Basic and Applied Herpetology 32 (2018) 57-70

Where to live in Lisbon: urban habitat used by the introduced Italian wall ( siculus)

Ricardo Ribeiro*, Paulo Sá-Sousa

ICAAM – Instituto de Ciências Agrárias e Ambientais Mediterrânicas, Universidade de Évora, Pólo da Mitra, Ap. 94, 7002-554 Évora,

*Correspondence: E-mail: [email protected]

Received: 29 March 2018; returned for review: 22 May 2018; accepted 11 September 2018.

Exotic invasions constitute a major threat to biodiversity worldwide. Our assessment deter- mined the core range occupied by the Italian wall lizard (Podarcis siculus) in the urban area of Parque das Nações (Lisbon, Portugal), where it was accidentally introduced two decades ago. Des- pite the apparent current scenario of non-expansion, the alien species interferes with the local dis- tribution pattern of the native P. virescens, with both lizard species shown to use the available mi- crohabitats differently. The native P. virescens population displays an overall heterogeneous dis- tribution in the urban matrix. On the other hand, the occupancy of the exotic species clusters with- in the original area of introduction (garden in front of the Lisbon Oceanarium), as well as in adja- cent gardens. There, P. siculus replaced the native P. virescens as the only lizard species present. Appa-rently, there is no known reason there that prevents the alien lizard from colonizing more available geographic area and expanding.

Key words: Invasive species; Podarcis siculus; Podarcis virescens; spatial segregation.

Invasive species currently represent logical tolerance and plasticity, allied with one of the major problems in nature con- high propagation capacity (Nevo et al., servation (Schulte, 2012). The damage 1972; Capula Ceccarelli, 2003; Crnobr- caused by invasive mainly comes nja-Isailovic et al., 2009; Silva-Rocha et from disruptions and changes in native al., 2014). Podarcis siculus is distributed conti food webs and ecosystem functions, with -nuously throughout the Italian Peninsula impacts ranging from predation on sensi- and East Adriatic coast, as well as for big tive species, intoxication of predators, islands - Sardinia (where recent studies competition and hybridization with native suggested that it may be allochtonous ins- species, vectorization of new parasites, as tead of native, Senczuk et al., 2017) and well as direct and indirect impacts on hu- Sicily - and a multitude of adjacent islets mans (Kraus, 2009; Fujisaki et al., 2010). (Corti Lo Cascio, 2002). Unlike the re- Among the European species, the ported pet trade introductions in the USA Italian wall lizard (Podarcis siculus, Sau- (Kolbe et al., 2013), it might have been in- ria: ) is considered as both an troduced by ship trade into Corsica, Bale- opportunistic species and a successful ex- arics and several port areas around the otic colonizer, characterized by wide eco- Mediterranean Basin e.g. SW ,

DOI: https://dx.doi.org/10.11160/bah.101 RIBEIRO & SÁ-SOUSA

Greece, Turkey, or Lybia affected by this P. siculus introduction, al- (Carretero Silva-Rocha, 2015). though negative impacts are still unknown Towards Lisbon, some P. siculus indi- (such as expansion, hybridization or extin- viduals might have been transported ction of native species). Both species under along with rough materials and ornamen- study coexist in sympatry with other lacer- tal plants (structures in which they would tids in their native distributions, evidencing most likely be sheltered in or basking on), ecological segregation (Capula, 1993; Capu- from their place of origin, during the la et al., 1993; Carretero, 2008; ValdeÓn et Expo98 event (González de la Vega et al., al., 2010; Grano et al., 2011; Carretero 2001; Silva-Rocha et al., 2012). This appears Silva-Rocha, 2015; Carretero Salvador, to be a recurrent issue, as similar cases 2016). were reported by Rivera et al. (2011) and However, the introduction of the Italian ValdeÓn et al. (2010), after the observation of wall lizard in other areas has been shown to several P. siculus individuals in olive trees, be detrimental to autochthonous lacertids, imported from Calabria (Italy) to Catalo- especially in micro-insular environments, nia (). with evidence of competitive spatial coex- In urban environments, which are istence or exclusion (Nevo et al., 1972; Cap- typically characterized by spatially and ula, 2002; Capula Ceccarelli, 2003; Pod- temporally heterogeneous thermal mos- nar et al., 2005; ValdeÓn et al., 2010; Mateo aics, ecological interactions with poten- et al., 2011; Carretero Silva-Rocha, tial competitors and predators may also 2015). influence patterns of occurrence and abun- Based on previous personal reports dance of individuals of a given species from Paulo Sá-Sousa and bibliography (Kolbe et al., 2016). In those environments, it from Loureiro et al. (2008), this study’s main has been observed that sympatric lacertids objectives consisted in determining the cur- (namely and P. siculus) rent range area occupied by the introduced are spatially organized according to each P. siculus and assessing the degree of spatial species specific ecological needs, and there- segregation exerted by the exotic popula- fore not limited to interspecific interactions tion upon the autochthonous species. This (Capula et al., 1993). Lizard species often tend required the knowledge of the current spa- to be associated with specific microhabitat tial distribution of both species in Lisbon, as patches, with minimized interspecific com- well as each species microhabitat prefer- petition through their spatial niche distri- ences, according to the available space. bution (Smith Ballinger, 2001; Rugiero Materials and methods Luiselli, 2007; Vitt Caldwell, 2014). However, there may be cases where the The study area covered the location microhabitat occupied by a certain species where P. siculus was first introduced is restricted by the presence of another and consequently reproduced (González (Arnold, 1987). That could be the case with de la Vega et al., 2001), within the so-called autochthonous Podarcis virescens (Geniez Parque das Nações, a leisure and residential et al., 2014; Dias et al., 2016), which might be area of Lisbon (38°45ʹ43.7ʺN 9°05ʹ39.0ʺW,

58 HABITAT OCCUPANCY BY PODARCIS SICULUS IN LISBON

Figure 1: Total prospected area limited in red; Podarcis siculus introduction spot highlighted by a black square.

Fig. 1). For lizard sampling one large poly- were favourable weather conditions for gon was delimited to address the possible lizard thermoregulation). However, some expansion and establishment of new po- sectors took longer to cover in cases of pulations towards adjacent spots. The high occurrence of observations. All lizard sampling area was subsequently divided observations (each corresponding to one in 16 plots or sectors with approximate individual) consisted of visual encounters dimensions, to facilitate the visual encoun- (Lambert, 1984; Eekhout, 2010), where the ter of . Although these plots consis- following data was recorded: GPS point of ted of urban areas, there are contrasting location, species (P. siculus or P. vi- differences between them, ranging from rescens), behaviour activity, perch type, height those that show predominance of artificial and slope, distance to vegetation cover, elements, to those that hold some garden refuge type and distance to refuge, along spots with lawn or a more rustic appear- with the substrate texture, number of ance, usually consisting of an eclectic se- trees, shrubs, non-woody plants and dead lection of plant species from various re- branches/trunks, found within a four me- gions of the world (Pedrosa, 2013). ters radius surrounding each observation Due to statistical and data indepen- point (the dissertation from which this dence reasons, the sectors were sampled article was adapted covered a wider range following a random order. Each sector was of variables, including sex and size class, surveyed by walking at a slow, steady which were considered negligible for the pace, during one sunny day (when there study´s purpose, primarily focused on

59 RIBEIRO & SÁ-SOUSA

Figure 2: Spatial distribution of both species (A - total area; B - focus in the pre- sence of Podarcis siculus). Red symbols – introduced Podarcis siculus; Green sym- bols - autochthonous Po- darcis virescens.

habitat use and microspatial distribution, 0.05) (Strode Brokaw, 2015). The chi- and therefore discarded from this paper). squared test was used for comparison be- The first round of sampling covered all (16) tween species, regarding the data collected sectors, providing a general acquaintance of on the constituent elements of the micro- both the study area and its lizard occupan- habitats used by both species, where the cy. Based on this previous data assessment, formulated null hypothesis was that “there the second and third rounds covered only 8 are no differences between the use given by of the 16 sectors, excluding those where P. the invasive and autochthonous species to siculus was clearly absent in the first round. the elements present in the microhabitat”. Thus, the first round took place between For this test’s application we used raw data, April 25th, 2016 and July 3rd, 2016; the sec- that is, simple counts (observations), ins- ond began on September 8th, 2016 and en- tead of percentages or proportions (Strode ded on September 21st, 2016; the third lasted Brokaw, 2015), presented in table, which from September 24th, 2016 to October 11th, included the observed and expected values 2016. for several categories, within each con- Further statistical analyses were per- sidered parameter (Dytham , 2011). Since formed using the SigmaPlot® 13.0, Statisti- multiple tests were performed simultane- ca 13® and Microsoft Excel 2016 softwares, ously, further statistical corrections were tested for a confidence level of 95% (α = made using the Holm-Bonferroni method,

60 HABITAT OCCUPANCY BY PODARCIS SICULUS IN LISBON

Table 1: Sampled sector maximums for both The native P. virescens population species in each sector. The three sectors with shows an overall heterogeneous distribu- occurrence of both species highlighted in grey. tion in the urban matrix. On the other hand, the occupancy of the invasive species only Sector Max. P. virescens Max. P. siculus clusters within the original area of intro- duction (garden in front of the Lisbon

1 26 1 Oceanarium), as well as in adjacent gardens 2 9 26 (Fig. 2a). A single individual of P. siculus 3 22 96 was also o-bserved in a previously 4 41 0 unknown location (a garden spot placed 5 13 0 some hundreds of meters away from the 6 7 0 main area), where P. virescens often occurs 7 4 0 (Fig. 2b). 8 8 0 9 27 0 Degree of spatial segregation between 10 24 0 Podarcis siculus and Podarcis virescens 11 2 0 The Chi-squared tests of independence 12 10 0 support the main differences found in the 13/14 33 0 spatial variables tested between P. siculus 15 9 0 and P. virescens, as explained in the follo- 16 16 0 wing sections concerning habitat, through Sub‐total 251 123 the analysis of the graphics and tables (P < 0.001 for nearly all values, Table 2), regar- ding the behaviour shown by the lizards during observation, the elements present in narrowing the possibility of generating a the microhabitat and its use by both spe- statistically significant result (type I error) cies. The only exception was the parameter (Holm, 1979). To enlighten these intricate “Distance to Refuge”, which was similar for multiple results, a Multiple Correspon- both species (P = 0.223, Table 2). The Holm- dence Analysis test was performed compre- Bonferroni correction method confirmed hending all parameters, to visualize the the obtained results, whereas the previous- pattern of relationships between the micro- ly mentioned parameter remained as the habitat features and their usage by both only to not reject the null hypothesis. species (Abdi Valentin, 2007). The Multiple Correspondence Analysis Results test plots for both species (Fig. 6) showed that, despite overlapping for the most part, Lizard occupancy P. siculus only occupies part of the spatial A total of 699 observations were regis- niche of P. virescens at the multivariate le- tered, 476 (68%) belonging to the native P. vel, which could provide some answers virescens and 223 (32%) to the introduced P. regarding the possible event of future ex- siculus, present in only three sectors (Table 1). pansion and its impacts on P. virescens.

61 RIBEIRO & SÁ-SOUSA

Table 2: Results of the chi-Squared statistical tests, used for comparison between species. Signifi- cant P-values highlighted in bold. Adjusted Holm-Bonferroni P-values on the right.

Holm‐Bonferroni P‐ Tested Parameters χ2 df P‐value values Behaviour 19.401 3 P < 0.001 P = 0.01

Perch type 81.089 3 P < 0.001 P = 0.005 Perch height 51.731 3 P < 0.001 P = 0.03 Perch slope 22.236 2 P < 0.001 P = 0.01

Refuge type 98.363 6 P < 0.001 P = 0.01

Distance to refuge 4.379 3 P = 0.223 P = 0.01

Number of Trees 34.2 1 P < 0.001 P = 0.02

Number of Shrubs 43.719 2 P < 0.001 P = 0.01 Number of non-woody plants 12.945 2 P = 0.002 P = 0.05

Number of dead branches/trunks 33.585 3 P < 0.001 P = 0.004

Substrate texture 62.558 2 P < 0.001 P = 0.01 Distance to vegetation cover 21.584 2 P < 0.001 P = 0.01

Among the variables which contributed but were also present in areas with 1 to 5 the most for the relative inertia values, (23% and 39%) shrubs. Both species used were the Refuge and Perch Type Rock, as areas with a moderate presence of dead well as Vertical Perch Slope, and Artificial wooden matter (up to 30 branches/trunks/ Perch Type and Substrate Texture. etc.), counting for 71% of P. siculus and 56% of P. virescens observations (Fig. 3d). Habitat use Substrate texture (Fig. 3e) enhances P. sicu- Both species seem to occur in larger lus as having occupation for earthy open spaces numbers (84% of the P. siculus total and (79%), while P. virescens appears to be a 97% of P. virescens) in areas with few or more generalist species, though often no trees (0 to 2) (Fig. 3a), with the autoch- found in earthy substrate (50%), dividing thonous species being less dependent on the remaining half of observations almost the existence of arboreal and non-woody equally between artificial and mixed plants cover on site (Fig. 3c - the congeners grounds. showed a marked preference for areas Micro‐habitat features without non-woody plants, 73% of P. sicu- The most used perch for both lacertids lus and 80% P. virescens). Similarly, 58% of (Fig. 4a) appears to be the ground (more P. siculus and 56% of P. virescens individuals evident for P. siculus, 81%, than for P. vi- appeared in spots without shrubs (Fig. 3b) rescens, 53% ), whereas P. virescens also choos-

62 HABITAT OCCUPANCY BY PODARCIS SICULUS IN LISBON

Figure 4: Results concerning each species use of the available micro-habitat: Perch Type (A), Figure 3: Results concerning micro-habitat Height (B), Slope (C) and Distance to Vegeta- elements: number of Trees (A), Shrubs (B), tion Cover (D). Non-woody Plants (C), dead Branches/Trunks (D) and Substrate Texture (E). es perches located in artificial stru-ctures (90% for P. siculus and 75% for P. vi- (34%). The rocky perches were the least rescens) of vegetation cover (herbaceous, chosen, by both species. Concerning to the shrubs, trees – Fig. 4d) near to the perch perch height, soil level was the most ob- (up to 0.5 m) was detected. served (Fig. 4b), with P. siculus showing The behaviour activity of lizards (Fig. ground dwelling attributes (82%), similar 5a) shows that both species were often to slightly more than half of the P. vi- seen basking (57% for P. siculus and 64% rescens individuals. Of the latter, 21% are still for P. virescens), but also active (18 to distributed at a reduced height (from 0 to 20%), suggesting a similar daily tasks 0.25 m), with only 9% of the individuals pattern. When disturbed, the lizards often found at heights above 0.75 m. The slope seek the available vegetation cover as ref- assumed by each lizard at perch site (Fig. uge (Fig. 5b), which was evident (50%) for 4c) was mostly horizontal for both species P. siculus, while the native lizard chose be- (84% of P. siculus and 70% of P. virescens). tween ve-getation cover and artificial The “Vertical” posture was the second structures (26% and 32%, respectively), the most observed in P. virescens and the least latter one which the exotic species appar- observed in P. siculus. High dependency ently tends to avoid. Approximately 22%

63 RIBEIRO & SÁ-SOUSA

Figure 5: Results concerning each spe- cies use of the available micro-habitat: Behaviour (A), Refuge Type (B) and Distance to Refuge (C).

of the observations for both species did servations. There, this species individuals not seek refuge, remaining in the perch show the behaviour and ecological without mo-ving, or escaping without patterns typical of their own species seeking shelter in the nearby elements. (Corti Lo Cascio, 2002). However, the About 40% of P. siculus and 47% of P. vi- obtained data suggests that local spatial rescens prefer to carry out their daily tasks segregation was most probably due to near (up to 0.25 m) to a possible refuge competitive exclusion, as P. siculus re- (Fig. 5c), with the number of observations placed P. virescens as the only lizard spe- decreasing as the distance to refuge in- cies present at the original introduction creases. site. In fact, P. siculus has a larger body size than P. virescens, which is probably Discussion an advantage in competitive encounters Although there were found some si- since, according to Downes Bauwens gnificant differences in the use of several (2002), larger species tend to be dominant categories of habitat tested between both over smaller ones. This appears to have lizard species, that is not the major evi- favoured the exotic wall lizard to the detri- dence. Indeed, all observations in Parque ment of the native species, since in Lisbon das Nações (Lisbon) point to a scenario of the species are shown to be sympatric but absence of expansion by the alien species never syntopic. P. siculus, as previously suggested by Lourei- Sympatric species, when in direct com- ro et al. (2008) and Sá-Sousaʹs personal ob- petition, often spatially separate them-

64 HABITAT OCCUPANCY BY PODARCIS SICULUS IN LISBON

Figure 6: Multiple Corre- spondence Analysis Scatter- plot map, comprehending all surveyed parameters for both species. Black symbols represent introduced P. siculus; purple, open symbols represent autochthonous P. virescens.

selves due to differences in the structural artificial substrates. It shows, to some ex- niche (e.g. diameter and height of the cho- tent, dependence on the existence of some sen perch) and, in some cases, in the mi- type of vegetation cover (herbaceous, croclimatic environment (eg. open vs. shrubs, trees) relatively close to the perch, shaded areas) or by displacement of indi- being mainly found at soil level. Despite viduals through both competition and anti its observable proximity to vegetation co- -predatorial/survival behaviour (Downes ver, the microhabitats used by P. siculus Bauwens, 2002; Žagar et al., 2015). Syntop- tend to be poor in tree and shrub cover, ic lizard populations were shown to alter with most of the individuals observed also their predation risk by using specific habi- showing preference for areas with little to tats based on the availability of refu-ges none dead wooden matter on the ground. that provide protection against shared It was also observed, in this species, ten- predators, which act as competition medi- dency to avoid artificial structures as pos- ators, indirectly inducing asymmetrical sible shelter, preferring the available vege- competition and shifts in segregation tation cover for this purpose - and thus patterns (Smith Ballinger, 2001; Žagar perhaps limiting its distribution in this et al., 2015). The results in Lisbon suggest that predominantly urban area. both species use the available microhabi- It is tricky to explain the present lack of tats differently. expansion of P. siculus in Lisbon, especial- The exotic species P. siculus preferen- ly since this species often spreads into ur- tially uses microhabitats having a mostly ban areas in native Italy, where it is sym- earthy substrate texture, avoiding fully patric with P. muralis: P. siculus prefers the

65 RIBEIRO & SÁ-SOUSA driest places, while P. muralis the moisten little or no shelter to these P. siculus indi- ones (Corti Lo Cascio, 2002). Perhaps it viduals, they might attempt to expand. If is still a question of a short time lapse (two landscape work is carried out in the adja- decades) after the presumed date of intro- cent areas and gardens, it may possibly duction (not yet the sufficient time and promote the dispersal of P. siculus, by al- effort required to efficiently use the newly tering their previously unfavourable con- occupied habitat - Stamps, 1995), the possi- ditions and resources, since dispersal be- bility of the exotic species larger body size haviour seems to be in some aspects influ- being a disadvantage at this particular in- enced by external factors, such as intraspe- troduction site (making this lizard more cific competition and habitat quality prone to predation or less capable of dea- (Vignoli et al., 2012). This brings us to the ling with the introduction site’s condi- single individual found off the core area of tions), and/or lack of a reproductive effe- introduction, which may occur most likely ctive high enough to promote recruitment due to the translocation of plants or trees of young lizards towards new adjacent between gardens of Parque das Nações, an spots (more individuals = more potential action witnessed during the sampling dispersers - Vignoli et al., 2012). rounds. Most of these movements are usu- This diminished reproductive effective ally carried out in the winter, due to the might also be due to high predation pres- reduced plant activity, which facilitates sure, as several individuals of Tarentola the success of the transplant, but also fa- mauritanica were observed in the P. siculus vours exotic reptile species introductions, place of occurrence and nearby sites, a often hibernating inside available cavities species which may consume individuals of in trees or plants, so that these movements the latter and other species of lacertids, do not cause the individual to escape from both immature and adult (Pellitteri-Rosa the refuge (ValdeÓn et al., 2010). Despite et al., 2015). This population growth control the contribution of such activities and reg- may be carried out by P. siculus adult in- ular maintenance work to introductions, dividuals as well, in cases of cannibalism they can also rake the soil and diminish (such as those previously described by the available vegetation cover, destroy Ouboter, 1981, Burke Mercurio, 2002, lizard eggs buried in the ground or sand, Cattaneo, 2005, Capula Aloise, 2011 reduce the availability of perches for ther- and Grano et al., 2011), or by cats, dogs or moregulation and disturb the existing mi- seagulls present in the area (Burke Ner, croclimate at the place of introduction – 2005). Other lacertid found inside the yet again providing a plausible argument study area limits was Psammodromus al- for the absence of expansion. This cluste- girus, which could spark interactions with yet ring could be due to high predation pres- unknown consequences in case of future sure, short time span since introduction, contact with the exotic population. competition with autochthonous species, Although the introduction area in lack of available favourable resources and/ Parque das Nações is surrounded by artifi- or microhabitat degradation – or synergy cial structures that apparently provide of all the previous factors. If expansion is

66 HABITAT OCCUPANCY BY PODARCIS SICULUS IN LISBON to occur, data suggests that it possibly to Leonor Melo for the additional review would not exclude the autochthonous spe- of the article. Miguel A. Carretero and one cies entirely, since P. siculus seems to not anonymous reviewer provided construc- occupy all the available habitats in the tive comments and suggestions on the Parque das Nações area, with a reduced manuscript. usage of the more artificial and/or rocky References ones. Nevertheless, the present study Abdi, H., Valentin, D. (2007). Multiple corre- demonstrates how there is no homogenei- spondence analysis. Encyclopedia of meas- ty of introduction/invasion cases, as natu- urement and statistics, 651-657. Arnold, E. N. (1987). Resource partition among ralized populations can vary enormously lacertid lizards in southern Europe. Journal in their ecological dominance, from those of Zoology 1(4): 739-782. that remain in small numbers in a single Burke, R. L., Mercurio, R. J. (2002). Food locality, to those that spread like wildfire habits of a New York population of Italian on a large scale and become numerically wall lizards, Podarcis sicula (Reptilia, Lac- dominant (Kraus, 2009). Similarly, for the ertidae). The American Midland Naturalist other known introduced populations of P. 147(2): 368-375. siculus in the Iberian Peninsula, there is no Burke, R. L. Ner, S. E. (2005). Seasonal and evidence of high expansion in Almeria, diel activity patterns of Italian wall lizards, Podarcis sicula campestris, in New York. North- while it seems to be decreasing in Canta- eastern Naturalist 12(3): 349-360. bria or even being extirpated from La Rioja Capula, M. (1993). Natural hybridization in and Catalonia (Carretero Silva-Rocha, Podarcis sicula and P. wagleriana (Reptilia: 2015). Since the eradication of alien reptile Lacertidae). Biochemical Systematics and populations is virtually impossible once Ecology 21(3): 373-380. established (Kraus, 2009), we suggest the Capula, M. (2002). Genetic evidence of natural monitoring and containment of the exotic hybridization between Podarcis sicula and population, as well as planning mainte- Podarcis tiliguerta (Reptilia: Lacertidae). Am- nance works considering the presence of phibia-Reptilia 23(3): 313-321. Capula, M. Ceccarelli, A. (2003). Distribu- the species, as prevention measures to tion of genetic variation and of avoid future territorial expansion and con- insular and mainland populations of the sequent impacts on native fauna. Italian wall lizard, Podarcis sicula. Amphibia Acknowledgement -Reptilia 24: 483-495. Capula, M. Aloise, G. (2011). Extreme feed- This article was adapted from Ricardo ing behaviours in the Italian wall lizard, Ribeiro´s master’s dissertation in Conser- Podarcis siculus. Acta Herpetologica 6(1): 11- vation Biology, titled “First assessment on 14. Capula, M., Luiselli, L. Rugiero, L. (1993). the introduction of the Italian wall lizard Comparative ecology in sympatric Podarcis (Podarcis siculus) in Parque das Nações muralis and P. sicula (Reptilia: Lacertidae) from (Lisbon)”, supervised by Paulo Sá-Sousa, the historical centre of Rome: What about available in http:// competition and niche segregation in an hdl.handle.net/10174/21333. Special thanks urban habitat?. Bolletino di Zoologia 60(3):

67 RIBEIRO & SÁ-SOUSA

287-291. niques and protocols for all taxa biodiversi- Carretero, M. A. (2008). An integrated assess- ty inventories. Belgium: Belgian National ment of a group with complex systematics: Focal Point to The Global Taxonomy Initiative the Iberomaghrebian lizard genus Podarcis 8: 530-557. (, Lacertidae). Integrative Zoology Fujisaki, I., Hart, K. M., Mazzotti, F. J., Rice, 4: 247–266. K. G., Snow, S. Rochford, M. (2010). Risk Carretero, M. A. Silva-Rocha, I. (2015). La assessment of potential invasiveness of ex- lagartija italiana (Podarcis sicula) en la otic reptiles imported to south Florida. Bio- Península Ibérica e islas Baleares. Ecology logical Invasions 12(8): 2585-2596. 22: 4829-4841. Geniez, P., Sá-Sousa, P., Guillaume, C. P., Carretero, M. A. Salvador, A. (2016). Cluchier, A. Crochet, P. A. (2014). Sys- Lagartija verdosa – Podarcis virescens, In A. tematics of the Podarcis hispanicus complex Salvador & A. Marco (eds.) Enciclopedia (Sauria, Lacertidae) III: valid nomina of the Virtual de los Vertebrados Españoles. Museo western and central Iberian forms. Zootaxa Nacional de Ciencias Naturales, Madrid. 3794(1): 001–051. DOI: http:// http://www.vertebradosibericos.org/. dx.doi.org/10.11646/zootaxa.3794.1.1 Cattaneo, A. (2005). L’erpetofauna della González de la Vega, J. P., González-García, Tenuta Presidenziale di Castelporziano J. P., García-Pulido, T. González García, (Roma). Atti del Museo di Storia Naturale G. (2001). Podarcis sicula (Lagartija italiana), della Maremma 21: 49-77. primera cita para Portugal. Boletín de la Corti, C. Lo Cascio, P. (2002). The lizards of Asociación Herpetológica Española 12(1): 9. Italy and adjacent areas. Frankfurt Contri- Grano, M., Cattaneo, C. Cattaneo, A. butions to Herpetology, 14th ed. Chimara, (2011). A case of cannibalism in Podarcis Frankfurt am Main. siculus campestris De Betta, 1857 (Reptilia, Crnobrnja-Isailovic, J., Vogrin, M., Corti, C., Lacertidae). Biodiversity Journal 2(3): 151- Pérez Mellado, V., Sá-Sousa, P., Cheylan, 152. M., Pleguezuelos, J., Sindaco, R., Romano, Holm, S. (1979). A simple sequentially rejective A. Avci, A. (2009). Podarcis siculus. (errata multiple test procedure. Scandinavian jour- version published in 2016) The IUCN Red nal of statistics 6(2): 65-70. List of Threatened Species 2009: Kolbe, J. J., Lavin, B. R., Burke, R. L., Rugiero, e.T61553A86151752 L., Capula, M. Luiselli, L. (2013). The Dias, G., Luis, C., Pinho, C. desire for variety: Italian wall lizard Kaliontzopoulou, A. (2016). A case of Po- (Podarcis siculus) populations introduced to the darcis carbonelli intake by Podarcis virescens. United States via the pet trade are derived Herpetology Notes 9: 105-108. from multiple native-range sources. Biologi- Downes, S. Bauwens, D. (2002). An experi- cal Invasions 15(4): 775-783. mental demonstration of direct behavioural Kolbe, J. J., Van Middlesworth, P., Battles, A. interference in two Mediterranean lacertid C., Stroud, J. T., Buffum, B., Forman, R. T. lizard species. Animal Behaviour 63(6): 1037 Losos, J. B. (2016). Determinants of spread -1046. in an urban landscape by an introduced Dytham, C. (2011). Choosing and using statis- lizard. Landscape Ecology 31(8): 1795-1813. tics – a biologist’s guide. 3rd ed. Wiley- Kraus, F. (2009). Alien reptiles and amphibian. Blackwell A scientific compendium and analysis. In- Eekhout, X. (2010). Sampling amphibians and vading nature: Springer series. Invasion reptiles. Manual on field recording tech- Ecology 4.

68 HABITAT OCCUPANCY BY PODARCIS SICULUS IN LISBON

Lambert, M. R. K. (1984). Amphibians and rep- Peninsula) on imported olive trees. Butlletí tiles, In J.L. Cloudsley-Thompson (ed.) Saha- de la Societat Catalana d’Herpetologia 19: 79-85. ra Desert. Pergamon Press, Oxford, United Rugiero, L. Luiselli, L. (2007). Null model Kingdom: 205-228. analysis of lizard communities in five urban Loureiro, A., Ferrand de Almeida, N., Carre- parks of Rome. Amphibia-Reptilia 28(4): 547- tero, M. A. Paulo, O. S. (2008). Atlas dos 553. anfíbios e répteis de Portugal. Instituto da Con- Schulte, U. (2012). Origin, climate niche, popula- servação da Natureza e da Biodiversidade, tion genetics and intraspecific hybridization of Lisboa. introduced wall lizard populations in Central Mateo, J., Ayres, C. LÓpez-Jurado, L. F. Europe (Ph.D dissertation, Universität Trier). (2011). Los anfibios y reptiles naturalizados Senczuk, G., Colangelo, P., De Simone, E., en España: historia y evolución de una Aloise, G., Castiglia, R. (2017). A combi- problemática creciente. Boletín de la nation of long term fragmentation and gla- Asociación Herpetológica Española 22: 447-454. cial persistence drove the evolutionary his- Nevo, E., Gorman, G., Soulé, M., Yang, S. Y., tory of the Italian wall lizard Podarcis sicu- Clover, R. Jovanovic, V. (1972). Competi- lus. BMC evolutionary biology 17(6): 1-15. tive exclusion between insular Lacerta spe- Silva-Rocha, I., Salvi, D. Carretero, M. A. cies (Sauria, Lacertidae). Oecologia (Berl.) (2012): Genetic data reveal a multiple origin 10: 183-190. for the populations of the Italian wall lizard Ouboter, P. E. (1981). The ecology of the island- Podarcis sicula (Squamata: Lacertidae) intro- lizard Podarcis sicula salfii. Amphibia- duced in the Iberian Peninsula and Balearic Reptilia 2(3): 243-257. Islands. Italian Journal of Zoology 79(4): 502 Pedrosa, J.P.F.L. (2013). Parque das Nações: -510. abordagem precursora ao desenho da cidade Silva-Rocha, I., Salvi, D., Harris, D. J., Freitas, sustentável. M.Sc. Thesis in Architecture, S., Davis, C., Foster, J., Deichsel, G., Faculdade de Ciências e Tecnologia da Adamopoulou, C. Carretero, M. A. Universidade de Coimbra. (2014). Molecular assessment of Podarcis Pellitteri-Rosa, D., Liuzzi, C. Bellati, A. sicula populations in Britain, Greece and Turkey (2015). First report of adult Podarcis siculus reinforces a multiple-origin invasion pattern (Rafinesque-Schmaltz, 1810) predation by in this species. Acta Herpetologica 9(2): 253- Tarentola mauritanica (Linnaeus, 1758). Herpe- 258. tozoa 28 (1/2): 89-92. Smith, G. R., Ballinger, R. E. (2001). The eco- Podnar, M., Mayer, W. Tvrtković, N. (2005). logical consequences of habitat and micro- Phylogeography of the Italian wall lizard, habitat use in lizards: a review. Contempo- Podarcis sicula, as revealed by mitochondrial rary Herpetology 2001(3): 1-13. DNA sequences. Molecular Ecology 14(2): Stamps, J. (1995). Motor learning and the value 575-588. of familiar space. The American Naturalist Ribeiro, R. (2017). Avaliação do estádio de 146(1): 41-58. introdução da lagartixa italiana Podarcis siculus Strode, P. Brokaw, A. (2015). Using biointer- no Parque das Nações (Lisboa). M.Sc. Thesis in active resources to teach Mathematics and Conservation Biology, Universidade de Évo- Statistics in Biology, In http:// ra. media.hhmi.org/biointeractive/guides/ Rivera, X., Arribas, O., Carranza, S. Ma- statistics/Statistics-Teacher Guide.pdf? luquer-Margalef, J. (2011). An introduction download=true - Accessed at February 25th, of Podarcis sicula in Catalonia (NE Iberian 2017

69 RIBEIRO & SÁ-SOUSA

ValdeÓn, A., Perera, A., Costa, S., Sampaio, F. Evolution 24(3): 244-256. Carretero, M. A. (2010). Evidencia de Vitt, L. J. Caldwell, J. P. (2014). Herpetology: una introducción de Podarcis sicula desde an introductory biology of amphibians and rep- Italia a España asociada a una importación tiles. 4th ed. Academic Press. de olivos (Olea europaea). Boletín de la Žagar, A., Bitenc, K., Vrezec, A., Carretero, Asociación Herpetológica Española 21: 122-126. M. A. (2015). Predators as mediators: Differ- Vignoli, L., Vuerich, V., Bologna, M. A. ential antipredator behavior in competitive (2012). Experimental study of dispersal be- lizard species in a multi-predator environ- haviour in a wall lizard species (Podarcis ment. Zoologischer Anzeiger - A Journal of sicula) (Sauria Lacertidae). Ethology Ecology & Comparative Zoology 259: 31-40.

70