Occurrence patterns of alien freshwater turtles in a large urban pond 'Archipelago' (Rome, Italy): S by M. P. Di Santo

Lakes and Reservoirs: Research and Management 2017 22: 56–64

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

mina - emozioni in natura Cultural and Environmental Association, 2Dipartimento di Scienze, University of ‘Roma Tre’, Xe and 3‘Torre Flavia’ LTER (Long Term Environmental Research) Station Environmental Service, Citt a 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 differing 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 biodiversity, 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 conservation 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 Lathouder et al. 2009; van Ham et al. 2013). In fact, lack of predators, large availability of food and space resources, *

Corresponding author: Email: c.battisti@cittametropolita

naroma.gov.it Accepted for publication 8 February 2017.

and human behaviours may facilitate natural or anthropogenic colonizations and invasions of AWBs (Marzluff 2008). Freshwater turtles have an important ecological role among alien species in aquatic ecosystems. They are generally held as pets. However, upon growing to large size, they are often released into the wild in any type of wetland, especially in suburban and urbanized areas (Piovano & 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 turtle species is occurring worldwide (Da Silva & Blasco 1995; Petterino et al. 2001; Ficetola et al. 2002; Lever

Doi: 10.1111/lre.12164

Alien freshwater turtles in urban ponds

~o-Mart ınez & Marco 2005; Chen 2006; Pupins 2003; Patin 2007; Gherardi et al. 2008). The occurrence of alien turtle species in wet Mediterranean 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 humaninduced 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 (Marzluff 2008), thereby facilitating biotic homogenization (Dar & Reshi 2014). Moreover, ponds in recently urbanized 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 0.011; n = 203); 2 Small basins (SB) – small artificial ponds with cemented edges, with scarce or absent water flow (average surface area of 0.01 ha 0.01; n = 54); and 3 Lakes (LA) – relatively large ponds with semi-natural vegetated edges (average surface area of 0.59 ha 1.27; n = 54). These artificial or semi-natural ponds are further embedded in three different landscape contexts, as follows: 1 Public parks (PuP) – public green areas with vegetation 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 sampling 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 freshwater 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 animals. 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

M. P. Di Santo et al.

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 indicate public and private parks; white areas indicate non-urbanized areas; black line indicates Great Ring Highway).

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 circular shape), or the two axes and perimeters (if of elliptic or irregular shape), was calculated, using a measuring tape Komelon ( 1 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) standardization (using a comparable method for all the study sites); (ii) data independence (each AWB being an independent 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.

ÂŠ 2017 John Wiley & Sons Australia, Ltd

Data analysis The pattern of turtle species occurrence was modelled by means of the generalized linear model procedure (McCullagh & 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 (continuous 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 variable. The model design included the main effects for each variable, and the interactive term between the categorical factors (McCullagh & Nelder 1989). The

Alien freshwater turtles in urban ponds

non-parametric Spearman rank correlation test (twotailed) 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 individual 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

PuP

1.74

28.91

PuP

0.13

122.18

PrP

0.046

13.62

PrP

0.0032

6.02

PrP

0.05

17.94

PrP

0.09

34.9

PuP

0.19

372.09

PuP

0.002

358.64

PuP

0.002

35.6

PuP

1.18

25.12

PrP

0.004

78.05

PuP

8.5

10.48

PrP

0.003

134.63

PrP

0.039

109.9

PrP

0.013

175.61

PrP

0.001

59.01

PrP

0.001

99.76

PrP

0.001

92.99

PrP

0.001

13.41

PrP

0.001

42.01

PuP

3.8

279.45

PuP

0.09

113.67

PrP

0.001

32.28

PuP

1.3

96.87

PuP

0.43

11.08

PuP

0.7

91.12

PrP

0.001

19.97

PuP

1.6

246.81

PuP

0.09

145.04

PuP

0.03

132.43

PuP

0.03

16.53

Total

Dist

T.s.

P.n.

P.c.

G.p.

G.k.

A.s.

T.s., Trachemys scripta; P.n., Pseudemys nelsoni; P.c., P. concinna; G.p., Graptemys pseudogeographica; G.k., G. kohni; A.s., Apalone spinifera; Type, pond type; Land, landscape context; A, size area; Dist, distance from nearest road, S, number of alien freshwater turtle species; see Methods for further abbreviations.

ÂŠ 2017 John Wiley & Sons Australia, Ltd

M. P. Di Santo et al.

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 percentage 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 species 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 single 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

Table 2. Synopsis of generalized linear model results, illustrating only pond type among the studied parameters significantly influencing the occurrence pattern and species richness of turtles in study area Type III Wald v2

d.f.

Intercept

35.92

<0.0001

Type

Species occurrence 17.053

<0.0001

Landscape

0.299

0.584

Area

1.268

0.26

Distance

1.466

0.226

Type 9 Landscape

0.821

0.663

Species richness Intercept

34.867

<0.0001

Type

31.945

<0.0001

Landscape

0.001

0.975

Area

0.481

0.488

Distance

3.176

0.075

Type 9 Landscape

1.879

0.391

Type, AWB type; landscape, landscape context; distance, distance from nearest road; area, AWB size.

ÂŠ 2017 John Wiley & Sons Australia, Ltd

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 attributed 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; Dordevi c & Andelkovi c 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 natural resource availability, and consequently a higher probability 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 turtles. 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 recapture rate), and the consequential process (local extinction), 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 progressive disappearance of released groups of individuals in smaller ponds is different from the classic process of local extinction of native populations that occurs when

Alien freshwater turtles in urban ponds

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 animals as the most ecologically suitable habitats among other pond types to accommodate the undesired pet turtles. Braun (2002) also suggested that people, although having no biological background, might nevertheless recognize the naturalness and suitability of a habitat (e.g. a pond type) for a pet species (a non-native freshwater turtle in this case). Terrestrial habitats surrounding isolated wet habitats are essential elements for enhancing biodiversity (Gibbons 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 nonurban 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 probably 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 medium-long term. The role of urban parks with large lakes has also been emphasized for several vertebrate groups (e.g. see Mart Äąnez-Arroyo & J auregui 2000; Vignoli et al. 2013; Di Santo et al. 2015). Among reptiles, these urban ecosystems also may host remnant populations (or isolated introduced individuals) of native turtle species (e.g. Emys orbicularis; Vignoli et al. 2009; Di Santo, personal observations). 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 species richness hosted. This is an expected result as, with increasing pond size, there should also be a parallel increase in habitat heterogeneity and resource availability, with a higher number of niches potentially available (B aldi 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 postulation 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 determinant 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 sampling design of the present study), this first effort regarding occurrence and richness patterns will help support the efficiency of the sampling scheme directed to management. Moreover, these data suggested two hypotheses 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 development strategies aimed to preserve local biodiversity and to educate the public about the conservation issue repreâ&#x201A;Źfvenhaft et al. 2002; Teilsented by the alien species (Lo lac-Deschamps et al. 2009).

ÂŠ 2017 John Wiley & Sons Australia, Ltd

M. P. Di Santo et al.

In conclusion, the following management recommendations 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 releasing 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, freshwater species might be considered experiential key species (Battisti 2016); that is, species useful to promote proenvironmental 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 developed 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 management actions), is to use a set of indicators (e.g. number 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 eradication actions (assessing the outcomes of conservation project 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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