Occurrence patterns of alien freshwater turtles in a large urban pond 'Archipelago'(Rome, Italy): Suggesting hypotheses on root causes

Occurrence patterns of alien freshwater turtles in a large
urban pond ‘Archipelago’ (Rome, Italy): Suggesting
hypotheses on root causes
Maria Paola Di Santo,1
Leonardo Vignoli,2
Giuseppe M. Carpaneto2
and Corrado Battisti3*
1
Xemina - emozioni in natura Cultural and Environmental Association, 2
Dipartimento di Scienze, University of ‘Roma Tre’,
and 3
‘Torre Flavia’ LTER (Long Term Environmental Research) Station Environmental Service, Citta Metropolitana di
Roma Capitale, Rome, Italy
Abstract
The patterns of the occurrence and distribution of alien freshwater turtle species in an urban pond archipelago (Rome,
Italy) were analysed, with the aim of exploring the role of a set of factors (type of ponds, landscape context, size area,
distance from the nearest road) with a generalized linear model approach. A total of 311 ponds subdivided in three types
(fountains, small basins, lakes) embedded in different landscape contexts (public parks, private parks, urban areas) at dif-
fering distances from the nearest road were sampled. Six non-native freshwater turtle species in 31 sites were recorded
(9.97%). Lakes exhibited the highest occurrence rates of alien freshwater turtles, compared to small basins and fountains.
Freshwater turtle species in urbanized areas were only observed in parks (both public and private). In both the public
and private parks, the lakes exhibited the highest percentage of occupied sites, with fountains being the lowest. A direct
and significant relationship was observed between pond size and species richness. The distance from the nearest road
did not appear to affect species richness. A first interpretation of the data from this study facilitated the postulation of
two a posteriori hypotheses that should be tested, as follows: (i) the causal process of turtle release is random, and the
rate of extinction (and recapture) is higher in smaller ponds, thus producing the observed pattern; and (ii) the turtle
release is not random, and people actively select the ponds they consider more suitable for their pet animals. In this
study, it appears the lakes were perceived by those who abandon their pets as the most ecologically suitable habitats
among other pond types to accommodate the different species of turtles. Knowledge of people’s attitudes in regard to
releasing pet animals also might assist managers of public green spaces to develop strategies aimed to preserve local bio-
diversity, and to educate the public about the conservation issue represented by the alien species.
Key words
alien species, artificial water bodies, Italy, roads, urban parks.
INTRODUCTION
Artificial water bodies (AWBs) represent multifunctional
habitats that can host resources important for the conser-
vation of many plant and animal species (Gledhill et al.
2004; Di Santo et al. 2015). They also often represent a
suitable habitat in urbanized landscapes for many alien
vertebrates and invertebrates (Burgin 2006; De Lathou-
der et al. 2009; van Ham et al. 2013). In fact, lack of
predators, large availability of food and space resources,
and human behaviours may facilitate natural or anthro-
pogenic colonizations and invasions of AWBs (Marzluff
2008).
Freshwater turtles have an important ecological role
among alien species in aquatic ecosystems. They are gen-
erally held as pets. However, upon growing to large size,
they are often released into the wild in any type of wet-
land, especially in suburban and urbanized areas (Pio-
vano Giacoma 1999; Cadi et al. 2004; Perry et al. 2007;
Teillac-Deschamps et al. 2008; Masin et al. 2014). Thus, a
dramatic and increasing colonization process by alien tur-
tle species is occurring worldwide (Da Silva Blasco
1995; Petterino et al. 2001; Ficetola et al. 2002; Lever
*
Corresponding author: Email: c.battisti@cittametropolita
naroma.gov.it
Accepted for publication 8 February 2017.
Lakes and Reservoirs: Research and Management 2017 22: 56–64
© 2017 John Wiley Sons Australia, Ltd Doi: 10.1111/lre.12164

2003; Pati~no-Martınez Marco 2005; Chen 2006; Pupins
2007; Gherardi et al. 2008).
The occurrence of alien turtle species in wet Mediter-
ranean areas constitutes a direct and indirect threat for a
large set of native species (e.g. turtles, water-related
birds, aquatic invertebrates, plants) (Soccini Ferri
2004; Teillac-Deschamps et al. 2008). The situation as
related to turtle invasion in AWBs may represent a minor
threat because these habitats undergo recurrent human-
induced disturbances and, consequently, typically host
poor biological assemblages and a lack of native species
of conservation concern (e.g. for birds, see Di Santo et al.
2015). Nevertheless, the presence of alien species in
urban ecosystems represents a potential threat to local
biodiversity, noting urban ponds may act as source of
colonist individuals that may disperse in suburban ponds
containing native species of conservation concern (Mar-
zluff 2008), thereby facilitating biotic homogenization
(Dar Reshi 2014). Moreover, ponds in recently urban-
ized areas may host relict or isolated populations of
native vertebrates and invertebrates of ecological interest
(Chovanec 1994; Vermonden et al. 2009; Vignoli et al.
2009, 2013).
Research on the occurrence and richness of alien
freshwater turtles in urban wet ecosystems is very
sparse, especially for the Mediterranean area. To this
end, this study analyses the pattern of occurrence and
distribution of alien freshwater turtle species in a large
set of ponds of different types embedded in an urbanized
landscape context (Rome, Italy). A particular goal is to
analyse the role of a set of selected factors (i.e. type of
AWB, landscape context, AWB area, distance from the
nearest road) that might help us better understand the
pattern of occurrence and richness of these reptiles in an
urban pond archipelago. As the occurrence of non-native
species in urban freshwater pond is the priority (Masin
et al. 2014), some management recommendations based
on a DPSIR approach also are presented (Kristensen
2004).
MATERIALS AND METHODS
Study area
The study area corresponds to the urban and suburban
sector of Rome and covers an area of about 36 000 ha.
Located at a mean altitude of 20 m a.s.l., about 46% of
this urbanized landscape is occupied by building areas
(about 16 500 ha), 48% by public and private parks and
green areas (about 17 300 ha), and 6% represents the
alluvial areas surrounding the Tiber and Aniene rivers
(about 2000 ha) (Zapparoli 1997; Zapparoli et al. 2003).
A total of 311 AWBs were located in the study area,
based on a regional map (scale 1:10 000), satellite images
(software Google Earth 5.1), personal communications
and local knowledge (Fig. 1). The recorded AWBs were
categorized into three water basin types, as follows:
1 Fountains (FO) – very small artificial ponds with
cemented edges, and a continuous or semi-continuous
artificially induced (i.e. mechanically by pumps) water
flow (average surface area of 0.005 ha Æ 0.011;
n = 203);
2 Small basins (SB) – small artificial ponds with
cemented edges, with scarce or absent water flow (aver-
age surface area of 0.01 ha Æ 0.01; n = 54); and
3 Lakes (LA) – relatively large ponds with semi-nat-
ural vegetated edges (average surface area of
0.59 ha Æ 1.27; n = 54).
These artificial or semi-natural ponds are further
embedded in three different landscape contexts, as fol-
lows:
1 Public parks (PuP) – public green areas with vege-
tation surrounding the ponds (at least 1 ha in size),
which are freely accessible by citizens (n = 130);
2 Private parks (PrP) – green areas or areas with
vegetation in the surrounding (at least 1 ha in size), and
with controlled access allowed only for scientific research
purposes (n = 110); and
3 Urbanized areas (Urb) – urban areas with little or
absent vegetation in their surroundings (i.e. only ruderal
herbaceous plant species are present in low densities).
Green (private or public) parks are isolated (300 m
far from the nearest park) and enclosed by buildings and
roads, the latter characterized by heavy vehicular traffic
and pedestrian traffic (n = 71).
Protocol
A single researcher (MPDS) carried out a periodic sam-
pling of each pond from July to September 2009, walking
along their shores. There was a total of approximately
300 h of sampling (about 1 h for large ponds [0.5 ha];
about 30 min for small ponds [0.5 ha]). Sampling was
carried out between 1100 and 1300 hours. There was a
higher detection probability for aquatic reptiles during
the hottest hours (Blomberg Shine 2006).
The occurrence of individuals belonging to alien fresh-
water turtle species was recorded for each pond, based
on their capture (and subsequent release after taxonomic
diagnosis) or on the direct observation of individuals. A
fishing net with 2 m stiff rod was used to capture the ani-
mals. Limited visual sampling was used only to confirm
the occurrence of species that were easier to detect and
classify (Trachemys). The size of each pond was
Alien freshwater turtles in urban ponds 57
© 2017 John Wiley Sons Australia, Ltd

measured (A, in ha), as well as the distance (Dist, in m)
from the nearest road. These measures were obtained
utilizing Google Earth 5.1 software for the larger ponds.
For the smallest ponds (0.01 ha), the radius (if of circu-
lar shape), or the two axes and perimeters (if of elliptic
or irregular shape), was calculated, using a measuring
tape Komelon (Æ1 cm; max length 3.5 m) for the smaller
ponds (0.01 ha). Data reliability was checked using the
approach of Battisti et al. (2014). The following checks
were carried out to further improve reliability: (i) stan-
dardization (using a comparable method for all the study
sites); (ii) data independence (each AWB being an inde-
pendent sample); (iii) detectability (the researcher did
training with senior experts); (iv) replication (a survey
was carried out on a large number of ponds); and (v)
stratification (data were stratified for water basin types
and landscape contexts; see above). Ernst and Lovich
(2009) and Francis (2012) were referred to for taxonomic
diagnoses.
Data analysis
The pattern of turtle species occurrence was modelled by
means of the generalized linear model procedure (McCul-
lagh Nelder 1989). Two models were constructed by
selecting the occurrence of the various species (binomial
distribution and log-link function) and the turtle species
richness in AWBs (Poisson distribution log-link function)
as dependent variables. The type of pond type and the
landscape context were included in the model as factors
(categorical predictors). The pond area and the distance
from the nearest road were used as covariates (continu-
ous variable) to reduce the within-group error variance,
allowing a more accurate assessment of the effects of the
categorical predictors, as well as removing the bias of
confounding variables (i.e. the distance from the nearest
road), thereby possibly influencing the dependent vari-
able. The model design included the main effects for
each variable, and the interactive term between the
categorical factors (McCullagh Nelder 1989). The
Fig. 1. Map of Rome (Italy) metropolitan study area (artificial water bodies (AWBs) presented as circles; empty circles indicate absence of
freshwater alien species; black circles indicate the presence of at least one species; dark grey areas indicate urbanized areas; grey areas indi-
cate public and private parks; white areas indicate non-urbanized areas; black line indicates Great Ring Highway).
58 M. P. Di Santo et al.

non-parametric Spearman rank correlation test (two-
tailed) was performed to compare the pond size areas
and both the distance from the roads and the number of
turtle species. All the statistical analyses were performed
with Statistica software (Statsoft, v. 8.0), with the alpha
value set to 5%.
RESULTS
Freshwater turtles were detected (i.e. at least one individ-
ual of a species) in 31 sites of the 311 sampled urban
ponds (9.97%; Table 1; Fig. 1). Six non-native species
belonging to two families, Emydidae with ﬁve species,
Trachemys scripta (three subspecies), Pseudemys nelsoni,
P. concinna, Graptemys pseudogeographica, G. kohni. and
Trionychidae with one species, Apalone spinifera, were
observed. T. scripta was the dominant species occurring
in all the 31 AWBs in the study system, where we found
at least one turtle species (both ssp. elegans and ssp.
scripta in 24 ponds, and ssp. troostii in three ponds);
Pseudemys nelsoni, P. concinna, G. pseudogeographica, and
Table 1. Occurrence pattern of alien freshwater turtle species in urban ponds of Rome, Italy
Type Land A Dist T.s. P.n. P.c. G.p. G.k. A.s. S
LA PuP 1.74 28.91 1 0 0 1 0 0 2
LA PuP 0.13 122.18 1 1 1 1 0 0 4
LA PrP 0.046 13.62 1 1 0 0 1 0 3
SB PrP 0.0032 6.02 1 0 0 0 0 0 1
LA PrP 0.05 17.94 1 0 0 0 0 0 1
SB PrP 0.09 34.9 1 0 0 1 0 0 2
LA PuP 0.19 372.09 1 0 0 0 0 0 1
LA PuP 0.002 358.64 1 0 0 0 0 0 1
FO PuP 0.002 35.6 1 1 0 0 0 0 2
LA PuP 1.18 25.12 1 0 0 0 0 0 1
FO PrP 0.004 78.05 1 0 0 0 0 0 1
LA PuP 8.5 10.48 1 0 0 0 0 0 1
SB PrP 0.003 134.63 1 1 0 0 1 0 3
LA PrP 0.039 109.9 1 0 0 0 0 0 1
LA PrP 0.013 175.61 1 0 0 0 0 0 1
SB PrP 0.001 59.01 1 0 0 0 0 0 1
SB PrP 0.001 99.76 1 0 0 0 0 0 1
SB PrP 0.001 92.99 1 0 0 0 0 0 1
LA PrP 0.001 13.41 1 0 0 0 0 0 1
FO PrP 0.001 42.01 1 0 0 0 0 0 1
LA PuP 3.8 279.45 1 0 0 0 0 0 1
LA PuP 0.09 113.67 1 0 0 0 0 0 1
SB PrP 0.001 32.28 1 0 0 0 0 0 1
LA PuP 1.3 96.87 1 0 0 0 0 0 1
LA PuP 0.43 11.08 1 0 1 0 1 0 3
LA PuP 0.7 91.12 1 0 1 1 0 1 4
SB PrP 0.001 19.97 1 0 0 0 0 0 1
LA PuP 1.6 246.81 1 1 1 1 1 1 6
LA PuP 0.09 145.04 1 0 0 0 1 0 2
SB PuP 0.03 132.43 1 0 0 0 0 0 1
SB PuP 0.03 16.53 1 0 0 0 0 0 1
Total 31 5 4 5 5 2
T.s., Trachemys scripta; P.n., Pseudemys nelsoni; P.c., P. concinna; G.p., Graptemys pseudogeographica; G.k., G. kohni; A.s., Apalone spi-
nifera; Type, pond type; Land, landscape context; A, size area; Dist, distance from nearest road, S, number of alien freshwater turtle spe-
cies; see Methods for further abbreviations.

G. kohni were found in five ponds; Apalone spinifera
occurred in two ponds (Table 1). The maximum number
of recorded species in a single AWB was six.
As for the AWB type, LAs exhibited the higher per-
centage of occupied sites (33.33%), compared to SBs
(18.52%) and FOs (1.48%). As for the landscape context,
freshwater turtle species were only observed in ponds in
the public and private parks. In these selected contexts,
LAs exhibited the highest percentage of occupied sites,
and FOs the lowest.
The pattern of occurrence (presence/absence) and
species richness of the turtles in the studied ponds were
affected solely by the type of pond, with the LAs category
exhibiting a higher occurrence and richness of turtle spe-
cies than the FOs (generalized linear models; Table 2).
The area and distance of the AWBs from the nearest
road did not exhibit any effects on the occurrence or the
richness of turtle assemblages.
DISCUSSION
A specific pattern of occurrence was observed in the
urban pond archipelago in the present study. At the sin-
gle species level, the largest number of sites at which
Trachemys scripta was observed could reflect the large
diffusion of this species as the most popular pet turtle in
Southern Europe (Perez-Santigosa et al. 2008). Moreover,
at the assemblage level, the highest occurrence rates of
non-native freshwater turtles were observed in lakes,
compared to small basins and fountains. Assuming the
presence of non-native turtles in artificial ponds is attribu-
ted primarily to direct release by humans (evidence for
their reproduction is very rare in urban ponds, at least in
the European context; Ficetola et al. 2002; Cadi et al.
2004; Dordevic Andelkovic 2015), and that dispersal
among sites is limited or absent (due to a strong urban
barrier effect and road-killing; Gibbs Shriver 2002;
Steen Gibbs 2004; Andrews et al. 2008; van Harn et al.
2013), two hypotheses about the processes behind this
pattern can be developed.
The first hypothesis may provide a random process of
turtle release by humans, independent of pond size. It is
probable that when single individuals are stochastically
released in urban ponds, they might survive over the
medium-long term only in larger ponds. Indeed, although
it has been observed that invasive freshwater turtles are
also highly adaptable under stressed contexts (Cadi et al.
2004; Polo-Cavia et al. 2011), they exhibit a higher natu-
ral resource availability, and consequently a higher proba-
bility of medium-long-term survival in larger ponds. All
the species have a similar ecology. In their native ranges
(North America, excluding Apalone spinifera, which also
occurs in Central America), they inhabit a variety of
freshwater habitats with abundant vegetation, including
ponds and lakes (Ernst Lovich 2009; Francis 2012).
Secondly, larger ponds might attract more people (e.g.
for aesthetic reasons or as key sites for children; Battisti
2016), so that animals may receive supplementary food
resource from humans in these areas (Bujes 2009). In
this latter case, a positive feedback between people and
non-native turtles might arise (i.e. larger ponds ? higher
habitat suitability ? attractive sites for people ? food
intake ? further increase in habitat suitability).
Conversely, the process of local extinction might be
non-random, but also skewed towards smaller ponds
where the lower habitat heterogeneity and an unstable
water regime may present unsuitable conditions for tur-
tles. Moreover, individuals may be easily recaptured in
small basins and fountains. These two factors (i.e. low
quantity of spatial and food resources and a high recap-
ture rate), and the consequential process (local extinc-
tion), may explain the low occurrence rate of these
turtles in small ponds. As extinction from smaller ponds
is likely due to a contingent event, this process of pro-
gressive disappearance of released groups of individuals
in smaller ponds is different from the classic process of
local extinction of native populations that occurs when
Table 2. Synopsis of generalized linear model results, illustrating
only pond type among the studied parameters significantly influ-
encing the occurrence pattern and species richness of turtles in
study area
Type III Wald v2
d.f. P
Species occurrence
Intercept 35.92 1 0.0001
Type 17.053 2 0.0001
Landscape 0.299 1 0.584
Area 1.268 1 0.26
Distance 1.466 1 0.226
Type 9 Landscape 0.821 2 0.663
Species richness
Intercept 34.867 1 0.0001
Type 31.945 2 0.0001
Landscape 0.001 1 0.975
Area 0.481 1 0.488
Distance 3.176 1 0.075
Type 9 Landscape 1.879 2 0.391
Type, AWB type; landscape, landscape context; distance, dis-
tance from nearest road; area, AWB size.

spatially structured (meta) population dynamics occur in
non-urban landscapes (Gibbs 1993; Sinsch 2014).
A second hypothesis may provide that the process of
turtle release is not random. Larger ponds (lakes), for
example, may be perceived by those who abandon ani-
mals as the most ecologically suitable habitats among
other pond types to accommodate the undesired pet tur-
tles. Braun (2002) also suggested that people, although
having no biological background, might nevertheless rec-
ognize the naturalness and suitability of a habitat (e.g. a
pond type) for a pet species (a non-native freshwater tur-
tle in this case).
Terrestrial habitats surrounding isolated wet habitats
are essential elements for enhancing biodiversity (Gib-
bons 2003). In the case of the present study, larger ponds
also may be more suitable for non-native turtles because
they are usually embedded in green areas (i.e. urban
parks). Thus, green areas surrounding lakes may provide
further resources that facilitate their survival in these
sites (see Ryan et al. 2008). Long-term research on non-
urban isolated wetlands reveals two terrestrial habitats
contiguous with it (i.e. terrestrial periphery; terrestrial
corridors that connect isolated wetlands) are vital for
most animal communities (Gibbons 2003; Guzy et al.
2013). Although vegetated corridors and ecotones proba-
bly do not play a local role in dispersal processes among
sites because of the strong effect of the urbanized matrix,
these habitats may represent a key spatial resource that
allows turtles to survive outside the AWBs over the med-
ium-long term.
The role of urban parks with large lakes has also been
emphasized for several vertebrate groups (e.g. see
Martınez-Arroyo Jauregui 2000; Vignoli et al. 2013; Di
Santo et al. 2015). Among reptiles, these urban ecosys-
tems also may host remnant populations (or isolated
introduced individuals) of native turtle species (e.g. Emys
orbicularis; Vignoli et al. 2009; Di Santo, personal obser-
vations). In this sense, the observed spread occurrence
of a large number of non-native turtles in ponds in which
native species also exist may represent a conservation
problem in urbanized landscapes due, for example to
competition for basking sites, or aggressive interactions
during feeding (Cadi Joly 2003a,b; Polo-Cavia et al.
2011).
The larger the size of the AWB, the greater is the spe-
cies richness hosted. This is an expected result as, with
increasing pond size, there should also be a parallel
increase in habitat heterogeneity and resource availabil-
ity, with a higher number of niches potentially available
(Baldi 2007; Allouche et al. 2012; Stein et al. 2014) which
might allow the colonization and permanence of a larger
number of freshwater species (Chovanec 1994; Knight
1997; Gaston et al. 2005; Chamberlain et al. 2007).
It was hypothesized that a AWB closed to the roads
may facilitate the occurrence of people intending to
release their pets. The distance of the AWB from the
nearest road, however, did not appear to affect the
chance of observing turtles at a given site. It may be,
therefore, that the decisive factors inducing people to
select suitable ponds for releasing their pets are not
linked simply to the distance from the nearest road.
Thus, as hypothesized, they could actively select sites
that may ensure long-term viability of their animals.
The present study represents the first large-scaled
data framed from an archipelago of urban ponds located
in a metropolitan context, at least for the Mediterranean
area. A first interpretation of the data allowed the postu-
lation of two a posteriori hypotheses that should be
tested in further research efforts (i.e. inductive
approach; Romesburg 1981; Guthery 2007). The first
hypothesis is that the causal process of turtle release is
dominated by stochasticity, with the rate of extinction
(and recapture) being higher in smaller ponds, thereby
producing the observed pattern. For this scenario, the
assumption is that people similarly consider the different
type of ponds (in terms of size, location and suitability
for turtles), with the turtle survival being the key deter-
minant of the observed pattern of turtle distribution
among AWBs. The second hypothesis is that turtle
release is not random and that people actively select the
ponds they consider more suitable for their pet animals.
In this latter case, the lakes are perceived by people
who abandon their pets as the ecologically most suitable
habitats among the other pond types to accommodate
the different turtle species. The lack of a significant
response between occurrence of turtles and the distance
of AWBs from the neighbouring road might support this
second hypothesis.
Although our data may be affected by some bias (e.g.
different detectability among species; stochastic pattern
in turtle release from people not intercepted by the sam-
pling design of the present study), this first effort regard-
ing occurrence and richness patterns will help support
the efficiency of the sampling scheme directed to man-
agement. Moreover, these data suggested two hypothe-
ses that should be tested in the future. These further
analyses on the root causal processes might facilitate the
ability of managers of public green spaces in develop-
ment strategies aimed to preserve local biodiversity and
to educate the public about the conservation issue repre-
sented by the alien species (L€ofvenhaft et al. 2002; Teil-
lac-Deschamps et al. 2009).

In conclusion, the following management recommen-
dations aimed to control the problem with this invasive
species in urban ponds, following a DPSIR approach (i.e.
driving force-pressure-state-impact-responses; Kristensen
2004), are presented. The first, considering driving forces
(e.g. illegal trade at regional/national scale; people releas-
ing turtles at local scale), improved specific regulations,
control, communication and education efforts directed to
increasing the awareness of the impact of these species
on native biodiversity is suggested. In this sense, fresh-
water species might be considered experiential key spe-
cies (Battisti 2016); that is, species useful to promote pro-
environmental behaviours through the communication of
their impacts. The second, considering pressures, an
eradication effort should be promoted by public agencies
at the scale of single AWBs. Such actions could be devel-
oped together with educational measures with schools,
and animals could be translocated in areas where they
cannot escape into the wild (see Ferri Soccini 2008).
The third, considering responses (i.e. operational man-
agement actions), is to use a set of indicators (e.g. num-
ber of eradicated ponds; number of captured animals)
might be used to monitor the state of these species (i.e.
occurrence and density) and the effectiveness of eradica-
tion actions (assessing the outcomes of conservation pro-
ject Hockings et al. 2000).
ACKNOWLEDGEMENTS
We thank all the people who facilitated the realization of
this study. Special thanks is given to Marianna Di Santo,
Prof. Bernardino Romano and Dr. Ph.D. Francesco Zullo
(DAISEE – GIS team, University of L’Aquila) for helping
us elaborate Figure 1. Two anonymous reviewers, and
the editor in chief Walter Rast, provided useful comments
and suggestions that largely improved the first draft of
the manuscript.
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