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Contributed Paper
Priority areas for conservation of Old World vultures
Andrea Santangeli ,1,2 ∗Marco Girardello,3Evan Buechley,4, 5 Andre Botha,6
Enrico Di Minin ,2,7, 8 and Atte Moilanen9,10
1The Helsinki Lab of Ornithology, Finnish Museum of Natural History, University of Helsinki, Helsinki FI-00014, Finland
2Helsinki Institute of Sustainability Science, University of Helsinki, Helsinki FI-00014, Finland
3cE3c - Centre for Ecology, Evolution and Environmental Changes/Azorean Biodiversity Group and Universidade. dos Ac¸ores – Depto
de Ciˆ
encias e Engenharia do Ambiente, Angra do Hero´
ısmo, Ac¸ores, PT-9700-042, Portugal
4HawkWatch International, Salt Lake City, UT 84106, U.S.A.
5Department of Biology, University of Utah, Salt Lake City, UT 84112, U.S.A.
6Endangered Wildlife Trust, Modderfontein 1609, South Africa
7Digital Geography Lab, Department of Geosciences and Geography, University of Helsinki, Helsinki, FI-00014, Finland
8School of Life Sciences, University of KwaZulu-Natal, Durban, 4000, South Africa
9Finnish Museum of Natural History Luomus, University of Helsinki, P.O. Box 17, Helsinki, FI-00014, Finland
10Department of Geosciences and Geography, University of Helsinki, Helsinki, FI-00014, Finland
Abstract: The prosperity and well-being of human societies relies on healthy ecosystems and the services
they provide. However, the biodiversity crisis is undermining ecosystems services and functions. Vultures are
among the most imperiled taxonomic groups on Earth, yet they have a fundamental ecosystem function. These
obligate scavengers rapidly consume large amounts of carrion and human waste, a service that may aid in
both disease prevention and control of mammalian scavengers, including feral dogs, which in turn threaten
humans. We combined information about the distribution of all 15 vulture species found in Europe, Asia, and
Africa with their threats and used detailed expert knowledge on threat intensity to prioritize critical areas for
conserving vultures in Africa and Eurasia. Threats we identified included poisoning, mortality due to collision
with wind energy infrastructures, and other anthropogenic activities related to human land use and influence.
Areas important for vulture conservation were concentrated in southern and eastern Africa, South Asia, and
the Iberian Peninsula, and over 80% of these areas were unprotected. Some vulture species required larger
areas for protection than others. Finally, countries that had the largest share of all identified important pri-
ority areas for vulture conservation were those with the largest expenditures related to rabies burden (e.g.,
India, China, and Myanmar). Vulture populations have declined markedly in most of these countries. Restor-
ing healthy vulture populations through targeted actions in the priority areas we identified may help restore
the ecosystem services vultures provide, including sanitation and potentially prevention of diseases, such as
rabies, a heavy burden afflicting fragile societies. Our findings may guide stakeholders to prioritize actions
where they are needed most in order to achieve international goals for biodiversity conservation and sustainable
development.
Keywords: African-Eurasian vultures, biodiversity benefits, ecosystem balance, ecosystem service, scavenger
conservation, Zonation software
´
Areas Prioritarias para la Conservaci´
on de Buitres del Viejo Mundo
Resumen: La prosperidad y el bienestar de la sociedad humana dependen de ecosistemas sanos y de los
servicios ambientales que ´
estos proporcionan. Sin embargo, la crisis de biodiversidad est´
a afectando a los servicios
ambientales y sus funciones. Los buitres se encuentran entre los grupos taxon´
omicos con mayor amenaza sobre
el planeta, a pesar de tener una funci´
on fundamental en los ecosistemas. Estos carro˜
neros obligados consumen
∗email andrea.santangeli@helsinki.fi
Article impact statement: Eighty percent of areas important for Old World vulture conservation are unprotected and in southern and eastern
Africa, South Asia, and Iberia.
Paper submitted April 7, 2018; revised manuscript accepted January 11, 2019.
This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction
in any medium, provided the original work is properly cited.
1056
Conservation Biology, Volume 33, No. 5, 1056–1065
C
2019 The Authors. Conservation Biology published by Wiley Periodicals, Inc. on behalf of Society for Conservation Biology.
DOI: 10.1111/cobi.13282
Santangeli et al. 1057
r´
apidamente grandes cantidades de carro˜
na y desechos humanos, un servicio que puede ayudar en la prevenci´
on
de enfermedades y en el control de mam´
ıferos carro˜
neros, incluyendo a los perros ferales, los cuales pueden ser
un peligro para los humanos. Combinamos la informaci´
on sobre la distribuci´
on de las 15 especies de buitres
en Europa, Asia y ´
Africa con las amenazas que presentan y usamos el conocimiento detallado de expertos
sobre la intensidad de las amenazas para priorizar las ´
areas cr´
ıticas para la conservaci´
on de buitres en ´
Africa
y en Eurasia. Las amenazas que identificamos incluyeron el envenenamiento, la mortalidad por colisiones con
infraestructura e´
olica y otras actividades antropog´
enicas relacionadas con el uso de suelo y la influencia humana.
Las ´
areas importantes para la conservaci´
on de buitres estuvieron concentradas en el sur y el este de ´
Africa, el
sur de Asia y la Pen´
ınsula Ib´
erica, y m´
as del 80% de estas ´
areas no contaban con protecci´
on. Algunas especies
de buitres requirieron ´
areas m´
as grandes para su protecci´
on que otras especies. Finalmente, los pa´
ıses que
tuvieron la mayor porci´
on de todas las ´
areas prioritarias importantes e identificadas para la conservaci´
on de
buitres tambi´
en fueron aquellos con los mayores gastos relacionados con la carga de la rabia (por ejemplo,
India, China y Myanmar). Las poblaciones de buitres han declinado marcadamente en la mayor´
ıa de estos pa´
ıses.
La restauraci´
on de poblaciones sanas de buitres por medio de acciones enfocadas en las ´
areas prioritarias que
identificamos puede ayudar a restaurar los servicios ambientales que proporcionan los buitres, incluyendo el
saneamiento y la prevenci´
on potencial de enfermedades, como la rabia, una carga pesada que aflige a las sociedades
fr´
agiles. Nuestros resultados pueden guiar a los interesados hacia la priorizaci´
on de acciones en donde m´
as se
necesitan para poder alcanzar los objetivos internacionales para la conservaci´
on de la biodiversidad y el desarrollo
sustentable.
Palabras Clave: balance ambiental, beneficios de la biodiversidad, buitres africanos – euroasi´
aticos, conservaci´
on
de carro˜
neros, servicio ambiental, software Zonation
:,
,
,,,
,
,
,
,80% ,
,
(),
,,
,
,:;:
:-, Zonation ,,,,
Introduction
The health and well-being of human societies heav-
ily relies on the services that healthy ecosystems pro-
vide, which in turn depend on biodiversity (Bennett
et al. 2015). However, current unprecedented biodi-
versity loss can undermine the foundations of ecosys-
tems resilience and associated services (Cardinale et al.
2012). The agenda for averting biodiversity decline has
been internationally formalized through the Convention
on Biological Diversity’s 2020 Strategic Plan for Biodi-
versity (Aichi targets; Secretariat of the Convention on
Biological Diversity 2014), which is linked to the UN
2030 Sustainable Development Goals (United Nations
2015).
Not all species are equally important in maintaining
ecosystems resilience (D´
ıaz et al. 2006), and species
groups have widely different population statuses and
trends (Butchart et al. 2004). As the sole obligate scav-
engers, vultures comprise a unique functional guild
among vertebrates and play an unparalleled role in
maintaining ecosystem balance (Buechley & S¸ekercio˘
glu
2016). Yet, they are among the species most threatened
with extinction (Buechley & S¸ekercio˘
glu 2016; O’Bryan
et al. 2018). By efficiently consuming carrion (Ogada et al.
2012), vultures may help control the spread of disease
and of facultative scavenger species that can cause hu-
man injury or death, such as feral dogs (Markandya et al.
2008; Ogada et al. 2012). Vultures also play a key role
in terms of waste-disposal services and nutrient cycling
(e.g., Gangoso et al. 2013; Mole´
on et al. 2014). Replacing
these services could entail substantial costs and added
greenhouse gas emissions, for example, from incinera-
tion of carcasses (Markandya et al. 2008; Morales-Reyes
et al. 2017; O’Bryan et al. 2018). Vultures are threat-
ened by many anthropogenic drivers, such as poisons
and other dietary toxins, direct persecution, collision
with infrastructures and electrocution, disturbance, and
Conservation Biology
Volume 33, No. 5, 2019
1058 Old World Vultures
habitat loss and degradation (Buechley & S¸ekercio˘
glu
2016; Botha et al. 2017). More regionally, for example,
in Europe, vultures are also threatened by food short-
age following sanitary regulations (Margalida & Mole´
on
2016) or abandonment of traditional farming practices
(e.g., Olea & Mateo-Tom´
as 2009). The extent of these
threats and their consequences on vulture population
persistence varies across the world’s regions (Buechley &
S¸ekercio˘
glu 2016; Ogada et al. 2016b; Botha et al. 2017);
threats are most intense in the Old World, where most
vulture species are at high risk of extinction (Buechley &
S¸ekercio˘
glu 2016).
Preventing extinctions of Old World vultures is pos-
sible, as examples from Europe and Asia demonstrate
(Chaudhry et al. 2012; Moreno-Opo & Margalida 2013).
However, given an accelerating decline of vulture popula-
tions (Buechley & S¸ekercio˘
glu 2016; Ogada et al. 2016b),
there is an urgent need for action. Recently, a Multi-
Species Action Plan to Conserve African-Eurasian Vul-
tures (MSAP) has been formalized (Botha et al. 2017) that
lists effective actions to conserve African-Eurasian vul-
tures and brings them to the top of the international con-
servation policy agenda. Although commitments to act
and knowledge about threats have been established, lim-
ited resources impair wide-scale implementation. There-
fore, there is a need to identify priority areas for vulture
conservation through conservation planning approaches
(Moilanen et al. 2005). Such approaches require in-
formation about the distributions of biodiversity and
associated threats; however, such information is often
lacking (Joppa et al. 2016).
We combined spatially explicit data sets of relevant
threats with vulture distributions to provide novel and
timely insight into priority areas for vulture conserva-
tion across the Old World. We first identified priority
areas where vultures and major threats, such as poison-
ing, wind energy infrastructure, and other human pres-
sures, co-occur. Second, we assessed the relationship
between these priority areas and geopolitical (e.g., gov-
ernance) and biodiversity conservation characteristics of
the countries hosting those priorities. Governance and
other national indicators are strong correlates of national
investment into biodiversity conservation (Amano et al.
2017; Baynham-Herd et al. 2018). Third, we explored
the relationship between vulture priority areas identified
and the national incidence of rabies mortality and asso-
ciated costs. This was assessed because the decline of
vultures has been linked with simultaneous increases in
numbers of feral dogs and other mammalian scavengers
(Markandya et al. 2008; Ogada et al. 2012) that spread
diseases such as rabies. Potential linkage between loss
of vultures and increased human disease burden under-
scores a potential synergistic opportunity for conserv-
ing vultures while helping control disease (Markandya
et al. 2008; Hampson et al. 2015; O’Bryan et al.
2018).
Methods
Vulture Distributions
We focused on all vulture species of Africa and Eurasia,
excluding the palm nut vulture (Gypohierax angolen-
sis), which is not an obligate scavenger and faces differ-
ent threats compared with other vultures (Buechley &
S¸ekercio˘
glu 2016). Thus, we examined the 15 species
that are the focus of the MSAP (Botha et al. 2017). We
combined different data sources and used geostatistics to
derive spatial layers of vulture distributions and threats.
Details on how different spatial layers were derived are
given in Supporting Information.
We extracted the resident and breeding range of each
of the 15 vultures (BirdLife International and NatureServe
2015) and refined occurrence within those ranges with
a statistical species distribution modeling (SDM) frame-
work. We combined vulture occurrence data from the
Global Biodiversity Information Facility and from the
African Raptor DataBank from 1980 onward (Supporting
Information). We filtered out duplicates and occurrences
closer than 30 km from each other to minimize spatial
autocorrelation (Aiello-Lammens et al. 2015). Vulture ob-
servations were then correlated with environmental vari-
ables (e.g., climate, land-cover, and topography [details
given in Supporting Information]) with SDMs (including
generalized linear models, random forest, boosted regres-
sion trees, and Maxent). Finally, we used an ensemble of
the above SDMs (Urban et al. 2016) to derive consensus
occurrence probabilities within the breeding and resi-
dent distribution range of each species.
Unintentional and Intentional Poisoning
A major threat to vultures is unintentional poisoning, in
which vultures are killed as a side-effect when farmers
use poison to kill carnivores following livestock depreda-
tion (Mateo-Tomas et al. 2012; Buechley & S¸ekercio˘
glu
2016; Ogada et al. 2016b). To a lesser degree and in
specific regions (e.g., Europe), poisoning may also occur
when hunters attempt to regulate competitor carnivore
populations (Mateo-Tomas et al. 2012). Overall, human–
carnivore conflict is a strong determinant of unintentional
poisoning risk (Mateo-Tomas et al. 2012; Santangeli et al.
2016a).
Therefore, we derived a map showing the intensity
of potential human–carnivore conflict across the study
region by interacting distributions of carnivores (IUCN
2017) with those of selected livestock (Robinson et al.
2014) matched by body mass (i.e., carnivores were
matched with potential livestock prey species). Matching
was done by searching literature for reported predation
of each carnivore species on each of 3 livestock cate-
gories (poultry, including duck and chicken; small stock,
including sheep, goats, and pigs; large stock, including
Conservation Biology
Volume 33, No. 5, 2019
Santangeli et al. 1059
cattle and buffalo) (Supporting Information). This liter-
ature search suggested that poultry could be predated
on by any carnivore, small stock by carnivores ࣙ2kg,
and large stock by carnivores ࣙ10 kg. We then multi-
plied the density of each of the 3 livestock classes with
the average per-pixel (10 ×10 km grid cell) body mass
of selected carnivores, resulting in 3 maps (Supporting
Information). We used average body mass of selected
carnivores because we were interested in a community-
weighted mean trait value of the carnivores composing
a specific assembly, following, for example, D´
ıaz et al.
(2007). To obtain an overall index of human–carnivore
conflict, we averaged the above 3 maps, weighted by the
natural log of the body mass of each livestock class (Sup-
porting Information). By weighting the maps by the log
of the body mass of each livestock class, we aimed at as-
signing a higher weight to the interaction between larger
stock and selected carnivores. This is associated with
higher economic losses (a cow has a much higher eco-
nomic value than a goat (details given in Supporting Infor-
mation), implying a stronger trigger for poisoning and el-
evated threat intensity because larger poisoned carcasses
are more likely consumed by vultures. Finally, we visually
validated the resulting priority areas for vulture conser-
vation (based on the 15 vulture species and poisoning
layers) with independent data on known poisoning loca-
tions (details given in Supporting Information).
Across Sub-Saharan Africa, a recently uncovered threat
to vultures is represented by poachers intentionally poi-
soning vultures to eliminate their sentinel function (i.e.,
indicating to authorities where poaching has occurred by
circling over carcasses) (Ogada et al. 2016a; Botha et al.
2017). To map this threat, we identified the herbivore
and carnivore species targeted by poachers based on in-
formation on the occurrence and frequency of ungulates
and carnivores found poisoned from 2007 onward (En-
dangered Wildlife Trust and the Peregrine Fund 2017).
This search suggested that the carcasses of medium- to
large-sized herbivores (e.g., body mass of 53 kg for im-
pala [Aepyceros melampus] and above) and 2 carnivores
(lion [Panthera leo] and leopard [Panthera pardus]) are
poisoned to intentionally kill vultures; some species were
targeted more often than others. Because not all poison-
ing incidences have been detected and reported in the
database, we conservatively selected all Cetartiodactyla
and Perissodactyla species of Africa with body mass ࣙ
20 kg and the African elephant (Loxodonta africana),
lion, and leopard (Ogada et al. 2016a). This resulted in
72 species, to each of which we assigned a conservative
weight based on the log of the frequency of its occur-
rence in the African wildlife poisoning database (Support-
ing Information). Thus, species that are more often re-
ported in the database had a comparatively higher weight
in driving the intentional poisoning map compared with
species reported once or never (the latter 2 equally re-
ceived the lowest weight) (Supporting Information). We
then used the International Union for Conservation of
Nature (IUCN 2017) range maps of the 72 target species
of intentional poisoning and the species-specific weight
to derive a single map of sentinel poisoning risk. In do-
ing so, we calculated the average of the species-specific
weight of intentional poisoning across all species present
in each 10 ×10 km pixel within the range of the study
area in Africa (Supporting Information).
Wind Collision Risk
We used Pogson et al.’s (2013) map of wind-power po-
tential as a proxy for exposure to collision with wind
turbines, a major threat to vultures (Pearce-Higgins &
Green 2014; Ogada et al. 2016b; Botha et al. 2017). This
map approximates installed and planned national wind
energy capacity (REN21 2017; Santangeli et al. 2018) and
has been used to evaluate impacts of wind energy ex-
pansion on biodiversity (Santangeli et al. 2016b, 2016c,
2018).
Human Influence Index
Collision with and electrocution on energy infrastructure,
human disturbance, habitat degradation, and decline in
food availability are further important threats to vultures
(Botha et al. 2017). These 5 threats are all linked to
human influence and were captured by a single proxy
layer: the Global Human Influence Index (GHII) (Wildlife
Conservation Society and Center for International Earth
Science Information Network 2005). The GHII combines
information on human population pressure, land use, in-
frastructure, and accessibility (details given in Supporting
Information).
Treatment of Expert Knowledge
The priority of each of the above threats to vultures varies
regionally and has been recently quantified as part of the
MSAP by experts using standardized classes of critical,
high, and medium or low priority (Botha et al. 2017). We
incorporated this information by assigning a weight of 2
to critical threats, 1.5 to high threats, and 1 to medium
to low threats by region (Botha et al. 2017) (Supporting
Information). We then refined the spatial threat layers
by multiplying their original values with the assigned
threat-specific regional weight (Supporting Information).
Because GHII represents a proxy for 5 threats, the sum
of weights of the 5 threats per region was used. The
resulting 4 spatial layers would ultimately represent the
spatial distribution of threats, weighted by priority, as
assessed by experts (Supporting Information).
Conservation Biology
Volume 33, No. 5, 2019
1060 Old World Vultures
Spatial Prioritization Analyses
We used the software Zonation version 4.0 (Moilanen
et al. 2014) to identify priority areas for vulture conserva-
tion across Africa and Eurasia. Heuristically expressed, we
sought to identify areas where many vultures occur and
threats are most intense. It is important that the threats
incorporated here can be reduced with specific actions
(e.g., Woodroffe et al. 2005; Northrup & Wittemyer 2013;
Botha et al. 2017; Murn & Botha 2018). Zonation devel-
ops spatial priority rankings based on the distributions
of biodiversity features (e.g., vultures) and, optionally,
on threats or costs. It is an important characteristic of
Zonation that complementarity is accounted for (i.e., a
balanced representation across all features is maintained
through the priority ranking) (Moilanen et al. 2014).
We used the core area method (CAZ; Moilanen et al.
2005) as the ranking method, with the interpretation
that high-priority areas should include locally high-
quality areas for all species individually (Moilanen et al.
2005). All feature layers (vulture distributions and their
threats) were rasterized to the resolution of 10 ×10
km, and each threat layer was rescaled to between 0
and 1 prior to analyses. The adopted resolution was
deemed most appropriate given the available distribu-
tion data on vultures and their threats. Commission
errors (i.e., predicting presence incorrectly) are mini-
mized for the vulture distributions because these species’
ranges are well known and because they have been re-
fined here with a robust SDM approach (details given in
Supporting Information). Similarly, the underlying data
used to derive the threat layers had a resolution of 10
×10 km or higher or an appropriate original resolution
given that used here (Montesino Pouzols et al. 2014). In
all analyses, each vulture species was given a specific
weight based on its IUCN Red List status following Di
Minin et al. (2016) (weights: 1, least concern; 2, near
threatened; 3, vulnerable, 4, endangered, 5, critically en-
dangered; none, data deficient).
We first ran 4 separate prioritization analyses, each
including the distributions of the 15 vultures and with
each of the 3 threats included in turn: unintentional and
intentional poisoning together, wind energy, and GHII.
Next, we ran a holistic scenario in which all 3 threats and
the 15 vultures were included. For all scenarios, threat
layers were weighted so that their aggregate weight
equaled the aggregate weight of all vulture species, fol-
lowing Montesino Pouzols et al. (2014). This ensured
a balanced representation between areas important for
vulture conservation and areas where threats are most in-
tense. These prioritization analyses deliver maps showing
the priority areas for vulture conservation where threats
are most intense. We further extracted the 30% of priority
areas most important (i.e., all pixels with ranked value
>0.7 [Fig. 1]) (rationale below) for vulture conservation
(hereafter, vulture priority areas) (rationale discussed be-
low), converted them into vector files, and calculated
the area of overlap with the global network of pro-
tected areas (PAs) (i.e., IUCN protected-area categories
I–VI obtained from UNEP-WCMC and IUCN [2017]) and
important bird and biodiversity areas (IBAs) (BirdLife In-
ternational 2014). We also identified the number of IBAs
in danger (i.e., under high pressure in 2018) (BirdLife
International 2014) that at least partly overlapped with
the above vulture priority areas. Robustness to the un-
certainty associated with the species distributions and
selected threat layers, as well as to changes in the rel-
ative weight assigned to each feature, was assessed by
means of sensitivity analyses (details given in Supporting
Information).
National-Level Analyses
We calculated the national share of the vulture priority
areas (pixels with rank >0.7) (Fig. 1) following Butchart
et al. (2015), Santangeli et al. (2018), and Santangeli et al.
(2016b). Although the top 30% threshold used here is
somewhat arbitrary, it represents a balanced trade-off
between allowing enough protection for vulture ranges
and the reality of resource limitations and societal con-
straints on implementation. We used this value as the
response in a beta regression model (because the re-
sponse is a percentage) aiming to quantify its relationship
with national socioeconomic, governance, and environ-
mental indicators (Di Minin et al. 2016; Amano et al.
2017; Baynham-Herd et al. 2018), as well as national
incidence of and costs related to rabies (Hampson et al.
2015) (Supporting Information). Prior to analyses, we
log transformed and rescaled all predictor variables. A
variance inflation analysis (VIF) run on the set of predic-
tors indicated that country size and human development
index had high VIF values (i.e., >3) and were therefore
excluded. The remaining predictors (governance, per-
cent terrestrial PAs, rabies costs, and incidences) were
largely uncorrelated (VIF <2). We applied multimodel
selection and averaging based on the best models (with
࢞AIC <4) (Burnham & Anderson 2002) to quantify the
relative importance and relationship of each predictor
with the response variable with the package MuMIn in
R version 3.0.3 (Barto´
n 2014). Model validation was per-
formed by inspecting the residuals. There was no sign of
violation of model assumptions. We repeated the above
analyses with national share of vulture priority areas as
the response variable, calculated by considering in turn
the top 20% and 40% of priority areas.
Results
The prioritization analysis indicated the highest priority
areas for vulture conservation across the Old World were
concentrated in southern and eastern Africa, southern
Conservation Biology
Volume 33, No. 5, 2019
Santangeli et al. 1061
Europe, Central and East Asia
West Asia
East Africa
West and Central Africa
North Africa
South Asia
Southern A
Conservation priority:
1
0.9
0.8
0.7
0.6
0.5
0.4
0.3
0.2
0.1
0
frica
South East Asia
Figure 1. Priority areas for vulture conservation identified through spatial conservation prioritization across
Africa and Eurasia (gray, outside breeding and resident range of any of the 15 vultures considered). Priorities are
ranked from highest (red) to lowest (green). The abrupt shift in priorities across some country borders is due to
the different weights assigned to threats within 8 subregions (black lines) based on expert knowledge (Supporting
Information).
Figure 2. Continental (black) and
regional (gray) share of the 30% of
priority areas most important for
vulture conservation (red areas in
Fig. 1). Geographic regions
considered are those defined in the
Multi-Species Action Plan to
Conserve African-Eurasian Vultures
(Botha et al. 2017) (Supporting
Information).
Conservation Biology
Volume 33, No. 5, 2019
1062 Old World Vultures
Figure 3. Zonation performance
curves showing the relation between
conservation coverage of the range
of each vulture species (y-axis: 1, all
species’ ranges protected) and
hypothetical proportions of the
landscape protected for vultures
(x-axis: 1, entire study area
protected) (gray, 30% of priority
areas most important for vulture
conservation). Species-specific
conservation coverage can be
determined from the y-axis, where
the rightmost edge of the gray area
(x =0.3) intersects the
species-specific performance curve.
Europe, the Arabian Peninsula, and the Indian subcon-
tinent (Fig. 1). About 95% of the top-ranked 30% pri-
ority areas for vulture conservation in the region fell
within Africa (51.6%) and Asia (43.5%), and within these
southern Africa, East Africa, and South Asia each sup-
ported over 20% of the top 30% ranked areas for vulture
conservation (Fig. 2). The high-priority areas for vulture
conservation as shown in Figure 1 are typically affected
by multiple threats, particularly poisoning and other
threats associated with human influence (Supporting In-
formation). The above results were robust (i.e., had low
sensitivity to the uncertainty associated with the vulture
distributions and selected threats or to changes in the
weight assigned to each feature) (Supporting Informa-
tion). About one-fifth of the top 30% vulture priority areas
shown in Figure 1 were covered by the global PA network
(19%), whereas 12% of them were covered by IBAs. More-
over, 38 of the IBAs overlapping vulture priority areas had
been classified by BirdLife International as being in dan-
ger, largely owing to high pressures to develop these ar-
eas. Species-specific performance curves showed the in-
crease in (conservation) coverage of each vulture species’
distribution as a function of area selected (Fig. 3). These
curves clearly indicated that protection efforts will not
be similarly effective for all species. Some species, such
as Gyps tenuirostris and Gyps coprotheres,wouldreach
almost full range coverage if just 30% of the landscape
were protected. Others, such as Aegypius monachus and
Gypaetus barbatus, would require a much larger fraction
of land to be protected for their ranges to be adequately
covered (Fig. 3). These differences between species were
explained by different distribution sizes and overlaps of
species distribution: small overlapping ranges can be pro-
tected much easier than large nonoverlapping ranges.
We found that countries harboring the highest share
of vulture priority areas were those that incurred the
Figure 4. Relationship between proportion of
national share of vulture priority areas (i.e., the 30%
of priority areas most important for vulture
conservation; red areas in Fig. 1) and the total
national costs related to the burden of rabies ($US in
2010 per year on a log scale; dots, separate countries;
black line, relationship as predicted by the beta
regression model [see Table 1 and Methods]).
highest economic costs, but not human mortality inci-
dences, associated with the burden of rabies (Fig. 4), and
those with good governance (Table 1). Analyses based on
the top 20% and 40% priority areas confirmed the above
results.
Discussion
By combining vulture distributions with their threats
and using regional expert knowledge on threat inten-
sity, we produced the first holistic map of priority areas
Conservation Biology
Volume 33, No. 5, 2019
Santangeli et al. 1063
Table 1. Fit of a beta regression model quantifying the relationship
between national share of the 30% of priority areas most important for
vulture conservation (red areas in Fig. 1) and 5 national-level variables
(predictors described in Supporting Information).
Variable βSE Z p
Intercept −4.69 0.14 32.46 <0.001
Governance 0.24 0.11 2.13 0.033
Terrestrial protected
areas (%)
0.12 0.11 1.10 0.273
Rabies costs 0.72 0.10 7.16 <0.001
Rabies incidence 0.03 0.11 0.28 0.782
for vulture conservation across Africa and Eurasia. We
found that high-priority areas were mostly concentrated
in southern and eastern Africa, South Asia, and the Iberian
Peninsula. These areas were largely unprotected. We
found major differences in the species-specific perfor-
mance curves, highlighting that some species would re-
quire larger areas for protection than others. Finally, we
showed that countries holding the largest share of pri-
ority areas for vulture conservation were those that also
paid the highest costs from rabies burden (such as India,
China, and Myanmar).
Priority areas for vulture conservation identified here
represented large areas that were clustered within spe-
cific regions and countries. Although this aggregation
of priorities may represent a challenge due to the dis-
proportionate responsibility of some countries toward
vulture conservation, it may also present an opportunity,
due to the limited number of countries and stakeholders
involved. Actions to revert the major threats to vultures
are broadly known (Buechley & S¸ekercio˘
glu 2016; Botha
et al. 2017). Although some of these actions, such as
rapid response interventions on poisoning events and
supplementary feeding stations, may reduce adverse im-
pacts from threats such as poisoning (Cortes-Avizanda
et al. 2016; Murn & Botha 2018), these are short-term
solutions only. Fundamentally, actions of wide temporal
and spatial scope and impact are needed. Among these,
design and strong enforcement of targeted legislation
would help restrict the distribution and use of drugs
and poisons that threaten vultures (Ogada 2014). Sim-
ilarly, strict regulations to ensure proper environmental
impact assessments and planning would help reduce risks
from wind energy and other infrastructure development
in areas important for vulture conservation. For region-
ally localized threats, locally targeted measures could
play a key role. For example, the Protection Areas for
the Feeding of Necrophagous Species of European In-
terest (EC 142/2011) program in the Iberian Peninsula
allows farmers to leave livestock carcasses in the field,
providing food for vultures (Morales-Reyes et al. 2017).
This practice was banned following bovine spongiform
encephalopathy in Europe. Ultimately, it will be impor-
tant to identify the relevant local stakeholders, such as
communities, nongovernmental organizations, govern-
ment institutions, private, and state-owned companies,
and address the threats with a participatory, community-
engaged approach.
Our results also highlight that restricting conservation
efforts toward vulture priority areas as identified here
(Fig. 1) may be effective for some species but inadequate
for others (Fig. 3). Species with a restricted distribution,
such as G. tenuirostris and G. coprotheres, would benefit
from actions that target threats inside the vulture priority
areas. Conversely, widespread species, such as G. bar-
batus and A. monachus, will require action across very
large areas.
We found a positive relationship between national gov-
ernance and the share of vulture priority areas. This indi-
cates that vulture priority areas are more concentrated
in countries with good governance. National govern-
ments can play a key role for vulture conservation, as
the Asian case indicates (e.g., Prakash et al. 2012). Over-
all, governance levels may drive the cost-effectiveness
of conservation (Amano et al. 2017), and the potential
implications of this should be considered when defin-
ing actions targeting vulture priority areas. To this end,
local and national stakeholder participation will be key
to designing national- and regional-level actions that will
be feasible to implement and cost-effective under each
specific context, governance level included.
We found correlative evidence that countries investing
large financial resources to counter rabies also held the
largest shares of vulture priority areas. In many of these
areas, vulture populations have declined markedly over
the past decades, leading to a loss of their waste removal
and potential disease regulating services (Pain et al. 2008;
Ogada et al. 2012; Buechley & S¸ekercio˘
glu 2016). By
rapidly consuming carrion, vultures reduce access to car-
rion and direct contact between mammalian scavengers
(Ogada et al. 2012) and thus have been theorized to help
mitigate the spread of diseases such as rabies (Markandya
et al. 2008). Spread of rabies leads to increased livestock
and human mortality and increased public health expen-
diture, causing high rabies-related economic costs in Asia
and Africa (Hampson et al. 2015). The positive correlation
between national economic spending for rabies and vul-
ture priority areas that we found may highlight a potential
opportunity for restoring vulture populations that could
simultaneously result in national savings from reduced
rabies burden. However, the extent and value of potential
disease control provided by vultures needs to be better
demonstrated with empirical evidence (O’Bryan et al.
2018). At present, this evidence is largely correlative and
localized, thereby preventing firm conclusions about the
link (or lack thereof) between vultures and disease, in-
cluding rabies. Localized evidence is available, for exam-
ple, from a study in India, which reported that when the
national vulture populations dropped by 99% from 1992
to 2003, feral dog numbers increased and so did cases
Conservation Biology
Volume 33, No. 5, 2019
1064 Old World Vultures
of human dog bites and rabies (Markandya et al. 2008).
This occurred despite widespread and very expensive
dog sterilization programs over the period (Markandya
et al. 2008).
Although there has been recent progress to bring vul-
ture conservation to the top of the international conserva-
tion science and policy agenda (Botha et al. 2017), there
is now an urgent need to mobilize funds and implement
action. Our findings can help guide direct action where
it is needed most. Saving vultures is not only a matter of
conservation ethics and principle, but also about saving
a unique functional guild that provides key ecosystem
services (Markandya et al. 2008; Buechley & S¸ekercio˘
glu
2016). No other functional guild is dominated by a group
of so few and yet so endangered species.
Acknowledgments
A.S. and E.D.M. are funded by the Academy of Finland
(grants 307909 and 296524) and E.R.B is funded by Hawk-
Watch International and National Geographic Society.
We thank C. Mclure and 3 other anonymous referees for
valuable comments on an earlier draft of the manuscript.
For providing African vulture observation data included
in the ARDB (African Raptor DataBank), we particularly
thank C.R. Barlow, Birds of The Gambia, E. Brouhaugh,
Sabi, N. and L. Baker, and U. Lieden, T. Wacher, and J.
Brouwer, who manage the West African Bird DataBase,
and T. Wacher (Sahara Conservation Fund and Zoological
Society London), who collected most of the WABDaB
vulture data for Chad, and A. Harouna, T. Rabeil,
T. Wacher, and No´
e Conservation, who collected data
for Niger.
Supporting Information
Additional methods (Appendix S1); count of vulture oc-
currence data (Appendix S2); list of land-cover categories
(Appendix S3); SDM model performance (Appendix S4);
list of carnivore species and attributes (Appendix S5);
interactions of large stock, small stock, and poultry
with carnivores (Appendix S6–8); livestock–carnivore in-
teractions (Appendix S9); validation of poisoning layer
(Appendix S10); list of species used for intentional poi-
soning layer (Appendix S11); intentional poisoning layer
(Appendix S12); threat intensity by region (Appendix
S13); threat weights by region (Appendix S14); descrip-
tion of national predictors (Appendix S15); priority ar-
eas from intermediate scenarios (Appendix S16); vali-
dation priority areas (Appendix S17); and sensitivity of
priorities to weight changes (Appendix S18) are avail-
able online. The authors are solely responsible for the
content and functionality of these materials. Queries
(other than absence of the material) should be di-
rected to the corresponding author. Priority maps of
the holistic scenario and alternative intermediate sce-
narios are available from https://vultureconservation.
shinyapps.io/vulturepriorities/.
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