Guest contribution Basic and Applied Herpetology 26 (2012): 5-31 Herpetofauna and roads: a review

Víctor J. Colino-Rabanal*, Miguel Lizana Area of Zoology, Department of Animal Biology, Ecology, Soil Science, Parasitology, and Agrochemistry, University of Salamanca, Salamanca, Spain

* Correspondence: Department of Animal Biology, Ecology, Soil Science, Parasitology, and Agrochemistry, Campus Miguel de Unamuno 37071 Salamanca, Spain. E-mail: [email protected] Received: 14 October 2012; received in revised form: 4 December 2012; accepted: 18 December 2012.

Roads and traffic are tightly related to some of the mains threats for biodiversity. Road network affects wil- dlife populations due to, among other effects, partial occupation and transformation of landscape, alteration of surrounding habitat, dispersal of physicochemical pollutants, fragmentation and loss of connectivity, or direct road-kills. Because of their ecological characteristics, amphibians and reptiles are very exposed to road effects. In this article we review the relationship between these faunal groups and the road network. Amphibians exhibit high road-kill rates that can condition viability of some populations, and are vulnerable to pollution of road margins. Reptiles also suffer casualties because of road-kills when they move to paved roads for thermoregulation. Roads, especially those with high traffic load, act as barriers that difficult move- ments and contribute to population isolation in both groups. However, road impacts do not have equal inten- sity over space and time, and consequently some spatio-temporal patterns can be defined. Not all species show the same degree of exposure to road impacts, which depend on specific ecological requirements in each case. Mobile species are generally more vulnerable than sedentary ones. There are also intra-specific differen- ces as a function of gender and age. All these considerations must be taken into account when designing and implementing the corresponding mitigation measures necessary to reduce the negative effects of roads on her- petofauna populations.

Key words: fragmentation; mitigation measures; road ecology; road-effect zone; road-kills; road pollution.

Herpetofauna y carreteras: revisión. Las carreteras y el tráfico rodado están estrechamente relacionados con varias de las principales amenazas para la biodiversidad. La red viaria impacta en las poblaciones de fauna silvestre, entre otros, mediante la ocupación y transformación de parte del territorio, la alteración del hábitat circundante, la dis- persión de contaminantes físico-químicos, la fragmentación y pérdida de conectividad, o la mortalidad directa por atropello. Debido a sus características ecológicas, tanto los anfibios como los reptiles presentan una gran exposición a los efectos de las carreteras. En este artículo hacemos una revisión de la relación entre estos grupos faunísticos y la red viaria. Los anfibios experimentan elevadas tasas de atropello que pueden condicionar la viabilidad de algunas poblaciones y son vulnerables a la contaminación ligada a los márgenes de las carreteras. Los reptiles también sufren bajas por atropello al acudir a la calzada a termorregular. Para ambos grupos, las carreteras, sobre todo las de alta capacidad, constituyen barreras que dificultan sus movimientos y aíslan sus poblaciones. Sin embargo, los impac- tos no revisten la misma intensidad ni en el espacio ni en el tiempo, siendo posible definir una serie de patrones espacio-temporales. No todas las especies presentan el mismo grado de exposición a los impactos de las carreteras sino que éste depende de los requerimientos ecológicos específicos de cada una de ellas. En general, las especies más móviles son las más vulnerables. También hay diferencias intraespecíficas en función del sexo y la edad. Todas estas consideraciones deben ser tenidas en cuenta a la hora de diseñar e implementar las medidas de mitigación corres- pondientes para tratar de reducir los efectos negativos de las carreteras sobre las poblaciones de herpetofauna.

Key words: atropellos; contaminación; ecología de carreteras; fragmentación; medidas de mitigación; zona efectiva de la carretera. 6 COLINO-RABANAL & LIZANA

The increment of both transport networks indirect effects of roads are among the main cau- and social concern about environmental issues ses contributing to the global amphibian decline has led to an increase in the interest for stud- (BLAUSTEIN & WAKE, 1990; HOULAHAN et al., ying the relationships between wildlife and 2000; COLLINS & STORFER, 2003; NYSTRÖM et roads. This has attracted the attention of many al., 2007). In this review, we summarize the pro- researchers, resulting in the emergence of a new gress made in the study of the effects of roads on discipline known as road ecology, whose main the herpetofauna at multiple scales. goal is the study of the interactions between Furthermore, we also analyse the mitigation organisms and the environment linked to road measures proposed to reduce these road impacts. networks and traffic (FORMAN et al., 2003). Roads impact wildlife by means of causing HERPETOFAUNA IN habitat loss, population fragmentation, direct ROAD MORTALITY STUDIES mortality, changes in animal behaviour, physi- cal and chemical alterations of the environ- The first studies in road ecology at the ment, and dispersal of exotic species (MALO et beginning of the 20th century alerted about al., 2004; JAARSMA et al., 2006; FAHRIG & the direct mortality of wildlife caused by RYTWINSKY, 2009). Furthermore, the construc- vehicles on roads. The first specific studies tion of new roads facilitates the use and modi- about herpetofauna focused mostly on snake fication of adjacent habitats by humans mortality (BUGBEE, 1945; FITCH, 1949; (FORMAN & ALEXANDER, 1998; TROMBULAK CAMPBELL, 1956), but also on amphibians & FRISSELL, 2000), which indirectly contribu- (CARPENTER & DELZELL, 1951). HODSON tes to additional impacts on wildlife. (1960) made regular counts in a 3.2 km road Amphibians and reptiles show certain ecolo- stretch near Northamptonshire (England) gical characteristics that make them highly vul- and found 683 vertebrates of 42 species killed nerable to roads impacts. For example, they on the road. The species with the highest show a low vagility in comparison to other ver- mortality rate was the European common tebrates, being especially susceptible to habitat frog (Rana temporaria) with 191 casualties. fragmentation by linear infrastructures. Most of the studies have been carried out Moreover, in reptiles, roads constitute an impor- in Europe (e.g. Belgium: BALLASINA, 1989; tant heat source for thermoregulation. In the Germany: PODLOUCKY, 1989; the case of amphibians, many species show complex Netherlands: ZUIDERWIJK, 1989; Switzerland: life cycles, usually involving periodical migra- RYSER & GROSSENBACHER, 1989; Portugal: tions among the various complementing habi- BRITO & ÁLVARES, 2004; France: LESBARRÈRES tats in order to complete their annual cycle. et al., 2006, Poland: BRZEZIŃSKI et al., 2012), Mortality rates during migrations associated North America (PALIS, 1994; ASHLEY & with direct road-kills are in some cases high ROBINSON, 1996; RAY et al., 2006) and enough to cause effects at the population level. Australia (SEABROOK & DETTMAN, 1996; Moreover, their permeable skin, with osmoregu- HOSKIN & GOOSEM, 2010), but in recent latory and respiratory functions, makes them times, new studies have been conducted in sensitive to road pollution. These direct and South America (CAIRO & ZALBA, 2007; HERPETOFAUNA AND ROADS 7

HARTMANN et al., 2011; COELHO et al., 2012; both with the type of landscape present in the QUINTERO-ÁNGEL et al., 2012) and Asia study area and the methodology followed in the (SESHADRI et al., 2009; ZHANG et al., 2010; road surveys. Thus, in some cases the number GU et al., 2011; TOK et al., 2011). of amphibian and reptile casualties is low due to If the herpetofauna is especially vulnerable the low suitability of the prospected areas for to road effects, road surveys will be expected to these groups, or because the census technique obtain a high rate of casualties in comparison to underestimates the real number of casualties of other vertebrate groups. Table 1 shows the these small-sized animals (MONTORI et al., results of several studies that have quantified 2003). Nevertheless, GRYZ & KRAUZE (2008) road mortality for all vertebrate groups in diffe- found in a two-year monitoring study of a local rent countries, and herpetofauna, especially road across Poland’s Biebrza River Valley that amphibians, appears in most cases as the group 90.7% of all the reported casualties were with the highest road-kill rates. The percentage amphibians, especially anurans like the com- distribution among the different groups varies mon toad (Bufo bufo), the moor frog (Rana

Table 1: Percentage of amphibian and reptile casualties in road surveys aimed to study road mortality for all vertebrate groups. Specific surveys for a certain group were not included in the table.

Study Amphibians Reptiles Survey methodology Location and landscape Traffic volume (%) (%) description (vehicles/day)

GONZÁLEZ-PRIETO et al. 89.2 5.0 Walking. Weekly surveys. Road stretch parallel to Miño River, Ourense n/a (1993) (Spain). Oak forest with some eucalyptus and pine spots, cultivated areas, scru- blands and sub-urban habitat.

ASHLEY & ROBINSON 93.8 2.7 Walking and bicycling. Three times Wetlands in the Long Point Causeway, ~ 3000 (1996) per week during spring-summer. Lake Erie (Canada).

CLEVENGER (1999) 23.3 - Vehicle and walking. Methodologies Bow River Valley, along the Trans-Canada > 14000 adapted to different specimen sizes. highway corridor in Banff National Park.

LODÉ (2000) 29.2 1.1 Vehicle. Department of Vendée (France). 19320

CLEVENGER et al. (2003) 7.1 Vehicle. From April to November. Central Rocky Mountains (Canada). ~ 14000

TAYLOR & GOLDINGAY 0.4 5.9 Vehicle. New South Wales (Australia). Coastal 5000-20000 (2004) lowlands and volcanic plateau. Open pastures, eucalypt forest, plantations, scattered areas of rainforest.

DÁVILA BLANES et al. 9.0 48.0 Vehicle. Daily surveys. Road of access to Carrascal de la Font Roja n/a (2007) Natural Park (SE Spain).

GLISTA et al. (2008) 93.3 1.3 Vehicle. Twice per week. Indiana (USA). Wetlands and ditches su- 1900-6300 rrounded by agricultural lands and hardwood.

GRYZ & KRAUZE (2008) 90.7 2.0 Walking. 3-7 days per month. Biebrza River Valley (Poland). River, oxbow ~ 850 lakes, meadows and flooded pastures.

HOBDAY & MINSTRELL - 0.8 Vehicle. Five regions, one survey Tasmania (Australia). Native and regenerated n/a (2008) per season. forest, woodland, grasslands and farming regions.

GEROW et al. (2010) 41.5 41.7 Vehicle and walking. Once per week. Saguaro National Park in south-eastern 2200-6000 Arizona (USA).

CARVALHO & MIRA 24.1-66.1 4.4-6.5 Vehicle. Every two weeks. Mediterranean agro-silvo-pastoral system 3000-7000 (2011) (Portugal).

GARRIGA et al. 62.0 12.2 Vehicle. Three times in spring Road stretches across Catalonia (Spain). 126-10466 (2012) and three times in autumn. 8 COLINO-RABANAL & LIZANA arvalis) and other Rana spp. that were killed mortality of the flat-tailed horned lizard during their migration to the breeding ponds. (Phrynosoma mcallii) caused by off-road vehi- GLISTA et al. (2008) reported a percentage of cles, although they caused other disturbances amphibians even higher (95%) for four road and indirect impacts that reduced habitat surveys conducted in Indiana, USA. quality for the species. However, some saurian Unfortunately, despite these evidences, species can reach high road-kill rates on a there are not too many studies addressing local scale. In a road near Barcelona (Spain), long-term trends in herpetofauna road-kills. the common wall gecko (Tarentola mauritanica) The direction of these trends is difficult to accounted for 20.2% of all herpetofauna foresee and may vary among areas. In some road-kills, being the second most killed spe- parts, road-kills have increased in recent deca- cies (MONTORI et al., 2003). Nevertheless, the des in line with the road network expansion comparison of road mortality rates among all and the increasing number of vehicles and these studies is very complex and the results displacements (CARVALHO & MIRA, 2011). are difficult to interpret due to differences in On the other hand, road-kills in other areas study areas, population abundance, species have decreased as a consequence of parallel richness, types of road, traffic densities, and population declines associated with the own species surveyed (JAKOB et al., 2003; road impacts (BROCKIE et al., 2009). PINOWSKI, 2005; GLISTA et al., 2008; Considerable variations among years are com- SILLERO, 2008; ELZANOWSKI et al., 2009). mon due to population fluctuations related to Just as with other issues in conservation, environmental conditions or stochastic phe- social perception of wildlife road-kills varies nomena (COOKE, 1995). Thus, long-term in relation to species size. In general little studies are needed to detect accurate trends. public awareness is given to small size faunal As mentioned above, amphibian road-kills groups such as amphibians and reptiles. can reach very high rates. GOLDINGAY & However, they are suffering numerous casual- TAYLOR (2006) estimated a mortality of more ties on the roads that can compromise popu- than 40 000 frogs per year in a 4-km stretch lation viability at a local scale (LANGTON, road in north-eastern New South Wales, 1989; FAHRIG et al., 1995). This situation is Australia. Among reptiles, snakes are also even more puzzling considering that the commonly killed on roads due to their use as implementation of effective solutions would thermoregulation sites (ROSEN & LOWE, be economically viable, at least for the main 1994). Freshwater turtles are another of the hotspots of herpetofauna road-kills. most vulnerable reptile groups to road morta- lity (GOODMAN et al., 1994; HAXTON, 2000). METHODOLOGIES TO STUDY Data about lizard road-kills are scarce, but ROAD MORTALITY this group does not usually seem to suffer an elevated rate of road mortality; for example, Road mortality is generally recorded by in a study about the impact of off-highway direct counting of both dead and alive speci- recreation in southern California desert lands, mens on roads (VAN GELDER, 1973). However, GRANT & DOHERTY (2009) found no direct when detecting all casualties by counting is HERPETOFAUNA AND ROADS 9 not viable because, for example, a high exten- we get to the real number, the better. These stu- sion of territory is aimed to be covered, a com- dies require walking surveys because during bination of counting and road fencing can be vehicle surveys many corpses remain undetec- used (GIBBS & SHRIVER, 2005). In these cases ted, and detection probabilities vary with the there is always a discrepancy between the species. Some herpetofaunal studies consider that actual and the quantified numbers. Apart the maximum vehicle speed allowing for detec- from species’ anatomical and ecological cha- tion of all road-killed specimens is 20 km/h racteristics, detection probability varies with (SANTOS et al., 2007). However, if the aim is to the number of surveys, methodology used, locate hotspots where mitigation measures and experience and skills of the staff involved have to be implemented, both walking and in the census. Other important factors to take vehicle surveys are valid. While walking surveys into account are the presence of scavengers increase detection probabilities, vehicle surveys that can remove the corpses, the topography allow covering greater distances in less time, and type of vegetation on the edges of the which is important considering the short time road, the weather and the time of the day of residence of the corpses on the road (ANTWORTH et al., 2005). Thus, it is estimated (LANGEN et al., 2007). that the actual number of road-kills can be up to 12-16 times higher than the estimated by a ROAD-KILL SPATIO-TEMPORAL daily census (SLATER, 2002). DISTRIBUTION Amphibian carcasses remain just a few hours on the road (SANTOS et al., 2011). Given Herpetofauna road-kills are not randomly that most road-kills occur at night, many car- distributed in either space or time, but are casses may have disappeared in the morning, concentrated in certain road segments during especially in roads with elevated traffic volumes. certain periods of time throughout the year. Furthermore, because of their small size and As amphibians and reptiles perform relatively their fragility they are difficult to detect. Some localized displacements, it is possible to iden- species like the common fire salamander tify the variables that explain the spatial dis- (Salamandra salamandra) may remain for lon- tribution of the hotspots, as well as the places ger on the road due to their tough skin and where priority to the installation of mitiga- unpalatability (SANTOS et al., 2011). The sea- tion measures should be given. The availabi- son is also important to get accurate estima- lity of suitable habitats (closeness to ponds tions; for example, to adequately study the road and rivers, natural vegetation, absence of mortality problem on amphibian populations, anthropogenic disturbance) is a factor com- sampling should be conducted preferably monly identified in road-kill spatial models during migration days. (SILLERO, 2008). LANGEN et al. (2009) found The method of sampling depends on the that, for amphibian and reptile species in the goals of the study. Quantifying mortality and north of New York State, road-mortality assessing potential population consequences hotspots were located within a distance of require a method that allows the detection of as 100 m from a wetland, especially in elevated many individuals as possible so that the closer road sections that presented wetlands on both 10 COLINO-RABANAL & LIZANA sides. SANTOS et al. (2007), working in the high number of casualties even with very low road network of Catalonia (NE Spain), iden- traffic volumes. Thus, VAN GELDER (1973) tified the presence of streams crossing the estimated that a traffic frequency of 10 vehi- road, little steep roadsides, and semi-natural cles per hour caused the loss of 30% B. bufo vegetation as the main explanatory factors of females that tried to cross the road to and B. bufo road-kill locations. ORŁOWSKI et al. from a breeding pond in the Netherlands. (2008) found that the proportion of habitat Furthermore, roads with low traffic volume occupied by forests and the presence of ponds can be more attractive for basking and fee- were the main determinants of the distribu- ding, as demonstrated by LEBBORONI & tion of amphibian road-kills in south-western CORTI (2006) in lizards from central Italy, Poland. Not only the presence but also the thus involving a higher risk of road-kill than size of water bodies in the road vicinity was roads with high traffic density. Nevertheless, also relevant (ORŁOWSKI, 2007). In other the relationship between road-kills and traffic cases, wet grasslands instead of forest are the volumes varies with the species considered. landscape types most associated with amphi- MAZEROLLE (2004a) found that increased bian road-kills (GU et al., 2011). For freshwa- traffic intensities elevated the number of ter turtles in New York State, hotspots were casualties in the American toad (Anaxyrus located at causeways that were larger than americanus) but decreased it in the spring pee- 200 m length, in close proximity to water, per (Pseudacris crucifer). For frogs of the genus and with high forest coverage (LANGEN et al., Lithobates the maximum number of road-kills 2012). It is important to take into account was obtained at medium traffic volumes. For that the spatial distribution of road-kills is a given species, it is possible to calculate the correlated with species local abundance probability of an individual being road-killed (ORŁOWSKI, 2007), which in turn depends by considering the speed, the angle of inter- on habitat features and varies throughout the section, and the traffic intensity. However, as year and among years. explained below, some animals show specific Apart from landscape variables, road para- behaviours in relation to traffic that reduce meters are also important to locate herpeto- accuracy of this kind of estimates. fauna road-kills. For example, the probability At regional scale, habitat variables are bet- of crossing highways is practically null (HELS ter indicators to define areas with high road & BUCHWALD, 2001, but see CARRETERO & mortality rates than traffic volume, since they ROSELL, 2000). Also, road-kill rate can be determine local distribution of the species lower in main roads than in secondary ones, (ORŁOWSKI et al., 2008). For this reason, it is which could be explained by the previous essential to understand the different spatial population decline caused by roads with high scales at which threat processes operate. In traffic intensity (ORŁOWSKI, 2007). In general this sense, road segment and population sca- terms, it is supposed that the number of road- les are more suitable than regional and species kills increases with traffic volume. Due to distribution scales to identify the best loca- their small sizes and relatively low speed of tion for implementation of the mitigation movements, amphibians and reptiles suffer measures (BEAUDRY et al., 2008). HERPETOFAUNA AND ROADS 11

The temporal distribution of herpetofauna al., 2005). For example, northern leopard road-kills is related to species’ activity patterns frogs (Lithobates pipiens) move at a slower (BERNARDINO & DALRYMPLE, 1992; BONNET speed and following more tortuous paths as et al., 1999). Inter-specific differences can also they approach roads. Furthermore, move- be partially explained by differences in species’ ment speed is also reduced as traffic volume ecological requirements. For amphibians, high grows, two synergistic factors that reduce the risk exists during breeding migrations, which probability of cross success in this species show high inter-specific variation in terms of (BOUCHARD et al., 2009). distance (MONTORI et al., 2003; KOVAR et al., In the case of snakes and other reptiles as 2009). In the Lozoya Valley (Madrid, Spain) the snapping turtle (Chelydra serpentina), the the peaks of road mortality for the natterjack number of road-kills increases as a conse- toad (Bufo calamita) and B. bufo occurred bet- quence of the intentional action of the dri- ween the last two weeks of March and the first vers. In a study conducted in Canada, up to two weeks of May, during the seasonal migra- 2.5% of the drivers positively selected to hit tions to the breeding sites (SCV, 2003). As reptiles (ASHLEY et al., 2007). In other migration distances increase, the probability of Australian study, 25% of drivers reported crossing roads also increases. Moreover, the that they intentionally ran over invasive cane breeding habitat requirements condition road- toads (Rhinella marina). However, field expe- kill locations. Thus, species that can breed in riments did not confirm this behaviour, but any accumulation of shallow water will have found a rate of collisions not different from less defined hotspots than those species that random (BECKMANN & SHINE, 2012). breed in ponds or streams. In turtles and snakes, breeding season also IMPACTS OF ROADS ON HERPETOFAUNA concentrates most road-kills (BONNET et al., 1999; CURETON & DEATON, 2012). The effects of road pollution Furthermore, daily variations in temperature and precipitation may also influence road The impact of the emission of pollutants mortality rates, as observed by SHEPARD et al. by vehicles and the use of certain chemicals in (2008a) in these two groups of reptiles, road maintenance (herbicides, de-icing salts) whose frequency of road-kills is positively on herpetofauna (Fig. 1) has been studied correlated with minimum daily temperatures. almost exclusively in amphibians, and most The behaviour in response to roads and examples point to a negative effects on their traffic is another important factor determi- populations. For example, the proximity to ning the spatio-temporal distribution of the road correlates with an increased probabi- road-kills, not only at the inter-specific but lity of suffering skeletal malformations and a also at the intra-specific level. Many indivi- smaller body size in larval wood frogs duals remain immobile when sensing the (Lithobates sylvaticus) (REEVES et al., 2008). arrival of a vehicle, which involves an increa- Although the causes are not entirely clear, an se in the crossing time, and consequently in increased risk of injury caused by predation the probability of being killed (MAZEROLLE et due to a small size, a change in the composi- 12 COLINO-RABANAL & LIZANA

Figure 1: Main road effects on herpetofauna populations. Construction of new roads can imply the loss of high quality habitats for herpetofauna. Moreover, amphibians and reptiles can be road-killed when trying to cross. Roads difficult their movements by increasing fragmentation and exerting a barrier effect; however, road ditches sometimes act as corridors. Traffic flow also impacts on populations through dispersal of che- mical pollutants or other types of pollution as noise or lighting. Some practices like the use of de-icing salt in winter maintenance can also impact amphibian or reptile populations. All these road impacts extend tens or hundreds of meters away from the road edge delimiting the road-effect zone. tion of predator community, or the presence trations of salt in the water act as an environ- of chemical contaminants from vehicle traffic mental stressor affecting aquatic fauna with could explain this phenomenon (REEVES et low tolerance to salinity. On amphibians, high al., 2008). Also, amphibian larvae near roads salt concentrations can induce death by dehy- with high traffic volume bioaccumulate lead dration. Increased water salinity in road from fossil fuels at doses that may have surroundings produced a reduction in survival physiological and reproductive effects rate, metamorphosis time, activity, and (BIRDSALL et al., 1986). However, this pro- weight, as well as an increase in the number of blem has been reduced after removal of this malformations in larval L. sylvaticus (SANZO & heavy metal from fuels. HECNAR, 2006). For this species and for the A widely extended maintenance practice is spotted salamander (Ambystoma maculatum), the use of de-icing salt to prevent the forma- KARRAKER et al. (2008) also found a reduction tion of ice and snow on the road. This affects in the survival rate of embryos and larvae large regions at high latitudes and mountai- along with an up to 50% decrease in the num- nous areas where frost and snow precipitation ber of egg masses in the vicinity of roads. They are common during winter. Winds or the concluded that these effects could lead to local water runoff can carry salt tens to hundreds of extinctions, especially of A. maculatum popu- meters away from the roadside, increasing sali- lations, given its high sensitivity to salinity. nity in rivers and ponds nearby. High concen- Laboratory experiments conducted in micro- HERPETOFAUNA AND ROADS 13 cosms with water collected from basins recei- duals living permanently in locations with ving runoff from high-capacity roads showed high traffic noise. This plasticity is essential total mortality of exposed L. sylvaticus larvae, to maintain acoustic communication in envi- while A. americanus larvae did not suffer lethal ronments with traffic noise. However, effects (SNODGRASS et al., 2008). In this sense, LENGAGNE (2008) did not detect the ability because of the inter-specific differences in sen- to modify the frequencies or temporal struc- sitivity, the salt used on roads could act as a ture of the call in the European tree frog stressor capable of changing the structure of (Hyla arborea), which suggests that those spe- amphibian communities (COLLINS & cies capable to acclimatize to traffic noise RUSSELL, 2009). may have a competitive advantage respect to less plastic species. In this regard, SUN & The impact of traffic noise and light NARINS (2005) found that in a community exposed to environmental noise, individuals of High levels of environmental noise caused the two-striped grass frog (Hylarana taipehensis) by traffic pose a great challenge for species took advantage of this factor by increasing its that use acoustic communications (Fig. 1). song rate while the other three studies species Thus, traffic noise reduces the ability of decreased it. female Cope’s gray treefrogs (Hyla chrysoscelis) Light is another element associated with to detect male calls (BEE & SWANSON, 2007). roads and traffic that may impact herpetofau- In an attempt to avoid masking by high levels nal populations. As many species are noctur- of environmental background sound, terres- nal, car lights may lessen their ability to pre- trial animals can introduce changes in the vent being killed by vehicles, since such lights features of their acoustic signals. This capa- saturate their retinas leaving them blind and city could be a key factor for reproductive disoriented for a few seconds. Light pollution success in noisy environments. In amphi- also affects the ability of some species to bians, some well-documented cases for this detect and capture prey (BUCHANAN, 1993). phenomenon show that the increases in sig- nal frequencies in order to avoid masking (i.e. Habitat fragmentation and loss of connectivity whistling tree frog, Litoria ewingii) are less marked than those identified for birds, but Roads act as barriers and/or filters, cau- also sufficient to improve communication sing habitat fragmentation and population capacity (PARRIS et al., 2009). Another spe- isolation (Fig. 1). Fragmentation is among cies, the Neotropical treefrog (Dendropsophus the largest threats for amphibian and reptile triangulum), is capable to increase its song populations (BECKER et al., 2007). Several rate (KAISER & HAMMERS, 2009). In an expe- studies have demonstrated the huge fragmen- riment exposing anurans inhabiting far away tation effect caused by roads on herpetofau- from roads to traffic noise recordings, nal populations. For instance, in an experi- CUNNINGTON & FAHRIG (2010) showed that ment carried out in six paved roads in animals immediately altered their vocaliza- Virginia and West Virginia (USA) with trans- tion characteristics in a similar way as indivi- located individuals of redback salamander 14 COLINO-RABANAL & LIZANA

(Plethodon cinereus) the rate of return for trial fauna in south-eastern South Australia, those who had to cross a road was about a including the bold-striped cool-skink 50% lower than for those who just had to (Bassiana duperreyi), fire-roads were not an pass through the forest (MARSH et al., 2005). obstacle. However, for the painted spadefoot In this species, genetic differences are visible toad (Neobatrachus pictus) no crosses of the in those populations bisected by a major fire-road were detected. highway but not in those separated by secon- Snake responses to habitat fragmentation dary roads (MARSH et al., 2008). by roads can vary substantially depending on As expected, road fragmentation does not the species’ ecological and anatomical featu- affect equally to all species. Short-term impact res, the smaller being generally more reluctant of fragmentation correlates positively with to cross (ANDREWS & GIBBONS, 2005). The species’ dispersal ability, although those spe- massasauga (Sistrurus catenatus) shows a clear cies with low dispersal abilities may be equally rejection to traverse roads. In Manitoba affected over long time periods (CUSHMAN, (Canada) the red-sided garter snake 2006). Most frog species in a wooded area (Thamnophis sirtalis parietalis) avoided gravel showed no rejection to the presence of roads roads (SHINE et al., 2004). The same results and forest roads, and even some species posi- were found for the eastern box turtle tively selected areas close to roads at certain (Terrapene carolina) and the western box tur- stages of development. The opposite happe- tle (Terrapene ornata). If this rejection was ned to urodeles as salamanders, whose popu- heritable, road-kills would decrease over time lations were bigger in remote areas than in because those individuals who tended not to zones close to roads (DEMAYNADIER & cross the roads would be selected, which in HUNTER, 2000). For forest salamanders, the turn would increase the degree of isolation edge effect of forest roads due to reduced between populations (SHEPARD et al., 2008b). moisture and vegetation cover is comparable The interruption of seasonal migrations cau- to recently cleared areas (MARSH & sed by roads reduced genetic diversity and BECKMAN, 2004). Roads also alter selection increased genetic differentiation in timber rat- patterns of the spawning sites in urodeles, tlesnakes (Crotalus horridus), even in a short especially in those species with little tolerance period of time (CLARK et al., 2010). to alteration, as CHAMBERS (2008) observed Some species can use roads as corridors for the Jefferson salamander (Ambystoma (Fig. 1). To move between favorable habitats, jeffersonianum) or the marbled salamander green frogs (Lithobates clamitans) frequently (Ambystoma opacum), whereas the more tole- used, with high survival rates, road drainage rant eastern newt (Notophthalmus viridescens) ditches inside a matrix of peat fields where suffered less severe alterations of spawning site they rarely ventured (MAZEROLLE, 2004b). due to road impacts. Furthermore, road ditches are suitable insola- Fire-roads can also act as barriers to herpe- tion areas in forested ecosystems. Roads can tofauna movements, although there is impor- also constitute a route of access to habitats tant variation among species. CARTHEW et al. with high vegetation cover for termophile (2009) found that for most species of terres- species (HEDEEN & HEDEEN, 1999). HERPETOFAUNA AND ROADS 15

However, the fact that roads can act as roads with high traffic volumes. These stu- corridors may also have negative effects dies were carried out with anurans but the because, similarly, they may favour the spre- results are similar for urodeles (SEMLITSCH et ad of invasive species. Road surroundings are al., 2007). Mortality rates can be higher in habitats with a substantial level of alteration new roads and tend to diminish through the that are favourable to invasive species. For time, which would be related to the fact that example, the progressive spread of R. marina road-kills contribute to progressively decre- in Australia has been especially fast in areas ase population size, thus causing population with high road density and high connectivity declines (CARRETERO & ROSELL, 2000). In (URBAN et al., 2008), which is an expected general, amphibian species richness decrea- outcome considering that this invasive toad is ses in presence of roads (FINDLAY & more abundant in the roads or tracks than in HOULAHAN, 1997; GARRIGA et al., 2012). It the surrounding habitats (SEABROOK & was estimated for A. maculatum in several DETTMAN, 1996). breeding pools in New York State that under the average displacement performed during Effects of roads on herpetofauna populations migration to breeding sites, one to three- quarters of the population could be affected A good review of the effects of roads on by road mortality. In those populations, herpetofauna abundance (and also for the road-kills involved the addition of more rest of the vertebrate groups) can be found than 10% to natural mortality, which would in FAHRIG & RYTWINSKI (2009). They jeopardize their long-term viability (GIBBS found in the literature 22 amphibians and & SHRIVER, 2005). six reptiles for which road effects had been Thresholds of both road density and traf- evaluated. The responses were negative for fic volume over which the implementation of more than 70% of amphibians and 80% of mitigation measures is justified can be defi- reptiles, although the results were someti- ned using life tables and migration distances mes contradictory. Population declines of of each species (GIBBS & SHRIVER, 2005). herpetofauna species have been attributed, However, differences in behaviour may make at least partially, to road mortality (FAHRIG some species more susceptible than others to et al., 1995; GIBBS & SHRIVER, 2002, 2005; road impact. Thus, the level of vulnerability MARCHAND & LITVAITIS, 2004; PUKY, depends on the mobility of each species. A 2006). FAHRIG et al. (1995) or SUTHERLAND research carried out in the Ottawa-Carleton et al. (2010) showed that amphibian density region (Ontario, Canada) revealed that, while was lower in roads with high traffic volumes a mobile species like L. pipiens showed a than in roads with little traffic. Moreover, negative correlation between their population the ratio between dead and alive individuals abundances and traffic density on nearby was higher as traffic intensity increased. roads, in another species with shorter displa- This fact supports the hypothesis that road- cements like L. clamitans there was no rela- kills can cause the decline of amphibian tionship between population size and traffic populations near roads, especially in those intensity (CARR & FAHRIG, 2001). 16 COLINO-RABANAL & LIZANA

Reptile populations are also vulnerable to the same happened to adults relative to imma- roads impacts. A study in Ontario, Canada, ture individuals. Moreover, a peak in the num- with radio-marked individuals of eastern rat ber of road-kills was found during the spring snake (Pantherophis obsoletus) showed that the (BRITO & ÁLVARES, 2004), and the same hap- species did not avoid the road and, although pened for populations of those two species in the probability of collision was low (less than northern Spain (MARTÍNEZ-FREIRÍA & BRITO, 1%), mortality was big enough to compromi- 2012). On the other hand, MONTORI et al. se the long-term population viability (ROW et (2003) suggested that for most snake species in al., 2007). For snakes, mobility is also a key Catalonia, including the horseshoe whip snake factor to explain the inter-specific differences (Hemorrhois hippocrepis), the Montpellier snake found in population vulnerability to road (Malpolon monspessulanus), the ladder snake impacts (BONNET et al., 1999). Thus, forager (Rhinechis scalaris) and the southern smooth snakes show higher vulnerability to roads than snake (Coronella girondica), immature indivi- sedentary ones (MEEK, 2009). A model inclu- duals would be more frequently road-killed ding road network, traffic volume and mobi- than adults, being the peak of road mortality lity of two species estimated an annual road coincident with juvenile dispersal in late sum- mortality rate about three times higher for mer and fall. However, because of the low mobile species than for sedentary ones (14-21 % detectability of small individuals the real for the plain-bellied watersnake, Nerodia impact of road-kills on immature specimens erythrogaster, vs. 3-5% in the Lake Erie water would be underestimated. snake, Nerodia sipedon) (ROE et al., 2006). Male-biased road mortality has also been It is necessary to point out that road morta- reported for other snake species like S. catenatus, lity can affect populations as long as these with a peak at the end of the summer populations are limited by mechanisms inde- (SHEPARD et al., 2008a), or C. horridus, with pendent from population density, in which males showing a road mortality rate 13 times case road-kills have an additive effect. higher than females (ALDRIDGE & BROWN, Moreover, the distribution of casualties in rela- 1995). This bias could be explained by the tion to sex and age is also very important to high mobility of males, especially during the assess the real impact of road-kills. For exam- mating season when they increase their ple, the mortality of females of oviparous spe- movements in search of females. Common cies on their egg-laying migrations is likely to green iguana (Iguana iguana) males suffer be more damaging to population viability than more road-kills than females, and popula- the same mortality rate affecting males or neo- tions near roads show a female-biased sex nates (BONNET et al., 1999). These sex- or age- ratio of the adult population (RODDA, 1990). related differences in magnitude of road For certain freshwater turtle species, road- impacts can modify the demographic structure kills constitute a serious threat for their popu- of herpetofauna populations. In northern lations (GIBBS & SHRIVER, 2002). A well- Portugal, males of Lataste’s viper (Vipera latastei) documented phenomenon in these species is and Seoane’s viper (Vipera seoanei) were more the disproportionately high number of fema- frequently found road-killed than females, and les road-killed during their displacements to HERPETOFAUNA AND ROADS 17 overland nesting locations, an effect that is forest anurans can be as high as the impact of not so pronounced in semi-aquatic and habitat loss, as demonstrated by EIGENBROD terrestrial turtles. As a result, freshwater tur- et al. (2008), who observed in Ontario tle populations near roads are biased towards (Canada) that the species richness and abun- males (STEEN & GIBBS, 2004; STEEN et al., dance of three of the six species studied were 2006) and this bias has increased linearly more correlated to traffic density than to the during last decades (GIBBS & STEEN, 2005). absence of forest. Moreover, the edges of the road may become As a consequence of the fragmentation attractive places to establish nests, which caused by linear infrastructures there is a attracts females to the vicinity of the road reduction in genetic exchange (VOS et al., (ARESCO, 2005a). Thus, in many aquatic tur- 2001). Fragmented populations are very vul- tles the nesting period coincides with the nerable to inbreeding processes. Low heterozy- maximum rate of road-kills (BEAUDRY et al., gosity values were found in agile frog (Rana 2010). On the contrary, for other species like dalmatina) populations living in ponds near the diamondback terrapin (Malaclemys terra- roads. The likely cause of this genetic homoge- pin) there is no relationship between the pro- nization is the reduction of the number of ximity to roads and variations in individual adult individuals, either by road-kills, noise or density or sex ratio (GROSSE et al., 2011). pollution (LESBARRÈRES et al., 2003). Beyond Road impacts do not act only at a local lower allelic richness, populations fragmented scale. On a regional scale, the presence of by roads have a higher degree of genetic diffe- roads is one of the main elements that explain rentiation than populations from non-frag- the presence of various species of salamanders, mented habitats (LESBARRÈRES et al., 2006). but with different results depending on the specific tolerance to altered environments: the Road-effect zone for herpetofauna tolerant species are benefited while the abun- dance of the sensitive ones decreases (WARD et The combined effect of all road impacts al., 2008). Road density is negatively correla- on herpetofauna populations delimits a ted to the presence of R. arvalis whose proba- “road-effect zone” (Fig. 1) that can be defined bility of occurrence in habitats adjacent to as the area in which ecological effects extend roads is halved compared to what happens in outward from a road (FORMAN & non-fragmented areas. This fact shows that ALEXANDER, 1998). In the Galapagos Islands, habitat fragmentation is one of the factors lava lizards (Microlophus albemarlensis) have a that explain the species’ spatial distribution lower density in the upper 100 m from the patterns (VOS & CHARDON, 1998). The viabi- road edge, and show a probability of having lity of a common spadefoot (Pelobates fuscus) experienced tail loss up to 30 times higher metapopulation isolated by roads is quickly than individuals from other populations compromised by a slight decrease of indivi- (TANNER & PERRY, 2007). The effect on the duals dispersing from source populations Tenerife lizard (Gallotia galloti) varies in rela- (HELS & NACHMAN, 2002). In fact, the mag- tion to the adjacent habitat; while roads can nitude of the impact of the road network on play their usual role as barriers or source of 18 COLINO-RABANAL & LIZANA mortality, in those cases where roads cross freshwater turtles by more than 99%, effecti- habitats unsuitable for the species, like the vely preventing the crossing attempts, which laurel forest, they may act as corridors had only a 2% of chance of success (ARESCO, (DELGADO GARCÍA et al., 2007). Lungless 2005b). However, although the installation salamanders avoid even the forest roads crea- of fences decreases the mortality rate due to ted for the timber industry, especially the collisions, it also reduces the connectivity oldest ones, within a band of about 35 m with the other side of the road, making the (SEMLITSCH et al., 2007). BOARMAN & migration to breeding sites difficult and SAZAKI (2006) found that the population enhancing population isolation. density of desert tortoises (Gopherus agassizii) In order to promote habitat defragmenta- increased with the distance to the road edge, tion, the adaptation of drainages and the cons- being especially small within a band of about truction of wildlife crossings designed for her- 800 m around the road. VON SECKENDORFF petofauna have been proposed. The effective- HOFF & MARLOW (2002) extended this ness of this measure is supported by the fact road-effect zone to a 4000 m bandwidth. that amphibian migration is facilitated by tun- The decrease in population density may nels constructed for drainage under roads not have linear relationship with the distance (HARTEL et al., 2009). The design and cons- to the road and it is possible to detect thres- truction features that increase the effectiveness holds; for example, EIGENBROD et al. (2009) of herpetofauna passages vary among species, identified in Ontario a threshold in popula- although there is considerable flexibility that tion abundance at 250-1000 m from road facilitates decision-making to find a compromi- edge for more than half of the studied spe- se considering the species present in the area. cies, as well as for the species richness itself. WOLTZ et al. (2008) found that all the studied Finally, off-road vehicles may add an adverse species – two freshwater turtles, C. serpentina and effect on populations inhabiting road proxi- the painted turtle (Chrysemys picta), and two mities (BURY & LUCKENBACH, 2002). anurans (L. clamitans and L. pipiens) – preferred tunnels with diameter widths above 50 cm and Mitigation measures to reduce road impacts on sand or gravel firm, together with a fence of herpetofauna about 60 cm. The species showed a strong dis- like for structures with diameters below 30 Various mitigation measures with diffe- cm. In this sense, longer tunnels require larger rent efficacies and costs have been proposed diameters (PUKY, 2003). LESBARRÈRES et al. in order to solve, or at least reduce the impact (2004) found that while B. bufo and the edible of road-kills and habitat fragmentation on frog (Pelophylax esculentus) used the tunnels, amphibians and reptiles. The construction of R. dalmatina rejected them. All species prefe- fences or walls that impede access to the road rred soil beds rather than bare concrete and has been effective in reducing mortality of corrugated steel. A viaduct construction toge- amphibians (RYSER & GROSSENBACHER, ther with the installation of a fence designed 1989; DODD et al., 2004). The installation of for amphibians and reptiles drastically reduced a temporary fence reduced the mortality in mortality in a road that run between two HERPETOFAUNA AND ROADS 19 wetlands (SCOCCIANTI, 2006). The accessibi- zone of collision risk, for most reptiles that lity must be guaranteed in order to keep the tend to use roads for thermoregulation. tunnels or other kind of herpetofauna cros- During road construction, habitat des- sings functional (PUKY, 2003). truction can affect negatively to herpetofauna The location of herpetofauna passages populations. GUYOT & CLOBERT (1997) pro- should be selected following the knowledge posed to minimize the impact on a popula- acquired in the studies about the spatio-tempo- tion of Hermann’s tortoise (Testudo hermanni) ral distribution of road-kills as well as about the by means of capturing and maintaining herpetofauna use of the space (PATRICK et al., them in fenced spaces during construction 2010). Decision-making must take into account of the road, and then releasing them after those routes positively selected by animals and completion of the works. It has also been the amplitude of their movement ranges (VAN proposed that, when aquatic habitats used GELDER et al., 1986; HARTEL et al., 2009). by amphibians for breeding are eliminated Several methodologies have been used to quan- as part of the road construction process, the tify the effectiveness of the mitigation measures: creation of replacement ponds close to where track plates (not specific for herpetofauna) (e.g. the destroyed ones were located would mini- MATA et al., 2005), funnel traps or pitfall traps at mize the impact for populations tunnel exits (DODD et al., 2004) or cameras to (LESBARRÈRES et al., 2010). monitor tunnel use (PAGNUCCO et al., 2011). Cost-benefit analysis is a possible appro- Additionally, the structures associated ach to facilitate decision-making about where with main roads, like ditches for drainage of to locate mitigation measures. This approach rain water, seemingly harmless, can become follows economic criteria and tends to maxi- real traps for amphibians during their migra- mize the return in measure investments. tion. ZHANG et al. (2010) described this pro- SHWIFF et al. (2007), following the principles blem for juveniles and sub-adults of Asian of ecological economics, quantified the eco- common toad (Duttaphrynus melanostictus). nomic losses associated with the herpetofau- A design with sloping side walls with a maxi- na road-kills in a Florida wilderness. mum tilt of 66°, with a firm edge of stone Contrarily to these estimations including, for and gravel with a cement grout and vegeta- example, large ungulates, where it is possible tion would minimize the impact of these to assess vehicle or human damages related to structures on amphibian populations. collisions, in the case of herpetofauna the Another suggested measure to reduce road authors selected the penalty that would be impacts on fauna is the maintenance of clear, imposed by law in the state of Florida for the unvegetated margins to allow drivers for collection of an individual of the species seeing animals before they begin to cross the found killed on roads in order to calculate the road (ROSELL & VELASCO, 1999). While this economic value of the losses. is a measure basically though for large mam- Most mitigation measures are usually mals, it can indirectly benefit reptiles; espe- thought and designed for their implementa- cially in forested areas, clear margins would tion at a local scale, following the recommen- constitute an area of insolation, out of the dations of the environmental impact assess- 20 COLINO-RABANAL & LIZANA ments. However, this scale fails to ensure ade- and inconclusive (ELZANOWSKI et al., 2009). quate consideration of the potentially serious Moreover, research results may sometimes be cumulative, indirect and synergistic ecological unexpected. For example, highway water effects of roads. An adequate plan to minimi- ponds may surprisingly contribute to increa- ze road impacts should start at the regional se amphibian biodiversity in altered landsca- scale by spatial planning and strategic environ- pes (LE VIOL et al., 2012). As we stated, the mental assessment of the road network results of the road effects on herpetofauna (TREWEEK et al., 1998), including the conser- populations can be contradictory (see FAHRIG vation of the herpetofauna species as another & RYTWINSKI, 2009). We should deepen in goal to achieve. For example, certain species the origins of these contradictions and the such as the common snake-necked turtle role that the differences in methodology play (Chelodina longicollis) use different types of on them. An important effort to integrate all water points as a function of hydroperiods and the information available is required. seasonal movements. Therefore, their conser- To increase our understanding about this vation requires not only the protection of topic we should exploit any technique or metho- water points and a land area around them, but dology available. Particularly promising are the should consider the diversity of habitats they advances in genetic analyses that allow the detec- use and ensure connectivity between them tion of small differences between populations (ROE & GEORGES, 2007). The first step could that have partially lost their connectivity. At this be the identification of areas with high herpe- respect, genetic results reveal that traffic intensity tofauna diversity. These would be the priority reduction could be a good solution for certain areas to install mitigation measures in the exis- species (e.g. the palmate newt, Lissotriton helveticus) ting roads, and at the same time, they would but not for others for which even the secondary be the areas protected from new infrastructure roads with low traffic volumes act as barriers (e.g. projects (BENAYAS et al., 2006). The same tre- the common midwife toad, Alytes obstetricans) atment should be applied to protected areas, (GARCIA-GONZALEZ et al., 2012). Therefore, where road-kill rates can be elevated due to the DNA analysis becomes a powerful tool to reception of visitors (GARRIGA et al., 2012). facilitate road planners and environmental managers the decision-making about the CONCLUSION most effective mitigation measures. This decision is not always easy since the species According to the results of dozens of stu- present can respond differently to the same dies about the relationship between herpeto- mitigation measure. Moreover, population fauna and roads, the increasing vehicular traf- consequences also vary among species both fic is widely suspected to compromise herpe- quantitatively and qualitatively. In this con- tofauna conservation and to play a role in text it becomes necessary to develop mecha- population declines. Nevertheless, the rese- nisms to reach a consensus solution. arch about the road impacts on the herpeto- Road effects have been quantified only for fauna is fragmented, limited for comparisons a few number of herpetofauna species. More among zones, with methodological problems, research on unstudied species and in different HERPETOFAUNA AND ROADS 21 habitats is required, especially in those areas REFERENCES comprising both high biodiversity levels and an increasing expansion of the road networks ALDRIDGE, R.D. & BROWN, W.S. (1995). (e.g. rainforests, HOSKIN & GOOSEM, 2010). Male reproductive cycle, age at maturity, Moreover, other possible road effects or and cost of reproduction in the timber mechanisms of affection should be conside- rattlesnake (Crotalus horridus). Journal of red. Thus, the loss of older individuals by Herpetology 29: 399-407. road-related mortality could lead long-lived ANDREWS, K.M. & GIBBONS, J.W. 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