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Biological Conservation 124 (2005) 397–405

BIOLOGICAL

CONSERVATION

Complementary use by vertebrates of crossing structuresalong a fenced Spanish motorway

C. Mata *, I. Hervas, J. Herranz, F. Suarez, J.E. Malo

Departamento Interuniversitario de Ecologıa, Facultad de Ciencias, Universidad Autonoma de Madrid, E-28049 Madrid, Spain

Received 18 October 2004; received in revised form 11 January 2005; accepted 21 January 2005

Abstract

Fenced roads fragment terrestrial vertebrate populations, the individuals of which are forced to cross these infrastructures using

transverse structures inherent to the road�s construction (culverts, over- and underpasses) or other structures specially adapted or

constructed for use by the fauna (enlarged culverts and bridges, ecoducts). The information available on the use of different crossing

structure types by vertebrates, and the role played by the structural variables, of the surroundings and of the human use of these

passages is still scarce. The use of 82 crossing structures of the A-52 motorway (Zamora, North-western Spain) by terrestrial ver-

tebrates was monitored in summer 2002 using marble dust beds and electronic cameras. A total of 1122 species track-days were

recorded, with an average of 1.37 species crossing structure�1 day�1. The results showed that structural aspects were the most deter-

mining factors for the species using these passages (MANCOVA test, p < 0.001), and a direct positive relationship between the size

of the animal and the size of the pass used existing in general terms. This complementary use of the different passage types by ver-

tebrate species suggest that, mitigation measures in new roads should focus to the establishment of several passages of different char-

acteristics instead of investment in a reduced number of large fauna-specific passages.

� 2005 Elsevier Ltd. All rights reserved.

Keywords: Barrier effect; Corridor; Fauna passage; Fragmentation; Road ecology

1. Introduction

Roads and railways are common infrastructures in

developed countries and generate a wide range of envi-ronmental effects. Among them, there is growing atten-

tion to the fragmentation of terrestrial vertebrate

populations. Linear infrastructures section up the land-

scape and divide terrestrial animal populations into

more-or-less isolated sub-populations, compromising

their conservation through the so-called barrier effect

(Bennett, 1991; Mader, 1984; Trombulak and Frisell,

2000; Forman et al., 2003). Roads with high levels oftraffic are usually fenced to avoid the entry of animals

given that vehicle collisions with animals of medium to

0006-3207/$ - see front matter � 2005 Elsevier Ltd. All rights reserved.

doi:10.1016/j.biocon.2005.01.044

* Corresponding author. Tel.: +34 914978011; fax: +34 914978001.

E-mail address: cristina.mata@uam.es (C. Mata).

large size represent a serious hazard (Conover et al.,

1995; Groot and Hazebroek, 1996; Romin and Bisson-

ette, 1996). Road fencing is relatively successful in

avoiding animal–vehicle collisions (Ludwig and Brem-icker, 1983; Putman, 1997), but reinforces the barrier ef-

fect of the infrastructure on the surrounding animal

populations. Medium and large vertebrates along fenced

roads are forced to use the transverse structures (over-

passes, bridges, culverts) in order to cross. For this rea-

son, new roads frequently include passages specifically

designed for use by the fauna or show modifications to

the integral transverse structures to achieve the sameobjective (Keller and Pfister, 1997; Rosell and Velasco,

1999; McGuire and Morrall, 2000).

After almost three decades of developing this type of

mitigation measures, the knowledge about their effec-

tiveness is still rather fragmentary, despite the interest

Benavente

Zamora

Pueblade Sanabria

A-52

A-6

A-6

N-630

N-630

N-631

N-120

N-122

20 Km

Benavente

Zamora

Pueblade Sanabria

A-52

A-6

A-6

N-630

N-630

N-631

N-120

N-122

20 Km20 Km

Fig. 1. Location of the study section of the motorway in the Iberian

Peninsula.

398 C. Mata et al. / Biological Conservation 124 (2005) 397–405

for allocation of funds for the conservation of terrestrial

species during road building (Reed et al., 1975; Ballon,

1985; Forman et al., 2003). In most cases, where wildlife

crossing structures have been installed there has been no

subsequent study of their effectiveness, or these studies

have only been directed to observing use of these specif-ically designed passages by the target species (i.e., Singer

and Doherty, 1985; Foster and Humphrey, 1995). How-

ever, it has been shown that culverts and other struc-

tures not designed specifically for the fauna are also

used (Hunt et al., 1987; Yanes et al., 1995; Rodrıguez

et al., 1996; Clevenger et al., 2001). In consequence,

studies to evaluate the use of wildlife crossing structures

as well as those passages originally designed for otherpurposes have started over the last few years, and the

number is still very limited (Cain et al., 2003; Clevenger

and Waltho, 2005). In addition, a large proportion of

the results obtained come from wooded areas, above

all in North America (see review in Forman et al.,

2003), with a lower number of studies from more open

landscape types and with stronger human impact.

The main research goal at present is the integratedanalysis of the influence of structural factors, of the sur-

roundings and of human activity on the use by wildlife

of crossing structures. On the one hand, the structural

parameters (i.e., width, length, location above or below

the road) of the potential passages for the fauna could

determine their use by the different species (Olbrich,

1984; Clevenger et al., 2001). On the other hand, the

surrounding landscape characteristics (distance to treecover, vegetation) and human disturbance could be

determinant in the use or not by wildlife of certain cross-

ing structures (Rodrıguez et al., 1997; Malo et al., 2004).

The majority of previous studies have shown the impor-

tance of the structural factors, though only a minority of

cases have undertaken a simultaneous analysis of both

groups of factors (Rosell et al., 1997; Ng et al., 2004;

Clevenger and Waltho, 2005). Indeed, the effect of cross-ing structure use by humans on their use by wildlife is

one of the poorest known points (Forman et al.,

2003). In this sense, the relative importance of the de-

sign, the location and the use by humans need to be ta-

ken in account as key factors at the moment of designing

the mitigation measures of a new road. All three factors

may determine the optimum number and type of pas-

sages which the road needs to be compatible with theconservation of the vertebrates present in the traversed

landscape.

The objectives of this study are: (i) to analyse the use

by vertebrates of the existing crossing structures in a

motorway in NW Spain, including the different types

of passages (over and under the road, specifically de-

signed for animal crossing and not expressly designed

for wildlife movement) and (ii) to evaluate the relativeweight of the design factors compared to those of the

surroundings and of human activity, in fauna passage.

From the results of this analysis we aim to generate

some directives applicable to the design of corrective

measures for the barrier effect generated by the con-

struction of fenced infrastructures.

2. Study area and methods

2.1. Study area

The study was undertaken along the stretch of the A-

52 motorway (Zamora Province, NW Spain, Fig. 1) be-

tween the towns of Benavente and Puebla de Sanabria

(kilometre posts 2.75–74.25). The road was opened totraffic in 1998, is dual carriageway and fenced externally

throughout its length. Average traffic levels are approx.

10,000 vehicles/day, with a little over 20% of these being

heavy transport vehicles.

The study road has an E–W orientation that coin-

cides with an increasing altitudinal gradient, decrease

in temperature and increase in rainfall. The road pas-

sages through an undulating landscape and lies between720–960 m a.s.l., with a mild Mediterranean climate, an

average annual temperature of 10–11.5 �C and 400–950

mm of rainfall. The first 20 km of the landscape is dom-

inated by non-irrigated arable crops interspersed with

patches of scrubby woodland dominated by holm oak

(Quercus rotundifolia) and gum Cistus (Cistus ladanifer).

The vegetation of the following 30 km is a mosaic of

sub-oceanic holm oak woods, patches of scrub of gumcistus and leguminous shrubs (Cytisus multiflorus, C.

scoparius) and Agrostis castellana pastures with a small

proportion of cultivated fields. The remaining section

passages between patches of Pyrenean oak (Quercus

pyrenaica) woodland, tall Cytisus spp. and Adenocarpus

complicatus scrub, low scrub (Genista tridentata, Hali-

mium ocymoides, H. lasianthum) and humid pastures.

C. Mata et al. / Biological Conservation 124 (2005) 397–405 399

In general terms, the road passes through areas of

high faunistic diversity and low human population due

to emigration. Consequently, there are areas with high

population densities of wolf (Canis lupus) and large her-

bivores such as red deer (Cervus elaphus), roe deer

(Capreolus capreolus) and wild boar (Sus scrofa ; Blanco,1998). As a result, various fauna passages and circular

drainage tunnels of 1.80 m in diameter were incorpo-

rated during the construction of the motorway. In addi-

tion, some of these were substituted by 2 · 2 m box

culverts.

3. Passage monitoring

Throughout the 71.5 km studied, 82 crossing struc-

tures were selected for monitoring of their use by terres-

trial vertebrates. These passages comprised circular and

wildlife-adapted (box) culverts, open span underpasses,

wildlife underpasses, overpasses and wildlife overpasses

(Table 1). The selection of the crossing structures was

aimed at (i) the inclusion of all the design types specifi-cally included for the fauna, (ii) a relatively balanced

presence of all crossing structure types and (iii) homoge-

neous distribution of all these throughout the length of

the study section.

Field work was carried out between the end of June

and the beginning of September 2002 using analyses of

tracks and signs. Records were obtained using marble

dust, a scentless material which produces imprint tracksof high quality and persistence given its high density

(Yanes et al., 1995). In each selected passage, a band 1

m wide and 3–10 mm deep of the marble dust was in-

stalled at the right angles to the direction of the pass

and across the whole width of the track at the half way-

point. The animal tracks present in each pass were iden-

tified, recorded and subsequently cleared on a daily

basis. Each pass was registered until 10 days worth ofvalid records were obtained, eliminating those in which

the meteorological conditions invalidated the correct

registering of the footprints.

Identification of the tracks was made following Stra-

chan (1995), Sanz (1996), Bang and Dahlstrom (1997),

Table 1

Basic characteristics of the six pass classes studied and their sample sizes

N Dimensions (m)

Width Hei

Circular culverts 33 ; 1.80

Adapted culverts 10 2–3 2

Open span underpasses 14 4–9 4–6

Wildlife underpasses 7 20 5–7

Overpasses 16 7–8 –

Wildlife overpasses 2 16 –

a In two cases 150 m.b One case of 96 m.

and Blanco (1998), with grouping of the records neces-

sary when identification to specific level was not possi-

ble. Consequently, apart from those species identified

specifically, the following groupings were recorded: anu-

rans (all frogs and toads), lacertids (Lacerta spp. and

Podarcis spp.), ophidians (all snakes and legless lacert-ids), small mammals (mice, voles and shrews), water

voles (Arvicola sapidus and A. terrestris), rats (Rattus

rattus and R. norvegicus), lagomorphs (Oryctolagus

cuniculus and Lepus granatensis), small mustelids (Mus-

tela nivalis and M. erminea), cats (Felis catus and F. sil-

vestris) and large canids (Canis familiaris and C. lupus).

To complement this, camera traps were installed in 47

of the structures with the aim of identifying those speciesfor which the tracks were impossible to identify to the

specific level. The photographic system was designed

specifically for the study and comprised a digital camera

(Sanyo VPC-R1, SANYO Electronic Co. Ltd., Osaka,

Japan) activated by a controller via a system of active

sensors comprising an infra-red emitter and two recep-

tors, one at ground level and the other at 20 cm above

it. The data obtained via this method were only usedto estimate the relative proportion of the different spe-

cies which made up each of the groups defined above,

and were not included in the analyses explained below.

4. Data analysis

The basic datum analysed has been the number ofdays in which a species (or group) was detected crossing

each passage studied. This avoids the problems of pseu-

doreplication associated with the counting of multiple

tracks of the same species on the same pass and day.

The patterns of crossing structure use were analysed

using Multidimensional Scaling (STATISTICA 5.1,

Statsoft Inc., Tulsa, Oklahoma), a procedure which al-

lows in a low-dimension space the case ordering (cross-ing structures) by the similitude of the observations

(animal crossing–days) obtained in them. This multivar-

iate method simplifies the analysis of general patterns of

change and avoids the problems of multiple inferences

associated with a species by species analysis. To order

Main function

ght Length

36–80 Drainage

35–50a Drainage, adapted for wildlife

34–66 Rural tracks and livestock paths

30–36b Wildlife, closed to vehicles

58–62 Rural tracks

60 wildlife, closed to vehicles

400 C. Mata et al. / Biological Conservation 124 (2005) 397–405

the structures we used the Euclidean distance as an in-

dex of similarity between them and the standard proce-

dure of ordering provided by the statistical program.

Based on the obtained fit (stress) we opted for the use

of the three-dimensional solution.

Once the ordering had been undertaken the existenceof tendencies of significant variation between the pas-

sages were analysed using a MANCOVA applied to

their coordinates along the axes x, y, z of the MDS. Gi-

ven the procedure of generation of the axes, the coordi-

nates corresponding to the observations are independent

and maintain the same metric. In the MANCOVA the

passage type was introduced as the fixed factor (inde-

pendent variable) along with four covariates: (1) the dis-tance (in m) to the nearest tree or shrub cover from the

entrances of the passage; (2) the human activity mea-

sured as the sum of the number of people, vehicles

and livestock herds counted during the 10 recording

days; (3) the distance (in m) to built-up areas, and (4)

the location of the passage along the environmental gra-

dient crossed by the road (determined by the kilometre

post). This procedure serves to keep the effects indepen-dent and to test if there are different patterns of use of

the structures associated with the type of passage, the

vegetation nearby, human disturbance and/or a change

in the vertebrate fauna associated with the environmen-

tal gradient included in the study. The level of signifi-

cance between the different passage types is given

Table 2

Average number of day-detections per crossing structure for species and specie

each crossing structure)

Circular

culverts n = 33

Adapted

culverts n = 10

Open span

underpasses n =

Species

Erinaceus europaeus 0.061 – 0.286

Eliomys quercinus 0.03 – –

Sciurus vulgaris – 0.1 –

Meles meles 0.152 1.7 0.5

Genetta genetta 0.03 – –

Vulpes vulpes 0.788 1.8 3.429

Cervus elaphus – – 0.214

Groups of species

Anurans 0.242 1.2 0.357

Lacertids 1.485 1 0.071

Ophidians 0.03 0.5 0.071

Small mammals 6.758 4.6 2.5

Rats 0.303 0.2 0.214

Water voles 0.121 0.6 –

Lagomorphs 0.455 0.1 3.429

Small mustelids 0.667 0.3 –

Cats 0.636 0.4 0.643

Large canids 0.818 0.7 3.429

Human activity

People 0.030 0.7 4.857

Livestock 0.030 – 0.571

Vehicles – – 7.929

Note that data for people, vehicles and livestock herds are total numbers (in

directly by the MANCOVA, while the influence of each

of the covariates was evaluated using the t statistic ap-

plied to the beta coefficient of the vector of the geometric

sum of its components x, y, z (Quinn and Keough,

2002).

The differences between the factor levels were ana-lysed a posteriori by comparing them in pairs in succes-

sive MANCOVAs and correcting the probability

obtained using the Bonferroni sequential correction

(Rice, 1989). Finally, the species which explained most

variance at the moment of interpreting the positions

on the three axes (x, y, z) of the MDS were established

using Spearman correlations, selecting those species

which maintained values of p < 0.05 after applicationof the Bonferroni sequential correction.

5. Results

Throughout the study period, a total of 1122 species

track-days were recorded, the equivalent of 1.37 species

crossing per passage and day. In addition, an average of0.02 livestock flocks/day, 0.31 people/day on foot and

0.34 vehicles/day were recorded per crossing structure.

Using the marble dust, a total of 17 species and taxo-

nomic groups were recorded as using the passages as

crossings (Table 2), with small mammals being the most

frequently detected (0.50 crossings/day), followed by

s groups detected throughout the whole monitoring period (10 days for

14

Wildlife

underpasses n = 7

Overpasses

n = 16

Wildlife overpasses

n = 2

Average

0.857 – – 0.147

– – – 0.012

– – – 0.012

1.571 – – 0.488

0.286 – – 0.036

3.143 1.438 – 1.671

– – 2 0.085

0.143 0.125 – 0.341

0.857 0.375 0.5 0.890

– 0.125 – 0.110

0.714 6.438 1 5.049

0.143 – – 0.195

– – – 0.122

4.714 3.25 4.5 1.927

– – – 0.305

0.714 0.438 – 0.561

1.714 2.938 0.5 1.732

0.857 10.250 3.0 3.073

– 0.563 – 0.220

0.429 10.063 1.500 3.390

stead of day-detections) by crossing structure in 10 days.

-1.6

-1.2

-0.8

-0.4

0.0

0.4

0.8

1.2

1.6

2.0

-2.0 -1.6 -1.2 -0.8 -0.4 0.0 0.4 0.8 1.2 1.6 2.0

-1.6

-1.2

-0.8

-0.4

0.0

0.4

0.8

1.2

1.6

2.0

-2.0 -1.6 -1.2 -0.8 -0.4 0.0 0.4 0.8 1.2 1.

-1.6

-1.2

-0.8

-0.4

0.0

0.4

0.8

1.2

1.6

2.0

-2.0 -1.6 -1.2 -0.8 -0.4 0.0 0.4 0.8 1.2 1.6 2.0-1.6

-1.2

-0.8

-0.4

0.0

0.4

0.8

1.2

1.6

2.0

-2.0 -1.6 -1.2 -0.8 -0.4 0.0 0.4 0.8 1.2 1.6 2.0

Z a

xis

Y a

xis

-1.6

-1.2

-0.8

-0.4

0.0

0.4

0.8

1.2

1.6

2.0

-2.0 -1.6 -1.2 -0.8 -0.4 0.0 0.4 0.8 1.2 1.6-1.6

-1.2

-0.8

-0.4

0.0

0.4

0.8

1.2

1.6

2.0

-2.0 -1.6 -1.2 -0.8 -0.4 0.0 0.4 0.8 1.2 1. 2.0

X axis

X axis

Fig. 2. Results of multidimensional scaling (x- vs. y- and x- vs. z-axis,

respectively) undertaken to synthesise the fauna detected crossing the

motorway transverse structures. The distinct types of structure

analysed are differentiated: circular culverts (empty circle), adapted

culverts (solid circle), open span underpasses (empty square), wildlife

underpasses (solid square), overpasses (empty triangle) and wildlife

overpasses (solid triangle).

Table 3

Results of the MANCOVA on the effect of crossing structure type and

the combination of the four covariates (milepost, distance to tree or

shrub cover, intensity of human activity and distance to urban areas)

on the position of the passages on the axes x, y, z of the MDS which

simplifies the patterns of variability of crossing structure use by

vertebrates (Fig. 2)

Factors Wilk�s k df = 1 df = 2 p

Structure type 0.348 15 193 <0.001

Covariates 0.658 12 185 0.003

C. Mata et al. / Biological Conservation 124 (2005) 397–405 401

lagomorphs (0.19 crossings/day), large canids (0.17

crossings/day) and red fox (Vulpes vulpes, 0.17 cross-

ings/day). Lacertids, Eurasian badger (Meles meles)

and cats (Felis spp.), were recorded crossing at lower fre-

quencies (between 0.09 and 0.05 crossings/day), while

the remaining species were detected at far inferior levels(less than 0.03 crossings/day).

Simultaneous photographic recording produced 3468

images relating to the detection of 285 species–days

crossing the motorway. With reference to the groups

of species not identified to specific level using tracks,

12 cases of small mustelids in both types of culverts were

obtained, which in all cases referred to weasel (Mustela

nivalis). Of the 50 lagomorph records, 20 correspondedto rabbit (Oryctolagus cuniculus) and 30 to Iberian hare

(Lepus granatensis), there being no significant difference

between these species in the frequency of use of the dif-

ferent passage types (v2 = 0.450, 4 df, p = 0.930).

Regarding cats, there were 26 records of feral cats (Felis

catus) and only one of European wildcat (Felis silvestris)

in a wildlife underpass. Finally, of the 33 records of

large canids, one corresponded to wolf (Canis lupus)crossing by an overpass and 32 to dogs (Canis familiaris)

which were spread across all passage types.

The variation patterns of the species which used the

passages, revealed using the multidimensional scaling,

can be seen in Fig. 2. In this representation a degree

of segregation in the spatial positioning of the different

passage types can be seen, which is highlighted by the

MANCOVA undertaken on these positions (Table 3).This analysis shows that the factor ‘‘passage type’’ is

highly significant, once the effect of the covariates is

eliminated (MANCOVA test, p < 0.001). Additionally,

the a posteriori test of differences between passage types

(Table 4) showed that (i) the fauna which crosses using

circular culverts is significantly different to that which

crosses via any of the passage types, with the exception

of the adapted culverts, (ii) the fauna which uses themultipurpose overpasses is significantly different to that

which crosses via culverts and underpasses, whether of

the normal type or specifically designed for fauna, and

(iii) the open span underpasses also show use by a signif-

icantly distinct fauna to that which uses the adapted

culverts.

This differential positioning of the crossing structure

types in the multidimensional scaling can be interpretedvia the correlations between species and axes of the anal-

ysis. In this sense, the negative values along the x axis

are significantly associated (Spearman rank correlation,

p < 0.05 after Bonferroni probability correction) with

the presence of lagomorphs, red fox and large canids.

The wildlife underpasses, open span underpasses and

wildlife overpasses appear in this part of the axis (Table

5, see also Table 2). In contrast, the positive values ofthe x axis are associated with lacertids, small mammals

and small mustelids, and in this part of the axis appear

principally circular culverts. The positive values of the y

axis are associated with small mammals and lag-

omorphs, the overpasses appearing in this zone, while

the adapted culverts appeared in the negative part of this

axis. Finally, the positive values of the z axis refer to

small mammals, Vulpes vulpes and large canids, the

wildlife overpasses only being of outstanding note in

the negative part of the z axis.The individualised analysis of the covariates (Table 6)

showed that the fauna detected crossing via the passages

varied significantly (t test, p < 0.01) throughout

the length of the geographic gradient crossed by the

Table 4

Results of the a posteriori comparison of the differences between pass types in the fauna crossing them, simplified by their position on the x, y, z axes

of the multidimensional scaling

Wildlife overpasses Overpasses Wildlife underpasses Open span underpasses Adapted culverts

Circular culverts 0.615 0.578 0.413 0.411 0.817

0.002 <0.001 <0.001 <0.001 0.051

Adapted culverts 0.477 0.429 0.584 0.469

0.138 <0.001 0.082 0.002

Open span underpasses 0.742 0.586 0.791

0.330 0.003 0.277

Wildlife underpasses 0.262 0.365

0.117 <0.001

Overpasses 0.439

0.011

The Wilk�s k value is given (upper line) and its probability value (lower line) corresponding to the MANCOVAs pairs comparison. The significant

results (p < 0.05) after Bonferroni sequential probability correction are shown in bold.

Table 5

Average position along the x-, y- and z-axes of the multidimensional

scaling of crossing structure types

x y z

Circular culverts 0.488 �0.053 �0.034

Adapted culverts 0.202 �0.421 �0.118

Open span underpasses �0.707 �0.022 0.129

Wildlife underpasses �0.963 0.017 �0.271

Overpasses 0.005 0.366 0.240

Wildlife overpasses �0.635 0.149 �0.728

Table 6

Results of the t test of the significance levels of the individual

covariates included in the MANCOVA carried out on the position of

the crossing structures in the x-, y-, z-axes of the MDS which

synthesises the patterns of variability of their use by vertebrates

Covariates b value t df p

Location (milepost) 0.0125 2.573 72 0.006

Distance to shrub cover 0.0002 0.421 72 0.337

Human activity index 0.0109 0.731 72 0.234

Distance to village 0.0002 1.333 72 0.093

402 C. Mata et al. / Biological Conservation 124 (2005) 397–405

motorway. The presence of small mustelids, lacertids

and Meles meles increased from east to west, but thatfor cats, lagomorphs and Erinaceus europaeus decreased.

In contrast, human frequency of use, measured as the in-

dex of human usage, and the distance from nearest tree

cover did not significantly alter the faunal use of each

passage type. In addition, there is a marginally signifi-

cant effect (0.05 < p < 0.1) of the proximity of the pas-

sage to urban areas.

6. Discussion

The results show the differential use by different spe-

cies of the distinct types of transverse structures crossing

the motorway, indicating that the different crossing

structures are complementary in the alleviation of the

barrier effect. In addition, it is seen that the type of pas-

sage has greater relevance than the surrounding environ-

mental variables determining which species use it. The

interest in these results is reinforced by (i) the fact that

virtually all of the mammal species in the area were de-

tected as using the passages to cross the motorway and

(ii) the number of monitored crossing structures

(N = 82) was far greater than that analysed in previousstudies (see review in Forman et al., 2003; Ng et al.,

2004). In addition (iii), until now there are very few stud-

ies on fauna passages in Mediterranean areas with a

fragmented landscape and dispersed human population

(Rosell et al., 1997).

It should be highlighted that across the range of pas-

sages studied, almost all the mammal species present in

the area have been recorded. In the results given here(Table 2) only roe deer, wild boar and otter were not

shown to cross the motorway (Palomo and Gisbert,

2002). The infrequency with which ungulates use these

crossing structures has been described in some studies

(Rodrıguez et al., 1996; Keller and Pfister, 1997; Rosell

et al., 1997), even though there are records of their use,

including via tunnels relatively narrow for some of them

(Reed et al., 1975; Brudin, 2003). In our case, the use ofthe crossing structures by roe deer and wild boar has

been recorded, although infrequently, in other sections

of the motorway and/or dates (C. Mata, unpublished

data) and the results support the conclusions presented

below. Roe deer have been proven to use wildlife

passages, both under- and over-, and open span under-

passes. Wild boars have been detected in wildlife over-

and underpasses and also in non-wildlife engineeredoverpasses. The detection of otters is more complex, as

much given the low density of the species as for the dif-

ficulty of monitoring the water body of rivers and

creeks. In the study area there have been no records of

this species using the passages, though in other geo-

graphic areas the use of wildlife underpasses has been

proven (Rosell and Velasco, 1999; C. Mata, unpublished

data).

C. Mata et al. / Biological Conservation 124 (2005) 397–405 403

The complementary nature of the different passage

types for crossing by vertebrates is the most notable re-

sult from our analysis. Thus, the differences in the verte-

brate fauna which cross via distinct passage types are

highly significant and independent from the possible

geographic effects and of the surroundings which indi-vidually characterise each passage. In general a direct

relationship is found between animal size and the dimen-

sions of the crossing structures used (Forman and Her-

sperger, 1996; Veenbass and Brandjes, 1999; Ng et al.,

2004). The circular and adapted culverts were selectively

used by small mustelids, amphibians, reptiles and small

mammals, while larger over- and underpasses were used

by lagomorphs, red fox and large canids. Equally, thered deer (Cervus elaphus) and wolves (Canis lupus) were

only detected in very wide passages, a tendency also

shown by wild boar and roe deer. That said, other

behavioural factors of each species play a determining

factor, as shown by the selection of wide underpasses

by Eurasian hedgehog (Erinaceus europaeus) (0.5–1.2

kg), in contrast to the use of all types of underpass by

Eurasian badger (4.8–9.3 kg). Moreover, this specieshas not been detected crossing through wider

overpasses.

This result highlights the need to focus the analysis of

the mitigation of the barrier effect of roads on the fauna

by taking into account the whole set of existing crossing

structures and not only those of specifically designed

character. Several studies have focussed on the effective-

ness of the passages specifically designed for animalcrossing (Singer and Doherty, 1985; Bekker and Can-

ters, 1997; review in Forman et al., 2003). However,

the studies which have taken into account other passage

types have shown that these can also help in the crossing

of roads and railways by vertebrates (Camby and Maiz-

eret, 1987; Yanes et al., 1995; Ng et al., 2004). In our

case, the 17 species (or faunal groups) detected used to

a greater or lesser degree the non-wildlife engineeredpassages, between 50% and 100% of the total number

of records coming from these. This is the case for small

mustelids, which were only recorded in circular culverts,

or that of the only photograph of a wolf which was ta-

ken on an overpass. At this point the important role

which culverts play for vertebrates of small and medium

size should be stressed, given that these are the common-

est crossing structures and also those with the lowest hu-man presence along motorways (Huijser et al., 1999;

Clevenger et al., 2001). Despite this, it should not be for-

gotten that the specifically designed passages are in gen-

eral the most effective for many species of maximum

conservation interest (Foster and Humphrey, 1995; Cle-

venger and Waltho, 2005). Additionally, the utility for

the fauna of passages with a mixed used may be heavily

affected by the intensity of human usage, which is highlyvariable between areas and can change dramatically

over time.

Secondly, we have shown that the characteristics of

the surroundings of the crossing structures play a lesser

role in the use of these passages by wildlife. The gradient

in landscape features along the road section studied pro-

duces a variation in the species detected, a logical fact

taking into account (i) the presence of variation in thefaunal community due to the change in environmental

conditions and (ii) the already mentioned use of the

crossing structures by a wide range of species. However,

our analyses indicate the absence of relationships be-

tween the fauna which uses the crossing structures with

the tree and shrub cover in their proximity and with the

degree of human use of the passages.

The presence of tree and shrub cover is considereddeterminant for the use of passages by fauna, but in

our study only played a minor role. Numerous studies

show the importance of cover in the surroundings of

the passage entrances for their use by certain animal spe-

cies (e.g., Bennett, 1991; Desire and Mallet, 1991; Rodrı-

guez et al., 1996; Clevenger and Waltho, 2005).

However, the distance from tree or shrub cover of the

passage was not a determining factor for the vertebrateswhich used it along the A-52 motorway. This could be

explained by the fact that most of the crossing structures

had tree or shrub cover in their proximity. The average

distance from the passages to cover was 70 m, and in

83% of the cases it was less than 50 m. These distances

are frequent in landscapes not heavily altered by man,

and so the response by many species may be poorly

marked (see however Clevenger and Waltho, 2005).Equally, the human presence in the passages and the

humanisation of the surroundings have a minimal effect

in our case. The effect of the frequency of human use on

the faunal use of the passages is very poorly known

(Forman et al., 2003), but is generally considered to be

negative (Rosell and Velasco, 1999; Iuell, 2003). The

average index of human use (daily use frequency of vehi-

cles, pedestrians and livestock groups combined) of thestudied passages was only 0.668, which may explain

the absence of changes in the fauna related to human

usage. In fact, in 73% of the passages this value was less

than one vehicle, person or livestock herd per day and

even the over- and underpasses with mixed use regis-

tered close to 50% of days with no passage of vehicles

or humans. The proximity to urban areas showed a mar-

ginally significant effect, in agreement with the locationof the passages at an average of 1,299 m from urban

areas, with 87% of the distances above 500 m. As a re-

sult, it can be deduced from the results obtained that

the effect of a low human presence is reduced, falling

into second place compared to other variables studied

(Clevenger and Waltho, 2000; Gloyne and Clevenger,

2001).

The results clearly show that the structural variablesof the passages are more important, for their use as cross-

ing structures by vertebrates, than human disturbance or

404 C. Mata et al. / Biological Conservation 124 (2005) 397–405

vegetation cover close to the entrances. Given that the

road studied had only been functioning for four years,

it can be supposed that the fauna is still at the early

phases of adapting to the presence of this infrastructure

(Clevenger and Waltho, 2003). This adaptation of the

surrounding vertebrate populations to the new infra-structure and its crossing structures lasts for at least 3

or 4 years, during which the use of the passages increases.

Clevenger and Waltho (2000) hypothesised that the

structural variables of the passages and their location

in relation to the natural faunal corridors existing prior

to the road�s construction will only be determinant in

the use of these during the first few years of use. This

would explain both our results and those of others anal-ysing the case of recently constructed passages (Olbrich,

1984; Ballon, 1985; Rosell et al., 1997). That said, the

determining role of the structural variables of the pas-

sages in their selection by certain species appears to

remain true even years after the construction of the

road, highlighting its relation with evolved behaviours

and life history traits of mammals (see data re-analysis

in Clevenger and Waltho, 2005).From the point of view of vertebrate conservation

and the design of mitigation measures, four main con-

clusions can be drawn. Firstly (i), the mitigation of the

barrier effect generated by infrastructures is achieved

by the installation of different passage types, comple-

menting those non-wildlife engineered passages inherent

to the infrastructure (culverts, over- and underpasses)

with adequate specifically designed wildlife crossingstructures (oversized underpasses, ecoducts). At this

point it is important to note that those studies which

have shown the effectiveness of passages with a mixed

fauna-human use were undertaken in areas with very

low human usage (Rodrıguez et al., 1996; Clevenger

and Waltho, 2005, this study). Such situation could

clearly be distinct given conditions of heavier human

use. In addition (ii), the strategy of how many and whattype of passages to install should be focused on the tar-

get species in the area, as mitigation actions for popula-

tions of small- and mid-sized mammals (e.g., mustelids)

will be radically different to those for larger species and

bias towards the latter would be both ineffective and

expensive (Andelman and Fagan, 2000).

A further point to highlight (iii) is that the relation of

the size of the passage with that of the vertebrates whichwill use it gives an indication of the appropriate distance

between the crossing structures (Bowman et al., 2002),

even if the existence of at least one passage in each terri-

tory of each species is an impossible objective (Clevenger

et al., 2001). Passages of large dimensions and greater

cost should cover the connectivity needs of the popula-

tions of species with larger physical and territorial sizes,

with ideally, enlarged bridges, viaducts or green bridgesbeing present every 3–5 km. The connectivity of the smal-

ler species can be undertaken using culverts (enlarged or

not) and passages of smaller size (i.e., oversized culverts/

small bridges in creeks), which appear with relative fre-

quency (1–2 per km) because those are infrastructure pas-

sages. Finally (iv), the possibility to predict which species

will use certain crossing structures allows for the optimal

positioning of the planned passages along the corridorswhich the species habitually use in their movements

(Land and Lotz, 1996; Malo et al., 2004), simplifying

the process of adaptation necessary by the population

to the presence of the new infrastructure.

Acknowledgements

This study has been funded by a research agreement

between the UAM, the Ministerio de Medio Ambiente

and the Centro de Estudios y Experimentacion (CE-

DEX), and by a FPI grant from the Comunidad de Ma-

drid to Cristina Mata. Help provided by Juan M. Varela

and Javier Cachon, as well as by Antonio and Teresa

from the Hostal Las Ventas was decisive during the

development of the project.

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