Influences of area, isolation and habitat features on ... - Springer Link

Biodiversity and Conservation 6, 1339±1351 (1997)

In¯uences of area, isolation and habitat features on distribution of snakes in Mediterranean fragmented woodlands LUCA LUISELLI Dipartimento di Biologia Animale e dell'Uomo, UniversitaÁ di Roma `La Sapienza', via Alfonso Borelli 50, I-00161 Roma, Italia

DARIO CAPIZZI Istituto Nazionale per la Fauna Selvatica, via Ca' Fornacetta 9, I-40064 Ozzano Emilia (Bologna), Italia

Received 2 September 1996; revised and accepted 24 January 1997 The eects of isolation-related and vegetational parameters on presence and relative abundance of snakes in patchy forested fragments of Mediterranean central Italy are studied. The most abundant species was Coluber viridi¯avus (accounting for 47.7% of the total snake sample observed) followed by Vipera aspis (22%), Elaphe longissima (21.5%), Natrix natrix (7.7%), and Coronella austriaca (1.1%). There was a clear trend for bigger species to be less distributed among the various forest fragments than the smaller species. Presence of Coluber viridi¯avus, Coronella austriaca and Natrix natrix was not in¯uenced by woodland area, whereas that of Vipera aspis and Elaphe longissima was positively in¯uenced by woodland area. Woodland isolation parameters did not in¯uence the presence of Coluber viridi¯avus, Coronella austriaca and Natrix natrix, but of Vipera aspis and Elaphe longissima. Discriminant stepwise analysis suggested that speci®c environmental features in¯uenced the occurrence and abundance of the various snake species, Vipera aspis being the taxon more aected by isolation-related parameters. Some conservation implications of our observations are also discussed. Keywords: snakes; isolation; environmental features; habitat fragmentation; Mediterranean.

Introduction Habitat loss and fragmentation are major causes of decreasing biodiversity in the developed and highly industrialized countries of western Europe (Ehrlich and Wilson, 1991; Wilson, 1992). This is not only due to extinction caused by disruption of dispersal by augmented isolation (see Beier, 1993), but also by fragmentation-induced habitat changes (Anglestam, 1992), stochastic extinction of small populations (Hinsley et al., 1996), as well as many other causes. Thus, the recent years have been characterized by a strong eort by ecologists to understand mechanisms of extinction in fragmented habitats and to de®ne the determinants of distribution of free-ranging animal populations in patchy biotopes (Wilson, 1992). Several ecological aspects (e.g. species minimum area requirements) have been inferred from incidence functions constructed from presence-absence data for fragmented habitats (see AndreÂn, 1994), whereas very few studies investigated regional population sizes as limiting factors (but see Hinsley et al., 1996). Moreover, most of these studies dealt with mammals and birds, whereas amphibians and reptiles have been scarcely studied up to now. This is a strong shortcoming to our knowledge, as amphibians and reptiles 0960-3115 Ó 1997 Chapman & Hall

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Luiselli and Capizzi

frequently form small, virtually isolated metapopulations that, due to their small size, are probably submitted to greater vulnerability and risk of stochastic extinction (Balletto and Giacoma, 1993a, b). Due to their nature as large sized predators, snakes are normally even less abundant in the ®eld than other reptiles, their populations being sometimes composed of a few adult specimens (e.g. see Rugiero and Luiselli, 1996). Thus, they probably are even more submitted to risks of local extinction due to habitat fragmentation and habitat loss, other than genetic isolation (Corbett, 1989). In fact, snakes are generally able of only limited dispersal across urbanized and cultivated areas (e.g. see Capizzi and Luiselli, 1996a), thus remaining virtually isolated when their natural habitats (woods) become fragmented by human practices (Corbett, 1989). In this paper we examine, for the ®rst time to our knowledge, the distribution and relative abundance of terrestrial Mediterranean snakes in an area of central Italy where considerable deforestation has occurred in the past. We have attempted to correlate the in¯uences of isolation, area, and wood ¯oristic composition and structure to the snake populations of this Mediterranean woodland. Materials and methods 1. Study areas All data given here were collected during surveys conducted in June±November 1995 and in March±June 1996 in a wide territory of northern Latium (province of Viterbo, central Italy). This territory, about 517 km2 includes 134 forested fragments interspersed with wide cultivations, roads and villages. Thirty dierent woodlots (i.e. 22.4% of the total number of forested fragments of the area) were surveyed in this study. The various wooded fragments diered from each other in terms of (i) surface area (size range 1.7±84 ha), (ii) degree of isolation and (iii) vegetation characteristics. Considering the whole study area, the total amount of habitat loss (sensu AndreÂn, 1994) was 78.1%. 2. Environmental variables For each wood fragment we measured ®ve isolation-related variables: (i) total wooded surface (TWS), (ii) number of fencerows (NF) radiating from the forested fragment, (iii) linear distance (in km) from the closest wood fragment (DCW), (iv) total surface of the closest wood fragment (SCW), and (v) residual habitat (RH) (sensu AndreÂn, 1994) in one kilometre radius from the woodlot centre. Moreover, in each woodlot we selected ®ve sampling transects well representative of the whole environmental characteristics. Each transect was 25 m long and 4 m wide, thus accounting for 100 m2. In every transect we measured the following variables: (i) tree species diversity (assessed with Simpson's (1949) index) composition (TSC), (ii) total density per ha of tree stems (DTS), (iii) mean height of trees (MHT, measured by means of an Haga altimeter to the nearest 0.5 m), (iv) mean diameter of trees (MDT, measured at 1.3 m from the ground), (v) number of vegetation strata (NVS, recorded in ten randomly selected sites within each transect, by checking for presence or absence of vegetation at dierent heights from the ground: 0.5 m, 1 m, 2 m, 4 m, 8 m, 16 m), (vi) undergrowth shrub species diversity (USD, assessed with Simpson's (1949) index), (vii) total number of

Snakes and fragmented forests

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shrub branches (NSB), and (viii) percentage occurrence of three key species of shrubs: Rubus sp. (POR), Cytisus scoparius (POC), and Phillyrea latifolia (POP). 3. Snake census Snakes were found during standardized routes along the study areas. The ®eld-trips were always done during sunny days, i.e. under atmospheric conditions ideal for thermoregulation and activity of snakes. Most of the trips were done between 08:00 and 16:30 (European Standard Time), but occasionally later. Snakes were captured by hand. If a snake was captured, it was permanently marked by scale-clipping and then dorsally painted with a white number for visual identi®cation at distance. After these procedures, the snake was set free unharmed at the point of capture. Repeated ®eld-trips enabled us to obtain a rather detailed list of the snake species present in each forest fragment. However, to have a reliable and standardized estimation of the relative frequency of the various species in each wooded fragment, we weighed our sampling eort depending on the woodlot area. For wood fragments 15 ha, our sampling eort was ®ve hours in each sampling period (repeated twice in the year). Since it is well known that sympatric snake species may show dierent seasonal peaks of activity (i.e. with some species more active in spring and other ones more active in autumn ± see Gibbons and Semlitsch (1987) and Filippi (1995), we surveyed each wood fragment in two dierent seasons (August±November and March±June). The total number of ®eld-eort hours was 216. We noted all the snake individuals observed in each wood fragment. 4. Variables regarding snakes For snakes, we calculated three dierent groups of variables. The ®rst group included general community parameters, i.e. (i) taxonomical diversity of snake community in each wood fragment (TDS, assessed with Simpson's (1949) index), and (ii) total number of snakes encountered per eort hour (NSH). The second group included the percentage shares of the various snake species in each snake assemblage observed in each wood fragment: percentage share of Coluber viridi¯avus is given by PCV, of Elaphe longissima by PEL, of Coronella austriaca by PCA, of Natrix natrix by PNN, and of Vipera aspis by PVA. The third group included the number of individuals of each snake species encountered per eort hour: number of Coluber viridi¯avus is given by NCV, of Elaphe longissima by NEL, of Coronella austriaca by NCA, of Natrix natrix by NNN, and of Vipera aspis by NVA. 5. Statistical analyses All statistical tests were two-tailed, and a was set at 5%. The SAS microcomputer package was used. All variables were normalized and the variance structure stabilized using Log10 (x+1) transformation (see Zar, 1984; Townsend and Crowl, 1991). Data from each forest fragment were checked for presence or absence of the various snake species. Then, discriminant analysis was done on every species but Coluber viridi¯avus and Coronella austriaca, as the former was present in all woods but one, and the latter was present in too low a number of woods for signi®cant analysis. Moreover, woods were grouped by using dierent Ôdegrees' of (i) snake species diversity and (ii) total number of snake species, and by using dierent Ôdegrees' of abundance (= total number of

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snakes per eort hour) of the various snake species (high abundance and low abundance). To avoid potential artifacts in the analyses due to the homogeneous distribution of the various snake-variables, in the latter set of analyses we excluded the wood fragments with intermediate values of snake abundance. Results We observed a total of 377 snakes belonging to ®ve dierent species: four Colubridae (Coluber viridi¯avus, Elaphe longissima, Coronella austriaca and Natrix natrix) and one Viperidae (Vipera aspis). The most abundant species was Coluber viridi¯avus, accounting for 47.7% of the total snake sample observed. Vipera aspis accounted for 22%, Elaphe longissima for 21.5%, Natrix natrix for 7.7% and Coronella austriaca for 1.1%. 1. Eects of wood area on occurrence of snakes Coluber viridi¯avus was found in 96.6%, Elaphe longissima in 73.3%, Coronella austriaca in 13.3%, Natrix natrix in 46.7%, and Vipera aspis in 66.7% of the surveyed wood fragments. Considering the average log (x+1) length/mass ratio for each snake species (data from our unpublished research), there was a clear trend for bigger species to be less distributed among the various wood fragments of the study area than the smaller species (Pearson's r = 0.870, P = 0.05), despite the low number of regression points (n = 5). The proportional incidence of the ®ve snake species in relation to woodland area is shown in Fig. 1. Proportional incidence is shown for ®ve woodland groups: (i) woods of

Figure 1. Proportional incidence of snakes in relation to woodlot area in the studied territory of Mediterranean central Italy.


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0±3 ha (n = 6), (ii) woods of 4±7 ha (n = 7), (iii) woods of 8±15 ha (n = 5), (iv) woods of 16±30 ha (n = 6), and (v) woods >31 ha (n = 6). The incidences of Coluber viridi¯avus, Coronella austriaca and Natrix natrix were not in¯uenced by woodland area (Fisher exact test, P > 0.3), whereas the incidences of Vipera aspis and Elaphe longissima were strongly positively in¯uenced by woodland area (Fisher exact test, P < 0.05). Moreover, the incidences of Coluber viridi¯avus, Coronella austriaca, Elaphe longissima and Natrix natrix were not signi®cantly in¯uenced by woodland isolation, whereas the incidences of Vipera aspis and Elaphe longissima were positively aected by higher proportions of RH (Fig. 2). 2. General correlations Statistically signi®cant correlations of NSH and TDS versus the various environmental variables are given in Table 1. According to the table, NSH was positively correlated with NF, RH, POC, SCW, and negatively with MDT, whereas TDS was positively correlated with TWS, NF, DTS, and negatively with MDT. 3. Speci®c correlations Statistically signi®cant correlations of percentage shares of occurrence of the various snake species versus the various environmental variables are given in Table 2. The Vipera aspis percentage share of occurrence was positively correlated with TWS, NF, RH, SCW, DTS, and negatively with MDT, POP. Coluber viridi¯avus percentage share of occurrence was positively correlated with POR, and negatively with NF, DTS. Coronella austriaca percentage share of occurrence was positively correlated with DCW, MHT, but it was not

Figure 2. Proportional incidence of snakes in relation to residual habitat (%) in the studied territory of Mediterranean central Italy.

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Luiselli and Capizzi Table 1. Statistics of the correlations between NSH, TDS and the various environmental variables recorded in each forest fragment within the studied territory in Mediterranean central Italy Variables

TDS

TWS NF DCW RH SCW DTS NSB TSC USD MDT MHT NVS POR POC POP

r r r r r r r r r r r r r r r

= = = = = = = = = = = = = = =

NSH 0.355; p = 0.055 0.688; p = 0.000001 0.213; p = 0.258 0.348; p = 0.059 0.333; p = 0.073 0.357; p = 0.053 0.025; p = 0.897 0.200; p = 0.289 0.186; p = 0.325 )0.547; p = 0.002 0.019; p = 0.92 0.315; p = 0.09 )0.28; p = 0.134 0.28; p = 0.134 )0.301; p = 0.106

r r r r r r r r r r r r r r r

= = = = = = = = = = = = = = =

0.259; p = 0.167 0.420; p = 0.021 0.034; p = 0.857 0.429; p = 0.018 0.458; p = 0.011 0.218; p = 0.246 0.221; p = 0.241 0.066; p = 0.73 0.149; p = 0.434 )0.408; p = 0.025 )0.032; p = 0.868 0.202; p = 0.285 0.001; p = 0.999 0.392; p = 0.032 )0.360; p = 0.05

Signi®cant correlations are presented in bold-face.

negatively correlated with any speci®c variable. Elaphe longissima percentage share of occurrence was positively correlated with NF, and negatively with MDT, POP. Natrix natrix percentage share of occurrence was positively correlated with TSC, NVS, but it was not negatively correlated with any speci®c variable. Statistically signi®cant correlations of number of individuals of each snake species encountered per eort hour versus the various environmental variables are given in Table 3. Number of Vipera aspis was positively correlated with TWS, NF, RH, SCW, DTS, POC, and negatively with MDT, POP. Number of Coluber viridi¯avus was positively correlated with POR, but was not negatively correlated with any variable. Number of Coronella austriaca was positively correlated with DCW, MHT, but was not negatively correlated with any variable. Number of Elaphe longissima was positively correlated with NF, DTS, and negatively with MDT. Number of Natrix natrix was positively correlated with NF, NVS, but not negatively with any variable. 4. Distance among wood fragments in the multivariate space A cluster (WPGMA amalgamation model) of distance among forested fragments as resulted from total number of snakes per hour is shown in Fig. 3. Three main clusters are formed: one is constituted essentially by all the cork oak fragments and the very isolated chestnut and deciduous oak forests, whereas the second group is constituted almost exclusively by deciduous oak forests and the third group is constituted primarily by chestnut forests. Scores of the ®rst three factors relative to the various wood fragment types from a principal component analysis (of both percentage shares of occurrence of the various snake species and number of snakes per hour) were divided quite well in the multivariate space (Fig. 4).


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Table 2. Statistics of the correlations between percentage shares of occurrence of the various snake species versus the various environmental variables recorded in each forest fragment within the studied territory in Mediterranean central Italy Variables

C. austriaca

C. viridi¯avus

E. longissima

N. natrix

V. aspis

TWS

r = )0.025; p = 0.896 r = 0.135; p = 0.478 r = 0.459; p = 0.011 r = )0.04; p = 0.832 r = )0.166; p = 0.381 r = 0.208; p = 0.269 r = )0.045; p = 0.813 r = )0.216; p = 0.252 r = )0.077; p = 0.687 r = )0.056; p = 0.77 r = 0.424; p = 0.02 r = 0.134; p = 0.48 r = )0.156; p = 0.411 r = 0.111; p = 0.559 r = 0.128; p = 0.499

r = 0.036; p = 0.851 r = )0.364; p = 0.048 r = )0.023; p = 0.904 r = )0.115; p = 0.547 r = )0.145; p = 0.445 r = )0.387; p = 0.035 r = )0.101; p = 0.594 r = )0.108; p = 0.569 r = 0.246; p = 0.19 r = 0.310; p = 0.095 r = )0.088; p = 0.644 r = )0.292; p = 0.118 r = 0.42; p = 0.021 r = 0.05; p = 0.795 r = )0.197; p = 0.298

r= p= r= p= r= p= r= p= r= p= r= p= r= p= r= p= r= p= r= p= r= p= r= p= r= p= r= p= r= p=

r = 0.012; p = 0.948 r = 0.288; p = 0.123 r = 0.167; p = 0.379 r = 0.022; p = 0.909 r = 0.203; p = 0.281 r = 0.005; p = 0.978 r = )0.011; p = 0.953 r = 0.369; p = 0.045 r = 0.278; p = 0.137 r = )0.308; p = 0.098 r = )0.200; p = 0.289 r = 0.377; p = 0.04 r = )0.239; p = 0.203 r = 0.210; p = 0.266 r = 0.124; p = 0.514

r = 0.455; p = 0.011 r = 0.680; p = 0.00001 r = 0.055; p = 0.774 r = 0.578; p = 0.001 r = 0.409; p = 0.025 r = 0.416; p = 0.022 r = 0.155; p = 0.413 r = 0.029; p = 0.88 r = 0.082; p = 0.667 r = )0.539; p = 0.002 r = 0.028; p = 0.884 r = 0.173; p = 0.362 r = )0.272; p = 0.146 r = 0.231; p = 0.22 r = )0.435; p = 0.016

NF DCW RH SCW DTS NSB TSC USD MDT MHT NVS POR POC POP

0.262; 0.162 0.653; 0.00001 0.062; 0.747 0.292; 0.117 0.241; 0.2 0.348; 0.06 )0.037; 0.846 0.086; 0.65 0.074; 0.696 )0.391; 0.032 0.129; 0.497 0.203; 0.282 )0.198; 0.294 0.089; 0.639 )0.359; 0.05


5. Distance among snakes in the multivariate space Loadings of the ®rst three factors resulting from a principal component analysis of number of snakes per hour are shown in Fig. 5. Based on the ®gure, it is clear that Vipera aspis and Elaphe longissima were very similar in their environmental requirements, whereas Coronella austriaca, Natrix natrix and Coluber viridi¯avus were quite distant from each other. 6. Factors in¯uencing presence/absence of snakes Discriminant stepwise analysis performed on three snake species indicated species-speci®c variations in the factors in¯uencing their presence or absence. In particular, presence of Vipera aspis (Wilks' k = 0.34, n = 30, ANOVA F5,24 = 9.3, P < 0.00001) was strongly

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Table 3. Statistics of the correlations between number of snake individuals encountered per eort hour versus the various environmental variables recorded in each forest fragment within the studied territory in Mediterranean central Italy Variables

C. austriaca

C. viridi¯avus

E. longissima

N. natrix

V. aspis

TWS

r = 0.082; p = 0.666 r =0.115; p = 0.546 r = 0.367; p = 0.046 r = )0.063; p = 0.74 r = )0.142; p = 0.453 r = 0.209; p = 0.268 r = )0.031; p = 0.872 r = )0.214; p = 0.256 r = )0.125; p = 0.509 r = )0.039; p = 0.838 r = 0.357; p = 0.053 r = 0.135; p = 0.476 r = )0.187; p = 0.324 r = 0.044; p = 0.816 r = )0.124; p = 0.515

r = 0.045; p = 0.812 r = )0.15; p = 0.428 r = )0.095; p = 0.616 r = 0.208; p = 0.27 r = 0.237; p = 0.207 r = )0.224; p = 0.234 r = 0.169; p = 0.373 r = 0.063; p = 0.742 r = 0.189; p = 0.318 r = 0.119; p = 0.531 r = )0.07; p = 0.715 r = )0.054; p = 0.777 r = 0.378; p = 0.039 r = 0.249; p = 0.184 r = )0.113; p = 0.554

r = 0.223; p = 0.236 r = 0.547; p = 0.002 r = 0.036; p = 0.852 r = 0.263; p = 0.161 r = 0.246; p = 0.191 r = 0.365; p = 0.047 r = 0.034; p = 0.857 r = 0.026; p = 0.891 r = 0.103; p = 0.587 r = )0.465; p = 0.01 r = 0.073; p = 0.701 r = 0.169; p = 0.373 r =)0.153; p = 0.419 r = 0.210; p = 0.266 r = )0.34; p = 0.066

r = )0.021; p = 0.914 r = 0.372; p = 0.043 r = 0.092; p = 0.63 r = 0.138; p = 0.466 r = 0.324; p = 0.081 r = 0.087; p = 0.648 r = 0.067; p = 0.724 r = 0.294; p = 0.115 r = 0.091; p = 0.632 r = )0.351; p = 0.057 r = )0.207; p = 0.272 r = 0.377; p = 0.04 r = )0.158; p = 0.403 r = 0.276; p = 0.14 r = 0.001; p = 0.999

r = 0.465; p = 0.010 r = 0.518; p = 0.003 r = 0.042; p = 0.827 r = 0.553; p = 0.002 r = 0.516; p = 0.004 r = 0.422; p = 0.02 r = 0.277; p = 0.138 r = 0.005; p = 0.979 r = 0.067; p = 0.727 r = )0.575; p = 0.001 r = 0.044; p = 0.816 r = 0.133; p = 0.485 r = )0.228; p = 0.226 r = 0.395; p = 0.031 r = )0.377; p = 0.04

NF DCW RH SCW DTS NSB TSC USD MDT MHT NVS POR POC POP


in¯uenced by NF (Wilks' k = 0.408, P < 0.04), whereas that of Elaphe longissima (Wilks'k = 0.563, n = 30, ANOVA F1,28 = 21.752, P < 0.00001) was in¯uenced only by NF (Wilks' k = 1.0, P < 0.0001), and that of Natrix natrix (Wilks' k = 0.617, n = 30, ANOVA F4,25 = 3.885, P < 0.02) was signi®cantly in¯uenced only by DCW (Wilks' k = 0.747, P < 0.03). 7. Factors in¯uencing abundance and diversity of snakes Discriminant stepwise analysis performed on Ôdegrees' of abundance of the total number of snakes per eort hour (Wilks' k = 0.499, n = 23, ANOVA F5,17 = 3.41, P < 0.03) indicated that only RH (Wilks' k = 0.655, P < 0.04) strongly in¯uenced the abundance of snakes at the local scale.


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Figure 3. Dendrogram (WPGMA method) based on the distance among forest fragments as resulted from the total number of snakes encountered per eort hour. C = Chestnut; D = Deciduous oak forest; K = Cork oak forest.

Discriminant stepwise analysis performed on the snake species diversity (Wilks' k = 0.398, n = 22, ANOVA F4,17 = 6.43, P < 0.003) indicated that NF (Wilks' k = 0.569, P < 0.02) and TWS (Wilks'k = 0.544, P < 0.03) strongly in¯uenced the above parameter. Discriminant stepwise analysis performed on three snake species indicated species-speci®c variations in the factors in¯uencing their degree of abundance (high and low abundance). In particular, degree of abundance of Vipera aspis (Wilks'k = 0.112, n = 14, ANOVA F8,5 = 4.98, P < 0.047) was strongly in¯uenced by DTS (Wilks'k = 0.475, P < 0.01) and NF (Wilks' k = 0.249, P = 0.05), whereas that of Elaphe longissima (Wilks' k = 0.655, n = 12, ANOVA F2,9 = 2.37, P > 0.14) and Coluber viridi¯avus (Wilks' k = 0.862, n = 19, ANOVA F2,16 = 1.28, P > 0.3) were not statistically signi®cant. Discussion In general, our analysis suggests that both isolation-related and vegetational parameters aect the distribution and relative abundance of snakes in the Mediterranean regions of central Italy, but that the former parameters are more important than the latter ones. The presence or absence of all snake species is strongly conditioned by the number of fencerows and the linear distance from the closest forest fragment, i.e. ultimately by the relative isolation of each wooded zone. The number of fencerows is likely to be important for snake dispersal, especially during the mating season (March±May, e.g. see Luiselli, 1996) when the males typically engage in long displacements searching for females (Madsen et al., 1993; Shine et al., 1997). To do this, they usually use Ôpreferential corridors'

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Figure 4. Scores of the ®rst three factors relative to the various wood fragment types as resulted from PCA of both percentage shares of occurrence of the various snake species and number of snakes encountered per eort hour.

Figure 5. Loadings of the ®rst three factors resulting from PCA of number of snakes encountered per eort hour. NN = Natrix natrix; CV = Coluber viridi¯avus; EL = Elaphe longissima; CA = Coronella austriaca; VA = Vipera aspis.


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as edges surrounding cultivated or semicultivated ®elds (see Saint Girons, 1996; Luiselli et al., unpublished). In this regard, it should be considered that the structure of several snake metapopulations (especially of the viperid ones) follows the prediction model of Boorman and Levitt (1973), with unidirectional gene ¯ow and extinction occurring primarily in the smaller sites (Capula and Luiselli, 1994). In this regard, however, we have no genetic data to de®nitely support this view in the cases of the species studied. Therefore, in this light, the linear distance of the closest wood could also be of some relevance, especially if one considers that vagility of snake populations is well known to be relatively low, especially in inadequate habitats (see Dodd, 1993). In general, habitat features proved to be less important than isolation-related variables. An exception is constituted by Vipera aspis, which was conditioned by speci®c habitat factors (see below). This may also be explained by considering that the viper distribution is dependent on speci®c prey types (i.e. the rodent Apodemus sylvaticus as far as central Italy is concerned ± see Luiselli et al., 1994) typically present in residual portions of Mediterranean forests (Capizzi and Luiselli, 1966b). The relative unrelatedness of other snake populations to speci®c habitat features could be explained by considering that these snake species are habitat generalists, able to inhabit extremely diverging biotopes in the plains and in the mountains as well (Bruno and Maugeri, 1990). The fact that Coluber viridi¯avus was the species less conditioned by the isolationrelated variables is not surprising as it is an opportunist predator (e.g. see Capizzi et al., 1995) able to reach high population densities even in highly anthropized or suburban areas (Bruno and Maugeri, 1990). This is also con®rmed by the fact that Coluber viridi¯avus was the only species found in the cork oak forests, which are the forest types more intensively managed by human practices in the study region. Number of fencerows also in¯uenced the abundance of snake populations and, to a lower degree, even the diversity of the snake community in each woodlot. Residual habitat, however, was the most important factor for snake diversity. Our multivariate analyses suggested that speci®c habitat features (e.g. total density per ha of tree stems and number of shrub branches) could in¯uence the degree of abundance of Vipera aspis. However, this tendency is not so clear for Elaphe longissima and Coluber viridi¯avus. We suggest that the above pattern could be due to the relative specialization of the viper as a predator of speci®c rodent taxa, whereas the latter two snake species are potential predators of lizards widely spread in Mediterranean biotopes (see Capizzi and Luiselli, 1996a). The fact that isolation rather than area has an important eect on snake occurrence mirrors data already published on the distribution of other taxa, e.g. the dormouse (Muscardinus avellanarius) in Britain (Bright et al., 1994). With regard to western European snakes, two further examples are useful to con®rm this conclusion. In the intensively cultivated regions of the ÔLoire Atlantique' (western France) the snakes Vipera aspis, Natrix natrix and Coluber viridi¯avus inhabit the mosaic of edges and small wood patches interspersed among cultivations (see Saint Girons, 1996), whereas in intensively cultivated areas of southern Italy where wooded patches are practically unavailable to snakes (e.g. in wide zones of Apulia, province of Lecce), the snakes Elaphe situla, Elaphe quatuorlineata and Coluber viridi¯avus are found only in the bushy strips (just a few metres wide) bordering the cultivations. Despite the very little area of suitable habitat available, stable populations of these snakes are able to survive due to the good rates of immigration from adjacent places connected by these natural bushy corridors (Agrimi and Luiselli, in prep.).

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Our observations have of course some conservation implications. In particular, any conservation programme intended to impede further decline of snake populations in the studied region should carefully take into consideration the need for maintaining a number of fencerows between wooded fragments to permit emigration and immigration between dierent metapopulations. This is especially true for eectively protecting populations of the species with low dispersal tendency, i.e. vipers (Vipera aspis), Aesculapian snakes (Elaphe longissima) and smooth snakes (Coronella austriaca), whereas minor problems are expected with regard to Coluber viridi¯avus and Natrix natrix, two taxa usually able to colonize new areas and to inhabit urbanized areas as well. With regard to Coronella austriaca, it is interesting to note that management suggestions similar to those given by us have also been proposed by various scientists involved in the conservation of the few remaining free-ranging populations in southern Britain, where this snake is seriously endangered (see Spellerberg, 1977, 1982, 1987, 1988; Goddard and Spellerberg, 1980). Acknowledgements We thank several friends who co-worked with us in the ®eld. Among them, it is a pleasure to thank Claudio Anibaldi, Fatima Evangelisti, Riccardo Guidoni, Roberto Papi, Jenny Rosario Aguilar, Lorenzo Rugiero, and Veronica Trujillo Jesus. Earlier versions of this manuscript bene®ted from the very helpful comments of Umberto Agrimi, Francesco M. Angelici, Massimo Capula, and an anonymous referee. References AndreÂn, H. (1994) Eects of habitat fragmentation on birds and mammals in landscapes with dierent proportions of suitable habitat: a review. Oikos 71, 355±66. Anglestam, P. (1992) Conservation of communities ± the importance of edges, surroundings and landscape mosaic structure. In Ecological principles of nature conservation: application in temperate and boreal environments (L. Hansson, ed.) pp. 9±70. London: Elsevier. Balletto, E. and Giacoma, C. (1993a) Struttura di popolazione e probabilitaÁ di sopravvivenza a medio termine in alcune specie di an®bi. Suppl. Ric. Biol. Selvaggina 21, 135±50. Balletto, E. and Giacoma, C. (1993b) Stochastic extinction probability for European populations of Hyla arborea: an approach by VORTEX. In Ecology and conservation of the European tree frog (A.M.T. Stumpel and U. Tester, eds) pp. 81±90. Potsdam. Beier, P. (1993) Determining minimum habitat areas and habitat corridors for Cougars. Conserv. Biol. 7, 94±108. Boorman, S.A. and Levitt, P.R. (1973) Group selection on the boundary of a stable population. Theor. Popul. Biol. 4, 85±128. Bright, P.W., Mitchell, P. and Morris, P.A. (1994) Dormouse distribution: survey techniques, insular ecology and selection of sites for conservation. J. Appl. Ecol. 31, 329±39. Bruno, S. and Maugeri, S. (1990) Serpenti d'Italia e d'Europa. Milano: Editoriale Giorgio Mondadori. Capizzi, D., Luiselli, L., Capula, M. and Rugiero, L. (1995) Feeding habits of a Mediterranean community of snakes in relation to prey availability. Rev. Ecol. (Terre et vie) 50, 353±363. Capizzi, D. and Luiselli, L. (1996a) Feeding relationships and competitive interactions between phylogenetically unrelated predators (owls and snakes). Acta Oecol. 17, 265±84. Capizzi, D. and Luiselli, L. (1996b) Ecological relationships between small mammals and age of coppice in an oak-mixed forest in central Italy. Rev. Ecol. (Terre et Vie) 51, 277±91.


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