Anton 1996; Arribas and Palmqvist
1998;Saunders and Dawson 1998). Apart from itssize, this
short-faced hyena differed from oth-er species in the relative
shortening of its dis-tal limb segments (Turner and Anton 1996):the
brachial index is close to 88%, whereas inmodern hyaenids the
values range between99% and 106%; the crural index (i.e.,
tibialength : femur length) is 74%, whereas the cor-
responding figures for modern species rangebetween 80% and 89%.
These differences sug-gest a less cursorial lifestyle for P.
brevirostris.It is also possible that the shortening of thedistal
limb segments could provide greaterpower and more stability to
dismember andcarry large pieces of carcasses, which perhapscould be
obtained from aggressive scavenging(i.e., kleptoparasitism).
The proportion of juveniles in a populationof a given species
depends on two factors(Palmqvist et al. 1996): the reproduction
rate(i.e., the annual birthrate) and the duration ofinfancy (i.e.,
the time spent as a juvenile in-dividual). Rates of birth and death
scale to the20.3 power of adult body mass (M), whereasgeneration
time (measured by life expectancyat birth, duration of infancy, or
age at death)is interspecifically related to body mass by apower 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), becauserates of birth and death per generation are
sizeindependent. A third factor, differences inage-specific
mortality rate, could be relevanthere, as high adult mortality
would increasethe proportion of juveniles in the populationand 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 expectancyat
birth fluctuates around 30% of total lifespan, with small
variations not related tobody size). Moreover, several studies on
thetiming of ontogeny in eutherian mammals(summarized in Peters
1983) indicate that, re-gardless of size, a given developmental
phaserequires a constant proportion of the mam-mals life; thus, the
relative time spent as a ju-venile individual does not scale with
bodymass.
The ratio of juvenile to adult individuals ina population would
be the product of annualbirthrate (Br) and duration of infancy
(Di):
20.3 0.3 0% juveniles ; B D 5 M M 5 M .r i
This relationship implies that the proportion
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523BEHAVIOR OF AN EXTINCT HYENA
TABLE 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; Richardson1980; 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 thewhole collection, b
5 estimated from the subset used for taphonomic analysis).
Characteristics of thebone assemblage
Primary assemblage,collected by predators
Secondary assemblage,collected by scavengers
Venta Micenaassemblage
Proportion of vertebrae andribs in relation to girdle andlimb
bones
High, 1:4 (range 5 1:35)
Low, 1:9 (range 5 1:4.525) 16.9% (429/2544)a
Abundance of articulatedbones, in anatomical connec-tion
Articulated elementsare quite abundant
Articulated bones are scarce(exceptions: metapodialsand
phalanges, vertebrae)
20.0% (204/1020)b
Abundance of major longbonespreserved complete
High and not relatedto their marrowcontent
Low, inversely related tomarrow yield; spiral andlongitudinal
fractures areabundant
27.6% (137/497)b
Abundance of limb boneepiphyses in relation to di-aphyses
High (2:1), withoutpreferential destruc-tion of skeletal partsof
low structuraldensity
Comparatively low (1.51:1), with evidence of pref-erential
consumption oflow-density epiphyses
139.4% (693/497)b
Carnivore/ungulate index, cal-culated from MNI counts
High (2550%) or veryhigh (.50%, indeath traps)
Low (515%), similar to thatfound in modern commu-nities
13.6% (27/198)a
Relative abundance of juvenileungulates, with deciduousteeth
High proportion(.25%)
Low proportion (,25%) 40.4% (80/198)a
Proportion of young/adult in-dividuals for ungulate spe-cies
Increases as a functionof species bodymass
Not related with the size ofspecies
Positively corre-lated with spe-cies mass
Range of body mass coveredby the species preserved inthe
assemblage
Narrow, usuallyaround the samesize as that of thepredator
Wide, in general more thantwo orders of magnitude(from ,10 kg to
.1000kg)
56000 kga
Richness of species (largemammals)
Comparatively low(only prey species)
High diversity (all scav-enged species)
19a
FIGURE 4. Least-squares regression analysis of the pro-portion
of juvenile individuals (estimated from MNIcounts) on adult body
mass (in kg) for ungulate species(n 5 9) of the Venta Micena
assemblage (data from Table1). Separate analyses were conducted for
two groups ofprey species, the first of which (,1000 kg of
estimatedmass 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-toothHomotherium latidens.
of juveniles in any ungulate population is ap-proximately
constant (3040%) and indepen-dent of species body size (Palmqvist
et al.1996).
As previously indicated, in the Venta Mi-cena assemblage the
juvenile/adult ratios ofungulates (estimated from MNI counts
basedon deciduous and permanent teeth) as a func-tion of adult body
mass suggests that mortal-ity age profiles differed depending on
the sizeof the prey. This would be the consequence ofselection by
predators, which increased theproportion of young and more
vulnerable in-dividuals of those ungulate species of largersize.
This interpretation is in accordance withavailable data on prey
selection by Recent car-nivores as a function of size and age of
theirpreferred prey (Palmqvist et al. 1996: Fig. 7;Arribas and
Palmqvist 1998: Table 3). Figure 4
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524 PAUL PALMQVIST AND ALFONSO ARRIBAS
FIGURE 5. Comparison between the relative abundanc-es of
ungulate size classes in the prey hunted and scav-enged by modern
spotted hyenas (Crocuta crocuta) in theSerengeti National Park
(data from Kruuk 1972) and thefrequencies 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 juvenilesand the mass estimated for the adults
indi-cates that the Venta Micena assemblage wasnot formed through
catastrophic mortalityevents during droughts (in such case
theabundance of juveniles of different specieswould 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 choiceof carnivores.
Bias II: Selective Transport of Carcasses andSkeletal Parts.
According to field data collect-ed by Kruuk (1972) in the Serengeti
and Ngo-rongoro National Parks (Tanzania), modernspotted hyenas are
efficient hunters that hunttheir prey in 58.3% of cases and
scavenge un-gulate carcasses in the remaining 41.7% of cas-es. Of
those ungulates scavenged, individualsdead by illness or accident
represent 19.4%,whereas the rest are carcasses of prey huntedand
partially defleshed by lions and painteddogs. The relative
abundances of ungulateprey of different body size classes hunted
bylions and painted dogs correlate well with thefrequencies of
ungulate populations (Kruuk1972; Schaller 1972).
The distribution of specimens among sizeclasses in the ungulate
assemblage from VentaMicena (Fig. 5; frequencies estimated fromMNI
counts in Table 1) is different from thefrequencies of ungulates
hunted by spottedhyenas according to a x2 test for the cumula-tive
differences (x2 5 148.2; df 5 4; p ,0.0001), but remarkably similar
to those inwhich spotted hyenas scavenge carcasses ofanimals killed
by lions and wild dogs (x2 517.8; p , 0.01 for all size classes; x2
5 4.3; df5 3; p . 0.1 for ungulates weighing .50 kg).The only
significant difference between thedistribution of ungulate size
classes in VentaMicena and in the prey scavenged by spottedhyenas
is the proportion of small species (,50kg), which are
underrepresented in the fossilassemblage (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 59.68; p , 0.0001). This indicates that short-faced
hyenas preferentially consumed smallungulates in situ and
selectively transportedcarcasses and body parts of larger species
totheir maternity dens.
These results suggest that the predatory be-havior of
Pachycrocuta differed from that ofCrocuta, because modern spotted
hyenas bothhunt and scavenge ungulates, whereas theshort-faced
hyenas seem to have relied moreheavily on prey hunted by other
predators;therefore, the behavior of Pachycrocuta wasprobably more
similar to that of modernbrown and striped hyenas, which are
predom-inantly scavengers (Mills 1989). This trophicdependence was
facilitated by the fact that un-gulate carcasses left by
machairodonts andhypercarnivorous canids would retain vari-able
amounts of flesh and all nutrients withinthe bones, given that the
slicing dentition ofthese carnivores made them incapable of
bone
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525BEHAVIOR OF AN EXTINCT HYENA
FIGURE 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 hindlimbbones).
Caprini indet., Praeovibos sp., and species .1000kg were excluded
from this analysis owing to their lowsample sizes. Species ordered
by decreasing values inthe ratio MNI(teeth) : MNI(bones).
cracking (Marean 1989; Arribas and Palm-qvist 1999).
The bone assemblage of Venta Micena canthus be considered as
mixed, showing somefeatures 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 selective transportof ungulate remains
is particularly evidencedby the differential representation of
preservedskeletal parts. The abundance of each taxoncan be
estimated by MNI counts obtainedfrom teeth and cranial elements
(i.e., antlersand horn bases in the case of ruminants), aswell as
from MNI counts based on minimumnumber of elements (MNE) estimated
frompostcranial remains (i.e., forelimb and hin-dlimb bones,
complete elements or those rep-resented by isolated epiphyses).
Figure 6shows that for small ungulates, such as the
goat (Hemitragus alba; 75 kg of estimated massfor adult
individuals) or the fallow deer (Damasp.; 95 kg), MNI(teeth) gives
a higher estimate ofabundance than MNI(bones) (x2-test: x2 5
5.33and 5.88; p , 0.05 in both cases; MNIteethcounts used as
expected frequencies). For Soer-gelia minor, a bovine of
intermediate mass (225kg), the two MNI counts are similar (x2 5
0.10;p . 0.5). Finally, ungulate taxa of larger size,such as the
horse (E. altidens; 350 kg) and thebuffalo (Bovini cf. Dmanisibos;
450 kg), are bet-ter represented by postcranial elements (x2 530.42
and 20.45, respectively, p , 0.0001 inboth 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 thatwere preferentially transported as completecarcasses,
the original abundances, estimatedfrom 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 majorlongbones and destroy limb bone epiphyses toget at
the marrow and fat, MNI estimates forthe assemblage that are based
on teeth shouldbe higher than those based on postcranial el-ements.
Therefore small ungulate species(,100 kg), which are represented by
anMNI(teeth) : MNI(bones) ratio of approximately 2:1 in the Venta
Micena assemblage (H. alba andDama sp.), were probably transported
in mostcases as complete carcasses. In the case oflarger species
(.300 kg), selective transport ofmarrow-rich body parts (i.e., the
forelimb inbuffalo and the hindlimb in horse) is suggest-ed by the
reverse ratio (MNIteeth : MNIbones 5 1:2). Finally, for ungulate
species of intermedi-ate size (100300 kg), such as S. minor,
post-cranial elements were transported by hyenaswith a somewhat
higher frequency than heads(after preferential consumption of major
long-bones, MNI counts calculated from teeth andbones are similar,
1:1).
The only exception to this trend is the largemegacerine deer E.
giulii. Although its bodymass is estimated at 380 kg for adult
individ-uals, MNI counts from teeth and bones arequite similar
(Fig. 6; x2 5 0.05; p . 0.5). Thismay be due to two reasons: (1)
major limbbones are relatively slender in this species and
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526 PAUL PALMQVIST AND ALFONSO ARRIBAS
TABLE 4. Number of forelimbs and hindlimbs (calculated from MNE
counts for each major limb bone) of Equusaltidens and Bovini cf.
Dmanisibos from Venta Micena. Total marrow yields and flesh weights
of forelegs and hindlegs estimated from values for modern Equus
caballus (Outram and Rowley-Conwy 1998) and Bison bison
(Brink1997).
Equus altidens
Forelimbs Hindlimbs
Bovini cf. Dmanisibos
Forelimbs Hindlimbs
Number of legs (right/left)Total marrow yields (g)Flesh content
(kg)
118 (59/59)77.114.0
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 theirdens 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 oflarge ungulate species suggests that
eachshort-faced hyena foraged alone in search ofscavengeable
carcasses, as do modern brownhyenas (Mills 1989). If they had
foraged ingroups, as spotted hyenas often do (Kruuk1972; Mills
1989), the members of the hyenaclan would have transported all the
anatomi-cal regions of each carcass scavenged to theirmaternity
den; large ungulate taxa would thenbe represented in the assemblage
by similarnumbers of postcranial bones and cranioden-tal elements,
rather than the skewed ratio weobserved.
Table 4 shows the number of forelimbs andhindlimbs calculated
from MNE counts foreach limb bone in two taxa well representedin
the assemblage, the equid E. altidens and thebuffalo Bovini cf.
Dmanisibos. The correspond-ing values for flesh and marrow
contents, es-timated from data for major longbones in twomodern,
similarly sized herbivoresthehorse, Equus caballus (Outram and
Rowley-Conwy 1998) and the North American plainbison, Bison bison
(Brink 1997), are also pro-vided. The ratio of forelimbs to
hindlimbs is0.837 in the Venta Micena horse, which isclearly
different from that of flesh yields pro-vided by forelimbs and
hindlimbs, 0.303, andcloser to the corresponding ratio estimated
formarrow contents, 0.668. In the case of the buf-
falo, the ratio of forelimbs to hindlimbs is1.073, again a value
different from that esti-mated for flesh contents, 0.296, but very
closeto the value obtained for marrow, 1.114. Thissuggests that
marrow content was the mainreason hyenas transported limb bones to
theirmaternity 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 forVenta Micena by
Arribas and Palmqvist (1998)and Arribas (1999). Three distinct
types ofbone-consuming activities by hyenas were es-tablished (Fig.
2), depending on the positionof 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) andmineral density:
1. Humerus, radius, tibia, ulna, and calca-neum: these are
consumed following an in-variant proximodistal pattern. The
reductionof these bones by hyenas starts with gnawingthe proximal
epiphysis, then is followed byfracturing the diaphysis, and is
finished bygnawing of the distal epiphysis, which usu-ally shows
abundant tooth marks.
2. Femur: this is the only element in whichthe sequence of
consumption follows a vari-able direction (i.e., from the proximal
epiph-ysis to the distal epiphysis or vice versa) andboth epiphyses
are lost.
3. Third metacarpal and metatarsal: thesebones are modified by
crushing, with a vari-able direction of activity, and they tend to
bemore abundantly preserved as complete ele-ments than other major
limb bones, owing totheir higher mineral density and lower mar-row
yields.
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527BEHAVIOR OF AN EXTINCT HYENA
FIGURE 7. Least-squares regression analysis of the rawabundance
at Venta Micena of preserved major limbbone 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 theskeletal elements
preserved in the fossil as-semblage are those remaining once all
within-bone nutrients were consumed by hyenas. Toevaluate
quantitatively this taphonomic biason the preservational
completeness of thebone assemblage, we performed a compara-tive
analysis of the preservational state andabundance of postcranial
elements in E. alti-dens and Bovini cf. Dmanisibos. We
hypothe-sized that there would be differences in theabundance of
postcranial elements becausethere are differences in their
within-bone nu-trients (Emerson 1990; Brink 1997; Arribasand
Palmqvist 1998; Outram and Rowley-Conwy 1998). Figure 7A shows the
raw abun-dance in which major limb bone epiphyses ofhorse are
preserved in the assemblage, as afunction of their mean marrow
content (esti-mated from values for E. caballus in Outramand
Rowley-Conwy 1998). A least-squares re-gression revealed an inverse
relationship be-tween both variables, which is statistically
sig-nificant (r 5 20.60; p , 0.05). This indicatesthat 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 onthose yielding
lower marrow values (e.g., me-tapodials, distal tibia).
The raw abundance of major longboneepiphyses of buffalo in
relation to their mar-row weight is shown in Figure 7B (data for
B.bison in Brink 1997). The regression line alsoshows a negative
slope (r 5 20.85, p ,0.0001), which indicates that the skeletal
partsbetter represented among the survivingepiphyses are those with
lower marrowyields. However, the regression obtained forthis
species is statistically more significantthan in the case of E.
altidens, owing to thehigher 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
elementsof both taxa in the bone assemblage.
Three major factors therefore appear tohave 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 wholecarcasses or
certain anatomical parts, depend-ing on the size of the ungulate
species scav-enged (bias II); and the preferential breakagein the
dens of bones with higher marrow con-tent (bias III). Although
these biases decreasedthe amount of paleobiological
informationpreserved in the assemblage, the representa-tion of the
original mammalian community isvalid, thanks to the scavenging
behavior of hy-enas. A collection of bones from the prey of asingle
predator may differentially sample par-ticular species because of
the predators preypreferences, and such accumulation wouldprovide a
poor estimate of standing diversity
-
528 PAUL PALMQVIST AND ALFONSO ARRIBAS
in the paleocommunity (Vrba 1980; Brain1981; Shipman 1981;
Behrensmeyer 1991).This is not the case at Venta Micena,
however,where the skeletal remains of a wide spectrumof ungulate
prey hunted by several species ofhypercarnivores in different
habitats were col-lected by hyenas, thus providing a
detailedpicture of the diversity of large mammals thatinhabited
southern Spain during early Pleis-tocene times. This is
corroborated by severalstudies of recent bone assemblages
collectedby 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 compositionof the mammalian fauna in areas adjacent tothe
maternity dens.
The assemblage from Venta Micena wasprobably accumulated over a
very short timespan; thus it is evidently not time-averagedand
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 byKruuk
(1972), the mean numbers of adult andjuvenile spotted hyenas per
den in Serengetiare 55 and 12, respectively. With Kruuks es-timate
of mean annual mortality at 16.7%, ap-proximately 11 individuals of
the hyena clandie each year, a figure remarkably similar tothe MNI
calculated for P. brevirostris in the fos-sil assemblage (10
individuals, 6 adults and 4juveniles; 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 permanentteeth, indicating that they
were at the end oftheir first year of life. This suggests that
dur-ing a single season, probably summer, all fourof these
individuals died.
Conclusions
Taphonomic processes have previouslybeen interpreted as solely
destructive forces.Information loss in terrestrial and fluvial
bio-
tas results largely from such processes astransport,
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 fordecoding paleobiological
information (Wilson1988; Fernandez-Lopez 1991; De Renzi 1997).The
assemblage of large mammals from VentaMicena constitutes a good
example of how an-alytical studies can contribute toward
re-cre-ating a significant fraction of paleobiologicalinformation
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, suchas the behavior of the extinct hyena P.
breviros-tris, a species that differed from the modernspotted hyena
in being a strict scavenger ofungulate carcasses selectively preyed
upon byhypercarnivores. This inference was based onthe quantitative
study of the preservationalbias introduced by the scavenging
behavior ofthis giant hyena, which is shown to have beenhighly
specialized.
However, similar paleobiological inferencesmay be obtained only
in assemblages thatwere collected during the biostratinomic stageby
biological agents, like hyenas, hominids, orporcupines. Other types
of terrestrial accu-mulations, where the bones were
accumulatedexclusively by physical agents (e.g., fluvial
as-semblages), would reveal useful sedimento-logical and
paleoenvironmental data (e.g.,strength and direction of water
currents), butbecause the skeletal remains of such assem-blages are
frequently mixed, hydrodynami-cally sorted, and even reworked,
decoding thetaphonomic information locked in these as-semblages
would contribute little reliable pa-leobiological information about
the structureand composition of the original paleocom-munity from
which they were derived. In thiscontext, the macrovertebrate
assemblage fromVenta Micena constitutes an exceptional win-dow for
the detailed study of the mammaliancommunities that inhabited
Western Europeduring the early Pleistocene and the relation-ships
among the species that lived withinthem.
-
529BEHAVIOR OF AN EXTINCT HYENA
Acknowledgments
Thanks to M. De Renzi, M. Foote, A. Miller,R. A. Reyment, and L.
Spencer for suggestionsthat led to significant improvements in
thiscontribution. We gratefully acknowledge M.Anton for providing
us the reconstructions ofcarnivores used in Figure 3. R. Bobe, J.
Saun-ders, S. L. Wing, and an anonymous reviewerprovided insightful
comments and helpfulcriticism of the manuscript. And, last but
notleast, N. Atkins improved the style of this ar-ticle.
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