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Oikos 124: 1391–1403, 2015
doi: 10.1111/oik.02222
© 2015 The Authors. Oikos © 2015 Nordic Society Oikos
Subject Editor: Paulo Guimares Jr. Editor-in-Chief: Dries Bonte. Accepted 11 December 2014
Carcass size shapes the structure and functioning of an African
scavenging assemblage
Marcos Moleón, José A. Sánchez-Zapata, Esther Sebastián-González and Norman Owen-Smith­
M. Moleón ([email protected]) and N. Owen-Smith, School of Animal, Plant and Environmental Sciences, Univ. of the
Witwatersrand, Wits 2050, Johannesburg, South Africa. – M. Moleón and J. A. Sánchez-Zapata, Depto de Biología Aplicada, Univ. Miguel
Hernández, Ctra. Beniel km 3.2, ES-03312 Orihuela, Alicante, Spain. – E. Sebastián-González, Depto de Ecologia, Univ. de São Paulo,
CEP 05508-900, São Paulo, Brazil.­
The particle size of the food resource strongly determines the structure and dynamics of food webs. However, the ecological implications of carcass size variation for scavenging networks structure and functioning have been largely overlooked.
Here we investigate differences in scavenging patterns due to carcass size in a complex vertebrate scavenger community, Hluhluwe-iMfolozi Park, South Africa, while taking into account seasonality. We monitored the consumption of
three types of experimental carcasses: ‘small’ ( 10 kg), ‘medium’ (10–100 kg) and ‘large’ ( 100 kg). We employed
general lineal models to explore the influence of carcass size on 1) scavenging network structure (scavenger species richness
per carcass) and 2) functioning (carcass detection time, consumption time, consumption rate and percentage of carrion
consumed). We also tested whether the structure of the scavenging network of each carcass size was nested, i.e. whether the
scavenging assemblage in species-poor carcasses was a subset of the assemblage consuming species-rich carcasses. We found
strong evidence indicating that carcass size is a major factor governing the associated scavenger assemblage. Scavenger
species richness per carcass and carcass consumption time and rate increased with carcass size, while carcass detection time and
percentage of carrion biomass consumed were negatively related to carcass size. Strikingly, most of the carrion biomass was
consumed by facultative scavengers, represented by large mammalian carnivores, rather than by obligate scavengers (i.e.
vultures). Scavenging network nestedness tended to be higher at larger carcasses, and nestedness was sensitive to the
removal of the most connected species in the network (spotted hyena) rather than vultures. When comparing scavenging and predation assemblages, crucial size-dependent differences emerge. Also, we identified a traditionally ignored
mechanism by which hunting large prey could be relatively less profitable for predators, namely the costs associated with
competition from scavengers and decomposers.
The importance of scavenging in community and food web
ecology and evolution has not been fully recognized until
quite recently (DeVault et al. 2003, Wilmers et al. 2003,
Selva et al. 2005, Selva and Fortuna 2007, Wilson and
Wolkovich 2011, Beasley et al. 2012, Barton et al. 2013,
Moleón et al. 2014a, b, Pereira et al. 2014). Neglecting the
direct and indirect interactions involving carrion could lead
to serious misinterpretations within food-web and energy flux
models (Wilson and Wolkovich 2011, Moleón et al. 2014a).
Understanding the factors that affect carcass use by scavenging animals therefore has wide ramifications for biodiversity
conservation and management (DeVault et al. 2003, Wilson
and Wolkovich 2011, Moleón et al. 2014a, b). Scavenging
patterns may depend on features of the carcass (e.g. cause
of death, spatio-temporal distribution), the consumer (e.g.
body size, sociality, circadian activity) or extrinsic variables
(e.g. weather conditions, availability of other food resources,
micro-habitat structure; DeVault and Rhodes 2002, DeVault
et al. 2003, 2004, Selva et al. 2003, 2005, Wilson and
Wolkovich 2011, Kendall et al. 2012, Olson et al. 2012,
Ruzicka and Conover 2012, Sebastián-González et al.
2013, Moleón et al. 2014a). However, scientific knowledge
about the relative contribution of each influence is still very
limited.
One of the major factors that may govern scavenging
patterns by vertebrates worldwide is carcass size (DeVault
et al. 2003, Sebastián-González et al. 2013, Moleón et al.
2014a). Prey (in a wide sense) size is closely associated with the
strength and direction of inter-specific interactions, which in
turn determine the structure and dynamics of food webs and
other ecological networks (Woodward et al. 2005). Prey size
has been a matter of research for many years in fields such as
the ecology of predation (Cohen et al. 1993, Sinclair et al.
2003, Owen-Smith and Mills 2008). However, although
terrestrial vertebrate carcasses span a very wide size range,
from a few grams (e.g. shrews) to several metric tons (e.g.
rhinoceroses and elephants), hardly any study has explicitly
explored the ecological implications of food particle size in a
scavenging context (but see DeVault et al. 2004). Recently,
Sebastián-González et al. (2013), who studied patterns of
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consumption of lagomorph carcasses, hypothesized that
larger carcasses may be partitioned between more scavenger
species, promoting facilitative and competitive processes that
might eventually lead to more organized (e.g. nested) scavenging networks. A nested scavenging pattern arises when
the assemblages of scavengers feeding on carcasses visited
by few scavengers are subsets of the scavenger assemblages
of carcasses visited by many scavengers (Selva and Fortuna
2007). This is supported by both theory (Moleón et al.
2014a) and findings of field studies that used ungulate
carcasses, where inter-specific interactions among several
carrion consumers were frequent (Cortés-Avizanda et al.
2012) and the scavenging pattern was indeed clearly nested
(Selva and Fortuna 2007). This contrasts with the pattern
identified for predator–prey relationships among large mammals, because smaller ungulates are killed by more species of
carnivore than larger ones (Sinclair et al. 2003). Regarding
scavenging efficiency, DeVault et al. (2004) found that the
probability of carcass removal by vertebrates was higher for
large than for small rodent carcasses. These authors suggested
that this is because larger carcasses are more conspicuous (i.e.
easier to find) and comparatively less exploited by decomposers due to a lower surface:volume ratio. These patterns
need further empirical support taking into account wider
variation in carcass size.
Besides carcass size, the structure and functioning of
scavenger communities can also vary between seasons. Most
mammalian carnivores, as well as avian meso-carnivores
such as raptors and corvids, are opportunistic or ‘facultative
scavengers’, as they shift from hunting to scavenging
depending on the opportunities presented (DeVault et al.
2003, Wilson and Wolkovich 2011, Moleón et al. 2014a,
Pereira et al. 2014). Among terrestrial vertebrates, only the
vultures are ‘obligate scavengers’, totally dependent on carrion as their food resource (Moleón et al. 2014a). Scavenging
opportunities for facultative scavengers depend strongly on
seasonal variation in prey susceptibility to mortality (Pereira
et al. 2014). Seasonal shifts in access to carrion by facultative
scavengers can change the scavenging rates of not only facultative scavengers (Wilmers et al. 2003, Selva et al. 2005), but
also of vultures through a wide array of direct and indirect
interactions (Moleón et al. 2014a). During the dry season,
less vegetation cover might also favor the detection of carrion
by scavengers, especially mammals (Ruzicka and Conover
2012). However, seasonal changes in scavenging patterns
have largely been ignored in the scientific literature.
The general goal of our study was to investigate
differences in scavenging patterns due to carcass size in a
complex African vertebrate scavenger community. We
addressed three main questions: 1) is the scavenging network
richer in species, and more nested, as carcass size increases?
2) Is consumption efficiency a function of carcass size? 3)
Do the scavenging network and the consumption efficiency
differ seasonally? We hypothesize that both the assemblage
structure and functioning may be carcass size-dependent.
Our predictions are that larger carcasses will be exploited by
a greater number of scavenger species, and that the scavenging network exploiting larger carcasses will be more nested
than that utilizing smaller carcasses. In turn, more species and
more organized assemblages could lead to higher consumption rates. Regarding seasonality, we expect that carcasses are
1392
detected earlier during the dry season when compared with
the wet season. Based on our findings, we discuss potential
structural differences between scavenging and predation
networks.
Material and methods
Study area
Hluhluwe-iMfolozi Park (HiP hereafter) is located in the
KwaZulu-Natal province of South Africa (28°00′–28°26′S,
31°43′–31°09′E). HiP is a ca 900 km2 wildlife reserve ranging from 60 to 750 m a.s.l., being hilly in the northern section
(Hluhluwe) and flatter in the south (iMfolozi). Mean annual
precipitation ranges from 985 mm in Hluhluwe to around
600 mm in parts of iMfolozi. The majority of rainfall occurs
in the summer months, from October to March. Perennial
surface water is irregularly available in the Hluhluwe River in
the north, and the Black and White Umfolozi Rivers in the
south. As a result of both topography and rainfall, there is a
north-to-south contrast in vegetation, from grassland-forest
mosaic with extensive thickets to thorn savannah (Grange
et al. 2012). Long-distance movements of herbivores are prevented by boundary fences, and neither severe droughts nor
disease outbreaks took place during our study period.
Herbivore and scavenger assemblages
HiP retains a rich assemblage of vertebrate herbivores and
carnivores. Ungulates ranged in size from 10 kg steenbok
Raphicerus campestris to rhinoceroses Ceratotherium simum
and Diceros bicornis and elephants Loxodonta africana weighing several metric tons, but with the greatest numeric abundance represented by antelopes in the size range 50–500
kg. Large mammalian carnivores included spotted hyena
Crocuta crocuta, lion Panthera leo, African wild dog Lycaon
pictus, leopard P. pardus and cheetah Acynomix jubatus. The
most frequent mammalian meso-carnivores and omnivores
were large-spotted genet Genetta tigrina, various mongooses
Ichneumia albicauda, Galerella sanguinea and Mungos mungo,
and bushpig Potamochoerus larvatus. Reptilian carnivores
included Nile crocodile Crocodylus niloticus and two monitor
species Varanus albigularis and V. niloticus. At least 17 species
of birds of prey (Family Accipitridae excluding vultures) and
two corvids Corvus albus and C. albicollis are commonly seen
in the reserve. Among vultures, the white-backed vulture
Gyps africanus is relatively abundant, while the lappet-faced
vulture Aegypius tracheliotos and white-headed vulture
A. occipitalis are uncommon. The Cape vulture G. coprotheres,
hooded vulture Necrosyrtes monachus and palm-nut vulture
Gypohierax angolensis are present only occasionally (Howells
et al. 2009–2013, Moleón unpubl.). Most of the scavenging
birds were resident year-round, but yellow-billed kites Milvus
aegyptius were present only during the wet season.
Study design and data sampling
Between 2010 and 2012, we investigated carcass consumption patterns by the vertebrate scavenger community of HiP.
We provided three types of experimental carcasses differing
categorically in size: ‘small’ ( 10 kg), ‘medium’ (10–100 kg)
and ‘large’ ( 100 kg). For small carcasses, we used six-week
old, dirty white feathered chickens weighing ca 2 kg (n  21).
For medium-sized carcasses (n  12) we used either impalas
Aepyceros melampus(weight: 40–55 kg, four adult males) or
nyalas Tragelaphus angasi (weight: 40–120 kg; three adult
males, three adult females, one juvenile male and one yearling female). Large carcasses (n  8) were constituted by blue
wildebeest Connochaetes taurinus (weight: 290 kg; one adult
male), African buffalo Syncerus caffer (weight: 354–650 kg;
one adult male and two adults of unknown sex), white rhino
(weight: 2000 kg; one adult male) and elephant (weight:
4000 kg; three adult males or part thereof ). Six additional
chickens, one impala, two nyala, one buffalo and two wildebeest carcasses were not included in the analyses because of
camera failure. Carcasses were located randomly across the
reserve, except for five large carcasses left where the animals
had died. Chickens were distributed over the same locations
as larger carcasses, after an interval of  5 months. Most
carcasses were intact when the camera was activated, except
for six large carcasses. Five of these were monitored  10 h
after scavengers had started to eat while the sixth consisted
of two legs without skin of a poached elephant (weight: 600
kg). Carcasses were equitably distributed between seasons
(Table 1), and always in sites with intermediate vegetation
cover (Ruzicka and Conover 2012). All carcasses but the
elephant and rhino carcasses (i.e. the heaviest ones) were
fixed to the ground or a tree trunk by means of wires or
chains to prevent scavengers from moving the carcass away
from the camera focus. Plant material was used to hide the
fixing devices. Carcasses were placed randomly in time
between dawn and dusk.
Carcasses where monitored using automatic cameras activated by movement. Cameras were located in discreet places
close to the carcasses (5–10 m away), and the intervening
area was cleaned of grass and shrubs in order to ensure good
visibility for the pictures. Cameras were programmed to
take one picture every two minutes, provided that there was
some movement, and worked 24 h a day (see Blázquez et al.
2009 for further details). Cameras were collected seven days
after their activation or following complete consumption of
the carcass. We considered a carcass to be totally consumed
when only parts of the skeleton (head and big bones) were
left or if taken away from the camera focus by a large scavenger. In the last case, we only considered carcasses in which
the part taken was small enough to be consumed completely
by the scavenger, usually a hyena.
From the pictures we calculated the following variables
related to scavenger species diversity: ‘richness’ (number of
scavenger species per carcass) and ‘total richness’ (total number
of scavenger species in all carcasses). For some purposes, we
grouped scavenger species as ‘obligate scavengers’ (OS; i.e. vultures) and ‘facultative scavengers’ (FS; avian, mammalian and
reptilian carnivores). Facultative scavengers were further separated in ‘large facultative scavengers’ (LFS; i.e. lion, leopard,
cheetah, hyena, wild dog and crocodile) and ‘meso facultative
scavengers’ (MFS; all of the smaller carnivores). Furthermore,
MFS were separated in ‘avian facultative scavengers’ (aFS) and
‘mammalian facultative scavengers’ (mFS; we did not use the
category ‘reptilian facultative scavengers’ because reptiles –
crocodiles – only appeared at one large carcass).
Regarding scavenging efficiency, we estimated for each
carcass: ‘carcass detection time’ (time elapsed since the
carcass was available until the arrival of the first scavenger), ‘carcass consumption time’ (time elapsed between
when the carcass became available and its complete
consumption), ‘carcass consumption rate’ (carrion biomass
consumed by scavengers divided by carcass consumption
time), and ‘percentage of carrion consumed’ (percentage
of the carcass, excluding the stomach content, consumed
by the scavengers). The stomach content was estimated
as 5% and 10% of the total carcass weight for chickens
and ungulates (Selva 2004), respectively. Non-consumed
parts were estimated visually from the camera pictures
and inspections of the carcass sites at the moment of the
camera inactivation as a proportion. We calculated the
biomass consumed by each scavenger group using the
carcass weight without the stomach content and nonconsumed parts, the information provided by the pictures,
the maximum food intake of each scavenger species (Estes
1992, Donázar 1993) and the minimum number of different individuals of each species at the carcass. Initial carcass
weight was 2 kg for chickens. For ungulates the body mass
was obtained from the literature taking into account sex
and age (Supplementary material Appendix 1 Table A1).
Statistical analyses
First of all, we constructed species richness curves with
BiodiversityPro (James and McCulloch 1990) to assess
whether our sample size was sufficient to detect all the
species that scavenge on a given carcass type. Species richness
analysis (Magurran 1991) randomly pools the samples and
examines how specific indicators accumulate as the samples
are pooled. We plotted a graph of the species richness (i.e.
number of scavenger species) against the number of pooled
samples (i.e. carcasses). The samples are pooled from left
to right. When an asymptote is reached all the species that
Table 1. Number of carcasses monitored and recorded pictures per carcass type. Small carcasses were placed during the winter–summer
transition. Scavenger species richness recorded at each carcass type is also shown, measured as mean richness (mean number of scavenger
species per carcass) and total richness (total number of scavenger species). Note that the sum of species found in all carcass types excludes
redundant species.
n
Carcass size
Small
Medium
Large
Total
Winter
Summer
Total
8
7
4
19
13
5
5
23
21
12
9
42
Mean no. of
pictures ( SD)
16.62  15.51
67.00  54.28
469.13  372.48
Total no. of
pictures
349
813
3753
4915
Mean
richness ( SD)
Total
richness
1.95  1.12
2.83  1.40
4.75  1.83
14
9
11
18
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scavenge on a given carcass type are supposed to have been
detected and no further sampling is required.
Then we tested whether scavenger species richness was
related to carcass size, season and section of HiP. To do so,
we fitted generalized linear models (GLMs) where ‘richness’ was the response variable, and ‘carcass size’ (small,
medium and large), ‘hour’ of carcass placement (morning
– from dawn to 12:00 h – and afternoon – from 12:00 h to
dusk), ‘season’ (wet and dry) and ‘section’ (Hluhluwe and
iMfolozi) were the categorical predictors. Within each of the
two sections of HiP, the management history, topography,
precipitation, vegetation and faunal composition (including vertebrate herbivores, carnivores and vultures) is quite
homogeneous (Brooks and Macdonald 1983, Grange et al.
2012). Thus, the variable ‘section’ probably captures the bulk
of the spatial variation component of our data. We evaluated
the complete set of models with four or less parameters (in
order to guarantee at least 10 observations per parameter)
that includes these three explanatory variables. We used Poisson error distributions and log link functions. Model selection was based on Akaike’s information criterion for small
sample sizes (AICc). This approach allows the most parsimonious model (lowest AICc) to be identified and ranks the
remaining models. Delta AICc (ΔAICc) was calculated as the
difference in AICc between each model and the best model
in the set. We considered models with ΔAICc  2 to have
similar support (Burnham and Anderson 2002). Following
Burnham and Anderson (2004), we computed the Akaike
weights (AICcw) for the set of models (ΔAICc  2) to assess
the weight of evidence in favor of each candidate model.
To explore the overall degree of support for the candidate
models we also calculated their proportion of explained
deviance (D2) according to this formula: D2  (null deviance – residual deviance) / null deviance  100 (Burnham
and Anderson 2002).
We also explored the scavenging network structure
separately for small, medium and large carcasses. In particular, we investigated whether the pattern of consumption of
each carcass size by the scavenger community was nested.
Given that scavenger species richness was only weakly related
to season (Results), we combined data from the wet and dry
seasons for this purpose. To analyze nestedness, we constructed a binary matrix for each carcass type where each
column represents a different scavenger species and each row
represents a different carcass. The matrix cells aij  1 when
the scavenger i used the carcass j and zero otherwise. We
used the ANINHADO software (Guimarães and Guimarães
2006), which uses a metric developed by Almeida-Neto et al.
(2008) called NODF (acronym for nestedness metric based
on overlap and decreasing fill). This metric has been identified to be good for any type of nestedness analysis (Ulrich
et al. 2009). The metric tends to 100 for highly nested communities, while random matrices will show intermediate
NODF values. As nestedness may arise from a random community, ANINHADO compares the NODF value of each
assemblage with the NODF of 1000 matrices constructed
following a null model. The null model considers that the
probability that any cell aij shows a presence is: (Pi / C 
Pj / R) / 2, where Pi is the number of presences in row i, Pj
is the number of presences in column j, C is the number of
columns, and R is the number of rows. We compared the
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degree of nestedness between carcass size categories using a
standardized effect size (SES) of the NODF value. This measure indicates the number of standard deviations that the
observed index is above or below the mean index of simulated
matrices. We calculated the SES as a Z-score (Z  observed
NODF – mean simulated NODF / SD simulated NODF).
Z-scores  0 indicate that the nestedness in a site was greater
than the median nestedness of randomized matrices, while
Z-scores  0 indicate that nestedness in a site was lower than
the median nestedness of randomized matrices. We then
re-calculated all these measures for each carcass size, but
excluding 1) the vultures and 2) the most connected
species (i.e. the species that appeared in more carcasses,
whether vulture or not) from the community to evaluate
if the impact of the major scavenger species on network
structure varies with carcass size.
In addition, we calculated quantitative matrices to
compare species specialization in small, medium and large
carcasses. First, to obtain a quantitative interaction matrix
of the scavenging network, we calculated the minimum
number of different individuals of each species that were
present in each picture (n  4915 pics; Table 1). Then, we
created matrices Q for each carcass type where each cell Qij
represented the number of individuals of the species i that
were photographed in the carcass j. Second, we calculated
the degree of specialization of each species on small, medium
and large carcasses. We used the d’ specialization index of
Blüthgen et al. (2006) derived from the Shannon diversity
index. This index ranges between 0 (no specialization) and
1 (perfect specialist). In our system, a species is highly
specialized if it was found consuming a carcass that no one
else consumed, and its specialization is low if it consumed
carcasses that were also exploited by other species.
To ascertain whether carcass size, season and section
affected carcass consumption efficiency, we fitted GLMs
where ‘detection time’, ‘consumption time’, ‘consumption
rate’ and ‘percentage of carrion consumed’ were the response
variables, and ‘carcass size’, ‘hour’, ‘season’ and ‘section’ were
the categorical predictors. In this case, we used Gaussian
error distributions and identity link functions. Model evaluation and selection was performed as explained above. All
the GLMs were done in R 3.0.2 ( www.R-project.org/ ).
Results
Community richness and structure
We detected a total of 18 vertebrate scavenging species
(Supplementary material Appendix 1 Table A2), with the
highest total species richness associated with small carcasses
(Table 1, Fig. 1). Species richness curves showed that sampling effort was probably sufficient to identify most scavenger species of small and medium-sized carcasses, but that
additional sampling would have detected more scavenger
species at large carcasses (Supplementary material Appendix 1
Fig. A1). Scavenger richness per carcass clearly increased
with carcass size (Table 1), as revealed by the GLM analyses:
carcass size was included in the two best models (Table 2, 3).
The most supported model also included season as predictor of scavenger richness (slightly more richness in the dry
Figure 1. Spotted hyenas Crocuta crocuta (A), lions Panthera leo (B) and white-backed vultures Gypsafricanus (C) dominated both mediumsized and large carcasses, while meso-facultative scavengers such as large-spotted genets Genetta tigrina (D), white-tailed mongooses
Ichneumia albicauda (E), slender mongooses Galerella sanguinea (F), and tawny eagles Aquila rapax (G) were frequent in small carcasses. All
pictures were obtained by automatic cameras during the fieldwork of this study.
Table 2. AICc-based model selection to assess the effect of carcass size (small, medium and large), hour of carcass placement (morning and
afternoon), season (wet and dry) and section of the study area (Hluhluwe and iMfolozi) on the richness (number of species) of scavengers per
carcass and the scavenging efficiency (detection time, consumption time, consumption rate and percentage of carrion biomass consumed)
in Hluhluwe-iMfolozi Park, South Africa. Number of estimated parameters (k), AICc values, AICc differences (∆AICc) with the highest ranked
model (i.e. the one with the lowest AICc), Akaike weights (AICcw) and the variability of the models explained by the predictors (deviance, D2)
are shown. Selected models are in bold.
Response variable
Model
k
AICc
∆AICc
AICcw
D2
Scavenger richness
size  season
size
size  season  hour
size  season  section
size  section
size  section  hour
season
season  section
season  hour
size  hour
section
hour
season  section  hour
section  hour
size  season  hour
size  season
size  season  section
season
season  hour
size  hour
size
season  section  hour
season  section
size  section  hour
size  section
hour
section
section  hour
size
size  hour
size  section
size  season
3
2
4
4
3
4
1
2
2
3
1
1
3
2
4
3
4
1
2
3
2
3
2
4
3
1
1
2
2
3
3
3
142.11
143.70
144.55
144.57
146.03
148.49
152.61
154.43
154.82
155.74
156.11
156.45
156.76
158.31
349.69
349.93
352.30
355.25
355.27
355.74
356.34
356.80
357.12
357.96
358.67
360.55
363.00
362.12
435.60
436.26
436.72
437.71
0.00
1.59
2.44
2.46
3.92
6.38
10.50
12.32
12.71
13.63
14.00
14.34
14.65
16.20
0.00
0.24
2.61
5.56
5.58
6.05
6.65
7.11
7.43
8.27
8.98
10.86
13.31
12.43
0.00
0.66
1.12
2.11
0.689
0.311
47.81%
37.90%
0.530
0.470
41.01%
36.73%
0.437
0.314
0.249
46.64%
48.84%
48.26%
Detection time
Consumption time
Continued
1395
Table 2. Continued.
Response variable
Consumption rate
% of carrion biomass consumed
Model
k
AICc
∆AICc
size  section  hour
size  season  hour
size  season  section
section
hour
season
season  section
section  hour
season  hour
season  section  hour
size
size  season
size  hour
size  section
size  season  hour
size  section  hour
size  season  section
section
hour
season
section  hour
season  section
season  hour
season  section  hour
size
size  section  hour
size  section
size  hour
section  hour
section
size  season
size  season  section
hour
size  season  hour
season  section  hour
season  section
season
season  hour
4
4
4
1
1
1
2
2
2
3
2
3
3
3
4
4
4
1
1
1
2
2
2
3
2
4
3
3
2
1
3
4
1
4
3
2
1
2
437.89
438.56
439.01
457.05
457.83
457.98
458.79
458.83
459.59
460.76
161.36
162.88
162.88
163.47
164.60
164.91
165.03
184.41
184.41
184.94
185.73
186.48
186.55
187.99
31.32
31.23
31.16
30.60
30.33
29.58
28.99
28.73
28.51
28.12
28.03
27.47
26.68
26.30
2.29
2.96
3.41
21.45
22.23
22.38
23.19
23.23
23.99
25.16
0.00
1.52
1.52
2.11
3.24
3.55
3.67
23.05
23.05
23.58
24.37
25.12
25.19
26.63
0.00
0.09
0.16
0.72
0.99
1.74
2.33
2.59
2.81
3.20
3.29
3.85
4.64
5.02
season; Table 3), although the contribution of season to the
deviance of the model was low (20.72%) if compared with
the contribution of carcass size (79.28%). The section of the
reserve where the carcass was located did not exert any influence (Table 2).
Meso-mammalian carnivores and birds of prey were the
species more frequently visiting small carcasses, while large
carcasses were visited typically by large facultative scavengers
such as hyenas (present at 47.60%, 83.33% and 100% of
small, medium and large carcasses, respectively) and lions
(4.83%, 41.70% and 62.50%). Vultures and avian facultative
scavengers became more frequent as carcass size increased. In
contrast, mammalian meso-carnivores were absent at medium-sized and large carcasses (Fig. 2).
Scavenging network structure was unaffected by carcass
size, but nestedness tended to be higher at larger carcasses
(Table 4). In fact, when considering medium-sized and large
carcasses together (total n  21 carcasses, i.e. same n as small
carcasses), the scavenging network was clearly nested. The
removal of vultures and the most connected species (always
the spotted hyena) produced no significant effect on the
scavenging network structure if compared with the models
1396
AICcw
D2
0.517
0.242
0.242
47.66%
48.74%
48.74%
0.217
0.208
0.200
0.151
0.132
0.091
15.86%
25.24%
20.33%
19.20%
13.75%
7.11%
that included such species, unless medium-sized and large
carcasses were joined. In this case, hyena removal, but not
vulture removal, led to a significant loss of nestedness, suggesting that the hyena was mainly responsible for the nestedness of the assemblage (Table 4). Moreover, we found a
negative relationship between species specialization and
carcass size: d’  0.606  0.206 (range: 0.232–0.875) for
small carcasses; d’  0.387  0.323 (range: 0.040–0.880) for
medium carcasses; d’  0.307  0.185 (range: 0.000–0.635)
for large carcasses. Basically, this means that larger carcasses
are shared by more species than smaller ones.
Community functioning
Carrion consumption efficiency was dependent on carcass
size: detection time was three times longer for small than for
large carcasses; consumption time was nearly four times longer for large than for small carcasses; consumption rate was
33 times higher for large than for small carcasses; percentage
of carrion biomass consumed was slightly higher for small
than for large carcasses (Table 5). GLM analyses supported
this conclusion, as size was included in the great majority of
Table 3. Selected generalized lineal models (GLMs) showing the relation between scavenger richness and scavenging efficiency (detection
time, consumption time, consumption rate and percentage of carrion biomass consumed) and carcass size, hour of carcass placement season
and section of the study area. The estimate of the parameters (including the sign), the standard error of the parameters (SE) and the degrees
of freedom of the models (DF) are shown.
Response variable
Scavenger richness
Model
size  season
size
Detection time
size  season  hour
size  season
Consumption time
size
size  hour
size  section
Consumption rate
size
size  season
size  hour
% of carrion biomass consumed
size
size  section  hour
size  section
size  hour
section  hour
section
Parameter
Intercept
size (medium)
size (small)
season (wet)
Intercept
size (medium)
size (small)
Intercept
size (medium)
size (small)
season (wet)
hour (morning)
Intercept
size (medium)
size (small)
season (wet)
Intercept
size (medium)
size (small)
Intercept
size (medium)
size (small)
hour (morning)
Intercept
size (medium)
size (small)
section (iMfolozi)
Intercept
size (medium)
size (small)
Intercept
size (medium)
size (small)
season (wet)
Intercept
size (medium)
size (small)
hour (morning)
Intercept
size (medium)
size (small)
Intercept
size (medium)
size (small)
section (iMfolozi)
hour (morning)
Intercept
size (medium)
size (small)
section (iMfolozi)
Intercept
size (medium)
size (small)
hour (morning)
Intercept
section (iMfolozi)
hour (morning)
Intercept
section (iMfolozi)
Estimate
1.778
 0.595
0.891
0.379
1.558
0.517
0.889
4.475
13.109
26.992
18.503
10.018
0.566
11.653
26.556
19.358
182.990
106.610
129.800
191.94
105.12
130.80
20.89
172.82
106.82
127.26
17.97
4.454
3.283
4.317
4.802
3.428
4.363
0.487
4.250
3.317
4.294
0.477
0.791
0.040
0.151
0.869
0.046
0.136
0.081
0.074
0.831
0.041
0.141
0.069
0.817
0.045
0.148
0.060
0.968
0.098
0.085
0.926
0.086
SE
DF
0.192
0.239
0.225
0.192
0.162
0.236
0.225
9.321
9.861
8.978
6.410
6.381
9.169
10.021
0.159
6.519
19.850
24.980
22.920
20.97
24.82
22.76
16.77
22.01
24.93
23.01
16.77
0.644
0.810
0.744
0.760
0.830
0.748
0.561
0.688
0.814
0.747
0.550
0.058
0.073
0.067
0.067
0.071
0.065
0.048
0.048
0.063
0.072
0.066
0.048
0.061
0.073
0.067
0.049
0.043
0.050
0.050
0.036
0.050
37
38
34
35
37
36
36
37
36
36
37
35
36
36
37
38
1397
Figure 2. Scavenger species richness per scavenger group in small, medium-sized and large carcasses. Values represent mean  SD number
of scavenger species per carcass (total number of scavenger species is given in parenthesis). Bubble diameter is proportional to mean values.
OS: obligate scavengers (i.e. vultures); FS: facultative scavengers; LFS: large facultative scavengers; MFS: meso facultative scavengers; aFS:
avian facultative scavengers; mFS: mammalian facultative scavengers.
Table 4. Nestedness degree of the scavenger network per carcass
size and scenario (total network, total network without vultures, and
total network without the most connected species), as indicated by
the NODF metrics. NODF1: nestedness of the observed matrix;
NODF2: mean nestedness of the 1000 matrices simulated under
the null model; Z-score: NODF standardized with the average
nestedness of simulated matrices. Significant results are in bold (see
main text for details).
Network
Small carcasses
total
without vultures
without most
connected spp.
Medium-sized
carcasses
total
without vultures
without most
connected spp.
Large carcasses
total
without vultures
without most
connected spp.
Medium-sized 
large carcasses
total
without vultures
without most
connected spp.
1398
NODF1
NODF2  SD p-value
Z-score
20.65
22.51
13.94
17.13  4.00 (0.19)
20.56  4.49 (0.33)
13.64  3.72 (0.43)
0.879
0.434
0.081
51.93
47.06
28.30
39.90  7.68 (0.06)
45.75  9.28 (0.44)
28.04  7.39 (0.46)
1.566
0.141
0.035
63.29
51.79
53.49
51.76  7.99 (0.07)
44.87  10.25 (0.25)
46.03  8.84 (0.19)
1.443
0.675
0.844
57.63
51.77
38.98
40.31  5.26 ( 0.01)
39.86  6.55 (0.04)
32.67  5.23 (0.12)
3.290
1.818
1.206
the selected models. Moreover, the model with size only was
the model with the lowest AICcw for consumption time, consumption rate and percentage of carrion biomass consumed
(Table 2, 3). The hour of carcass placement exerted some
influence on all the variables related to carrion consumption
efficiency (Table 2): detection time, consumption time and
percentage of carrion biomass consumed were lower, and
consumption rate was higher, when carcasses were placed in
the morning (Table 3). Detection time and consumption rate
were also explained by season (Table 2): detection time was
considerably longer in the wet season, while consumption
rate was slightly higher in the dry season (Table 3). We also
detected some influence of the park section on consumption efficiency: consumption time was slightly higher and
percentage of carrion consumed lower in iMfolozi compared
to Hluhluwe (Table 2, 3).
Most of the carrion biomass available was consumed by
facultative scavengers, especially large mammalian carnivores. Among them, hyenas were the main carrion consumers (44.59%, 48.52% and 46.83% of the biomass of small,
medium-sized and large carcasses, respectively), followed by
lions (0.64%, 32.15% and 23.46%). Both avian and mammalian meso-facultative scavengers consumed a considerable proportion of small carcasses. Vultures consumed near
20% of the medium-sized and large carcasses, but less than
5% of small carcasses (Fig. 3). From the pictures, the role of
microbial and invertebrate decomposers in carrion biomass
removal was negligible.
Table 5. Consumption efficiency of each carcass type, measured as detection and consumption times (h), consumption rate (kg h1) and
percentage of carrion biomass consumed. All values represent mean  SD (minimum-maximum).
Carcass size
Small
Medium
Large
Detection time
Consumption time
Consumption rate
% of carrion consumed
39.11  25.80 (0.50–82.83)
20.29  17.95 (1.12–55.22)
13.47  7.52 (0.75–22.98)
53.18  28.86 (1.58–104.67)
76.38  36.50 (18.80–117.17)
182.99  108.57 (21.73–419.12)
0.14  0.31 (0.012–1.171)
1.17  1.13 (0.30–4.05)
4.45  3.91 (0.78–12.06)
94.22  10.05 (52.26–97.37)
90.67  3.14 (87.00–100)
79.14  11.68 (50.00–89.00)
Discussion
In accordance with our expectations, we found strong
evidence that carcass size was a major factor governing
the structure and functioning of scavenging assemblages.
Scavenger species richness, scavenger network nestedness
and all measures of scavenging efficiency (detection and consumption times, consumption rate and percentage of carrion
biomass consumed) were influenced by the range in carcass
size covered by our study, which varied in three orders of
magnitude (from ca 2 kg to ca 4000 kg).
The mean number of scavenger species exploiting a
particular carcass increased with carcass size, probably because
the longer temporal availability and higher conspicuousness
of larger carcasses (DeVault et al. 2004) allowed more species to aggregate. However, the frequency of occurrence of
small mammalian scavengers did not increase with carcass
size, perhaps because large carcasses were perceived as high
predation risk sites by mongooses and genets due to frequent
large-predator presence. In other words, ungulate carcass
sites may act as ‘hills’ or ‘hot spots’ in the ‘landscape of fear’
of these meso-carnivores (Laundré et al. 2001, Willems and
Hill 2009). This is in line with other studies that found lower
herbivore densities in the vicinities of dead ungulates due to
higher predator occurrence (Cortés-Avizanda et al. 2009).
Big predators have been recognized to limit meso-predator
abundance through different intraguild interactions (Ritchie
and Johnson 2009), but limiting the access to high quality
food resources such as large carcasses has been overlooked.
Our results regarding nestedness support the hypothesis
of Sebastián-González et al. (2013): the larger the carcass,
the more the interacting species and the more nested the
scavenging network. Nestedness was only significant after
combining medium-sized and large carcasses, although
larger sample sizes would probably have led to nested
patterns for each carcass size separately (Table 4). One of
the probable factors favouring the nestedness–carcass size
relationship is the higher number of scavengers associated
Figure 3. Percentage of the total carrion biomass consumed per scavenger group in small, medium-sized and large carcasses. Bubble
diameter is proportional to percentages. OS: obligate scavengers (i.e. vultures); FS: facultative scavengers; LFS: large facultative scavengers;
MFS: meso facultative scavengers; aFS: avian facultative scavengers; mFS: mammalian facultative scavengers.
1399
with larger carcasses. However, this condition is not enough
to explain nestedness. The null models partially accounted
for the differences in matrix size by comparing the nestedness
of the empiric matrix with that of randomly created matrices
that preserved the number of species, carcasses and proportion of interactions. Thus, our analyses indicate that, besides
the possible passive sampling effects, scavenger communities
in large carcasses present a more organized structure than
those in the small ones, probably due to the intervention of
a sort of inter-specific interaction (Sebastián-González et al.
2013). Theoretical studies suggest that nested structures
may reduce effective competition in the community (at least
in mutualistic assemblages; Okuyama and Holland 2008,
Bastolla et al. 2009, Sugihara and Ye 2009, Rohr et al. 2014).
In such a case, the nested structure of the larger carcasses
scavenging network could minimize the negative effects of
competitive interactions and promote scavenger diversity to
some extent. Moreover, our results indicate that nestedness
in scavenging assemblages is sensitive to the most connected
species in the network rather than to obligate scavengers,
given that the virtual removal from the network of hyenas,
but not vultures led to a loss of nestedness. This suggests
that hyenas were involved in some interactions that enhance
community structure, such as carcass signaling and tearing
open of thick-skinned animals (Moleón et al. 2014a). It
also indicates that the extinction of the spotted hyena might
trigger important structural changes in the studied scavenging assemblage. The dependence of nestedness on the most
connected species is also a feature of mutualistic networks
(Saavedra et al. 2011).
Cortés-Avizanda et al. (2012) have recently highlighted
the importance of spatiotemporal unpredictability of carrion availability in promoting species diversity in scavenger
guilds, but the relationship between resource unpredictability and resource size had not been addressed to date in
scavenging contexts. Our analysis of quantitative matrices
supported that chance may play a greater role in determining which species feeds on small carcasses than on larger carcasses. Many different species of meso-facultative scavenger
exploited small carcasses in our study, probably because they
had the opportunity of finding such carcasses before more
narrowly selective scavengers, namely vultures, hyenas and
lions, had arrived (carcass detection time decreased with
carcass size). However, a low number of scavengers shared
a given small carcass, as the first species to find it usually
consumed most of it.
In relation to carrion consumption efficiency, small
carcasses were detected slower and consumed faster than
larger carcasses, which could indicate an effect of carcass
conspicuousness and usable biomass availability, respectively.
In addition, consumption rates of larger carcasses were much
higher. The fact that the percentage of carrion biomass consumed decreased as carcass size increased could be due to
the higher presence of large bones that can only be partly
eaten by hyenas and sometimes lions. Large facultative scavengers (especially hyenas and lions), but not vultures (i.e. the
obligate scavengers), were mainly responsible for the higher
carrion consumption rates. This could be the result of two
interacting factors. First, maximum food intake of hyenas
and lions, which are the most important scavengers among
large carnivores (Pereira et al. 2014), is much higher than
1400
that of vultures: while a hyena and a lion can consume one
third and one quarter of their respective body weights (i.e.
ca 17–20 kg and 30–50 kg of food, respectively; according
to Estes 1992), a vulture rarely eats more than 1.5 kg in a
meal (Donázar 1993). Many vultures are needed, therefore,
to compensate this differential per capita intake. According
to population estimates in 2012, there were 303 spotted
hyaenas, 200 lions and 398 breeding pairs of white-backed
vulture in HiP (Howells et al. 2009–2013, D. Druce and G.
Clinning pers. comm.). This would lead to maximum food
intake of 6000–10 000 kg and 5151–6060 kg for the whole
population of lions and hyaenas, respectively, and 1194 kg
for breeding white-backed vultures. Thus, maximum consumption by the breeding sector of the vulture population
meant 7.43–10.71% of the maximum food intake by lions
and hyaenas, which indicates that the food demand of lions
and hyenas greatly exceeded that of vultures. Second, these
large carnivores can displace vultures from carcasses and successfully defend them until satiation (Moleón et al. 2014a).
The influence exerted by the hour of carcass placement
seems to be related with the activity rhythm of scavengers.
Detection and consumption times, as well as consumption
rate, diminished if carcasses were placed in the morning.
This is the time of the day when vultures and other avian
scavengers such as birds of prey and corvids are more active,
and it is well established that avian scavengers are more
efficient in finding carcasses than mammals (Wilmers et al.
2003, Ruxton and Houston 2004). In contrast, the percentage of carrion biomass that was consumed increased if
carcasses were placed after midday, because hyenas, lions and
other mammalian carnivores, which are able to ingest bones
and other hard issues that are barely consumed by birds,
forage more actively nocturnally. We also detected some
spatial effect on the scavenging patterns: the section of the
park (Hluhluwe and iMfolozi) contributed partly to explain
differences in consumption time and percentage of carrion
consumed, although its influence was considerably lower
than that exerted by the size of the carcass. Finally, we
found some seasonal variation in community structure and
functioning: mean scavenger richness and carcass consumption rate were slightly higher during the dry season, while
carcass detection time was much longer during the wet
season. Several factors could explain these patterns, although
their relative contribution is difficult to determine. First,
less vegetation cover during the dry season probably facilitates carrion searching success of opportunistic, facultative
scavengers (Ruzicka and Conover 2012). Second, rainy
days could reduce the foraging activity of vultures and large
raptors (Houston 1979, Selva et al. 2005) and the smell
capacity of mammalian scavengers (Savage 1977) during the
wet season.
Comparison between predation and scavenging
systems
Several key size-dependent differences can be identified
between the resource use patterns in scavenging versus
predation networks in diverse African vertebrate systems.
First, it is established that larger ungulates, especially megaherbivores, have fewer predator species than smaller ungulates (Sinclair et al. 2003, Owen-Smith and Mills 2008,
Figure 4. Conceptual networks depicting hypothetical sizedependent resource use patterns in vertebrate predation and scavenging assemblages in relation to total resource pool (i.e. all prey/
carcasses into a given prey/carcass size category; (A)) and individual
resources (i.e. individual prey/carcasses of a given prey/carcass size
category; (B)). Black circles represent predator/scavenger species,
while grey circles show the resource (dark and light grey for live
prey and carrion, respectively). Grey circles size indicate resource
size, i.e. ‘small’, ‘medium’ and ‘large’ prey/carcasses. A link represents the consumption of a given resource pool (A) or individual
(B) by a predator/scavenger species. A) As prey size increases,
less predator species are able to kill them (Sinclair et al. 2003,
Owen-Smith and Mills 2008, Pereira et al. 2014). In contrast,
species richness of scavengers for large carcasses is similar than that
found for small carcasses (compare framed networks in the figure;
present study). B) As prey size increases, more individuals die from
causes besides predation (Sinclair et al. 2003, Owen-Smith and
Mills 2008, Pereira et al. 2014), while all carcasses in our study area
were widely exploited by scavengers (present study). Note that a
given prey individual can only be eaten by one predator species; a
second predator species that displaces the original predator from its
kill is not predating the kill, but scavenging, or kleptoparasiting, it.
In contrast, a given carcass can be scavenged by several scavenger
species, in particular larger carcasses. In our study case, medium
and large carcasses consumption was nearly nested (see text for
further details).
Pereira et al. 2014). In contrast, we have found that larger
carcasses supported a richer scavenging assemblage (Fig. 4A).
Second, while small and medium ungulates mostly die due
to predation, megaherbivores are rarely predated and mostly
when young (Sinclair et al. 2003, Owen-Smith and Mills
2008, Pereira et al. 2014). On the contrary, we found that all
carcasses were subjected to scavenging, irrespective of their
size, and that more links per individual resource appear in
scavenging than in predation networks, especially as carcass
size increases (Fig. 4B). In our system, this led to a more organized (i.e. nested) scavenging at larger carcasses (Table 4).
Which are the factors behind such structural differences
between predation and scavenging networks? Predator size
and numbers contribute to determine live prey hunting
success, so in general relatively large prey can only be killed
by large social predators (Sinclair et al. 2003, Owen-Smith
and Mills 2008). Larger and social scavengers have also
advantages to exploit large carcasses, due to their competitive superiority and their ability to access the interior of
thick-skinned animals (Moleón et al. 2014a). In contrast to
very large prey, very large carcasses can be exploited by many
consumer species, especially after dominant scavengers have
been satiated. Small and medium-sized carcasses can be
completely or mostly monopolized by a single scavenger
species, but very large carcasses contain enough meat to feed
more scavengers. In addition, smaller scavengers may gain
access to the meat after a dominant scavenger has opened the
carcass and has left (Moleón et al. 2014a).
Optimal foraging theory suggests that incorporating
a food resource in the diet depends on a tradeoff between
the energy intake and the costs of searching and handling (capturing and manipulating) the prey (MacArthur and Pianka
1966, Pyke et al. 1977). Such costs would be much lower
for carcass than for live prey consumption because capturing
and manipulating efforts are absent and reduced respectively.
This fact may allow for a larger number of consumers and
a wider range of resource size use (Fig. 4). Besides, defending large carcasses entails further costs for predators against a
wide array of potential scavengers and losses from the putrefaction and toxifying activity of decomposers (DeVault et al.
2003, Hayward et al. 2006, Moleón et al. 2014a, Pereira
et al. 2014). Such costs, associated with the interactions
between predators and carrion consumers (either vertebrates,
invertebrates or microbes), have not been considered in
previous models of optimal foraging.
Concluding remarks
Our findings support the idea that the particle size of the
resource affects the structure and functioning of vertebrate
scavenging networks. The relevance of the size of the
food resource had been hardly recognized until now in a
scavenging context, despite being pervasive in other trophic
assemblages (Woodward et al. 2005). Wide size variation
of available carcasses allows a wide spectrum of species to
differentially access the carrion resource, which might promote scavenger diversity. We have explicitly shown that
the scavenger assemblage is more organized as carcass size
increases, but full understanding of the mechanisms and
consequences of nestedness in scavenging and other competitive networks requires detailed investigation. Also, we have
highlighted the pivotal role that large facultative scavengers
play in the structure and functioning of diverse scavenging
networks. Finally, we have identified several size-dependent
differences in scavenging networks structure compared
with predator–prey systems. For predators, the costs associated with competition from carrion consumers might be
an important feature limiting the benefits of capturing large
live prey. The consequences of carcass size variation over time
and space for scavenging networks deserve further theoretical
and applied research effort, especially in the light of the current scenario of global environmental change (DeVault et al.
2003, Wilson and Wolkovich 2011, Moleón et al. 2014a,
Pereira et al. 2014). Our experimental provision of carrion
needs to be complemented by future studies on the carrion
naturally available, quantifying live prey versus carrion intake
by facultative scavengers and recognizing that animal deaths
are frequently hastened through the agency of a predator.
1401
­­­­­­­­
Acknowledgements
– G. Clinning and D. Druce decisively helped
with fieldwork logistics. J. Bautista, J. R. Fernández-Navarro,
D. Carmona-López, E. Ramos, M. S. García-Heras, E. McCain,
Thamalina, L. Munro, C. Geoghegan, H. Druce, E. Virgós,
S. Cabezas-Díaz, J. Lozano, N. Yelo, S. Eguía, I. Moleón, L.
Moleón, E. Moleón, E. Moleón, S. Justicia, A. J. Paiz, E. Moyano,
J. M. Molina, C. Hue, B. Whittington-Jones, J. Bird, as well as
several rangers and personnel at Hluhluwe Research Centre and the
abattoirs kindly helped at different fieldwork stages. We also thank
Ezemvelo KZN Wildlife for permissions and logistic facilities. The
study was partly funded by the Spanish Ministry of Economy and
Competitiveness through grant CGL2012-40013-C02-02. MM
was supported by a postdoctoral fellowship from the Spanish Ministry of Education (Plan Nacional de I D i 2008-2011). ES-G
benefitted from a São Paulo Foundation grant from Brazil (Ref.:
2011/17968-2).
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Supplementary material (available online as Appendix
oik.02222 at  www.oikosjournal.org/readers/appendix ).
Appendix 1. Table A1. Weights of the ungulate species
considered in this study. Table A2. Scavenger species detected
in this study, according to carcass size. Figure A1. Species
richness curves.
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