Reptile Road Mortality in a Fragmented Landscape of the Middle Magdalena Valley, Colombia

Herpetology Notes, volume 11: 81-91 (2018) (published online on 27 January 2018)

Reptile road mortality in a fragmented landscape of the middle Magdalena Valley, Colombia

Eliana Ramos1 and Fabio Leonardo Meza-Joya1,*

Abstract. Wildlife-vehicle collisions kill millions of wild animals around the world; however, this number could be underestimated given the absence of monitoring of road-kill events. Here, we aimed to examine reptile road mortality in three (3) routes (Departmental Route 01, National Route 66, and National Route 45), located on a fragmented landscape in the Middle Magdalena Valley, Santander department, Colombia. We described the species composition affected by road mortality, estimated the road-kill rates for each road segment studied, and analyzed the spatial and temporal distributions of reptile road- kills, identifying road-kill hotspots, and proposing mitigation measures. During an 8-month period, we recorded a total of 66 road-killed reptiles belonging to 18 species. There was a difference in the number of road-kills among seasons; most road-kill events occurred during the rainy season. The road with the highest number of road-kill events was Departmental Route 1 (DR01), which also exhibited the highest road-kill rates compared to the other road segments assessed. Spatial distribution of road-killed reptiles was non-random for route DR01, indicating that mortalities were aggregated in some locations, which correspond to potential road-kill hotspots. The road-kill hotspots identified in this study offer a unique opportunity for the designing of efficient mitigation measures. Based on our results, as well as the social and economic context of the study region, we consider that mitigation measures should focus mainly on designing and promoting effective educational activities and materials among adults and children to increase public awareness and to promote a behavioral change among drivers towards the protection of wildlife.

Keywords: road mortality, road-kill hotspots, mitigation measures, spatial distribution

Introduction Roads have a crucial role in modern economy and society providing connectivity between human settlements and access to critical services, resources, and activities (Forman et al., 2003; Maschio et al., 2016). However, the physical presence of roads in the landscape also threatens biological diversity directly through wildlife mortality by vehicle collisions and indirectly by promoting habitat loss, fragmentation, disturbance, and barrier effects (Seiler, 2001; Forman et al., 2003; Lester, 2015). Although the understanding of the relative importance of road impacts on biodiversity has yet to be accomplished, road mortality has been proposed as the leading direct human cause of vertebrate mortality on Earth (Forman and Alexander, 1998;

Figure 1. Study area indicating the three surveyed road 1 Colombia Endémica, Asociación para el Estudio y la segments in the Middle Magdalena Valley (Santander Conservación de los Recursos Naturales, Calle 35 # 27-78, department, Colombia). Red dots indicate the locations of Bucaramanga, Colombia road-killed specimens. Inset: location of the study are in * Corresponding author. E-mail: [email protected] Santander department, Colombia. 82 Eliana Ramos & Fabio Leonardo Meza-Joya

1Table Table 1. 1. General General description description of the surveyed of the route surveyed segments, route landscape, segments, and anthropogenic landscape, features and (urbanization anthropogenic level). features (urbanization level).

Route Segment description Length Landscape description Urbanization level

DR01 2-lane paved road with irregular center line; 26 km Smooth hills dominated by oil exploration and Suburban absent to narrow shoulder, some roadside extraction areas, pastures, herbaceous and shrubby ditches; speed limit 80 km/h vegetation

NR66 2-lane paved road with center line; absent to 31 km Smooth hills characterized by pastures, Rural wide shoulder, intermittent roadside ditches; heterogeneous agricultural areas, small forest speed limit 100 km/h patches, and dump and construction sites

NR45 2-lane paved road with center line; wide 18 km Smooth hills and plains dominated by pastures, Rural shoulder; discontinuous roadside ditches; heterogeneous agricultural areas, herbaceous and speed limit 100 km/h shrubby vegetation, and forest patches

Seiler, 2001; Forman et al., 2003). This phenomenon measures. Here, we aimed to examine reptile road is thought to have a significant impact on populations mortality in three routes located on a fragmented of vertebrate species that are especially vulnerable to landscape in the Middle Magdalena Valley, Santander vehicle collisions, including species that are attracted department, Colombia. We described the species (or show no avoidance to roads or traffic disturbance) composition affected by road mortality and estimated and are unable to evade individual cars; and species the road-kill rates for each studied road segment. We with large home ranges and low reproductive rates and also analyzed the spatial and temporal distributions of densities (Fahrig and Rytwinski, 2009). reptile road-kills, identifying the location of road-kill Although most road mortality studies have focused hotspots, and proposing mitigation measures. 1 on mammals, vehicle collision is an important source of mortality to many species of reptiles in temperate Materials and Methods and tropical regions (e.g., Rosen and Lowe, 1994; Study area.—This study was carried out in the Middle Klingenbock et al., 2000; Gibbs and Steen, 2005; Magdalena Valley (06°59’41.6’’N, 73°44’51.5’’W, 90 m Lebboroni and Corti, 2006; Glista et al., 2007; Hartmann elevation), municipality of Barrancabermeja, Santander et al., 2011; Maschio et al., 2016). In Colombia, most department, Colombia (Fig. 1). This region is located studies in this topic have focused on wild terrestrial within the Tropical Moist Forest life zone (Holdridge, vertebrate groups (e.g., de la Ossa-Nadjar and de la 1987) and comprises extensive lowland alluvial plains Ossa-V., 2013, 2015; Castillo et al., 2015; de La Ossa-V. with many swampy ecosystems interspersed with non- and Galván-Guevara, 2015; Monroy et al., 2015), and flooded areas (Garzón and Gutiérrez, 2013). The climate rarely have attempted to evaluate exclusively reptile is characterized by a bimodal rainfall regime, with a road-kills (e.g., Vargas-Salinas et al., 2011; Quintero- mean annual precipitation of 2,917 mm, a mean annual Ángel et al., 2012; López-Herrera et al., 2016). As a temperature of 27.9°C, and a relative humidity of 80% consequence, we are still far from understanding the (IDEAM, 2016). Human activities such as cattle and main factors related to reptile road mortality as well as oil exploitation have historically modified the Middle the road segments where most reptiles are killed by cars, Magdalena Valley (Garzón and Gutiérrez, 2013). which impedes the implementation of effective roadway Consequently, the study region is a land mosaic formed mitigation measures. by human settlements, highly disturbed small native Assessing the main drivers that influence wildlife road vegetation patches and extensive areas of pastures and mortalities is necessary to better understand spatial and oil infrastructure, including a complex network of roads temporal road-kill patterns (Lester, 2015). In particular, it aimed to connect the oil wells that make part of the La is important to identify the location of road-kill hotspots Cira Infantas petroleum field. as critical points to establish prevention and mitigation measures that lessen road mortalities (Ramp et al., Data collection.—Surveys were performed along 2005; Magnus, 2006; Lester, 2015). If increased rates of 75 km in three two-lane road segments (Fig. 1): mortality by collisions with vehicles are detected on a Departmental Route 01 (DR01: km 0+000 to km 26+000; segment of a road, this segment should be prioritized for from municipality of Barrancabermeja to National the implementation of conservation and management Route 45), National Route 66 (NR66: km 1+000 to Reptile road mortality in a fragmented landscape in Colombia 83

2 Table 2. Reptile road mortality and road-kill estimates for each surveyed route segment. Road-kill animals indicates the number 3 Table 2.of reptiles Reptile recorded road mortality during and road-kill monitoring estimates surveys for each surveyed with the route number segment. of Road-kill accidental animals encounters indicates the innumber parenthesis. of reptiles recorded For estimates during monitoring of road-kill

4 surveysrates with we theexcluded number of the accidental data fromencounters accidental in parenthesis. encounters. For estimates of road-kill rates we excluded the data from accidental encounters.

Route Road-kill Road-kill Length Total Total km Road-kill rate Road-kill rate Road-kill rate animals species (S) (km) surveys surveyed per km per day per year DR01 34 (8) 15 26 16 416 0.12 3.22 1,175 NR66 11 (4) 6 31 16 496 0.03 1.04 380 NR45 7 (2) 4 18 16 288 0.04 0.66 241 Total 52 (14) 18 75 48 1,200 ------1,796 5

km 32+000; from municipality of Barrancabermeja Lynch, 2009; Folleco-Fernández, 2010; Morales- to National Route 45), and National Route 45 (NR45: Betancourt and Lasso, 2012; Ramos-Pallares, 2016): km 54+000 to km 36+000; from National Route 66 mean body size (mm), main activity patterns (diurnal to Corregimiento Peroles). Surveyed roads varied and nocturnal), and substrate use (fossorial, terrestrial, in length and were chosen to represent a mixture of arboreal, semi-arboreal, aquatic, and semi-aquatic). geographic, anthropogenic, and landscape features Data analyses.—�� (Table 1). Although quantitative data on the daily calculated as the number of species (S) found dead on intensity of the traffic along the studied roads is absent, the surveyed road segments. To assess species richness direct observations indicates that DR01 is the road and inventory completeness we used a combined with the highest traffic of all kind of vehicles (specially method of extrapolation and rarefaction (Colwell et al., motorcycles, pickup trucks, and passenger and public 2012) implemented in the R package iNEXT version transportation vehicles) whereas NR45 is the road with 2 2.0.9 (Hsieh et al., 2016), estimating the species richness the lowest vehicular traffic (which is composed mainly by public transportation and heavy vehicles). via the Chao estimator (Chao 1984, 1987). A relative Road-kill surveys were conducted by two observers road mortality index (RMI) was estimated dividing the (driver and passenger) driving a car at slow speed (≤ 40 number of road-kill for each species by the total number km/h), twice per month from June 2013 to January 2014 of road-kills for all species. We explored if differences during rainy (August to November) and dry seasons in road mortality were related to the ecological (June to July and December to January). The observers characteristics of the road-killed species based on drove along the roadside searching on both sides of the descriptive analyses. We used a Mann-Whitney U test studied roads for reptile mortalities. This survey scheme to determine if differences of observed counts of road- was selected to cover relatively long road segments kills among the wet and dry seasons were statistically (i.e., 75 km) in relatively short time periods. Road- significant (P < 0.05). kills detected out of the regular sampling surveys were Mortality rates (i.e., per day and per km) were estimated considered as accidental encounters and were excluded for each road using Siriema (Spatial Evaluation of from the analyses; however, the data was retained to Road Morality) Software v2.0, a free software package show the diversity and ecological characteristics of the developed to evaluate spatial distribution of wildlife- species. Road-killed reptiles were identified in the field vehicle collisions along roads (Coelho et al., 2014). To to the species level using the taxonomy of Uetz et al. avoid overestimations in mortality rates, we used the (2016). When possible, animals were removed from the upper limit of the “searchers’ efficiency” for reptiles (i.e., road to avoid subsequent recounts. Animals severely 0.33) estimated by Teixeira et al. (2013a) and the upper deteriorated were categorized as unidentified taxa. limit of the removal time (2 days) calculated by Santos For each road-killed reptile, we recorded the date, et al. (2011). Our estimates of daily mortality rates were and geographic coordinates using a GPS ��ver. The multiplied by 365 to generate an annual estimate. For following ecological characteristics of each species practical purposes, we compared our results with those found were obtained from the literature (Dixon and from other studies estimating a relative road mortality Michaud, 1992; Dixon et al., 1993; Martins and rate by dividing the number of road-kill occasions into Oliveira, 1998; Rossman, 2002; Savage, 2002; Pizzatto, the total sampling effort (i.e., the overall number of km 2005; O’Shea, 2007; Rueda-Almonacid et al., 2007, surveyed). 84 Eliana Ramos & Fabio Leonardo Meza-Joya 6 Table 3. General list of reptiles recorded as road-killed during monitoring surveys with the number of accidental

Table 3. General 7list ofencounters reptiles in parenthesis,recorded and as theroad-killed road mortality during index (RMI). monitoring For estimates surveys of RMI withwe excluded the number the data from of accidental encounters in parenthesis, and the8 roadaccidental mortality encounters. index (RMI). For estimates of RMI we excluded the data from accidental encounters.

Taxa Road-kills RMI Crocodylia Alligatoridae Caiman crocodilus (Linnaeus, 1758) 10 (3) 0.185 Squamata Iguanidae Iguana iguana (Linnaeus, 1758) 13 (4) 0.241 Boidae Boa constrictor (Linnaeus, 1758) 3 (1) 0.056 Colubridae Spilotes pullatus (Linnaeus, 1758) 4 (2) 0.074 Chironius spixii (Hallowell, 1845) 4 (1) 0.074 Leptophis ahaetulla (Linnaeus, 1758) 3 0.056 Helicops danieli (Amaral, 1938) 2 0.037 Mastigodryas sp. 2 0.037 Clelia clelia (Daudin, 1803) 1 0.019 Erythrolamprus melanotus (Shaw, 1802) 1 0.019 Oxybelis aeneus (Wagler, 1824) 1 0.019 Oxyrhopus petolarius (Reuss, 1834) 1 0.019 Spilotes sulphureus (Wagler, 1824) 1 0.019 Unidentified sp1 1 0.019 Unidentified sp2 1 0.019 Viperidae Bothrops asper (Garman, 1883) 1 0.019 Testunides Emydidae Trachemys callirostris (Gray, 1855) 2 (2) 0.037 Kinosternidae Kinosternon leucostomum (Duméril, Bibron and Duméril, 1851) 1 (1) 0.019 Total road mortalities 54 (14) --- 9

The dispersion of road-kill events on different spatial confidence level of 95% and 1,000 simulations. Values scales was evaluated using a modified Ripley’s K for aggregation intensity above the upper confidence (Coelho et al., 2008) with an initial radius of 100 m, level of 95% indicate significant road-kill hotspots. For a radius increase of 400 m, confidence level of 95%, analyses in this section we used Siriema v2.0 (Coelho and 1,000 Monte Carlo simulations, following Teixeira et al., 2014). 3 et al. (2013b). Values above the confidence limit (95%) obtained from the simulations indicate scales Results with significant aggregations (Teixeira et al., 2013b). To detect the road sections with high mortality rates During an 8-month period and 16 surveys, we (aggregations), we implemented the 2D HotSpot recorded a total of 66 road-killed reptiles belonging to Identification analysis. For this, each road was divided 18 species (Table 2): 14 snakes, 2 turtles, 1 lizard, and 1 into 200 m segments and a circle of 400 m radius (based alligator (Table 3). Of this total, 52 road-killed reptiles on the 2D Ripley’s K test) was centered at the midpoint were found during the surveys and 14 by accidental of the first segment, summing the values for all road-kill encounters. The number of events per survey ranged events inside the circle area. This sum was multiplied from 0 to 8 road-killed reptiles (X = 2.75). The most by a correction factor that considers the length of the frequently road-killed reptiles during monitoring surveys road analyzed inside the circle in this position. This (Fig. 2; Table 3) were the lizard Iguana iguana (n = 13; procedure is repeated for all segments, resulting in a RMI = 0.241) and the alligator Caiman crocodilus (n road-kill aggregation intensity value for each segment = 10; RMI = 0.185). For snakes and turtles, the most of road (for details see Coelho et al., 2014). The frequently identified species were Spilotes pullatus (n significance of potential aggregations was evaluated at a = 4; RMI = 0.074) and Chironius spixii (n = 4; RMI = Reptile road mortality in a fragmented landscape in Colombia 85

Figure 2. Reptile carcasses found on the study area in Middle Magdalena Valley (Santander department, Colombia). Caiman crocodilus (A), Iguana iguana (B), Bothrops asper (C), Oxyrhopus petolarius (D), Chironius spixii (E), Spilotes pullatus (F). Photos by F. Leonardo Meza, Eliana Ramos, and Diana Cardona.

0.074), and Trachemys callirostris (n = 2; RMI = 0.037), on their activity patterns and substrate use. Over half of respectively. Together, these species represent about the road-kill specimens (61%) were diurnal (n = 38; 8 50% of the reptile road mortalities in the study area. species). Specimens of semi-arboreal (48.4%; n = 30; Most road-kills were individuals of large species (≥ 500 4 species), primarily aquatic (27%; n = 17; 2 species), mm SVL), summing 85% of the mortalities (n = 56; 16 and terrestrial (15%; n = 9; 6 species) species were most species). Four of the specimens (6%) were too damaged frequently found as road-killed. Most of road-kill events to identify the species and could not be classified based occurred during the rainy season (Z = 1.98, DF = 1, P = 86 Eliana Ramos & Fabio Leonardo Meza-Joya

10 Table 4.Table 4.Survey Survey methods methods and relative and road relative mortality road rate (RMR,mortality road-kills rate per (RMR, km surveyed) road-kills for road-kill per km studies surveyed) including reptilesfor road-kill in Colombia. studies Road-kill including animals reportedreptiles

11 forin thisColombia. study indicates Road-kill the number animals of road-kills reported recorded for during this the study moitoring indicates surveys. the number of road-kills recorded during the moitoring surveys.

Study Survey methods Location Elevation (m) Road-kill Total km RMR animals surveyed This study Car ( 40 km/h), twice per Middle Magdalena Valley, Santander 74-100 52 1,200 0.043 month, 8 months department Vargas-Salinas et al. (2011) Walking, twice per week, 6 Andean region, Cordillera Occidental, 1,200-1,700 20 115 0.174 months Valle del Cauca department Quintero-Angel et al. (2012) Walking, twice per month, 5 Andean region, Cordillera Central, Quindío 1,700-2,100 105 973 0.108 months department Castillo et al. (2015) Motorcycle (25 km/h), four times Andean region, Cordillera Occidental, 639-1757 58 4,600 0.013 per week, 5 months Cauca department López-Herrera et al. (2016) Walking, 6 months Andean region, Cordillera Central, Quindío 1,500-2,600 64 129 0.496 department de la Ossa-Nadjar and de la Motorcycle, four times per week, Caribbean region, Sucre department 45-307 220 9,536 0.023 Ossa-V (2013) 6 months de la Ossa-Nadjar and de la Motorcycle (15 km/h), six times Caribbean region, Sucre department 45-307 219 19,066 0.011 Ossa-V (2015) per week, 8 months de La Ossa-V and Galván- Motorcycle (14 km/h), twice per Caribbean region, Sucre department 6-64 94 1,306 0.071 Guevara (2015) week, 6 months Monroy et al. (2015) Motorcycle (15 km/h), twice per Caribbean region, Sucre department 14-32 189 2,352 0.080 week, 6 months 12

0.047). There were two road-kill peaks: the first one in The estimated relative road mortality rate (road-kills per May, when 14 reptiles were found, with a high number km) was variable when compared to other studies (Table

of snakes (n = 9); and a second one in November, when 4). Sampling coverage (Fig. 3) was greater for NR664 11 reptiles were found, with a higher number of iguanas (81%) and DR1 (80%) than for NR45 (70%). The Chao (n = 9). estimator produced an estimate of 18 (CI 14-37) species The road with the highest and lowerst number of for DR1, 11 (CI 7-44) species for NR66, and 7 (CI 5- road-kill events were, respectively, DR01 (n = 42; 15 26) species for NR45, predicting an increase in species species) and NR45 (n = 9; 4 species; Table 3). Similarly, richness (i.e., road-killed species) with additional road- the route DR01 showed the highest road-kill rates kill surveys (i.e., larger sample size). relative to the other road segments assessed (Table 3).

Figure 3. Sampling coverage curves of road-killed reptiles for the studied routes in Middle Magdalena Valley (Santander department, Colombia). Reptile road mortality in a fragmented landscape in Colombia 87

The results of Ripley’s K analyses showed that spatial diurnal, and semi-arboreal snakes are more prone to distribution for road-kill reptiles was non-random for the road mortality. These results are probably related to route DR01, indicating that mortalities were aggregated several factors. First, larger snakes are thought to be in some locations, which correspond to potential road- highly mobile, have larger home ranges, and apparently kill hotspots. 2D HotSpot analyses identified five disregard roads (see Macartney et al., 1988; Andrews, hotspots in this road, the first between km 0 and 0.6 and 2004; Jochimsen, 2005). In addition, diurnal snakes the resting four between km 11 to 17 (Fig. 4). There was may be more sensible to road-kills because their no aggregation of road-kill events in the other studied activity pattern coincides with increased traffic volume roads (i.e., NR45 and NR66), indicating the absence of in the studied roads. Lastly, semi-arboreal snakes in the road-kill hotspots. study area apparently use terrestrial substrates for long displacement because they are often found across open areas and roads (e.g., Boa constrictor, Chironius spixii, and Spilotes pullatus). Road mortality is assumed to be concentrated on one or few species, usually abundant, highly mobile, and habitat generalists (Forman et al., 2003). This trend was found in our study, in which road mortalities (45%) were more frequent in two species, the green iguana (Iguana iguana) and the spectacled caiman (Caiman crocodilus). These species display wide habitat requeriments and are common in the study area (Meza-Joya et al., in preparation), still mortality rates are related to environmental conditions. For example, similar to reports from the Llanos of Venezuela (Rodda, 1990), most male iguana mortalities (56%) occur during the rainy season, which coincides with the mating season (octuber-november), whereas female road moratities occurred primarily during the dry season, which coincides with the nesting season (january-february; see Figure 4. Significant reptile road-kill hotspots (in red) along Ramos-Pallares, 2016). In turn, most road mortalities of the route DR01 in the Middle Magdalena Valley, Colombia. spectacled caiman (60%) occur during the dry season The blue zone represents the function N events - N simulated (january-march), probably due to the fact that animals and the grey zone represent confidence limits. inhabiting temporal water bodies adjacent to the roads are forced to find new habitats, which could result in an increase in the rate of road mortality. Lastly, reptiles in general may be attracted to paved road surfaces for Discussion thermoregulation (Andrews and Jochimsen, 2007). Most reptile species found road-killed in the study Vehicular traffic presumably play a key role on reptile area were snakes (78% of the road-killed species, Table declines, but information about the actual impact of 3). A similar pattern has been reported by other studies road mortality on reptile populations is scattered and in roads of the Colombian Caribbean region, in which sometimes contradictory because differences in survey snakes are the reptile group most sensible to road-kill methods (Colino-Rabanal and Lizana, 2012; Köhler et events (e.g., de la Ossa-Nadjar and de la Ossa-V, 2013, al., 2016). Our estimates of the relative road mortality 2015; de La Ossa-V and Galván-Guevara, 2015; Monroy rate (road-kills per km) was variable when compared to et al., 2015). Reptiles possess many characteristics that other researches. Studies from Andean and Caribbean increase their probability of being involved in vehicle regions have reported lower and higher numbers of collisions, including ectothermy, age, sex, body size, road-kills while sampling shorter and larger road activity pattern, vagility, home range size, foraging sections during similar or shorter time periods (Table 4). strategy, defense mechanism, habitat requirements, The reptile mortality by road-kill in the study area was among others (reviewed in Jochimsen et al. 2004; lower than the road-kill of mammals observed in the Andrews, 2004). Our results indicate that large-sized, same samplings (66 against 112 road-killed specimens, 88 Eliana Ramos & Fabio Leonardo Meza-Joya respectively; Meza-Joya et al., 2015). Similar patterns surveys. Lastly, our estimates of road-kill rates should of reptile road-kill have been reported for the Caribbean be interpreted with caution because temporal variation region (e.g., Castillo et al., 2015; de La Ossa-V and of reptile habitat requirements (e.g., mates, refuges, Galván-Guevara, 2015), but contrasting results has also preys) and traffic volume, but it calls for new studies been reported for the Andean and Caribbean regions focused on the potential impacts of road mortality on (e.g., Vargas-Salinas et al., 2011; Quintero-Angel et al., reptile populations in the study area. 2012; de la Ossa-Nadjar and de la Ossa-V, 2013, 2015; Sampling coverage curves for all road segments studied Table 4). do not reach stability, suggesting that more reptile species Animals perceive, use, and cross the roads are target of road mortality in the studied roads (Fig. differentially from road to road, and even between 4). This incomplete sampling is not surprising, rather different sections of the same road (Havlick, 2004; represent a common trend in road-kill studies (e.g., Lester, 2015). In agreement, we found that route DR01 Santana, 2012; Braz and Franca, 2016; López-Herrera presented the highest number of road-kill events (n = et al., 2016). In fact, of 47 reptile species recorded in 42; 15 species), as well as the highest road-kill rate per the study region (Meza-Joya et al., in preparation), we km (0.12) and per day (3.22), when compared with the only recorded 16 species (34%) as road-killed during other studied roads (Table 2). Our estimates of road- our surveys. Although the road-killed species are not kill rate per year indicates that in this road segment listed as threatened by the IUCN Red List, species with nearby 1,175 reptiles are kill every year. The landscape life histories characterized by low reproductive rates in this road is highly fragmented and dominated by oil and low adult mortality, such as turtles, large snakes, exploration and extraction areas, pastures, herbaceous and vipers, are more vulnerable to the demographic and shrubby vegetation, as well as for several human consequences of road mortality (Forman et al., 2003, settlements (see Table 1). This road shows the highest Braz and França, 2016). However, it must be considered traffic of all kind of vehicles in the study area, principally that we were not able to estimate how these road-kills motorcycles and pickup trucks. Indirect evidence are affecting the species’ populations due to the absent (informal interviews with local people) also suggest that of data about abundance of reptiles in the study area. some drivers will intentionally run over reptiles in the The road-kill hotspots identified in the route DR01 study area, a common practice of drivers in Colombia (Fig. 4) coincides with sections of the road adjacent to (Quintero-Angel et al., 2012) and many regions around human settlements, most of them (four) into the area the world (e.g., Langley et al., 1989; Ashley et al., 2007; of direct influence of the La Cira Infantas petrolium Beckmann and Shine, 2012; Secco et al., 2014). field oil, an area with high daily vehicular traffic due Overall, our road-kill rate estimates suggest that to the need to transport workers from several sites of at least 1,796 reptiles are kill by vehicle collisions in the study region, mainly Barrancabermeja municipality. the study area per year (see Table 2). However, this The identification of these hotspots offer a unique number likely underestimates actual rates because in opportunity for the designing of efficient mitigation our analyses we used the upper limits for searchers’ measures, minimizing monetary costs. Based on our efficiency and removed time parameters. For example, results, as well as the social and economic context of our survey method (searches by car) allows the record the study region, we consider that mitigation measures of many reptile road-kills, but due to the car speed should focus on changing driver behavior, involving (~ 40 km/h) it may overlook some animals, specially educational plans to increase public awareness and to small-sized reptiles, which have very low detection rate promote a change in the behaviour of drivers to benefit resulting in bias (see Teixeira et al., 2013a). Similarly, wildlife conservation. This represents a hard work searching at shorter time intervals (e.g., once per week) because of the bad reputation that reptiles, specially allows for the record of animals that are usually not snakes, have in Colombian people. Alternatively, recorded because they quickly disappear (e.g., removal measures involving speed bumps and road wildlife by scavengers, complete obliteration by vehicle signals, especially on the road-kill hotspots identified, actions). In addition, roadside mowing and injuries would alert drivers about the presence of animals and that result in delayed mortality may also bias to lower encourage them to reduce speed and/or be more alert. estimates. Nevertheless, the survey method used in this In Colombia, the implementation of roadway mitigation study permits the inspection of a great road extension measures is becoming increasingly common, but studies in a short amount of time maximizing the available that rigorously evaluate the sites for implementation of resources, and results are comparable to other road-kill mitigation measures as well as their effectiveness, are Reptile road mortality in a fragmented landscape in Colombia 89 absent. In this sense, successful management efforts to linking individual-based and sample-based rarefaction, mitigate vehicle-wildlife collisions should include data extrapolation and comparison of assemblages. Journal of Plant of the locations of road-kill hotspots, landscape patterns, Ecology 5: 3-21. De la Ossa Nadjar, O., de la Ossa-V.J. (2013): Fauna silvestre wildlife movement patterns, and animal distribution, atropellada en dos vías principales que rodean los Montes density, behavior, and ecology. de María, Sucre, Colombia. Revista Colombiana de Ciencia Animal 5: 158-164. Acknowledgements. We thank Asociación Colombia Endémica De la Ossa-Nadjar, D., De La Ossa-V.J. (2015): Vehicle collisions for their support in completing this study, as part of the project with wild fauna on the two roads that pass through the Montes “Atropellamiento vehicular de mamíferos silvestres en el de María, Sucre, Colombia. Revista UDCA Actualidad & Magdalena Medio Santandereano, Colombia”. We also thank Divulgación Científica 18: 503-511. Diana Cardona and Mauricio Guzmán for their help during road- De la Ossa-V.J., Galván-Guevara, S. (2015): Registro de kill surveys and Mauricio Torres for comments and suggestions mortalidad de fauna silvestre por colisión vehicular en la on the manuscript. 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Accepted by Ariel Rodríguez