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Primate remains from African crowned eagle (Stephanoaetus coronatus) nests in Ivory Coast's Tai Forest Implications for primate predation and early hominid taphonomy in South Africa.

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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 131:151–165 (2006)
Primate Remains from African Crowned Eagle
(Stephanoaetus coronatus) Nests in Ivory Coast’s
Tai Forest: Implications for Primate Predation
and Early Hominid Taphonomy in South Africa
W. Scott McGraw,1* Catherine Cooke,1 and Susanne Shultz2
1
2
Department of Anthropology, Ohio State University, Columbus, Ohio 43210-1364
Population Biology Research Group, University of Liverpool, Liverpool L69 7ZB, UK
KEY WORDS
monkeys; raptors; predation; Taung child
ABSTRACT
Understanding the initial processes of
deposition can help with interpretations of fossil assemblages. Here we discuss the taphonomy of primate
remains collected under 16 nests of African crowned
eagles (Stephanoaetus coronatus) in the Tai Forest, Ivory
Coast. From 1,200 bones collected, including 669 primate
bones, we calculated minimum number of individuals
(MNI), survivability profiles, and damage profiles using
methods identical to those employed by Sanders et al.
([2003] J. Hum. Evol. 44:87–105) in their analysis of bones
from eagle nests in Uganda. Crowned eagles leave a consistent taphonomic signature on their prey remains;
hence, results from our analysis of the Tai assemblage are
similar to those from the Ugandan sample. Hindlimb and
cranial bones are relatively abundant in the sample, while
ribs, vertebrae, carpals, and tarsals do not survive well.
Primate crania typically display puncture marks around
the eye, long bones remain largely intact, and scapulae exhibit raked breakage. These data have implications for
understanding the dynamic between extant primates and
one of their principle predators, as well as the taphonomy
of hominid-bearing caves in South Africa. We concur with
Berger and Clarke ([1995] J. Hum. Evol. 29:275–299) that
a large raptor could have been responsible for the death of
the Taung child, Australopithecus africanus. Am J Phys
Anthropol 131:151–165, 2006. V 2006 Wiley-Liss, Inc.
Anthropologists have long had a keen interest in the
behavior of primates as both predators and prey (e.g., Lee,
1968; Brain, 1981; Stanford, 1998; Hart and Sussman,
2005). Predation likely plays a significant role in primate
mortality, and is widely regarded as a prime mover in the
evolution of primate sociality (Van Schaik, 1983; Boinski
and Chapman, 1995; Hill and Lee, 1998; Treves, 1999;
Boinski et al., 2003; Janson, 2003). The main primate
predators are large cats, raptors, snakes, chimpanzees,
and humans (Cheney and Wrangham, 1987). In general,
these primate predators can be classified as either pursuit
or ambush hunters, and the differences in hunting strategies are reflected in a monkey’s responses to each predator type (Noe and Bshary, 1997; Zuberbuhler, 2000, 2001).
For example, chimpanzees are pursuit hunters who initially search for and approach monkey groups in silence.
Hunts by chimpanzees in the Ivory Coast’s Tai Forest are
cooperative activities involving multiple hunters that last
up to 40 min (Boesch and Boesch-Achermann, 2000). In
most cases, monkeys killed by Tai chimpanzees are aware
they have been targeted; after giving an initial alarm call,
monkeys typically fall silent at the sound of approaching
chimpanzees, who nevertheless continue to pursue after
the alarm is made. The attacking strategies of pursuit hunters such as chimpanzees are well-documented (Boesch and
Boesch, 1989; Boesch, 1994; Stanford et al., 1994).
In contrast to pursuit predators, ambush predators rely
more on surprise. Leopards in the Tai Forest are typical
ambush hunters that hide in patches of dense undergrowth and wait motionless to surprise unsuspecting
monkeys (Zuberbuhler and Jenny, 2002). Raptors are also
ambush predators, and are believed to exert significant
selective pressure on primates (Terborgh, 1983; Cheney
and Wrangham, 1987; Gautier-Hion et al., 1983; Isbell,
1994; Csermely, 1996; Zinner and Pelaz, 1999; Karpanty,
2003; Karpanty and Grella, 2001; Shultz, 2002; Gild-daCosta et al., 2003; Kerbis et al., 2004; Shultz et al., 2004).
Ambush hunters such as raptors and leopards may stalk
prey for extended periods of time (Zuberbuhler et al.,
1999; Shultz, 2001). However, the attack distance tends to
be short, such that capture and attack are essentially simultaneous events. Considering the potential irregularity
and short duration of ambush hunts, as well as the
required secrecy on the part of the predator, collecting systematic data on ambush hunters under natural conditions
is difficult. For these reasons, observations of ambush
hunting behavior on primates in forested environments
are largely opportunistic, and systematic data on attacks
C 2006
V
WILEY-LISS, INC.
C
Grant sponsor: Leakey Foundation; Grant sponsor: Wildlife Conservation Society; Grant sponsor: Peregrine Fund; Grant sponsor:
National Science Foundation; Grant sponsor: British Council; Grant
sponsor: University of Liverpool; Grant sponsor: Ohio State University.
*Correspondence to: W. Scott McGraw, Department of Anthropology, Ohio State University, 114 Lord Hall, 124 West 17th Ave.,
Columbus, OH 43210-1364. E-mail: mcgraw.43@osu.edu
Received 20 July 2005; accepted 26 September 2005.
DOI 10.1002/ajpa.20420
Published online 4 April 2006 in Wiley InterScience
(www.interscience.wiley.com).
152
5.1
10.0
6
1
0
5
3
7
1
1
2
6
0
0
2
0
0
0
34.0
1.9
4.9
2.0
0.44
0.9
9.0
4.4
2.2
4.4
9.0
15.1
2.2
31.0
13.7
12.1
28.0
10.7
12.8
22.0
1
24.9
Grand total NISP, 669; grand total MNI, 204.
24.0
10.01
49.0
28.1
44.0
21.5
0
2
0
0
0
3
2
0
1
1
0
0
0
0
0
1
0
2
0
0
0
5
3
0
1
1
0
0
0
0
0
1
13.0
0
0
0
0
0
0
0
0
1
0
0
0
1
0
0
0
0
0
0
0
0
0
0
0
1
0
0
0
2
0
0
0
3.0
3
0
0
0
1
2
0
0
0
2
0
0
1
0
0
0
8
0
0
0
1
2
0
0
0
2
0
0
2
0
0
0
15.0
0
1
0
3
2
0
0
0
1
1
0
0
1
0
0
0
0
1
0
4
4
0
0
0
2
2
0
0
2
0
0
0
15.0
2
2
0
1
7
5
2
0
3
3
0
0
4
2
0
0
6
3
0
1
23
13
3
0
5
12
0
0
12
3
0
0
81.0
7
1
0
2
6
8
1
0
0
2
1
0
0
0
0
0
19
3
0
2
19
26
1
0
0
13
3
0
0
0
0
0
86.0
3
1
1
1
3
2
2
1
2
2
1
1
1
0
0
1
7
1
1
8
15
7
3
1
6
6
6
2
2
0
0
2
67.0
9
0
2
2
7
8
2
1
3
4
1
2
5
2
0
1
24
0
3
3
57
21
3
2
6
6
2
46
7
2
0
6
188.0
18
2
2
14
43
22
1
1
6
15
13
0
18
6
4
2
167.0
1
2
3
4
5
6
7
8
9
10
12
14
15
18
25
26
Total NISP
Total MNI
% primate NISP
% primate MNI
5
1
1
3
9
7
1
1
3
4
1
0
5
1
1
1
MNI
NISP
MNI
NISP
MNI
NISP
MNI
NISP
MNI
NISP
MNI
NISP
MNI
Procolobus
verus
Procolobus
badius
Cercocebus
atys
Unidentified
Cercopithecus
NISP
MNI
NISP
MNI
NISP
Nest no.
Perodicticus
potto
American Journal of Physical Anthropology—DOI 10.1002/ajpa
Colobus
polykomos
Unidentified
colobine
Data on crowned eagles were collected in the Ivory
Coast’s Tai Forest between 1998–2001 (Shultz, 2003). The
Tai Forest is home to 11 primate species, including eight
cercopithecid monkeys that have been studied since 1989.
Details of the study site and additional information on the
monkey fauna can be found in McGraw (1996, 1998).
Bones were collected from beneath 16 nests located near
the research station of the Tai Monkey Project. During
each visit to a nest, a 5-m radius of ground beneath the
nest was systematically searched for prey remains.
Twelve nests were visited monthly during the breeding
season. The remaining four nests were farther from the
Cercopithecus
diana
METHODS
Cercopithecus
campbelli and
Cercopithecus
petaurista
TABLE 1. Distribution of primate remains from 16 crowned eagle nests in the Tai Forest1
are nonexistent (e.g., Cordeiro, 1992, 2003; Zuberbuhler
et al., 1999; Shultz, 2001).
Researchers have therefore devised alternative approaches to measure the impact and nature of primatekilling birds, including examining the discarded remains
of prey from the nests of carnivorous birds (Daneel, 1979;
Skorupa, 1989; Struhsaker and Leakey, 1990; Boshoff
et al., 1994; Shultz, 2002; Sanders et al., 2003; Shultz
et al., 2004). Raptors routinely transport their prey back
to their nest sites, where bones are discarded, and examination of remains from raptor meals can be used to develop
prey profiles. These profiles can then be used to examine
characteristics that eagles use to target specific prey.
This study expands on previous analyses of African
crowned eagle Stephanoaetus coronatus nest remains
(Shultz, 2002; Shultz et al., 2004), and investigates survivability, fragmentation, and damage patterns of primate
bones collected from the Tai National Park, Ivory Coast.
Tai is home to eight cercopithecid monkeys and at least
two prosimians. Common names, species names, and
mean male and female body weights (Smith and Jungers,
1997) for primates in the taphonomic assemblage are red
colobus (Procolobus badius, 8.36 and 8.21 kg), olive colobus (Procolobus verus, 4.7 and 4.2 kg), western black and
white colobus (Colobus polykomos, 9.9 and 8.3 kg), sooty
mangabey (Cercocebus atys, 11 and 6.2 kg), Diana monkey
(Cercopithecus diana, 5.2 and 3.9 kg), Campbell’s monkey
(Cercopithecus campbelli, 4.5 and 2.7 kg), lesser spotnosed monkey (Cercopithecus petaurista, 4.4 and 2.9 kg),
greater spot-nosed monkey (Cercopithecus nictitans, 6.67
and 4.26 kg), potto (Perodicticus potto, 1.25 and 1.21 kg),
and Demidoff ’s galago (Galago demidoff, 63 and 60 g).
The diet composition of crowned eagles in Uganda’s
Kibale Forest was studied (Struhsaker and Leakey, 1990;
Mitani et al., 2001). Comparison of prey profiles between
sites (discussed below) reveals that crowned eagles should
not be considered prey ‘‘specialists;’’ nor do the same characteristics consistently predict which primates are most
likely to fall victim to these raptors. Sanders et al. (2003)
discussed the taphonomy of prey remains from crowned
eagles at Kibale, and the present paper contains a similar
analysis of primate prey remains from Tai, to provide
additional information on the taphonomic signature left
by crowned eagles. Examining similarities and differences
in prey profiles of eagles between forests is important for
understanding the formation and composition of the
taphonomic record, and after discussing the taphonomic
signature left on primate remains by crowned eagles at
Tai, we use this information to test the hypothesis that
the Taung child (Australopithecus africanus) was the victim of a large bird of prey (Berger and Clarke, 1995; Sanders et al., 2003).
Unidentified
primate, NISP
W.S. McGRAW ET AL.
153
EAGLE KILL REMAINS FROM TAI FOREST
Fig. 1. Typical assemblage of primate
bones from nest (nest 5) of crowned eagle
in Tai Forest, Ivory Coast.
research station, and were visited only once to collect prey
remains. During nonbreeding periods, one of us (S.S.) also
removed prey remains from the nesting material of three
of the monitored nests.
Primate bones were identified using a reference collection of monkey skeletons from Tai housed at Ohio State
University. For each element, we recorded age (mature vs.
immature), sex, species, and degree of wear/state according to the criteria set forth by Sanders et al. (2003). The
remains of Cercopithecus campbelli and C. petaurista are
difficult to distinguish from each other, and were grouped
together in the analysis. This should not affect the results
or conclusions, since these guenon species are similar in
body size, habitat use, group size, and general ecology
(McGraw, 2000). Another guenon (Cercopithecus nictitans
stampflii) is sparsely distributed in the northern portion
of the Tai Forest (Eckardt and Zuberbuhler, 2004). There
are no specimens of this guenon in the reference collection, and it is possible that some of the unidentified Cercopithecus remains can be assigned to this taxon. We calculated the number of individual specimens (NISP) and minimum number of individuals (MNI) for each nest and the
entire sample and measured bone survivability and bone
fragmentation, using methods identical to those outlined
in Sanders et al. (2003).
TABLE 2. Composite MNI scores from 16 crowned eagle nests
in the Tai Forest
Minimum number of individuals
Cercopithecus diana
C. campbelli/C. petaurista
Unidentified Cercopithecus
Cercocebus atys
Procolobus badius
Procolobus verus
Colobus polykomos
Unidentified colobines
Perodicticus potto
Total
Adult
Immature
Total
28
33
9
15
22
7
7
0
6
16
16
13
13
9
2
2
2
4
44
49
22
28
31
9
9
2
10
204
RESULTS
Over the course of 34 months, approximately 1,200
bones were collected within and beneath 16 crowned eagle
nests. A complete profile of the prey assemblage, including
nonprimates, can be found in Shultz et al. (2004). In total,
669 primate elements were collected from 16 nests, and of
these, 635 bones could be assigned to at least family level
(Table 1). The number of primate elements collected from
a single nest ranged from 4–167, a disparity reflecting the
interval in which bones were retrieved from a particular
nest, rather than idiosyncrasies of individual eagle diets.
Four nests were monitored continuously over a 34-month
period, four were visited only once, and the number of visits to the remaining eight nest sites fell between these two
extremes. An assemblage of primate bones from a typical
nest is shown in Figure 1. The minimum number of pri-
Fig. 2. Minimum numbers of adult and immature individuals for eight primate species from 16 crowned eagles in Tai Forest, Ivory Coast.
mate individuals for the entire sample is 204, and the
most abundant species in the collection is Cercopithecus
diana (MNI ¼ 44; 21.6% of primate sample) (Table 2, Fig.
2). The combined remains of C. petaurista and C. campbelli constituted the largest overall MNI (49), but it is not
possible to confidently distinguish between these guenon
taxa. Despite their similar body sizes, there is a marked
difference in the minimum number of red (n ¼ 31) and
black and white (n ¼ 9) colobus monkeys in the sample. A
American Journal of Physical Anthropology—DOI 10.1002/ajpa
154
W.S. McGRAW ET AL.
true for the entire sample (Fig. 3a), and when adults (Fig.
3b) and immature individuals (Fig. 3c) are examined separately. The most striking age-related difference is the
greater number of femora (43%) that survive from immature individuals compared to mature individuals (25%).
Survivability profiles for individual species are shown
in Figure 4a–g.
Femora and tibiae are generally the most common surviving bones for all species. Cranial remains with the
highest survivability quotients are derived from the largest (sooty mangabey) and smallest (potto) primates. Few
intact skulls were accompanied by their mandibles. The
prosimian sample consists of cranial elements and little
else: potto crania are far more likely to survive than other
portions of the skeleton. Large bones dominate the assemblage, and there are relatively few small, fragile bones. A
large percentage of the ribs recovered can be assigned to a
single individual (Fig. 5). This individual (a male Cercopithecus petaurista), represented by approximately 60% of
its skeleton, is the most complete primate specimen from
the 16 nests. Survivability profiles for the guenon species
are similar (Fig. 4a,b), as are those of the two large, similarly sized colobines (Fig. 4d,e). Within both groups, long
bones of both limbs generally survive best, followed by
cranial bones. In contrast, the only surviving bones from
the smallest colobine, the olive colobus, are those of the
hindlimb (Fig. 4f).
Damage patterns (fragmentation)
Fig. 3. Bone survivability profiles for all primates (a), adults
only (b), and immatures (c).
minimum of 10 pottos was calculated for the sample, and
no galago remains were found despite the presence of one
and possibly two galago species in the Tai Forest. As discussed elsewhere (Shultz, 2003), there is no difference in
the number of males and females in the prey collection;
nor is the proportion of adults in the eagle diet significantly greater than that of immature individuals for any
primate species individually or for all primate species
combined (Fig. 2).
Bone survivability
Using the methods applied to the Kibale sample
(Sanders et al., 2003), we find that long bones and cranial
remains are the most common elements in the Tai collection, and smaller, more fragile bones are more poorly represented. There are few ribs, phalanges, tarsals, or carpals, and comparatively few vertebrae (Fig. 3a). Hindlimb
elements survive better than those of the forelimb; this is
Eagles inflict unequal degrees of damage to the bones of
the primates they kill (Fig. 6a). Considering the entire
assemblage, the greatest damage is concentrated on the
bones of the head, shoulder, and pelvic girdles, as well as
bones of the hands and feet. Mature bones are more durable than immature ones (Fig. 6b,c), although damage tendencies are similar across age categories: long bones and
mandibles survive best, and radii and femora are the least
fragmented bones for both age categories. Long bones are
more durable than smaller, irregularly shaped, or flat
bones, and when long bones are modified, damage is concentrated at the ends, with minimal harm to bone shafts.
Among adults, fragmentation percentages of forelimb
bones are similar to those of the hindlimb. The most striking age-related difference is the absence of any ribs, damaged or otherwise, in the immature sample. Most immature bones are not intact. However, it is possible that disassociated epiphyses are the consequence of sutural
disintegration after whole bones were discarded by eagles,
rather than direct feeding activity. Subadult mandibles
are quite durable.
Damage profiles of all species are unique. However, a
comparison of interspecific patterns reveals some trends.
With few exceptions, damage frequencies of bones from all
species do not exceed 50% (Fig. 6d–j). For most species,
the tibia is the least fragmented hindlimb bone, and the
radius is the most durable bone in the forelimb. The few
clavicles and phalanges recovered (assigned to Cercopithecus campbelli/C. petaurista) were not fragmented. Bones
of the sooty mangabey, particularly those of the forelimb,
are generally more fragmented than those of smaller cercopithecines.
Most crania show evidence of aggressive manipulation
and damage from eagle talons and beak activity (Fig.
7a,b). At a minimum, most skulls were fractured, presumably from the great force applied by the eagle grip. The
sample contains 10 relatively complete monkey skulls
American Journal of Physical Anthropology—DOI 10.1002/ajpa
EAGLE KILL REMAINS FROM TAI FOREST
155
Fig. 4. Bone survivability profiles for Cercopithecus diana (a), Cercopithecus petaurista/C. campbelli (b), Cercocebus atys (c),
Procolobus badius (d), Colobus polykomos (e), Procolobus verus (f), and Perodicticus potto (g).
with the face still attached to the calvarium (Fig. 7a,b, top
two rows). Of these, six skulls are adult, and four are from
immature cercopithecids. Seven specimens in this sample
of 10 had been opened to access the brain. Three of the
immature skulls had been opened at the base, and one
had not been opened at all. In the adult sample, three
American Journal of Physical Anthropology—DOI 10.1002/ajpa
156
W.S. McGRAW ET AL.
Fig. 5. Remains of Cercopithecus petaurista. This skeleton
represents most complete individual from any nest.
skulls had been opened at the base, one had been opened
at the side, and two, including the largest skull, had not
been opened at all. There appears to be little relationship
between the size of complete adult monkey skulls recovered and the chance that it was modified for brain removal. For example, two adult male guenon skulls were
recovered from the same nest: one was opened at the base
(Fig. 7b, second row, far left), while the other is intact
(Fig. 7b, first row, second from left). This is not the case
for potto skulls recovered, all of which had openings of
varying sizes in the occipital region (Fig. 8a,b). Holes from
talon punctures were common in adult skulls, and tended
to be located at the pterion on the lateral wall (Fig. 9a).
Several specimens exhibited circular punctures more
superiorly in the frontal bone, or where the frontal contacts the parietal (Fig. 9b). Punctures from talons are
found inside the orbital cavities, on the orbital floor, on
the interorbital septum, and on the lateral orbital wall,
where there was damage behind the postorbital septum
(Fig. 9c).
Numerous isolated occipitals and parietals from subadult monkeys were recovered, most having been disassociated along sutural lines (Fig. 10). Frontal bones and calvaria of immature monkeys also tend to be broken along
suture lines. However, several partial calvaria and isolated
parietals exhibit signs of breakage not associated with sutural borders, including the characteristic V-shaped breaks
from eagle beaks or talons described by Sanders et al.
(2003) and Berger and Clarke (1995) (Fig. 11, top row).
Incidents of isolated damage, including V-shaped punctures and ‘‘can-opener’’ perforations, both of which can produce bony flaps, are present in the Tai assemblage, but
these instances of manipulative damage are not common
(Fig. 11, center row). Several calvaria from immature monkeys exhibited parietal tears that are linear or slightly
curved fissures of varying lengths (Fig. 11, bottom row).
These were not observed on any adult skull. No isolated
cranial bones from subadult pottos were recovered, despite
the presence of immature limb bones in the sample. With
the exception of three elements, all mature and immature
mandibles were recovered in unfragmented condition (Fig.
12). Isolated maxilla or maxillary fragments are rare, and
only two are present in the entire collection.
Not a single scapula recovered was undamaged by eagles, and most show the characteristic raked breakage
and puncture marks on the blades described by Sanders
et al. (2003) (Fig. 13). These modifications include circular
puncture holes, rectangular gaps, V-shaped channels, and
irregularly shaped fissures. Humeri are generally intact,
and those that are not were damaged on the proximal and
distal articular surfaces. Humeral shafts remain virtually
untouched (Fig. 14, top row). Of the forelimb long bones,
ulnae are most likely to be fragmented, and breakage usually occurs at the distal ends (e.g., missing styloids),
although some specimens show evidence of damage to the
olecranon (Fig. 14, center row). Radii are slightly more
likely to be found intact, with damage concentrated at the
proximal and distal surfaces. Several specimens recovered
on the forest floor beneath nests showed additional damage from rodent gnawing (Fig. 14, bottom row).
The flat bone of the pelvic girdle shows damage similar
to that of the shoulder: the iliac blade of every specimen
recovered had been raked along the crest, though to lesser
degrees than seen in scapulae (Fig. 15, top two rows). Pubic bones are frequently broken, while ischia are damaged
less frequently. Most femora are intact, and damage is
usually concentrated on the femoral head, greater trochanter, or condyles (Fig. 15, bottom two rows). Several
adult femora are missing significant portions of their
proximal or distal ends; however, shaft fragments are
rare. These tendencies also apply to the tibia: fragmented
tibiae are frequently missing the tibial plateau and/or distal articular surface, including the medial malleolus (Fig.
16, top two rows). Most fragmented fibulae are broken immediately adjacent to epiphyseal lines; only two fibular
shaft fragments are present in the collection (Fig. 16, bottom row). When ribs and vertebrae are found, they tend to
be intact.
DISCUSSION
African crowned eagles (Stephanoaetus coronatus) are
large (3.8 kg) raptors that prefer forested habitats
throughout their range in sub-Saharan Africa. Compared
to other eagles, these birds of prey are exceptionally
strong, with powerful hindlimbs and large talons (Brown,
1971). They feed primarily on medium-sized (3–10 kg) animals, and are capable of killing and transporting prey
weighing up to 20 kg. In Africa, crowned eagles are the
only large raptors that live in rain-forest habitats, and are
frequently cited as major selective agents against forest
monkeys (Gartlan and Struhsaker, 1972; Waser, 1980;
Gautier-Hion et al., 1983; Shultz et al., 2004). A host of
factors including the speed and sudden nature of attacks,
the potential rarity of predation events, observation conditions within a closed canopy setting, habituation effects,
American Journal of Physical Anthropology—DOI 10.1002/ajpa
Fig. 6. Fragmentation profiles for all primates (a), adults only (b), immatures (c), Procolobus badius (d), Colobus polykomos (e),
Procolobus verus, (f), Cercopithecus diana (g), Cercopithecus petaurista/C. campbelli (h), Cercocebus atys (i), and Perodicticus potto (j).
American Journal of Physical Anthropology—DOI 10.1002/ajpa
158
W.S. McGRAW ET AL.
Fig. 8. Superior (a) and inferior (b) views of potto crania
from crowned eagle nests in the Tai Forest. Each specimen has
been opened at its base (b) for brain extraction.
2001, 2002, 2003; Shultz et al., 2003ab, 2004). At both
sites, the effect that eagle predation has on the primate
community, including criteria for selecting prey, was
deduced from analyses of discarded prey remains found
beneath eagle nests. The major conclusions from these
studies provide the background for the present study, and
are summarized as follows:
Fig. 7. Sample of skulls from eagle nests: superior (a) and
inferior (b) views. Note that majority of specimens have base
removed to access the brain. However, not all skulls are damaged in this way. Two similarly sized skulls recovered from
same nest differ in that one retains intact basicranium (b, first
row, second from left), while the other was opened via occipital
bone (b, second row, far left).
and the density of eagles relative to that of primate
groups, contribute to the low chance of witnessing successful predation events. The literature contains numerous reports of isolated incidents (e.g., Gautier-Hion and
Tutin, 1988; Maisels et al., 1993; Vasquez and Heymann,
2001). However, regular observations of eagle attacks in
rain-forest environments are rare. Thus, despite the recognized significance of the predator-prey dynamic
between crowned eagles and African rain-forest primates,
intensive studies of these large birds in forested habitats
were carried out at only two sites: Uganda’s Kibale Forest
(Skorupa, 1989; Struhsaker and Leakey, 1990; Mitani
et al., 2001) and the Ivory Coast’s Tai Forest (Shultz,
1. Primates comprise approximately 80% of crowned
eagle diets at Kibale, and 58% of eagle diets at Tai.
Although crowned eagles at Kibale were described as
‘‘monkey specialists’’ (Struhsaker and Leakey, 1990)
and as demonstrating a ‘‘strong preference for cercopithecids’’ (Sanders et al., 2003), this is not the case
at Tai. Monkeys comprise a large percentage of eagle
diets, not because of eagles’ preference per se, but
rather due to the relative abundance of monkeys in
the forest. When prey remains are examined using
an independent assessment of availability in the habitat (density estimates), Tai eagles demonstrate a
preference for small duikers (Cephalophus maxwelli)
and small carnivores (Crossarchus obscurus). The
only primates that occurred in the diet more than
expected were pottos, mangabeys, and Campbell’s/
lesser-spot nosed monkeys. However, as a whole, nonprimate prey were preferred to primate prey (Shultz,
2002). Additionally, a reanalysis of primate prey
assemblages (Sanders et al., 2003) using relative density estimates (Struhsaker, 1997) indicated that
ungulates are very strongly preferred at the two
Kibale sites. Thus, the notion that these raptors preferentially target cercopithecid monkeys is misleading
(Shultz et al., 2004).
American Journal of Physical Anthropology—DOI 10.1002/ajpa
EAGLE KILL REMAINS FROM TAI FOREST
159
Fig. 10. Isolated and damaged cranial bones of primarily
immature cercopithecid monkeys, including damaged occipital
bones (top two rows), parietal bones (center two rows), and frontal bones, some with attached parietals (bottom two rows).
Fig. 9. a: Lateral views of cercopithecid skulls, showing location of talon punctures in pterion region of lateral skull wall. b:
Superior view of calvaria, showing talon punctures in frontal bone
(left) and on coronal suture. c: Views of cercopithecid crania,
showing location of talon punctures within orbital cavity, including orbital floor, lateral orbital wall, and interorbital septum.
2. The overall eagle predation rate on primates was
higher in Tai than estimated at either Kibale site.
Estimated eagle predation rates on the Tai primate
species ranged between 2% (Colobus polykomos) and
13% (Cercocebus atys) of each of the cercopithecid
populations, and up to 16% of the Perodicticus population (Shultz, 2003; Shultz et al., 2004). The pro-
Fig. 11. Top row: Skullcaps and isolated parietal bones
showing V-shaped breaks from eagle beaks (see Fig. 12 in Berger
and Clarke, 1995). Center row: Isolated parietal and skullcap
with can-opener puncture and surrounding bony flaps. Bottom
row: Parietal tears in two skullcaps and isolated parietal bone.
American Journal of Physical Anthropology—DOI 10.1002/ajpa
160
W.S. McGRAW ET AL.
Fig. 12. Sample of cercopithecid and prosimian jaws recovered from eagle nests. All adult mandibles show no damage and
are intact. Only two maxillae were recovered (lower right), both
from subadult monkeys. One was broken along palate, and the
second was disassociated from face along sutural lines.
Fig. 14. Top row: Damaged cercopithecid humeri recovered
from eagle nests. Damage is concentrated at ends of diaphyses,
with shafts showing little modification. Center row: Damaged
cercopithecid ulnae recovered from eagle nests. Styloid processes of all specimens are missing, but proximal ends of bones
from larger primates are generally undamaged. Ulnar shafts
show little damage. Bottom row: Damaged radii from eagle
nests. Distal ends of all radii except that of smallest specimen
(far right) were removed. Note evidence of rodent chewing on
specimen fourth from right.
Fig. 13. Cercopithecid scapulae recovered from eagle nests.
All specimens show signs of eagle damage, ranging from isolated talon holes to (more typically) raked blades described by
Sanders et al. (2003).
jected predation rates in the two forests are dependent on the estimated eagle density. At Tai, the breeding density was based on 12 active nest sites adjacent
to our monkey study grid, whereas in Kibale, because
adjacent nest sites were unknown, the population
density was assumed to be the same as in East African open woodland (Struhsaker and Leakey, 1990;
Mitani et al., 2001). As this estimate is likely conservative, it is probable that eagle predation rates are
more comparable between the two sites than the estimates suggest.
3. At Kibale, adult male primates are overrepresented in
the sample (Mitani et al., 2001; Sanders et al., 2003).
In contrast, there is no significant difference in the
number of males vs. females found in the prey
remains for any of the individual Tai primate species.
In addition, at Tai there was no difference between
the number of adults and immature primates killed
overall or by individual species (Shultz, 2003). However, the MNI differ between the two sites, with 68
primate individuals identified from Kibale vs. 204
from Tai. Additionally, because of the small sample,
the bias toward males in Kibale was not statistically
significant, and it is not possible to discriminate
whether the bias was the result of sampling, or
reflects an actual preference by the eagles.
4. When prey taken by eagles is considered relative to
their abundance, mangabeys and pottos are killed
more often than their abundance predicts, while Procolobus badius and Colobus polykomos are generally
avoided (Shultz et al., 2003a).
Despite differences in prey selectivity between sites
(Struhsaker and Leakey, 1990; Mitani et al., 2001; Shultz
et al., 2004), patterns of bone survivability for the Tai
monkey sample are in many ways similar to those
reported for the Kibale sample from Uganda (Sanders et
al., 2003). At both sites, feeding remains discarded by
crowned eagles at their roosts are dominated by long
bones and cranial bones, while smaller bones, including
ribs, phalanges, tarsals, carpals, and vertebrae, do not
survive nearly as well. Interestingly, skulls from mediumsized primates such as guenons and small colobines do not
survive as well as those from both larger (sooty mangabeys) and smaller (potto) primates. Hindlimb bones are
more common than those of the forelimb, and elements of
the forelimb from one species (Procolobus verus) are
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EAGLE KILL REMAINS FROM TAI FOREST
161
Fig. 15. Top two rows: Innominate bones recovered from
eagle nests. All specimens were damaged along iliac crest by
raking behavior of eagles (see Sanders et al., 2003). Pubic bones
tend to be broken more often than ischia. Bottom two rows:
Sample of damaged femora collected from eagle nests. Damage
is concentrated to proximal and distal ends, with shafts exhibiting little, if any, modification. Eagles access marrow within
bones by chewing open holes in femoral heads, trochanters, and
condyles.
entirely lacking. The bias of hindlimb bones at nests
seems to be characteristic of raptors feeding on a variety
of small to medium-sized mammals throughout Africa.
For example, roosts of Verreaux’s eagles (Aquila verreauxi) in South Africa also contain greater proportions of
hindlimb bones from rock hyraxes (Cruz-Uribe and Klein,
1998). These diurnal mammals fall well within range of
body weights of both the Tai and Kibale monkeys.
Differences between sites include the absence of any
prosimian remains in the Kibale collection, and the low
survivability of mandibles associated with skulls at Tai.
Bones from neither galagos nor pottos have yet been
recovered at nests of crowned eagles at Kibale, despite the
abundance of these primates in that forest (Struhsaker,
1997). Galago remains are not present in the Tai sample.
However, potto remains are comparatively abundant, and
when the MNI of Tai Perodicticus is considered relative to
potto densities, the conclusion is that these prosimians
are preferentially hunted by crowned eagles (Shultz et al.,
2003). Few systematic data are available on the predators
of nocturnal prosimians. However, Charles-Dominique
(1977) claimed that diurnal raptors (including crowned
eagles) did not pose a significant threat to the five prosimians he studied in Gabon. Others stated that raptors
Fig. 16. Top two rows: Sample of damaged tibii collected
from eagle nests. Damage is concentrated to proximal and distal
ends, though shafts of several specimens in collection are broken. Bottom row: Sample of fibulae collected from eagle nests.
Most fragmented fibulae are broken at epiphyses, and there are
virtually no shaft fragments in collection.
generally, even nocturnal ones such as owls, are probably
not a major selective force in the lives of African prosimians (Cheney and Wrangham, 1987; Zimmerman,
1995). The composition of the Tai sample clearly indicates
that this is not the case with regard to pottos, and our
ideas about the selective impact of diurnal raptors on
small nocturnal primates require revision. Whether the
absence of galagos in the Tai assemblage is a sampling artifact or truly represents some aspect of selectivity and/or
feeding idiosyncracies on the part of crowned eagles must
await further study.
In reviewing survivability patterns, Sanders et al.
(2003; citing Lyman, 1994) noted that biases in bone fre-
American Journal of Physical Anthropology—DOI 10.1002/ajpa
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W.S. McGRAW ET AL.
quencies are unlikely due to attrition resulting from differences in bone densities. The subequal presence of skeletal elements from primates in or near nests therefore
reflects some aspect of feeding behavior, including feeding
on and processing portions of primate carcasses away
from the nest, or ingestion, digestion, and elimination of
smaller bones throughout a broader area. Detailed
accounts of dismemberment and consumption of primates
by crowned eagles are few. However, Gargett (1990)
described how Verreaux’s eagles process small and medium-sized animals. Among other things, Gargett (1990)
noted that these eagles typically ingest ribs, feet, and
most of the vertebrae. It is likely that the larger crowned
eagle feeds in a similar fashion, which explains the scarcity of these bones in the vicinity of their nests.
In many ways, damage patterns present in the Tai primates bones are similar to those described for the Kibale
sample. Immature crania are rarely found intact, while
isolated skull bones from infants and juveniles are common, resulting from fractures imposed by the great grasping strength of crowned eagles. Adult skulls that do survive are usually opened in the occipital region to access
the brain, and some, but not all, exhibit punctures from
talons and/or beaks in the pterion region, on the face, on
the vaults, or inside the orbital cavity. Mandibles of both
age classes exhibit little damage. Long bones tend to be
minimally damaged, and modifications are concentrated
at the ends of diaphyses where eagles opened the bones to
access marrow. All recovered scapulae exhibit some kind
of eagle activity, ranging from a single talon puncture
mark to (more characteristically) evidence of strong raking by eagle talons. Smaller bones that survive, including
ribs, phalanges, vertebrae, carpals, and tarsals, show little damage. The congruence of damage patterns means
that damage profiles can be reliably used to infer crowned
eagle involvement in the formation of bone assemblages,
despite site differences in prey selectivity.
Results from the present study and those for the Kibale
sample bear on our understanding the taphonomy of hominid cave sites in South Africa. Building on observations
made by Dart (1926), Berger and Clarke (1995) formulated the ‘‘bird of prey hypothesis’’ to argue that a raptor
similar to a crowned eagle was responsible for at least
part of the taphonomic assemblage at Taung including the
Taung child, Australopithecus africanus. Berger and
Clarke (1995, p. 280) compared fossil remains from Taung
with the taphonomy of modern bone assemblages from
extant eagle nests and concluded that crowned eagles
were ‘‘the best modern homologue of our hypothetical
Taung Plio-Pleistocene bird of prey.’’ Among their criteria
to identify crowned eagles as the depositional agent were:
1) the absence of large bones in the Taung sample, 2) the
high incidence of reasonably complete skulls, several of
which still have their mandibles attached, 3) the removal
of the braincase in many skulls, 4) small puncture marks
in the vaults of several skulls, 5) V-shaped marks on the
broken margins of the brain case, 6) the presence of radiating fractures on several cranial bones, 7) the frequent
crushing of skulls, 8) the presence of fractured and distorted maxillae, and 9) the presence of fractured and distorted mandibles. Sanders et al. (2003, p. 99) discussed
similarities between their Kibale sample and that from
Taung, and concluded that there was sufficient taphonomic similarity between them to ‘‘generally support an
interpretation of some contribution by large raptors to the
Taung fossil assemblage.’’
Fig. 17. Left lateral view of skulls of juvenile sooty mangabey (Cercocebus atys) (top) and adult red colobus (Procolobus
badius) (bottom), with damage from eagles accessing cranial
contents. Cranial damage is similar to that seen in several fossil
baboon skulls from Taung, as described by Berger and Clarke
(1995, Figs. 10 and 12b).
In several ways, the assemblage of primates from Tai
provides additional support for eagle involvement at the
Taung site. Taken together, the fossil and bone assemblages at Taung, Kibale, and Tai are relatively homogeneous in size and dominated by small to medium-sized
mammals; many of the skulls have their bases removed
for brain extraction; the presence of V-shaped breaks near
the broken margins of cranial vaults are common; and
many skulls are crushed. Indeed, fracture patterns in the
skulls of several primates in the Tai sample (Fig. 17)
resemble those found on fossil baboons from Taung (Figs.
10 and 12b in Berger and Clarke, 1995). One feature used
to eliminate eagles as a potential depositional candidate is
the absence of talon holes in the Taung skull (McKee,
2001; but see Fig. 13 in Berger and Clarke, 1995). The fact
that several skulls from Tai contain no talon puncture
marks means that the absence of this feature cannot be
used to eliminate eagles as potential depositional agents.
On the other hand, several significant features of the
Tai sample do not characterize either the Kibale or Taung
samples. Despite an MNI of 204, no skulls from Tai were
found with attached mandibles; we did not observe any
radiating fractures similar to those shown in Figure 10 of
Berger and Clarke (1995); and none of the mandibles are
distorted, nor are the two maxillae (although one maxilla
has been broken). Additional studies are required to establish where the presumed distinctive features of the Tai
sample fall within the range of damage inflicted by eagles
at other African sites. For example, in drier habitats, the
connective tissue on prey remains has a much longer life,
American Journal of Physical Anthropology—DOI 10.1002/ajpa
EAGLE KILL REMAINS FROM TAI FOREST
such that eagle prey remains in South Africa were found
with connective tissue attached. Thus there is a higher
probability that bones from these nests would remain
articulated in the fossil record.
Perhaps the result most significant for interpreting the
Taung fauna concerns the upper size limit of prey regularly captured by Tai crowned eagles. Several authors
used a biomechanical model of bird load-lifting capabilities to argue that large eagles could lift and carry a maximum of 6.1 kg over short distances, and that the weight
capacity of prey carried in an eagle’s talons over sustained
distances does not exceed 1.7 kg (Marden, 1990; Hedenstrom and Alerstam, 1992). On these grounds, Hedenstrom (1995) suggested that if a large raptor was responsible for killing the 12-kg hominid toddler at Taung, it
could not carry much more than the child’s skull. Sanders
et al. (2003, p. 101) added that ‘‘there is no evidence of
crowned hawk-eagles or other raptors attempting to take
infant chimpanzees, which are similar in size to the estimated body mass of 10–12 kg for the Taung child . . . at
Ngogo or elsewhere.’’ Berger and Clark (1996) responded
to Hedenstrom (1995) by noting that the 12-kg estimated
body weight for the Taung child is a maximum value, and
they provided several examples of African raptors carrying loads of up to 6 kg over varying distances.
The taphonomic assemblage from Tai bears directly on
this issue. Large colobines weighing up to 9 kg form a significant part of the Tai sample (Table 1, Fig. 2), yet adult
male sooty mangabeys averaging 11 kg have an even
greater relative abundance in the Tai assemblage and are
selectively hunted by eagles. Large, terrestrial, adult male
mangabeys would be formidable opponents for any raptor.
However, information from Tai indicates that crowned
eagle are not only capable of killing, lifting, and transporting at least portions of adult male mangabeys, but that
they routinely do so. The estimated body weight of the
Taung hominid child falls well below the upper limit of
eagle prey: eagles were observed to kill prey of up to 20 kg
(Daneel, 1979; Brown et al., 1982). Additionally, the assertions about load-lifting restrictions in eagles overlook the
hunting and prey-processing behavior of these raptors. As
they do not transport their prey whole, their load-lifting
capacity has bearing on how they process their prey, and
not on whether they are capable of killing them. Many
raptors, including crowned eagles, dismember their prey
and cache pieces before transporting them back to the nest
site (Daneel, 1979). In Tai, S.S. saw several primates that
had been recently killed by crowned eagles, and they
showed characteristic prey-processing where hair or feathers were first removed, and then the prey was eviscerated
before the head and limbs were removed. These pieces are
then cached in nearby trees and transported individually
back to the nest site. Thus, the comment by Hedenstrom
(1995) about eagles being unable to carry much more than
the skull of the Taung child in no way renders it improbable that an eagle could have killed the hominid. In fact, a
crowned eagle is known to have killed a young child (ca. 6
years old) in East Africa (Simon Thomsett, personal communication). It is therefore probable that a bird of prey
could have performed the same activities on a 3–4-year-old
hominid that probably weighed less.
CONCLUSIONS
We conclude that the taphonomic patterns of primate
bones left by crowned eagles in the Tai Forest (Ivory
Coast) are similar to those described by Sanders et al.
163
(2003) for crowned eagles in Uganda’s Kibale Forest.
Although the Tai assemblage exhibits some features not
found among the Kibale bones, patterns of survivability
and damage across the two samples are consistent. Bone
survivability is a function of eagle feeding idiosyncracies,
and is not due to characteristics of bone density. This is
generally true not only for samples of extant taxa, but also
for fossil assemblages (e.g., Pickering and Carlson, 2002)
where differences in bone-mineral density have little explanatory power.
Examining the remains from predator accumulations
offers estimates of predation effects on a primate community, and can provide taphonomic information for interpreting fossil assemblages. There is growing evidence that
multiple carnivores, including large raptors, were partially responsible for fossil bone assemblages in some hominid-bearing Plio-Pleistocene caves of South Africa (Avery
et al., 1997; Cruz-Uribe and Klein, 1998; Marean et al.,
2000; Klein and Cruz-Uribe, 2000; Pickering et al., 2004).
Fossil primates in some of these caves exhibit features
present in the feeding remains of extant African raptors
at sites in East, West, and South Africa. Further, the monkey sample from Tai is clear evidence that crowned eagles
routinely prey on large-bodied primates averaging 11 kg
(Cercocebus atys). Results from Tai, in combination with
those from Kibale (Struhsaker and Leakey, 1990; Mitani
et al., 2001; Sanders et al., 2003) and elsewhere, are therefore consistent with the hypothesis that a large predatory
bird played a role in accumulating the Taung fauna,
including the Australopithecus africanus child (Berger
and Clarke, 1995).
ACKNOWLEDGMENTS
We thank the Ministère d’Enseinment Supérieur et Recherche Scientifique, the Ministère d’Agriculture et
Ressources de Côte d’Ivoire, and the Directorate of the
Institut d’Ecologie Tropicale for permission to work in the
Tai Forest. As always, many thanks go to the Centre
Suisse de Recherche Scientifique and its director for logistical and research support. Additional research support
was generously provided by Ohio State University. We
thank all members of the Tai Monkey Project for help during all phases of this project. S.S. thanks the following
organizations for postgraduate support and financial support for the Tai Eagle Project: the Leakey Foundation,
Wildlife Conservation Society, Peregrine Fund, National
Science Foundation Graduate Assistant in Areas of
National Need Fellowship, the British Council, and the
University of Liverpool. Clark Larsen, Randall Susman,
Jeff McKee, and two anonymous reviewers provided helpful comments on an earlier version of the manuscript.
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implications, nest, coast, taphonomic, tai, south, remains, stephanoaetus, predation, ivory, coronatus, forest, early, eagle, crowned, primate, africa, hominis
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