Animal Conservation. Print ISSN 1367-9430
Effect of human activities on the behaviour of breeding
Spanish imperial eagles (Aquila adalberti): management
implications for the conservation of a threatened species
L. M. González1, B. E. Arroyo2, A. Margalida3, R. Sánchez4 & J. Oria5
1 Dirección General para la Biodiversidad, Ministerio de Medio Ambiente, Madrid, Spain
2 Centre for Ecology and Hydrology, Banchory, Scotland, UK
3 Bearded Vulture Study and Protection Group, El Pont de Suert (Lleida), Spain
4 Fundación CBD-Habitat, Madrid, Spain
5 c/San Agustı́n, Segovia, Spain
Keywords
buffer zone; human disturbance; Spanish
imperial eagle.
Correspondence
Antoni Margalida, Bearded Vulture Study
and Protection Group, Apdo. 43. E-25520 El
Pont de Suert (Lleida), Spain.
Email: [email protected]
Received 10 January 2005; resubmitted 30
August 2005; accepted 30 September 2005
doi:10.1111/j.1469-1795.2005.00016.x
Abstract
We studied (14 500 h of field observations during 20 breeding attempts by 10 pairs)
the effects of human activities on the behaviour of breeding Spanish imperial
eagles. The probability that human activities around nest sites provoked a flight
reaction varied significantly among territories and among types of activity, and
increased when the distance between the activity and the nest site decreased, and
increased when the number of people involved in each intrusion was higher.
Pedestrian activities (mainly by hunters, campers and ecotourists) caused more
flight reactions than vehicles. Overall, the probability of a reaction increased
sharply when activities occurred at less than 450 m from the nest, but was
negligible if they occurred at 800 m. Reaction probability was lower in territories
with higher intrusion frequencies (which suggests that some habituation occurs),
where the nest was not visible from the tracks, and in less ‘plain’ or ‘accessible’
territories. Hatching rate was affected negatively by the frequency of human
activities. Our results suggest that the critical inner buffer zone around Spanish
imperial eagle nests should be established at a minimum radius of 500 m, and the
vulnerable zones at a minimum of 800 m, bearing in mind the physiography of the
terrain and the visibility of the nests. Finally, in future studies of nest-site selection
with this species, it would be advisable to use a variable that quantifies (through
field observations) human disturbance frequency.
Introduction
Different studies of the effects of human activities on bird
populations have documented the relationships between human disturbance and productivity (White & Thurow, 1985;
Ruhlen et al., 2003), changes in the use of habitat or breeding
sites (e.g. McGarigal, Anthony & Isaacs, 1991; FernándezJuricic, 2002) or its interference with foraging and the amount
of parental care (e.g. Fernández & Azkona, 1993; Verhulst,
Oosterbeek & Ens, 2001; Bautista et al., 2004). In raptors,
human activities during incubation and early chick-rearing
stages can alter normal breeding behaviour and influence
breeding success (Holmes et al., 1993; Steidl & Anthony,
1996; Richardson & Miller, 1997; Swarthout & Steidl, 2001).
If disturbance in the vicinity of eyries provokes temporary nest
abandonment, it may have fatal consequences on the development of embryos or nestlings (Grier & Fyfe, 1987). Nevertheless, the behavioural response may vary in relation to
individual differences or characteristics of the breeding territories (Richardson & Miller, 1997).
The Spanish imperial eagle Aquila adalberti, a globally
threatened bird of prey (BirdLife International, 2004), only
inhabits the central and south-western regions of the Iberian
Peninsula, and its current breeding population has been
estimated at around 200 breeding pairs (GTAI, 2005). In the
central and western parts of this species’ range, nesting
habitat selection and breeding success are conditioned by
the degree of humanization (e.g. the distance from the
nearest inhabited area, from roads and paths, the kilometres
of paved roads and electric power lines) and the inaccessibility of the terrain to humans, which suggest that
the Spanish imperial eagle avoids human disturbance
(González, 1991; González, Bustamante & Hiraldo, 1992;
Castaño & Guzmán, 1995). Moreover, in Doñana National
Park, a southern, marginal and small subpopulation located
in a habitat that is very different from the rest of the species’
distribution range (González, 1991), nest-site selection and
hatching rate were also affected by human presence, in
addition to vegetation structure (Calderón et al., 1987;
Bisson, Ferrer & Bird, 2002).
c 2006 The Authors. Journal compilation c 2006 The Zoological Society of London
Animal Conservation 9 (2006) 85–93 85
Human disturbance and the behaviour of breeding Spanish imperial eagles
As a result of the above studies and based on qualitative
observations, it was recommended as a precautionary measure that, for example, no public use or forestry works
should be allowed within a radius of 300–500 m around nests
from February to August (González et al., 1992; González,
1996). As a consequence, official buffer zones around this
species’ nests were established in central Spain (Consejerı́a de
Medio Ambiente de Castilla-La Mancha, 2003; Consejerı́a
de Medio Ambiente de Castilla y León, 2003) and in Doñana
(PND, 1992). However, these studies did not quantify the
type and frequency of human activities in the territories of
the Spanish imperial eagles, and did not measure the eagle’s
reaction to human activities, so the size of these buffer zones
was not calculated using empirical data. This information is
necessary in order to create and optimize effective management and conservation measures. Therefore, the need to
obtain this information was one of the recommendations of
the management plans and conservation strategies for this
species (González, 1996; MMA, 2001).
The aims of this study were: (1) to measure and identify
whether human activities surrounding the nest sites significantly affect eagle reproductive behaviour, (2) to assess
whether the response of the birds depends on the distance
from the nest or on the characteristics (e.g. visibility, degree
of humanization) of the nest areas, (3) to evaluate the
potential effect of habituation on eagle behaviour, (4) based
on the former, to recommend the distances that would
constitute the most effective buffer zones for this species.
Materials and methods
The study was carried out in the provinces of Ávila and
Madrid (central Spain). The study pairs were located in an
area with a dense population of wild rabbit Oryctolagus
cunniculus, the Spanish imperial eagle’s primary prey in the
L. M. González et al.
area (González, 1991), and dominated by smooth terrain
with rolling plains, where holm oak Quercus rotundifolia
predominates (MMA, 2003). This corresponds to the habitat most commonly occupied by the Spanish imperial eagle
in Spain (see González, 1991; González et al., 1992).
Observations were carried out during the period 1992–2002
within the framework of a nest surveillance programme in the
Castilla y León and Madrid Autonomous Communities. We
analysed the data from 20 breeding attempts by 10 pairs (range
1–4 breeding attempts per pair). The number of breeding pairs
studied is not as high as in studies of more common species
(e.g. Rodgers & Smith, 1995; Fernández-Juricic et al., 2005)
because of the rarity of the species. The birds were not
disturbed intentionally in order to study their reaction because
of their threat status (e.g. White & Thurow, 1985).
Observations were carried out between 8:00 and 21:00 h
from locations overlooking the territory at a distance of
around 800 m from the nest and using 20–60 spotting
scopes. Observations carried out at this distance did not
alarm the birds or alter their behaviour. The total observation time was 14 500.5 h (average SD/pair= 1444.7 912.4 h, range 268.5–2869.8 h).
Study pairs displayed adult plumage (A), except in six
territories (Table 1) where the pairs consisted of individuals
with subadult plumage (SA, see González, 1991; Forsman,
1999). Individuals were sexed and individually identified
based on: (1) individual plumage differences in the extent and
the shape of the white feathers on the leading edge of the wing
above and below, as well as the lesser coverts and the
scapulars; the bird maintains this appearance throughout its
adult life, after successive moults, without the extent or shape
changing (L. M. González, R. Sánchez & J. Oria, unpubl.
data) and (2) voice: the male’s calls are higher pitched than
the female’s (L. M. González, R. Sánchez & J. Oria, unpubl.
data).
Table 1 Territories, monitoring years and descriptive variables of the area surrounding the Spanish imperial eagle nests (600 m) used during this
study (see explanations in methodology)
Territory
M-18
M-30
M-14/27
M-27/14
M-27/14
M-13
M-20
AV-03
AV-04
AV-04
M-11
M-11
M-16
M-15
M-15
86
Ageclasses
Year
A-A
SA-D
SA-A
A-A
A-A
A-A
SA-A
A-A
A-SA
A-A
A-A
A-A
A-A
A-A
A-A
A-A
1992
2001–2002
1996
1999
2001
1999–2000
2001–2002
2002
1994
1993
1994
1996
2002
1996
1999–2001
1996
Forest
cover (%)
28.3
73.8
26.9
43.21
0
18.11
98.6
70.7
100
95.9
92.1
92.5
72.0
94.5
100
Shrub
cover (%)
Paved
road (m)
Forest
tracks (m)
Relief
INACC
Nest
view (%)
Nest
visibility
Nest
height (m)
71.6
16.7
17.7
0
28.1
12.3
1.105
0
0
0
0
0
502
646
2.510
1119
0
2.495
40
30
20
6
9
14
130
110
50
22
28
78
76.0
73.23
39.0
81.82
71.54
70.64
1
1
1
0
1
0
21
14
14
16
6
15
0
29.3
0
4.1
7.9
7.5
0
5.5
0
0
0
0
0
0
0
0
0
0
1.728
1.348
2.872
2.529
214
664
1.817
1.151
1.132
34
15
8
8
24
49
39
49
47
168
80
66
66
148
148
178
198
194
63.25
68.80
63.26
69.38
55.14
53.63
58.0
78.0
73.0
0
1
1
0
0
1
0
0
0
21
21
16
16
15
6
25
15
15
c 2006 The Authors. Journal compilation c 2006 The Zoological Society of London
Animal Conservation 9 (2006) 85–93 L. M. González et al.
Human disturbance and the behaviour of breeding Spanish imperial eagles
The human activities observed in the vicinity of the nests
that can potentially cause disturbance included people with
tents and campers staying in the area (Campers), people
hiking in the vicinity of the nest (Hikers), birdwatchers,
photographers and other people interested in wildlife and
observing the nest (Ecotourists), people walking and/or
speaking while fishing or collecting mushrooms or other
products (Gatherers/Fishermen), people with their livestock
(Shepherds) and people with firearms and dogs (Hunters),
cyclists passing through the area making noise of varying
intensity (Bicycles), cars parked in the vicinity of the nest
(Cars parked) or passing (Cars passing), passing lorries,
tractors and similar (Trucks passing), helicopters and planes
passing over the nest (Helicopter/Small plane) and passing
motorcycles (Motorcycles). There were a few observations
(Table 2) of military activities, infrastructure works and a
balloon, which were classed as ‘Others’ (and were not
included in the analyses).
Each time one of these activities was observed at distances of less than 1 km from a nest, the following variables
were noted: the date, the linear distance to the nest area (not
including altitude differences), the type and duration of the
human activities (in minutes), the number of people or
vehicles involved in the activity (Intrusion load) and the
behaviour of the birds, if possible. They were coded as
follows: (1) No reaction, the bird displayed no apparent
change in behaviour or in the activity it was carrying out
when observed; (2) Alert reaction: the bird changed its
behaviour or activity, stood up in the nest with its head
outstretched and looked in the direction of the human
activity, but did not leave the nest; (3) Flight reaction, the
bird flew off and left the nest. When the latter occurred, we
also measured the amount of time (in minutes) during which
the nest was unattended (duration of the reaction).
Table 2 Impact of various human activities on the behaviour of
breeding Spanish imperial eagles
Activity
n
Proportion of
observations
with alert
reaction
Campers
Hikers
Ecotourists
Hunters
Shepherds
Gatherers/fishermen
Cyclists
Cars parked
Cars passing
Trucks passing
Helicopter/small plane
Motorcycles
Others
9
336
31
7
37
71
254
53
857
103
28
228
4
22.2
10.1
41.9
57.1
0.0
2.8
2.4
5.7
0.5
0.0
25.0
2.2
100.0
n, number of observations.
Proportion of
observations
with flight
reaction
11.1
6.3
35.5
57.1
0.0
2.8
0.4
5.7
0.4
0.0
3.6
0.4
100.0
For each breeding attempt, we differentiated two breeding periods: incubation (from laying until hatching) and
nestling (from the hatching of the first egg to the fledgling
of the last chick). Hence, we could allocate a breeding
period to each observed activity and we could also calculate
the observation effort (number of monitoring visits) for
each pair in each breeding period. We also calculated
the frequency of intrusions as the total number of human
activities recorded for each breeding attempt, divided by the
total number of monitoring days.
In order to study the relationship between the environmental characteristics of the nest site and the Spanish
imperial eagles’ response to human disturbance, we measured variables of the nest site and the area surrounding the
nest that in previous studies had been significant for nest site
selection in our study area (González et al., 1992) or in other
areas (Bisson et al., 2002). Within a circular area with a 600m radius (distance at which eagles stop responding to
human intrusions; see ‘Results’) we measured (Table 1), on
1:50 000 National Forestry Inventory maps (MMA, 2004),
the percentage of forest cover (Forest cover) and shrub cover
(Shrub cover), and on 1:50 000 Spanish Military Geographical Service maps the kilometres of paved (Roads) and
unpaved roads (Forest tracks). Finally, we calculated an
Inaccessibility index defined as a combination of the relief
index (number of contour lines 20 m equidistant, which cut
through an imaginary line drawn by the steepest slope in the
area and crossed the location of the nest) and the percentage
of shrub cover (as relief shrub cover 2, see González
et al., 1992).
Moreover, we measured: (1) the % of surface area of land
visible from the nest or the view of the nest (Nest viewshed).
This was calculated by drawing a polygon whose sides are
formed by projecting imaginary straight lines from the nest
in all directions. The vertices of this polygon are formed
when any obstacle crosses the imaginary lines. This portion
of the vicinity of the nest is called the visible zone and the
zone not visible from the nest is known as the hidden zone;
(2) the visibility of the nest (Nest visibility) from the tracks,
paths and roads, i.e. whether the nest was visible (1) or not
(0) from any spot on a track, path or road and (3) the height
of the nest from the ground (Nest height) from the outer rim
of the nest measured with a metric scale and a 1-m precision.
Statistical analyses
We analysed whether human activities influenced the Spanish imperial eagles’ behaviour using general linear models
(using the GENMOD procedure in SAS 8.0). For the
response variables ‘probability of alert reaction’, or ‘probability of flight reaction’, we fitted a binomial distribution
and a logit link function. For the response variable ‘duration
of flight reaction’ we fitted a Poisson distribution and a log
link function. As explanatory variables, we included ‘type of
activity’, ‘duration of the activity’, ‘distance between activity
and nest’, ‘breeding period’ (incubation vs. nestling) and the
interactions that had maximum implications for management: distance and type of activity, distance and breeding
c 2006 The Authors. Journal compilation c 2006 The Zoological Society of London
Animal Conservation 9 (2006) 85–93 87
Human disturbance and the behaviour of breeding Spanish imperial eagles
period and distance and territory. We used Type 1 analyses,
including ‘territory’, ‘year’ and ‘territory year’ as fixed
effects in all models, before including any other explanatory
variable. The significance of all variables was thus calculated
once the within - and among-year effect of ‘territory’ had
been taken into account.
Secondly, to test for variables potentially affecting behavioural differences among territories, we used a GENMOD
analysis, using the ‘number of flight reactions’ as a response
variable, with a Poisson distribution and a log link function,
and using the log of the ‘number of intrusions’ as an offset.
We evaluated whether the frequency of reactions to human
activities varied in relation to the age of the breeding pair, to
habitat variables potentially influencing the reaction as
defined above (see Table 1) and to the frequency of human
activities.
Finally, in order to observe the impact of human activities
on the breeding parameters of each territory, we calculated
for each territory the frequency of those human activities
that caused alert or flight reactions, and used Spearman
correlations to determine whether the percentage of days
with human activities and the frequency of human activities/
day were related to hatching success (i.e. the proportion
clutches that hatched) or fledging rate (number of fledglings
per nest). The latter two variables were calculated as the
average in each studied territory over the last 5 years. We
assumed that the frequencies and types of human activities
recorded in each territory in the study years were representative of those that would have been recorded over the last
5 years, as in this period there were no notable changes in the
land use or occupation (e.g. large infrastructures, human
settlements or roads or railway lines), or in tourist, agricultural, cattle farming or forestry exploitation (MMA, 2004)
in the territories of these nesting pairs.
Results
Table 2 summarizes the human activities recorded near the
nests, and whether they caused the breeding eagles to
become alarmed and flee. The average alert distance was
252.34 115.28 m (range 50–580), and the average flight
distance was 260.98 190.92 m (range 1–1000).
The most common human activities recorded in the
vicinity of the nests were cars (passing), hikers, cycles and
motorcycles (83%, n = 2018) (Table 2). Passing surface
vehicles (trucks, cars, motorcycles or cyclists) were very
commonly reported but never or almost never provoked
reactions (Table 2). They were eliminated from further
analyses. In subsequent analyses, we grouped other activities as follows: ‘stationary cars’, ‘passing noisy aerial
vehicles’ (including planes and helicopters), ‘passing people’
(including hikers, shepherds and gatherers), ‘campers’ (stationary people), ‘hunters’ and ‘ecotourists’.
The probability that the human activities around nest sites
provoked an alert or flight reaction in Spanish imperial eagles
varied significantly among territories and among types of
activity, and increased when the distance between the activity
and the nest site decreased (Table 3). The probability of an
88
L. M. González et al.
Table 3 Results of the GLM analyses explaining the probability of the
eagles’ alert or flight reactions to a human activity occurring in the
nest area
Probability of
alert reaction
Probability of
flight reaction
Variable
d.f.
w2
P
d.f.
w2
P
Territory
Year
Territory year
Type of activity
Distance
Length
Period
Intrusion load
Distance territory
Distance type
Distance period
10
4
5
5
1
1
1
1
10
5
1
140.4
4.53
2.92
26.49
22.79
1.12
0.67
0.65
21.26
5.89
0.18
0.0001
0.34
0.71
0.0001
0.0001
0.29
0.41
0.42
0.02
0.31
0.66
10
4
5
5
1
1
1
1
10
5
1
119.9
4.53
4.28
28.73
8.14
0.00
1.05
16.74
6.16
11.42
0.01
0.0001
0.33
0.50
0.0001
0.004
0.97
0.30
0.0001
0.81
0.91
0.92
Significant values (Po0.05) are highlighted in bold.
GLM, general linear models.
alert reaction increased at short distances from the nest, and
was most marked for ecotourists, hunters and campers (Fig.
1). Additionally, there was a significant interaction between
distance and territory (Table 3). The probability of flight
reaction also varied among territories and types of activity
(being highest for ecotourists, hunters and passing people)
and increased significantly with distance (Table 3, Fig. 1).
Additionally, it increased with the intrusion load (the number
of people or vehicles intruding, Table 3). If the eagle fled and
the nest was left unattended, the amount of time that the nest
remained unattended increased with the duration of the activity (partial w21 ¼ 98:6, Po0.0001), was higher in the nestling
than the incubation period (partial w21 ¼ 6:75, Po0.009) and
varied with the type of activity (partial w21 ¼ 60:6, Po0.0001),
once again being longest with ecotourists (82 110 min) and
hunters (81 24 min).
Differences in behaviour between territories were not
because of differences in the age of the territory’s occupants,
nor to the height of the nest. Flight reactions were however
less frequent in territories where the nest was not visible
from the tracks, and in more inaccessible territories (Table
4). Additionally, they were negatively related to the frequency of human activities, with reactions being less frequent in areas with higher human activity frequencies (Table
4), which suggests that some habituation occurs.
The frequency of human activities appeared to affect the
Spanish imperial eagle’s breeding success. We found a
significant, negative correlation between the percentage of
clutches that hatch and the percentage of days with intrusions during the incubation period (rs =0.63, Po0.05,
n = 10). Similarly, we found an almost significant correlation with the frequency of interferences/day (rs =0.52,
P40.05, n = 10). In contrast, we found no correlation
between fledging rate and frequency of human activities
during the nestling period (rs =0.14 and 0.07, n = 10,
respectively) (Table 5).
c 2006 The Authors. Journal compilation c 2006 The Zoological Society of London
Animal Conservation 9 (2006) 85–93 L. M. González et al.
Human disturbance and the behaviour of breeding Spanish imperial eagles
Probability of alert reaction
(a) 1.00
Aerial vehicles
Campers
Hunters
Ecotourists
Passing people
Stationary cars
0.80
0.60
0.40
0.20
0.00
0
250
500
Distance (m)
750
1000
Probability of flight reaction
(b) 1.00
Aerial vehicles
Campers
Hunters
Ecotourists
Passing people
Stationary cars
0.80
0.60
0.40
0.20
0.00
0
250
500
Distance (m)
750
1000
Figure 1 Probability of alert (a) and flight (b) reactions to human
activities in Spanish imperial eagles in relation to the distance to the
nest and type of activity.
Discussion
The average flight distance recorded in breeding pairs of
Spanish imperial eagle faced with the presence of human
activities in the vicinity of their nests was similar to those
recorded in other large raptors such as Aquila chrysaetos
(Holmes et al., 1993), and slightly higher than those
recorded in Haliaetus leucocephalus (Stalmaster & Newman,
1978; Fraser, Frenzel & Mathisen, 1985; Grubb & King,
1991). The fact that the average flight distance was similar
to the average alert distance, unlike what has been found
in the majority of bird studies (Fernández-Juricic, Jiménez
Table 4 Results of the GENMOD analysis explaining the frequency of
flight reactions in each territory
Frequency of flight reactions
Variable
d.f.
w2
P
Parameter
estimate
Intrusion frequency
Nest viewshed
Nest visibility (0)
Age (ad)
Inaccessibility
Nest height
1
1
1
1
1
1
38.13
0.49
4.30
0.89
11.04
0.51
0.0001
0.48
0.04
0.34
0.001
0.47
0.06 0.01
0.96 1.35
0.85 0.40
0.47 0.51
0.05 0.01
0.04 0.04
Significant values (Po0.05) are highlighted in bold.
& Lucas, 2002), is probably because the Spanish imperial
eagle, like several other bird species (Blumstein et al.,
2003), can detect threats without necessarily expressing
signs of alarm. The Spanish imperial eagle can even
become immobile, especially while incubating. Thus, early
alert reactions (as opposed to flight reactions, which are
easily detected) may not be perceived by the observer until
the human presence is very near the nest and a flight reaction
occurs. We have therefore concentrated our discussion on
the flight reactions, rather than on alert reactions.
Our study revealed that there is a considerable amount of
human activity around Spanish imperial eagle’s nests,
mostly consisting of passing vehicles. This species breed in
relatively humanized habitats (see González, Bustamante
& Hiraldo, 1990), which would explain the levels of human
activity recorded. However, we found that the Spanish
imperial eagles’ responses can vary greatly depending on
the type of activity, as observed in other raptor studies
(Fraser et al., 1985; Grubb & King, 1991; Grubb et al., 1992;
Steidl & Anthony, 2000). As in the case of other raptors
(Richardson & Miller, 1997), we found that pedestrian
intrusions (mainly by campers, ecotourists and hunters),
led to the highest number of flights, leaving nests temporarily abandoned. What hunters, campers and ecotourists
have in common is that, if they enter the area surrounding
the nest, they remain there for some time and stop frequently. Moreover, they ‘prowl’ around walking in no
particular direction, stopping at irregular intervals and (in
the case of hunters or ecotourists) looking up towards the
sky or at the surrounding area, unlike people carrying out
other pedestrian activities (e.g. shepherds, hikers, etc.), who
cross the Spanish imperial eagle’s territory stopping very
rarely and quickly leave the birds’ field of view. Moreover,
ecotourists try intentionally to find the birds, frequently
looking through binoculars or cameras directly at the nest,
which also would explain the strong reaction of Spanish
imperial eagles’ to the proximity of this kind of pedestrians.
A review recorded negative effects of wildlife observation
and photography on birds in 19 of the 27 studies examined
(Boyle & Samson, 1985).
Another pedestrian activity that had a great impact on
the frequency of flight reactions was hunting. Birds of prey,
in general, and large eagles, in particular, have been persecuted by humans for many years (Bijleveld, 1974). In the
case of the Spanish Imperial Eagle, the most frequent cause
of mortality in the 1970s was shooting (Garzón, 1977;
González, 1991). Although the amount of shooting has
decreased in the period of the study, it still remains a
substantial problem in local areas (L. M. González, R.
Sánchez & J. Oria, unpubl. data). Moreover, a relatively
large number of the juvenile Spanish imperial eagles (12%)
examined that died because of causes other than shooting
were found to have lead pellets in different (non-vital) parts
of their body (M. Hernández, pers. comm.). Therefore, we
think that the flight reaction in the presence of hunters is
probably determined by the level of human persecution that
the Spanish imperial eagles have suffered – or suffer – in the
study area.
c 2006 The Authors. Journal compilation c 2006 The Zoological Society of London
Animal Conservation 9 (2006) 85–93 89
Human disturbance and the behaviour of breeding Spanish imperial eagles
L. M. González et al.
Table 5 Proportion of clutches hatching, frequency of intrusions recorded per day and number of alert and flight reactions in the territories
considered during the incubation and nestling periods
Incubation period
Nestling period
Territory
% of
hatching (n)
Intrusions/
day (n)
Days with
intrusions (%)
Alert
(n)
Flight
(n)
Intrusions/
day
Days with
intrusions (%)
Alert
(n)
Flight
(n)
AV-03
M-16
M-30
M-14/27
AV-04
M-11
M-18
M-20
M-13
M-15
25.0 (4)
60.0 (5)
100 (3)
80.0 (5)
80.0 (5)
90.0 (11)
100 (4)
20.0 (5)
100 (5)
100 (6)
2.46 (57)
8.81 (57)
0.29 (66)
0.34 (122)
2.07 (60)
0.62 (42)
0.33 (6)
0.75 (36)
0.14 (62)
1.28 (84)
63.15
100
22.73
22.95
58.33
42.86
33.3
50
14.52
52.38
1
3
3
1
0
3
2
1
0
5
0
0
5
18
0
5
0
0
0
0
–
–
0.11 (62)
0.26 (35)
4.13 (169)
0.09 (127)
0.33 (61)
–
0.25 (221)
0.45 (240)
–
–
–
–
2
0
0
0
4
–
0
7
–
–
0
5
1
2
6
–
5
4
Otherwise, our results showed that there were strong
variations between territories in the frequency and type of
response to human disturbance. The frequency of response
was affected by two variables (topographic accessibility and
visibility) that are important in the Spanish imperial eagle’s
nest site selection (González et al., 1992; Bisson et al., 2002).
Reactions were less frequent in those territories that were
more inaccessible and where the nest was more hidden from
humans (presumably, those territories that are considered as
‘better’ by the eagles). Higher frequencies of response were
found in those territories where the nest was more exposed,
either because it was visible or because it was in a more
accessible habitat.
Additionally, the fact that the Spanish imperial eagle’s
flight reactions were less frequent in territories with the
highest frequency of intrusion (Table 4), and that some pairs
occupy areas that are relatively humanized and frequented
by humans, appears to indicate that these birds – as found in
the studies of other birds (Lord, Waas & Innes, 1997; Miller,
Knight & Miller, 2001; Ikuta & Blumstein, 2003) and with
raptors in particular (Fraser et al., 1985; Steidl & Anthony,
2000) – can get used to repetitive human disturbance, at least
to a certain extent.
However, and despite these potential habituation or
territory variations in response, our results show that, as
found in other studies of raptors (White & Thurow, 1985;
Holthuijzen, 1990; Steidl & Anthony, 2000), human disturbances that cause flight reactions have a negative impact on
breeding success, in our case on the hatching rate. Another
described effect of the human disturbance in birds is that it
reduces the potential available and occupied habitat
(Fernández-Juricic, 2002) and can force the bird to occupy
lower-quality habitats (McGarigal et al., 1991). Breeding
Spanish imperial eagles, like other raptors studied (Fraser
et al., 1985; Garret, Watson & Anthony, 1993; Steidl &
Anthony, 2000), respond to long-term human activity by
choosing nesting habitats and nest sites in locations with
relatively low levels of human infrastructures (e.g. roads,
urban areas, power lines) (González et al., 1992; Bisson
90
9.68
22.86
80.47
5.51
26.23
–
23.9
69.58
et al., 2002). For this reason, in future studies of nest-site
selection in this species, the quantification of human disturbance activities, besides of the human infrastructures,
should be taken into account as an important variable, but
based on field observations that measure the birds’ reaction
to human activities.
Conservation implications
One of the tools used and recommended by managers to
protect raptors during periods of extreme sensitivity (i.e. the
breeding period) is the creation of spatial and temporal buffer
zones (USFWS, 1981; Howard & Postovit, 1987; Knight &
Skagen, 1988; Knight & Temple, 1995; Richardson & Miller,
1997), the size of which should be based on empirical
estimates at the distances at which humans disturb animals
(Stalmaster & Newman, 1978; Richardson & Miller, 1997).
For some species, a general rule cannot be established, as the
individual variability detected is so great that it makes it
difficult to use a single model for all nests in large areas or for
different populations (Fraser et al., 1985; Knight & Skagen,
1988). In our case, the fact that no significant effect was
found for the interaction between ‘territory’ and distance on
the probability of flight reaction suggests that, in the case of
the Spanish imperial eagle, it is safe to implement a buffer
zone that is similar for all nests (at least in the study area).
Buffer zones may be estimated through different methods
(see the review in Fernández-Juricic et al., 2005). Taking
into account that our reaction data do not display a normal
distribution, we suggest using the upper percentiles of the
prediction of the probability of flight distances (Fig. 2). This
method has been used in specific studies, e.g. 70% and
90–95% in H. leucocephalus (Stalmaster & Newman, 1978;
Grub & King, 1991; McGarigal et al., 1991; Anthony, Steidl
& McGarigal, 1995) and 90% in wintering A. chrysaetos
(Holmes et al., 1993). In our case, with a 100% prediction of
the probability of flight reaction, the safety distance would
be 1000 m. With 99% it would be 800 m and with 95% it
c 2006 The Authors. Journal compilation c 2006 The Zoological Society of London
Animal Conservation 9 (2006) 85–93 L. M. González et al.
Human disturbance and the behaviour of breeding Spanish imperial eagles
1.00
Alert
Flight
Probability
0.80
0.60
0.40
0.20
0.00
0
250
500
Distance (m)
750
the Dirección General para la Biodiversidad del Ministerio
de Medio Ambiente and the Consejerı́a de Medio Ambiente
de la Comunidad de Madrid. Valuable information was
provided by the autonomous communities of Madrid,
Castilla-León, Castilla-La Mancha, Extremadura and Andalucı́a, all represented in the National Spanish Imperial
Eagle Working Group. We would also like to thank two
anonymous referees for improving the manuscript, and
Dave Elston for the statistical advice.
1000
Figure 2 Probability of alert or flight reactions in the Spanish imperial
eagle (all human activities pooled) in relation to the distance to the nest.
would be 450 m (Fig. 2). In view of the fact that the Spanish
imperial eagle is an endangered species, it appears reasonable to use a minimum distance of 500 m for the radius of the
inner buffer zone, where no human activity should be
allowed during the breeding season. A distance of between
500 and 800 m could be used for the radius of the vulnerable
zone or the outer buffer zone, which is similar to that used
for a 99% predicted flight reaction, where some human
activities such as vehicles passing may be authorized. Beyond this outer buffer zone, any activities authorized by the
general habitat conservation restrictions may be allowed. It
is interesting to note the similarity of this inner distance
to the distance recommended previously based on personal
experience (González, 1991, 1996).
Moreover, two additional issues must be borne in mind
when designing these buffer zones for the Spanish imperial
eagle: (1) they should include both visible and hidden zones, in
accordance with what was discovered in other studies (Beale
& Monaghan, 2004); and (2) as intrusion load also had a
significant effect on the probability of flight reactions, buffer
zones should bear in mind the number of people involved in
each type of activity, especially in nesting areas that are open
to the public and are visited by large numbers of people, such
as national parks (e.g. Doñana or Cabañeros in Spain). It is
advisable that buffer distances should be increased considerably where human activities involve large groups of visitors.
Overall, our study shows that human disturbance can be
an important variable affecting raptor behaviour and reproduction, and that empirical studies like the present one can
be used to optimize management guidelines.
Acknowledgements
We are indebted to Javier Sánchez, Javier Sanz, Aitor
Sierra, Julio Caballero, Marı́a Fernández and Raúl Tomás
for their help with the fieldwork. We are particularly grateful to Victor G. Matarranz, who, with his usual skill and
know-how, tagged all the nestlings. Thanks are also due to
Luis Prada for support of the study. Sheila Hardie translated the text into English. This study was jointly funded by
References
Anthony, R.G., Steidl, R.J. & McGarigal, K. (1995). Recreation and Bald Eagles in the Pacific Northwest. In Wildlife
and recreationalists: coexistence through management and
research: 223–241. Knight, L. & Gutzwiller, K.J. (Eds).
Washington: Island Press.
Bautista, L.M., Garcı́a, J.T., Calmaestra, R.G., Palacı́n, C.,
Martı́n, C.A., Morales, M.B., Bonal, R. & Viñuela, J.
(2004). Effect of weekend road traffic on the use of space by
raptors. Conserv. Biol. 18, 1–7.
Beale, C.M. & Monaghan, P. (2004). Human disturbance:
people as predation-free predators? J. Appl. Ecol. 41,
335–343.
Bijleveld, M. (1974). Birds of prey in Europe. London: The
MacMillan Press Ltd.
BirdLife International. (2004). Threatened birds of the world
2004. CD-ROM. Cambridge: BirdLife International.
Bisson, I.A., Ferrer, M. & Bird, D.M. (2002). Factors influencing nest-site selection by Spanish Imperial Eagles.
J. Field Ornithol. 73, 298–302.
Blumstein, D.T., Anthony, L.L., Harcourt, R.G. & Ross, G.
(2003). Testing a key assumption of wildlife buffer zones: is
flight initiation distance a species – specific trait? Biol.
Conserv. 110, 97–100.
Boyle, S.A. & Samson, F.B. (1985). Effects of nonconsumptive recreation on wildlife: a review. Wildl. Soc. Bull. 13,
110–116.
Calderón, J., Castroviejo, J., Garcı́a, L. & Ferrer, M. (1987).
El Águila Imperial (Aquila adalberti) en Doñana: algunos
aspectos de su reproducción. Alytes 5, 47–72.
Castaño, J.P. & Guzmán, J.A. (1995). Aspectos sobre la
reproducción de Aquila adalberti y Aquila chrysaetos en
Sierra Morena Oriental. Ardeola 42, 83–89.
Consejerı́a de Medio Ambiente de Castilla-La Mancha.
(2003). Plan de Recuperación del Águila imperial ibérica
en Castilla-la Mancha. Boletı́n Oficial CLM 131,
14335–14370.
Consejerı́a de Medio Ambiente de Castilla y León. (2003).
Plan de Recuperación del Águila imperial ibérica en
Castilla y León. Boletı́n Oficial CyL 195, 13335–13354.
Fernández, C. & Azkona, P. (1993). Human disturbance
affects parental care of marsh harriers and nutritional
status of nestlings. J. Wildl. Manage. 57, 602–608.
c 2006 The Authors. Journal compilation c 2006 The Zoological Society of London
Animal Conservation 9 (2006) 85–93 91
Human disturbance and the behaviour of breeding Spanish imperial eagles
Fernández-Juricic, E. (2002). Can human disturbance promote nestedness? A case study with breeding birds in urban
habitat fragments. Oecologia 131, 269–278.
Fernández-Juricic, E., Jiménez, M.D. & Lucas, E. (2002).
Factors affecting intra- and inter-specific variations in the
difference between alert and flight distances in forested
habitats. Can. J. Zool. 80, 1212–1220.
Fernández-Juricic, E., Venier, P., Renison, D. & Blumstein,
D.T. (2005). Sensitivity of wildlife to spatial patterns of
recreationist behavior: a critical assessment of minimum
approaching distances and buffer areas for grassland birds.
Biol. Conserv. 125, 225–235.
Forsman, D. (1999). The raptors of Europe and the Middle
East. A handbook of field identification. London: T & A.D.
Poyser.
Fraser, J.D., Frenzel, L. & Mathisen, J.E. (1985). The impact
of human activities on breeding bald eagles in north-central
Minnesota. J. Wildl. Manage. 49, 585–592.
Garret, M.G., Watson, J.W. & Anthony, R.G. (1993). Bald
eagle home range and habitat use in Columbia River
estuary. J. Wildl. Manage. 57, 19–27.
Garzón, J. (1977). Birds of prey in Spain: the present situation. In Proceedings of the world conference on birds of prey:
159–170. Chancellor, R.D. (Ed.). Vienna: I.C.B.P.
González, L.M. (1991). Historia Natural del Aguila Imperial
Ibérica (Aquila adalberti Brehm, 1861). Colección Técnica.
Madrid: ICONA, Ministerio de Agricultura.
González, L.M. (1996). Action plan for the Spanish imperial
eagle (Aquila adalberti). In Globally threatened birds in
Europe. Action plans: 175–189. Heredia, B., Rose, L. &
Painter, M. (Eds). Strasbourg: Council of Europe Pub.
González, L.M., Bustamante, J. & Hiraldo, F. (1990).
Factors influencing the present distribution of the
Spanish Imperial Eagle (Aquila adalberti). Biol. Conserv.
51, 311–319.
González, L.M., Bustamante, J. & Hiraldo, F. (1992). Nesting
habitat selection by the Spanish Imperial Eagles Aquila
adalberti. Biol. Conserv. 59, 45–50.
Grier, J.W. & Fyfe, R.W. (1987). Preventing research and
management disturbance. In Raptor management techniques manual: 173–182. Giron Pendleton, B.A., Millsap,
B.A., Cline, K.W. & Bird, D.M. (Eds). Washington: Natl.
Wild. Fed.
Grubb, T.G, Bowerman, W.W., Giesy, J.P. & Dawson, G.A.
(1992). Responses of breeding bald eagles, Haliaetus leucocephalus, to human activities in northcentral Michigan.
Can. Field Nat. 106, 443–453.
Grubb, T.G. & King, R.M. (1991). Assessing human disturbance of breeding bald eagles with classification tree
models. J. Wildl. Manage. 55, 500–511.
GTAI. (2005). Resumen del estado actual de la población del
Águila Imperial Ibérica. Grupo de Trabajo del Águila
Imperial. Madrid: DGB-Ministerio de Medio Ambiente.
Holmes, T.L., Knight, R.L., Stegall, L. & Craig, G.R. (1993).
Responses of wintering grassland raptors to human disturbance. Wildl. Soc. Bull. 21, 461–468.
92
L. M. González et al.
Holthuijzen, A.M. (1990). Effects of blasting on behavior and
productivity of nesting prairie falcons. Wildl. Soc. Bull. 18,
270–281.
Howard, R. & Postovit, B.C. (1987). Impacts and mitigation
techniques. In Raptor management techniques manual:
183–208. Giron Pendleton, B.A., Millsap, B.A., Cline,
K.W. & Bird, D.M. (Eds). Washington: Natl. Wild. Fed.
Ikuta, L.A. & Blumstein, D.T. (2003). Do fences protect birds
from human disturbance? Biol. Conserv. 112, 447–452.
Knight, R.L. & Skagen, S.K. (1988). Effects of recreational
disturbance on birds of prey: a review. In Proceedings of
southwest raptor management symposium and workshop:
355–359. Inst. Wildl. Res. Natl. Wildl. Fed. Sci. Tech. Ser.
No. 11.
Knight, R.L. & Temple, S.A. (1995). Wildlife and recreationists: coexistence through management. In Wildlife and
recreationists: coexistence through research and management: 327–333. Knight, R.L. & Gutzwiller, K.J. (Eds).
Covelo: Island Press.
Lord, A., Waas, J.R. & Innes, J. (1997). Effects of human
activity on the behaviour of northern New Zealand dotterel
(Charadrius obscurus aquilonius) chicks. Biol. Conserv. 82,
15–20.
McGarigal, K., Anthony, R.G. & Isaacs, F.B. (1991). Interactions of human and bald eagles on the Columbia River
estuary. Wildl. Monogr. 115.
Miller, S.G., Knight, R.L. & Miller, C.K. (2001). Wildlife
responses to pedestrians and dogs. Wildl. Soc. Bull. 29,
124–132.
MMA. (2001). Estrategia nacional para la conservacion del
Aguila imperial ibérica (Aquila adalberti). Madrid: Dirección General para la Biodiversidad. Ministerio de
Medio Ambiente.
MMA. (2003). Atlas y Manual de los Hábitats de España.
Madrid: Dirección General para la Biodiversidad. Ministerio de Medio Ambiente.
MMA. (2004). Inventario Nacional Forestal. Madrid: Dirección
General para la Biodiversidad.Ministerio de Medio Ambiente.
PND. (1992). El Plan del Manejo del Parque Nacional de
Doñana, su entorno y áreas de dispersión juvenil. Huelva:
ICONA, Parque Nacional de Doñana.
Richardson, C.T. & Miller, C.K. (1997). Recommendations
for protecting raptors from human disturbance: a review.
Wildl. Soc. Bull. 25, 634–638.
Rodgers, J.A. & Smith, H.T. (1995). Set-back distances to
protect nesting bird colonies from human disturbance in
Florida. Conserv. Biol. 9, 89–99.
Ruhlen, T.D., Abbott, S., Stenzel, L.E. & Page, G.W. (2003).
Evidence that human disturbance reduces Snowy Plover
chick survival. J. Field Ornithol. 74, 300–304.
Stalmaster, M.V. & Newman, J.R. (1978). Behavioral responses of wintering bald eagles to human intrusion.
J. Wildl. Manage. 42, 506–513.
Steidl, R.J. & Anthony, R.G. (1996). Responses of Bald
Eagles to human activity during the summer in interior
Alaska. Ecol. Appl. 6, 482–491.
c 2006 The Authors. Journal compilation c 2006 The Zoological Society of London
Animal Conservation 9 (2006) 85–93 L. M. González et al.
Steidl, R.J. & Anthony, R.G. (2000). Experimental effects of
human activity on breeding Bald Eagles. Ecol. Appl. 10,
258–268.
Swarthout, E.C.H. & Steidl, R.J. (2001). Flush responses of
Mexican spotted owls to recreationists. J. Wildlife Manage.
65, 312–317.
USFWS. (1981). Bald eagle. Management guidelines. OregonWashington: U.S. Fish & Wildlife Service.
Human disturbance and the behaviour of breeding Spanish imperial eagles
Verhulst, S., Oosterbeek, K. & Ens, B.J. (2001). Experimental
evidence of effects of human disturbance on foraging and
parental care in oystercatchers. Biol. Conserv. 101,
375–380.
White, C. & Thurow, T.L. (1985). Reproduction of ferruginous hawks exposed to controlled disturbance. Condor 87,
14–22.
c 2006 The Authors. Journal compilation c 2006 The Zoological Society of London
Animal Conservation 9 (2006) 85–93 93