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EV-1
An assessment of tree availability as a possible cause of population
declines in scavenging raptors
CorinneJ.Kendall, DanielI.Rubenstein, PamelaL.Slater and AraMonadjem
C. J. Kendall (http://orcid.org/0000-0003-4429-4496) (corinne.kendall@nczoo.org) and P. L. Slater, North Carolina State Univ., Raleigh, NC,
USA. CJK also at: North Carolina Zoo, Asheboro, NC. – D. I. Rubenstein, Princeton Univ., Princeton, NJ, USA. – A. Monadjem, Savanna
Research Center, Dept of Biological Sciences, Univ. of Swaziland, Kwaluseni, Swaziland and Mammal Research Inst., Dept of Zoology and
Entomology, Univ. of Pretoria, Pretoria, South Africa.
Lack of suitable nesting trees is an increasingly common issue for avian conservation given rampant habitat and tree
destruction around the world. In the African savannah, habitat loss and particularly tree damage caused by elephants
have been suggested as possible factors in the decline of large bird species. Given the recent declines of vultures and other
scavenging raptors, it is critical to understand if nest availability is a limiting factor for these threatened populations.
Loss of woodland, partially due to elephant populations, has been reported for the Mara-Serengeti ecosystem. Data on
characteristics of trees used for nesting were collected for white-backed, lappet-faced, white-headed vulture, and tawny
eagle nests in Masai Mara National Reserve, Kenya. Nest tree characteristics were compared with the distribution of a
random subsample of trees to assess nest preferences and determine suitability of available trees. Nearest neighbor distances
were estimated as well as availability of preferred nesting trees to determine if tree availability is a limiting factor for
tree-nesting vultures. Tree availability was found to greatly exceed nesting needs for African vultures and tawny eagles.
We thus conclude that on a landscape scale, tree availability is not a limiting factor for any of the species considered here
(white-backed, lappet-faced, white-headed vultures and tawny eagles).
Success of conservation eorts may be enhanced by focusing
on the factors that limit population growth of threatened
species. For many birds, breeding success can be mediated
by external factors, such as food availability, disease, or rain-
fall, but also by characteristics of the nest itself, which may
impact suitability or susceptibility to disturbance (Arroyo
and Razin 2006, Monadjem and Bamford 2009). e
availability of suitable nesting sites thus has potential to be a
limiting factor for population growth (Newton 1994, 2010).
Rapid declines in African raptors, particularly avian scaven-
gers, have been documented locally, such as in the Masai
Mara National Reserve, Kenya (hereafter referred to as the
Mara) and more broadly throughout Africa (iollay 2006a,
b, 2007, Viranietal. 2011, Ogadaetal. 2016). e decline
of African vultures has been of particular concern, given the
recent Asian vulture crisis, which saw precipitous declines
of three vulture species in less than a decade (Greenet al.
2006). Although the causal factor in the Asian vulture crisis
has been well established as a single factor, diclofenac expo-
sure (Painetal. 2003), the reason for the decline in African
populations is more complicated. Direct and indirect poi-
soning, direct persecution, collision with and electrocution
by powerlines are among the long list of threats thought to
be negatively impacting African vultures (Ogadaetal. 2016).
However, tree availability has not been tested as a limiting
factor for African vulture populations in the Masai Mara or
elsewhere, and could be related to the declines.
Woodland areas have declined across much of the
African savannah over the last thirty years, potentially due
to increases in elephant density (Laws 1970, Caughley
1976, Kuiper and Parker 2014). Similar woodland declines
have been noted across the Mara-Serengeti ecosystem
(Glover 1968, Lamprey et al. 1967, Dublin et al. 1990,
Walpoleetal. 2004). With ongoing destruction of big trees
in protected areas with large elephant populations (Jacobs
and Biggs 2002, Edkinsetal. 2008, Vanaketal. 2012), there
is a concern that suitable nesting sites for raptors may disap-
pear from such areas (Hustler and Howells 1986, Monadjem
and Garcelon 2005, Viranietal. 2010).
In addition, little is known about tree nesting preferences
of many tree-nesting African vultures, particularly lappet-
faced Torgos tracheliotos and white-headed vultures Trigono-
ceps occipitalis, and there have been few studies of tree nesting
behavior in East Africa (Houston 1976, Viranietal. 2010).
In addition, the majority of studies describe nest character-
istics or breeding success, but few have considered nesting
preference in relation to tree availability (Monadjem 2003,
Bamfordetal. 2009b). White-backed vultures Gyps africanus
are known to frequently use tall trees near rivers, particularly
in the Mara, and tawny eagles Aquila rapax have also been
Journal of Avian Biology 48: 001–008, 2017
doi: 10.1111/jav.01497
© 2017 e Authors. Journal of Avian Biology © 2017 Nordic Society Oikos
Subject Editor: Ronald Ydenberg. Editor-in-Chief: omas Alerstam. Accepted 28 August 2017
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shown to have a preference for nesting near rivers (Houston
1976, Monadjem and Garcelon 2005, Herholdt and
Anderson 2006, Bamfordetal. 2009a, b, Viranietal. 2010).
e particular tree species selected by nesting white-backed
vultures vary greatly from site to site. For example, some
populations are known to prefer thorny trees such as various
species of Acacia (Mundyetal. 1992), whilst in Swaziland,
white-backed vultures actively avoid Acacia trees (Monadjem
2003). Other studies in the Mara found Ficus and Balanites
species to be most commonly selected (Viraniet al. 2010).
For white-headed vultures, studies of nests of 22 breeding
pairs in Kruger National Park in South Africa, reported the
most common nesting tree to be Senegalia nigrescens, and
the average nest tree height to be 14 m, which was taller
on average than 30 randomly selected trees (Murn and
Holloway 2014). An understanding of the ne-scale nesting
preferences, particularly the characteristics of the nest tree
and its immediate surroundings, can be useful for predicting
the distribution of suitable nesting sites; hence there is value
in further exploration of these characteristics (Bamfordetal.
2009a, b).
us, the primary objective of this study was to deter-
mine if tree availability was a limiting factor for avian scaven-
gers, namely vulture and tawny eagle populations. In order
to determine this, we rst describe the nest tree preferences
for all tree-nesting avian scavengers found in Masai Mara
National Reserve, Kenya, and compare these with the char-
acteristics of a random sample of trees. We predicted that
white-backed vultures and white-headed vultures would pre-
fer tall trees while lappet-faced vultures would prefer short
trees (Mundyetal. 1992, Bamfordetal. 2009b, Murn and
Holloway 2014). We expected that white-backed vultures
would prefer to nest near rivers, where the density of desired
trees is higher (Houston 1976, Viraniet al. 2010). Tawny
eagles are known to prefer at-topped trees in riverine areas
(Hustler and Howells 1989). We thus predicted that tawny
eagles would prefer to nest near rivers. We then used nesting
preferences established by our study to estimate the avail-
ability of trees suitable for nesting for each species. By com-
paring suitable tree density with density of breeding pairs,
we were able to address the question of whether or not tree
availability is a limiting factor, which would restrict breeding
opportunities and could thus aect population growth, for
several critically endangered vulture species, as well as tawny
eagles, in the Mara.
Material and methods
Study area
e Mara-Serengeti ecosystem is one of the most impor-
tant areas for avian scavengers in Africa (Kendall 2013), due
in part to the open savannah habitat and high densities of
ungulates, including the migratory herds of blue wildebeest
Connochaetes taurinus, Burchell’s zebra Equus burchelli, and
omson’s gazelle Gazella thomsonii. Masai Mara National
Reserve, Kenya, covers approximately 1523 km2 and is pri-
marily composed of savannah habitat with patches of wood-
land. Rainfall in Masai Mara National Reserve is bimodal
with long rains falling from March to June and short
rains from November to December (Ogutuet al. 2008).
Tree-nesting vultures are known to start breeding in the
Mara-Serengeti ecosystem from mid-April to May and for
chicks to edge from August to October, which maximizes
the overlap between edging and the high mortality period
of the migratory ungulate herds (Houston 1976, Viranietal.
2010). Tawny eagles are known to lay eggs from May to June
(Hustler and Howells 1986, Herholdtetal. 1996). Pastoral
community areas surrounding the Mara have undergone
considerable habitat degradation, but are still used by avian
scavengers (Ogutuetal. 2009, Kendall 2013).
Nests
Active avian scavenger nests were recorded during eldwork
conducted from May to July 2009, February to May and
July to September 2010, and March to May and July to
October 2011 in Masai Mara National Reserve, Kenya. We
searched for nests of all tree-nesting avian scavenger species
commonly found in the area including bateleur Terathopius
ecaudatus, tawny eagle, white-backed vulture, lappet-faced
vulture, white-headed vulture, and hooded vulture Necrosy-
rtes monachus. Nests were searched for opportunistically by
vehicle throughout the reserve, though the Mara Conser-
vancy Trust area to the west of the Mara River was surveyed
less frequently, as were communal lands to the north and east
of the reserve, Koiyaki and Siana respectively. Data were only
collected from active nests, dened as nests where a bird was
sitting on or building the nest when sighted. Where possible,
nests that had been empty upon rst sighting were re-visited
during the breeding season to determine whether they were
used in a given season or not. Following Berkelman (1997),
nest site characteristics were recorded including tree species,
height of nesting tree, and diameter at breast height of nest-
ing tree (DBH). In addition habitat characteristics such as
distance to nearest tree, and distance to nearest river were
estimated using ArcGIS. e tree genus Acacia has recently
been split into Vachellia and Senegalia. To avoid confusion
and to allow our results to be compared with previous stud-
ies, we retain all these species within Acacia. However, we
refer to them by their correct current names in the list of
tree species utilized for nesting (Table 4, 5, Supplementary
material Appendix 1).
Random trees
e same information (mentioned in the previous section
above) was recorded for an evenly distributed sample of
200 trees along road-based transects that had been set up
for the purpose of surveying raptors in the study area. Every
kilometer along the transect, trees were sampled by choosing
a random direction and sampling the closest tree. If no tree
was within 500 m of the road in the direction chosen, then
tree sampling was omitted for that particular point and we
continued on to the next kilometer.
Calculation of tree density, breeding pair density and
the proportion of suitable nesting trees
Data from Crowtheretal. (2015) were used to extract esti-
mates of tree counts for the study site including within
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Masai Mara National Reserve and in the two surrounding
conservancies of Koiyaki and Siana. ese data are based on
a global model of tree density and include only trees larger
than 10 cm in DBH.
Using transect data for the reserve, the avian scavenger
population was estimated for the study site (Virani et al.
2011). We assumed that during transects birds could be seen
for 500 m on either side and thus treated transect estimates of
birds per 100 km as density estimates of birds per 100 km2.
We then calculated population numbers for each study spe-
cies within the Masai Mara National Reserve (1523 km2)
and across Mara-Serengeti ecosystem (roughly 25 000 km2).
Assuming that 50% of birds are adults, that 75% of these
adults would breed in a given year, and that 50% of these
are breeding pairs (i.e. two birds sharing a single nest), we
calculated the number of breeding pairs that would require a
nest site annually within Masai Mara National Reserve and
across all of Mara-Serengeti (Murnetal. 2016).
We then calculated the proportion of trees available for
nesting. Suitable nesting trees were dened as tree species
that a given vulture or eagle species had been observed nest-
ing in as part of this study. Furthermore, we specied that
the height of these tree species, should be within one stan-
dard deviation of the mean height of known nesting trees
used by each of the scavenging species. Because taller trees
were found to be preferred and trees with larger diameter at
breast height (DBH) were preferred by white-backed vul-
tures, all trees with height or DBH larger than average minus
one standard deviation of nesting trees were included (i.e.
tree heights of 7.9 m or taller and DBH of 34 cm or larger)
for this species. We then determined the total trees suitable
for nesting within the reserve by multiplying the tree count
by the proportion of trees likely to be suitable for a given
species. From this, we determined a total count of suitable
nesting trees in the Masai Mara National Reserve for each
vulture or eagle species.
Data analysis
A student t-test was used to test whether the characteristics of
nesting trees (listed above) was dierent from the randomly
sampled trees. For nesting preference analysis, we developed
generalised linear mixed models to examine the eect of the
following covariates: DBH of nesting tree (DBH), height of
nesting tree (tree height), distance of nesting tree to the near-
est tree (nearest tree) and distance of nesting tree to nearest
river (nearest river), on the response variable: presence or
absence of a nest in the tree. We included land use (protected
area, conservancy or settlement) and year as random eects
to account for dependence of nests situated in the same land
use or sampled in multiple years. Models were ranked using
the corrected Akaike’s information criterion (AICc) (Burn-
ham and Anderson 2002). e model with the lowest AICc
was deemed the best model; where delta AICc (the dierence
in AICc between models) for any two (or more) models was
≤ 2.0, they were both deemed to be equally good. Analyses
were conducted in R statistical software ver. 3.2.4. (R Core
Team), using the lme4 package (Batesetal. 2014).
For nearest neighbor analysis, only nests within a given
year were considered and for white-backed vultures, only
nests from 2011 (when largest nest survey eorts were
made) were considered. Following Monadjem (2003), the
proportions of each tree species used by white-backed,
lappet-faced, white-headed vultures and tawny eagles and
expected usage given availability (calculated from random
sample) was calculated. Note that tree species used for just a
single nest by any of the four scavenging species were lumped
as ‘other’. Trees were lumped by genus where multiple species
occurred (e.g. Acacia and Ficus).
Data deposition
Data available from the Dryad Digital Repository: <http://
dx.doi.org/10.5061/dryad.bb775> (Kendalletal. 2017).
Results
Scavenger nests in Masai Mara National Reserve
Across the three years of our study, 113 white-backed
vulture, 51 lappet-faced vulture, 15 white-headed vulture,
and 21 tawny eagle distinct nests were located. Only one
bateleur nest was located during this study and no hooded
vulture nests were found, despite the regular presence of
these vultures at carcasses.
Nesting preferences and aggregations
ough survey eort was less outside of protected areas,
the majority of the nests were located in the Masai Mara
National Reserve, suggesting that all species prefer nesting
in areas with less human habitation and higher wildlife den-
sity. Results from t-tests comparing tree and spatial charac-
teristics for nests and random trees are presented in Table
1. White-backed vultures selected for taller trees with larger
DBH. Lappet-faced vultures preferred shorter trees than
expected, but there was no dierence in DBH between nest-
ing and random trees. Tawny eagles showed no preference in
relation to tree or spatial characteristics. Both white-backed
and white-headed vulture nests were closer to the river than
random and distance to nearest tree did not appear to be
important for nest selection for any species considered.
White-backed and lappet-faced vultures nested close to
conspecics, possibly due to congregation of nests in the
Mara or near rivers, whereas white-headed vulture and tawny
eagle nests tended to be farther apart. Average distance to
nearest neighboring nest are reported in Table 2.
Results for GLMM analysis are shown in Table 3. For the
African white-backed vulture, the best model included just
‘tree height’ and had a model weight of 0.451. e next best
model had delta of almost 2.0 and included ‘tree height’ and
‘nearest river’. e remaining models, which included the
‘full’ model (including all the covariates) and the ‘null’ model
(including no covariates), had delta AICc ≥ 2.0 with declin-
ing AICc weights (results not shown), and were therefore
discounted as best candidate models.
For the lappet-faced vulture, the best model included
just tree height and had a model weight of 0.403. e next
two models had delta AICc ≤ 2.0 and were hence compet-
ing models, and both of them included the covariate ‘tree
height’ with either ‘DBH’ or ‘nearest river’. e remaining
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models, which included the ‘full’ model (including all the
covariates) and the ‘null’ model (including no covariates),
had delta AICc ≥ 2.0 with declining AICc weights (results
not shown), and were therefore discounted as best candidate
models.
For the white-headed vulture, the best models were the
‘null’ model and the model that included only the ‘nearest
tree’; both of these two models had weights of 0.157 each.
ere were ve competing models which included various
combinations of all the measured covariates. For the tawny
eagle, the best model included just ‘DBH’ and had a model
weight of 0.262. Competing models included the ‘null’
model, ‘tree height’ and ‘tree height’ plus ‘DBH’.
Tree species utilized for nesting
e numbers of nests situated in dierent species of trees
by the various scavenging raptors and their proportional
use is shown in Tables 4 and 5, respectively. e majority
of white-backed vulture nests were located in just ve spe-
cies of trees (Table 4), of which Boscia angustifolia, Ficus spp.
and Albizia gummifera were utilized more frequently than
expected, whereas Acacia spp. in proportion to that expected
(Table 5). In contrast, lappet-faced vultures used Balanites
aegyptiaca and Gardenia ternifolia more than expected and
Acacia (Vachellia and Senegalia) spp. less so. White-headed
vultures used Boscia angustifolia and Olea europea more
than expected, whereas tawny eagles used Boscia angustifo-
lia and Euclea divinorum more than expected. Details on
all tree species seen are provided in Supplementary material
Appendix 1–2.
Estimating tree density and number of breeding
birds
Based on Crowther et al. (2015), there are an estimated
13 million trees in the Masai Mara National Reserve. We
determined the proportion of trees likely to be suitable for
nesting for each bird species based on preferred tree species
and height, and DBH for white-backed vultures for which
this was an important characteristic, and also calculated the
potential number of breeding pairs (Table 6). e propor-
tion of suitable nesting trees ranged from 20% for tawny
eagles to 49% for white-backed vultures. As a result, there
are likely to be anywhere from 2 to 6 million suitable nest-
ing trees for these raptors. In contrast, estimates for breeding
pairs ranged from nine for white-headed vultures to 74 for
white-backed vultures. 74 breeding pairs for white-backed
vultures is clearly an underestimate as we found 113 nests
during our survey. If we assume that birds ranging across
Mara-Serengeti might nest exclusively in Masai Mara
National Reserve, which would likely be an overestimate, it
would increase the potential number of white-backed vul-
ture breeding pairs needing a nest to roughly 1219. We thus
found that the number of available nesting trees in Masai
Mara was three orders of magnitude greater than the num-
ber of potential breeding pairs even across the entire Mara-
Serengeti ecosystem.
Table 1. Comparison of tree characteristics for random trees and trees in which four species of avian scavengers nested in the Masai Mara,
Kenya. The values are presented as means ± SE with the t-test test statistic and p-values provided in parentheses. Bold values are significant
at p < 0.055 level.
Tree characteristics
Random tree
(n = 200)
White-backed vulture
nest trees (n = 113)
Lappet-faced vulture
nest trees (n = 51)
White-headed vulture
nest trees (n = 15)
Tawny eagle nest trees
(n = 21)
Tree height (m) 9.6 ± 4.0 11.6 ± 3.7 (t = 4.539,
p < 0.001)
7.5 ± 2.4 (t=4.723,
p < 0.001)
9.1 ± 2.5 (t = 0.717,
p = 0.482)
10.5 ± 2.0 (t = 1.754,
p = 0.087)
Tree DBH (cm) 59.8 ± 35.7 67.6 ± 33.6 (t = 1.937,
p = 0.054)
56.7 ± 30.2 (t = 0.622,
p = 0.536)
55.2 ± 34.1 (t = 0.494,
p = 0.628)
59.6 ± 39.9 (t = 0.020,
p = 0.985)
Nearest tree (m) 79.7 ± 247.1 64.8 ± 139.3
(t = 0.683, p = 0.495)
217.6 ± 743.3 (t = 1.306,
p = 0.197)
133.9 ± 272.5
(t = 0.747, p = 0.466)
84.0 ± 196.5
(t = 0.092, p = 0.927)
Nearest river (m) 4713.9 ± 4828.5 2751.4 ± 4177.6
(t = 3.769, p < 0.001)
3751.4 ± 6326.1
(t = 1.0139, p = 0.314)
2660.4 ± 3119.5
(t = 2.347, p = 0.030)
3727.3 ± 3441.0
(t = 1.196, p = 0.241)
Table 2. Distance to nearest conspecific neighbor nest for four rap-
tor species nesting in the Masai Mara National Reserve, Kenya. The
values are means ± SE.
Species Distance to nearest neighbor (m)
White-backed vulture 1454.9 ± 1749.5 (n = 48)
Lappet-faced vulture 2208.4 ± 1717.5 (n = 43)
White-headed vulture 5397.2 ± 5322.1 (n = 13)
Tawny eagle 5439.7 ± 3857.1 (n = 19)
Table 3. Results from GLMM investigating preferences for different
nesting tree characteristics for four avian scavenger species. Each
species is shown separately. The number of estimated parameters is
indicated by ‘n’. The models are arranged from best (top of table) to
worst (bottom) based on the corrected Akaike’s information criteria
(AICc). Only competing models (delta AICc < 2.0) are shown. Also
included is the difference in AICc from the best model (delta AICc),
and the weight of each model (AICc weights).
Model n AICc Delta AICc AICc weights
White-backed vulture
Height 4 202.3 0 0.451
Height + Nearest river 4 204.3 1.97 0.169
Lappet-faced vulture
Height 4 137.2 0 0.403
Height + DBH 5 138.7 1.49 0.191
Height + Nearest river 5 139.0 1.80 0.164
White-headed vulture
Null 3 50.0 0 0.157
Nearest tree 4 50.0 0 0.157
Height + Nearest tree 5 50.6 0.54 0.120
Nearest river 4 50.7 0.69 0.111
DBH 4 51.0 1.02 0.095
Height + Nearest river 5 51.2 1.17 0.088
Height 4 51.2 1.20 0.086
Tawny eagle
DBH 4 56.1 0 0.262
Null 3 56.9 0.77 0.178
Height 4 57.9 1.83 0.105
Height + DBH 5 57.9 1.83 0.105
EV-5
Discussion
Given the ongoing vulture declines, it is essential to deter-
mine the relative importance of factors that aect vulture
population persistence and growth (Virani et al. 2011,
Ogadaetal. 2016). Tree availability for tree-nesting vultures
and raptors has been suggested as a potential limiting factor
(Newton 2010), but our results strongly suggest this is not
the case for avian scavengers in the Masai Mara National
Reserve, Kenya. ere are approximately 5000 times more
trees than there are likely to be breeding pairs, even if we
assume the entire Mara-Serengeti population nests in Masai
Mara for the most populous species considered here, the
white-backed vulture. Even if we assume a total breeding
population of 4000 (10 × our estimate for white-backed
vultures in Masai Mara National Reserve and four times
greater than higher estimates from Viranietal. 2010), the
vultures would only need about 2.6 suitable nesting trees
per square kilometer. Since nearly 50% of trees are suitable
for nesting for this species, this would require only 5.2 trees
per square kilometer (or 7919 trees in the entire Masai
Mara National Reserve). So while tree counts derived from
Crowther’s estimates are likely overestimates (estimates over
13 million trees in the Masai Mara National Reserve), these
numbers would have to be o by more than four orders of
magnitude (or 1640 times) for nesting availability to be a
limiting factor for breeding birds, which is highly improb-
able. We can thus conclude that tree availability is not a
limiting factor for any of the species considered here (white-
backed, lappet-faced, white-headed vultures, and tawny
eagles).
If territoriality is an important factor, this could also
impact nesting densities. Nesting density varies consid-
erably by vulture species and sites studied, and can even
vary signicantly within a site (Hustler and Howells 1988,
Mundyetal. 1992, Murnetal. 2002, 2013, Monadjem and
Garcelon 2005, Bamfordetal. 2009b, Viraniet al. 2010,
Murn and Holloway 2014). In this study as elsewhere, dis-
tance between conspecic nests, was lowest for white-backed
vultures as might be expected for a semi-colonially nesting
species. For white-backed vultures, distances between con-
specic ness were considerably lower than previously found
in the Mara, probably due to larger and more representative
sampling (Viranietal. 2010). Distance between conspecic
nests was comparable to other sites for white-headed, lappet-
faced vultures, and tawny eagles (Hustler and Howells 1986,
Table 4. The number of times a particular tree species was used as a nesting site by four raptor species in the Masai Mara National Reserve,
Kenya. Also shown is the number of times each tree species appears in the random sample of trees. All species of Vachellia and Senegalia are
lumped under ‘Acacia spp.’
Tree species
Number of trees with
AWB nests
Number of trees with
LFV nests
Number of trees with
WHV nests
Number of trees
with TE nests
Number of trees in
random sample
Boscia angustifolia 32 10 4 5 32
Ficus sp. 26 1 0 0 8
Acacia sp. 20 1 3 2 33
Olea europea 12 4 5 1 18
Albizia gummifera 10 0 0 1 6
Diospyros abyssinica 3 0 0 0 13
Warburgia ugandensis 3 0 0 0 1
Balanites aegyptiaca 2 15 2 1 38
Gardenia ternifolia 0 16 1 1 7
Maytenus senegalensis 0 2 0 0 0
Euphorbia candelabrum 0 0 0 6 12
Euclea divinorum 0 0 0 4 7
Other 4 0 0 0 23
Unidentified 1 1 0 0 2
Total 113 50 15 21 200
Table 5. The proportion that a tree species was used for nesting in (i.e. the number of times a tree species was used to nest in by one of the
four avian scavengers/total nests located for each species of avian scavenger) and the proportion that a tree species was expected to be used
(i.e. the number of times that a tree species appears in the random sample/total number of trees in the random sample) in the Masai Mara
National Reserve, Kenya.
Tree species Proportion used (AWB) Proportion used (LFV) Proportion used (WHV) Proportion used (TE) Proportion expected
Boscia angustifolia 0.283 0.200 0.267 0.238 0.160
Ficus sp. 0.230 0.020 0.000 0.000 0.040
Acacia sp. 0.177 0.020 0.200 0.095 0.165
Olea europea 0.106 0.080 0.333 0.048 0.090
Albizia gummifera 0.088 0.000 0.000 0.048 0.030
Diospyros abyssinica 0.027 0.000 0.000 0.000 0.065
Warburgia ugandensis 0.027 0.000 0.000 0.000 0.005
Balanites aegyptiaca 0.018 0.300 0.133 0.048 0.190
Gardenia ternifolia 0.000 0.320 0.067 0.048 0.035
Maytenus senegalensis 0.000 0.040 0.000 0.000 0.000
Euphorbia candelabrum 0.000 0.000 0.000 0.286 0.060
Euclea divinorum 0.000 0.000 0.000 0.190 0.035
Other 0.044 0.020 0.000 0.000 0.125
EV-6
1988, 1989, Mundyet al. 1992, Monadjem and Garcelon
2005, Viraniet al. 2010, Murn and Holloway 2014). is
variability in nearest neighbor distance for nests suggests
that tree availability rather than territoriality may determine
where vultures nest. Furthermore, vultures can have large
foraging ranges and some species nest colonially suggesting
that nesting density is determined by the availability of trees
with desired characteristics and is unlikely to be aected by
over-crowding (Jacksonetal. 2008, Mateo-Tomas and Olea
2011, Phippsetal. 2013, Kendalletal. 2014).
Issues such as elephant impact on trees and nesting dis-
turbance have been considered as potential threats to vul-
tures and it has been suggested that elephants may impact
tree availability for nesting raptors in the Mara (Viranietal.
2010). e impact of elephants on tree-nesting vultures is
not yet fully understood, although at high elephant densities,
the number of suitable nesting trees are signicantly dimin-
ished (Monadjem and Garcelon 2005). However, work in
the Mara-Serengeti ecosystem suggests that while elephants
may be able to maintain woodland density at a lower level,
elephants were not the primary drivers in decreasing wood-
land density here (Dublinetal. 1990). Woodland density
in the Mara is lower now than in the 1980s, however as our
estimates demonstrate, tree availability is still high. In addi-
tion, where breeding success for scavenging birds has been
studied, rainfall has generally been found to be the primary
factor determining nesting success rather than tree avail-
ability (Monadjem and Bamford 2009, Viraniet al. 2012).
Similarly, while nest disturbance can inuence behavior and
breeding success in cli-nesting vultures, it is unlikely to be
the determining factor in breeding success for tree-nesting
species, which can easily move nests should disturbance arise
(Donazaretal. 1993, Arroyo and Razin 2006, Zuberogoi-
tiaetal. 2008). Finally, while nest disturbance could impact
nesting success, it is unlikely to aect adult survival, which
is more closely tied to population dynamics (Bamfordetal.
2009b).
Nesting preferences
While tree availability does not appear to be a limiting
factor for nesting, understanding nesting preferences may
assist in vulture conservation. In our study we found con-
siderably more nests in the Masai Mara National Reserve
than outside of it. is is consistent with similar studies of
breeding vultures, which have reported that vultures tend
to nest in protected areas, with lappet-faced and white-
headed vultures nesting exclusively in protected areas in
Swaziland (Monadjem and Garcelon 2005, Bamfordetal.
2009a).
Our results indicate that white-backed vultures tend to
select, and in some cases prefer, tall trees (Houston 1976,
Herholdt and Anderson 2006, Bamfordetal. 2009b). is
is consistent with other studies that have indicated that
white-backed vultures prefer tall trees and, in some cases,
riparian areas which may be indicative of suitable tree
availability (i.e. more tall trees along the river) rather than
a specic characteristic being selected for, though charac-
teristics can vary by area (Houston 1976, Monadjem and
Garcelon 2005, Bamfordetal. 2009b, Viranietal. 2010).
Lappet-faced vultures are known to nest in short trees and to
use Acacia, Balanites, and Terminalia trees though little work
has been done on their nesting preferences (Mundyet al.
1992). In the Mara, lappet-faced vultures appear to prefer
shorter trees, particularly Gardenia, which oer wide tree
tops for larger nests. Other common tree species used were
Balanites and Boscia. In the Mara, we found no particular
tree species or characteristic preferences for white-headed
vulture nests, but Olea, Boscia, and Acacia (Vachellia or
Senegalia) were the most common species of tree chosen.
Tawny eagle showed no specic preferences in relation to
tree height or diameter, but preferred Euphorbia, Boscia, and
Euclea species.
Conclusion
Given that vultures are long-lived species, factors inuencing
adult survival are likely to be more important for popula-
tion stability than breeding success (Bamfordet al. 2009b,
Monadjemetal. 2013, 2014). We feel that the focus of future
vulture conservation eorts should be on the major issues
that impact adult survival and thus population growth. In
this respect, poisoning appears to be the primary threat to
most populations, particularly in East Africa (Ogada 2014,
Murn and Botha 2017). Based on our ndings, concerns
related to tree availability or nesting disturbance are thus
likely to be minor issues in comparison.
Acknowledgements – We would like to thank Wilson and Jon Masek
and Wilson Kilong, who provided eld assistance during the study.
We would like to thank Narok County Council, the sta of Masai
Mara National Reserve, and the neighboring group ranches and
conservancies for their assistance and permission to conduct this
research as well as Africa Eco-Camps for their support. We would
like to thank Julie Shapiro for her assistance with initial analysis of
satellite imagery. We would like to thank Munir Virani and Simon
omsett for their assistance in nest discovery.
Funding – Research was conducted in collaboration with e
Peregrine Fund’s Pan African Raptor Conservation Program and as
part of CK’s dissertation at Princeton Univ. Funding for this study
Table 6. Estimates of proportion and number of suitable nesting trees, the total populations of avian scavengers, and the total number of
breeding pairs by avian scavenger species in Masai Mara National Reserve, Kenya and Mara-Serengeti ecosystem.
Species Proportion of
trees suitable
Estimate of
suitable trees in
Masai Mara
National Reserve
Estimate of total
population in
Masai Mara
National Reserve
Estimate of total
breeding pairs in
Masai Mara
National Reserve
Estimate of total
population in
Mara-Serengeti
Estimate of total
breeding pairs in
Mara-Serengeti
White-backed vulture 0.49 (96/198) 6 420 302 397 74 6500 1219
Lappet-faced vulture 0.24 (48/198) 3 144 638 183 34 3000 563
White-headed vulture 0.32 (64/198) 4 192 850 46 9 750 141
Tawny eagle 0.20 (39/198) 2 620 531 113 21 1850 347
EV-7
was provided by Pompeo M. Maresi Memorial Fund from Princeton
Univ., Hawk Mountain Sanctuary and e Peregrine Fund. is is
Hawk Mountain Sanctuary contribution to conservation science
no. 286.
Author contributions – CJK conceived of study, collected data,
developed methods and wrote the paper. DR supervised the study
and designed methods. PM analyzed data for analysis of tree
availability. AM designed methods, analyzed the data and wrote
parts of the paper.
Permits – Research was conducted under research permit
NCST/5/002/R/448.
References
Arroyo, B. and Razin, M. 2006. Eect of human activities on
bearded vulture behaviour and breeding success in the French
Pyrenees. – Biol. Conserv. 128: 276–284.
Bamford, A. J., Monadjem, A. and Hardy, I.C.W. 2009a. Nesting
habitat preference of the African white-backed vulture Gyps
africanus and the eects of anthropogenic disturbance. – Ibis
151: 51–62.
Bamford, A. J., Monadjem, A., Anderson, M. D., Anthony, A.,
Borello, W. D., Bridgeford, M., Bridgeford, P., Hancock, P.,
Howells, B., Wakelin, J. and Hardy, I. C. W. 2009b. Trade-os
between specicity and regional generality in habitat associa-
tion models: a case study of two species of African vulture.
– J. Appl. Ecol. 46: 852–860.
Bates, D., Maechler, M., Bolker, B. and Walker, S. 2014. lme4:
Linear mixed-eects models using Eigen and S4. R package,
ver. 1. – <https://cran.r-project.org/package=lme4>.
Berkelman, J. 1997. Habitat requirements and foraging ecology of
the Madagascar sh-eagle. – PhD thesis, Fisheries and Wildlife
Sciences, Virginia Polytechnic Inst. and State Univ., VA, USA.
Burnham, K. P. and Anderson, D. R. 2002. Model selection and
multimodel inference: a pratical information-theoretic
approach. – Springer.
Caughley, G. 1976. e elephant problem – an alternative hypoth-
esis. – Afr. J. Ecol. 14: 265–283.
Crowther, T. W., Glick, H. B., Covey, K. R., Bettigole, C.,
Maynard, D. S., omas, S. M., Smith, J. R., Hintler, G.,
Duguid, M. C., Amatulli, G., Tuanmu, M. N., Jetz, W., Salas,
C., Stam, C., Piotto, D., Tavani, R., Green, S., Bruce, G.,
Williams, S. J., Wiser, S. K., Huber, M. O., Hengeveld, G. M.,
Nabuurs, G. J., Tikhonova, E., Borchardt, P., Li, C. F.,
Powrie, L. W., Fischer, M., Hemp, A., Homeier, J., Cho, P.,
Vibrans, A. C., Umunay, P. M., Piao, S. L., Rowe, C. W.,
Ashton, M. S., Crane, P. R. and Bradford, M. A. 2015.
Mapping tree density at a global scale. – Nature 525: 201–205.
Donazar, J. A., Hiraldo, F. and Bustamante, J. 1993. Factors
inuencing nest-site selection, breeding density, and breeding
success in the bearded vulture (Gypaetus barbatus). – J. Appl.
Ecol. 30: 504–514.
Dublin, H. T., Sinclair, A. R. E. and McGlade, J. 1990. Elephants
and re as causes of multiple stable states in the serengeti-mara
woodlands. – J. Anim. Ecol. 59: 1147–1164.
Edkins, M. T., Kruger, L. M., Harris, K. and Midgley. J. J. 2008.
Baobabs and elephants in Kruger National Park: nowhere to
hide. – Afr. J. Ecol. 46: 119–125.
Glover, P. E. 1968. e role of re and other inuences on the
savannah habitat, with suggestions for further research. – Afr.
J. Ecol. 6: 131–137.
Green, R. E., Taggart, M. A., Das, D., Pain, D. J., Kumar, C. S.,
Cunningham, A. A. and Cuthbert, R. 2006. Collapse of Asian
vulture populations: risk of mortality from residues of the
veterinary drug diclofenac in carcasses of treated cattle. – J.
Appl. Ecol. 43: 949–956.
Herholdt, J. J., and Anderson, M. D. 2006. Observations on
the population and breeding status of the African white-
backed vulture, the black-chested snake eagle, and the
secretarybird in the Kgalagadi Transfrontier Park. – Ostrich
77: 127–135.
Herholdt, J. J., Kemp, A. C. and Du Plessis, D. 1996. Aspects of
the breeding status and ecology of the bateleur and tawny eagle
in the Kalaharai Gemsbok National Park, South Africa.
– Ostrich 67: 126–137.
Houston, D. C. 1976. Breeding of white-backed and ruppells
grion vultures, Gyps africanus and Gyps rueppellii. – Ibis 118:
14–40.
Hustler, K. and Howells, W. W. 1986. A population study of tawny
eagles in the Hwange National Park, Zimbabwe. – Ostrich 57:
101–106.
Hustler, K. and Howells, W. W. 1988. Breeding biology of the
white-headed vulture in Hwange National Park, Zimbabwe.
– Ostrich 59: 21–24.
Hustler, K. and Howells W. W. 1989. Habitat preference, breeding
success and the eect of primary productivity on tawny eagles
Aquila rapax in the tropics. – Ibis 131: 33–40.
Jackson, A. L., Ruxton, G. D. and Houston, D. C. 2008. e eect
of social facilitation on foraging success in vultures: a modelling
study. – Biol. Lett. 4: 311–313.
Jacobs, O. S. and Biggs, R. 2002. e status and population
structure of the marula in the Kruger National Park. – S. Afr.
J. Wildl. Res. 32: 1–12.
Kendall, C. 2013. Alternative strategies in avian scavengers: how
subordinate species foil the despotic distribution. – Behav.
Ecol. Sociobiol. 67: 383–393.
Kendall, C. J., Virani, M. Z., Grant, J., Hopcraft, C., Bildstein, K.
L. and Rubenstein, D. I. 2014. African vultures don't follow
migratory herds: scavenger habitat use is not mediated by prey
abundance. – PLoS One 9: e83470.
Kendall, C. J., Rubenstein, D. I., Slater, P. L. and Monadjem, A.
2017. An assessment of tree availability as a possible cause of
population declines in scavenging raptors. – Dryad Digital
Repository, <http://dx.doi.org/10.5061/dryad.bb775>.
Kuiper, T. R. and Parker, D. M. 2014. Elephants in Africa: big,
grey biodiversity thieves? – S. Afr. J. Sci. 110: a0058.
Lamprey, H. F., Glover, P. E., Turner, M. I. M. and Bell, R. H. V.
1967. Invasion of the Serengeti National Park by elephants.
– Afr. J. Ecol. 5: 151–166.
Laws, R. M. 1970. Elephants as agents of habitat and landscape
change in East Africa. – Oikos 21: 1–15.
Mateo-Tomas, P. and Olea, P. P. 2011. e importance of social
information in breeding site selection increases with popula-
tion size in the Eurasian grion vulture Gyps fulvus. – Ibis 153:
832–845.
Monadjem, A. 2003. Nesting distribution and status of vultures in
Swaziland. – Vulture News 48: 12–19.
Monadjem, A. and Bamford, A. J. 2009. Inuence of rainfall
on timing and success of reproduction in Marabou Storks
Leptoptilos crumeniferus. – Ibis 151: 344–351.
Monadjem, A. and Garcelon, D. K. 2005. Nesting distribution
of vultures in relation to land use in Swaziland. – Biodivers.
Conserv. 14: 2079–2093.
Monadjem, A., Botha, A. and Murn, C. 2013. Survival of the
African white-backed vulture Gyps africanus in north-eastern
South Africa. – Afr. J. Ecol. 51:87–93.
Monadjem, A., Wolter, K., Neser, W. and Kane, A. 2014. Eect of
rehabilitation on survival rates of endangered Cape vultures.
– Anim. Conserv. 17: 52–60.
Mundy, P. J., Butchart, D., Ledger, J. A. and Piper, S. E. 1992. e
vultures of Africa. – Acorn books and Russel Friedman books,
Randburg, South Africa.
Murn, C. and Botha, A. 2017. A clear and present danger: impacts
of poisoning on a vulture population and the eect of poison
EV-8
response activities. – Oryx doi.org/10.1017/S0030605316
001137.
Murn, C. and Holloway, G. J. 2014. Breeding biology of the
white-headed vulture Trigonoceps occipitalis in Kruger National
Park, South Africa. – Ostrich 85: 125–130.
Murn, C., Anderson, M. D. and Anthony, A. 2002. Aerial survey
of African white-backed vulture colonies around Kimberley,
Northern Cape and Free State provinces, South Africa.
– S. Afr. J. Wildl. Res. 32: 145–152.
Murn, C., Combrink, L., Ronaldson, G. S., ompson, C. and
Botha, A. 2013. Population estimates of three vulture species
in Kruger National Park, South Africa. – Ostrich 84: 1–9.
Murn, C., Mundy, P., Virani, M. Z., Borello, W. D., Holloway, G.
J. and iollay, J.-M. 2016. Using Africa's protected area
network to estimate the global population of a threatened and
declining species: a case study of the critically endangered
white-headed vulture Trigonoceps occipitalis. – Ecol. Evol. 6:
1092–1103.
Newton, I. 1994. e role of nest sites in limiting the numbers of
hole-nesting birds: a review. – Biol. Conserv. 70: 265–276.
Newton, I. 2010. Population ecology of raptors. – Poyser.
Ogada, D. L. 2014. e power of poison: pesticide poisoning of
Africa's wildlife. – Ann. N. Y. Acad. Sci. 1322: 1–20.
Ogada, D., Shaw, P., Beyers, R. L., Buij, R., Murn, C., iollay,
J.-M., Beale, C. M., Holdo, R. M., Pomeroy, D., Baker, N.,
Krueger, S., Botha, A., Virani, M. Z., Monadjem, A. and
Sinclair, A. R. E. 2016. Another continental vulture crisis:
Africa's vultures collapsing toward extinction. – Conserv. Lett.
9: 89–97.
Ogutu, J. O., Piepho, H. P., Dublin, H. T., Bhola, N. and Reid,
R. S. 2008. Rainfall inuences on ungulate population
abundance in the Mara-Serengeti ecosystem. – J. Anim. Ecol.
77: 814–829.
Ogutu, J. O., Piepho, H. P., Dublin, H. T., Bhola, N. and Reid,
R. 2009. Dynamics of Mara-Serengeti ungulates in relation to
land use changes. – J. Zool. 278: 1–14.
Pain, D. J., Cunningham, A. A., Donald, P. F., Duckworth, J. W.,
Houston, D. C., Katzner, T., Parry-Jones, J., Poole, C., Prakash,
V., Round, P. and Timmins, R. 2003. Causes and eects of
temporospatial declines of Gyps vultures in Asia. – Conserv.
Biol. 17: 661–671.
Phipps, W. L., Willis, S. G., Wolter, K. and Naidoo, V. 2013.
Foraging ranges of immature african white-backed vultures
(Gyps africanus) and their use of protected areas in southern
Africa. – PloS One 8: e52813.
iollay, J. M. 2006a. e decline of raptors in West Africa: long-
term assessment and the role of protected areas. – Ibis 148:
240–254.
iollay, J. M. 2006b. Severe decline of large birds in the Northern
Sahel of West Africa: a long-term assessment. – Bird Conserv.
Int. 16: 353–365.
iollay, J. M. 2007. Raptor population decline in West Africa.
– Ostrich 78: 405–413.
Vanak, A. T., Shannon, G., aker, M., Page, B., Grant, R. and
Slotow, R. 2012. Biocomplexity in large tree mortality:
interactions between elephant, re and landscape in an African
savanna. – Ecography 35: 315–321.
Virani, M., Kirui, P., Monadjem, A., omsett, S. and Githiru, M.
2010. Nesting status of African white-backed vultures Gyps
africanus in the Masai Mara National Reserve, Kenya. – Ostrich
81: 205–209.
Virani, M. Z., Kendall, C., Njoroge, P. and omsett, S. 2011.
Major declines in the abundance of vultures and other
scavenging raptors in and around the Masai Mara ecosystem,
Kenya. – Biol. Conserv. 144: 746–752.
Virani, M., Monadjem, A., omsett, S. and Kendall, C. 2012.
Seasonal variation in breeding Rüppell’s Vultures (Gyps
rueppellii) at Kwenia, southern Kenya with implications for
conservation. – Bird Conserv. Int. 22: 260–269.
Walpole, M. J., Nabaala, M. and Matankory, C. 2004.
Status of the Mara Woodlands in Kenya. – Afr. J. Ecol. 42:
180–188.
Zuberogoitia, I., Zabala, J., Martinez, J. A., Martinez, J. E.
and Azkona, A. 2008. Effect of human activities on
Egyptian vulture breeding success. – Anim. Conserv. 11:
313–320.
Supplementary material (Appendix JAV-01497 at <www.
avianbiology.org/appendix/jav-01497>). Appendix 1–2.
