Journal of Ecology and Environment

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Published online July 18, 2022
https://doi.org/10.5141/jee.22.035

Journal of Ecology and Environment (2022) 46:18

© The Ecological Society of Korea.

A field evaluation of two external transmitter attachment methods for small snakes

Il-Kook Park , Hojun Jeong and Daesik Park *

Division of Science Education, Kangwon National University, Chuncheon 24341, Korea

Correspondence to:Daesik Park
E-mail parkda@kangwon.ac.kr

Received: May 2, 2022; Revised: July 5, 2022; Accepted: July 5, 2022

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Background: Radio-telemetry is a useful method to investigate the spatial ecology of species in the wild, by tracking the signal of a transmitter attached to an individual. The method of attaching a transmitter to a snake is representatively divided into surgical implantation, and external attachment, which latter is often used in small snake species.
Results: In this study, we evaluated and compared the utility of two external attachment methods, the nylon thread method and the tape method, applied to a small grassland snake species of approximately 50 cm snout–vent length, the Slender racer (Orientocoluber spinalis), on an island in the Republic of Korea. The nylon thread method and the tape method were applied to four and five individuals, and radio-tracked for an average of eight and eleven days, respectively. The nylon thread method caused individual injury and disturbed their movement, while using the tape method, the transmitter package sometimes dropped off, but no injury or movement problems occurred.
Conclusions: Considering that poor understanding of how to attach the transmitter makes it difficult to investigate the spatial ecology of small snake species, the tape method, evaluated in this study, could be applied to attach a transmitter and to study spatial ecology of such snakes.

Keywords: nylon thread method, Orientocoluber spinalis, radio-telemetry, tape method

The secret lifestyle of wild animals is effective at foraging prey and protecting them from predators, but it also makes them difficult to observe in the field. These characteristics limit the investigation of the lifecycles and ecology of wild animals, specifically snakes (Gerald et al. 2006). Radio-telemetry is a highly effective method to investigate the spatial ecology of animals in the wild (Balmori 2016; Bergman 2005). Radio-telemetry generally requires direct capture of individuals and attaching the transmitter to the individuals. Also, before attaching the transmitter to the individual, various considerations must be made, such as the attachment method of the transmitter, the body size of the snakes, and the tracking period to achieve the study goal.

The transmitter attachment method to snakes is largely divided into surgical implantation and external attachment. Surgical implantation, which has been applied to various snake species (Gerald 2006; Kim et al. 2012a; Lee et al. 2011; Lee and Park 2011; Mohammadi et al. 2014; Webb and Shine 1998), is a method of inserting the transmitter into the subcutaneous layer or the abdominal cavity of an individual, and if necessary, fixing the transmitter to the ribs (Reinert and David 1982; Weatherhead and Anderka 1984). Implantation of the transmitter into the abdominal cavity causes the fewest side effects caused by the transmitter for radio-tracking snakes, and its strong fixation makes stable long-term study possible. However, veterinary surgery is required for operation, anesthesia, abdominal cavity incision, and suture. This method also needs about a two-week recovery period after the surgery, often resulting in the death of the individual from various infections (Lee and Park 2011; Lentini et al. 2011; Shine and Lambeck 1985; Smith et al. 1988). Subcutaneous implantation is relatively simple since only the skin incision and suture are necessary to insert the transmitter under the skin (Újvári and Korsós 2000). However, the protrusion of the transmitter insertion site may interfere with the snake movement by contact with external objects, and break the suture (Újvári and Korsós 2000; Weatherhead and Anderka 1984). Therefore, the surgical implantation method is often not applicable to small-sized snake species (Anderson and Talcott 2006; Madrid-Sotelo and García-Aguayo 2008; Wylie et al. 2011).

If the body size of the species is too small to apply surgical implantation, or surgery is not affordable, the external attachment method can be adopted. This method is a much more non-invasive method than surgical implantation and is a convenient technique to replace or remove the transmitter from the individual (Wylie et al. 2011). Typical external attachment methods to snakes include the nylon thread method (Ciofi and Chelazzi 1991), tape method (Wylie et al. 2011), and glue attachment method (Riley et al. 2017), although the transmitter can often be attached with a harness for lizards, which have legs (Kim et al. 2012b; Park et al. 2019). The nylon thread method fixes the transmitter by inserting a nylon thread that is connected to the transmitter into the tail of a snake (Ciofi and Chelazzi 1991). The nylon thread method has been applied to various snake species (Wolfe et al. 2018; Scali et al. 2008), but the suitability for slender-bodied small snakes has not been verified. The tape method uses tape to fix a transmitter to the body parts of an individual and is easy to apply without surgery (Madrid-Sotelo and García-Aguayo 2008; Tozetti and Martins 2007; Wylie et al. 2011). But in the tape method, transmitters often detach, particularly during the long-term study (Tozetti and Martins 2007; Wylie et al. 2011). The glue attachment method attaches the transmitter to the dorsum of a snake using super glue, and can be applied restrictively to species that have low activity and do not use crevices as shelters (Cobb et al. 2005; Riley et al. 2017). If a suitable method of external transmitter attachment is selected based on a species’ ecological characteristics, it could provide diverse ecological information, such as habitat preference, daily movement patterns, and temporary range expansion (Harris et al. 1990).

In this study, we evaluate two transmitter attachment methods of the nylon thread method and the tape method to externally attach a transmitter to small grassland snakes of the species, Slender racer (Orientocoluber spinalis), whose small body size is inapplicable for surgical internal implantation of the transmitter. We did not test the glue attachment method, considering the high mobility of O. spinalis in grasslands.

Orientocoluber spinalis, which has approximately 50 cm of snout-vent length (SVL) and 40 g of body weight, is reported to prey on small rodents, lizards, and juvenile snakes (Kharin 2011; Kim and Han 2009; Park et al. 2021; Won 1971). This snake species is distributed in the Korean Peninsula, China, Russia, Mongolia, and Kazakhstan (Kharin and Akulenko 2008), and mainly inhabits grassland and shrublands (Shannon 1956). We radio-tracked O. spinalis on Oeyeon Island (N 36.22°, E 126.08°) with an area of 2.18 km2 in Boryeong, Republic of Korea. The land cover of Oeyeon Island is composed of forest (70.2%), bareland (12.0%), grassland (10.2%), residential area (6.4%), and cropland (1.2%) (https://egis.me.go.kr/main.do). There are three small mountains on the island, and 3 m wide stone-tiled trails run along the coast and head to the mountaintop.

We captured O. spinalis for radio-telemetry around the trail and transported the snakes to the field research station to attach the transmitter. Before transmitter attachment, we measured each individual’s SVL in units of 1 mm and body weight (BW) in units of 0.01 g using an electronic scale (MH-200; Changxie, Dongguan, China). Also, we made two small cuts on ventral scales between the 2nd and 14th scales (Brown and Parker 1976) and confirmed its sex by cloacal probing (Blanchard and Finster 1933). We determined the transmitter package weight by measuring the weight difference before and after the transmitter attachment, and also calculated the proportion of the package to BW. We ensured that the transmitter package weight was less than 5% of the BW (Baxley and Qualls 2009; Hardy and Greene 1999; Miller et al. 2012). We used PicoPip AG376 (Biotrack, Wareham, UK; 150 MHz, 0.56 g, body dimension of 17 mm × 8 mm × 5 mm, whip antenna length of 175 mm, battery life of 75 days) as a transmitter, considering the BW of O. spinalis.

To attach transmitters, we used the nylon thread method and the tape method. To apply the nylon thread method, we connected two 0.33 mm nylon fishing threads (X-hard 4.0; Essen, Tokyo, Japan) to the holes in the front and rear parts of the transmitter, passed the threads through near the 23rd ventral scales on the tail from the cloaca using the suture needle, and tied threads to the transmitter (Ciofi and Chelazzi 1991). Because the needle and thread can cause potential damage to internal visceral organs and blood vessels when fixing the transmitter to the body, we attached the transmitter to the tail to exclude such risks. After attaching the transmitter, we applied small amounts of epoxy on the front of the transmitter, making the part streamlined in shape so that herbs and branches would not disturb the individual movement, as far as was possible (Fig. 1). Because the antenna of the transmitter was very flexible, we did not fix it on the body, so as not to interfere with the snake’s movement. Since a thin and sharp nylon thread may scratch the skin, Ciofi and Chelazzi (1991) encased the nylon thread, first, in a rubber tube of which an external diameter is around 1 mm when applying to a large snake, Hierophis viridiflavus (total length 110 cm, BW 300 g). Because the tail of O. spinalis is too slender to insert a rubber tube, we did not encase the nylon thread in a rubber tube.

Figure 1. Radio-transmitters externally attached to Orientocoluber spinalis applying (A) the nylon thread method, and (B) the tape method. The transmitter was fixed on the dorsal side of the tail with nylon thread and epoxy. Two arrows indicate the points where the transmitter was tied with nylon thread (A). The transmitter was placed on the ventral side and fixed with beige duct tape (B).

In the tape method, a transmitter-attached tape is wrapped around the body part of the snake (Wylie et al. 2011). First, we attached the transmitter to 3 cm wide beige duct tape (Task and More Inc., Gyeryong, Korea), which could completely wrap the 1.7 cm long transmitter. Next, the transmitter was fixed once again by covering it with double-sided tape (Woolim-tape, Seongnam, Korea), which tightly attached the transmitter to the duct tape, and also affixed the tape tightly to the snake body. We placed the transmitter at the ventral side of 2/3 SVL from the head, and fixed it by wrapping the body in 1.5 turns of duct tape. We wrapped the tape a little tight, so that the transmitter was slightly pushed into the abdominal cavity side, and did not protrude too much from the snake’s body. This ventral placement procedure of the transmitter could help to prevent snakes from snagging off the package when passing through various obstacles (Wylie et al. 2011). Lastly, we applied super glue (Super glue 412; Amos, Seoul, Korea) to the outermost edge part of the tape to prevent accidental tape detachment (Fig. 1). In this method, we also did not fix the antenna of the transmitter.

After confirming that the transmitter did not disturb O. spinalis movement, and was attached stably in a breed box (15 cm × 24 cm × 17 cm) for over four hours, we released individuals to the point of capture after 5 PM on the day of capture. We tracked individuals with the nylon thread method in the summer, from 13 July 2021 to 9 August, and individuals with the tape method in the autumn, from 2 September to 14 October. We terminated the radio-telemetry study in early August, because the air temperature was too high for O. spinalis to be active, and in early October because the air temperature dropped. We tracked the snakes once in the morning between 8 AM and 12 PM, and once in the afternoon between 4:30 PM and 7 PM, respectively, using a tracking receiver (Biotracker VHF Receiver; Lotek Wireless, Inc., Newmarket, ON, Canada) and Yagi antenna (Wildlife Materials Inc., Murphysboro, IL, USA). We recorded tracking location data with a GPS device (eTrex Vista Cx; Garmin International Inc., Olathe, KS, USA). We defined it as moving only when the signal location moved over 0.5 m if the direct observation was not possible, considering the size of the snake. We considered the status of the tracked O. spinalis into five categories. 1) Injury: when we observed severe injury on the body due to the attached transmitter package, and ended its tracking. 2) Transmitter detachment: when we observed a snake whose transmitter was removed, or when the signal did not move over seven days under the rocks, or in a rock crevice. For the latter case, in the tape method, we considered the case a transmitter detachment, but 3) in the nylon thread method, as a snake dead. 4) Signal loss: when the transmitter signal could not be followed, possibly due to transmitter failure. 5) Case complete: when we successfully tracked a snake over 15 days, considering the battery life of the transmitter. To compare the moved distance of O. spinalis according to the two methods, we calculated the daily moved distance of individuals as the shortest straight distance between sequential tracked points in the morning. We calculated the moved distance of each individual based on relocation data using QGIS v. 3. 4. 7. (QGIS 2021).

We conducted Mann–Whitney U-test to verify the difference in individual size, transmitter package weight, the proportion of transmitter package to body weight between the two attachment methods, and the mean daily moved distance. All numerical data are presented as mean ± 1 standard error unless otherwise noted.

During the study, we radio-tracked total nine O. spinalis individuals. Applying the nylon thread method, we tracked four individuals (two females and two males; OS01−OS04), of which mean SVL was 51.4 ± 2.1 cm and BW was 32.0 ± 1.0 g. The transmitter package weight was 0.86 ± 0.07 g, and its ratio to BW was 2.7 ± 0.3%. In case of the tape method, we tracked five individuals (one female and four males; OS05–OS09), of which mean SVL was 51.2 ± 1.0 cm and BW was 40.8 ± 4.1 g. The weight of the transmitter package was 1.28 ± 0.05 g, and the ratio to BW was 3.3 ± 0.4% (Table 1). Whereas the SVL of snakes was not different between the two methods (p = 0.905), the BW was heavier in the tape method (z = 2.21, p = 0.032). Although the transmitter package was heavier in the tape method (z = 2.46, p = 0.016), the ratio of the transmitter package to body weight was not different between the two methods (p = 0.291). Also, the mean daily moved distance between the two methods was not significantly different (p = 0.730).

Table 1 . Comparison of the tracked Orientocoluber spinalis harboring the transmitters, which applied either the thread method or tape method.

IDSexDays tracked (relocations)SVL (cm)BW (g)PW (g)PW/BW (%)Mean daily moved distance (m)Reason for ending
Thread method
OS01F3 (4)49.331.890.862.718.6 ± 20.1Dead
OS02F10 (12)55.432.000.882.873.0 ± 47.2Injury
OS03M15 (16)54.334.950.681.928.8 ± 49.4Completion
OS04M5 (5)46.629.071.023.54.6 ± 4.8Injury
9 ± 751.4 ± 4.231.98 ± 2.400.86 ± 0.142.7 ± 0.731.3 ± 29.5
Tape method
OS05M7 (9)50.735.461.313.74.1 ± 2.3Signal loss
OS06M7 (15)49.833.951.374.030.2 ± 44.5Transmitter detachment
OS07M11 (19)54.856.781.091.916.0 ± 38.9Transmitter detachment
OS08M15 (28)51.340.431.33.239.6 ± 50.5Completion
OS09F15 (26)49.437.391.313.511.3 ± 17.5Completion
16 ± 952.6 ± 2.141.24 ± 7.301.26 ± 0.143.1 ± 0.620.2 ± 14.4

Values are presented as mean ± standard deviation.

SVL, snout-vent length; BW, body weight; PW, package weight.



Nylon thread method

We tracked the snakes applying the nylon thread method for 8.3 ± 5.4 standard deviation (SD) days (range: 3−15) over 9.3 ± 5.7 SD relocations (range: 4−16). They daily moved 31.3 ± 14.8 m (range: 4.6−73.0). The signal of OS01 was stuck for more than seven days under the rock from three days after its release. So, we considered OS01 dead and ended the tracking trial. We observed OS02 to be severely injured on the tail where the transmitter was attached, so ended its tracking (Fig. 2). OS03 was successfully tracked for more than 15 days, and the case was considered complete. We found OS04, which was stuck in a rock crevice due to the transmitter package, on the fourth day of its release. We rescued it and ended its tracking (Fig. 2). After removing transmitters and applying anti-virus ointment (Madecassol Powder, Dongkook Pharmaceutical, Seoul, Korea) to the wound area, we released OS02 and OS04 into the wild.

Figure 2. (A) Injured, and (B) stuck Orientocoluber spinalis by applied nylon thread to attach transmitter on the tail. Tied nylon thread caused the severe injury (OS02; A), and the transmitter package was stuck between rock crevices, resulting in the individual being immobile (OS04; B).

Tape method

Individuals applying the tape method were tracked for 11.0 ± 4.0 SD days (range: 7−15) over 19.4 ± 7.8 SD relocations (range: 9−28). The snake daily moved 20.2 ± 6.5 m (range: 4.1−39.6). We lost the signal of OS05 six days after release and considered it as signal loss. The signals of OS06 and OS07 did not move under the rock from five and three days after their release, respectively, so we considered them as cases of transmitter detachment. Later, we found OS07, of which the transmitter package was detached 6 days after ending our tracking trial. OS08 and OS09 were successfully radio-tracked for more than 15 days and were considered complete cases.

In the results, the nylon thread method had the advantages that the transmitter package was light, and was attached tightly. However, this technique is not suitable for snake species that use narrow rock crevices as shelters or corridors, because the transmitter package disturbed the movement of snakes, and makes them get stuck between crevices such as the case of the OS04. Also, the front part of the attached transmitter might be stuck with grasses or obstacles while the snakes move forward. Backward forces pull the package and the nylon thread toward the tip of the tail. As a result, the nylon thread, which is strongly pulling backward, may have been responsible for the injury of OS02. Although the epoxy was applied to the front part of the package in a streamlined shape to reduce the backward force, this was not effective enough to prevent such injury. As in previous studies (Ciofi and Chelazzi 1991), wrapping the nylon thread in a rubber tube might help to prevent from such injuries to some extent, but the tail of O. spinalis is too slender to insert a rubber tube. The species successfully applied with the nylon thread method using a rubber tube were mostly large-sized snakes, such as Hierophis viridiflavus (Ciofi and Chelazzi 1991; Scali et al. 2008), Pseudonaja affinis (Wolfe et al. 2018), Sistrurus catenatus, and Pantherophis guttatus (Riley et al. 2017), whose body size were bigger than O. spinalis, as the total length was over 100 cm, and the BW was over 100 g. Even if inserting the rubber tube is applicable, it is questionable as to whether it limits the activities of O. spinalis, which mainly moves through grasses in the grassland, and uses narrow rock crevices as shelters. Based on the cases of OS01 and OS04, whose signal was located under the rock without moving, snakes also might have died due to the transmitter package being stuck between rock crevices. According to our results, the nylon thread method disturbs the movement of O. spinalis and often causes severe injuries. Therefore, this method should not be used for small grassland snakes like O. spinalis.

In previous studies, the tape method of transmitter attachment was applied to Thamnophis gigas (Wylie et al. 2011) and Crotalus durissus (Tozetti and Martins 2007), whose body sizes were bigger than O. spinalis at 1 m in total length and 250 g of BW. Our study shows that the tape method can be applicable to attaching the transmitter to small snake species. We did not find any individuals who were injured or stuck in rock crevices. This is supposed that not only the transmitter attachment method but also the transmitter placement procedure resulted in such positive results. The transmitter attached to the ventral side did not protrude too much from the body trunk of the snake. So, it would have been easier to pass through a narrow area or crevices by shrinking the abdomen if necessary. In contrast, in nylon thread method, it would be difficult to move forward at same situations because a tail cannot shrink when caught the tail in a gap such as rock crevices. Also, the tracked snakes had moved more than a few hundred meters, showing they had no problem with long-distance movement. Although this method does not cause serious injuries to the snake or significantly disturb movement, the attachment duration of the transmitter is relatively varied. The transmitter-attached duration using tape varied 14.3 days (range: 0−88) in T. gigas (Wylie et al. 2011), 69.2 days (range: 1−195) in C. durissus (Tozetti and Martins 2007), and 48.3 ± 18.2 days in Oxybelis aeneus (Madrid-Sotelo and García-Aguayo 2008). The attachment duration of the tape method might depend on the degree of tape wrapping, the wrapping strength, precipitation during the study period, and the habitat types (Riley et al. 2017). Additional studies on the appropriate handling of the diverse situation considering the aforementioned variables could provide more stable application techniques of the tape method for small grassland snakes.

Poor understanding of how to attach the transmitter makes it difficult to investigate the spatial ecology of small snake species. For this reason, the study of several Korean snakes, including the endangered Chinese many-tooth snake (Sibynophis chinensis) and the Japanese Keelback (Hebius vibakari), is still insufficient. Our study suggests that although additional research is needed, the tape method of transmitter attachment can apply to small snake species.

IKP did conceptualization, data curation, formal analysis, investigation, writing-original draft, and writing-review and editing. HJ did data curation, investigation, and writing-review and editing. DP did conceptualization, funding acquisition, supervision, writing-original draft, and writing-review and editing.

This research was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF), funded by the Ministry of Education (No. 2020R1I1A3051885).

This research was conducted within the guidelines and approval of the Institutional Animal Care and Use Committee of Kangwon National University (KW-200707-3).

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Journal of Ecology and Environment

pISSN 2287-8327 eISSN 2288-1220