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Motion capacity, geography and ecological features explain the present distribution of a migratory top predator


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Presence and distribution of ecological barriers shapes the distribution of migratory birds as well as any other living organism. In Italy, short-toed snake eagles (Circaetus gallicus) breed in the northern and western areas of the peninsula but the species is rare in the south or the islands. The Italian population of this species migrates across the Mediterranean at the Strait of Gibraltar rather than crossing the large stretch of sea between Sicily and Tunisia. This suggests that, in Italy, fall migration is oriented south–north and spring migration north–south. In this paper we test the hypothesis that the accessibility of the suitable habitat area along the Italian Peninsula is in relation to the geographical migration pattern of the studied species. We integrated information from the movement ecology, the geography and the traditional ecological features in order to provide an ecological explanation of the current biogeographical pattern of our model species. We compared statistical models with and without latitude as a predictor. Each model was based on ecological and geographical variables, including land use, prey availability, spatial distribution of environmental elements (patch analysis), geomorphology, and geography. These models predict two patterns of suitability for short-toed snake eagles in Italy. Our results suggest that the abundance of this species increases with latitude despite the existence of large areas of suitable habitat in southern Italy. We suggest that the actual distribution of the short-toed snake eagle in Italy is influenced by the particular migration path used by this population, supporting the hypothesis that this species is still colonizing the Italian Peninsula through an unexpected colonization direction from north to south.
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1 23
Ecological Research
ISSN 0912-3814
Volume 30
Number 1
Ecol Res (2015) 30:181-190
DOI 10.1007/s11284-014-1226-2
Motion capacity, geography and ecological
features explain the present distribution of
a migratory top predator
Michele Panuccio, Giuseppe Lucia,
Nicolantonio Agostini, Dario Ottonello
& Giuseppe Bogliani
1 23
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Michele Panuccio Giuseppe Lucia Nicolantonio Agostini
Dario Ottonello Giuseppe Bogliani
Motion capacity, geography and ecological features explain the present
distribution of a migratory top predator
Received: 14 July 2014 / Accepted: 24 November 2014 / Published online: 6 December 2014
The Ecological Society of Japan 2014
Abstract Presence and distribution of ecological barriers
shapes the distribution of migratory birds as well as any
other living organism. In Italy, short-toed snake eagles
(Circaetus gallicus) breed in the northern and western
areas of the peninsula but the species is rare in the south
or the islands. The Italian population of this species
migrates across the Mediterranean at the Strait of
Gibraltar rather than crossing the large stretch of sea
between Sicily and Tunisia. This suggests that, in Italy,
fall migration is oriented south–north and spring
migration north–south. In this paper we test the
hypothesis that the accessibility of the suitable habitat
area along the Italian Peninsula is in relation to the
geographical migration pattern of the studied species.
We integrated information from the movement ecology,
the geography and the traditional ecological features in
order to provide an ecological explanation of the current
biogeographical pattern of our model species. We com-
pared statistical models with and without latitude as a
predictor. Each model was based on ecological and
geographical variables, including land use, prey avail-
ability, spatial distribution of environmental elements
(patch analysis), geomorphology, and geography. These
models predict two patterns of suitability for short-toed
snake eagles in Italy. Our results suggest that the
abundance of this species increases with latitude despite
the existence of large areas of suitable habitat in
southern Italy. We suggest that the actual distribution of
the short-toed snake eagle in Italy is influenced by the
particular migration path used by this population, sup-
porting the hypothesis that this species is still colonizing
the Italian Peninsula through an unexpected coloniza-
tion direction from north to south.
Keywords Colonization direction ÆAccessibility Æ
Migratory detour ÆEcological barriers ÆShort-toed
snake eagle ÆCircaetus gallicus ÆItaly
The present distribution of an organism is the result of
the interaction between ecological, movement-related
and geographical features (Cumming et al. 2012). In
particular the ecological niche and the probability of
colonization affect the distributional limits of a species
(Begon et al. 2006). Ecological niche is related to several
different factors, including foraging and nesting oppor-
tunities. The probability of colonization depends on the
dispersal abilities of the species and its dispersal behav-
iour, as well as geographic features such as natural
barriers (Alerstam 1990; Tellerı
´a et al. 2009). Therefore,
the current biogeographical patterns might be explained
by hypotheses that are related to environmental, mor-
phological and historical data (Cumming et al. 2012).
Europe has been colonized by several species of birds
since the end of the last glacial age about 10,000 years
ago. Several species have colonized areas located at
higher latitudes through a northern extension of their
breeding ranges (Mayr and Meise 1930; Bruderer and
Salewski 2008). From the end of last glaciation, Palae-
arctic migrants have followed a colonization path from
south to north and were assisted by the process of dis-
persal (Alerstam 1990; Berthold 2001; Rappole and
Jones 2002).
Electronic supplementary material The online version of this article
(doi:10.1007/s11284-014-1226-2) contains supplementary material,
which is available to authorized users.
M. Panuccio (&)ÆG. Bogliani
DSTA-Department of Earth and Environmental Sciences,
University of Pavia, Via Ferrata 9, 27100 Pavia, Italy
Tel.: 0039-349-2340719
M. Panuccio ÆG. Lucia ÆN. Agostini
MEDRAPTORS (Mediterranean Raptor Migration Network),
Via Mario Fioretti 18, 00152 Rome, Italy
D. Ottonello
DAIS-Department of Environmental Sciences, Informatics and
Statistics, Ca
`Foscari University of Venice, Dorsoduro 2137,
30123 Venice, Italy
Ecol Res (2015) 30: 181–190
DOI 10.1007/s11284-014-1226-2
Author's personal copy
The short-toed snake eagle (Circaetus gallicus)isa
widespread summer breeder in Europe and in the
Mediterranean basin and overwinters in a wide area of
Africa south of Sahara (Cramp and Simmons 1980;
Ferguson-Lees and Christie 2001). It is a highly spe-
cialized raptor, preying predominantly on snakes (up to
100 %; Ferguson-Lees and Christie 2001); therefore, as
a specialized predator, its distribution should coincide
with the distribution of its prey (Newton 1998). A study
carried out in Spain (Moreno-Rueda and Pizarro 2007)
showed that short-toed snake eagles are found mainly in
areas with shrub-lands, where they can easily locate and
capture their prey, and in forests, which provide suitable
nesting habitat. Eagle presence also correlates with
snake species richness (Moreno-Rueda and Pizarro
2007). Research in Greece also showed that the presence
of short-toed snake eagle is linked to forests for nest
building and to open areas like pasturelands and culti-
vation for foraging (Bakaloudis et al. 1998,2005). The
European population of short-toed snake eagle is esti-
mated to be less than 10,000 pairs and its status is Rare;
its low reproductive rate and high diet specialization
makes it vulnerable to extinction (Birdlife International
2004). The population in Italy is estimated to 350–400
breeding pairs (Birdlife International 2004), but recent
counts at some migration hotspots have shown that their
numbers are increasing (Baghino and Premuda 2007;
Panuccio et al. 2012,2013). Most of the breeding pairs in
Italy are distributed in northern Italy and along the
western slope of central Italy (Campora and Cattaneo
2006). In Southern Italy few tens of pairs do breed but it
seems that the species has been expanding in recent years
(Mellone et al. 2011). The short-toed snake eagle is a
broad-winged raptor that uses soaring-gliding flight ra-
ther than powered flight; as a result this species tends to
migrate over land and to avoid water crossing where
thermal currents are absent and it would be forced to use
active flight (Kerlinger 1989). Individuals belonging to
the Italian population migrate both during spring and
autumn across the Strait of Gibraltar (14 km of water
crossing) rather than taking the Central Mediterranean
flyway that is shorter, although the water crossing is
longer (at least 130 km; Agostini et al. 2002a,b,2004;
Mellone et al. 2011). Similarly, individuals breeding in
Greece migrate through Turkey and cross the sea at
Bosphorus (Panuccio et al. 2012). Since most breeding
pairs of this species in Italy are located along its
migration route, Agostini and Mellone (2008) suggested
that the short-toed snake eagle may still be colonizing
Italy from the western part of its European breeding
range and that, therefore, the population has not yet
reached its carrying capacity.
The distribution of living organisms is a widely
studied subject in ecology but, on the other hand, the
interaction between distribution and migration routes is
a poorly investigated topic. In this paper we test the
hypothesis that the actual distribution of short-toed
snake eagle in Italy reflects the colonization history and
is strongly influenced by the migration route more than
other ecological parameters such as prey availability and
the spatial distribution of vegetation and morphology.
For this purpose in the analysis we considered several
ecological (land use and prey richness), topographic
(altitude), and latitudinal parameters in order to deter-
mine which affect the breeding distribution of short-toed
snake eagle in Italy and to determine whether some areas
of Southern Italy are not suitable for short-toed snake
eagles or, although if suitable, they have not been col-
onized or re-colonized yet.
Study area
The study was performed in Italy (301,302 km
including the large islands of Sicily and Sardinia. On the
01-Jan-2010 the human population was 60,340,328
(ISTAT, website:
html). The climate varies considerably with latitude. In
the south it is warm, with almost no rain in summer,
while in the Northern part of the Peninsula temperature
is cool with rainfall more evenly distributed throughout
the year. The mean altitude in Italy is 337 m above sea
level. According to Corine Land Cover 2000, Italy is
composed of 152,435 km
of cultivated lands (50.6 %),
18,835 km
of permanent pasture lands (6.3 %),
79,425 km
of woodlands (26.4 %), 22,555 km
shrubs (7.5 %), 3,827 km
of wetlands (1.3 %) and
14,340 km
of urbanized areas (4.8 %). In the lowlands
agriculture is very intensive and devoted mainly to
monoculture, while on the hills and mountains tradi-
tional and less intensive agriculture is still practiced al-
though land abandonment is spreading. Mainland Italy
may be divided into four major geographical and vege-
tational areas: the Alps and the Padana plain in the
north, the Apennines and the coastal slopes (7,456 km
of coastlines) in the center and the south. The Alpine
area is relatively unspoiled, with deciduous, mixed
coniferous forests, alpine pastures above the timberline,
and snowfields and glaciers on higher peaks. The Po
valley is the largest lowland area in Italy, mainly covered
by intensive agriculture. Large areas of the Apennine
mountains are still covered by semi-natural deciduous
forests, mostly oak (Quercus spp.), beech (Fagus sylvat-
ica) and sweet chestnut (Castanea sativa), although large
areas have been cleared for agriculture and pasture.
Coastal areas in Italy are dominated by shrub and in
particular by typical Mediterranean scrub. The pro-
tected areas in Italy cover a surface of 13,000 km
(4.3 %; Brandmayr 2002).
Sampling units
The geographical grid we used to divide the Italian
peninsula in several sampling units is the same used from
Author's personal copy
Military Geographical Institute (IGM) to draw the
1:25,000 maps of Italy in UTM projections; we consid-
ered 3,541 square cells of 10 ·10 km. Because the Ital-
ian peninsula is located over three ‘‘zones’’ of 6 degrees
in latitude, at the transition from one zone to another
the grid is compressed and rotated, so some squares (less
than 5 % of the total) have an area less than 100 km
similar limitation of extension involves also coastal cells.
To avoid effects due to the difference in size among cells,
we included variables that used percent coverage instead
of absolute cell surface. To determine prey availability
(reptile species richness), we used the grid and data set
used by Sindaco et al. (2006) for the atlas of the reptiles
and amphibians of Italy made available by SHI (Soci-
etas Herpetologica Italica).
Presence data of short-toed snake eagle
Short-toed snake eagle presence data was obtained by
consulting several atlas of bird distribution in Italy; we
assumed that the coverage effort for each local atlas was
similar since all atlas were realized following similar
guidelines (Fig. 1; Mingozzi et al. 1988; Fraissinet and
Kalby 1989; Brichetti and Fasola 1990; Meschini and
Frugis 1993; Gruppo Vicentino Studi Ornitologici
‘‘NISORIA’’ 1994; Boano et al. 1995; Ravasini 1995;
Tellini Florenzano et al. 1997; Bon et al. 1999; Gellini
and Ceccarelli 2000; Fracasso et al. 2003; Bordignon
2004; Pedrini et al. 2005; Bionda and Bordignon 2006;
Giacchini 2007; Mezzavilla and Bettiol 2007; Ientile and
Massa 2008; La Gioia 2009) and also by using personal
observations of nest locations. In the atlas, the presence
of species in each sample unit is listed in three ways:
certain, probable and possible, following the indications
of EBCC (Hagemeijer and Blair 1997). In this study, we
considered only the first two categories to classify pre-
sence. In most cases we used the same grid as that used
in the atlas; when the atlas grid was smaller than ours,
we assigned a presence value to our cell if at least one of
the atlas cells were included in our sampling units. At the
end of data collecting we had 94 cells (10 ·10 km) with
presence data.
Predictive variables
To model the relationship between habitat features and
short-toed snake eagle presence, we first considered 30
environmental variables (Table S1) grouped into 5 cat-
egories: land use, prey availability, spatial distribution of
environmental elements (patch analysis), geomorphol-
ogy, and geography (latitude and longitude). Variables
representing land use were obtained by Corine Land
Cover 2000 to the third level. We first grouped land use
categories that had similar ecological significance for the
study species into seven new variables: forests, shrubs,
crops and orchards, meadows and pastures, populated
areas, bare rock, and wetlands. For each cell we calcu-
lated the percentage coverage of land use variables. Prey
availability was measured as the number of reptile spe-
cies (snakes and lizards, excluding Gekkonidae for lack
of daytime activities of this family) present in each cell.
Data on the presence of reptiles were derived from the
atlas of Sindaco et al. (2006). Analysis of the spatial
distribution of land use patches was carried out with the
Esri ArcMap 9.2 Patch Analyst extension (Rempel and
Carr 1999). This analysis investigates the geometry of
selected patches (here, land use polygons) and perime-
ters (for details on these measures see Elkie et al. 1999).
Data on the geomorphology were derived from digital
elevation model (DEM) of Italy with a spatial resolution
of 250 m. In each cell six measures of altitude were
calculated: minimum, maximum, average, median,
standard deviation, and the coefficient of variation.
Geographical variables were represented by values of
latitude and longitude of the cell centroid. In particular
we used the latitude as a proxy of the distance from the
main migration route of the studied species. Finally we
squared the following variables to evaluate if the values
of forest cover, mean altitude and mean patch fractal
dimension were non-monotonically related to the suit-
ability of the study area for the short-toed snake eagle.
Statistical models and procedure
We compared models with and without latitude as a
predictor to test the hypothesis that our studied species
Fig. 1 Distribution map of short-toed snake eagle in Italy,
according to the data compilation from different local atlases.
Each dot denotes presence in a 10 ·10 km
Author's personal copy
is still colonizing Italy along north–south gradient. Here
following are the details of the procedure we followed to
build the different models.
We first tested for collinearity of variables within the
categories inside the sampling units in order to select
variables to use in the models. To do this we tested the
normality of variables with Kolmogorov–Smirnov test,
and if any variables were not normally distributed we
transformed the data (square root, arcsine or natural
logarithm depending on the variable). We used a logistic
regression to test which predictive variables affect the
distribution of the species in Italy. In order to verify
which variables influenced the presence of short-toed
snake eagles we compared variables in squares with
presence data (n= 94) with the same number of cells
without presence (n= 94); these cells were randomly
selected among those in which the species was not
present according to the distribution reported in the
atlas we consulted. We also generated new variables by
squaring those variables that were non-monotonically
related to the presence of the species. We retained a
priori the latitude as predictor since it is in our starting
hypothesis, but also the three variables that have been
previously considered significant in explaining short-
toed snake eagles presence. These variables are: prey
availability, proportion of forests, proportion of shrubs
´nchez-Zapata and Calvo 1999; Bustamante and
Seoane 2004; Bakaloudis et al. 2005; Moreno-Rueda
and Pizarro 2007;Lo
´pez-Iborra et al. 2011). After that
we tested 23 random combination of models (all con-
taining those four retained variables) excluding those
variables who were auto-correlated. The starting set of
variables for the logistic regression is shown in Table 1.
Model selection was made choosing the model with the
smallest value of Akaike information criterion (AIC;
Manly et al. 2002). As model B we run the same selected
model without the latitude as predictor. In the models
we forced all of the chosen variables in the same run
with the Enter method in SPSS software.
We then obtained a value of probability of presence
between 0 and 1 for each cell that varies depending on
the model and we used this difference to compare each
model including ‘‘Y_CENTR’’ and the corresponding
model without this variable.
Moreover, to test the results of logistic regression
models we generated a further model based on boosted
regression trees analysis (BRT). Unlike the logistic
regression, BRT fits a large number of relatively simple
models which are then combined for prediction. BRT
uses two algorithms: regression trees and boosting builds
and combines a collection of models (De’ath and Fab-
ricius 2000; Friedman et al. 2000; Schapire 2003;
Leathwick et al. 2006; Elith et al. 2006,2008). For the
BRT model we used the same variables used in the
regression model and we chose the best model selected
according to lower deviance value and the area under
curve (AUC) of its receiver operating characteristic
Variables used to run the analysis are shown in Table 1.
The best model (Model A) with the lowest value of AIC
included nine variables (Table 2). This model achieved
an overall value of correct percentage of 77.7 % (84.1 %
for absence and 64.9 % for presence). The AUC value of
the ROC curve was 0.848. We tested the same model
without the latitudinal variable; this second model
(Model B) showed a higher AIC value and included
eight variables (Table 2). This model achieved an overall
value of correct percentage of 74.5 % (81.5 % for ab-
Table 2 Logistic regression statistics (Wald), parameter estimates (B) and significance (P) of the variables included in the short-toed snake
eagle distribution Model A and B, in Italy
Model A Model B
B Wald PB Wald P
Latitude 0.000 20.655 0.000
Mean altitude 0.001 1.943 0.163 0.002 3.453 0.063
(Mean altitude)
0.000 3.280 0.070 0.000 8.125 0.004
Proportion of forest 10.547 22.306 0.000 10.960 24.842 0.000
(Proportion of forest)
8.895 13.975 0.000 8.390 12.763 0.000
Number of reptile species 0.185 19.102 0.000 0.212 28.727 0.000
Proportion of shrubs 1.937 2.785 0.095 488.816 0.061 0.805
Mean patch fractal dimension 534.33 0.766 0.381 187.219 0.710 0.399
(Mean patch fractal dimension)
201.555 0.738 0.390 0.308 0.704 0.402
Table 1 Variables used to perform logistic regression
Category Variables
Land use Proportion of meadows and pastures
Proportion of crops and orchards
Proportion of forests
(Proportion of forests)
Proportion of shrubs
Prey availability Number of reptile species
(snakes and lizards)
Spatial distribution of
environmental elements
(land use—patch analysis)
Mean patch edge
Mean patch fractal dimension
(Mean patch fractal dimension)
Geomorphology Mean altitude
(Mean altitude)
Geography Latitude
Author's personal copy
sence and 60.4 % for presence); the AUC value of the
ROC curve was 0.824. Using the results of these two
models we created two different distribution maps of
probability. Model A, which includes latitude as a var-
iable, predicts that the potential distribution of short-
toed snake eagles is mainly restricted to central and
northern Italy (Fig. 2a). By contrast, Model B, which
does not include latitude as a variable, predicts a wider
potential distribution that includes southern Italy
(Fig. 2b).
Similarly, plotting the probability of occurrence of
short-toed snake eagles in the sample units in relation to
latitude, a clear difference between the two models ap-
pears. Model B predicted a more homogeneous proba-
bility of species distribution along the latitudinal
gradient (Fig. 3b). On the other hand, according to the
same model tested with latitude as predictor, the prob-
ability of occurrence of the studied species is restricted to
the northern and the central part of the Italian penin-
sula (Fig. 3a).
The model obtained using boosted regression trees
(deviance = 0.244, deviance Cross-validation esti-
mate = 0.161; SE = 0.006) confirmed that the three
most important predictive variables for the presence of
short-toed snake eagle are latitude, mean altitude and
the number of prey species (Fig. 4). For all these
parameters, increasing values increased the fitted func-
tion of the model. Plotting the interaction between the
mean altitude and the number of prey species we ob-
tained a maximum fitted value of 0.57 (Fig. 5) in cor-
respondence of the large number of species and a
medium–high value at mean altitude. The increase of
value of the forest variable was also linked to an increase
in model fitting despite its low contribution in the model.
Ecological parameters
This study shows that, of the variables that potentially
affect the breeding distribution of the short-toed snake
eagle, the strongest predictors are prey richness, forests,
and the mean altitude of the territory. This result was
obtained using both models A and B as well as the
boosted regression tree model. Forests are important for
short-toed snake eagles because the species nests in these
habitats; this is in agreement with previous research
´nchez-Zapata and Calvo 1999; Bustamante and
Seoane 2004; Bakaloudis et al. 2005;Lo
´pez-Iborra et al.
2011). As shown by the high Wald value of the variable
‘‘square root forest’’ (Table 2), the increase of forested
areas is important for the presence of short-toed snake
eagles; however, there is a threshold value beyond which
the extension of forests becomes limiting for this species,
since snake eagles hunt in open areas where reptilian
prey are probably abundant and most accessible (see
Moreno-Rueda and Pizarro 2007; Bakaloudis 2009;
´pez-Iborra et al. 2011). Mean altitude may be
important in the BRT model because, in Italy, forests
are almost absent from lowlands, such as the Po valley,
and because agriculture on the Italian plains is inten-
sive (monoculture). Therefore, lower altitudes do not
Fig. 2 Probability classes of the short-toed snake eagle distribution
according to Model A (a) and Model B (b) in Italy
Author's personal copy
provide suitable nesting habitat for short-toed snake
eagles in Italy. Prey richness was the other variable that
explained eagle distribution in all models. A previous
study of short-toed snake eagles in southern Spain found
a relationship between the presence of eagles and species
richness of reptiles (Moreno-Rueda and Pizarro 2007).
Despite its high trophic specialization, the short-toed
snake eagle behaves as a taxonomic generalist within this
prey type, and selects optimal prey sizes regardless of the
species (Gil and Pleguezuelos 2001).
What factors, then, explain the correlation between
prey species richness and eagle distribution? Different
hypotheses have been proposed to explain this correla-
tion. One possibility is that the abundance of reptile
individuals correlates with reptile species richness and
the abundance of individuals determines the presence of
raptors (Evans et al. 2005; Moreno-Rueda and Pizarro
2007). Intra- and inter-species interactions have also
been proposed. It has also been hypothesized that the
presence of short-toed snake eagles increases reptile
species richness by controlling the most abundant spe-
cies and reducing the intensity of competition in the
reptile community through a top-down process (Mo-
reno-Rueda and Pizarro 2007).
Differently from previous research, our model did not
reveal shrubland to be an important variable. This may
be because other variables have a higher importance in
explaining the probability of the occurrence of the
studied species in the study area (i.e. number of reptile
species and proportion of forests).
The role of the latitude
In our first Model (A) latitude also had a significant
effect on the breeding distribution of short-toed snake
eagles in Italy. Its effect is the opposite of that docu-
mented in Spain (Lo
´pez-Iborra et al. 2011), where lati-
tudinal increase was shown to have a negative effect on
the distribution of the species. By contrast, we found
that eagle presence seems to increase with latitude.
However, the distribution of the short-toed snake eagle
in Europe does not lead to the conclusion that latitude
could have, at a continental scale, the effect showed in
the model A. In fact, this eagle is widely distributed in
southern Europe at the same latitude of southern Italy in
Spain, Greece and Turkey (Handrinos and Akriotis
1997; Man
˜osa 2003; Kirwan et al. 2008). In addition,
our model B clearly showed that large areas, especially
in the southernmost part of the peninsula, are suitable
for this species although the known distribution, showed
by data available for Italy, is well represented by the
map obtained with the Model A. The discrepancy be-
tween model B and the actual distribution of the short-
toed snake eagle in Italy (well reflected by Model A)
could result from the interaction between the motion
capacity of the species and the geography of the Italian
Peninsula. The Central Mediterranean is a dispersal
barrier for this species, since short-toed snake eagles
avoid crossing large bodies of water during migration by
using soaring-gliding flight over land (Agostini et al.
2002a,b; Mellone et al. 2011; Panuccio et al. 2012). The
majority of birds breeding in Italy migrate to and from
Africa through the Strait of Gibraltar; in spring they
arrive in Italy about 1,000 km NW of southern regions
of the Peninsula via southern France. As suggested by
previous research (Agostini and Mellone 2008), the ac-
tual distribution in Italy may reflect the particular
migration path used by this population. Considering the
increasing number of breeding pairs and of the occupied
territories in central and southern Italy (Baghino and
Premuda 2007; Mellone et al. 2011), our results support
the hypothesis that short-toed snake eagles are still
colonizing the country moving from north to south of
the peninsula primarily along its western slope. How-
ever, we cannot exclude that the increasing number of
the short-toed snake eagle in Italy reflects a recovery
from a previous reduction of the population (i.e. con-
servationist effort, urbanization) but also in this case our
results indicate that the latitudinal gradient could ex-
plain the actual distribution of the species.
Does the distribution reflect the colonization process?
All the above considerations lead us to further
questions: from where is the short-toed snake eagle
Fig. 3 The probability of occurrence of short-toed snake eagles at
different latitudes in the two different models with (a) and without
(b) latitude variable
Author's personal copy
colonizing the Italian peninsula? What is the original
range distribution of short-toed snake eagle? These are
topics linked to the origin of the Palearctic-African
migration system and of migration itself. Most authors
agree that birds started to migrate from tropical to
temperate areas (Alerstam 1990; Rappole 1995; Safriel
1995; Berthold 2001; Rappole and Jones 2002;Bo
Gaese and Oberrath 2003; Jahn et al. 2004). According
to this hypothesis, migration is an adaptation of tropical
birds to use seasonally abundant resources in temperate
regions in order to optimize breeding success or to avoid
seasonal resource depression (Alerstam 1990; Rappole
1995; Rappole and Jones 2002; Alerstam et al. 2003).
Alerstam and Enckell (1979) indicate that competi-
tion in Africa savannas during the breeding season was
a prerequisite for the evolution of the Palearctic-Afri-
can migration system. Glaciations were also events of
paramount importance in the evolution of migrations.
During cold glacial phases, the earth surface available
for many bird species drastically decreased (Moreau
1972). Since the northern polar front shifted south,
temperate forests and bush vegetation were reduced;
furthermore the range extension of tundra, deserts and
steppes reduced the Mediterranean and the tropical
vegetation to a minimum (Hooghiemstra et al. 2006;
Bruderer and Salewski 2008). During interglacial
Fig. 4 Variation in probability occurrence of short-toed snake eagle predicted by BRT model (Ylatitude, ALTM mean altitude, NSP
number of reptile species, CVALT standard deviation of altitude, FOR2 square root forests, FOR forests, COLINT crops and orchards,
ARB shrubs, PRAPAS meadows and pastures, ED urbanized areas)
Fig. 5 Prediction surface of the decision tree realized combining
the two main predictor variables of the model: mean altitude
(ALTM) and the prey species richness (NSP)
Author's personal copy
periods, including the current one, ancestral species
diverged into what are known as ‘‘twin’’ species, dis-
tinctly sedentary, partially migrants and completely
migrants (Berthold 2001; Rappole, 2005). Rappole and
Jones (2002) provide evidence that most species that
currently migrate descended from tropical residents.
For the Palearctic-African migration system, 42 of 185
species of migrants (23 %) have conspecific populations
that breed in the Tropics while 139 (75 %) have
Tropical-breeding congeners (Rappole and Jones 2002).
Of the snake eagles (Circaetus spp.), only the short-
toed snake eagle is a complete migrant while the other
five species (Beaudouin’s snake eagle, C. beaudouini,
black-chested snake eagle, C. pectoralis, brown snake
eagle, C. cinereus, east African snake eagle, C. fasciol-
atus, banded snake eagle, C. cinerascens) live in tropical
Africa and are mainly resident (Ferguson-Lees and
Christie 2001). However, it is hard to generalize a
model like the southern-home theory since birds con-
tinuously adapt their migratory behavior according to
changes in resource availability (Bruderer and Salewski
2008). In fact, the current migratory system began
evolving about 15,000 years ago at the end of the last
glaciation and is still evolving; the consequence of this
process is not fully predictable (Berthold 2001). Rap-
pole and Jones (2002) proposed a mechanism for the
evolution of long distance migration, via gradual col-
onization at the edge of the breeding range furthest
from the wintering area, with populations on the edges
more exposed to extinction risk. Consistently with this
hypothesis, we suggest that the Italian population of
the short-toed snake eagles should be considered as
part of a metapopulation comprising those of Western
Europe (France, Spain). Small and isolated populations
of southern Italy, despite the increasing number, could
be considered as small patches of this metapopulation
system cut off from the bulk of the population of
Western Europe. As a matter of fact, distribution and
abundance of migrants could be influenced by the cost
of reaching areas located far away from the main
migratory pathways (Henningsson and Alerstam 2005a,
b; Tellerı
´a et al. 2009) and several studies show that
isolation could lead small and periphery patches to
local extinction (Lomolino et al. 1989; Peltonen and
Hanski 1991; Hanski et al. 1995; Whitcomb et al. 1996;
Smith and Gilpin 1997; Thomas and Hanski 1997;
Hanski 1998; Dunham and Rieman 1999; Clinchy et al.
2002; Wahlberg et al. 2002). In support of this
hypothesis, historical data confirm that the short-toed
snake eagle was breeding in areas of southern conti-
nental Italy and Sicily at least until the end of the 19th
century (Salvadori 1872; Lucifero 1898; Arrigoni degli
Oddi 1929) while current data show that it is no longer
found in those areas. Its failure to re-colonize the
southernmost areas of Italy may, therefore, be due to
the distance from the center of its current metapopu-
lation range. In this scenario, we predict that this trend
will lead to increasing occupancy in the future in
southern Italy but, being at the edge of population
distribution, it is likely that density remains lower than
in Northwestern Italy, despite the availability of suit-
able areas for this species.
The direction of migration is the result of natural
selection; for this reason it is likely that only migration
routes leading to survival areas and avoiding ecological
barriers are favored by natural selection through an
increasing of survival rates and fitness. Therefore, it is
expected that migratory populations may follow their
historical expansion route (Salewski and Bruderer 2007),
and the main migration flyways of short-toed snake
eagles breeding in Europe may restrict accessibility to
and colonization of other potential breeding regions
(Henningsson and Alerstam 2005a,b). The southerly
direction of colonization of Italy performed by short-
toed snake eagle suggests that birds facing a natural
barrier show behavioural plasticity leading to unex-
pected migratory and colonization directions.
Acknowledgments We wish to thank Massimo Campora, Guido
Cattaneo, Ugo Mellone and Paolo Forconi for their help in pro-
viding data of short-toed snake eagles presence and the Societas
Herpetologica Italica (SHI) for allowing to use the data of prey
species richness. We are grateful to Simona Tarantino for her
assistance in setting out the figures. We appreciate the improve-
ments in English usage made by Christina Riehl through the
Association of Field Ornithologists’ program of editorial assis-
tance. MEDRAPTORS ( is a network of
ornithologists that works to improve research and conservation of
migrating birds of prey.
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... As a result, we focused the analysis on this species. Since this eagle does not breed in the study area (Panuccio et al. 2015), our observations involved migrating birds. The median date of the passage of this species was on 26 September, and among aged eagles (N = 40) 33 (82.5%) were first calendar year (cy) birds. ...
... This would have led to the evolution of the extremely detoured path in birds breeding both in Italy and Greece, favored by the partial overlap in the migration periods of individuals belonging to different age classes (Agostini et al. 2002;Panuccio et al. 2012). Notably, nearly all short-toed snake eagles breeding in Italy cross the Mediterranean Sea at the Strait of Gibraltar during both spring and autumn, probably retracing the colonization process (Agostini & Mellone 2008;Panuccio et al. 2015). Most juveniles learn this flyway by following adults (see also Mellone et al. 2016), while some, migrating later in the season than older (experienced) birds, head southward passing along southern continental Italy and concentrating over the island of Marettimo (western Sicily; Figure 1) located 130 km NE of the Cap Bon promontory (Tunisia), and rarely also over Malta (Agostini et al. 2002;Sammut & Bonavia 2004;Mellone et al. 2016). ...
... In reference to birds passing over Malta, their reluctance to continue migrating over the water surface makes them more vulnerable to poaching, since they probably remain on the island longer than other migrating birds do (Del-Hoyo et al. 1994). In a recent paper, Panuccio et al. (2015) suggested that the Italian population of the shorttoed snake eagle should be considered part of a metapopulation comprising those in Western Europe (France, Spain). Small and peripheral populations of southern Italy could be considered small patches of this metapopulation system cut off from the bulk of the population of Western Europe (Panuccio et al. 2015). ...
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We investigated the directions of migration (reversed vs. expected) of raptors approaching a geographical strait in relation to local wind conditions, time of day, flock size and location of the observation post (coastal zone vs. inland zone). Fieldwork was conducted during autumn migration in 2011, 2012 and 2013 at a migratory bottle neck located in the southernmost part of the Italian Peninsula (Calabrian Apennines), using four watch points. In this area, migrating birds face the narrowest water surface between continental Italy and Sicily, the Strait of Messina. The only species showing substantial reverse migration was the short-toed snake eagle (Circaetus gallicus). In particular, eagles, mostly first cy birds, showed this behavior when passing closer to the coast (5 km inland of the Strait of Messina). Our results could reflect the reluctance of these birds to head south when approaching this relatively short stretch of sea, even before reaching the coastline. This behavior could be evidence of the strong selective pressure, which would have led to the evolution of the extremely detoured flight path of birds breeding in Italy.
... At the 25 km 2 scale, slope and elevation were highly correlated (r = -0.72); we chose to enter elevation in the models since it has been found to predict the presence of the short-toed snake eagle at a larger scale (Panuccio et al. 2015). The best models (ΔAIC < 2) for both spatial scales are shown in Table 1. ...
... The highlight of this study is the strong relationship between snake species richness and the occurrence of breeding short-toed snake eagles at both spatial scales (1 and 25 km 2 ). The same link was found in other Mediterranean environments, such as southeastern Spain and across Italy, but at a much larger scale (100 km 2 ; Moreno-Rueda & Pizarro 2007;Panuccio et al. 2015). The result that prey species richness can explain nest-site selection at a very fine scale (1 km 2 ) suggests that optimal breeding sites are placed as close as possible to hunting areas, as has previously been shown for another raptor species, the red kite (Milvus milvus, Pfeiffer & Meyburg 2015). ...
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Birds of prey, as top predators, play a key role in ecosystem functioning by regulating prey populations and, by means of cascade effects, promoting biodiversity. This makes them adequate sentinels of ecosystem health. Here we analyse the relationship between the occurrence of breeding short-toed snake eagle (Circaetus gallicus) and both the richness of potential prey species and landscape characteristics by taking into account two different spatial scales (i.e. nest-site scale and landscape scale). The short-toed snake eagle offers an interesting case study for investigating the relationships between top predators, prey diversity, and habitats, because it is an extremely specialised raptor that feeds on mesopredators, mostly snakes. Additionally, short-toed snake eagles are mainly threatened by changes in agriculture and land use in Europe, which have reduced the extent of suitable hunting habitats, and by the decrease in snake populations. Our study was conducted in the Latium Region (central Italy) in 2007, where most of the Italian breeding population is concentrated. By means of habitat selection analyses using generalised linear models, our results showed that the species selected breeding areas characterised by low elevations, rugged slopes, and high snake species richness at the nest-site scale (1 km²). At the landscape scale (25 km²), the best model showed that birds selected areas characterised by lower elevations for nesting, with a tendency towards intermediate values of wood cover and high snake species richness. Our study highlights the strong relationship between snake species richness and the occurrence of breeding eagles at both spatial scales, with optimal breeding sites located closer to hunting areas than expected by chance. This study provides further support for the role of short-toed snake eagles as sentinel species for Mediterranean habitats, and highlights the link between the location of nesting sites and the occurrence of human-modified landscapes characterised by high prey richness.
... This comparison among the three species highlights how the response to a major obstacle like the sea crossing is species-specific and depends mainly upon wing morphology (Agostini, Panuccio, & Pasquaretta, 2015). Such differences in motion capacity have profound effects also on the colonization patterns of these raptors: while the osprey is virtually cosmopolitan, the short-toed eagle is absent from large Mediterranean islands, perhaps because its colonization pathways are much more constrained by the distribution of land masses (Panuccio, Lucia, Agostini, Ottonello, & Bogliani, 2015). ...
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In focus: Santos, C. D., Silva, J. P., Muñoz, A.-R., Onrubia, A., & Wikelski, M. (2020). The gateway to Africa: What determines sea crossing performance of a migratory soaring bird at the strait of Gibraltar? Journal of Animal Ecology, 89, 1317-1328. Migrating birds undertake long journeys which pose several challenges. Water bodies are the most demanding ecological barriers for soaring birds, due to the increase in energy consumption and mortality risk. Through high-resolution GPS, Santos et al. (2020), analysed how the flight performance of 73 black kites crossing the Strait of Gibraltar was affected by external (e.g. weather conditions) and internal factors (individual experience). Kites waited for weaker crosswinds to start the crossing to minimize energy consumption, drift and altitude loss. Moreover, adults were quicker and lost less altitude than juveniles. These processes are likely to occur in all soaring species and have consequences also at a much wider spatial scale. In the Mediterranean region, species- and population-specific migration strategies appear to be influenced by interactions between species' morphology and the distribution of the land masses they traverse.
... In other words, coexistence requires some form of niche difference or partitioning where species' niche consists of four major axes: resources, natural enemies, space and time (Chesson 2000). It has been recently pointed out that, in order to understand mechanisms of species distribution patterns, it is essential to account not only for classical ecological features but also for the movement and dispersal ability of an organism, defined as a change in spatial location in time (Nathan et al. 2008, Cumming et al. 2012, Panuccio et al. 2015. All of these processes interact in shaping the structure and dynamics of populations, communities and ecosystems. ...
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... Only 34 species schemes were run on an international geographical scale. These involved two programmes monitoring only non-breeding populations: 'Mission Migration' from France including 32 species schemes; Short-toed Snake Eagle Circaetus gallicus satellite tracking from Italy (Panuccio et al. 2015); and one programme monitoring breeding populations of Redfooted Falcon Falco vespertinus based in Hungary (Solt et al. 2010 ...
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Capsule: Territory monitoring using playback of calls is a reliable approach for assessing population trends of Tawny Owls Strix aluco, particularly when human resources are limited or survey areas are difficult to access. Aims: To explore whether response calls of Tawny Owls towards broadcast conspecific and heterospecific male owl playback calls would provide similar estimates of population size and trends over time as nest-box monitoring. Methods: Between 1998 and 2017, Tawny Owls were monitored in a predominantly forested area of central Slovenia. Throughout the year, territories were monitored using a playback protocol comprising silent listening during five minutes before and after ten minutes of broadcasting male Tawny Owl. Seasonal variation in response rate was examined and results from the playback method were compared to data on occupancy rate of nest-boxes. Results: Territory monitoring using playback calls showed a similar direction of population trends as nest-box monitoring but a different population dynamics pattern. The overall response rate in occupied territories to conspecific playback calls at first visits was 70%. This was significantly higher than for heterospecific playback calls and the frequency of spontaneous vocalizations. The response rate to conspecific playback calls when including two visits rose to nearly 90%. There was no difference in response rate between seasons. The average time to respond to conspecific playback calls was five minutes. Conclusions: Compared to nest-box monitoring of breeding pairs, territory monitoring of breeding and non-breeding Tawny Owls using playback provides a robust and cost-effective method for monitoring. We recommend conducting territory monitoring between January and May during the breeding season, with two visits to each site using conspecific playback of territorial male hoot calls using the 5 + 10 + 5 minutes protocol.
... Only 34 species schemes were run on an international geographical scale. These involved two programmes monitoring only non-breeding populations: 'Mission Migration' from France including 32 species schemes; Short-toed Snake Eagle Circaetus gallicus satellite tracking from Italy (Panuccio et al. 2015); and one programme monitoring breeding populations of Redfooted Falcon Falco vespertinus based in Hungary (Solt et al. 2010 ...
Capsule: A questionnaire identified 1196 raptor monitoring species schemes within 236 monitoring programmes across 37 countries. Aims: To assess the level of monitoring of status/trends of raptors across Europe, to produce a web-based inventory of activities. Methods: A questionnaire promoted by voluntary national coordinators assessed monitoring coverage, focusing on breeding populations. Results: One thousand one hundred and ninety-six species schemes (236 monitoring programmes; 90% active in 2012) were reported from 37 countries. Sixty per cent of schemes were of over 10 years duration and nine countries ran schemes of over 40 years duration. Nineteen species had at least one scheme in 10 or more countries, and 15 species had schemes that ran for over 10 years. Thirteen species had breeding monitoring schemes in over 50% of countries where they breed, including widespread species (e.g. Peregrine Falcon Falco peregrinus) and localized species (e.g. Rough-legged Buzzard Buteo lagopus). Lanner Falcon Falco biarmicus, Levant Sparrowhawk Accipiter brevipes and Booted Eagle Hieraaetus pennatus had the least representative coverage, and four rare species had no coverage. Coverage was more representative in north and west Europe than further south and east. Coverage was more representative for widespread species and those with more favourable conservation status. Conclusions: Large potential exists to enhance reporting on status/trends, ecotoxicology analyses and volunteer-based monitoring at the pan-European scale. National coordinators provide an ideal network to develop and disseminate best practice guidance across Europe.
... L'areale dell'Italia centromeridionale del Nibbio bruno è frammentato e localizzato principalmente lungo la fascia tirrenica dell'Italia centrale e in alcune province dell'Italia meridionale (Basilicata), altrove, la specie è estremamente localizzata e nidificante con pochissime coppie (Nardelli et al. 2015). Probabilmente, analogamente ad altre specie di rapaci migratori (Panuccio et al. 2015), le coppie di Nibbio bruno nidificanti nell'Italia peninsulare rappresentano una sub-popolazione di un sistema di meta-popolazione che hai il suo centro nell'Europa (Whitcomb et al. 1996, Hanski 1998. Nel complesso quindi la necessità di monitorare ed operare interventi per la conservazione di questa specie non deriva unicamente dal fatto che il Nibbio bruno è specie inserita nella Direttiva "Uccelli" 79/409/CEE, ma anche perché si registra un forte declino di alcune colonie storiche del Lazio (Aradis et al. 2008, Calvario et al. 2008, De Giacomo et al. 2015) e perché si tratta di una popolazione vicina al margine dell'areale. ...
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Capsule: Juvenile Short-toed Snake Eagles Circaetus gallicus hatching in the peripheral populations of Greece and Italy have limited opportunities for social learning of migration routes compared to those hatched elsewhere. Aims: To test the prediction that there would be a higher degree of migration synchrony between adult and juvenile Short-toed Snake Eagles originating from peripheral populations and using an extremely detoured flyway, when compared to other populations using a direct overland flyway. Methods: We use linear regression models to compare seasonal changes in the age distribution of migrating Short-toed Snake Eagles counted at two migration watch-sites in Italy (Arenzano) and Georgia (Batumi), along a detoured and a direct flyway, respectively. Results: Juveniles migrated a fewdays later thanadults at both sites and the age ratios recorded at these two sites was similar. The daily proportion of juveniles increased along a similar slope during the migration season, thus showing a similar degree of synchrony between the age classes on both flyways. Conclusions: Contrary to our hypothesis, juvenile and adult migration is not more synchronized in peripheral populations using a detoured flyway compared to a core population using a direct migration flyway. Our results suggest that juveniles do not learn detours to complete transMediterranean migration from their parents, but from other elders.
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Migrating juvenile birds rely on endogenous information in choosing the direction in which to fly, but such input may be over-ridden by social interactions with experienced individuals. We tagged seven juvenile Short-toed Eagles Circaetus gallicus with GPS transmitters in southern Italy. This trans-Saharan migrant flies mainly by soaring and is therefore not well adapted to performing long water crossings. Five of the seven tagged juveniles used the longer but apparently safer route towards the Strait of Gibraltar, while two migrated along a southerly trajectory and subsequently spent the winter in Sicily, apparently forced to do so by the 150-km wide Sicily Channel. One of these individuals took the longer route the following autumn. These results, combined with long-term (15 years) visual field observations involving thousands of individuals, suggest that inexperienced Short-toed Eagles may learn their migratory routes from experienced adults, while some of them migrate south in response to an innate orientation instinct. Transport costs, inherited information and geography apparently interact, forcing some Short-toed Eagles to winter 3000 km to the north of the majority of their conspecifics. This article is protected by copyright. All rights reserved.
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Abstract – New data on the circuitous spring migration of short-toed eagle Circaetus gallicus in Italy. The spring migration of the short-toed eagle Circaetus gallicus was studied from 6th to 21st March 2004-2006 at two coastal sites in northwestern Italy, Arenzano (Liguria) and Capriglia (Tuscany). During this 3-years period, 3007 and 2481 short-toed eagles were recorded at Arenzano and Capriglia, respectively, confirming these sites as the major “hotspots” for this species during spring migration over Italy. All the birds observed at Arenzano were migrating towards east-northeast, while at Capriglia towards the southeast. Counts at the two sites were positively correlated. These observations confirm that, during spring migration, short-toed eagles breeding in central Italy (and probably in southern Italy as well) perform a “circuitous migration” from the northwest along the Ligurian coast, moving south through the Italian peninsula. Thus, during northward migration, they seem to avoid crossing the Sicilian Channel, in order to minimize the energy expenditure and risks of the sea crossing.
Conference Paper
The apparent nomadism of Palearctic migrant birds during the wintering period in Afrotropical savannah resulted in their characterisation as wandering interlopers, subordinate to Tropical residents, forced to subsist on temporary resource concentrations in marginal habitats. These ideas persist, and, indeed, provide the theoretical basis for many modern studies of migrant evolution. However, recent studies have established that migrant ecology is more complex, with many migrants using stable resources and demonstrating site fidelity to a broad range of Tropical habitats, both within and between wintering seasons. Furthermore, intra-Tropical movements are now known to occur in a number of Tropical resident species as well as migrants, and appear related to resource and habitat seasonality. These findings, plus extensive taxonomic evidence, indicate that most long-distance migrants to temperate and boreal breeding sites are derived from Tropical-breeding resident birds, emphasising the critical importance of taking into account selective factors and evolution occurring during the non-breeding portion of the life cycle. The three principal Holarctic migration systems are similar in these and many other aspects, but differ in that, while roughly one third of the Nearctic/Neotropical and eastern Palearctic/Asian Tropical migrants winter in forest, almost none of European/Afrotropical migrants do so. We propose that habitats connecting Holarctic and Tropical regions serve as a filter for potential migrants to the Holarctic, and that absence of forest from northern Africa has limited exploitation of European forests by Afrotropical species.
In Rappole & Jones (2002), a hypothesis was presented explaining how migration between temperate and tropical regions could have evolved from normal dispersal of tropical-breeding resident birds, citing taxonomic, ecological, biogeographic, physiological, and behavioral evidence in support of the theory. In addition, contrasts were made between Old and New World migration systems, e.g., the relative absence of long-distance migrants from European forests, and an explanation was provided for how these differences could have developed given a tropical origin for most temperate migrants. Bell (2005 - this issue) has presented a detailed critique of this hypothesis in which he dismisses much of the reasoning and evidence for the theory, and proposes an alternative "northern home" theory in which migration derives from gradual genetic change in dispersal direction and distance favored by an environmental gradient, presumably climatic deterioration on temperate, breeding grounds. Herein a response is provided to Bell's critique, clarifying our arguments where they appear to have been misunderstood, and providing additional information in support of ideas on tropical origin for many migratory bird species.
This chapter presents the results of a long-term study of a metapopulation that appears ideal with regard to the measurement of parameters of a metapopulation. The metapopulation is large, relative to lifetime movements of the animals. Not all patches have been occupied in any census period. Both numerous extinctions and recolonizations have been recorded over the 20 plus years of observation of the metapopulation. The study organism is the American pika (Ochotona princeps), a small (132 g) alpine lagomorph, and the study site is the abandoned gold-mining area of Bodie, Mono County, California. A spatially explicit model is introduced that successfully integrates patch-specific population growth with these size and distance effects for the Bodie pika metapopulation. The results of the study suggest need for metapopulation models to incorporate explicit spatial dimensions and to examine a range of spatial and temporal scales in their analyses.
This is the first study reporting patterns of island occupancy in a guild of mammals with detailed information on the processes affecting these patterns: dispersal, colonization, and extinction. We surveyed the presence of three species of shrews, Sorex araneus, S. caecutiens, and S. minutus, on 108 islands in three lakes in Finland. A significant compensatory effect between island area and isolation was detected in one species, but most islands were so little isolated (< 1 km) that isolation played no great role in this study. The position and the slope of the incidence function varied greatly among the species. Fitting the model J = 1/(1 / y/A^x) to the observed incidence functions, and assuming that the annual extinction probability is 1 on islands of A = 0.5 ha, yielded quantitative predictions of the rates of colonization and extinction in the three species. Observed rates agreed remarkably well with the predicted ones (median difference 20%). Overwater dispersal rate and/or ability was lowest in the smallest species (S. minutus), probably because of its short starvation time and slow swimming rate. Unexpectedly, this species had the highest colonization ability (rate of successful colonization conditional on arriving at an island). There were no significant differences between the species in colonization rate, but interspecific differences in extinction rate were highly significant and negatively correlated with body size. We suggest that these differences are due to increasing importance of environmental stochasticity with decreasing body size in shrews. This hypothesis is supported by larger coefficients of variation of abundance in small than in large species on the mainland.