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Original article
Sexual differences in microhabitat selection of breeding
little bustards Tetrax tetrax: Ecological segregation
based on vegetation structure
M.B. Morales*, J. Traba, E. Carriles, M.P. Delgado, E.L. Garca de la Morena
Terrestrial Ecology Group (TEG), Departamento de Ecologa, Facultad de Ciencias, Universidad Autonoma de Madrid,
c/ Darwin 2, 28049 Madrid, Spain
a r t i c l e i n f o
Article history:
Received 19 November 2007
Accepted 26 June 2008
Published online 15 August 2008
Keywords:
Agriculture intensication
Ecological constraints
Farmland birds
Niche segregation
Steppe birds
a b s t r a c t
We examined sexual differences in patterns of vegetation structure selection in the sexu-
ally dimorphic little bustard. Differences in vegetation structure between male, female and
non-used locations during reproduction were examined and used to build a presence/
absence model for each sex. Ten variables were measured in each location, extracting
two PCA factors (PC1: a visibility-shelter gradient; PC2: a gradient in food availability)
used as response variables in GLM explanatory models. Both factors signicantly differed
between female, male and control locations. Neither study site nor phenology was signif-
icant. Logistic regression was used to model male and female presence/absence. Female
presence was positively associated to cover of ground by vegetation litter, as well as overall
vegetation cover, and negatively to vegetation density over 30 cm above ground. Male pres-
ence was positively related to litter cover and short vegetation and negatively to vegetation
density over 30 cm above ground. Models showed good global performance and robustness.
Female microhabitat selection and distribution seems to be related to the balance between
shelter and visibility for surveillance. Male microhabitat selection would be related mainly
to the need of conspicuousness for courtship. Accessibility to food resources seems to be
equally important for both sexes. Differences suggest ecological sexual segregation result-
ing from different ecological constraints. These are the rst detailed results on vegetation
structure selection in both male and female little bustards, and are useful in designing
management measures addressing vegetation structure irrespective of landscape compo-
sition. Similar microhabitat approaches can be applied to manage the habitat of many
declining farmland birds.
2008 Elsevier Masson SAS. All rights reserved.
1. Introduction
Extensive cereal farmland holds the main populations of
endangered grassland birds in Europe (Bureld, 2005), most
of which are considered of conservation priority (Birdlife
International, 2004; Bureld, 2005). The main cause of their
decline is agriculture intensication (Sanderson et al., 2005;
Santos and Sua rez, 2005), which tends to produce changes in
* Corresponding author. Tel.: 34 91 497 8005; fax: 34 91 497 8000.
E-mail address: manuel.morales@uam.es (M.B. Morales).
avai l abl e at www. sci encedi r ect . com
j our nal homepage: www. el sevi er . com/ l ocat e/ act oec
1146-609X/$ see front matter 2008 Elsevier Masson SAS. All rights reserved.
doi:10.1016/j.actao.2008.06.009
a c t a o e c o l og i c a 3 4 ( 2 0 0 8 ) 3 4 5 3 5 3
Author's personal copy
habitat structure at different spatial scales (Morales et al.,
2005a; Sanderson et al., 2005; Wolff, 2005). A main effect of
agriculture intensication is the change of vegetation struc-
ture at small spatial scales (Donald and Vickery, 2000; Sander-
son et al., 2005; Wilson et al., 2005) which has been shown to
inuence habitat choice, local abundance and breeding
success of birds, since they are related to the suitability and
availability of critical resources such as food, shelter, access
to mates, etc. (Rotenberry and Wiens, 1980; Donald and Vick-
ery, 2000; Wolff et al., 2001; Whittingham and Evans, 2004;
Devereux et al., 2006). Consequently, determining the vegeta-
tion structure or microhabitat (cover, spatial architecture)
preferred by breeding farmland birds is a key conservation
requirement.
The little bustard Tetrax tetrax is a Palaearctic steppe bird
suffering strong population and range reductions (Goriup,
1994; Del Hoyo et al., 1996). It is classied as Near Threat-
ened at global scale (Goriup, 1994) and Vulnerable (Birdlife
International, 2004) in Europe. Seventy to eighty per cent of
the European population is concentrated in Spain (Garc a de
la Morena et al., 2004). The main habitat of the little bustard
in western Europe is extensive cereal farmland, although it
can also be found in natural steppe and extensive pastureland
(Cramp and Simmons, 1980; Mart nez, 1994; Salamolard and
Moreau, 1999; Wolff et al., 2001; Morales et al., 2005a).
The little bustard is a sexually dimorphic species (females
are cryptic and weigh 700900 g, while breeding males present
strong black and white contrast in neck plumage, and bright
white ventral plumage, weighing 8001000 g, Cramp and Sim-
mons, 1980) breeding in exploded leks (Jiguet et al., 2000), and
in which males and females are subjected to different
ecological constraints. For example, breeding males seek
conspicuousness in sexual display, while females pursue
concealment to avoid predators and sexual harrassment
(Cramp and Simmons, 1980; Jiguet, 2001). Therefore the little
bustard is an adequate model to examine how different
ecological constraints associated with sex may be reected
in the respective use of vegetation structure, and how that
can be accounted for in predictive distribution models with
relevance to habitat management. However, and in spite of
the important research effort devoted to this species habitat
selection at landscape and substrate scales, only a few studies
have considered the role of vegetation structure (mainly
height and cover) in habitat choice by breeding little bustards
(Martnez, 1998; Moreira, 1999; Wolff et al., 2001). Moreover,
and due to the extremely secretive behaviour of females
during the breeding season, these studies are focused mainly
on males, so that habitat use and selection studies of little
bustard females are generally scarce and limited, and
completely lacking at a microhabitat scale (Morales et al.,
2006).
Here we analyse the differences in vegetation complexity
and microhabitat in two study areas between sites used by
little bustard males, sites used by little bustard females and
unoccupied sites during the breeding season. We test the
following predictions: (i) the microhabitat structure selected
by males and females should differ according to their behav-
ioural and ecological particularities, (ii) if selection of vegeta-
tion structure by breeding little bustards is based on
constraints related to their reproductive ecology, birds should
tend to select similar microhabitat features in both study
areas, and (iii) the presence of male and female birds can be
predicted on the basis of vegetation structure or microhabitat
variables. To evaluate these predictions we used two different
and complementary approaches. First, we elaborated an
explanatory model using GLM analysis and then we tried to
predict the presence or absence of male and female little
bustards by means of logistic regression.
2. Materials and methods
2.1. Study sites
Our study was carried out in two localities of central Spain
(Fig. 1). Both are at or slightly undulated areas dominated
by extensive cereal cultures and a varying fallow cover, with
an average precipitation of 500 mm/year. In Valdetorres del
Jarama (40

40
0
N, 3

25
0
W, 700 m a.s.l., 1500 ha) cereal-sown
elds, ploughs and short fallows younger than 2 years (here-
after simply fallows) occupy 80% of the land, the remaining
corresponding to long-term fallows, vetch and, marginally,
vineyards and shrubs. Mean eld size is 1.68 ha (S.D. 3.50).
In Campo Real (40

19
0
N, 3

18
0
W, 800 m a.s.l., 1600 ha) the
proportion of surface occupied by substrates other than cereal
cultures, ploughs and fallows is slightly larger (28%). Among
these, vetch, short shrubs and vineyards show the greatest
covers (18% in total). Mean eld size is 1.09 ha (S.D. 1.49).
These landscape differences between study sites were highly
statistically signicant (Student t-test for mean eld size:
t 4.75, df 1830, P < 0.0001; Chi-square test for crop type
composition: c
2
55.56, df 15, P < 0.001). Consequently,
Campo Real is dominated by an overall more mosaic-like
and diversied landscape than Valdetorres, which is indica-
tive of less intensied agricultural practices (On ate et al.,
2000).
2.2. Bird surveys
Fieldwork was carried out between April 15 and June 15, 2005,
which encompass the peak of male sexual display and most of
the laying and incubating periods of little bustard in central
Iberia (Cramp and Simmons, 1980; Martnez, 1994). We used
two different survey methods to obtain little bustard records.
One method was particularly appropriate to census breeding
males, and consisted of car routes using the existing rural
track and road network, which is quite dense in both areas,
and completely covering each site, along which survey points
separated by 500 m were established. In order to assure a full
cover of the study areas in a single bustard activity period (for
example, in a single morning), each site was surveyed by two
car-teams, each covering a half of the territory. Observation
time at each point was 10 min, during which all little bustard
males detected within telescope reach were recorded. Males
detected acoustically were searched for by telescope in order
to determine their actual position, so that virtually all active
males present were nally detected visually. After each
survey, we compared the observations made by each car-
team in order to eliminate possible double counts. Routes
were exactly repeated every 2 weeks over the breeding season
a c t a oe c ol o g i c a 3 4 ( 2 0 0 8 ) 3 4 5 3 5 3 346
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at both study sites, which guaranteed uniformity of survey
effort between censuses and sites. 2060 telescopes and
1040binoculars were used in all surveys. This survey proce-
dure is an adaptation to the species of the mapping method
(Bibby et al., 2000) and is frequently used in little bustard
studies (e.g. Salamolard and Moreau, 1999; Wolff et al., 2001;
Traba et al., 2008). Males were mapped on geo-referenced
digital cartography under ESRI Arc-Pad software, a SIG appli-
cation for hand-held devices or PDAs, which were provided
with a GPS receiver, so that our exact position relative to
that of recorded males was always known. The digital cartog-
raphy used included an orthorectied aerial image of each site
and an updated layer of parcel limits plus agrarian substrate
composition. These tools allowed minimizing mapping errors
and a correct assignment of the point in which the bird was
observed. We carried out ve of such censuses between April
1 and May 31, 2005, but only the one corresponding to the
display activity peak was used to select sampling points (see
below). The ve censuses were used to control for the
constancy of male locations and assured that the selected
ones effectively corresponded to male-used plots. Addition-
ally, we used these censuses to estimate male abundance
and density.
The second survey method was designed to obtain reliable
and unbiased female locations. We randomly determined
a number of 500 500 m squares in each study site. Habitat
composition (measured as relative proportion occupied by
each habitat type) within these squares did not differ as
compared to global habitat composition in any of the two
study sites (Valdetorres: c
2
11.94, df 7, P 0.1; Campo
Real: c
2
7.61, df 7, P 0.25). Female survey dates were
May 1112 for Valdetorres and May 1314 for Campo Real.
The number of random squares surveyed was 12 in Valde-
torres (300 ha, 20% of the total study area) and 11 in Campo
Real (275 ha, 17% of the total area). Each square was systemat-
ically surveyedby a walking teamof 46 experiencedobservers
separated by a 1020 m distance from each other, which
walked at a uniform speed a series of linear parallel transects
within the square. The constancy of between-surveyor
distance and walking speed guaranteed a fairly homogeneous
between-square survey effort. We carried out one female
survey per study site, taking a maximum of 2 days to
completely cover all squares in one site. This method maxi-
mizes the detection of female little bustard locations within
the square. Careful sexual differentiation was required each
time a female-like (female or juvenile male) individual was
detected. This was made on the basis of morphological traits
and behaviour (see also Jiguet and Wolff, 2000) by sufciently
experienced surveyors. Displacement of females was carefully
controlled and recordedondetailedmaps inorder to minimize
potential double counts. Female locations were digitally map-
ped following the same procedure described for males.
Fig. 1 Location of the two study areas within the Region of Madrid (Central Spain). Agrarian substrate composition and
500 3500 m squares randomly selected for female sampling are shown.
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2.3. Microhabitat sampling
In order to characterise microhabitat in male locations, vege-
tation structure was measured shortly after (within the
following 7 days) the survey corresponding to the maximum
number of males in each site (May 9 and 16 Valdetorres and
Campo Real, respectively), basically coinciding with the peak
of the sexual display period. Sampling male locations were
selected randomly among those that had remained continu-
ously occupied up to then as shown by previous the censuses,
so that all male sampling plots could be considered indepen-
dent male-occupied locations. To obtain microhabitat
measurements in female locations, we sampled all recorded
female locations in each survey. Randommicrohabitat control
locations were generated automatically after each survey over
geo-referenced cartography of each study area using ARCGIS
9.0. Random locations were produced using a 100 m exclusion
buffer around each bird location in order to minimize the
probability that little bustards were using those parts of the
territory. At each of these bird and random locations, ve
microhabitat sampling points were systematically dened:
a central point at the mapping or random UTM coordinates,
and four more points placed at 10 m N, S, E and W from the
central coordinate. Ten vegetation structure variables
describing cover and architecture (Rotenberry and Wiens,
1980) were measured at each sampling point (Table 1). The
total number of locations sampled was 78 (24 males, 14
females, and 40 random) at Valdetorres, and 58 (14 males, 19
female, and 25 random) at Campo Real. The type of agrarian
substrate corresponding to each location was also recorded.
2.4. Statistical analyses
A Principal Component Analysis (PCA) using vegetation struc-
ture variables was conducted to determine independent vari-
ables measuring little bustard microhabitat features.
Continuous variables were log-transformed, while cover
percentages were arcsine transformed. This approach was
chosen mainly for two reasons. First, all the ten original vari-
ables were highly inter-correlated, as shown by pair-wise
correlation analyses (see below). Second, the resulting factors
can be easily interpreted as ecologically meaningful gradients
in microhabitat features such as shelter or food availability.
We assessed potential differences between agrarian substrate
types in each PCA factor by means of a General Linear Model
(GLM) analysis.
Analyses then proceeded in two steps. First, differences in
microhabitat features between male, female and random
locations were examined controlling for the effect of study
area by means of a GLM in which the independent PCA factors
were the response variables, and type of location and study
site were included as categorical factors. In order to control
for a potential effect of vegetation phenology, the number of
days passed since the rst day of the reproductive period
(set at April 1 for both study areas) until the sampling date
was introduced as a covariate in the model. We used Tukeys
post hoc test to look for signicant differences between GLM
factors.
Second, we used logistic binary regression to obtain predic-
tive models of male and female presence using the original
microhabitat measures as predictive variables and bird pres-
ence/absence as the response variable. In order to avoid
collinearity among the predictors we calculated pair-wise
Pearson correlations, excluding variables with coefcients
greater than 0.7 (Tabachnick and Fidell, 1996) from subse-
quent analyses. Models were built according to Akaikes Infor-
mation Criteria (AIC) which retains the most explanatory
variables providing the best relative t for the number of vari-
ables included (Akaike, 1974; Burnham and Anderson, 2002).
We built one model for females, and one for males in which
observations were pooled irrespective of locality under the
assumption that differences between study sites are irrele-
vant at a vegetation structure scale.
We assessed these models performance by testing their
goodness of t, accuracy, and robustness. Goodness of t
was evaluated by means of the HosmerLemeshow test,
which is a measure of the models calibration or the degree
of coincidence between predicted and observed probabilities
(Hosmer and Lemeshow, 2000). We evaluated the models
accuracy through the use of a ROC (Receiver Operator Charac-
teristic) plot, which graphs the proportion of true positives
(sensitivity) in relation to the proportion of false positives
(specicity) for a range of threshold values (Hanley and
McNeil, 1982). The area under the ROC curve (AUC) is a reliable
measure of overall model accuracy and commonly varies from
0.5 (random classication) to 1 (perfect discrimination). AUC
values over 0.8 indicate good or very good model performance
(Fielding and Bell, 1997; Manel et al., 2001). Finally, we tested
the models robustness by applying the method of variable
randomization by permutation described in Pellet et al.
(2004), which recalculates the explained variance of the tted
models with 1000 permutations of the binary response vari-
able. When explained variance is higher than the one
measured in 5% of the permutations, the model cannot be
considered robust because the observed explained variance
can be randomly obtained. In addition, we validated the
models on real data collected the following year (May 2006)
in a third study site (Camarma de Esteruelas, Madrid region,
ca. 15 km from Valdetorres de Jarama) from a small sample
of 13 males and 6 females (control samples were also 13 and
Table 1 Vegetation structure variables measured at
1 31 m sampling squares (total n [841)
Variable Code Mean S.D.
Bare ground cover
a
BGC 46.81 36.51
Litter cover
a
LC 24.39 35.00
Total vegetation cover
a
TVC 41.18 32.47
Green vegetation cover
a
GVC 51.15 44.94
Green weed cover
a
GWC 36.16 46.10
Number of contacts below 5 cm height
b
NC<5 1.17 1.40
Number of contacts from 5 to 10 cm height
b
NC510 0.83 1.15
Number of contacts from 10 to 30 cm height
b
NC1030 1.28 1.77
Number of contacts from over 30 cm height
b
NC>30 0.70 1.48
Total number of contacts
b
TNC 3.94 4.01
Maximum vegetation height MVH 24.47 26.10
a Percentage of ground within squares.
b Number of contacts of vegetation with a 0.5 cm diameter metal
rod.
a c t a oe c ol o g i c a 3 4 ( 2 0 0 8 ) 3 4 5 3 5 3 348
Author's personal copy
6, respectively). Analyses were made with STATISTICA6.0 and
SPSS 14.0 (SPSS inc., 2004). The permutation validation of
regression models was performed in S-plus 6.0. Unless other-
wise stated, all means are expressed as mean S.E. and
signicance levels set at P < 0.05.
3. Results
3.1. Abundance and density estimates
The highest little bustard abundances yielded by surveys were
29 males and 21 females in Valdetorres and 39 males and 21
females in Campo Real, which corresponds to 1.93 males/
km
2
and 1.4 females/km
2
, and 2.4 males/km
2
and 1.3
females/km
2
, respectively. Sex ratios resulting from these
gures are 0.72 females/male in Valdetorres and 0.54
females/male in Campo Real.
3.2. Microhabitat features of male and female locations
The PCA of vegetation structure extracted two components
accounting for 73.84% of variation (Table 2). Factor 1 (PC1)
was positively associated to Bare ground cover (BGC), and
negatively associated to average Total Vegetation Cover
(TVC), average Green Vegetation Cover (GVC), average Number
of Contacts below 5 cm height (NC<5), average Number of
Contacts from 5 to 10 cm height (NC510), and average
Number of Contacts from 10 to 30 cm height (NC1030), as
well as to average and variation coefcient of Total Number
of Contacts (TNC) and average Maximum Vegetation Height
MVH (all measures loaded heavily onto PC1: over 0.7 within-
factor correlation, P < 0.001). This factor opposes bare ground
to total vegetation cover and vegetation density at low height
from the ground, and thus may be interpreted as a visibility
shelter gradient. Factor 2 (PC2), was negatively associated to
average Litter Cover (LC) and average Green Weed Cover
(GWC), and positively to average Number of Contacts over
30 cm height (NC>30) and average MVH (again, these four
variables showed a within-factor correlation over 0.7,
P < 0.001). This factor opposes litter and green weed cover to
vegetation density high above ground, and may be interpreted
as a gradient in food (green weeds and ground arthropods;
Jiguet, 2002) availability. The value of both PC1 and PC2 varied
signicantly betweenagrariansubstrate types (GLM, F 25.33,
df 10, P < 0.001, see Fig. 2), which reects the existing differ-
ences in the above explained gradients between different
macrohabitats.
Both PCA factors showed signicant differences between
female, male and random locations (GLM, F 8.88, df 4,
P < 0.001, see Fig. 3), that is, vegetation structure differed
with location type, although the study site and the time
passed since the beginning of reproduction turned out not
to be signicant (GLM, F 0.60, df 2, P 0.55, and
F 0.56, df 2, P 0.57). No signicant interaction was
either found between location type and study sites (GLM,
F 2.00, df 4, P 0.095). PC1 varied signicantly between
female and random locations (Tukey post hoc test, P < 0.05)
although such differences were not found, however,
between random and male locations, or between male and
female locations (P > 0.05, in both cases). PC2 was signi-
cantly different between female and control locations, as
well as between the latter and male locations (Tukey post
hoc test, P < 0.05) although, again, no differences were found
between male and female locations. However, when a GLM
analysis of PCA factors was performed excluding control
locations, male and female locations turned out to differ
signicantly (GLM, F 5.30, df 2, P 0.007), mainly due to
signicant differences in PC1 in Campo Real (Tukey post
hoc test, P < 0.05).
3.3. Distribution models
The results of the logistic binary regression analyses of the
distribution of male and female little bustards, in relation to
vegetation structure variables are presented in Table 3. The
variables nally accepted in the female distribution model
were the TVC and LC, which were positively correlated to
Table 2 Results of the Principal Component Analysis
conducted to determine independent vegetation
structure variables featuring little bustard and random
locations. Asterisks correspond to loading values greater
than 0.7
Variable PC1 PC2
BGC 0.879* 0.267
LC 0.313 0.690
TVC 0.934* 0.010
GVC 0.689 0.260
GWC 0.423 0.702*
NC<5 0.854* 0.236
NC510 0.858* 0.018
NC1030 0.806* 0.342
NC>30 0.563 0.638
TNC 0.971* 0.158
MVH 0.714* 0.520
CV of TNC 0.739* 0.033
Eigenvalue 6.826 1.980
Explained variance (%) 56.88 16.50
-2
-1,5
-1
-0,5
0
0,5
1
1,5
2
fallow cereal wasteland plough pulses margins olives vines
PC1
PC2
Fig. 2 Differences in ACP factors (mean S.E.) describing
little bustard microhabitat gradients between agrarian
substrate types.
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female presence, and NC>30, which is negatively associated
to female locations. This model explained 38% (Nagelkerkes
R-square) of the observed variance in female locations. The
model for male distribution included LC and NC<5 as vari-
ables positively correlated to male presence, and NC>30 as
a negatively associated variable. The total variance in male
locations explained by this model was 36%.
Bothmodels showed good calibration and accuracy level as
indicated by the corresponding HosmerLemeshow test and
AUC values (Table 3). None of the 1000 permutations of the
response variables gave explained variance values higher
than those yielded by the tted models. Global performance
and robustness can thus be evaluated as quite good for both
distribution models. Model validation with the samples from
the third site yielded fairly good tness (HosmerLemeshow
test: males, c
2
0.76, df 6, P 0.99; females, c
2
0.0001,
df 7, P 0.99) and classication performance (males: 11
out of 13 males correctly classied, 12 out of 13 controls
correctly classied, 86% global classication performance;
females: 6 out of 6 correctly classied, no control misclassi-
cation, 100% correct classication).
4. Discussion
4.1. Population estimates
The abundance and population estimates obtained are consis-
tent with those yielded in other populations of the Madrid
region and the Spanish southern Plateau during the rst little
bustard National Census (Garc a de la Morena et al., 2006).
Additionally, the male-biased sex ratio pattern obtained in
both sites is similar to that obtained in other declining popu-
lations of the species (Morales et al., 2005b). This result reveals
the unbalanced state of the study populations (see also
Morales et al., 2008), whose improvement might benet from
a detailed knowledge of sex-specic habitat requirements.
4.2. Features of male and female little bustard
microhabitat selection and effects on substrate
level selection
Although previous works have already looked at the micro-
habitat selection of breeding little bustard males (Mart nez,
1998; Moreira, 1999), our results are the rst specically
relating vegetation structure selection by females and how it
differs with respect to selection by males, as well as the rst
attempt to predict male and female occurrence on the basis
of such microhabitat features. In this context, they contribute
to understanding sexual ecological segregation within species
in which the behaviour and ecological constraints of the two
sexes differ due to life history traits (mating system, parental
investment, dispersion; see, for example, Clutton-Brock et al.,
1982).
As already pointed out, the two main factors extracted by
the PCA of vegetation structure can be interpreted as two
different environmental gradients acting on little bustards at
a microhabitat scale, that is, irrespective of the particular
type of agrarian substrate in which locations are found. PC1
can be interpreted as a gradient ranging from highly visible
points, with no or very little vegetation cover, where little
bustards become fairly conspicuous, to sheltered locations
with high vegetation cover and spatial density at low to
medium heights, in which birds can search for concealment.
-0,8
-0,6
-0,4
-0,2
0
0,2
0,4
0,6
0,8
control females males
PC1
PC2
Fig. 3 Differences in ACP factors (mean S.E.) describing
little bustard microhabitat selection gradients between
control (c), female (f) and male (m) locations.
Table 3 Logistic regression models predicting female and male little bustard distribution on the basis of vegetation
structure variables. Notations b and AUC respectively indicate the variables estimates and the Area Under the ROC Curve
Variable b c
2
P Nagelkerkes R
2
HosmerLemeshow AUC
c
2
df P
FEMALES
TVC 0.02
LC 0.01 30.92 0.000 0.38 7.75 8 0.46 0.83
NC>30 1.79
Constant 2.20
MALES
LC 0.016
NC>30 1.480 31.584 0.000 0.36 4.88 8 0.77 0.81
NC<5 1.780
Constant 1.080
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On the other hand, PC2 would describe a gradient ranging
from areas with high availability of food resources such as
green weeds (locations with high green weed cover like
fallows), to areas of high and dense vegetation (mainly at
heights over 30 cm above ground) which seem less suitable
for feeding. Our results show that the different types of
agrarian substrates found in our study sites (and most cereal
pseudo-steppe landscapes in central Iberia) differ in relation
to such microhabitat features, as can be expected from their
different vegetation types, human use, physiography, etc.
According to this interpretation of PCA factors, the loca-
tions where either males or females were observed differed
from random points in visibility and availability of trophic
resources. Females tended to occur in more sheltered (high
PC1 values) locations than control points, that is, in locations
where vegetation cover and spatial density at low to medium
heights (up to 30 cm above ground) is higher than what can be
expected at random. In relation to PC2 (food availability
gradient) female locations also tended to present higher litter
and green weed cover than control points. Green weeds are
the majority component of adult little bustard diet (Jiguet,
2002) while agrarian substrates allowing a higher accumula-
tion of litter can be expected to hold greater arthropod abun-
dance (Clere and Bretagnolle, 2001), which is the main food
resource of little bustard chicks, and a qualitatively important
component of adult diet in the breeding season (Jiguet, 2002).
Therefore, our results suggest that the microhabitat selection
pattern shown by little bustard females is determined by two
main constraints: the need for shelter and anti-predator
surveillance, and the need for food.
On the contrary, the need for shelter does not seem to be
a relevant constraint for breeding males, as can be clearly
expected from their main activity during spring: sexual
display at leks, for which conspicuousness is often required
(Mart nez, 1998; see Cramp and Simmons, 1980 for a thorough
description). This conclusion is further supported by the
appearance of statistically signicant differences in PC1 (the
visibilityshelter gradient) between male and female locations
when random points are removed from the analysis. On the
other hand, male locations also tend to present a higher avail-
ability of potentially food-abundant substrates than random
locations (but not than female locations), which might be
related with two different aspects of their mating strategy.
First, the courtship activity of little bustard males, as in all lek-
king species, is highly energy-consuming (e.g. Badyaev et al.,
1998), so that male territories must contain enough food to
cope with those requirements (Traba et al., 2008). Second,
the little bustard mating system is an exploded or dispersed
lek one (Jiguet et al., 2000), which allows males to defend large
enough mating territories as to hold sufcient food resources
to be used by females when visiting them for mating, thus
potentially contributing to increase mating success (Jiguet
et al., 2000).
These microhabitat selection patterns remain constant
over the entire breeding season, as suggested by the lack of
a signicant effect related to phenology. On the other hand,
the lack of a signicant effect associated to the study site
supports our initial prediction that male and female little
bustards prefer a given range of variation in vegetation archi-
tecture irrespective of habitat composition of the landscape at
each study area. Howis this reected at the larger spatial scale
of agrarian substrate selection? Several studies have already
shown that the pattern of agrarian substrate selection by little
bustards may markedly vary between localities, depending on
each sites particular landscape composition and structure
(Mart nez, 1994; Salamolard and Moreau, 1999; Wolff et al.,
2001; Morales et al., 2005a; see a revision in Morales et al.,
2006). On the other hand, in the present paper we show that
there exist signicant differences between substrates in the
microhabitat gradients considered. By looking at Fig. 2,
however, it is possible to realize that there are several
substrate types whose ranges of vegetation structure roughly
coincide (cereals, wastelands, margins, and fallows for the
visibilityshelter gradient, or wastelands and fallows for the
food availability gradient), which are the habitat types more
frequently reported as selected by the species in the literature
(Morales et al., 2006). Our results suggest that the selection of
these substrates is based on their particular vegetation
structure.
4.3. Is there a microhabitat-based ecological segregation
of the sexes? Conservation implications
The logistic regression models were robust and accurate, pre-
dicting that male and female little bustards should be found at
locations differing in their respective vegetation structure, as
could be expected from GLM results. This ecological segrega-
tion of the sexes during the breeding season implies a certain
degree of intraspecic niche differentiation (Krebs, 1994;
Pianka, 1994), which would be based on the selection of vege-
tation structure traits. In the case of females, the model points
out to a balance between shelter (positive effect of overall
vegetation density) and visibility for anti-predator surveil-
lance (marked negative effect of vegetation density over
30 cm above ground), as a main determinant of female distri-
bution. The importance of these microhabitat features is
consistent with the high female mortality rates during
breeding known in this species (and most ground, open
habitat, nesting birds; Sua rez et al., 1993; Jolivet and Bretag-
nolle, 2002). The nal regression model of male distribution
included vegetation density at low height above ground as
the main factor positively associated to male presence, and
vegetation density at height over 30 cm as negatively associ-
ated with presence. The importance of these factors could
result from the males need of conspicuousness for sexual
display, although the selection of areas with dense low vege-
tation might also be favoured by the pressure for males to
defend food-rich substrates. Nevertheless, the inclusion of
littler cover both in the male and the female model supports
the importance of food availability for both sexes. These
results support our initial prediction on different ecological
constraints shaping male and female microhabitat selection.
Little bustards tend to select a given range of vegetation
structure as a result of a trade-off between different
constraints. As intensication of farming practices increases,
vegetation structure of cultures and grasslands becomes more
uniform (Donald and Vickery, 2000; Sandersson et al., 2005),
and thus the opportunities for species to properly respond to
ecological trade-offs are reduced (Wilson et al., 2005), along
with the efciency of individuals in critical survival-related
a c t a o e c o l og i c a 3 4 ( 2 0 0 8 ) 3 4 5 3 5 3 351
Author's personal copy
activities such as foraging and anti-predator defence (Whit-
tingham and Evans, 2004; Devereux et al., 2006). The strong
differences in both PCA factors between control plots and
both male and female locations (Fig. 3) indicate that the envi-
ronmental availability of microhabitat conditions that would
allow little bustards to properly respond to their respective
ecological trade-offs are reduced in both study areas regard-
less of macrohabitat composition. In this context, the regres-
sion models of male and female little bustard distribution
obtained may be useful in habitat management aimed at the
species conservation, since they allow action on precise
microhabitat variables, rather than to simply favour certain
agrarian substrates. For example, vegetation structure could
be adequately modied by different means (regulating the
timing of agricultural labours such as ploughing or pesticide
spraying, manipulating seed density, increasing or decreasing
grazing intensity, etc., see Whittingham et al., 2006) to favour
female anti-predator defence, and thus increase female
survival and breeding success, both of which have been
proved to be critical factors for population viability in this
species (Morales et al., 2005b). Finally, although similar
measures may be applied to favour male density and survival
(e.g., delaying fallow ploughing to favour areas providing both
short vegetation and litter), it should be emphasized that
detailed results on female microhabitat selection are pre-
sented for the rst time, which may help ll existing gaps in
habitat management and develop more balanced conserva-
tion strategies for the little bustard.
Acknowledgements
Thanks to all eld assistants, particularly to M.A. Sanza for
providing microhabitat measurements from Camarma.
J. Seoane helped us in the use of S-plus. Finally, we thank
two anonymous referees, whose comments have sensibly
improved the manuscript. This paper contributes to project
CGL2004-06147-C02-02 of the Spanish MEC as well as to the
REMEDINAL research network of the CAM.
r e f e r e n c e s
Akaike, H., 1974. A new look at the statistical model identication.
IEEE Trans. Autom. Control 19, 716723.
Badyaev, A.V., Etges, W.J., Faust, J.D., Martin, T.E., 1998. Fitness
correlates of spur length and spur asymmetry in male wild
turkeys. J. Anim. Ecol. 67, 845852.
BirdLife International, 2004. Birds in Europe II. BirdLife
International, Cambridge.
Bureld, I., 2005. The conservation status of steppic birds in
Europe. In: Bota, G., Morales, M.B., Man osa, S., Camprodon, J.
(Eds.), Ecology and Conservation of Steppe-land Birds. Lynx
Edicions, Barcelona, pp. 119140.
Burnham, K.P., Anderson, D.R., 2002. Model Selection and
Multimodel Inference: a Practice Information-Theoretic
Approach. Springer Verlag, New York.
Clere, E., Bretagnolle, V., 2001. Food availability for birds in
farmland habitats: biomass and diversity of arthropods by
pitfall trapping technique. Rev. E

col. (Terre et Vie). 56,

275297.
Clutton-Brock, T.H., Guinness, F.E., Albon, S.D., 1982. Red Deer.
Behaviour and Ecology of Two Sexes. Chicago University
Press, Chicago.
Cramp, S., Simmons, K.E.L. (Eds.), 1980, The Birds of the Western
Paleartic, Vol. II.. Oxford University Press, Oxford.
Handbook of the birds of the World. In: Del Hoyo, J., Elliott, A.,
Sargatal, J. (Eds.), Hoatzin to Auks, Vol. 3. Lynx Edicions,
Barcelona.
Devereux, C.L., Whittingham, M.J., Krebs, J.R., Fernandez-
Juricic, E., Vickery, J.A., 2006. What attracts birds to newly
mown pasture? Decoupling the action of mowing from the
provision of short swards. Ibis 148, 302306.
Donald, P.F., Vickery, J.A., 2000. The importance of cereal elds for
breeding and wintering Skylarks Alauda arvensis in the UK. In:
Aebischer, N.J., Evans, A.D., Grice, P.V., Vickery, J.A. (Eds.),
Ecology and Conservation of Lowland Farmland Birds. BOU,
Tring, UK, pp. 140150.
Fielding, A.H., Bell, J.F., 1997. A review of methods for the
assessment of prediction errors in conservation presence/
absence models. Environ. Conserv. 24, 3849.
Garca de la Morena, E.L., De Juana, E., Martnez, C., Morales, M.B.,
Sua rez, F., 2004. Siso n Comu n (Tetrax tetrax). In: Madron o, A.,
Gonza lez, C., Atienza, J.C. (Eds.), Libro Rojo de las Aves de
Espan a. SEO-BirdLife-MMA, Madrid, pp. 202207.
Garca de la Morena, E.L., Bota, G., Ponjoan, A., Morales, M.B.,
2006. El Siso n Comu n en Espan a. I Censo Nacional (2005). SEO-
BirdLife, Madrid.
Goriup, P., 1994. Little Bustard Tetrax tetrax. In: Tucker, G.M.,
Heath, M.F. (Eds.), Birds in Europe: their Conservation Status.
BirdLife International, Cambridge, pp. 236237.
Hanley, J.A., McNeil, B.J., 1982. Maximum attainable
discrimination and the utilization of radiologic examinations.
J. Chronic Diseases 35, 601611.
Hosmer, D.W., Lemeshow, S., 2000. Applied Logistic Regression.
John Wiley and Sons, New York.
Jiguet, F., 2001. Defense des Ressources, Choix du Partenaire et
Mecanismes de Formation des Leks chez lOutarde
Canepetie` re. PhD thesis, Universite de Paris 6, Paris.
Jiguet, F., 2002. Arthropods in diet of little bustard Tetrax tetrax
during the breeding season in western France. Bird Study 49,
105109.
Jiguet, F., Wolff, A., 2000. De terminer lage et le sexe des outardes
canepetie` res Tetrax tetrax a` lautomne. Ornithos 7, 3035.
Jiguet, F., Arroyo, B., Bretagnolle, V., 2000. Lek mating systems:
a case study in the Little Bustard Tetrax tetrax. Behav. Proc. 51,
6382.
Jolivet, C., Bretagnolle, V., 2002. Loutarde canepetie` re en France:
e volution re cente des populations, bilan des mesures de
sauvegarde et perspectives davenir. Alauda 70, 9396.
Krebs, C.J., 1994. Ecology: The Experimental Analysis of
Distribution and Abundance. Blackwell Science, Ltd, Harper
Collins, New York.
Manel, S., Williams, C.H., Ormerod, S.J., 2001. Evaluating
presenceabsence models in ecology: the need to account for
prevalence. J. Appl. Ecol. 38, 921931.
Martnez, C., 1994. Habitat selectionbythe Little BustardTetraxtetrax
in cultivated areas of central Spain. Biol. Conserv. 67, 125128.
Martnez, C., 1998. Seleccio n de microha bitat del siso n comu n
Tetrax tetrax durante la estacio nreproductora. Ardeola 45, 7376.
Morales, M.B., Garcia, J.T., Arroyo, B.E., 2005a. Can landscape
composition changes predict spatial and annual variation of
little bustard male abundance? Anim. Conserv. 8, 167174.
Morales, M.B., Bretagnolle, V., Arroyo, B.E., 2005b. Viability of the
endangered little bustard Tetrax tetrax population of western
France. Biodivers. Conserv. 14, 31353150.
Morales, M.B., Sua rez, F., Garca de la Morena, E.L., 2006. Reponses
des oiseaux de steppe aux differents niveaux de mise enculture
et dintensication du paysage agricole: une analyse
a c t a oe c ol o g i c a 3 4 ( 2 0 0 8 ) 3 4 5 3 5 3 352
Author's personal copy
comparative de leurs effets sur la densite de population et la
selection de lhabitat chez lOutarde Canepetie` re Tetrax tetrax et
lOutarde Barbue Otis tarda. Rev. E

col. (Terre et Vie). 61, 261269.

Morales, M.B., Garca de la Morela, E.L., Delgado, M.P., Traba, J.,
2008. Tendencia reciente y viabilidad futura de las poblaciones
de siso n comu n (Tetrax tetrax) en la Comunidad de Madrid.
Anuario Ornitolo gico de Madrid 11, 4055.
Moreira, F., 1999. Relationships between vegetation structure and
breeding bird densities in fallow cereal steppes of Castro
Verde, Portugal. Bird Study 46, 309318.
On ate, J.J., Andersen, E., Peco, B., Primdahl, J., 2000. Agri-
environmental schemes and the European agricultural
landscapes: the role of indicators as valuing tools for
evaluation. Landscape Ecol. 3, 271280.
Pianka, E.R., 1994. Evolutionary Ecology. Harper Collins, New York.
Pellet, J., Guisan, A., Perrin, N.A., 2004. Concentric analysis of the
impact of urbanization on the threatened European tree frog
in an agricultural landscape. Conserv. Biol. 18, 15991606.
Rotenberry, J.T., Wiens, J.A., 1980. Habitat structure, patchiness,
and avian communities in North American steppe vegetation:
a multivariate analysis. Ecology 61, 12281250.
Salamolard, M., Moreau, C., 1999. Habitat selection by Little
Bustard Tetrax tetrax in a cultivated area of France. Bird Study
46, 2533.
Sanderson, F.J., Donald, P.F., Bureld, I.J., 2005. Farmland birds in
Europe: from policy change to population decline and back
again. In: Bota, G., Morales, M.B., Man osa, S., Camprodon, J.
(Eds.), Ecology and Conservation of Steppe-land Birds. Lynx
Edicions, Barcelona, pp. 211236.
Santos, T., Sua rez, F., 2005. Biogeography and population trends
of Iberian steppe birds. In: Bota, G., Morales, M.B., Man osa, S.,
Camprodon, J. (Eds.), Ecology and Conservation of Steppe-land
Birds. Lynx Edicions, Barcelona, pp. 69102.
SPSS Inc., 2004. SPSS, 14.0. Apache Software Foundation, Chicago.
Sua rez, F., Yanes, M., Herranz, J., Manrique, J., 1993. Nature
reserves and the conservation of Iberian shrub-steppe
passerines: The paradox of nest predation. Biol. Conserv. 63,
7781.
Tabachnick, B., Fidell, L., 1996. Using Multivariate Statistics.
Harper Collins, New York.
Traba, J., Morales, M.B., Garca de la Morena, E.L., Delgado, M.P.,
2008. Selection of breeding territory by little bustard (Tetrax
tetrax) males in Central Spain: the role of arthropod
availability. Ecol. Res. 23, 615622.
Whittingham, M.J., Evans, K.L., 2004. The effects of habitat
structure on predation risk of birds in agricultural landscapes.
Ibis 146, 210220.
Whittingham, M.J., Devereux, C.L., Evans, A.D., Bradbury, R.B.,
2006. Altering perceived predation risk and food availability:
management prescriptions to benet farmland birds on
stubble elds. J. Appl. Ecol. 43, 640650.
Wilson, J.D., Whittingham, M.J., Bradbury, R.B., 2005. The
management of crop structure: a general approach to
reversing the impacts of agricultural intensication on birds?
Ibis 147, 453463.
Wolff, A., 2005. The conservation status of steppic birds in
Europe. In: Bota, G., Morales, M.B., Man osa, S., Camprodon, J.
(Eds.), Ecology and Conservation of Steppe-land Birds. Lynx
Edicions, Barcelona, pp. 141168.
Wolff, A., Paul, J.P., Martin, J.L., Bretagnolle, V., 2001. The benets
of extensive agriculture to birds: the case of the little bustard.
J. Appl. Ecol. 38, 963975.
a c t a o e c o l og i c a 3 4 ( 2 0 0 8 ) 3 4 5 3 5 3 353