Living Safely: Low Road Mortality in Squamates near Burgas, Bulgaria

Abstract

The study represents the results of a long-term (2016 to 2021) survey on the herpetofauna inhabiting the vicinity of a heavily loaded section of the road E 87. The investigated road splits a Protected site from the net NATURA 2000 BG0000271 “Mandra-Poda”. The Protected site is known for its high biodiversity and its dense populations of vertebrates, which thrive in the area. Directly near the inspected road and on the pavement, we were able to detect five species of snakes, three species of turtles and two species of lizards. Among the squamates, rare observations were made of the European nose-horned viper (Vipera ammodytes), detected twice, and the European glass lizard (Pseudopus apodus), detected three times. Three other species—the Bloched snake (Elaphe sauromates), the Caspian whipsnake (Dolichophis caspius) and the Rhodos green lizard (Lacerta dyplochondrodes)—were found in larger numbers during some of the field surveys and here we provide information concerning the hot moments of their activity in the vicinity of the road. The Grass snakes (Natrix natrix) and the Dice snakes (N. tessellata) formed dense groups in the direct vicinity (closer than one and half meters) of the investigated road section. Despite the high number of recorded snakes and lizards, only isolated cases of vehicle collisions were observed. We suggest that the local squamate population had developed a complex of ethological specifics related to feeding, basking, shading, and copulation, which helped them to benefit from the road and avoid the risks related to the heavy traffic.

1. Introduction

Roads, as a key element of urbanisation, provide connectivity between areas, but also cause direct harm to wildlife through habitat destruction and mortality during construction or collisions with vehicles when operational [1]. The effect of the transportation of goods and people has been recognised for centuries as a factor influencing land use and the environment [2]. With the development of paved road networks and the increases in vehicle numbers, the first investigations of the impact of traffic on wildlife were conducted [3,4,5,6]. These early reports were focused on herpetofauna mortality (with the exception of [7], which also included birds and mammals) and this was not a coincidence. Ectothermic tetrapods were recognised as among the most vulnerable groups of animals in wildlife–vehicle conflicts [2,8,9].

A holistic understanding of the complex and multifactorial interactions between road traffic and vertebrate populations can be achieved using large databases collected during long-term monitoring programs [10]. Models based on large amounts of field data possess high prognostic potential (see [11,12,13,14,15]). The impact of roads (and mitigation measures) on herpetofauna is often unpredictable and sometimes produces surprising outcomes, such as the extreme efficiency of simple mitigation measures [16], the effects of new road infrastructure [17], and the influence of locomotor performance on species-specific mortality rates [18].

In the present study, we report on the specific behaviour of the squamates inhabiting the vicinity of a road section with intense traffic near Burgas city (SE Bulgaria). The road section is the main road connection to the numerous costal resorts south of the city. In the present study, we report our data concerning the presence and mortality of the target species on the road. We compare our data concerning the use of the road and the road vicinity of the lizards and snakes to those previously published for turtles [19], and discuss the ethological characteristics of the local reptiles.

2. Materials and Methods

The object of this 6-year monitoring was a section of the road E 87, which connects the southern industrial zone of Burgas to the neighbourhood district of Kraymorie. The monitoring was performed by pairs of experts on a strict transect along the cycle alley beside the traffic lanes. The track crossed a channel connecting the Black Sea and the Mandra lake. Each transect started at the entrance of the “Poda” Nature Conservation Centre, and took a course north toward the industrial zone. After about 4.8 km the route was walked in the opposite direction. Both experts walked slowly in an attempt to avoid overlooking any objects. We chose only days with sunny weather and light to moderate wind. We always started the transects in the afternoon and worked for about 4–6 h. The investigated road section splits a freshwater habitat densely covered with reeds and other aquatic plants. The road is built over two large artificially constructed water reservoirs, which served as industrial sedimentary containers in the past. The reservoirs were in use until the late sixties and afterwards were filled with fresh water. The water basins which formed the aquatic habitat besides the road were positioned about 100 m from the Black Sea coast. The habitat is known for its richness of vertebrate species, some of which form dense populations [19]. The direct vicinity of the road section that was investigated is included in the NATURA 2000 Protected site BG0000271 “Mnadra-Poda”. More details about habitat specifics, timing, locations, and general procedures were described in [19].

In the present study we included one additional category—“cut”, referring to snakes killed by grass trimmers during roadside maintenance. For each observation, we documented the type of displayed behaviour. We collected data on the presence of the specimens, on injured or killed squamates, and on shed skin fragments in the road vicinity. All objects were photographed and the position in which they were found was registered by the use of the “Garmin Etrex 30” GPS system (Garmin International Inc., Olathe, KS, USA). Very often we recorded in the same position more than one object, as sometimes they were very close to each other (within the accuracy interval of the GPS system we used). We used datum WGS84 UTM35N.

The attached species maps were prepared using the ArcGIS Pro 10.8.2 software. We used an orthophoto map for the base, digital layers in ESRI *.shp format and the WGS84 UTM35N coordinate system. In the production of each map, the following products were created: a linear layer of the surveyed route and five point layers (one for each surveyed species) from the collected field data, containing coordinate points of the exact locations where the objects were observed. The specific visualisation was performed by using points to indicate dead individuals (Single symbol—points) and a heat map (Heat map) to indicate the density of the detected live specimens.

Skin sheds were examined and the species identification was based on [20]. All fieldworkers were trained to identify local squamates species using the same literature source.

Carcasses of dead animals were photographed in situ and their persistence was monitored during subsequent surveys. Freshly killed animals were recorded as new mortalities, whereas old remains were re-documented when still present. The interest of the local predators on the corpses on and near the road was minimal.

3. Results

During our field surveys we produced 1363 original scripts on squamates in the GPS database (Figure 1 and Figure 2). The European nose-horned viper (Vipera ammodytes and the European glass lizard (Pseudopus apodus) were detected only sporadically. One female V. ammodytes was found in May of 2018 and one male in June of 2019. Three legless lizards were detected in two consecutive days in May of 2018.

The blotched snake (Elaphe sauromates) was detected every year of the field surveys with single specimens documented in the spring and the early summer (see

Table 1. Data on the detected specimens of E. sauromates.

Year	March		April		May		June		July		August		September		October		Total
	Dead	Alive	Dead	Alive	Dead	Alive	Dead	Alive	Dead	Alive	Dead	Alive	Dead	Alive	Dead	Alive
2016					1			2									3
2017						1		2									3
2018				2		3		1									6
2019				1				2									3
2020						2		5									7
2021				2		3											5
Total	0		5		10		12		0		0		0		0		27

, Figure 3). A single dead specimen of the blotched snake was detected at the beginning of the survey. No other victims were found for the whole duration of the study. All specimens were detected basking and resting directly on the pavement of the road.

The Caspian whipsnake (Dolichophis caspius) was detected every year from April to September (

Table 2. Data on the detected specimens of D. caspius.

Year	March		April		May		June		July		August		September		October		Total
	Dead	Alive	Dead	Alive	Dead	Alive	Dead	Alive	Dead	Alive	Dead	Alive	Dead	Alive	Dead	Alive
2016								2						1			3
2017						1						3					4
2018				4	2	4	2										12
2019								1									1
2020						3		2		1							6
2021				1													1
Total	0		5		10		7		1		3		1		0		27

, Figure 4). In our survey, we found two female specimens, which had been run over at the road in May 2018. Another two adult specimens were detected dead on the road in June of the same year—one female was found hit by a bicycle and one female was presumably initially cut by trimmer and afterwards ran over by a bicycle.

The Grass snakes (Natrix natrix) were detected very often from March to October during our research (see

Table 3. Data on the detected specimens of N. natrix.

Year	March		April		May		June		July		August		September		October		Total
	Dead	Alive	Dead	Alive	Dead	Alive	Dead	Alive	Dead	Alive	Dead	Alive	Dead	Alive	Dead	Alive
2016							3	6						1		1	11
2017		6			1	54		15		8		26				5	115
2018				18	2	90	1	13		3							127
2019		9	2	39				53		14							117
2020					4	29	6	35	1	5							80
2021				18		9											27
Total	15		77		189		132		31		26		1		6		477

, Figure 5). We were able to register 458 live specimens and 19 dead, from which 4 were killed by bicyclists and 5 were found cut down during road maintenance in June 2020. In the vicinity of the road, we detected three copulations.

A total of 750 live Dice snakes (Natrix tessellata) were detected in the five years of monitoring (Figure 6,

Table 4. Data on the detected specimens of N. tessellata.

Year	March		April		May		June		July		August		September		October		Total
	Dead	Alive	Dead	Alive	Dead	Alive	Dead	Alive	Dead	Alive	Dead	Alive	Dead	Alive	Dead	Alive
2016							2	1					3	2			8
2017		10				16		18	1	3		38				3	89
2018				21	7	151	12	58		3							252
2019		1	2	59			3	71	2	39							177
2020					11	55	12	81	1	12							172
2021				30	2	20											52
Total	11		112		262		258		61		38		5		3		750

). Like the Grass snakes, the Dice snakes were active from the early spring until the autumn (Table 4). In total, 10 specimens of N. tessellata were found run over by bicyclists, 9 were found cut by trimmers in June 2020, and a total of 39 were found killed by motor vehicles on the road. The Dice snakes were detected copulating near the road on two occasions (Figure 7).

The Rhodos green lizard (Lacerta diplochondrodes) was detected predominantly in the southeast and the northern section of the transect (Figure 8). A total of 83 adult specimens were detected from March to September (

Table 5. Data on the detected specimens of L. diplochondrodes.

Year	March		April		May		June		July		August		September		October		Total
	Dead	Alive	Dead	Alive	Dead	Alive	Dead	Alive	Dead	Alive	Dead	Alive	Dead	Alive	Dead	Alive
2016								1									1
2017		2			1	3		2									8
2018				4		10	1	4		1				2			22
2019		3		7				11		1							22
2020						3	1	12		5							21
2021				4		5											9
Total	5		15		22		32		7		0		2		0		83

). In total, one adult male was detected hit by a car on the road in May 2017 and two more specimens were detected dead -one in June of 2018 and one in the same month in 2020. One copulation was observed on 24 May 2017 at the pavement edge.

Two skin sheds of Caspian whipsnakes, one shed of blotched snake and a total of eighteen skins of Natricide snakes were documented in the road vicinity. One fully melanistic specimen of the Dice snake was recorded in June 2019.

4. Discussion

Modern road ecology recognises five mechanisms of direct wildlife–infrastructure interactions: car avoidance, noise avoidance, road surface avoidance, road attraction and wildlife–vehicle collisions [9,21]. In general, increasing traffic density correlates with a higher number of collisions [22]. However, the road attraction effect (based on increased resource availability [23,24], nesting areas [25] or thermoregulation in snakes [26]) and the shoulder effect of the road can be highly positive—lower traffic may increase the number of collisions [13,21].

Our data indicated that local squamate populations have developed ethological adaptations that allowed them to inhabit the immediate road verge and benefit from its advantages (like the lack of predators, higher temperature of the substrate, and others), while avoiding the pavement itself. This is an interesting behavioural adaptation, which may be specific to the squamates living along the particular road section we investigated. The population of local European pond turtles suffers severe damage due to the busy traffic, especially in the late spring and the early summer [19]. According to our results, the local snakes and lizards were run over rather seldomly despite their presence at the very edge of the road in the spring and in the summer. This is partially in line with the results reported by [13], however, in our study the peak was in spring and the “September mortality” was absent due to the specific hydrological conditions in the vicinity of the road section south of Burgas [19]. The percentage of motor traffic victims in all investigated squamate species was very low, even in the Caspian whipsnake. This species was known to be often included in WVC [18,20]. In the present study, the situation was rather specific as only one of the killed snakes was actually a typical case of “hit on the road by motor vehicle”. Of the others, one of the dead D. caspius was hit by a bicycle, another one was cut by a trimmer, and one (Figure 9) was a victim of an intentional motor vehicle–wildlife collision [27]. In the video sequence (Supplementary Materials; https://youtu.be/8UDKXjROlD8), it can be noticed that the drivers avoided the inner line of the right curve, where the snake was hit. The natural driving trajectory was towards the middle line of the road. In fact, the driver of the vehicle that hit the snake had probably intentionally changed his trajectory to kill the animal.

Our data on the investigated section of road E 87 indicated the low impact of the busy traffic on the local population of lizards and snakes. The mitigation measures, which are normally planned and realised at road infrastructure, may not be suitable for this particular road section. The constructions for prevention of WVC were normally designed in accordance with the ethology of the species which were the object of protection. Wild mammals travel along the path of least resistance [28,29]. Many researchers have suggested that the use of wildlife underpasses or drainage culverts becomes a learned behaviour [30,31,32]. Research has demonstrated that wildlife overpasses and underpasses, in combination with fencing, have significantly reduced WVCs and have enabled large vertebrates [30,33,34,35], and amphibians and reptiles [35,36,37], to cross roads safely. As the local squamate populations have developed ethological mechanisms to use the road vicinity with a lower risk of harm, the construction of protective screens like those constructed on Lot 4 of the Bulgarian “Struma” motorway (high and smooth walls) is redundant. Such constructions can even be dangerous for road safety as they reduce visibility and may cause a “corralling effect” for animals onto the road pavement [38]. The construction of mitigation measures at the road section of E87 that we investigated had to be designed predominantly to protect the local European pond turtles (see [19]). Buried fencing dramatically increased the effectiveness of the prevention of wild animals ingressing onto the road [39,40,41]. In many countries, special structures for preventing the access of turtles onto the road were built and these constructions vary in their design [42,43]. Most of the devices are built similarly to those used for the protection of turtles (e.g., Gopher tortoises and Alabama Red-Bellied Turtles, Pseudemys alabamensis) in the USA [42]. Fencing by the use of nets has proven a highly suitable tool for reducing road mortality in turtles (for an overview, see [25,42,43]).

To better protect the squamate population inhabiting the vicinity of the investigated road section, a simple and cheap measure can be realized. Our data indicated the increased mortality of snakes immediately after road maintenance works, which include grass removal. This was normally performed two times per year—once in June and once in August. As there was a decrease in the number of squamates inhabiting the road vicinity after July, the authorities should concentrate on improving the organisation of the June grass trimming. We propose the trimming should be accomplished in the dark hours, or, in case this is not safe for the workers, a specially trained person should have to accompany the trimmer teams at several meters and scare the squamates away from the gear. This will contribute to diminishing the number of destroyed specimens, especially at the younger ontogenetic stages (Figure 10).

5. Conclusions

Our results indicated that the decision-making concerning the implementation of measures for mitigation of the impact of roads on squamate populations should be based on long-term on-spot monitoring. In the case of this study, besides the threat of direct collision with motor vehicles, the ectothermic vertebrates living around the investigated road section were endangered by additional factors, such as grass trimming and bicyclists. The adequate management of road maintenance activities and information campaigns against the intentional killing of squamates will result in securing a safer environment for the lizards and, especially, the local snakes.