are protected areas truly protected? the impact of road traffic on vertebrate fauna

ORI GIN AL PA PER

Are protected areas truly protected? The impact of roadtraffic on vertebrate fauna

Nuria Garriga • Xavier Santos • Albert Montori • Alex Richter-Boix •

Marc Franch • Gustavo A. Llorente

Received: 9 January 2012 / Accepted: 6 July 2012 / Published online: 25 July 2012� Springer Science+Business Media B.V. 2012

Abstract The extension of road networks is considered one of the major factors affecting

fauna survival. Roadkill has been documented widely and affects all taxonomic groups.

Although roadkill is associated mainly with traffic density, some life-history traits of

species and the area surrounding roads are expected to modify number of roadkills both

taxonomically and geographically. Here we studied the number of roadkills of vertebrates

in an extensive region in the northeastern Iberian Peninsula. We surveyed 820 km of 41

roads in two different seasons (spring and autumn), that differ in traffic intensity. In

addition, we covered zones with distinct climatic characteristics and levels of protection of

the surrounding habitats. Amphibians showed the highest number of roadkills whereas

reptiles, birds and mammals had similar rates. General Linear Model tests showed no

differences in roadkills by climatic region; however, differences in number of roadkills

were linked to protection status, with the highest number of casualties in highly protected

areas. Redundancy Analysis demonstrated that the number of amphibians and reptiles

killed was associated with roads in highly protected areas whereas that of mammals and

birds was linked to unprotected areas. Protected areas often receive many visitors, which in

turn may increase wildlife casualties as a result of greater traffic density. We recommend

that correction measures be taken to reduce the high number of vertebrate fauna killed

along roads that cross protected areas.

Electronic supplementary material The online version of this article (doi:10.1007/s10531-012-0332-0)contains supplementary material, which is available to authorized users.

N. Garriga (&) � X. Santos � A. Montori � M. Franch � G. A. LlorenteDep. Biologia Animal, Universitat de Barcelona, Avgda. Diagonal 643, 08028 Barcelona, Spaine-mail: [email protected]

X. SantosCentro de Investigacao em Biodiversidade e Recursos Geneticos (CIBIO), Universidade do Porto,Campus Agrario de Vairao, 4485-661 Vairao, Portugal

A. Richter-BoixDepartment of Population Biology and Conserv Biol, Uppsala Universitet, Norbyvagen 18 D,752 36 Uppsala, Sweden

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Biodivers Conserv (2012) 21:2761–2774DOI 10.1007/s10531-012-0332-0

http://dx.doi.org/10.1007/s10531-012-0332-0

Keywords Roadkills � Protected area � Habitat fragmentation � Road ecology �Vertebrates

Introduction

In recent decades, anthropogenic disturbance of wildlife habitats and biota has increased

because of human population growth and human–environment interactions (Wittmeyer

et al. 2009). The extension of road networks is one of the major disturbances for fauna

(Jaarsma et al. 2006). Road construction and exploitation entails habitat destruction,

population fragmentation (Mader 1984), and consequently vertebrate mortality (Forman

and Alexander 1998; Trombulak and Frissell 2000; Lesbarreres et al. 2003; Malo et al.

2004). Demographic decline in fauna located near roads has occurred (Jones 2000;

Mumme et al. 2000; Gibbs and Shriver 2005; Row et al. 2007), even for common species

that have, a priori, large enough populations to sustain high road mortality (Forman and

Alexander 1998).

The incidence of animals killed on roads is influenced by extrinsic (e.g. habitat near

roads, climate and local weather conditions, and transportation characteristics) and

intrinsic (e.g. species life-history traits) factors (Ashley and Robinson 1996; Clevenger

et al. 2003; Puky 2005), among others. Trombulak and Frissell (2000) reported that traffic

volume is the greatest contributor to roadkills, whereas Hels and Buchwald (2001)

observed that amphibian’s vulnerability to road mortality were mainly determined by the

velocity of species, their diurnal activity patterns, as well as the diurnal traffic activity.

Despite evidence that road mortality has no geographical or taxonomical restrictions

(Taylor and Goldingay 2004), it does not affect all taxonomic groups in the same way.

Amphibians and reptiles are the most affected (Ashley and Robinson 1996; Forman and

Alexander 1998; Smith and Dodd 2003; Glista et al. 2008), and the decline of their

populations has been attributed to road mortality worldwide (Fahrig et al. 1995; Gibbs and

Shriver 2002, 2005; Marchand and Litvaitis 2004; Steen and Gibbs 2004). Most amphibian

roadkills occur during individual adult migration to breeding ponds (van Gelder 1973;

Cooke, 1995; Glista et al. 2008). Such migration is strongly related to rainfall pattern and

annual pond flooding (Salvador and Carrascal 1990; Jakob et al. 2003). With regard to

reptiles, their activity is more related to temperature oscillations (Adolph and Porter 1993)

and their use of the road surface as a thermoregulatory source (Bernardino and Dalrymple

1992; Rudolph et al. 1999). Roadkill also occurs in mammals and birds, which use roads as

dispersal corridors (Huey 1941; Getz et al. 1978) or food sources (Dhindsa et al. 1988;

Pinowski 2005).

Road traffic is also detrimental to wildlife in protected areas (Bernardino and Dalrymple

1992; Drews 1995; Clevenger et al. 2003; Ramp et al. 2006), and is a major concern of US

National Park Service managers (Ament et al. 2008). Protected areas are commonly fre-

quented by tourists and local residents, and therefore subjected to regular traffic. Local

fauna is thus endangered by roads that cross natural areas (Hartmann et al. 2011). Ber-

nardino and Dalrymple (1992) reported an example in the Everglades National Park, where

the seasonal activity of the snake community coincides with the periods of greatest tour-

ism. This finding suggests that wildlife populations in National Parks are not necessarily

more protected than those inhabiting areas outside the boundaries of these areas (Newmark

1995; Ament et al. 2008). When a particular site is protected because of its wildlife

diversity and quality, it would be reasonable to assume that road traffic will decrease

wildlife unless appropriate measures are taken to minimize this impact.

2762 Biodivers Conserv (2012) 21:2761–2774

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The following factors may simultaneously affect road mortality rates: protection status

of the area, number of species present, traffic intensity, and the climate and season sur-

veyed. Most studies addressing road mortality have designed surveys in small local

regions, comprising a few lineal kilometers (e.g. van Gelder 1973; Vijayakumar et al.

2001; Smith and Dodd 2003; Langen et al. 2007, 2009; Elzanowski et al. 2009), but over

extensive periods (Cooke 1995; Clevenger et al. 2003) or intensively surveyed (Ashley and

Robinson 1996; Clevenger et al. 2001b; Glista et al. 2008).

Nevertheless, comparison of the relevance of these factors calls for the design of

stratified surveys on a road network within an extensive region. European countries are

suitable candidates for this purpose as not only do they have dense road networks but also

many protected areas. This is the case of Catalonia (northeastern Spain), where

1,244,876 ha of protected area (39.6 % of the total extension) coexist with more than

12,000 km of a dense road network. We quantified vertebrate number of roadkills in

Catalonia and examined the most significant factors (extrinsic and intrinsic) that explain

this cause of death. Here we sought to determine some of the factors that influence roadkill

occurrence. For this purpose we addressed the following questions: (1) Are there more

roadkills in spring (breeding season) than in autumn (dispersion season)?; (2) Is there any

difference, in terms of number of roadkills, between vertebrate groups?; (3) Does clima-

tology affect the number of casualties by, for example, increasing amphibian roadkills in

the rainiest areas?; (4) Do protected areas register a higher incidence of roadkills?

Materials and methods

Study area

Catalonia has high climatic variability, with annual rainfall ranging from less than 400 to

1,000 mm, and temperatures showing wide differences throughout the region, with a mean

August temperature lower than 16 �C in some localities, while in others it exceeds 26 �C.

Following the study by Martin-Vide (1992), the study area was organized in four main

equally represented climatic regions on the basis of annual rainfall and temperature: Py-

renean, Continental Dry, Humid, and Littoral (Fig. 1a). The Pyrenean region is moun-

tainous with elevations above 1,000 meters. It is characterized by cold winters and mild

summers and high rainfall throughout the year, with the maximum in the summer and the

minimum in the winter. The Continental Dry region is characterized by cold winters and

hot summers and low rainfall, which is concentrated mainly in spring and autumn. The

Humid region has mild winters and hot summers. Although it has lower rainfall than the

Pyrenean region, the Humid region has a high rainfall pattern, which is concentrated

mainly in spring and autumn, with the maximum falling in autumn and the minimum in

winter. Finally, the Littoral region is a little drier and warmer than the Humid region, but

with small thermal fluctuation (Martin-Vide 1992). We classified roads in these climatic

regions on the basis of the predominant climate each road passes through.

Given the geographic location of the study area, fauna from several biogeographic

origins, namely Centro European, Ibero–Maghrebian and circum-Mediterranean con-

verge, thus implying high species richness (Carretero et al. 1999). Excluding fish, the

study area includes 14 amphibians, 33 reptiles, 96 mammals and 395 bird species. The

list of vertebrate species present in the 10 9 10 km UTM squares where roads are located

was obtained from the published atlases of the region (Llorente et al. 1995; Pleguezuelos

et al. 2002; Estrada et al. 2004; Palomo et al. 2007; Herrando et al. 2011). Moreover, in

Biodivers Conserv (2012) 21:2761–2774 2763

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Catalonia there are 165 areas of natural interest with low environmental protection, and

14 Natural Parks and one National Park, these with high protection (Fig. 1b). Each road

was classified into one of three protection categories (high, low, and unprotected areas)

on the basis of the predominant protection status of the area through which each road

crosses.

IV

II

I

III

(a)

(b)

Fig. 1 Maps of the area of study. a Counties of the area of study and the Climatic regions: Pyrenean (I),Continental Dry (II), Humid (III) and Littoral (IV). b Roads surveyed (black), low protection areas (lightgreen) and high protection areas (dark green). (Color figure online)


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Road network and sampling

Catalonia has an extension about 31,895 km2, organized in 41 counties, and a road network

of 12,068 km, with 10.1 % of highways and 89.9 % of secondary roads (Generalitat de

Catalunya 2003a). To ensure uniform sampling in the study area, roadkills were surveyed

in spring and autumn 2002 in the 41 counties, thus covering the four climatic regions and

protected and unprotected areas. In each county we randomly selected a 20-km stretch of

secondary road. These were chosen because they are uniformly distributed throughout the

study area and are mainly two-way roads, with moderate speed traffic and without a central

reservation or lateral fences. Surveys were made by observers in a car traveling at a

maximum speed of 20 km/h as slow speed is required to detect small animals such as

amphibians (Ashley and Robinson 1996; Smith and Dodd 2003; Glista et al. 2008). Even

so, there is a misdetection of carcasses, taking into account that the missing of carcasses in

by foot surveys was estimated in a 7–67 % of the total number of road victims (Hels and

Buchwald 2001). Nevertheless, as the methodology used was the same in all the roads, the

results of all the surveys are comparable. All roads were surveyed by volunteer staff on

warm sunny days (air temperature approximately between 20 and 25 �C) and during the

same days. In the Pyrenean counties, where faunal activity begins later because of low

temperatures, spring surveys were delayed by 15 days. Each road was surveyed three times

in spring (from 15 April to 20 May 2002) and three times in autumn (from 10 October to 15

November 2002). Consequently, we conducted 246 surveys covering a total of 4,920 km.

To avoid replication by counting a carcass twice, roads were surveyed fortnightly, and

animal carcasses were removed from the road once they had been registered. The

extraction of the carcasses did not bias the results by reducing the possible number of

scavengers killed, since the interval between surveys was enough to recover the dynamics

of the road casualties. Roadkills were classified into four taxonomic groups (amphibians,

reptiles, birds and mammals) and identified to species level whenever possible. The geo-

graphic location of carcasses on the road was recorded with an accuracy of 100 m.

Statistical procedures

We performed a General Linear Model (GLM) analysis to check for differences in the

number of potential species killed on each road between the four climatic regions and

levels of protection considered.

We then performed different GLMs to test for differences in the number of roadkills

(dependent variable), using the taxonomy of specimens, season, climatic region and pro-

tection status, as explanatory variables (Table 1). The model that best fitted the data also

included the interactions ‘‘taxonomy 9 season’’, ‘‘taxonomy 9 protection’’ and ‘‘season 9

protection’’. Given that traffic intensity may influence the number of roadkills, we included

IMD (Daily Mean vehicle Intensity, data from Generalitat de Catalunya 2003a) in the

GLM analysis as a covariate, nevertheless, this covariant was not informative and finally

was not included in the chosen model.

The association between number of roadkills of particular species and explanatory

variables (i.e. climatic region and protection status) was checked by Redundancy Analysis

(RDA) with the CANOCO 4.0 software (ter Braak and Smilauer 1998). RDA is a con-

strained linear ordination method in which the species data are defined as a linear com-

bination of the explanatory variables (ter Braak and Smilauer 1998). The species data

corresponded to the number of roadkills registered on each road. Species with less than 5

specimens and specimens without species attribution were excluded from the analysis.


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Values were squareroot-transformed to reduce the over-representation of some amphibian

species that showed high number of roadkills on single roads, and the IMD was used as a

covariate. The explanatory power of the first ordination axis and all axes together were

tested in a Monte Carlo permutation test (9,999 unrestricted permutations).

Results

The GLM analysis showed that the number of species present in the UTM squares of the

roads surveyed did not differ either by climatic region (F3,35 = 0.840, P = 0.481) or

protection status (F2,35 = 0.959, P = 0.393). In other words, the number of potential

species vulnerable to roadkill did not differ between areas.

We registered a total of 2,013 roadkills (Table 2): 853 in spring and 1,160 in autumn.

Roadkills were composed of 267 mammals (13.3 %), 253 birds (12.6 %), 245 reptiles

(12.2 %) and 1,248 amphibians (62.0 %). During the surveys we identified 11 species of

amphibians (78.6 % of all amphibian species present in the area), 17 reptile (51.5 %), 18

mammal (18.8 %) and 39 bird (9.9 %) species. The species with the highest number of

roadkills were amphibians: Salamandra salamandra with 432 roadkills, Bufo bufo with

360, and with 305. The snake Malpolon monspessulanus, with 63 specimens, was the

reptile with the highest number of casualties. Passer domesticus and Rattus norvegicuswere the bird and mammal most killed respectively, both with 52 specimens.

The whole GLM model was highly significant (F20,307 = 9.641; P \ 0.001; Table 3).

The GLM test showed differences in the number of roadkills by season (F1,307 = 8.913,

P = 0.003). The beta coefficient indicates a higher incidence in autumn than in spring

(Table 4). The number of roadkills by taxonomical group also showed significant differ-

ences (F3,307 = 45.270, P \ 0.0001), and Scheffe post hoc comparison detected differ-

ences between amphibians and the rest of the groups (P \ 0.0001). As the beta coefficients

indicated, there were more amphibians than birds and more birds than the other two

Table 1 Explanatory variables used in roadkills GLM analysis

Variable Definition Type Categories/range

n

Taxon Taxonomical group to which each roadkill belongs Nominal Amphibian 1,248

Bird 253

Mammal 267

Reptile 245

Season Season when each roadkill was found Nominal Spring 853

Autumn 1,160

Region Predominant climate of the region where each roadpasses through

Nominal Pyrenean 212

Continental dry 391

Humid 847

Littoral 563

Protectionstatus

Category of protection of thearea where the road passes through

Nominal No protection 1,140

Low protection 276

High protection 597

IMD Daily Mean vehicle Intensity Scale 126–10,466


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taxonomical groups. The GLM did not show differences for climatic regions, and the

interaction season 9 taxon (Table 3). Nevertheless, there was a negative significant beta

for the interaction [amphibian vs. birds 9 spring vs. autumn], which indicated higher

number of amphibian roadkills in autumn and of birds in spring (Table 4). In contrast, the

protection status of the roads sampled showed significant differences as well as its inter-

action with taxonomic group and season. The Scheffe post hoc test for the protection status

indicated differences between the number of roadkills in roads classified as high protected

and the low and non protected. The post hoc tests for the interactions showed differences in

the number of casualties of amphibians in the high protection status areas and in autumn

also in the high protected areas, than the rest of combinations (Table 3). The sign of the

betas indicated that roads with high protection status showed more amphibian and bird

roadkills than low and non protected roads. Finally, in autumn there were more roadkills in

high protected than in low protected areas (Table 4).

RDA showed a relation between roadkills registered and the two explanatory variables.

The test of significance of the RDA for the climatic region for all axes (F = 2.397,

P = 0.0023) and for the first axis (F = 4.708, P = 0.0056) were significant. The species

with the highest explained variance (% Expl), i.e., the amount of variation of each species

explained by climatic region, were B. bufo (24.05 %), B. calamita (21.98 %), S. salam-andra (20.72 %), Sylvia melanocephala (20.34 %) and Podarcis muralis (20.02 %)

(Fig. 2a). S. salamandra and B. bufo were more associated with Humid regions, while B.calamita and S. melanocephala were linked to Littoral areas. In contrast, P. muralis was

Table 2 Road mortality of the four taxonomic groups, both in spring and autumn

Taxonomic group Spring Autumn Total

n % n % N %

Amphibians 468 54.9 780 67.2 1,248 62.0

Birds 158 18.5 95 8.2 253 12.6

Mammals 100 11.7 167 14.4 267 13.3

Reptiles 127 14.9 118 10.2 245 12.2

Total 853 1,160 2,013

Table 3 GLM analyses of the number of roadkills for the different explanatory variables

Effect Adjusted R2 SS d.f. MS F P

Whole model 0.346 26,757.89 20 1,337.90 9.641 <0.001

Intercept 12,456.32 1 12,456.32 89.761 <0.001

Season 12,36.92 1 1,236.92 8.913 0.003

Region 243.76 3 81.25 0.586 0.625

Taxon 18,846.50 3 6,282.17 45.270 <0.001

Protection status 2,582.87 2 1,291.44 9.306 <0.001

Season 9 Taxon 1,003.91 3 334.64 2.414 0.067

Season 9 Protection status 1,455.41 2 727.71 5.244 0.006

Taxon 9 Protection status 11,145.97 6 1,857.66 13.386 <0.001

Error 42,602.93 307 138.77

In bold there are the significant effects


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associated with Pyrenean areas. The RDA for the protection status was also significant for

all axes (F = 2.429, P = 0.0159) and for the first one (F = 3.950, P = 0.0168).

Amphibians and reptiles were associated with high protected areas, whereas mammals and

birds were related to non-protected areas (Fig. 2b).

Discussion

Composition of roadkills

The present study shows taxonomic differences in roadkills, with herpetofauna, especially

amphibians, accounting for 74.2 % of all vertebrate roadkills found on the roads studied,

both in spring and autumn. Our results are consistent with other comparative roadkill

patterns detected in surveys performed by bicycle or walking, or even by car at slow speed

(\40 km/h), which reported higher road casualties of amphibians and reptiles than other

vertebrate groups (Ashley and Robinson 1996; Smith and Dodd 2003; Dodd et al. 2004;

Glista et al. 2008). Nevertheless, Glista and DeVault (2008) also performed surveys at slow

speed (\40 km/h) and detected mammals as the most common vertebrate taxon killed. In

this case the authors stated that the seasonal sampling contributed to a bias towards

detection of larger carcasses such as raccoons or opossums to the detriment of smaller

carcasses such as birds and amphibians. As in those studies, our surveys were performed by

observers in a car travelling at low speed (\20 km/h), to facilitate the detection of small

carcasses, even though there is always a misdetection (Hels and Buchwald 2001). Puky

(2005) reported that the sampling methodology can bias the detection of vertebrate groups

killed on roads because surveys performed by vehicles travelling at high speed ([40 km/h)

Table 4 Parameter estimates and b coefficients of the significant intra-effect comparisons

Intra-effect comparison Parameterestimate

St errparam

t P b St errb

Intercept 7.962 0.840 9.474 \0.001

Spring vs autumn 2.346 0.786 -2.986 0.003 -0.161 0.054

Amph vs birds 15.850 1.361 11.645 \0.001 0.771 0.066

Rept vs birds -4.740 1.361 -3.483 \0.001 -0.231 0.066

Mamm vs birds -5.738 1.361 -4.216 \0.001 -0.279 0.066

Non vs high prot -3.242 1.081 -2.998 0.003 -0.156 0.052

Low vs high prot -2.810 1.124 -2.499 0.013 -0.122 0.049

Spring vs autumn 9 Non vs highprot

2.439 0.932 2.616 0.009 0.139 0.053

Spring vs autumn 9 Amph vsbirds

-2.869 1.127 -2.546 0.011 -0.139 0.055

Amph vs birds 9 Non vs highprot

-12.127 1.615 -7.511 \0.001 -0.487 0.065

Amph vs birds 9 Low vs highprot

-7.398 1.785 -4.144 \0.001 -0.238 0.058

Mamm vs birds 9 Non vs highprot

5.243 1.615 3.248 0.002 0.211 0.065

St err param standard error of the parameter, St err b standard error of the b, Amph amphibians, Reptreptiles, Mamm mammals, Prot protection status


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(b)

(a)

Fig. 2 Biplots of the RDA with a climatic region and b protection status as explanatory variables, and IMDas covariate. P value from the Monte Carlo test of significance of the first axes (9,999 iterations). PirPirenean, Hum Humid, Cont Continental, Lit Littoral. Aal: Atelerix alfgirus, Afr: Anguis fragilis, Bbu: B.bufo, Bca: B. calamita, Cca: Carduelis carduelis, Cgi: Coronela girondica, Eru: Erithacus rubecula, Mca:Miliaria calandra, Mmo: M. monspessulanus, Nma: Natrix maura, Nna: N. natrix, Ocu: Oryctolaguscuniculus, Pal: Psammodromus algirus, Pdo: Passer domesticus, Pli: Podarcis liolepis, Pmu: P. muralis,Rsc: Rinechis scalaris, Sar: Sorex araneus, Sme: Sylvia melanocephala, Ssa: S. salamandra, Tme: Turdusmerula, Vas: Vipera aspis. Prot protection


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show a high incidence of mammals and birds (Slater 2002; Clevenger et al. 2003; Taylor

and Goldingay 2004). This disparity of results indicates that small animals may not be

detected at higher speed, and thus bias the casualties detected to mammals and birds, even

when more amphibians or reptiles are in fact killed by traffic.

Reptile and bird roadkills were more frequent in spring, when their activity is high

because of reproduction. This result is consistent with the observation that roadkills are

usually associated with major wildlife activity during the reproductive season and with

thermoregulatory behavior in ectotherms (Bernardino and Dalrymple 1992; Rudolph et al.

1999). However, this general statement does not fit amphibians and mammals. Amphibian

activity is regulated particularly by the rainfall regime. In the study area, their main

breeding season is in spring, with a second breeding period in autumn (Richter-Boix et al.

2006), mainly in the Littoral and Humid regions, as a result of high rainfall and mild

temperatures during this season. At the time when the present study was performed, the

rainfall registered in autumn was almost two-fold that in spring (Generalitat de Catalunya

2003b). This seasonal pattern was also observed in amphibian roadkills, as we observed

almost twice the number of casualties in autumn than in spring. The association between

rainfall and amphibian roadkills is dramatic in regions with an infrequent and unpredict-

able rainfall regime, such as the Mediterranean area (Carvalho and Mira 2011). Mammals

also showed their highest number of roadkills in autumn. Several rodents, such as

Apodemus sylvaticus (the third most frequently killed mammal), breed from spring to

autumn; therefore populations reach a peak density in September (Kikkawa 1964; Torre

et al. 2002), and also increase their locomotor activity (Flowerdew 2000), which is

reflected in increased number of roadkills.

The main victims on the roads covered by our surveys were three amphibian species

with high terrestrial mobility: S. salamandra, B. bufo and B. calamita. This result supports

previous studies showing that some activity patterns, such as high migratory activity (Bar-

David et al. 2007; Schmidt et al. 2007) and terrestrial dispersion (Moore 1954; Miaud et al.

2000), make species highly vulnerable to traffic. Furthermore, the two toad species show

fidelity to breeding ponds, a behavior that makes them highly susceptible to fragmentation,

especially when there are massive migrations during the breeding season (Sinsch 1989).

The site fidelity of B. bufo is very high, with 93 % of females and 96 % of males that

survived between years returning to the same breeding ponds (Reading et al. 1991). An

example of this fidelity was registered by Cooke (1995), who recorded high number of

roadkills of B. bufo on roads near a breeding point during 21 years. However, the three

species most killed could be more detected due to a higher durability on the asphalt than

other amphibians or vertebrate species, because of their size, tough skin or unpalatability.

Therefore, further studies to determine the durability of the species on the road and

evaluate the real number of victims of the roads are needed.

Explanatory variables and number of roadkills

RDA has demonstrated that several species and groups are linked to particular climatic or

protected areas. The species with the highest amount of variation explained by the climatic

region were S. salamandra, B. bufo and B. calamita, P. muralis and S. melanocephala. This

finding indicates that species roadkills are associated with the climates for which the

species show clear preferences; for example, S. salamandra and B. bufo are more asso-

ciated with Humid areas (Llorente et al. 1995), while B. calamita and S. melanocephala are

most commonly found in Littoral areas (Dıaz et al. 1996; Gasc et al. 1997), and P. muralisin Pyrenean regions (Llorente et al. 1995).


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We did not detect differences in the number of species found killed per road between

the four climatic regions. This result is consistent with the lack of differences in the

number of vertebrate species present in each climatic region (see Results). In contrast, we

demonstrate that the incidence of roadkills increases as the protection level increases. It

could be proposed that this relationship is due to a greater number of species in protected

areas; however, this was not the case, as GLM analyses of species presence did not differ

between protection status areas. The most plausible explanation for this higher number of

roadkills is that wildlife populations in protected areas have higher densities and a greater

number of animals cross or use roads than in unprotected areas (Rodrigues et al. 2004). Our

results therefore agree with previous studies performed in protected areas worldwide

(Bernardino and Dalrymple 1992; Drews 1995; Kline and Swann 1998; Mazerolle 2004;

Ament et al. 2008). Paradoxically, all these studies indicate that protected areas increase

the vulnerability of wildlife to road traffic.

Conclusions

The finding that protected areas registered the highest number of roadkills is relevant for

the future management of wildlife conservation. In fact, protection status may produce a

network of roads and tourism services and consequently an increase in the number of

visitors, which in turn can degrade natural resources (Manning 2001). Roads crossing

protected areas endanger local fauna (Clevenger et al. 2003; Hartmann et al. 2011),

especially when peaks in wildlife seasonal activity coincides with tourism high seasons

(Bernardino and Dalrymple 1992). This phenomenon has been reported in one of the Parks

included in the present study. In that park, the highest number of visitors occurred in

autumn (Diputacio de Barcelona 2011), coinciding with the period of greatest number of

roadkills detected in the present study. On the other hand, the IMD did not result infor-

mative, since a single car is enough to kill a lot of animals on the asphalt. This result

indicated that, in protected areas, probably is more important animals activity patterns than

traffic intensity. Nevertheless, it would be interesting to evaluate the relation between

roadkills and season activity of species along all the year. Accordingly, the roadkills in the

protected areas should be considered by park conservation managers. Given that

amphibians is the group with the highest number of roadkills, especially in the protected

areas, correction measures should be directed to this taxonomic group and areas. Due to

their dependence on water for breeding and fidelity to breeding sites, drift fences (Langton

1989) and changes in breeding sites (Schlupp and Podloucky 1994) have been proved as

effective and can be applied in protected area (Clevenger et al. 2001a; Aresco 2003; Dodd

et al. 2004). Moreover, the enforced speed limit for cars crossing protected areas could also

be an effective measure.

Our findings demonstrate that roadkills of herpetological fauna, especially amphibian

populations in protected areas, should not be underestimated. Assessing number of road-

kills for vertebrate groups and species may shed light on their specific vulnerability to road

networks (Clevenger et al. 2003; Steen et al. 2006). Information from studies of this nature

contributes to the design of specific measures to mitigate the impact of road traffic on

wildlife.

Acknowledgments We thank the volunteers P. X. Alborna, X. Bayer, J. Camprodon, E. Cipriano, J.Galbany, D. Guixe, P. J. Jimenez, M. Martin, J. Nicolau, M. Pascual, L. Perez, L. Plaza, S. Ramos, L. Solerand F. Sort for their help with the surveys, and the two anonymous reviewers for their comments. Thanks


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also go to A. Sorolla for logistic support. This research was funded by the Departament de Medi Ambient,Territori i Sostenibilitat of the Generalitat de Catalunya (FBG301492). Xavier Santos was supported by apost-doctoral grant (SFRH/BPD/73176/2010) from the Fundacao para a Ciencia e a Tecnologia (FCT,Portugal).

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are protected areas truly protected? the impact of road traffic on vertebrate fauna

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