Ecological Indicators 11 (2011) 353–361

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Ecological Indicators
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Original article

Monitoring urban environments on the basis of biological traits

Marie-Hélène Lizée a,b,∗ , Jean-François Mauffrey a , Thierry Tatoni b , Magali Deschamps-Cottin a
a
Laboratoire Population Environnement Développement, UMR 151, Université de Provence, 3 place Victor Hugo, 13331 Marseille Cedex 03, France
b
Institut Méditerranéen d’Ecologie et de Paléoécologie, UMR 6116, Faculté des Sciences St Jérôme, 13397 Marseille Cedex 20, France

a r t i c l e i n f o a b s t r a c t

Article history: Urbanization induces changes in species abundance and richness that are beginning to be extensively
Received 5 February 2010 described. However, the functional structure of urban communities still requires attention to provide a
Received in revised form 11 May 2010 basis for a more accurate understanding of urban ecosystems’ functioning. This study has been performed
Accepted 4 June 2010
in order to assess functional changes in ecological communities related to changes of urban landscape
features along an urbanization gradient. Species abundance and richness of birds and butterflies in the
Keywords:
city parks of Marseille (south-east France) have been used to assess these changes. On the basis of easily
Birds
accessible traits (reproduction parameters, size, feeding habits), we have examined whether different
Butterflies
Urbanization
contexts of urbanization favour some strategies more than others. Some differences occur between but-
Functional attributes terflies and birds in terms of species abundance and richness through the urbanization gradient, showing
Community that at least some species of birds manage to colonize city centre and/or exploit urban resources bet-
ter than butterflies. But our results also clearly reveal general patterns in biological traits for both birds
and butterflies that further reflect the gradient of urban features from outskirts to city centre. Species
associated with the city centre tolerate a wide range of conditions whereas species associated with city
outskirts have more specialized abilities. Urbanization acts as an environmental filter for bird and but-
terfly communities selecting species able to colonize and settle in the city centre on the basis of their
biological traits. In our context, environmental filters induce a biotic homogenization with urbaniza-
tion through loss of species (taxonomic homogenization) and over-representation of generalist species
(functional homogenization). This homogenization reflects an underlying process of disruption of biotic
interactions for butterflies and birds. This study has enabled us to identify a combination of biological
traits sensitive to urban features that may represent useful indicators for both theoretical and applied
purposes in order to understand the impact of urbanization on animal communities.
© 2010 Published by Elsevier Ltd.

1. Introduction Biotic homogenization appears to be a major consequence of

Urbanization, through habitat loss and fragmentation
(McKinney, 2002), is a major component of the current changes of
ecosystems (Turner et al., 2004), and is one of the most important
threats to local and global biodiversity (Wilcox and Murphy,
1985). Several studies have described changes in composition and
structure of ecological communities associated with urban land
use (Blair, 1999; Clergeau et al., 2006a; Posa and Sodhi, 2006;
Sadler et al., 2006). Clergeau et al. (2006b) have also demonstrated
that urbanization tends to act as an environmental filter (Statzner
et al., 2004) selecting species on the basis of their biological traits.
Anthropogenic disturbance and human-assisted dispersal of exotic
species induce changes in the distribution of species in urban
areas, with many declining species, but also some species that
succeed in these environments.
∗ Corresponding author. Tel.: +33 04 91 10 62 18; fax: +33 04 91 08 30 36.
E-mail address: marie-helene.lizee@univ-provence.fr (M.-H. Lizée).
anthropogenic alteration of ecosystems for animal and plant com-
munities (Julliard et al., 2006; Warren et al., 2001). This process
refers most of the time to an increase of taxonomic similarity among
biotas (Olden and Rooney, 2006). But the replacement of native
species by more tolerant or non-indigenous species (Blair, 2001;
Croci et al., 2008; Holway and Suarez, 2006; McKinney, 2006) may
result, at a higher level of organization, in functional homogeniza-
tion. This other aspect of homogenization is defined as an increase
in functional similarity of biotas associated with a high redundancy
of biological traits of species (Olden and Rooney, 2006). Thus, sen-
sitivity of species to human disturbance seems to depend on some
particular functional attributes: large size, low fecundity, slow dis-
persal, high specialization, rarity (McKinney and Lockwood, 1999).
The relative amount of specialist and generalist species is very
likely to influence ecosystem functioning (Lawton and Brown,
1993). The generalist/specialist concept has been proved to be
helpful in the understanding of changes in community composi-
tion and structure along different environmental gradients such
as fragmentation (Barbaro and Van Halder, 2009), habitat loss and

1470-160X/$ – see front matter © 2010 Published by Elsevier Ltd.

doi:10.1016/j.ecolind.2010.06.003
354 M.-H. Lizée et al. / Ecological Indicators 11 (2011) 353–361
isolation (Niell et al., 2007), rural/urban gradient (Blair and Launer,
1997; Posa and Sodhi, 2006). Considering that the success of species
in human-altered environments partly depends on some particu-
lar biological traits, we address the question of which functional
changes in community structure correspond to an intra-urban gra-
dient.
Characteristics of species able to persist in urban environment
deserve further investigation in order to achieve a more accu-
rate understanding of urban ecosystems’ functioning (Sochat et al.,
2006). Moreover, it has been suggested that ecosystem processes
depend more on functional diversity than on species richness per se
(Diaz and Cabido, 2001). So, given the vast scale of urbanization in
terms of land cover, indentifying functional types of species sensi-
tive to urbanization is of increasing importance for both theoretical
and applied purposes (McGill et al., 2006).
In this paper, we examine how the urbanization context could
be related to particular combinations of biological traits on the basis
of the distribution of butterfly and bird species in the city parks of
the third-largest French metropolitan area (Marseille, south-east
France). These two taxa are known to be good indicators of habitat
and landscape changes (Blair, 1999; Brown, 1991; Furness et al.,
1993) and have been extensively documented. Moreover, they also
represent different dispersion abilities (Pearson and Carroll, 1998)
and thus different spatial scales of perception of urban features
(Hostetler and Holling, 2000; Kotliar and Wiens, 1990; Thomas,
1994).
Our study focuses on the city parks of a large metropolitan area.
Studies in urban ecology often focus on remnant fragments of nat-
ural or semi-natural habitats (Krauss et al., 2003; Niell et al., 2007;
Smith, 2007). But understanding the functioning of man-made
and/or artificialized habitats, such as city parks or private gardens,
is an essential first step toward understanding urban ecosystems
in as much as they represent a major and growing part of avail-
able habitats in urban areas (Gaston et al., 2005; Mathieu et al.,
2007).
Our goal is to: (1) characterize the composition and structure of
butterfly and bird communities of the urban parks in the city of Mar-
seille and (2) based on easily accessible functional traits, analyse
whether urbanization favours some strategies more than others.
2. Materials and methods
2.1. Study site and park selection
This study was carried out in the coastal city of Marseille
(France) during the spring and summer of 2008 and 2009. The
region has a Mediterranean climate characterized by cool winters,
irregular precipitation (between 700 and 1000 mm per year) and
pronounced summer drought that limits the growing season to
brief periods in spring and autumn (Joffre et al., 2007).
Marseille was selected for two reasons: (i) this study site is
located in the Mediterranean region which is classified as one of
the 34 biodiversity hotspots (Myers et al., 2000; Mittermeier et al.,
2005); and (ii) it is the second most populous French city, spreading
over 240 km2 , as well as the oldest city in France.
Marseille is the core of the third-largest French metropolitan
area with a population estimated at 1,605,000 in 2007. Moreover,
in contrast to several European cities, it is not surrounded by a
peripheral agricultural belt, but by calcareous massifs which bring
natural and semi-natural areas to the gates of the city. This con-
figuration offers a range of landscape contexts from city centre of
high building density to natural massifs, and thus different degrees
of isolation from regional species source areas.
Fifteen city parks (out of a an earlier sample of 24 parks) have
been selected to be studied according to size (1–15 ha), land cover
(Corine Land Cover, 2006) and distance to city centre in order to be
representative of the diversity of urbanization contexts occurring in
Marseille (Fig. 1). In order to assess the impact of landscape and iso-
lation on the selection of species’ life history traits, parks have been
grouped in three categories according to the urbanization context:
parks in the town centre (corresponding to “continuous urban fab-
ric” on Corine Land Cover, 2006), parks on the outskirts and parks
in intermediate position (Fig. 1).
2.2. Butterfly and bird surveys
Butterfly communities were sampled during the spring and the
summer of 2008 (May–August). Seven to 13 transects were per-
formed in each park according to park size and were replicated
four times during the survey period (once a month). Transects were
chosen in order to represent the habitat diversity of each park.
The heterogeneity of the park vegetation led us to a compromise
between usual transect count and point count, in order to perform
samples in homogeneous vegetation units. So transects in this study
correspond to linear surveys on 25 m × 10 m where all individuals
crossing this feature were recorded during 5 min. In order to stan-
dardise the climatic conditions, plots were sampled between 9 h
and 17 h on days when the temperature was above 20 ◦ C, cloud
cover was less than 50% and wind speed was less than 20 km/h.
For birds, members of a local natural history society carried out
the surveys during the spring of 2009 (April–June). Point counts
without limited distance were used (Blondel et al., 1981). They con-
sisted of 30 min–2 h of survey according to park size and each park
was sampled twice. Point counts were performed early in the morn-
ing, beginning at the onset of increased bird activity. Days with rain
and strong wind were avoided.
Each group of parks represents the same sampling effort: two
parks of less than 3 ha, two parks between 3 and 10 ha and one park
larger than 10 ha, which correspond to 44 butterfly transects and
5 h of bird survey per month for each urbanization context.
2.3. Data analysis
To verify differentiation of the groups of parks according to land-
scape features, the surrounding context of each of the 15 parks has
been characterized. Within a 250 m buffer zone, density of build-
ings, density of roads, density of trees, density of grasslands and
mean patch area (m2 ) have been computed from maps (IGN, 2004,
2006) and land plot data. Distance from park to natural areas sur-
rounding the city was measured from a municipal town planning
document. Then, a principal component analysis (PCA) was per-
formed on these data to assess the discrimination of the three
groups of parks. Finally, to test the statistical significance of these
differences, analysis of similarities (ANOSIM) was used (the non-
normal distribution of grassland density values precludes the use
of MANOVA). ANOSIM is a non-parametric test of significant differ-
ence between two or more groups, based on any distance measure
(Clarke, 1993). Here, Euclidean distance has been used. The test
is based on comparing distances between groups with distances
within groups. Large positive R statistic value (up to 1) indicates
dissimilarity between groups, whereas weak or negative value (up
to −1) indicates strong similarity between groups. The significance
is computed by permutation of group membership, with 10,000
replicates.
Only species more abundant than 5 individuals in the earlier
sample of 24 parks were kept for statistical analysis (which allows
removal of migrant bird species). For birds, aquatic species have
also been removed from records, as their occurrence depends more
on local park features than on landscape characteristics.
A canonical correspondence analysis (CCA) (Ter Braak, 1987)
was finally performed for each biological model to test whether
 M.-H. Lizée et al. / Ecological Indicators 11 (2011) 353–361 355

Fig. 1. City of Marseille with land cover according to Corine Land Cover 2006 nomenclature and studied parks (1–5: town centre parks, 6–10: intermediate parks, 11–15:
parks on the outskirts).

Table 1
Life history traits selected for CCA.

Model Life history trait Categories Abbreviation in

figures

Butterflies (1) Wingspan Mean anterior wing length Wingspan

(2) Voltinism Monovoltine species Monoviltine
Bivoltine species Bivoltine
Multivoltine species Multivoltine
(3) Larval diet Number of plant genera used as HP genera
host-plant
(4) Larval diet Number of plant families used as HP families
host-plant
(5) Wintering stage Stage 1: egg or larvae Wintering stage 1
Stage 2: pupa or adult Wintering stage 2

Birds (1) Wingspan Distance from the left wingtip to the Wingspan
right wingtip
(2) Egg production Number of eggs per clutch * number of Eggs year
clutches per year
(3) Adult diet Granivorous Feed grani
Omnivorous Feed omni
Insectivorous Feed insect
(4) Nesting habitat Cavernicolous species using buildings Nest cav.buildings
Cavemicolous species using trees Nest cav.tree
Cavernicolous species using buildings Nest cav.mixt
or trees
Species using vegetation for nesting Nest veg
non-cavernicolous
356 M.-H. Lizée et al. / Ecological Indicators 11 (2011) 353–361
Fig. 2. Graphical interpretation of the PCA computed on landscape variables (circles:
central parks, squares: intermediate parks, triangles: outskirts parks).
biological traits can predict species distribution between the three
contexts of urbanization. CCA is a way of measuring the linear rela-
tionship between two multidimensional datasets. Two tables have
been used for each biological model (butterflies and birds). The first
table is the matrix of k species abundances recorded at the three
urbanization contexts. The second table is the matrix of n biological
traits characterizing the k species. These two tables are linked by
their rows (species). CCA looks for coefficients of biological traits
to obtain a species score that maximises the variance of average
positions of urbanization contexts. The gradient of biological traits
is known a priori and the variations of species abundance in the
three urbanization contexts are considered to be a response to this
gradient. The ordination axes are thus linear combinations of these
biological traits. Biological traits shown in Table 1 have been con-
sidered (Lafranchis, 2000; Santin, 2004; Hume et al., 2009) (see
Appendices 1 and 2).
The significance of the relationships between species distribu-
tion in the first table and species traits in the second table was
assessed by a Monte Carlo test based on 999 permutations.
All statistical tests and analyses have been performed using the
“ade4” package in R software v.2.9.2 (R Development Core Team,
2010) and P.A.S.T. software v.1.93 (Hammer et al., 2001). The map
has been designed using MapInfo Professional® v.9.5 (Mapinfo,
2010).
3. Results
3.1. Park discrimination according to landscape features
On the basis of the PCA plot, the three groups of parks corre-
spond to different urbanization contexts. These three groups are
well individualised on the first principal component which repre-
sents approximately 72% of inertia (Fig. 2). Town centre parks are
regrouped on the left of the plot, associated with high road density
(roads), high building density (buildings) and greater distance from
natural areas (natural dist). Inversely, parks on the outskirts are
associated with high density of trees (trees) and grasslands (grass-
Table 2
Averages of environmental variables for each urbanization context.
Urbanization context Building density Road density Grassland density Number of trees/hectare
Centre 0.43 ± 0.11 0.26 ± 0.10 0.00 ± 0.00 27.19 ± 11.77
Intermediate 0.21 ± 0.05 0.14 ± 0.05 0.06 ± 0.14 56.89 ± 17.74
Outskirts 0.15 ± 0.06 0.08 ± 0.01 0.30 ± 0.18
Table 3
Abundance and richness of butterflies and birds in the three groups of parks.
Centre Intermediate Outskirts Total
Butterflies abundance 327 356 1016 1699
Butterflies richness 20 25 35 36
Birds abundance 547 484 285 1316
Birds richness 17 24 26 29
lands) and high mean patch area (patch area). Parks in intermediate
position from centre and outskirts have an intermediate position
on the plot. Averages of environmental variables for each group of
parks are shown in Table 2.
The results of ANOSIM are congruent with the differenti-
ation shown in the PCA plot. In pairwise comparisons, city
centre parks are very different from parks on the outskirts
(R = 0.99; p(same) = 0.02) and from intermediate parks (R = 0.76;
p(same) = 0.03). The R statistic obtained for pairwise comparison
between intermediate and outskirts parks reveals a lower differ-
entiation (R = 0.34; p(same) = 0.06).
3.2. Species and biological traits distribution
The 15 selected parks correspond to 36 butterfly species (1699
individuals) and 29 bird species (1316 individuals) (see Appendices
1 and 2). Species and individuals are distributed between the three
groups of parks as shown in Table 3.
From city centre to outskirts, we can note a high increase
in species richness for butterflies (+15 species), and a slightly
lower increase for birds (+9 species). Patterns of abundance differ
between the two taxonomical groups. Abundance of birds regularly
increases from outskirts to city centre, while abundance of butter-
flies drastically decreases in intermediate and city centre parks.
The two CCAs show that the distribution of species between
the three groups of parks is associated with particular trait assem-
blages.
For butterflies, biological traits explain 52.56% (p = 0.033 based
on 999 permutations) of the species distribution (Fig. 3a). The
first axis of the CCA accounts for most of the variance (86.45%)
and clearly separates city centre and intermediate parks from
outskirts parks. City centre and intermediate parks record an over-
representation of multivoltine species, polyphagous species and
species overwintering at adult or pupal stages. Inversely, mono-
voltine and more specialized feeding species are over-represented
in outskirts parks.
Biological traits associated with the second component should
be considered with caution because of its low representation
(13.55% of total inertia). However, wing size contribution to this
component is high and probably due to the association of the
largest species (Charaxes jasius, Pieris brassicae, Papilio machaon,
Iphiclides podalirius) to intermediate and outskirts parks (Fig. 3b).
We may also note that Mediterranean species (excepting Leptotes
pirithous) are all associated with either intermediate or outskirts
parks (Fig. 3b).
For birds, biological traits explain 66.67% (p = 0.031 based on 999
permutations) of the species distribution between the three urban-
ization contexts (Fig. 4a). The first axis of the CCA accounts for most
of the variance (65.61%) and clearly separates central parks from
Mean patch area (hectare) Distance to natural areas (Km)
0.09 ± 0.08 4.80 ± 1.23
0.31 ± 0.13 2.21 ± 0.66
74.1 ± 6.75 0.39 ± 0.13 1.47 ± 1.04
 M.-H. Lizée et al. / Ecological Indicators 11 (2011) 353–361
Fig. 3. CCA ordination diagram with butterfly species (䊉) (see abbreviations in
Appendix 1), urbanization contexts (boxes, C, city centre parks; I, intermediate
parks; P, outskirts parks) and biological traits (arrows). Mediterranean species are
marked with ** (Lafranchis, 2000).
outskirts and intermediate parks. The second axis of CCA accounts
for a non-negligible part of the variance (34.39%) and discriminates
outskirts parks from city centre and intermediate parks. Building
nesters are over-represented in the city centre parks, while parks on
the outskirts record an over-representation of insectivorous feed-
ers and species depending from vegetation for nesting. In parks
at intermediate position, granivorous species and cavernicolous
species using vegetation as well as buildings are over-represented.
Wingspan plays little part in differentiation, while high egg pro-
duction and omnivorous diet are associated with species recorded
in intermediate and central parks.
Although the association of range-restricted bird species with
the outskirts is lower than for butterflies, none of these species is
associated with the city centre (Fig. 4b).
4. Discussion
Our results confirm the interest of a functional attribute-based
approach to study animal communities in urban areas. This study
clearly highlights patterns in biological traits for birds and butter-
flies that differentiate the three groups of parks. This allows us to
357
Fig. 4. CCA ordination diagram with bird species (䊉) (see abbreviations in Appendix
2), urbanization contexts (boxes, C, city centre parks; I, intermediate parks; P, out-
skirts parks) and biological traits (arrows). Species with an Atlantic-Mediterranean
distribution range are marked with **, and species only present in summer are
marked with *** (Hume et al., 2009).
identify a combination of biological traits sensitive to urban fea-
tures that may represent useful indicators to understand the impact
of urbanization on animal communities.
Our results show that species associated with the city centre are
highly tolerant of a range of conditions whereas species associated
with the outskirts have more specialized abilities. This is an indica-
tion of a simplification in butterfly and bird community structure
which further reflects the gradient of urban features from outskirts
to city centre.
4.1. Landscape variables
ACP and ANOSIM show that urban landscape features discrimi-
nate the three groups of parks. Thus, in this study the gradient from
outskirts to city centre corresponds to an increase in habitat isola-
tion (greater distance to natural areas), habitat loss (decrease in
non-built surfaces) and habitat fragmentation (decrease in mean
patch area). Although the landscape differentiates intermediate
parks from parks on the outskirts, the main disruption in urban
features occurs between central and intermediate parks.
358 M.-H. Lizée et al. / Ecological Indicators 11 (2011) 353–361
4.2. Structure of butterfly and bird community
These three groups of parks also differ in species richness and
abundance. The number of species increases from city centre to
outskirts for both butterflies and birds which corresponds to a
general response of animal communities to human disturbance
(Clergeau et al., 1998; Rottenborn, 1999; Jokimäki and Hutha,
2000; Kitahara and Fujii, 1994; Yamaguchi, 2004; Sadler et al.,
2006). Patterns of abundance differ between the two taxonom-
ical groups. The pattern of increased abundance of birds with
urbanization has already been discussed in many studies (Niemelä,
1999; Clergeau et al., 2006a) and usually corresponds to the dom-
ination of the community by few species (e.g., Columba livia, or
Passer domesticus) able to exploit urban resources in food and habi-
tat, and even showing some preferences for the city centre (Blair,
1996). These resources, often fragmented, can be less easily acces-
sible for smaller and less mobile organisms (Pickett et al., 2001;
Lundholm, 2006). This can explain the decreased abundance of
butterflies toward the city centre as maintenance of the animal
population in fragmented landscapes depends on the ability to
disperse between patches (Ericson et al., 1988). The difference in
abundance patterns could be linked to different patterns of colo-
nization and settlement abilities of birds and butterflies. Birds are
capable of flight over long distances, hence buildings and roads do
not represent a barrier to their dispersal (Niemelä, 1999), whereas
butterflies can encounter difficulties, such as road kill, in coloniz-
ing the most urbanized areas (McKenna et al., 2001; Ries et al.,
2001).
This difference in the response of the two taxonomical groups
to urban landscape features also appears at biological trait level.
Biological traits explain a larger part of the species distribution
for birds than for butterflies. Moreover, the main disruption in
the structure of the bird community corresponds to the main
disruption in urban features, whereas changes in butterfly com-
munity seem to be more independent of these landscape changes
(Figs. 2–4). There might be limiting factors at both landscape and
local scale that prevent butterflies from settling in the most urban-
ized areas.
However, a general pattern in biological trait assemblages
through the urbanization gradient can be highlighted for both but-
terflies and birds.
4.3. Feeding habits
For butterflies and birds, feeding habits appear to be key indi-
cator traits for species response to urbanization. Omnivorous
birds favour city centre and intermediate parks whereas insec-
tivorous birds respond negatively to urbanization. Omnivory has
been shown to be more common in urbanized areas (Clergeau
et al., 1998; Jokimäki and Suhonen, 1998) while the decline
of insectivorous birds is often related to human disturbance
through urbanization (Lim and Sodhi, 2004), habitat fragmenta-
tion (Barbaro and Van Halder, 2009) or vegetation artificiality
(White et al., 2005). In the same way, the most polyphagous but-
terfly species are associated with central and intermediate parks.
This is consistent with various studies showing the high sensi-
tivity of monophagous and oligophagous species to urbanization,
habitat fragmentation and habitat loss (Kitahara and Fujii, 1994;
Steffan-Dewenter and Tscharntke, 2000, 2002; Posa and Sodhi,
2006).
Thus, landscape urban features seem to act as filters on the
potential colonizing species pool (Clergeau et al., 2006b; Croci et al.,
2008) favouring generalist feeders or species able to exploit urban
resources whereas species with more specialized feeding habits
respond negatively to urbanization.
4.4. Reproductive parameters and size
In our study, bird species with high annual egg production and
multivoltine butterfly species are associated with the highest level
of urbanization. These traits are known to be associated with dis-
turbance and often inversely correlated with body size (Barbaro
and Van Halder, 2009; Baguette and Van Dyck, 2007).
The association “multiple broods/small wing size” holds for but-
terflies in the city centre, but not for birds. This is explained, as
in other studies (Croci, 2007; Barbaro and Van Halder, 2009), by
the fact that some species of both small (Passer domesticus) and
large birds (Columba livia, Streptopelia decaocto) occur in city centre
(Fig. 4b).
For butterflies, monovoltine and bivoltine phenologies are con-
sidered as typical in Mediterranean climates (Shapiro, 2002). The
predominance of multivoltine species in the city centre could thus
be explained by new exploitable resources such as water supply,
ornamental plants and grasses (Blair and Launer, 1997; Graves and
Shapiro, 2003). But this pattern highlights a disturbing situation
as the absence of monovoltine species in the city centre is asso-
ciated with the quasi-absence of Mediterranean species. This is
consistent with other studies showing the sensitivity of endemic
or range-restricted species to human disturbance (Kuussaari et al.,
2007; Posa and Sodhi, 2006; Van Swaay et al., 2006).
Finally, high mobility is considered for butterflies and other
insects to be an adaptation to disturbed habitat and is generally
expected to prevent species from declining (Maes and Van Dyck,
2001; Warren et al., 2001; Bergman et al., 2004). So we might have
expected that large butterflies would be associated with the city
centre because of their higher dispersal abilities. But this is not the
case. The smaller size of butterflies associated with central parks in
our study is not significant enough to make conclusions, but could
recall the results of Cheptou et al. (2008) showing that reduced
dispersal ability could constitute a response of populations to frag-
mentation.
4.5. Wintering stage and nesting habits
For birds, the quasi-absence of arboreal nesters from the city
centre while building nesters are over-represented is consistent
with several other studies (Lim and Sodhi, 2004; Barbaro and Van
Halder, 2009). Moreover, we may note the general predominance
of cavernicolous species in the three urbanization contexts which is
a classical characteristic of bird communities in disturbed habitat
related to nest predation (Lancaster and Rees, 1979; Croci et al.,
2008; Barbaro and Van Halder, 2009).
For butterflies, the city centre records a strong over-
representation of species overwintering as adult or pupa while
the two categories of overwintering stage include approximately
the same number of species (see Appendix 1). This strategy can
represent advantageous foraging behaviour at the favourable sea-
son. The latter species are able to move to find resources, whereas
species overwintering as egg or larvae depend on the presence of
their host-plants where they overwinter.
Thus, these traits seem to reveal for both birds and butterflies
changes in dependence of species on vegetation along the urban-
ization gradient.
Moreover, the abundance of butterflies overwintering at adult or
pupal stages in central and intermediate parks could also be linked
to the heat island phenomenon in cities (Sochat et al., 2006), since
this trait has been proved to depend partly on climatic conditions
(Virtanen and Neuvonen, 1999). In northern Europe, the positive
trend in occupancy of species overwintering as adult has been high-
lighted by Kuussaari et al. (2007) who link this phenomenon to
warming average spring temperatures.
 M.-H. Lizée et al. / Ecological Indicators 11 (2011) 353–361 359

5. Conclusion These differences in the responses of birds and butterflies also

This functional attribute-based approach provides useful infor-
mation on potential changes in ecosystem functioning following
changes in the composition of species communities. It allows iden-
tification of groups of species more prone to decline than others
in urban environment. Therefore, biological traits constitute effi-
cient and easily accessible tools for purposes of both biological
conservation and urban management.
Our study also highlights the importance of citizen-based sur-
veys in monitoring biodiversity of urban areas. Bird counts in this
study provide a useful comparison between the two taxonomical
groups, and overall, allow generalization of the observed patterns.
Although some differences related to dispersal abilities and sen-
sitivity scales of the two taxonomical groups occur, general patterns
of biological traits suggest the replacement of specialist, urban-
sensitive species by generalist species better adapted to urban
environment (Blair, 1996; Clergeau et al., 2006b). This replacement
of non-tolerant species by urban-tolerant species underlines a risk
of functional biotic homogenization (Olden and Rooney, 2006) and
has been identified as a consistent signature of the current changes
of animal communities (Julliard et al., 2006; Kuussaari et al., 2007).
In our study, this functional homogenization consists in a dis-
ruption of biotic interactions highlighted by nesting habits for birds,
overwintering stage for butterflies and feeding habits for both.
Moreover, the important reproductive potential of these species
that thrive in the city centre (e.g., Cacyreus marshalli for butterflies
and Columba livia for birds) may in some cases generate nuisances
(Herrero et al., 2002; Savard et al., 2000) through rapid multipli-
cation. But, if some bird species, such as Columba livia and Passer
domesticus, are able to exploit resources of the city centre in terms
of habitat and food, none of the butterfly species, except Cacyreus
marshalli, which is a southern African introduced species (Sarto and
Monteys, 1992), shows a preference for the city centre. This sim-
plification of functional community structure with urbanization is
all the more worrying given the loss of endemic or range-restricted
species in the city centre of Marseille.
highlight the necessity of thinking these green networks at differ-
ent spatial scales, i.e. for different taxonomical groups representing
different sensitivity scales. Moreover, in our results, the disruption
in biotic interactions, the decreased species richness and the loss of
endemic species toward the city centre are related to habitat loss
and fragmentation, suggesting that green infrastructures constitute
a basic foundation for organisms of urban areas.
These preliminary results suggest the possibility of identifying
several indicator species that could constitute interesting moni-
toring tools for planners and managers of urban green areas. If
variations in functional traits are consistently correlated to vari-
ations in the structure of urban green networks, the survey of
functional composition of communities would allow park man-
agers to evaluate in real time the impact of urban planning or green
area management on ecosystem functioning.
The various environmental factors interacting along the urban-
ization gradient and their relative impact on changes in community
structure merit further investigation in order to provide a basis for
predicting which landscape features need more urgently to be pre-
served or restored in order to preserve functional diversity of urban
ecosystems.
Acknowledgements
We thank the Parks and Gardens authority of the City of Mar-
seille and in particular Patrick Bayle for facilitating our access to the
city’s parks. We would like to thank the members of the associa-
tion “La Chevêche” for their contribution to this work and especially
Eric Barthélémy. We also acknowledge the help of Bernard Brun in
reading the paper. We are grateful to Michael Paul for improving
the English. This study was carried out as part of the PIRVE Program
and the ANR “ville durable” Program (#VD08 321105).
Appendix 1.
Distribution and biological traits of butterfly species.

Abbreviations Centre Intermed. Outskirts Wingsize Voltinism HP family HP genius Overwintering

in figures stage

Pieris rapae (Linne, 1758) Pie rap 105 113 267 25 Multivoltine 7 22 Adult or pupa
Pararge aegeria (Linne, 1758) Par aeg 33 76 66 20.5 Multivoltine 1 9 Both
Polyommatus icarus (Rottemburg, 1775) Pol ica 47 21 99 15 Multivoltine 2 15 Egg or larvae
Maniola jurtina (Linne, 1758) Man jur 1 3 121 24 Monovoltine 2 14 Egg or larvae
Colias crocea (Geoffroy, 1785) Col cro 46 9 45 25 Multivoltine 1 18 Both
Aricia agestis (Denis & Schiffermuller, 1775) Ari age 0 14 60 13.5 Multivoltine 2 4 Egg or larvae
Iphiclides podalirius (Linne, 1767) Lepjpir 25 12 19 12.5 Multivoltine 4 19 Both
Melitaea didyma (Esper, 1779) Mel did 0 0 51 20 Bivoltine 7 16 Egg or larvae
Lasiommata megera (Linne, 1767) Las meg 2 10 34 22.5 Multivoltine 1 11 Egg or larvae
Carcharodus alceae (Esper, 1780) Car ale 6 11 25 14.5 Multivoltine 2 4 Egg or larvae
Iphiclides podaiirius (Linne, 1758) Iph pod 8 17 17 36 Bivoltine 1 9 Adult or pupa
Cacyreus marshalli (Butler, 1898) Cac mar 26 7 2 12 Multivoltine 1 2 Both
Lycaena phlaeas (Linne, 1761) Lyc phl 1 4 30 13.5 Multivoltine 1 3 Egg or larvae
Pieris napi (Linne, 1758) Pie nap 0 0 32 22.5 Multivoltine 3 23 Adult or pupa
Celastrina argiolw (Linne, 1758) Cel arg 8 12 11 15 Bivoltine 19 43 Adult or pupa
Pieris brassicae (Linne, 1758) Pie bra 2 11 17 30.5 Multivoltine 5 18 Adult or pupa
Papilio machaon (Linne, 1758) Pap mac 3 4 15 36 Multivoltine 5 43 Adult or pupa
Pontia daplidice (Linne, 1758) Pon dap 0 0 21 21.5 Multivoltine 2 17 Adult or pupa
Vanessa atalanta (Linne, 1758) Van ata 5 7 7 29.5 Bivoltine 6 9 Adult or pupa
Vanessa cardui (Linne, 1758) Van car 4 6 8 30.5 Multivoltine 16 55 Adult or pupa
Gonopteryx cleopatra (Linne, 1767) Gon cle 1 3 12 27.5 Monovoltine 1 1 Adult or pupa
Melanargia galathea (Linne, 1758) Mel gal 0 0 11 26.5 Monovoltine 1 11 Egg or larvae
Charaxes jasius (Linne, 1767) Cha jas 1 6 2 44 Bivoltine 7 8 Egg or larvae
Polygonia c-album (Linne, 1758) Pol c-al 2 1 6 24 Bivoltine 9 11 Adult or pupa
Pyroma cecilia (Vallantin, 1894) Pyr cec 0 0 8 17.5 Monovoltine 1 3 Egg or larvae
Euchloe crameri (Butler, 1869) Euc era 0 0 7 21 Bivoltine 1 7 Adult or pupa
Pyrgus cirsii (Rambur, 1839) Pyr cir 0 1 5 13.5 Monovoltine 1 1 Egg or larvae
Brintesia circe (Fabricius, 1775) Bri cir 0 0 5 37 Monovoltine 1 7 Egg or larvae
Limenitis reducta (Staudinger, 1901) Lim red 1 2 2 27 Bivoltine 1 1 Egg or larvae
Pieris mannii (Linne, 1758) Pie man 0 2 3 23 Multivoltine 1 3 Adult or pupa
Lampides boeticus (Linne, 1767) Lam boe 0 3 0 15.5 Multivoltine 2 27 Both
360 M.-H. Lizée et al. / Ecological Indicators 11 (2011) 353–361

Appendix 1 (Continued )

Abbreviations Centre Intermed. Outskirts Wingsize Voltinism HP family HP genius Overwintering

in figures stage

Thymelicus acteon (Rottenburg, 1775) Thy act 0 0 3 12 Monovoltine 1 6 Egg or larvae

Pyronia bathseba (Fabricius, 1793) Pyr bat 0 1 1 20.5 Monovoltine 1 3 Egg or larvae
Satyrium escidi (Hubner, 1804) Sat esc 0 0 2 16 Monovoltine 1 1 Egg or larvae
Coenonympha dorus (Esper, 1782) Coe dor 0 0 1 18 Monovoltine 1 3 Egg or larvae
Libythea celtis (Laicharting, 1782) Lib cel 0 0 1 19.5 Bivoltine 1 1 Adult or pupa

Appendix 2.

Distribution and biological traits of bird species.

Abbreviations Centre Intermed. Outskirts Wingspan Eggs year Nesting habitat Adult diet
in figures

Columba livia domestica (Gmelin, 1789) Col liv 225 81 67 66.5 6 Nest cav.buildings Feed omni
Passer domesticus (Linne, 1758) Pas dom 113 100 12 21 28 Nest cav.buildings Feed omni
Larus michahellis (Naumann, 1840) Lar mic 40 75 37 140 3 Nest cav.buildings Feed omni
Apus apus (Linne, 1758) Apu apu 80 23 40 45 3 Nest cav.buildings Feed insect
Pica pica (Linne, 1758) Pic pic 18 30 37 57 8 Nest veg Feed omni
Parus major (Linne, 1758) Par maj 5 21 19 23.5 11 Nest cav.tree Feed insect
Streptopelia decaocto (Frivaldszky, 1838) Str dec 18 13 10 51 6 Nest veg Feed grani
Sylvia atricapilla (Linne, 1758) Syl atr 8 14 10 21.5 10 Nest veg Feed insect
Corvus monedula (Linne, 1758) Cor mon 5 25 1 70.5 6 Nest cav.buildings Feed omni
Parus caeruleus (Linne, 1758) Par cae 6 11 8 18.5 16 Nest cav.mixt Feed insect
Serinus serinus (Linne, 1766) Ser ser 9 8 6 19 12 Nest veg Feed grani
Sylvia melanocephala (Gmelin, 1789) Syl mel 5 8 9 16.5 10 Nest veg Feed insect
Hirundo rustica (Linne, 1758) Hir rus 0 9 10 33.5 18 Nest cav.buildings Feed insect
Sturnus vulgaris (Linne, 1758) Stu vul 2 15 0 39.5 14 Nest cav-mixt Feed omni
Psittacula krameri (Scopoli, 1769) Psi kra 0 15 1 45 5 Nest cav-mixt Feed grani
Carduelis carduelis (Linne, 1758) Car car 4 10 0 23 12 Nest veg Feed grani
Motacilla alba (Linne, 1758) Mot alb 3 7 2 27.5 18 Nest cav.buildings Feed insect
Carduelis chloris (Linne, 1758) Car chl 5 4 1 26 12 Nest veg Feed grani
Corvus corone (Linne, 1758) Cor cor 0 4 3 98.5 6 Nest veg Feed omni
Phoenicurus phoenicurus (Linne, 1753) Pho pho 0 5 2 22 7 Nest cav.tree Feed insect
Phylloscopus collybita (Vieillot, 1817) Phy col 1 2 1 18 12 Nest veg Feed insect
Certhia brachydactyla (CL.Brehm, 1820) Cer bra 0 2 1 19.5 6 Nest cav.tree Feed insect
Columba palumbus (Linne, 1758) Coljal 0 0 3 77.5 4 Nest veg Feed grani
Erithacus rubecula (Linne, 1758) Eri rub 0 1 1 21 12 Nest veg Feed insect
Accipiter nisus (Linne, 1758) Ace nis 0 0 1 70 5 Nest veg Feed insect
Fringilla coelebs (Linne, 1758) Fri coe 0 0 1 26.5 5 Nest veg Feed insect
Luscinia megarhynchos (C.L. Brehm, 1831) Lus meg 0 0 1 24.5 5 Nest veg Feed insect
Parus cristatus (Linne, 1758) Par cri 0 1 0 18.5 7 Nest cav.tree Feed insect
Picus viridis (Linne, 1758) Pic vir 0 0 1 41 7 Nest cav.tree Feed insect

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