Spatial Heterogeneity in Resource Distribution Promotes

Facultative Sociality in Two Trans-Saharan Migratory

Birds
Ainara Cortés-Avizanda1*, Pablo Almaraz2, Martina Carrete1,3, José A. Sánchez-Zapata2, Antonio
Delgado4, Fernando Hiraldo1, José A. Donázar1
1 Department of Conservation Biology, Estación Biológica de Doñana, Consejo Superior de Investigaciones Cientı́ficas, Sevilla, Spain, 2 Department of Applied Biology,
Universidad Miguel Hernández, Orihuela, Alicante, Spain, 3 Department of Physical, Chemical and Natural Systems, Universidad Pablo de Olavide, Sevilla, Spain,
4 Laboratorio de Biogeoquı́mica de Isótopos Estables, Estación Experimental del Zaidı́n, Consejo Superior de Investigaciones Cientı́ficas, Granada, Spain

Abstract
Background: Migrant populations must cope not only with environmental changes in different biomes, but also with the
continuous constraints imposed by human-induced changes through landscape transformation and resource patchiness.
Theoretical studies suggest that changes in food distribution can promote changes in the social arrangement of individuals
without apparent adaptive value. Empirical research on this subject has only been performed at reduced geographical
scales and/or for single species. However, the relative contribution of food patchiness and predictability, both in space and
time, to abundance and sociality can vary among species, depending on their degree of flexibility.

Methodology/Principal Findings: By means of constrained zero-inflated Generalized Additive Models we analysed the
spatial distribution of two trans-Saharan avian scavengers that breed (Europe) and winter (Africa) sympatrically, in relation
to food availability. In the summering grounds, the probability of finding large numbers of both species increases close to
predictable feeding sources, whereas in the wintering grounds, where food resources are widespread, we did not find such
aggregation patterns, except for the black kite, which aggregated at desert locust outbreaks. The comparison of diets in
both species through stable isotopes revealed that their diets overlapped during summering, but not during wintering.

Conclusions/Significance: Our results suggest that bird sociality at feeding grounds is closely linked to the pattern of spatial
distribution and predictability of trophic resources, which are ultimately induced by human activities. Migrant species can
show adaptive foraging strategies to face changing distribution of food availability in both wintering and summering
quarters. Understanding these effects is a key aspect for predicting the fitness costs and population consequences of
habitat transformations on the viability of endangered migratory species.

Citation: Cortés-Avizanda A, Almaraz P, Carrete M, Sánchez-Zapata JA, Delgado A, et al. (2011) Spatial Heterogeneity in Resource Distribution Promotes
Facultative Sociality in Two Trans-Saharan Migratory Birds. PLoS ONE 6(6): e21016. doi:10.1371/journal.pone.0021016
Editor: Brock Fenton, University of Western Ontario, Canada
Received February 15, 2011; Accepted May 16, 2011; Published June 22, 2011
Copyright: ß 2011 Cortés-Avizanda et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This work was supported by the project CGL2004-00270 of Spanish Government. The funders had no role in study design, data collection and analysis,
decision to publish, or preparation of the manuscript.
Competing Interests: The authors have declared that no competing interests exist.
* E-mail: [email protected]

Introduction competitive ability [10–11] and life history traits [12]. Recently,
some authors have suggested that behavioural flexibility, i.e. the
The distribution of key resources affects the spatial structure and ability of individuals to express distinct behaviours in different
the social organization of animal populations [1–3]. Large contexts through innovation and learning processes [13–14],
aggregations of food may relax intraspecific competition, thus might also influence the balance between migratory and resident
promoting the recruitment of individuals without any apparent strategies in environments with sharp seasonal changes [15].
adaptive value [3–5]. Nevertheless, most studies showing this link Obligate migratory species are logically enforced to respond to
between animal distributions and resource availability are variable conditions when moving from summering to wintering
theoretical [4]. When empirical studies were performed, they grounds. Within this scenario, however, the lack of studies tracking
were done at a reduced geographical scale (usually local) and/or the response of migrant organisms to large-scale changes in the
from a monospecific approach [6], so generalizations beyond the degree of heterogeneity in the spatial distribution of food resources
population level (i.e., guilds or communities) are difficult to make. is striking. Recent research suggests that animals, in particular
Migratory species, from invertebrates to vertebrates, develop birds, may develop specific behavioural strategies to compensate
their life cycles in distant biomes, occupying wintering grounds far for the negative effects of environmental variability [16–17]. Thus,
from their breeding areas [7]. Explanations proposed to it seems important to discern whether migrant birds have flexible
understand migration include variation among species in depen- responses to variations in environmental conditions between
dence on temporally and spatially variable food resources [8–9], summering and wintering grounds, such as changes in the

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 Migrant Responses to Resource Spatial Distribution

availability of food resources. In addition, this information may be scenarios that these trans-Saharan migrants encounter deter-
useful in understanding large-scale variability in the role of limiting mine parallel or asymmetric responses in their distribution,
factors on the viability of populations of migrant species of abundance and trophic strategies in the two visited biomes. We
conservation concern [18–19]. hypothesize that the spatial distribution of our focal species will
Here, we examined the spatial response of individuals to closely follow that of clumped resources in Europe, whereas in
changes in the distribution and availability of feeding resources sub-Saharan Africa the species will be widespread, only showing
between wintering and summering grounds using as a study aggregated distributions linked to pulsed resources (i.e. the
system two long-lived migratory and facultative scavenger birds, desert locust outbreaks). According to the envisaged intraspecific
the black kite Milvus migrans and the globally endangered differences in spatial aggregated distribution we predict that
Egyptian vulture Neophron percnopterus. These species have trophic overlap between the two species will be higher in their
relatively similar foraging strategies and diets (relying on summering areas compared to wintering ones.
invertebrates and small to medium-sized vertebrates) and,
although being territorial during breeding, they can feed Results
together thus potentially competing for similar resources [20–
21]. Previous studies of our monitored and other western Bird abundance and food resource availability
European populations of Egyptian vultures and black kites Egyptian vultures were detected in 20.6% of the African (n = 85)
indicate that individuals winter in the Sahelian region, between and in 35.2% of the European (n = 141) point counts, while the
Senegal and Mali, as do the rest of the Western Palearctic frequencies of detection of black kites were 34.7% and 50.7%,
populations [22], also overlapping their wintering areas. respectively. Large numbers of both Egyptian vultures and black
Throughout their annual cycles, these species exploit food kites feeding together were detected at predictable European
resources that are strongly affected by human economies [23]. feeding sources (i.e. rubbish dumps and vulture restaurants),
Specifically, in the European summering grounds, birds rely on reaching maximums around 73 and 143 birds, respectively. At
rubbish dumps and supplementary feeding stations (so-called those places, large numbers of another six different species were
vulture restaurants) created after the prohibition of abandon- also found (see Table 1). At the few predictable African feeding
ment of carcasses derived from extensive livestock in the field sources (slaughterhouses), Egyptian vultures were absent and only
[24–25]. In contrast, food availability in the African wintering black kites, reaching a maximum of 500 birds, and two raven
areas is mostly unpredictable, since livestock is under an species used them.
extensive regime and widespread in the field [23], with Availability of food resources was different in summering and
predictable carcasses only available at very few dispersed wintering grounds. In 91.9% (n = 99) of the African transects, we
slaughterhouses in the vicinity of cities. In sub-Saharan biomes, detected some kind of livestock while in Europe only 13% (n = 77)
moreover, there are particular emerging phenomena such as the of transects contained livestock (x2 = 107.144; P,0.0001) (Fig. 1).
outbreaks of desert locusts Schistocerca gregaria. This superabun- When we considered each livestock species separately, we also
dant pulsed resource plays a key role in this arid ecosystem by detected higher frequencies of presence in transects performed in
providing food for some predators that aggregate in their wintering grounds (Africa: sheep and goat = 78.8%; cat-
surroundings [see 26 for details]. Under this framework, we tle = 62.6%; horse = 61.6%; dromedary = 36.4%; Europe: sheep
specifically test whether the variability in the ecological and goat = 11.7%; cattle = 1.3%; N6M exact Test; P = 0.0024).

Table 1. Abundance of scavenger species (measured as the maximum number of individuals observed per day during all surveys)
at European (n = 8) and African (n = 3) predictable feeding sources.

Species Europe Africa

Rubbish dumps Vulture restaurants Slaughterhouses

Neophron percnopterus 30 34 40 29 73 10 59 58 18
Milvus migrans 55 41 0 143 100 26 6 1 4 500 300 45
Gyps fulvus 100 20 0 0 35 505 259 357 522
Gypaetus barbatus 2 0 0 0 0 0 0 0 0
Milvus milvus 11 24 0 3 15 13 1 2 5
Aquila chrysaetos 0 0 0 0 0 0 1 0 0
Buteo buteo 1 0 0 0 0 0 0 0 0
Ciconia ciconia 0 160 30 0 51 0 0 0 0
Larus cachinnans 0 130 5 0 150 0 0 0 0
Corvus corax 60 97 2 2 109 0 5 8 4
Corvus corone 6 50 0 0 0 0 1 9 0
Corvus ruficollis 55 1 1
Corvus albus 110 20 100
Pica pica 0 3 0 0 1 3 1 4 0
N survey days 6 8 4 2 8 7 12 8 7 3 2 2

Focal species are shown in bold.

doi:10.1371/journal.pone.0021016.t001

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 Migrant Responses to Resource Spatial Distribution

decreases sharply with the distance to the nearest feeding source

(Fig. 2). Note that this relationship is statistically significant (that is,
the partial residual plots do not overlap 0) at distances lower than
40 km for both species. Thus, although it seems that the spatial
abundance of both species increases at large distances to the
feeding sources, the confidence limits widen as well (Fig. 2b and e).
This effect is due to a single point in both figures. Moreover, the
parameter measuring the homogeneity of Zero-inflation (d) is
positive for both species and statistically significant for the
Egyptian vulture (Table 2), suggesting that the zero counts tend
to accumulate at large distances from feeding sources.
In the wintering grounds, however, neither the distance to the
nearest feeding source nor human presence (measured as
abundance of cattle, cattle) seems to have an effect on the spatial
distribution of vultures, although human presence was linked to
the abundance of black kites (Fig. 3). Additionally, the proportion
of zero counts was larger and the relative density of birds
(nu birds/km2) was smaller than in Europe (Table 2), perhaps
because the surveyed area was larger in Africa than on the other
continent. It is thus worth noting that Fig. 3a depicts the location
of only 18 birds in 11 groups scattered over a large area, so
although the Egyptian vulture seems to be more aggregated in
wintering grounds, we emphasize that the proportion of 0 counts
was very high (78%) and the average group size was very small for
this species (1.63 birds per contact). For the black kite, although
the effect of the covariates was negligible for both years, the spatial
distribution of birds was rather different in years with or without
locust outbreaks. In Fig. 4, we plot the non-parametric terms for
the spatial component of the abundance of each species in the
years without (Fig. 4a, c) and with locusts (Fig. 4b, d). A shift in the
spatial distribution of kites is evident, from the first (a scattered
distribution) to the second year (an aggregation around the central
portion of the study area, in which the population core of the
Figure 1. Cattle abundance a) (measured as percentage of locust outbreaks was located). Average group size increases
positive contacts with cattle during road counts) and herd size accordingly, from 6.63 (61.53) black kites per positive contact in
b) in the summering (Europe; white) and wintering (Africa; the year without locusts to 32.47 (610.84) birds in the year with
grey) grounds of two trans-Saharan migrant species. Box plots the locust outbreak (t-test for samples with unequal variances,
of cattle sizes represent median values (horizontal line marks), the t19 = 2.09, P = 0.029). In the Egyptian vultures, there are no
central 50% of the data (boxes), the range (whiskers) and outliers (dots).
doi:10.1371/journal.pone.0021016.g001
significant changes in bird abundances associated with desert
locust outbreaks (1.6360.34 in the year without locusts to
2.5060.77 in the year with locusts; t18 = 2.10, P = 0.317).
Food distribution, human presence and the spatial
abundance of species Trophic overlap between species
A preliminary analysis suggested no seasonal differences in the Isotopic signatures of feathers grown in Africa were different
way that functional forms relate covariates to bird counts. among species (Wilks’ lambda = 0.68, F2,47 = 10.81; P,0.001),
Therefore, we pooled data in a single model for each species but no interspecific differences were detected for feathers grown in
and spatial unit. The results of the fitting of each COZIGAM are Europe (Wilks’ lambda = 0.87, F2,24 = 1.73; P = 0.2; Fig. 5).
shown in Table 2. The model selection approach consistently Accordingly, when considering each isotope separately, significant
selected models including distance to the nearest feeding source interspecific differences were found among African samples,
and cattle for both species on the two continents. mainly regarding d15N values (d13C: F 1,48 = 4.02; P = 0.051;
Additionally, parametric (functionally linear) terms linked to d15N: F 1,48 = 18.8; P,0.001), while European samples did not
human presence (slope in Europe and cattle in Africa) were selected show significant differences among species in the isotopic
for the black kite in both areas and for the Egyptian vulture in signatures (d13C: F 1,26 = 2.86; P = 0.1; d15N: F 1,26 = 2.2; P = 0.15).
Europe. Although model structure was similar across species and
continents, the profile of the non-parametric functions measuring Discussion
the effects of the covariates on species abundance differed among
continents, but not among species. Only for illustrative purposes, Food distribution, bird abundance and trophic overlap
Fig. 2 and 3 depict the spatial non-parametric function fitted to the Our results show how trans-Saharan migrant bird populations
abundance of Egyptian vultures and black kites in Europe and can exhibit different spatial arrangements depending on the food
Africa, respectively. Although these terms were not included in the distributions found in their wintering and summering grounds.
final model (Table 2), they are useful for devising the spatial Sub-Saharan regions hold numerous and diverse herds of domestic
distribution of the focal species. After controlling for the effect of livestock widespread in the field (see results for details). European
human presence in Europe (measured through the variable slope), areas, however, are long-term human-modified ecosystems where
the spatial abundance of Egyptian vultures and black kites food resources for vertebrate scavenger species have been subject

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 Migrant Responses to Resource Spatial Distribution

Table 2. Relationship between species abundance and food distribution.

Species & season Probability of Zero-inflation Effect of covariates

%0 a (± SE) d (± SE) Spatial Distance Cattle Slope BIC{

Egyptian Vulture
Wintering 78 1.251 (0.810) 20.979 (0.717) 21.320 2 2 2 35.957
Wintering 5.642 (3.251) 24.173 (1.979) 2 6.302 7.718 2 5.189
Wintering 0.600 (0.405) 0.034 (2) 21.895 1.119 8.839 2 81.327
Summering 65 4.195 (2.654) 21.703 (1.194) 28.910 2 2 2 26.841
Summering 20.727 (0.653) 1.639 (0.680) 2 2.97 2 0.021 (0.010)* 2143.762
Summering 1.389 (0.349) 3.271 (2.533) 28.859 8.793 2 20.086 (0.044)* 58.645
Black Kite
Wintering 64 0.301 (0.575) 20.204 (0.186) 26.310 2 2 2 2280.850
Wintering 0.330 (0.458) 20.273 (0.164) 2 8.909 0.006 (0.001) * 2 2446.654
Wintering 0.459 (0.251) 20.002 (2) 28.063 8.256 0.005 (0.001) * 2 222.526
Summering 49 1.052 (0.378) 20.403 (0.197) 27.970 2 2 2 2232.916
Summering 0.357 (0.378) 0.215 (0.231) 2 4.752 2 20.059 (0.013) * 2321.818
Summering 1.408 (0.513) 0.014 (0.243) 27.605 8.183 2 20.119 (0.036) * 297.737

Models were fitted using a COZIGAM with a Poisson link function and measuring the joint effects of distance to the nearest feeding source (distance) and human
presence (slope in Europe and cattle in Africa) on the spatial abundance of Egyptian Vultures and black
kites in their summering (Europe) and wintering (Africa) grounds
Results for each spatial unit are shown for all seasons pooled in a single model. The table shows the proportion of 0 counts (% 0) in the dataset for each spatial unit.
A linear model with a logit link function relates the probability of Zero-inflation (pi) to the covariates through the estimated spatial abundance in the GAM; in this model
a is a constant and d is a parameter measuring the homogeneity of Zero-inflation. The column for the ‘‘Effect of covariates’’ contains the estimated degrees of freedom
(e.d.f) for each non-parametric term in the GAM, unless a parametric (functionally linear) term is selected; in these cases, denoted with the symbol ‘*’, the parametric
estimate is shown instead. Statistically significant terms are shown in bold. Human density was measured as the density of cattle in Africa and the slope of the terrain in
Europe. {The BIC denotes the Bayesian Information Criterion; the model minimizing this quantity is selected as the best descriptor of the dataset within the pool of
fitted models, and is shown in bold type.
doi:10.1371/journal.pone.0021016.t002

to different pressures and management decisions that have unpublished). Although the information is partial [31–32] these
favoured their patchiness across years. As a consequence of these diet differences probably also took place in Europe some decades
differences, the same birds must aggregate during summering, ago within a scenario of healthier Mediterranean ecosystems,
when food is clumped and patchily distributed, but can remain important extensive grazing and low number of predictable
widely and near randomly distributed during wintering, when feeding points [33]. For its part, d13C values show a slight
resources are widespread. But changes in bird distribution go enrichment with trophic level, but can reveal micro-habitat
beyond the species level, and interspecific trophic overlap also information on terrestrial ecosystems used due to the differential
becomes apparent in the summering scenario of resource importance in the distribution of C3 and C4 plants [30,34]. In our
aggregation. Conversely, when both species track resources in results, the marginally significant differences in stable carbon
the less managed habitats, they have the opportunity to find and isotopes in African samples again seem to indicate a higher
exploit pulsed resources when possible. Indeed, during the desert consumption by black kites of arthropods dependant on C4
locust outbreaks, the black kites shifted their spatial distribution in herbaceous vegetation [26].
a conspicuous way, increasing group sizes markedly. In contrast,
the spatial distribution of the Egyptian vulture did not change after On the adaptive value of changing grouping patterns
the appearance of locust outbreaks. The above-described scenarios, where bird populations change
These findings show that variability in the response to their local abundances following resource distribution, raise a key
environmental changes differs between species, leading to question: are bird aggregations in European locations with
scenarios with different degrees of resource partitioning, diet predictable food adaptive or, on the contrary, a maladaptive
overlap and, consequently, interspecific competition and proba- result of the global scarcity of food and/or trophic distribution
bility of coexistence [4,28–29]. Stable isotope analyses demon- patterns? Clumped food seems to lead to high intra- and
strated that the diets of our focus species completely overlapped in interspecific competition [25,35–36], which may negatively affect
European summering areas, whereas in the African wintering individual fitness [3,6]. But on the other hand, the role of some
grounds, they were segregated. It is well-known that stable aggregations (particularly roosts) in mate finding [37] and
nitrogen isotope values show a stepwise enrichment with each information transfer [38–39] has been described. It should be
trophic level [30]. In our case, there is a between-species difference taken into account, however, that although roosts and abundant
in average d15N (10.1 vs. 12.9) during wintering, indicating food resources are frequently associated [33], selective forces
separated trophic levels. The analyses of pellets of the two species leading to both kinds of aggregations may not be the same. In fact,
in the study area revealed that black kites relied on a mixed diet of at an interspecific level, individuals clump at feeding places but
arthropods and carcasses of domestic ungulates whereas Egyptian clearly separate for roosting even when the habitat requirements
vultures consume more wild and domestic vertebrates (authors are very similar (pers. obs.), which lends evidence to a scenario of

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Figure 2. Plots of the additive terms (s (?) in equation 1) of the COZIGAM fitted to the Egyptian vulture (a–c) and black kite (d–f) in
their summering grounds (Europe). In a) and d) the contour plot of the spatial effect in Eqn. 1, s(Latitude, Longitude), is shown. The coloured
surface depicts the local probability density of the spatial distribution of counts, from low density areas (red) to high density areas (white). These
colours correspond to areas with low and high bird density, respectively. The right diagrams show the partial residual plots for the effect of distance
to the nearest feeding source (vulture restaurants and/or rubbish dumps; b, e) and human distribution (measured as the slope of the terrain; c, f) on
the estimated spatial abundance of each species. The additive function is depicted as a solid black line, while the dotted lines show the 95%
confidence intervals. For clarity, the location of each data point is presented as a rug plot along the bottom of each plot. Note that the terms have
been scaled to have a 0 mean to make the model identifiable [37].
doi:10.1371/journal.pone.0021016.g002

competition for food. At an intraspecific level, trade-offs between population dynamics of migrant birds. In particular, it would be
social costs and benefits could represent a challenge to properly interesting to focus on the individual response to a changeable
managing endangered species. In our study model, for example, environment, as well as on its consequences at the population
implications of changes in food distributions on aggregations level. Populations composed of individuals behaving differently
would be different for vultures and kites, as the latter seem to be might have higher probabilities of success under changeable
able to exploit different resources while the former, more environments that those formed by more homogeneous individuals
endangered species, is less variable. Clearly, although the study [43–44]. Thus, under a scenario of global change, this approach
of the adaptive value of living in groups is an old topic in ecology can be useful in establishing probabilities of population persistence
[40–41] some main questions still remain unanswered. and conservation priorities.
In conclusion, our results show that the spatial distribution of
food might not only affect the behaviour and success of local Conservation implications for trans-Saharan migrant
individuals [6,41–42], but can also shape the foraging strategies of birds
entire populations, going beyond the species and potentially More than 50% of European birds are trans-Saharan migrants,
triggering consequences at multispecies levels. Future research and many of them show long-term population declines [19]. This
should focus on the output of these strategies in the long-term is particularly true for some species like our focal Egyptian vulture,

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Figure 3. Plots of the additive terms of the COZIGAM fitted to the Egyptian vulture (a–c) and the black kite (d–f) in their wintering
grounds (Africa). In a) and d) the contour plot of the spatial effect is shown. The right diagrams show the partial residual plots for the effect of
distance to the nearest food source (nearest town with slaughterhouses; b, e) and the degree of humanization (cattle, measured as the number of
livestock; c, f) on the estimated spatial abundance of each species. See Fig. 2 for further details.
doi:10.1371/journal.pone.0021016.g003

which is considered ‘‘globally endangered’’ [45]. Thus, the considered of major concerns for the population viability of many
identification of potential limiting factors operating at wintering predatory species [52–53]. In fact, in Europe the few food
and breeding grounds is a key point to understanding their resources available for avian scavengers are carcasses derived from
population trends [46–47]. Recent studies suggest that mortality intensive livestock, which are clumped and predictably disposed at
rates of migrant birds are mainly determined by factors operating supplementary feeding points [25]. Interspecific competition,
at wintering grounds. In particular, survival rates of short and which is enhanced in these situations, can promote the extinction
long-lived species, including the Egyptian vulture, have been of a species, even when it is a slow process not likely to be observed
positively associated with rainfall in the Sahelian region [48–50]. on the time scale of most scientific studies [54]. Besides ecological
Regarding our results, we found that foraging avian scavengers in aspects of species and individual aggregations, other constraints
Africa follow a distribution pattern very similar to that in which such as the spread of illness, veterinary drugs and other
these scavenger species have co-evolved, i.e. environments where contaminants [55–56] are also negatively affecting species using
food resources are dispersed and sometimes appeared as pulsed these feeding points. Indeed, preliminary analysis shows that the
events [51]. However, the Sahel region has degraded during detrimental effects of ingested antibiotics and the acquisition of
recent decades as a consequence of a severe drought and human pathogens at feeding points may decrease the health of vultures
activities [23]. In this scenario, social and searching strategies - with a lethal potential, especially in nestlings and fledglings [57].
such as those described in this paper, could be scarcely efficient The relative importance of these negative factors operating
when food resources are highly depleted in space and/or time. during summer should be compared to that existing in the African
In the European breeding areas, landscape transformation and wintering grounds in order to properly assess conservation criteria
habitat loss have affected the availability of food resources, being and priorities. Meanwhile, the appropriate management of trophic

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 Migrant Responses to Resource Spatial Distribution

Figure 4. Contour plots of the spatial effect estimated by the COZIGAM fitted to the abundance of Egyptian vulture (a, b) and black
kite (c, d) in Africa in two different years. For this plot only, the effect is shown for each species during the year without a locust outbreak (a, c)
and the year with an outbreak (b, d).
doi:10.1371/journal.pone.0021016.g004

resources focused on reducing feeding costs for birds should be and the Ebro Valley. The area has great orographic and climatic
promoted. In this sense, future actions in Africa should focus on variation, with altitudes ranging between 300 to 2,400 m a.s.l.
reducing the impoverishment of environments, avoiding landscape (Fig. 6). Human populations concentrate in valleys with large
transformation by human overexploitation. In Europe, new towns and villages [25]. This region holds one of the most
management procedures should be implemented to generate a important European populations of both avian scavengers [25,48].
rather more heterogeneous pattern of food availability for birds, There are 380 breeding territories of Egyptian vultures (ca. 30% of
for example by promoting traditional, extensive agro-grazing the Iberian population) with several communal roosts where
practices [24], thus increasing individual health conditions and hundreds of birds regularly gather [25,33]. Although no precise
reducing intraguild competition. information is available for black kites, the species is abundant
with more than 500 breeding pairs [58].
Materials and Methods In the Western Sahel region, the relief is mostly barren
with sparse rocky outcrops. Human population density is low
Study areas (3 inhabitants/km2; United Nations World Population Prospects;
Our study was performed in the Ebro Valley (Northern Spain) http://esa.un.org/unpp/). Large concentrations of people inhabit
and in the Western Sahel region (Southern third of Mauritania a few cities such as Nouackchott, Kiffa, Aioun and Nema [26].
and the adjacent areas of Senegal and Mali), covering the Nomadic shepherds inhabit temporary sparse settlements (Fig. 6).
summering and wintering grounds of the Egyptian vulture and the In this area there are no breeding populations of the two study
black kite populations (Fig. 6). The first region extends over species but large concentrations of Western Palaearctic migrants
10,000 km2 lying between the Pyrenees, the Iberian mountains can be found [23]. Indeed, radiotracking studies carried out in

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 Migrant Responses to Resource Spatial Distribution

performed in Europe (large towns are situated in flatter areas; [25])

and in Africa, the number of livestock (cattle) because in rural areas
the size of the livestock population is linked directly with number
of inhabitants [23]. We also took into account the availability of
additional trophic resources in Africa such as locust outbreaks.
During November-December 2004 there was an important
outbreak covering broad regions of Mauritania, Mali, Senegal
and Morocco. Before this event, the number of locusts was very
low in the region [26]. Consequently, we distinguished counts
performed during the desert locust outbreak (November–
December 2004) from those obtained in previous seasons
(January 2004) (see below for details of statistical procedures).
Spatial modelling of count data. Due to the nature of the
survey, a large portion of sampling points contained a zero count
on both continents, which yielded zero-inflated distributions with a
larger proportion of zeros than expected from a standard Poisson
count process [60]. Zero-inflated distributions are a mixture
distribution in which a strong probability mass is located around
0 (the so-called 0-atom) and the remaining data behaves as a
Figure 5. Stable carbon and nitrogen isotope values (mean ±
standard Poisson process, which gives rise to a regular distribution.
SE, %) in feathers of Egyptian vultures (triangles) and black
kites (circles) grown in their summering (Europe: green) and During recent years several statistical approaches have been
wintering (Africa: red) grounds. Numbers in brackets indicate proposed for analyzing this particular distribution [60–63].
sample sizes. Irrespective of the method, the standard procedure has been to
doi:10.1371/journal.pone.0021016.g005 analyze the mixture distribution in a two-stage approach. First, the
response is dichotomized into zero and non-zero counts and
Spain have shown that individuals summering in this area are analyzed using a presence/absence analysis. Then, a second
wintering in the Sahel region, so we are confident that we are analysis is conducted using only the non-zero data. It is well
compiling information about factors affecting the same popula- known, however, that the two-stage approach can very easily lead
tions during summering and wintering. For further details on the to conflicting results [64]. Thus, we used a recent and new method
study areas see [23,26]. for ecological field data dealing with the excess 09s while allowing
us to test, in a robust manner, whether the differing spatial
Bird abundance and food resource availability resource distribution among continents promotes different spatial
Following established methodologies by Sánchez-Zapata et al. patterns of bird distribution. The base model, proposed by Liu &
[26], we surveyed the abundance of black kites and Egyptian Chan [64], uses a Generalized Additive Model (GAM), where no
vultures by means of 30-minute point counts (Africa: n = 42 in functional relationship is a priori assumed in the effects of the
January 2004, and n = 43 in November-December 2004; Europe: covariates on the response [65]. However, in our setting the
n = 64 in May 2005, and n = 77 in July-August 2005; Fig. 6). response is assumed to follow a given distribution from the zero-
Points were randomly distributed along both study areas, and were inflated exponential family where the probability of zero-inflation
at least 10 km apart to avoid recounting birds. We recorded all the is simultaneously supposed to be some monotone function of the
birds observed within a radius of 2 km. Additionally, for each expected response. Therefore, the mixture distribution is analyzed
point, we conducted 5-km car transects to determine the number with a flexible, non-parametric model for the effects of some
of livestock: cattle Bos primigenius, sheep Ovis aries, goat Capra hircus, covariates on the response variable with the further, on-line
donkey Equus asinus and dromedary Camelus dromedarius in Africa constraint that the probability of zero-inflation in the response is a
and sheep, goat, cattle, horse Equus ferus and donkey in Europe. lineal function of the expectation. The resulting model is the so-
The presence and frequency of livestock species on the two called constrained zero-inflated Generalized Additive Model
continents were compared through Chi-square tests. (COZIGAM) [64]. The constrained nature of the COZIGAM is
We also carried out censuses of scavenger birds at predictable useful when modelling spatio-temporal animal abundance data
feeding sources (three slaughterhouses in Africa, and four ‘vulture because the processes generating the 0 and non-0 inflation are
restaurants’ and five rubbish dumps in Europe) during 2004–2005. linked through the same behavioural mechanisms [64].
Visits lasted 30 min and on each occasion we recorded the To build the model, we consider that yi is a count recorded in a
maximum number of individuals observed. random sampling point of the survey, and xi is a value of the
measured covariate. The mixture distribution, denoted by h(yi) is
Food distribution, human presence and the spatial then defined as
abundance of species
Field procedures. To determine whether predictable feeding 8
sources influenced the spatial distribution of birds on both < 0 with probability 1pi
>
continents, we considered as a sample unit the abundance of yi ,~Yi jxi eh(yi )~
>
:
Egyptian vultures and black kites at each observation point. As an f (yi jhi ) with probability pi
explanatory variable, we considered the distance to the nearest
predictable feeding source, i.e. nearest town with associated
slaughterhouses in Africa, and vulture restaurants and/or rubbish where the 0-atom models the zero inflation and the regular
dumps in Europe, calculated by the use of ArcView ‘‘Nearest distribution (the non-zero portion) comes from an exponential
feature’’ [59]. To control for the potential effects of humanization, family with probability density f(yi |hi), in our case a Poisson
we included the slope of the terrain (slope) at each count point distribution. A constraint is imposed so that the probability of

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 Migrant Responses to Resource Spatial Distribution

Figure 6. Maps of the studied areas with observation points (black dots) and predictable feeding sources (white dots).
doi:10.1371/journal.pone.0021016.g006

zero-inflation, denoted by pi, is a monotone function of the accumulate along some gradient of the predictor variable. The
expected values of the response variable, denoted by mi. Using a response, with expected values denoted as mi in Eqn. 1a, is
logit link function, this restriction is written as modelled non-parametrically with a Generalized Additive Model
[27]. For Europe, this model can be written in a simplified form as
logit(pi )~azd(mi ) ð1aÞ
m~czsðLatitude, LongitudeÞzsðDistanceÞzsðSlopeÞ ð1bÞ
where a is a constant and d is a parameter measuring the amount
of homogeneity in zero inflation. Interestingly, if d is found to be while for Africa it would be written as
distinct from 0 this would indicate that the distribution of 09s is not
homogeneous, which means that a large proportion of zero counts m~czsðLatitude, LongitudeÞzsðDistanceÞzsðCattleÞ ð1cÞ

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 Migrant Responses to Resource Spatial Distribution

where c is a parametric constant and s (?) are the smooth functions their feathers in wintering and in breeding regions [72–73]. For
measuring the non-parametric effects of covariates on the this study, we only sampled skins of individuals collected in
response. The term s(Latitude, Longitude) measures the non- February-April, after their immediate arrival from wintering areas.
parametric spatial component of the abundance survey [64]. From each skin, we sampled two feathers: one new, brilliant and
Although a preliminary analysis with a non-parametric spline with non-abraded edges, presumably grown in Africa, and another
correlogram [66] suggested that the abundance data for both one older, with faded colour and with worn fringes presumably
species lack spatial autocorrelation, we included the spatial term in grown during the previous year in Europe. Very old feathers were
eqn. 1c to check whether some spatial residual variation can be not considered to avoid mixing samples of unclear origin.
detected after estimating the covariate effects. Laboratory procedures. Stable carbon and nitrogen isotope
Eqns. 1b and c were fitted to the dataset for the corresponding assays were performed on 0.5 and 1 mg subsamples of feathers
spatial unit (Africa or Europe), and we further constructed that were combusted in an elemental analyzer (Carlo Erba
alternative models by sequentially dropping the spatial term or 1500NC) on-line with a Delta Plus XL mass spectrometer (EA-
the terms for the distance to the nearest feeding source and for IRMS). Analysis of d13C and d15N were in triplicate. The overall
human presence. For each covariate effect in eqn. 1 we tested precision of analyses was 60.1 % for d13C and d15N. The stable
whether a non-parametric (‘‘wiggly’’) function is preferred over a isotope composition is reported as d values per mil: d = (Rsample/
constant or parametric (‘‘functionally linear’’) one by testing if the Rstandar –1) *1000, where R = 13C/12C for d13C or 15N/14N for
estimated degrees-of-freedom (e.d.f.) of the non-parametric d15N values. The international reference standard for 13C/12C is
function deviates significantly from a pure parametric one, where PDB (Pee Dee Belemnites, a fossil marine carbonate of biogenic
e.d.f = 1 [27]. We measured the statistical performance of each origin) and for 15N/12N in the AIR (average of Atmospheric Air).
model by subtracting the log-likelihood of each COZIGAM. We Analytical procedures. For both carbon and nitrogen,
then calculated the Bayesian Information Criterion (BIC) of each differences in isotopic signatures between the two study species
fitted model [67]. This information criterion more heavily within each biome were tested first for the two isotopes combined
penalizes over-parameterized models with respect to alternative (MANOVA), then for carbon and nitrogen taken separately (one-
information criteria, such as the AIC. The model minimizing the
way ANOVA) [74]. Values are expressed as means 6 SE. The
BIC was selected as the best model. All the statistical analyses were
statistical software used was SPSS version 17.0.
conducted in R 2.11.1 [68], using the COZIGAM 2.0.3 package
[64].
Acknowledgments
Trophic overlap between species We thank Josefina Barreiro and José Cabot for allowing access to
Feather collection. We used stable isotope analyses to collections of the MNCN and the EBD (CSIC). We are particularly
examine the diet overlap of our focal species in Africa and grateful to N. Markina and M. Rodriguez for their help during fieldwork.
Europe. This methodology has been applied to studies on trophic M. de la Riva helps with digital cartography and two anonymous reviewers
made helpful comments on earlier version of the manuscript.
relationships within vertebrate communities as well as to address
specific questions regarding temporal and spatial variability in
diets [69–70]. Here, we performed stable isotope analyses of Author Contributions
nitrogen (15N/14N, d15N) and carbon (d13C/12C, d13C) from Conceived and designed the experiments: AC-A MC JAS-Z JAD.
feathers [30,71] collected on 41 black kite and 36 Egyptian vulture Performed the experiments: AC-A MC JAS-Z FH JAD. Analyzed the
skins deposited in the Museum of Natural History of Madrid and data: AC-A PA MC JAD. Contributed reagents/materials/analysis tools:
in the Estación Biológica Doñana (CSIC). Focal species moult AD. Wrote the paper: AC-A PA MC JAS-Z FH JAD.

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