Influence of Recent Geography and Paleogeography on the Structure of Reptile Communities in a Land-Bridge Archipelago Author(s): Simone Fattorini Source: Journal of Herpetology, 44(2):242-252. 2010. Published By: The Society for the Study of Amphibians and Reptiles DOI: 10.1670/09-046.1 URL: http://www.bioone.org/doi/full/10.1670/09-046.1

BioOne (www.bioone.org) is an electronic aggregator of bioscience research content, and the online home to over 160 journals and books published by not-for-profit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder.

BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. Journal of Herpetology, Vol. 44, No. 2, pp. 242–252, 2010 Copyright 2010 Society for the Study of Amphibians and Reptiles

Influence of Recent Geography and Paleogeography on the Structure of Reptile Communities in a Land-Bridge Archipelago

SIMONE FATTORINI

Water Ecology Team, Department of Biotechnology and Biosciences, University of Milano Bicocca, Piazza della Scienza 2, I-20126, Milan, Italy; E-mail: [email protected]

ABSTRACT.—The herpetofauna of the Tuscan Islands (Central Italy) is well known and represents an ideal subject to understand the role of current and historical factors responsible for biogeographical patterns in a complex archipelago. Multidimensional Scaling, cluster analyses, species-area relationships, Mantel tests and co-occurrence statistics were used to investigate the influence of current geography and Pleistocene connections with the mainland on the structure of insular communities. Although reptile colonization likely occurred via land bridges for islands that were connected to the mainland in the Pleistocene, a long time relaxation (species extinction by island habitat loss after disconnection and new colonization by over sea dispersal or human-assisted introductions) equilibrated the faunas according to island area. Biogeographical similarities among islands increased for islands located farther from Corsica and , thus suggesting that, for remote islands, interisland faunal exchanges occurred more frequently than mainland-island colonization. Also, a possible influence of Pleistocene geography emerged more clearly when populations suspected to be introduced by man were removed. Co-occurrence analyses indicated a nonrandom distribution influenced by island area and distance, suggesting that the time elapsed since post-Pleistocene disconnection may have reshaped biogeographical similarities by an increase in competition resulting from reduction in island areas and introduction of certain species. From a conservation viewpoint, the land-bridge distribution of organisms with poor mobility should be carefully considered in conservation biogeography, because depletion of island populations cannot be balanced by new immigrations from the mainland, whereas introduction of nonnative species may have a negative impact on the original fauna.

The biogeography of the Tuscan Islands from Tuscany. In fact, recent studies demon- (Fig. 1) has long been studied to highlight the strated that, at least in animals with high major ecological and historical factors that are mobility (such as chrysidid hymenopterans potentially responsible for present day distribu- and butterflies), a transitional pattern can be tional patterns, making this archipelago one of simply explained by current geography alone the best investigated in the Mediterranean Basin (Fattorini, 2009a). (e.g., Baroni Urbani, 1971; Societa` Italiana di Although for oceanic islands (i.e., islands Biogeografia, 1974; Piantelli et al., 1990; Fattor- never connected to the mainland) a general ini, 2009a). model has been recently proposed that takes Because of their location between the Corsar- into account island evolution through time dian plate (Corsica plus Sardinia) and Tuscany (Whittaker et al., 2008; Fattorini, 2009b), there region (Central Italy), the Tuscan Islands are is no comprehensive theory on the evolution of expected to show transitional faunas, and this land-bridge islands. According to the model has already been well demonstrated for several postulated by Fattorini (2009a) for the Tuscan groups (Fattorini, 2009a). The common opinion Islands, land-bridge islands were largely colo- is that paleogeography is a key factor in nized (and possibly saturated) by different determining the distribution of plants and groups during the Pleistocene sea regressions, animals on these islands, which have been and then there have been extensive extinctions regarded as a classical example of land-bridge as a result of area and, hence, habitat loss. islands (see references in Mariotti, 1990; Dap- However, although mobile animals were able to porto and Cini, 2007). According to this view, currently colonize virtually all islands, mostly islands that were connected to Tuscany during erasing the historical signal and resulting in a Pleistocene glacial maxima are characterized by negative correlation of species richness and a preponderance of species that reached the distance, even small distances preclude less Tuscan Islands from the Italian mainland, mobile groups such as tenebrionid coleopterans whereas islands closer to Corsardinia (but from colonizing an island regularly, such that which were isolated during Pleistocene glacial no correlation between species richness and maxima) exhibit a larger proportion of species distance appears in these insects (Fattorini, distributed in Corsica and Sardinia but absent 2009c). Thus, the role of dispersal should be REPTILE BIOGEOGRAPHY ON LAND-BRIDGE ISLANDS 243

FIG. 1. The and its relative position in the Mediterranean. Present day land (black) and extent of land mass during the last (Pleistocene) glacial maximum (dark grey) are indicated. Depth contours are also shown for 200 m (light grey). CAP: , ELB: , GIA: , GIG: Giglio, GOR: , MON: , MTA: Mt. Argentario, PIA: . accurately considered for understanding the phy (Whittaker et al., 2005) stresses the impor- evolution of archipelagos that include land- tance of considering biogeographical informa- bridge islands. Compared with other groups, tion in assessing conservation priorities. Thus, reptiles are relatively less mobile; thus, their the understanding of the processes underlying island faunas tend to be usually relictual (e.g., reptile biogeographical patterns in the Tuscan Foufopoulos and Ives, 1999). Therefore, the Islands may serve as a case study to address reptiles of the Tuscan Islands may represent some general problems of biological conserva- an excellent model to investigate the role of tion in land-bridge archipelagos. current and historical factors in determining The aims of this paper were as follows: (1) to biogeographical patterns in a composite archi- investigate the biogeographical relationships of pelago, which includes both land-bridge and reptile faunas of the Tuscan Islands; (2) to oceanic islands. determine the relative importance of current The herpetofauna of the Tuscan Islands has (Recent) and historical (Pleistocene) geography been investigated by naturalists for more than a in determining such patterns; (3) to assess the century, and all of these islands are faunistically mechanisms that may explain the role of Recent well known (Balletto, 2005; Vanni and Nistri, and Pleistocene factors; and (4) to discuss some 2006). However, there is no detailed study implications for biodiversity conservation. aimed to understand the role of current and historical factors responsible for biogeographi- cal patterns. An analysis of the relative impor- MATERIALS AND METHODS tance of current and historical factors is partic- ularly compelling because of the conservation Data Sources.—The study islands included concern of these islands, which are included in Capraia, Gorgona, Montecristo, Elba, Pianosa, the Tuscan Archipelago National Park. The Giglio, Giannutri, and the fossil-island of Mt. recent development of conservation biogeogra- Argentario (Dapporto and Cini, 2007; Fig. 1). 244 S. FATTORINI

TABLE 1. Reptile distribution in the Tuscan Archipelago. Presence/absence indicated by 1/0.

Gorgona Capraia Elba Pianosa Giglio Montecristo Giannutri Mt. Argentario Tarantola mauritanica 1 111 1 0 1 1 Hemidactylus turcicus 1 111 1 1 1 1 Euleptes europaea 0 111 1 1 1 1 Lacerta bilineata 0 010 0 0 0 1 Podarcis sicula 0 111 1 1 1 1 Podarcis muralis 1 011 0 0 0 1 Chacides chalcides 0 010 0 0 0 1 Hierophis viridiflavus 1 111 1 1 1 1 Coronella austriaca 0 010 0 0 0 0 Zamenis longissimus 0 010 0 0 0 1 Elaphe quattorilineata 0 000 0 0 0 1 Natrix natrix 0 010 0 0 0 1 Vipera aspis francisciredi 0 010 0 0 0 1 Vipera aspis hugyi 0 000 0 1 0 0

Distributional data are taken from Fattorini (Elba, Portoferraio islet, Palmaiola, Scoglio della (2009a; Table 1). Field research was performed Paolina, fossil islands of Massoncello and Punta on Giglio and Giannutri in August 2008. Ala), Podarcis muralis insulanica (Pianosa and La The turtle Testudo hermanni was excluded as it Scarpa islet), Podarcis muralis marcuccii (Argen- has been introduced into the Tuscan Archipel- tarola islet, Mt. Argentario W), Podarcis muralis ago by humans (Vanni and Nistri, 2006). The muellerlorenzi (La Scola), Podarcis muralis paulinii occurrence of Vipera aspis on Montecristo is also (Mt. Argentario), Podarcis muralis vinciguerrai problematic (Zuffi and Bonnet, 1999). In fact, the (Gorgona), Podarcis sicula calabresiae (Monte- taxonomic status of Italian populations of vipers cristo), Podarcis sicula caporiaccoi (Capraia and is disputed. Recently, Zuffi (2002) proposed to La Peraiola islet), Podarcis sicula cerbolensis consider Vipera aspis francisciredi synonymous (Cerboli), Podarcis sicula roberti (Formica Grande with the typical form and Vipera aspis hugyi as a di Grosseto), and Podarcis sicula tyrrhenica good species. However, this interpretation has (Giglio, Giannutri). Most authors tend to con- been criticized (Filippi, 2003), and V. a. francis- sider all these taxa synonymous with the typical ciredi is retained as valid (Sindaco et al., 2006). form (Sindaco et al., 2006), and I have refrained Recent molecular investigations showed a para- from attribution of insular populations to phyletic status of V. a. hugyi, which has been subspecies. In fact, low values of genetic interpreted as a result of an introgressive variability in specimens of P. sicula from hybridization and capture of francisciredi-like Montecristo and Elba have suggested the lineages in the hugyi mitochondrial genome possibility that populations on these islands (Barabanera et al., 2009). The population of were founded by a small number of individuals Montecristo has been initially classified as an originating from episodes of human transpor- endemic subspecies (Vipera aspis montecristi). tation (Capula, 1994). However, low genetic However, successive analyses based on mor- variability is everywhere expected in island phological characters, and genetic data revealed populations, which are inherently less numer- that this population has to be referred to the ous than mainland populations, especially if subspecies hugyi, which lives in southern Italy they originated from few individuals (as ex- (for details, see Barbanera et al., 2009). This pected also in case of natural overseas dispersal) contrasts with the distribution of V. aspis in or if they underwent bottlenecks (as expected if central Italy, because Tuscan populations, as island populations underwent demographic well as those of Elba and Mt. Argentario, belong drops, such as by habitat loss). The native status to the subspecies francisciredi. At present, it is of the geckos Tarentola mauritanica and Hemi- controversial whether Montecristo vipers are dactylus turcicus, two anthropophylous species native (and established by unlikely overseas cited from all of the studied islands, is also dispersion from southern Italy) or introduced questioned (Harris et al., 2004; Carranza and from southern Italy (Zuffi and Bonnet, 1999; Arnold, 2006). Based on the absence of fossils of Barbanera et al., 2009). H. turcicus in the Mediterranean region and the For both Podarcis sicula and Podarcis muralis a recency of recorded arrivals in many parts of number of taxa endemic to single islands of the the New World, Carranza and Arnold (2006) Tuscan Archipelago have been described, in- considered the occurrence of this species cluding Podarcis muralis beccarii (Port’Ercole around most of the Mediterranean (excluding islet, Mt. Argentario SE), Podarcis muralis colosii the Middle East) as recent and anthropogenic. REPTILE BIOGEOGRAPHY ON LAND-BRIDGE ISLANDS 245

Harris et al. (2004) found that a single haplotype modeled a species-area relationship (SAR) characterizes populations of T. mauritanica using a power function (S 5 CAz, where S is across Spain, Portugal, Italy, Menorca, Crete, the number of species, A is area, and C and z are and Tunisia, raising the possibility of an fitting parameters) with a nonlinear fitting anthropogenic introduction followed by rapid procedure (Quasi Newton algorithm; Fattorini, population expansion throughout southern Eu- 2006c). If colonization occurred via land-bridge rope. Moreover, although repeatedly reported connections, Pianosa, as well as the other in literature also from Montecristo Island, T. islands connected to Tuscany, are expected to mauritanica has not been found on this island have more species than predicted by the model during recent studies (M. A. L. Zuffi, pers. (i.e., positive residuals; Fattorini, 2006b) as a comm.); thus, its actual occurrence on this consequence of larger area and greater accessi- island is doubtful, and I have omitted it from bility during the Pleistocene. Calculations were this island in all analyses. Finally, the snake done using STATISTICA software (vers. 6, Zamenis longissimus has been recently found on StatSoft, Inc., Tulsa, OK, available from www. the island of Elba, but it is really uncertain statsoft.com). whether it is native or introduced to the island Biogeographical Relationships among Islands.— (Vaccaro and Turrisi, 2007). Cluster analyses of biogeographical similarities Because of the uncertain origin of some have been proposed as a tool to investigate the populations, in this study I performed two sets influence of current and historical factors in of analyses. A first set of analyses was conduct- species distributions (e.g., Graham et al., 2005; ed considering all populations as native (i.e., Guerrero et al., 2005; Dapporto et al., 2007), including all records of T. mauritanica, H. whereas Dapporto and Cini (2007) used an turcicus, P. sicula, Z. longissimus, and V. aspis). ordination technique (Multidimensional Scal- This represented the most ‘‘conservative’’ sce- ing). nario. A second set of analyses was performed In fact, biogeographical relationships hardly according to the ‘‘worst’’ wilderness scenario can be contrived in a dendrogram if areas did (i.e., excluding V. aspis from Montecristo, T. not originate by dichotomous splits; therefore, mauritanica and H. turcicus from all islands, P. ordination techniques usually are preferred sicula from all islands except Mt. Argentario, (Fattorini, 2002a; Fattorini and Fowles, 2005). and Z. longissimus from Elba). However, interpretation of results from ordina- Recent and Pleistocene data about island tion analyses is more arbitrary because there is isolation and areas are the same as in Fattorini (2009a; for details about calculations, see that generally no obvious way to find groups of paper). Here Pleistocene always indicates Pleis- objects in a space. This is critical particularly tocene glacial maxima. when there are few points (as for the Tuscan Influence of Recent and Pleistocene Factors on Archipelago), and different arrangements can Species Richness.—Species richness was correlat- be subjectively recognized by the researcher. In ed with Recent and Pleistocene factors (namely, such a case, a dendrogram may provide a more area and isolation; Dapporto and Cini, 2007; objective, albeit crude, way to define relation- Dapporto et al., 2007). Because of the occur- ships. For these reasons, I have applied both rences of several tied values, I applied the techniques here. Non-Metric Multidimensional gamma statistic G to test levels of associations. Scaling (NMDS) was applied to obtain a According to Dapporto et al. (2007), if representation of multiple interisland relation- paleogeography determined species richness in ships, whereas a cluster analysis was conducted the Tuscan Archipelago, one should also expect to ‘‘force’’ islands into hierarchical arrange- that Pianosa (which in the Pleistocene was ments that may serve as testable hypotheses. If connected to Elba and Tuscany) should have a current geography is the dominant factor, greater richness compared with all other islands species assemblages are expected to be random (except Elba). In fact, the hypothesis is not well samples mostly regulated by island area and formulated, because the Pleistocene richness of distance (Fattorini, 2007b); therefore, islands are Pianosa is expected to have decreased because expected to cluster in a chained dendrogram the island was disconnected and reduced in reflecting species richness. By contrast, under size. Thus, if paleogeography favored island the influence of historical factors, islands are colonization and species accumulation, and its expected to cluster according to relationships influence is superior to (i.e., not still erased by) that are largely independent from current current factors, Pianosa is not expected to have species richness. In particular, for the Tuscan a larger number of species than other islands Islands, we expect to find the small islands of but a larger number of species than predicted by Montecristo and Gorgona to cluster close to its current area (Fattorini, 2009a). To obtain the Elba (the largest island), all being close to the expected number of species for Pianosa, I mainland in the Pleistocene. 246 S. FATTORINI

In this study, biogeographical similarities islands based on the minimal sums of distances among islands based on species presence/ across the sea from Tuscany and Corsica- absence were calculated using Kulczynski 2 Sardinia (for details, see Fattorini, 2009a). In coefficient (for a discussion about the use of this Mantel tests, the null hypothesis H0 is that the coefficient in biogeographical analyses, see distances in a dependent matrix A (e.g., a matrix Hausdorf and Hennig, 2005). Similarity values of biogeographical dissimilarities between is- were then converted to dissimilarities and lands) are independent of those between the clustered with the UPGMA amalgamation rule, same objects in the independent matrix B (e.g., a which is considered the clustering strategy that matrix of geographical distances between the minimizes the distortion of the original data same islands). Although the use of Mantel tests matrix (Shi, 1993; McGarigal et al., 2000); has been questioned because it is difficult to therefore, it is favored particularly in biogeo- express overall geographical and historical graphical studies in a variety of contexts (e.g., relationships among areas by simply using Fattorini, 2002a; Graham, et al., 2005; Guerrero geographical distances or a dissimilarity coeffi- et al., 2005; Smith and Bermingham, 2005). cient (Fattorini, 2006a), more complex ap- Kulczynski 2 dissimilarities were also used proaches appeared not appropriate for the for a NMDS analysis. The NMDS attempts to Tuscan Islands because of the small number of arrange ‘‘objects’’ (islands) in a space with a islands and variables involved. I applied Mantel particular number of dimensions to reproduce tests using the Pearson correlation coefficient the observed distances. The NMDS does not (r). For each test, probability values were have to try to reproduce the dissimilarities but calculated using the exact number of permuta- only their order. I used an ordinal algorithm for tions. For each correlation, probability values which the order of the distances in the repre- were assessed using one-tailed tests with P , sentation space must correspond to the order of 0.05. Calculations were done using XLSTAT the corresponding dissimilarities, but if there 7.5.2 software (Addinsoft, available from www. are two dissimilarities of the same rank, then xlstat.com). there are no restrictions on the corresponding Although many tests were done, in accor- distances. The NMDS iteratively moves objects dance with the suggestions of Moran (2003), I around in the space defined by the requested did not apply the Bonferroni correction but number of dimensions searching for the config- focused on P-values and consistence of results. uration that minimizes lack-of-fit (i.e., which Species Interactions.—To study whether spe- minimizes the distortion between the original cies interactions play a key role in structuring distances among objects and the new distance in species assemblages on islands, I tested possible the new n-dimensional space). As a criterion of nonrandom distributions of species among goodness-of-fit to build an optimal representa- islands by co-occurrence analysis. Special pat- tion, I used the raw stress (the smaller the stress terns of co-occurrence are indicative of either value, the better is the fit of the reproduced mutual exclusion or positive species associa- distance matrix to the observed distance ma- tions, with the former commonly interpreted as trix). In each analysis, the algorithm was a result of competitive exclusion (Gotelli and repeated from 100 randomly generated config- Ellison, 2002). urations with 1,000 iterations and the conver- For this approach, I used the Ecosim7 gence criterion was set at 0.00001. Calculations software (N. J. Gotelli and E. L. Entsminger, were done using XLSTAT 7.5.2 software (Ad- available from http://homepages.together.net/ dinsoft, available from www.xlstat.com). ,gentsmin/ecosim.htm). I considered two in- Influence of Recent and Pleistocene Factors on dices of co-occurrence: the number of checker- Biogeographical Patterns.—To study the influence boards (Checker index) and the C-score. The of current and historical factors on biogeograph- number of checkerboards is defined as the ical patterns I applied Mantel tests between number of species pairs in the matrix that form matrices of biogeographical distances (i.e., perfect checkerboards and never co-occur. In a Kulczynski 2 dissimilarities) among islands competitively structured community, the ob- and the following matrices of island character- served number of checkerboard species pairs istics: (1) Recent interisland isolation; (2) Pleis- should be significantly larger than expected by tocene interisland isolation; (3) Recent isolation chance. The C-score measures the tendency for from Corsica and Tuscany; (4) Pleistocene species to not occur together. The larger the C- isolation from Corsica and Tuscany. Recent score, the less the average co-occurrence among and Pleistocene interisland isolations were species pairs. If a community is structured by measured as minimal sums of distances across competition, we would expect the C-score to be the sea between islands, whereas Recent and large relative to a randomly assembled commu- Pleistocene isolations from Corsica and Tuscany nity. To generate random matrixes, I applied the were measured as Euclidean distances between Sim9 algorithm, which uses fixed row and REPTILE BIOGEOGRAPHY ON LAND-BRIDGE ISLANDS 247 column sums (those of the original matrix) and ally low, with Pianosa having a residual of 0.12. which is recommended for these two indexes When Pleistocene area is used, the SAR was because it is less prone to Type I errors. For both poorly fitted (S 5 0.483A0.388, R2 5 0.472). indices, 5,000 null matrices were produced Biogeographical Relationships among Islands.— using the sequential swap algorithm. To explic- The two matrices resulting from the different itly include the effect of area and isolation, I treatment of possibly introduced populations incorporated as weights the ratio ‘‘island area / gave partially similar results (Fig. 2A, B). island distance’’ (with distance of Mt. Argen- Cluster analysis under different treatments for tario set at 0.1). The underlying null model is an doubtfully native occurrences grouped islands ‘‘area-distance based random sampling’’ model, in accordance with their position in the NMDS, in which islands represent ‘‘targets’’ of different and the resulting patterns may be simply areas placed at different distances, and species explained by species richness (Fig. 2C, D). represent ‘‘darts’’ that are tossed randomly at However, the NMDS plot obtained omitting the set of different targets. If islands passively doubtfully native occurrences indicates a paleo- intercept individual colonists of different spe- geographical trend along Axis 1 for land-bridge cies, each island behaves as a target, and its islands (Pianosa, Elba and Mt. Argentario). chances of getting hit are directly proportional Influence of Recent and Pleistocene Factors on to its area and inversely to its distance from the Biogeographical Patterns.—Reptile island dissim- mainland source. ilarities calculated omitting possibly introduced taxa were negatively correlated with recent distances to Corsardinia and Tuscany (r 5 RESULTS 20.365, P 5 0.035), whereas no significant correlation was found when all occurrences Influence of Recent and Pleistocene Factors on were considered. Species Richness.—Reptile species richness was Species Interactions.—Using all occurrences positively correlated with Recent island area (G and including the area : distance ratio as a 5 0.714, P 5 0.032) and Pleistocene island area probability constraint, the observed C-score (G 5 0.889, P 5 0.016), and negatively with (0.374) was significantly higher than the value Recent isolation (G 520.714, P 5 0.032), expected by chance (0.074 [6 0.065 SD]), G 52 P 5 Pleistocene isolation ( 1.000, 0.008), suggesting a negative pattern of species co- G 5 and Pleistocene distance to Tuscany ( occurrence (P [Observed $ Expected] 5 0.001). 2 5 1.000, P 0.008). When possibly introduced Under the same conditions, the total number of species were omitted, significant correlations checkerboards (10) was also significantly higher 5 were found with Pleistocene area (G 0.867, P (P [Observed $ Expected] 5 0.001) than the 5 52 5 0.034), Pleistocene isolation (G 1.000, P value expected by chance (0.412 [6 1.240 SD]). 5 0.033), Pleistocene distance to Tuscany (G When possibly introduced populations were 2 5 1.000, P 0.033), as well as with Recent omitted, neither the C-index nor the number of 52 5 isolation (G 0.778, P 0.031) and Recent checkerboard pairs was significantly different 52 5 distance to Tuscany (G 1.000, P 0.037). from the values expected by chance. To take into account a possible bias in species richness for the fossil island of Mt. Argentario, which is currently connected with the main- DISCUSSION land, the last analysis was repeated omitting Mt. A positive SAR is an obvious result because Argentario singletons. In this case, species species richness tends to increase at larger areas richness resulted correlated with Pleistocene (Fattorini, 2007a). A significant SAR may result area (G 5 1.000, P 5 0.014), Pleistocene isolation from both current immigration/extinction pro- (G 521.000, P 5 0.033), and Pleistocene cesses (as postulated by dynamic models based distance to Tuscany (G 521.000, P 5 0.033). on current geography and ecology) and histor- Using a power function to model SARs, Re- ical processes consisting of island saturation cent island area explained a good proportion of 0.263 2 during land-bridge connections with the main- variance (S 5 3.049A , R 5 0.766). Anal- land followed by extensive extinctions when the ysis of residuals showed that all residuals were islands were disconnected and their area and low, with Pianosa having a residual of about habitats were consequentially reduced (faunal 0.37. When Pleistocene area is used, the SAR 0.242 2 relaxation after saturation) (Fattorini, 2007b). If was less adequately fitted (S 5 1.1916A , R current immigration is a key factor in deter- 5 0.566). mining species richness on islands, a negative When possibly introduced species were correlation with current isolation is expected omitted, Recent island area still explained (Fattorini, 2002b). For the reptiles of the Tuscan a relatively good proportion of variance (S 5 Islands, species richness was actually correlated 1.200A0.376, R2 5 0.620). Residuals were gener- with current isolation but even tightly with 248 S. FATTORINI

FIG. 2. Cluster analyses (A and B) and Non-Metric Multidimensional Scaling (NMDS) plots (C and D) based on Kulczynski 2 dissimilarities, showing patterns of reptile biogeographical relationships among the Tuscan Islands, assuming all populations as native (A and C) and removing all occurrences suspected to be recent introductions (B and D). Numbers after island names indicate species richness.

Pleistocene isolation. However, Pianosa does and does strongly contrast with biogeographical not show a large residual, as expected if patterns found in other groups, such as tene- paleogeography still determines species rich- brionid coleopterans, chrysidid hymenopterans, ness. This suggests that relaxation operated for and butterflies, which have transitional faunas, a time sufficient to equilibrate the faunas, as with several species that colonized various evidenced by the high proportion of variance islands from Corsardinia (Fattorini, 2009a). explained by the power function model. Hence, In fact, in other animal groups, such as although reptile colonization likely occurred via tenebrionids, chrysidids, and butterflies, it was land bridges for islands that were connected to possible to distinguish between Sardo-Corsican the mainland in the Pleistocene, a long time species (i.e., species occurring in both Corsardi- relaxation equilibrated the faunas according to nia and the Tuscan Archipelago but not in island area, leading to a significant relationship Tuscany) and the Tuscan species (i.e., species of species richness with current island area and occurring in both Tuscany and the Tuscan isolation. In fact, when species occurrences Archipelago but not in Corsardinia). For rep- suspected to be caused by human introductions tiles, there are no Sardo-Corsican species; thus, were omitted, correlations increased, thus sup- it is obvious that biogeographical similarities do porting a Pleistocene colonization followed by not show a twofold colonization process. human-aided colonization. In particular, a Also, Mantel tests indicated that, rather negative correlation with Pleistocene distance surprisingly, biogeographical similarities to Tuscany (coupled with the lack of correlation among islands increased for islands located with distance to Corsardinia) indicates that farther from Corsica and Tuscany. This result colonization occurred from Tuscany. can be explained by assuming that, for remote Current biogeographical similarity patterns islands, interisland faunal exchanges (favored do not fit either Pleistocene or Recent geogra- by stepping-stone dispersal or interisland land- phy but simply reflect gradients in species bridge connections) occurred more frequently richness. This suggests a random colonization than mainland-island colonization. REPTILE BIOGEOGRAPHY ON LAND-BRIDGE ISLANDS 249

Thus, it appears that Pleistocene geography subject to high tourism pressures, notably Elba had an important role in determining island and Giglio, which are leading tourist destina- colonization (as shown by strong influence of tions. A serious consequence of mass tourism Pleistocene geography on species richness), (and partly also of the so-called ecotourism) is possibly superior to current immigration (as the rapid degradation of fragile natural habitats, shown by the inverse correlation between which are becoming more and more attractive biogeographical patterns and distance from to tourists just because of their increasing rarity. Tuscany and Corsardinia) but that relaxation This led to high tourism pressure also on the after saturation led the system to a virtually island of Giannutri. Although most of the complete equilibration (as shown by the excel- footways on this island are currently forbidden, lent fit of the SAR for the data set including this is not known by most tourists, who reach possibly nonnative populations and the influ- the island by ferry-boats and concentrate in the ence of species richness in determining island few accessible places. However, field research similarities), which mostly erased the Pleisto- revealed that, in spite of the high tourist cene influence. Now, the question is which pressure on these islands, Podarcis populations mechanisms regulated the relaxation process. of Giglio and Giannutri are characterized by Co-occurrence analyses using all occurrences very confident animals that frequently came indicated mutually exclusive distributions of near the researcher, thus suggesting that they reptile species, whereas a random pattern of co- are not severely disturbed by man. Also, on the occurrence was found omitting possibly intro- island of Giglio, we were able to detect the duced populations. These results suggest that occurrence of Hierophis viridiflavus (Campese, the time elapsed since post-Pleistocene discon- road to Vado dell’Allume), as well as a number nection may have reshaped biogeographical of P. sicula (most of the island) and Euleptes similarities by an increase in competition, likely europaea (Cannelle) (60% of species richness), in because of reduction in island areas. The model few hours of research. This suggests that postulated here is that land-bridge islands were populations are likely numerous, although largely colonized (and possibly saturated) by literature data are usually relatively scarce and reptiles during the Pleistocene island connec- old (no detailed records of E. europaea were tions with the mainland and that there have reported after 1982) (Balletto, 2005). been extensive extinctions drawn by competi- The influence of man on the reptiles of the tion when islands were disconnected as a result Tuscan Archipelago in the past was particularly of area and, hence, habitat loss. However, this complex. Human activity probably affected the process of faunal impoverishment was contrast- natural turnover of species assemblages by ed by man, who imported accidentally (or not, increasing extinction rates in the most anthro- as in the case of tortoises), sometimes success- pized islands and introducing some species, fully, sometimes not, many taxa, and this thus contributing to conceal the influence of immigration was sometimes enough to balance historical factors on the current composition of depletion of island populations. island faunas. For example, the occurrence of T. The nonrandom distribution of organisms hermanni on the islands of Elba, Capraia, with poor mobility should be carefully consid- Montecristo, and Pianosa is caused by intro- ered in conservation biogeography, because ductions by man. The occurrence on Monte- local species extinction is not easily compensat- cristo of V. a. hugyi, which is distributed in ed by present immigration (Fattorini, 2008a). south Italy, instead of V. a. francisciredi, which Island populations of species with high dispers- occurs in Tuscany (as well as in other regions of al power can be at least partially reconstituted northern and central Italy) is still puzzling. First, by new immigrants from adjacent source areas. it is questioned whether vipers are present as By contrast, depletion of island populations of the result of long-distance dispersal (e.g., by reptiles, which have relatively low dispersal floating objects) or historical introduction by power, is hardly balanced by new immigrations man. According to Barbanera et al. (2009), from mainland populations, whereas human- vipers were introduced in ancient times, when assisted introduction may represent an addi- these snakes were thrown as weapons during tional serious threat for native species. At attack to vessels coming from Africa and present, the most important influence of man Sardinia to pirate the rich Etruscan towns. They on the Tuscan Islands is represented by tourism were protected as commercial partners by and associated threats. All islands are included Greeks, who established a military base on in the Tuscan Archipelago National Park (al- Montecristo Island. Vipera aspis hugyi speci- though not the entire territory of Capraia, mens, carried by the ancient militia from Magna Giglio, and Elba is under protection). Accesses Graecia during centuries VIII to III BC could to Montecristo, Gorgona, and Pianosa are have originated the Montecristo population strictly regulated. However, other islands are (Barbanera et al, 2009). Also, Zuffi and Bonnet 250 S. FATTORINI

FIG.3. Euleptes europaea under Eucalyptus bark on the Giglio Island.

(1999) put forth the hypothesis that competition flat island because of competition with T. molded the current distribution of the two mauritanica and H. turcicus. subspecies. If in the past the two taxa had been Finally, the occurrence of Z. longissimus on in close proximity in southern Tuscany, a Elba has been long disputed. The species was possible colonization from coastal populations not found after a first record in 1954, which was would have been possible and francisciredi could considered very doubtful, until 2002 (Vaccaro have successively pushed hugyi southward. and Turrisi, 2007). Rarity of Z. longissimus on Indeed, it is possible that a recent establish- Elba has been attributed to habitat degradation ment of V. aspis in Montecristo and P. sicula, T. and loss (in particular, reduction of oak forests), mauritanica, and H. turcicus in several islands but it cannot be excluded that the species has contributed to the final structuring of reptile been imported (Vaccaro and Turrisi, 2007). Lack communities by increased competition. Podarcis of records of this snake for a long time may also sicula is known to be a superior competitor with suggest repeated introductions. respect to other native lizards (Capula, 1992); The continued influence of mankind on the thus, it could be responsible for the absence of Tuscan Islands shaped so profoundly the P. muralis from various islands. Lack of non- natural environment that unnatural habitats random patterns of species co-occurrence ob- may be also of conservation value for reptiles, tained when this species was omitted in tandem such as old constructions that offer shelter for with T. mauritanica and H. turcicus from all various species. This is also the case of islands, V. aspis from Montecristo, and Z. Eucalyptus trees that have been frequently longissimus from Elba supports this hypothesis. planted as ornamental plants. Eucalypts shed However, especially for P. sicula, which occurs their bark regularly. If the outer part of the bark on the adjacent mainland with populations is completely shed but not completely detached genetically close to those of the sampled islands from the trunk (a condition found in a great (Capula, 1992), natural colonization cannot be number of eucalypt species), the shedding excluded in favor of human introductions. process provides suitable resting places for a Similarly, the recent colonization of the geckos number of animals (Fattorini, 2008b). A survey T. mauritanica and H. turcicus, possibly intro- on the Island of Giglio in summer 2008 revealed duced by humans, could have been responsible that these trees now play an important role in for the current absence of E. europaea from reptile conservation providing refuge for E. Gorgona. In continental France, E. europaea europaea, which finds shelter under their bark seems present only in places at higher altitude (Fig. 3). Thus, although conservation and resto- where T. mauritanica and H. turcicus are absent ration plans usually include the extirpation of (Renet et al., 2008). It might be postulated that E. introduced plants and removal of human-made europaea was originally present on Gorgona and habitats, before this happens it should be that it disappeared on this very small and rather necessary to evaluate the implications on REPTILE BIOGEOGRAPHY ON LAND-BRIDGE ISLANDS 251 conservation of animals that appear to rely on ———. 2006b. Detecting biodiversity hotspots by older established exotics or other anthropogenic species-area relationships: a case study of Medi- habitats. terranean beetles. Conservation Biology 20:1169–1180. Acknowledgments ———. 2006c. To fit or not to fit? A poorly fitting .—I wish to express my procedure produces inconsistent results when the gratitude to my wife Federica for her assistance species-area relationship is used to locate hotspots. in the field, to L. Dapporto for continued Biodiversity and Conservation 16:2531–2538. discussions on the biogeography of the Tuscan ———. 2007a. Levels of endemism are not necessarily Islands, and to T. M. Doan, R. Sindaco, A. biased by the co-presence of species with different Venchi, and M. A. L. Zuffi for critical comments range sizes: a case study of Vilenkin & Chikatu- on a first draft of this paper. nov’s models. Journal of Biogeography 34:994–1007. ———. 2007b. Non-randomness in the species-area LITERATURE CITED relationship: testing the underlying mechanisms. Oikos 116:678–689. BALLETTO, E. 2005. Amphibia e Reptilia. In S. Ruffo and F. Stoch (eds.), Checklist e Distribuzione della ———. 2008a. How island geography and shape may Fauna Italiana. 10.000 Specie Terrestri e delle influence species rarity and biodiversity loss in a Acque Interne, pp. 283–287. Museo Civico di Storia relict fauna: a case study of Mediterranean beetles. Naturale di Verona, Verona, Italy. Open Conservation Biology Journal 2:11–20. BARBANERA, F., M. A. L. ZUFFI,M.GUERRINI,A.GENTILI, ———. 2008b. Ecology and conservation of tenebrio- S. TOFANELLI,M.FASOLA, AND F. DINI. 2009. nid beetles in Mediterranean coastal areas. In S. Molecular phylogeography of the asp viper Vipera Fattorini (ed.), Insect Ecology and Conservation, aspis (Linnaeus, 1758) in Italy: evidence for pp. 165–297. Research Signpost, Trivandrum, introgressive hybridization and mitochondrial India. DNA capture. Molecular Phylogenetics and Evo- ———. 2009a. Both Recent and Pleistocene geography lution 52:103–114. determines animal distributional patterns in the BARONI URBANI, C. 1971. Studien zur Ameisenfauna Tuscan Archipelago. Journal of Zoology Italiens XI. Die Ameisen des Toskanischen Archi- 277:291–301. pels. Betrachtungen zur Herkunft der Inselfaunen. ———. 2009b. On the General Dynamic Model of Revue Suisse de Zoologie 78:1037–1067. oceanic island biogeography. Journal of Biogeog- CAPULA, M. 1992. Competitive exclusion between raphy 36:1100–1110. Podarcis lizards from Tyrrhenian islands: Inference ———. 2009c. Faunal patterns in tenebrionids (Cole- from comparative species distributions. In Z. optera: Tenebrionidae) on the Tuscan Islands: Korso´s and I. Kiss (eds.), Proceedings of the 6th the dominance of paleogeography over recent Ordinary General Meeting of the Societas Euro- geography. European Journal of Entomology paea Herpetologica, Budapest 1991, pp. 89–93. 106:415–423. Hungarian Natural History Museum, Budapest. FATTORINI, S., AND A. FOWLES. 2005. A biogeographical ———. 1994. Population genetics of a colonizing analysis of the tenebrionid beetles (Coleoptera, lizard: loss of variability in introduced populations Tenebrionidae) of the island of Thasos in the of Podarcis sicula. Experientia 50:691–696. context of the Aegean Islands (Greece). Journal of CARRANZA, S., AND E. N. ARNOLD. 2006. Systematics, Natural History 39:3919–3949. biogeography and evolution of Hemidactylus geck- FILIPPI, E. 2003. On the proposed elevation of Vipera os (Reptilia: Gekkonidae) elucidated using mito- aspis subspecies to full species rank: a cautionary chondrial DNA sequences. Molecular Phyloge- note. Amphibia-Reptilia 24:235–241. netics and Evolution 38:531–545. FOUFOPOULOS, J., AND A. R. IVES. 1999. Reptile extinc- DAPPORTO, L., AND A. CINI. 2007. Faunal patterns in the tions on land-bridge islands: life-history attributes Tuscan archipelago butterflies: the dominant in- and vulnerability to extinction. American Natural- fluence is recent geography not paleogeography. ist 153:1–25. European Journal of Entomology 104:497–503. GOTELLI, N. J., AND A. M. ELLISON. 2002. Assembly rules DAPPORTO, L., H. WOLF, AND F. STRUMIA. 2007. Recent for New England ant assemblages. Oikos geography determines the distribution of some 99:591–599. flying Hymenoptera in the Tuscan Archipelago. GRAHAM, C. H., T. B. SMITH, AND M. LANGUY. 2005. Journal of Zoology 272:37–44. Current and historical factors influencing patterns FATTORINI, S. 2002a. Biogeography of the tenebrionid of species richness and turnover of birds in the beetles (Coleoptera, Tenebrionidae) on the Aegean Gulf of Guinea highlands. Journal of Biogeography Islands (Greece). Journal of Biogeography 32:1371–1384. 29:49–67. GUERRERO, J. C., J. VARGAS, AND R. REAL. 2005. A ———. 2002b. Relict versus dynamic models for hypothetico-deductive analysis of the environmen- tenebrionid beetles of Aegean Islands (Greece) tal factors involved in the current reptile distribu- (Coleoptera: Tenebrionidae). Belgian Journal of tion pattern in the Canary Islands. Journal of Zoology 132:55–64. Biogeography 32:1343–1351. ———. 2006a. Spatial patterns of diversity in the HARRIS, D. J., V. BATISTA,P.LYMBERAKIS, AND M. A. tenebrionid beetles (Coleoptera, Tenebrionidae) of CARRETERO. 2004. Complex estimates of evolution- the Aegean Islands (Greece). Evolutionary Ecology ary relationships in Tarentola mauritanica (Reptilia: Research 8:237–263. Gekkonidae) derived from mitochondrial DNA 252 S. FATTORINI

sequences. Molecular Phylogenetics and Evolution SMITH, S. A., AND E. BERMINGHAM. 2005. The biogeog- 30:855–859. raphy of lower Mesoamerican freshwater fishes. HAUSDORF, B., AND C. HENNING. 2005. The influence of Journal of Biogeography 32:1835–1854. Recent geography, palaeogeography and climate SOCIETA` ITALIANA DI BIOGEOGRAFIA (ED.). 1974. Il Popola- on the composition of the fauna of the central mento Animale e Vegetale dell’Arcipelago Tos- Aegean Islands. Biological Journal of the Linnean cano. Atti del XX Congresso della Societa` Italiana Society 84:785–795. di Biogeografia. Lavori della Societa` Italiana di MARIOTTI, M. 1990. Floristic connections between the Biogeografia, 5, Forli, Italy. Sardo-Corsican Dominion and the Ligurian area. VACCARO, A., AND G. F. TURRISI. 2007. Ritrovamento di Atti Convegni Accademia Nazionale dei Lincei Zamenis longissimus (Laurenti, 1768) (Reptilia, 85:429–448. Colubridae) sull’Isola d’Elba (Toscana, Italia). Acta MCGARIGAL, K., S. CUSHMAN, AND S. STAFFORD. 2000. Herpetologica 2:59–63. Multivariate Statistics for Wildlife and Ecology VANNI, S., AND A. NISTRI. 2006. Atlante degli Anfibi e dei Research. Springer, New York. Rettili della Toscana. Regione Toscana, Museo di MORAN, M. D. 2003. Arguments for rejecting the Storia Naturale dell’Universita` degli Studi di sequential Bonferroni in ecological studies. Oikos Firenze Sezione di Zoologia ‘‘La Specola,’’ Firenze, 100:403–405. Italy. PIANTELLI, F., F. GIUSTI,F.BERNINI, AND G. MANGANELLI. WHITTAKER, R. J., M. B. ARAU´ JO,P.JEPSON,R.J.LADLE,J. 1990. The mollusc and oribatid fauna on the E. M. WATSON, AND K. J. WILLIS. 2005. Conservation Aeolian and Tuscan archipelagos and the island biogeogarphy: assessment and prospect. Diversity equilibrium theory. Atti Convegni Accademia and Distributions 11:3–23. Nazionale dei Lincei 85:117–154. WHITTAKER, R. J., K. A. TRIANTIS, AND R. J. LADLE. 2008. A RENET, J., O. GERRIET,M.JARDIN, AND D. MAGNE. 2008. general dynamic theory of oceanic island biogeog- Les populations de phyllodactyle d’Europe Eu- raphy. Journal of Biogeography 35:977–994. leptes europaea Gene´, 1839 Reptilia Sauria Gekkoni- ZUFFI, M. A. L. 2002. A critique of the systematic dae dans les Alpes-Maritimes: premiers e´le´ments position of the asp viper subspecies Vipera aspis sur leur re´partition et leur e´cologie. Faune de aspis (Linnaeus, 1758), Vipera aspis atra Meisner, Provence 24/25:117–126. 1820, Vipera aspis francisciredi Laurenti, 1768, Vipera SHI, G. R. 1993. Multivariate data analysis in palaeoe- aspis hugyi Schinz, 1833 and Vipera aspis zinnikeri cology and palaeobiogeography—a review. Pa- Kramer, 1958. Amphibia-Reptilia 23:191–213. laeogeography Palaeoclimatology Palaeoecology ZUFFI, M. A. L., AND X. BONNET. 1999. Italian subspecies 105:199–234. of the asp viper, Vipera aspis: patterns of variability SINDACO, R., G. DORIA,E.RAZZETTI, AND F. BERNINI (EDS.), and distribution. Italian Journal of Zoology Atlante degli Anfibi e dei Rettili d’Italia/ Atlas of 66:87–95. Italian Amphibians and Reptiles. Societas Herpe- tologica Italica Edizioni Polistampa, Firenze, Italy. Accepted: 22 October 2009.