Urban Ecosyst
DOI 10.1007/s11252-014-0375-y
Urban biodiversity hotspots are not related to the structure
of green spaces: a case study of tenebrionid beetles
from Rome, Italy
Simone Fattorini
# Springer Science+Business Media New York 2014
Abstract At global and regional scales, area prioritisation is frequently done by the identification of hotspots based on species extinction risk. The logic of the hotspot identification has
never been used in urban contexts. In this paper, the tenebrionid beetles (Coleoptera
Tenebrionidae) of urban Rome were studied as an exercise to show how the hotspot approach
can be profitably used in an urban area to identify priority areas for biodiversity conservation.
For this, tenebrionid species from 16 green spaces were scored according to their vulnerability
on the basis of their geographical distribution, habitat specificity and abundance. Species
vulnerability scores were then used to calculate two indices of area prioritisation (the
Biodiversity Conservation Concern and the Biodiversity Conservation Weight) for each green
space. Values of these indices were correlated with site characteristics and compared with those
obtained from other, more natural contexts. Except for distance to other sites, no significant
correlation was found between conservation values and site characteristics, which indicates
that the conservation importance of green spaces cannot be predicted on the basis of their
geographical characteristics, but must be established on the basis of the species that they
actually host. The importance of urban green spaces for biodiversity conservation may be
questioned because of the large presence of ubiquitous and alien species in urban areas.
Conservation values obtained for tenebrionids of green spaces in Rome are similar to those
of various animal groups in more natural contexts and hence highlight the actual importance of
green areas for insect biodiversity conservation.
Keywords Coleoptera Tenebrionidae . Conservation Planning . Green Spaces . Mediterranean .
Rarity . Species Vulnerability
S. Fattorini (*)
Departamento de Ciências Agrárias, Azorean Biodiversity Group (CITA-A) and Platform for Enhancing
Ecological Research & Sustainability (PEERS), Universidade dos Açores, Angra do Heroísmo, Terceira,
Açores, Portugal
e-mail: [email protected]
Urban Ecosyst
Introduction
Urban green spaces are known to be extremely important for biodiversity conservation
(Angold et al. 2006; Jones and Leather 2012) and there is increasing interest in their inclusion
in urban planning and global biodiversity conservation actions (Adams 2005; Secretariat of the
Convention on Biological Diversity 2012).
Since their inception (e.g. Faeth and Kane 1978), biodiversity studies in urban areas have
been inspired by the theory of island biogeography (Marzluff 2005) and have been mainly
addressed to the identification of the effects of urbanization on species richness (McKinney
2008). However, results for invertebrates largely varied according to the species’
sensitivity to patch size, landscape characteristics surrounding patches, and patch
isolation, and little is known about the best methods to maximise green spaces for
use by wildlife (Jones and Leather 2012).
Use of island biogeography principles for conservation purposes in fragmented
landscapes has been severely criticised (see Laurance 2010 for a review). However,
island biogeography still inspires urban biodiversity studies focusing on numbers of
species and characteristics of green spaces which correlate with species richness (see
Clarke et al. 2008; Sattler et al. 2011; McDonnell and Hahs 2013).
At global to regional level, area prioritisation is frequently done by the identification of
hotspots based on species extinction threats (Dobson et al. 1997; Griffin 1999; Ceballos and
Ehrlich 2006; Fattorini 2006, 2009). The logic of identifying as priority areas those having a
concentration of threatened species may be also applied at local scale, but – to my knowledge –
it has never been used in urban contexts. However, identifying the areas that host high
concentrations of the most vulnerable species may be particularly important for biodiversity
conservation also in urban areas. It has been frequently claimed that urban green spaces are
important biodiversity reservoirs (Hunter and Hunter 2008; Dearborn and Kark 2009;
McDonnell and Hahs 2013). But, if the high species richness recorded in urban areas is only
composed of non-native (alien) species and species that are omnipresent and abundant in other,
more natural, ecosystems (McKinney and Lockwood 1999; McKinney 2006), then their actual
value for biodiversity conservation would be strongly diminished, and overemphasis on urban
land protection might have negative consequences for bioconservation at larger scales, by
diverting public attention from more important natural sites (Battisti and Gippoliti 2004). Thus,
it is of paramount importance to assess if urban green spaces host assemblages of species that
are vulnerable at a larger scale of analysis and hence can really contribute to species
conservation.
In this paper, I used the tenebrionid beetles (Coleoptera Tenebrionidae) of urban Rome as
an exercise to show how the hotspot approach can be profitably used in an urban context to
identify priority areas for biodiversity conservation. Present-day urban arthropod species are
frequently relicts from pre-urban ecosystems (Germann et al. 2008), and this is also the case of
Rome, where native insects are rapidly declining as a result of urban expansion (Fattorini
2011a,b). Because not all species are equally vulnerable, it is important to weight species
according to their differential conservation status and then to consider their differential
contribution to the overall diversity observed in each site to establish conservation priorities
(Fattorini 2006, 2009; Fattorini et al. 2012a). For this, I calculated indices of site conservation
concern using species vulnerability scores based on a set of species rarity measures from local
to national scale. Then, I used these results to see if the conservation values found for urban
green spaces were similar to those of more natural contexts and to test if green space
parameters frequently used to drive conservation planning are related to the observed conservation concern of the study green spaces.
Urban Ecosyst
Methods
Study area
With a population of about 3 million inhabitants, Rome is the largest city in Italy and one of the
largest in Europe. Urban Rome was defined here as the territory of the town encompassed by
the great motorway ring that circumscribes an area of about 360 km2 (see Fattorini 2011a, b).
Approximately one-half of this area is covered by built-up surfaces, whereas the other half is
occupied by green spaces, including historical villas, archaeological sites, meadows, grasslands, public gardens, parks, and suburban cultivated and uncultivated grounds. Several green
spaces represent relicts of the late ‘Campagna Romana’, a traditional landscape composed of a
mosaic of agricultural, grazing and woodland patches. A few larger green spaces extend
outside the urban territory, being in direct connection with the rural landscape. On the basis
of data availability, I considered 16 green spaces evenly distributed from the city centre to the
borders of the study area (Table 1, Fig. 1).
Site characteristics
For each green space, the following structural parameters, which might influence tenebrionid
communities and which have been frequently evoked in reserve design (see Pullin 2002;
Laurance 2010), were measured (Table 1):
–
–
–
–
–
–
area (A): Larger green spaces will tend to support larger populations with lower extinction
risks (see Lomolino et al. 2010 for a general discussion; Soga et al. 2013 for urban
insects).
minimum distance to the city centre (Piazza Barberini) (D): Because of the radial urban
development of Rome, D expresses the urban-rural gradient. More peripheral populations
are less threatened by the multiple negative effects of human disturbance that increase
with urbanization intensity (McKinney 2002); they are closer to the areas that are source
of immigrants (Dias 1996), and benefit of rescue effects (Gosselin 1996).
mean distance of adjacent green spaces (Dn): Proximity to other green spaces favours
inter-site dispersal of immigrants (Magura et al. 2001) and provides enough suitable
environment to sustain a meta-population (Davis 1979). Populations living in less isolated
areas are less subject to the effects of genetic isolation (Davies et al. 2001). Small green
spaces, even if unable to sustain a stable population of a given species, may sustain
individuals that are dispersing towards more suitable areas (Thomas et al. 2000).
amount (F) and percentage (%F) of forested area, i.e. area of the surface covered by trees:
Larger fragments of natural habitats increase the long-term viability of populations and
hence support more species dependent on native habitats (Andrén 1994; Fahrig 1997;
Donnelly and Marzluff 2004).
shape of the green space (S): More rounded area shapes favour the presence of interior
species (Yamaura et al. 2008; Kotze et al. 2012) and reduce the risk of extinction because
circularization promotes conspecific interaction and positively affects dispersal rates
(Diamond 1975).
shape of the forested area inside the green space (Sf): Rounded shapes of habitat
fragments reduce edge effects (Sisk et al. 1997; Davies et al. 2001; Yamaura et al. 2008).
To quantify area circularization, I calculated a shape index (S) that express how the
observed shape is similar to a circle. For this, I calculated the ratio between the circumference
N
N
41.88922 12.48685
41.89075 12.49730
41.88610 12.48170
41.93380 12.50100
41.93385 12.44980
41.85285 12.51951
41.93980 12.52020
41.91678 12.43088
2 - Palatino
3 - Colle Oppio
4 - Circo Massimo
5 - Villa Ada
6 - Monte Mario
7 - Appia Antica
8 - Aniene
9 - Pineto
41.80980 12.46900
15 - Cervelletta
16 - Laurentino
N
N
N
A
N
0.143 0.116 0.114
0.429 0.419 0.405
0.214 0.279 0.179
0.250 0.163 0.250
0.238 0.233 0.214
0.163 0.186 0.163
0.190 0.093 0.143
0.048 0.023 0.048
0.143 0.070 0.095
0.143 0.070 0.095
0.159 0.233 0.143
0.057 0.047 0.057
0.214 0.140 0.143
0.333 0.326 0.310
0.429 0.349 0.343
0.286 0.140 0.190
0.098
0.415
0.244
0.171
0.220
0.195
0.073
0.024
0.049
0.049
0.220
0.049
0.098
0.317
0.293
0.098
216.0
80.0
284.0
381.9
973.3
668.5
3.5
84.0
284.1
1997.8
240.6
165.1
16.1
18.9
37.2
0.9
20,429
15,293
14,997
14,313
13,220
11,904
9,705
8,687
8,900
7,536
6,545
4,518
3,497
2,487
2,145
1,456
124
14
96
159
134
190
278
310
250
160
270
260
23
230
71
102
19.8
5.7
17.3
14.5
240.4
373.0
2.1
22.9
149.2
293.9
165.5
120.0
2.5
6.2
4.1
0.6
0.765
0.662
0.639
0.474
0.409
0.342
0.679
0.376
0.403
0.507
0.387
0.750
0.569
0.720
0.804
0.744
0.195
0.069
0.218
0.216
0.087
0.086
0.041
0.089
0.208
0.115
0.189
0.320
0.804
0.310
0.350
0.403
Area
Distance to
Mean distance
Forested Area shape Forest
BCW
BCW BCC
shape
(hectares) city centre (m) to other sites (m) Area
Kattan
Kattan
(hectares)
modified modified
Green space types: A Archaeological site, N Natural park, V Historical Villa
41.85128 12.55375
41.91413 12.58662
14 - Acquedotti
41.84300 12.40000
41.95810 12.55870
13 - Monte Sacro
N
41.95548 12.42749
11 - Insugherata
12 - Infernaccio Magliana
V
10 - Scuola Principe Piemonte 41.85845 12.47490
A
N
V
A
A
A
V
41.89626 12.48723
1 - Villa Aldobrandini
Longitude Type BCC
Latitude
Name
Table 1 Characteristics of green spaces investigated in urban Rome and values of Biodiversity Conservation Concern (BCC) and Biodiversity Conservation Weights (BCW) indices
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Fig. 1 Map of Rome with indication of studied green spaces. Green space numbers as in Table 1
of a theoretical circle of equal surface to that of the green space and the perimeter of the green
space (Patton 1975; Hill 1994). This index is 1 for a perfectly circular green space and tends to
0 as the shape tends to diverge from a circle. The same approach was used to express the shape
of the forested area (Sf). The Sf index expresses the extent of the interface between forested
and open areas within a green space, end hence is a measure of the ecotone development.
Many studies on urban biodiversity considered forested areas as particularly important for
biodiversity conservation (e.g. Dreistadt et al. 1990; Kotze et al. 2012; Soga et al. 2013) and
the percentage of forested surface has been even used as a measure of the degree of
urbanization (Donnelly and Marzluff 2004). To identify green spaces and to take the aforementioned measures, I used the GIS facilities of the National Geoportal (http://www.pcn.
minambiente.it/GN/index.php?lan=en).
Rome’s millenary natural heritage includes a variety of green space types, which were
classified here into three basic categories: (1) old villas, i.e. green spaces typically deriving
from the enclosure of the Roman countryside and estates, mainly located within the inner city
area; (2) archaeological sites; i.e. green spaces mainly occupied by ancient ruins; (3) “natural
parks”, i.e. fragments of the natural and seminatural vegetation of the so called Campagna
Romana landscape.
Species records
Primary data of tenebrionid records from these 16 green spaces were taken from Fattorini
(2011a), with a few, minor additions and corrections (Table 2). These data were derived from:
(1) an extensive literature survey of entomological papers on tenebrionids in Italy; (2) the
examination of material preserved in various insect collections, which were the most complete
for the study area; and (3) personal field research conducted through the entire study area from
1985 to 2000. The very large sampling efforts made by a number of collectors interested in
different insect groups and who used any kind of collecting methods (hand searching, pitfall
traps, aerial traps, light traps, soil examination, etc.) ensures that these data collectively form a
‘random’ sample, not affected by biases due to collector preferences for certain biotopes, sites
or species. Author’s specialized researches conducted from 1996 to 1999 were specifically
Urban Ecosyst
performed in the areas that were less intensively sampled in the past. Species that are strictly
associated with man, and which are proved or suspected to be recent introductions, such as
Alphitophagus bifasciatus, Gnatocerus cornutus, Latheticus oryzae, Tribolium castaneum,
Tribolium confusum, and Alphitobius diaperinus, all associated with stored food, were not
considered.
Only records from 1980 to nowadays were considered. It is well known that to obtain a
complete species inventory long term researches are needed, which suggests to consider also
relatively old records as contemporary presences, although some species might be went locally
extinct in the meantime. Most of the records collected in the period 1980–2012 were obtained
in the 1990s, which minimizes the risk of considering as present species that went in fact
extinct in the meantime.
Table 2 Tenebrionid species found in green spaces in urban Rome
Species
Original Modified
Kattan Kattan
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16
Accanthopus velikensis
1
1
0 0 0 0 1 1 0 0 1 0
1
1
0
0
1
1
Akis bacarozzo
4
3
0 1 1 0 0 0 1 0 0 0
0
0
0
1
0
0
Akis italica
7
7
0 1 1 0 0 0 0 0 0 0
0
0
0
0
0
0
Asida luigionii luigionii
4
3
1 1 1 1 0 0 0 0 1 0
0
0
0
1
0
0
Blaps gibba
1
1
1 0 1 1 0 1 0 1 0 0
1
0
0
1
1
0
Blaps mucronata
3
4
0 0 1 0 0 0 0 0 0 0
0
0
0
1
0
0
Catomus rotundicollis
1
1
0 0 0 0 0 1 0 0 0 0
1
1
0
0
0
0
Colpotus strigosus
strigosus
1
1
0 0 0 0 1 1 1 0 1 1
1
1
0
0
0
0
Dendarus coarcticollis
2
2
0 0 0 0 0 0 0 0 0 0
0
1
0
1
0
0
Diaclina testudinea
8
8
0 0 0 0 0 0 0 0 0 0
0
0
0
0
1
0
Diaperis boleti
2
2
0 0 0 0 1 0 0 0 0 0
0
0
1
0
0
0
Gonocephalum
granulatum nigrum
1
1
0 0 0 0 0 0 0 0 0 0
0
0
0
1
0
1
Helops caeruleus
2
2
0 0 0 0 0 0 0 0 0 0
1
0
0
0
0
0
Nalassus dryadophilus
1
1
0 0 0 0 1 1 0 0 0 0
0
0
0
0
0
0
Nalassus planipennis
1
1
0 0 0 0 0 1 0 0 0 0
0
0
0
0
0
0
Opatrum sabulosum
sculptum
1
1
0 0 0 0 0 0 0 0 0 0
0
0
0
0
1
0
Palorus depressus
3
4
0 0 0 0 0 0 0 0 0 0
0
0
1
0
0
0
Pedinus meridianus
2
2
0 0 0 0 0 0 0 1 0 0
0
0
0
0
0
1
Platydema violacea
6
5
0 0 0 0 0 0 0 0 0 0
0
0
0
0
1
0
Scaphidema metallica
2
2
0 0 0 0 1 1 0 0 0 1
0
0
0
0
0
1
Scaurus striatus
1
1
0 1 1 1 0 0 1 1 0 0
0
0
0
1
0
0
Stenosis brenthoides
brenthoides
7
7
0 0 0 0 0 1 0 0 0 0
1
1
0
0
1
0
Stenosis sardoa ardoini
4
3
1 1 0 1 0 1 0 0 0 1
0
1
1
1
0
1
Uloma culinaris
2
2
0 0 0 0 0 0 0 0 0 0
1
0
1
0
0
0
Table includes vulnerability scores (high scores indicate more vulnerable species) for each species on the basis of
the original and modified Kattan index schemes as well as presence (1)/absence (0) per green space. Green space
identification numbers as in Table 1
Urban Ecosyst
Species vulnerability scores
Species conservation concern was expressed as species vulnerability using the Kattan index
(Kattan 1992), which is based on species rarity. I used Kattan values already available for the
tenebrionids of Rome as given in Fattorini (2011a). Therefore, I resume here only the basic
steps used to calculate the Kattan index of each species, because the primary data and a
complete description of both the rationale and the adopted protocols can be found in Fattorini
(2011a).
First, species rarity was assessed using a multidimensional characterisation that takes into
account: (1) geographical distribution (wide/narrow distribution), (2) habitat specificity (broad/
restricted habitat specificity) and (3) abundance (abundant/scarce population). Geographical
rarity was measured as the number of Italian administrative regions from which each species is
known. Habitat specificity was evaluated by assessing species distribution across the 15 main
phytoclimatic units occurring in Latium and defined on the basis of climatic indices and
vegetational settings (the larger the number of phytoclimatic units occupied by a species, the
wider the species’ ecological tolerance). On the basis of the examination of some 1800
museum specimens collected in urban Rome, the number of specimens collected for each
species was considered as a measure of local rarity, assuming contactability as a proxy for
population size. Then, for each of these three rarity measures, species were dichotomised into
two groups (common and rare) according to whether they were above or below the median.
Finally, using Kattan’s approach, an eight-score scale was created that reflected different types
of rarity and commonness, and each species was assigned to a score as follow: 1: species that
are not rare; 2: scarce species (i.e. species rare for abundance); 3: species with narrow habitat
specificity; 4: restricted species (i.e. species rare by range); 5: scarce species with narrow
habitat specificity (i.e. species rare for both habitat specificity and abundance); 6: scarce and
restricted species (i.e. species rare for both geographical range and abundance); 7: restricted
species with narrow habitat specificity (i.e. species rare for both habitat specificity and
geographical distribution); 8: restricted and scarce species with narrow habitat specificity
(i.e. species rare for geographical distribution, habitat specificity and abundance).
This weighting scheme assigns higher importance to geographical rarity. This is appropriate
at global and regional scales, because species with a narrow geographical distribution are more
vulnerable at a global or regional level (e.g. endemics) (Kattan 1992). At a local scale,
however, this approach may be questioned, because the probability of persistence of a species
in a given site is more strongly influenced by its ability to adapt to changing environmental
conditions, and hence by its ecological tolerance: the wider the ecological tolerance of a
species, the higher its chances to find suitable biotopes in a changing landscape. For this
reason, a modified scale of values was also used, changing scores 3–6 as follows: 3: restricted
species; 4: species with narrow ecological tolerance; 5: scarce and restricted species; 6: scarce
species with narrow ecological tolerance. These changes gave more importance to ecological
tolerance than to range.
For Diaclina testudinea, a species not considered in Fattorini (2011a) but found in one of
the green spaces considered here, a Kattan value of 8 was used because it is a geographically
very rare species, known from few specimens and ecologically strictly associated with relicts
of mesophilic woodlands.
Green space ranking
Green spaces were ranked on the basis of the vulnerability of their tenebrionid communities.
For this, two different measures of prioritisation, the Biodiversity Conservation Concern
Urban Ecosyst
(BCC) index (Fattorini 2006), and the Biodiversity Conservation Weight (BCW) index
(Fattorini et al. 2012a), were used. In the BCC index, species occurring in a given area are
classified into categories of endangerment and weighted by the respective vulnerability. The
BCC index also combines the vulnerability of each species with total richness to obtain a
measure of relative conservation.
The BCC can be calculated as:
L
X
BCC ¼
ðαi −αmin Þ
i¼1
Lðαmax −αmin Þ
ð1Þ
where L is the local species richness, αi is the weight assigned to the ith category of vulnerability
(as defined above), αmin is the minimum weight among all species; and αmax is maximum weight
among all species. This formulation ensures the index ranges from 0 (all species belonging to the
lower conservation category, α1 =1) to 1 (all species belonging to the highest endangerment
category, αmax =8). The BCC index has been previously applied to identify priority areas or
biotopes for butterflies in Mediterranean islands and European countries (Fattorini 2006, 2009;
Dapporto and Dennis 2008), fish in France (Bergerot et al. 2008; Laffaille et al. 2011), tenebrionids, butterflies, birds and mammals in the Central Apennines (Fattorini 2010a, b), and
arthropods in Azorean forest fragments (Fattorini et al. 2012a).
The BCC index is a ‘relative measure’, which means that it is not sensitive to species
richness. This may be an advantage to compare species assemblages with different species
richness (Fattorini 2006, 2010b), but poses some problems. For example, an assemblage with a
single species, having this species αmax, would receive the same score as an assemblage with 10
species, all with αmax. Or worse, an assemblage with a single species with αmax would receive a
higher score than an assemblage with 10 species, 9 with αmax and one with αi <αmax. The BCW
index was introduced to overcome these problems, but it is dependent on species richness.
The BCW can be calculated as:
L
X
BCW ¼
i¼1
S
X
ðαi −αmin Þ
ðαi −αmin Þ
i¼1
where S is the total species richness for all sites (other symbols are as in the BCC).
In general, an absolute index like the BCW might be preferable to prioritise the areas with
the highest numbers of vulnerable species, but a relative index like the BCC may help the
identification of areas with few, but highly imperilled species. Thus, the BCC and the BCW
should be used in tandem for a ‘balanced’ overview of conservation priorities (Fattorini et al.
2012a).
BCC and BCW indices were calculated using both the original and the modified version of
the Kattan index of species vulnerability. Values of BCC index obtained for urban green spaces
were compared with those recorded for the tenebrionids, butterflies, birds and mammals of
Apennine biotopes (data extracted from Fattorini 2010a,b) and the arthropods of a very
different ecosystem, the forest fragments of the Azorean Islands (data extracted from
Fattorini et al. 2012a). In particular, Mann–Whitney U tests were used to test if median values
of BCC values obtained for urban green spaces were significantly different from those
recorded in more natural systems.
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Correlations between BCC and BCW values with green space characteristics were investigated using Spearman’s non parametric correlation coefficients. To test if BCC and BCW
values varied according to green space types (villas, archaeological sites and natural
parks), a non parametric Kruskal-Wallis ANOVA was adopted. All tests were twotailed, with α set at 0.05.
Results
Use of the original or modified version of the Kattan index gave only slightly different results
(Table 1). The BCC index calculated with the original version was strongly correlated with that
obtained using the modified version (rs =0.970, p<0.00001). An even stronger correlation was
found between the BCW index calculated with the original version and that obtained using the
modified version (rs =0.993, p<0.00001). Thus, only results for the original version of the
Kattan index will be discussed.
BCC values ranged from 0.048 to 0.429 (mean value ± SE: 0.215±0.028). BCW values
ranged from 0.024 to 0.414 (0.181±0.029). BCC and BCW indices were strictly correlated
(rs =0.839, p<0.00001).
Correlations of BCC and BCW indices with green space characteristics revealed significant
relationships only for the mean distance from adjacent areas (rs =−0.653, p=0.006 for BCC;
rs =−0.579, p=0.019 for BCW).
BCC and BCW values did not vary significantly among green space types (Kruskal-Wallis
ANOVAs: H=1.296, p=0.523 for BCC; H=2.766, p=0.251 for BCW).
Comparative analyses with Apennine biotopes showed that urban tenebrionids had
significantly higher BCC values than Apennine tenebrionids (U=92.5, Z=−2.315, p=
0.020), birds (U=73.0, Z=−2.912, p=0.003) and mammals (U=88.0, Z=−2.452, p=
0.014), and similar values to those of Apennine butterflies (U=116.0, Z=−1.594, p=
0.111). BCC and BCW values obtained from Rome green spaces were also compared
with those found in 16 forest fragments on the Azorean Islands. The tenebrionid beetles
of urban Rome had lower median values (18 sampled forests) than those of the Azorean
arthropods for both the BCC (U=48, Z=3.312, p=0.001) and the BCW (U=84, Z=
2.070, p=0.038) when all Azorean endemics were considered as geographically rare
species. By contrast, when only single island endemics were considered as geographically rare species, urban tenebrionids had a higher median BCC value (U=45, Z=3.416,
p=0.0006), whereas no significant differences was observed for the BCW index (U=113,
Z=−1.070, p=0.285).
Discussion
The two indices used to prioritise urban green spaces, i.e. the BCC and BCW indices, gave
very similar results, even when different species vulnerability scores were used. Although the
BCW was significantly influenced by species richness, the two indices gave very similar site
rankings. In particular, three green spaces were consistently recovered as the highest priority
sites: a natural park (Cervelletta), and two archaeological sites (Palatino and Colle Oppio).
Cervelletta is one of the few relicts of the wetlands that occurred in Rome area before extensive
urbanization. This area is known to host a rich flora and fauna. For example, eighteen species
of Diptera Stratiomyidae (20.7 % of the entire Italian fauna) were collected from here,
including several species associated with endangered microhabitats and one previously
Urban Ecosyst
unrecorded from Italy (Mason and Mei 2002). This area, which is part of the Aniene natural
park, also hosts a large number of scarabaeid and carabid species (Fattorini, unpublished data).
The two archaeological sites of Palatino and Colle Oppio are two close green spaces used as
urban parks and occupied by some of the most famous Roman ruins, such as the Colosseum,
the Arch of Costantine, the Domus Aurea, the Forum Romanum, the Flavian Palace, and the
Domus Livia. In their recent review of urban green spaces, Hunter and Hunter (2008) cite a
number of categories of urban habitats useful for insect conservation, spanning from private
gardens to abandoned industrial areas, without reference to archaeological sites. The results
obtained in this research support the call for considering the importance of archaeological sites
in insect conservation (Fattorini 2011a). Archaeological sites are not rare in many ancient
cities, and they are already protected in virtue of their historical importance. Thus insect
conservation measures in these areas would be easy to adopt.
In a study on the conservation value of Apennine biotopes for various animal groups using
the BCC index (Fattorini 2010b), the highest mean value of BCC scores was recorded for
butterflies (mean BCC±SE=0.158±0.031), followed by tenebrionids (0.135±0.044), mammals (0.126±0.028) and birds (0.116±0.028). The biotopes with the highest BCC values were:
(1) pastures (for tenebrionids BCC=0.538; for butterflies BCC=0.367); (2) bare rocks (for
tenebrionids BCC=0.701; for butterflies BCC=0.449; for mammals BCC=0.333); and (3)
inland wetlands (for birds BCC=0.391; for mammals BCC=0.429). Thus, BCC values of the
tenebrionid beetles of Rome green spaces are similar to those of the tenebrionids of Apennine
biotopes, and the highest BCC values for Rome tenebrionids were similar to the highest scores
recorded in natural biotopes. Moreover, the tenebrionids of urban green spaces in Rome had
values of BCC and BCW lower than those of the arthropod communities in natural forest
fragments in a true island system, the Azorean Islands (Fattorini et al. 2012a), only when a
broad definition of species geographical rarity was used for island species. All these comparative observations lead to the general conclusion that the tenebrionid assemblages of Rome
green spaces have conservation values not only similar to those of tenebrionids and other
animal groups in natural biotopes on the Apennines, but also similar to those recorded for
arthropods from relict forests on oceanic islands. While the conservation value of urban green
spaces has been questioned (Battisti and Gippoliti 2004) and high species richness in urban
areas have possibly been attributed to the presence of ubiquitous species (McKinney and
Lockwood 1999; McKinney 2006), use of BCC and BCW indices highlighted the actual
importance of green areas for insect biodiversity conservation.
The present paper is the first that attempted to relate BCC (and BCW) indices to area
characteristics. Both indices were negatively correlated with the distance from adjacent green
spaces, which means that more isolated sites host species assemblages of lower biodiversity
conservation interest. This points to the importance of maintaining and possibly enhancing
connectivity among green spaces for preserving the most vulnerable species. The possible
underlying mechanisms responsible for the importance of a reduced distance among green
spaces were not explored in this study, but inter-site proximity is known to facilitate dispersal
of immigrants, provide more suitable environments, and reduce the effects of genetic isolation
(Davis 1979; Thomas et al. 2000; Davies et al. 2001; Magura et al. 2001).
Surprisingly, all other relationships of BCC and BCW with area characteristics were
insignificant. These results strongly contrast with common prescriptions about area size and
shape for reserve design (reviewed in Pullin 2002 and Laurance 2010). For the tenebrionids of
Rome, even small areas may host species assemblages of few, but vulnerable species of high
conservation concern, which makes BCC and BCW values independent from area size. The
lack of correlation with the percentage of forested area can be explained by the ecological
setting of Rome area. Previous studies in urban ecology that have showed the importance of
Urban Ecosyst
forest size and shape for various animal groups (Andrén 1994; Fahrig 1997; Donnelly and
Marzluff 2004) have been conducted in areas where cities grew into agricultural and forested
landscapes (e.g. Breuste et al. 2013; Kotze et al. 2012; Schiller and Horn 1997; Heneghan et al.
2012). By contrast, urban Rome is placed in the Mediterranean biome, and the landscape
predating modern urban expansion was mainly composed of a mosaic of wild grazing,
grasslands, cultivated plots and Mediterranean maquis, with few patches of true forests
(Fattorini 2011a,b). Thus, the “pristine” vegetation in urban Rome was a mosaic of open
habitats, more than forests, and most of the species that composed the “original” tenebrionid
fauna in Rome area were not strictly associated with forest habitats. Moreover, the tenebrionids
of Rome include both species associated with arid and sandy soils (such as Tentyria italica,
Gonocephalum spp., Opatrum sabulosum and Cossyphus tauricus), which can be considered
urban avoiders, and species associated with ruderal and archaeological sites (such as Asida
luigionii, Scaurus striatus, Akis bacarozzo, Blaps spp.), which can be considered as urban
adapters (see Fattorini 2011a). The presence of species with opposite responses towards the
urban-rural gradient may explain the lack of relationship between conservation concern values
and urbanization.
In the Mediterranean basin, tenebrionids tend to be an important component of the
urban fauna. For example, a rapid survey in Athens (Greece) in summer 2005
revealed the occurrence of many tenebrionid beetles in several archaeological sites,
whereas a short sampling in a ruderal site in Alicante (Spain) in summer 2013 led to
the collection of four species in a space of about 100 m2 with 10 min hand searching.
Thus investigations in other Mediterranean cities might produce results comparable
with those obtained in Rome and might be useful to offer recommendations for insect
conservation in urban contexts.
On the whole, the results obtained in this study indicate that the conservation importance of
green spaces cannot be predicted on the basis of their geographical characteristics, but must be
established on the basis of the species that they actually host. The results obtained in this study
are based on a single animal group, whereas the identification of priority areas should include
cross-taxon analyses (Fattorini et al. 2011, 2012b). However, the idiosyncratic patterns found
in this study demonstrate the need for detailed fieldwork to assess the actual distribution of
hotspot green spaces in urban areas, whose location cannot be predicted on theoretical
grounds.
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