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Radiotelemetry is a widely used and informative tool in studies of animal ecology, behavior, and conservation. Over the past 50 years, many different methods have been used to outfit animals with radiotransmitters. Radiotelemetry studies on snakes typically require anesthesia and surgery to internally implant transmitters; however, internal implantation methods can increase snake mortality and infection rates, and may alter natural behaviors, thereby reducing data validity. We qualitatively compared 3 methods of external transmitter attachment (i.e., glue-only, tape-and-glue, and a subdermal stitch), and compared their utility for collection of spatial data from April to November 2012 and 2013 at Magnetawan First Nation near Britt, Ontario, Canada. Transmitters attached with glue-only and tape-and-glue methods fell off shortly after deployment because of environmental factors and snake shedding. Both methods also resulted in skin irritation and slightly impeded snake movements. Conversely, the subdermal stitch method was long lasting in both the field and lab, and did not cause significant skin irritation. Also, the subdermal stitch method did not affect movement or the rattlesnake's ability to rattle. Additional quantitative research is required to determine if the subdermal stitch method triggers immune responses, infections, or negatively affects snake fitness. Our results suggest that the subdermal stitch method may be a viable external attachment method for use in radiotelemetry of snakes.
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Tools and Technology
A Comparison of Three External Transmitter
Attachment Methods for Snakes
JULIA L. RILEY ,
1,2
Magnetawan First Nation, 10 Ontario-529, Britt, ON P0G 1A0, Canada
JAMES H. BAXTER-GILBERT,
2
Department of Biology, Laurentian University, 935 Ramsey Lake Road, Sudbury, ON P3E 2C6, Canada
JACQUELINE D. LITZGUS, Department of Biology, Laurentian University, 935 Ramsey Lake Road, Sudbury, ON P3E 2C6, Canada
ABSTRACT Radiotelemetry is a widely used and informative tool in studies of animal ecology, behavior, and
conservation. Over the past 50 years, many different methods have been used to outfit animals with
radiotransmitters. Radiotelemetry studies on snakes typically require anesthesia and surgery to internally
implant transmitters; however, internal implantation methods can increase snake mortality and infection
rates, and may alter natural behaviors, thereby reducing data validity. We qualitatively compared 3 methods
of external transmitter attachment (i.e., glue-only, tape-and-glue, and a subdermal stitch), and compared
their utility for collection of spatial data from April to November 2012 and 2013 at Magnetawan First Nation
near Britt, Ontario, Canada. Transmitters attached with glue-only and tape-and-glue methods fell off shortly
after deployment because of environmental factors and snake shedding. Both methods also resulted in skin
irritation and slightly impeded snake movements. Conversely, the subdermal stitch method was long lasting
in both the field and lab, and did not cause significant skin irritation. Also, the subdermal stitch method did
not affect movement or the rattlesnake’s ability to rattle. Additional quantitative research is required to
determine if the subdermal stitch method triggers immune responses, infections, or negatively affects snake
fitness. Our results suggest that the subdermal stitch method may be a viable external attachment method for
use in radiotelemetry of snakes. Ó2017 The Wildlife Society.
KEY WORDS conservation, Pantherophis guttatus, radiotagging, radiotelemetry, Sistrurus catenatus, wildlife
management.
Animals endeavor to move through and exist within their
environment undetected by prey or predators. Such stealthy
behavior, although useful for the animal, makes data
collection challenging for researchers. Radiotelemetry is a
widely used tool for gathering information about otherwise
hard-to-locate animals (Balmori 2015). Radiotelemetry
relies on external transmitter attachment (e.g., collars,
backpacks, and belts; Goodman et al. 2009, Price-Rees
and Shine 2011) or internal placement (e.g., ingestion of the
transmitter or surgical implantation; Fitch and Shirer 1971,
Landreth 1973, Reinert and Cundall 1982, Weatherhead
and Blouin-Demers 2004). External attachment is often
dependent on the presence of a distinctly shaped body (e.g.,
pronounced head, pectoral or pelvic girdle) to prevent the
transmitter package from sliding off. Thus, external
attachment methods have generally been avoided for snakes
and internal implantation is more common (Reinert and
Cundall 1982, Weatherhead and Blouin-Demers 2004).
Every research method has its trade-offs; snake radio-
transmitter attachment methods each have their own unique
ethical and logistical challenges. Ingestion of transmitters is
only a short-term method because of transmitter loss during
defecation and snake behavior may be altered by eliciting
postingestion activities such as decreased movement and
increased basking and sheltering (Brown and Parker 1976,
Henderson et al. 1976, Nickerson et al. 1978, Lutterschmidt
and Reinert 1990). Surgical implantation can be harmful or
lethal because of negative reactions to anesthesia, infections,
or inadequate healing (Anderson and Talcott 2006). In
addition, internal implantation has been associated with
moderate levels of snake mortality (11–28%; Rudolph et al.
1998), decreased growth rates, reduced clutch sizes
(Weatherhead and Blouin-Demers 2004), and infection
rates as high as 60% (Sperry et al. 2009, Lentini et al. 2011).
High infection rates in study animals call into question
validity of these data, because behavior of sick individuals
differs from that of healthy conspecifics (Mech and Barber
2002, Dixon 2011). Furthermore, surgical procedures can be
expensive and require additional handling and transportation
to bring snakes to a skilled veterinarian (Goodman et al.
2009). Potential negative effects of internal implantation
(increased mortality, increased research costs, etc.) have
driven researchers to devise alternative transmitter attach-
ment methods for snakes. These methods include taping
Received: 18 June 2016; Accepted: 5 December 2016
1
E-mail: julia.riley87@gmail.com
2
Present address: Department of Biological Sciences, Macquarie
University, Sydney, New South Wales 2109, Australia.
Wildlife Society Bulletin; DOI: 10.1002/wsb.748
Riley et al. External Transmitter Attachment for Snakes 1
(Tozetti and Martins 2007, Wylie et al. 2011), stitching
(Ciofi and Chelazzi 1991), and gluing transmitters externally
(Cobb et al. 2005, Figueroa 2006, Jellen and Kowalski 2007).
The effectiveness of external transmitter attachment
methods is largely unknown, likely because studies that
employ them are not focused on assessing their efficacy and
information on failed techniques may remain unpublished.
We tested 3 external radiotransmitter attachment methods
for snakes (glue-only, tape-and-glue, and a subdermal
stitch). Our qualitative comparison examined the utility of
each method for collection of spatial data, longevity of
attachment, and any potential negative impacts on snake
health or behavior. It was our goal to present both the
positive and negative aspects of each method to provide other
researchers with guidance for selecting a viable, alternative
option to internal transmitter placement.
STUDY SPECIES AND LOCATIONS
We examined external transmitter attachment methods
using 2 North American snake species: eastern massasauga
(Sistrurus catenatus) and corn snake (Pantherophis guttatus).
Fieldwork on eastern massasaugas (n¼23) occurred from
April to November 2012 and 2013 at Magnetawan First
Nation near Britt, Ontario, Canada (see Supporting
Information for site description). From January to April
2013, our pilot test of the subdermal stitch attachment
method was conducted on captive corn snakes at Scales
Nature Park, Orillia, Ontario (see Supporting Information
for captive housing details).
METHODS
Field Survey Methods
We conducted systematic road surveys (as described in
Baxter-Gilbert et al. 2015) and visual encounter surveys, in
available habitat, to locate eastern massasaugas for transmit-
ter attachment. We recorded capture locations with a
handheld global positioning system (GPS) unit. We also
recorded sex, tail length, total length, snout–vent length, and
mass and then individually marked each snake while we
restrained it in a clear plastic tube (for details see Supporting
Information). While the snake was restrained, we externally
attached a 1.2-g radiotransmitter (Model R1655; Advanced
Telemetry Systems, Isanti, MN, USA) using 1 of the 3
methods described below. All snakes included in our study
weighed 100 g to ensure the transmitter was never 1.2%
of a snake’s body mass. We held all rattlesnakes <24 hr, and
released individuals at their site of capture. Post-release, we
located each rattlesnake every 2–3 days and recorded its
location, behavior, any external injuries that may have
resulted from transmitter attachment, and status of the
transmitter attachment package itself (i.e., detachment,
presence of debris, etc.).
Field Test of the Glue-Only Attachment Method
From 5 to 28 May 2012, we attached transmitters to 8 snakes
using a combination of cyanoacrylate glue and colostomy
paste (Fig. 1; Fig. S1). We adapted this protocol from a
method used to radiotrack greater short-horned lizards
(Phrynosoma hernandesi; K. Fink, University of Alberta,
personal communication) and neonate timber rattlesnakes
(Crotalus horridus; Cobb et al. 2005, Howze et al. 2012). To
attach the radiotransmitter, we placed glue (Nailene Ultra
Quick Nail Glue Clear, Aliso Viejo, CA, USA) on the
underside of the transmitter, and then placed the transmitter
onto the snake’s skin two-thirds of the way along the body
immediately to the right-hand side of the spine (Fig. S1). We
placed the transmitter posterior to the widest part of the
snake’s body to ensure the transmitter attachment package
did not add to the maximum circumference of the snake.
After the glue had dried, we surrounded the transmitter
package with colostomy paste (Stomahesive Paste, Ref #
183910; Convatec, Greensboro, NC, USA), and streamlined
the package (Fig. S1). During radiotracking, if we noticed
the transmitter lifting off the skin, we captured the snake and
added more adhesive.
Field Test of the Tape-and-Glue Attachment Method
From 8 June to 7 September 2012, we attached transmitters
using both glue and tape to 19 eastern massasaugas (6 of
which were previously radiotracked using the glue-only
method; Fig. 1). Wylie et al. (2011) verified that tape worked
to externally attach transmitters to the semiaquatic giant
gartersnake (Thamnophis gigas). We coated the underside of
the transmitter with cyanoacrylate glue and placed it onto the
snake in the same position as described above. We then used
a 2.5-cm-wide piece of duct tape (Printed Duck Tape
1
Figure 1. Examples of the 3 external radiotransmitter attachment methods
for snakes: glue-only (top left), tape-and-glue (top right), and subdermal
stitch (bottom) using eastern massasaugas (Sistrurus catenatus; pictured) and
corn snakes (Pantherophis guttatus). This study occurred during 2012 and
2013 at Magnetawan First Nation near Britt, Ontario, Canada.
2 Wildlife Society Bulletin 9999()
Brand Duct Tape; Leopard, Avon, OH, USA) to encapsu-
late the transmitter and the snake’s body at the attachment
site (Tozetti and Martins 2007, Wylie et al. 2011; Fig. S2).
We varied the length of the duct tape with each snake, so that
the duct tape was not constrictive (Tozetti and Martins 2007,
Wylie et al. 2011). The duct-tape we used had a leopard-
print pattern, which was similar to the eastern massasauga
color pattern (Fig. 1).
During radiotracking, we noted any signs of shedding,
which would cause the transmitter package to be sloughed off
with the old layer of skin. If we saw signs of shedding (e.g.,
opaque eyes, whitening of the ventral scales), we collected the
snake and removed the transmitter. We gently peeled off the
transmitter, tape, and dead skin underneath the transmitter
(Fig. S3) and retained the snake to allow the new skin to dry
overnight. This drying period was necessary because glue did
not properly adhere to fresh scales when they were still soft
and damp. Once the newly exposed scales had dried, we
reattached the transmitter and released the snake where it
was collected within 24 hr of capture.
Pilot Test of the Subdermal Stitch Attachment Method
From 2 January to 1 April 2013, we conducted a pilot study
on 4 captive corn snakes to assess a modification of the Ciofi
and Chelazzi (1991) subdermal stitch attachment method
used in a field study on western whip snakes (Coluber
viridiflavus). This method created an attachment point on
both sides of the body by running a subdermal catheter and
thread under the subcaudal scales (Fig. S4). Then, the thread
was used to tie the transmitter to the dorsal surface of the
snake. We modified methods from Ciofi and Chelazzi
(1991) in that we used a needle to guide the catheter, silk
instead of nylon suture thread, and a local anesthetic. We
began by injecting the snake intramuscularly with a local
anesthetic (1.5 mg/kg of bupicavaine; Mader 2006) on the
lateral and ventral sides of the tail around the 20th subcaudal
scale. After administering bupicavaine, we waited 15 min for
the drug to take effect. We determined that the snake had
reached a surgical plane of anesthesia by a lack of motor
response upon tail pinching (Mader 2006).
We chose the piercing location to align with the 20th
subcaudal scale posterior to the cloaca so that the insertion
site would occur distal to male copulatory organs (i.e., corn
snake hemipenes extend from the 9th to 15th subcaudal
scales; Laszlo 1975). Furthermore, this placement ensured
the transmitter did not add to the maximum body
circumference of the snake. We measured a silicone catheter
(1 mm in external diameter, 3.5 French single lumen silicone
umbilical venous catheter; Model 4173505, Utah Medical
Products, Inc., Midvale, UT, USA) and cut it to match the
snake’s specific tail width and height. We then threaded the
catheter with suture thread (2-0 silk black braided suture,
0.3 mm in diameter, product code SA75H, Ethicon,
Cincinnati, OH, USA). To create the piercing, we used a
14-gauge needle to make a subcutaneous path that extended
transversely across the snake’s body under the 20th subcaudal
scale. With the needle in place, we inserted the threaded
catheter through the needle, with the threaded catheter
extending beyond both sides of the tail. Then we removed
the needle, leaving only the catheter within the tail of the
snake (Fig. S4). The radiotransmitters had 2 small metal
rings embedded into the waterproofing on each side
(Fig. S5D). We inserted the catheter ends through the
metal rings, and with a square knot tied the suture thread
extending from the ends of the catheter to snugly attach the
transmitter to the snake’s dorsal surface in a ‘backpack’ style
Figure 2. Examples of irritations and injuries of snakes from transmitters attached with glue-only and tape-and-glue attachment methods tested during 2012 at
Magnetawan First Nation near Britt, Ontario, Canada. When transmitters were attached using only glue, these irritations were minor and consisted of
malformed scales and minor bleeding between the scales (A). With the tape-and-glue attachment method, skin irritations were more severe, exhibiting scale
malformations and minor bleeding (B), severe bleeding (C), and removal of scales (D).
Riley et al. External Transmitter Attachment for Snakes 3
placement (Price-Rees and Shine 2011). Housing the suture
thread within the catheter ensured it did not rub on the
snake’s skin, and that it was protected from wear. Lastly, we
used a drop of superglue (Lepage
1
Ultra Gel Control Super
Glue, IDH no. 1662532; Henkel Canada Corporation,
Mississauga, ON, Canada) to secure the knot and prevent it
from unravelling (see Supporting Information Video S1 to
view the procedure).
We weighed and measured total length of each snake every
2 days postattachment, at which time we also recorded
information on: the status of the insertion area (e.g., noting
any discoloration, discharge, swelling, infection, or other
medical issues), activity level of the snake, and whether the
snake was shedding. We also constructed an enclosed
obstacle course (1.0 m 0.25 m 0.15 m), which was
densely stuffed with twigs, leaf litter, and other debris.
We observed each snake’s movements through the obstacle
course, noting how well they handled or avoided potential
snags. On 1 April 2013, we removed transmitters by cutting
the suture thread, swabbing the catheter with alcohol, and
removing it from the snake. We inspected the insertion sites
for signs of infection, scale irritation, and healing. Finally, we
wiped the insertion sites with an alcohol swab and returned
the snake to the enclosure. We inspected the transmitter
attachment sites 1 week (8 Apr 2013) and 9 months
postremoval (6 Oct 2013).
Field Test of the Subdermal Stitch Attachment Method
Between 20 June and 7 September 2013, we attached
transmitters with the subdermal stitch method to 4 wild
eastern massasaugas (2 M and 2 F; Fig. 1; Fig. S5). The
attachment method was the same as in our pilot test on
corn snakes, except when we probed the rattlesnakes to
determine sex, we also measured the distance the probe
extended posteriorly by counting subcaudal scales. We used
this measurement as a guideline for the placement of the
piercing for each snake. Postattachment, we allowed snakes
to rest overnight so that the anesthetic could wear off (the
effects of bupivacaine last 4–12 hr; Mader 2006), and then
released them at their sites of capture (within 24 hr). Upon
each radio location, we visually assessed the snake (if
possible), noted whether it was shedding, and observed the
attachment. If the snake was accessible, we gently prodded it
with a snake hook to elicit antipredator behaviors (e.g.,
rattling and escaping through dense vegetation) to determine
whether this attachment method impeded normal snake
behavior.
On 31 August 2013, we removed the transmitter package
from 3 of the 4 snakes using the method described above.
During removal of the transmitter package, we inspected the
attachment site for signs of infection, scale irritation, and
healing. The fourth snake did not have its transmitter
removed because it was struck and killed by a motor vehicle
while crossing a road before the end of this study.
We conducted our research under authorization from
Magnetawan First Nation’s Chief and Council, Environ-
ment Canada (permit no. SARA-OR-2012-0210), and the
Ontario Ministry of Natural Resources and Forestry
(MNRF; permit nos. 1067714, 1073064, PS-B-001-11,
and PS-B-001-13). Our protocols were approved by the
Laurentian University and MNRF Wildlife Animal Care
Committees (AUP#2013-03-01).
Data Analyses
The distance (m) between consecutive radio locations for
each snake was calculated using the command pointdistances
in Geospatial Modelling Environment software (Version
0.7.2.0; Beyer 2009). We determined minimum daily
distance moved (m) by each individual by dividing the
distances between radio locations by the number of days
between each location, and then averaging across the entire
radiotracking period of each snake.
RESULTS
Glue-Only Attachment Method
Attachment duration for the glue-only method was the
shortest of all 3 methods examined. Snakes in the glue-only
group exhibited the greatest daily movements and behavior
appeared unaltered (Table 1). There were some negative
consequences of the glue-only method: 2 snakes displayed
malformed scales and minor bleeding (Table 1 and Fig. 2).
Most importantly, the adhesives dissolved in water, so we
lost 2 of 8 snakes from the study when their transmitters fell
off (Table 1). We would have likely lost the 6 other snakes if
we did not shift to an alternate attachment method.
Tape-and-Glue Attachment Method
Transmitters attached with tape and glue remained attached
to snakes for the longest duration, but these snakes exhibited
the shortest daily movements (Table 1). However, variation
in movement duration may be attributable to seasonality of
movement patterns. There were major limitations to the
tape-and-glue attachment method: 1) 5 of 17 snakes
exhibited severe skin irritations (malformed scales, minor
to moderate bleeding between the scales, and scale loss;
Fig. 2); 2) it required the longest handling time; 3) the
attachment package hindered snake movements by getting
caught on brush and debris; and 4) 59% of transmitters fell
off during shedding (Table 1). While we were testing this
method, 3 snakes died (1 from road mortality, and 2 from
natural causes as determined by the Canadian Cooperative
Wildlife Health Centre at the University of Guelph, ON,
Canada). We cannot reject the possibility that added stress
from increased handling during testing of this attachment
method may have contributed to the non-road mortalities.
Pilot Test of the Subdermal Stitch Method
We encountered no complications during transmitter attach-
ment using the stitch method. During our pilot study, we did
not observe any external injuries to snakes, transmitters did not
detach, shedding occurred normally (Fig. S4), and there was
negligible disruption to the snakes’ movements (Table 1).
Most snakes (3 of 4) increased in body condition (calculated as
the relationship between total length and mass), with 1 snake
decreasing in body condition (6% loss in mass). However, the
latter result was difficultto interpret because the individual that
declined in body condition was suffering from unrelated
4 Wildlife Society Bulletin 9999()
Table 1. Comparison of external transmitter attachment methods examined with Sistrurus catenatus and Pantherophis guttatus (captive pilot study only) in 2012 and 2013 at Magnetawan First Nation near Britt,
Ontario, Canada. Values after means are standard error. If a section is not applicable, it is indicated by a hyphen (–).
Subdermal stitch
Glue-only Tape-and-glue Captive pilot study Field study
Sample size 8 19
a
44
b
Attachment effectiveness
Mean attachment duration (days) 18 4599 45 31.33 6.44
Range of attachment duration (days) 2–32 days 3–153 days 45 days for all snakes 23–44 days (restricted by the duration of our
study and depends on capture date)
No. of snakes from which the
transmitter detached
2 out of 8 10 out of 17 0 out of 4 0 out of 4
Reason for transmitter detachment Glue dissolved Shedding
Handling requirements
Proportion of track days that the snake
was handled (no. of days handled/total
days tracked)
0.11 0.06 0.066 0.018 0.062 0.01
Range of track days handled 1–3 days 1–8 days Only handled on attachment day (1 day)
Evidence of injury
No. of snakes observed with skin
irritation
2 of 8 5 of 17 None None
Description of injury Several malformed scales
Minor bleeding at attachment site
Many malformed scales
Moderate bleeding between scales
Scale loss
––
Snake movement and behavior
Rattling behavior observed Yes Yes Yes
Snagging on debris No Yes Mild
Movement paused for <1 sec
Mild
Movement paused for <1 sec
Debris caught in attachment None Regularly grass, sticks and
substrate often caught in tape of
many snakes
Irregularly 2 blades of grass observed under the
catheter of one snake during one tracking
location
Shedding Not observed Caused transmitter loss Observed 4 times with no detachment issues Not observed
Daily distance moved (m) 44.76 13.13 34.4 7.55 42.81 7.41
Procedural observations
Attachment procedure notes Easily completed in the field Easily completed in the field Needle inserted at the 20th subcaudal scale
Minor bleeding (>1 mL)
Easily completed in the field
Needled inserted at the 20th subcaudal scale in
males, and the 10th and 12th scale in
females
Minor bleeding (>1 mL)
Removal procedure notes No signs of infection
Quick recovery and healing of “piercing”
postremoval
No signs of infection
Slight tail compression (<1 mm) and scale
wear in 2 snakes
a
Data summarized from n¼17 snakes because 1 snake died from motor vehicle strike, and 1 snake’s transmitter signal was lost.
b
Data summarized from n¼3 snakes because 1 snake died from motor vehicle strike.
Riley et al. External Transmitter Attachment for Snakes 5
hyperthyroidism during our study (J. Hathaway, Scales Nature
Park, personal communication).
The pilot study affordedus an opportunity to observe healing
posttransmitter attachment and removal. We noted a crust of
dried lymph in each of the piercing sites on all snakes. The
formation of this crust is part of the normal immune response
when the skin is breached, particularly if there is no blood
present to form a scab. During both postattachment and
postremoval inspection of the insertion sites, we observed no
signs of infection (e.g., discoloration, discharge, swelling,
sensitivity to touch, unpleasant smell, etc.). Postremoval,
insertion sites resembled healed “piercings” in other taxa (e.g.,
dorsal fin transmitter attachment; Sonne et al. 2012). One
week postremoval, we observed that crusts of dried lymph had
again formed in insertion sites. Nine months postremoval, all
snakes’ insertion sites had completely healed and only a small
scar remained (Fig. S6).
Field Test of the Subdermal Stitch Method
We experienced no complications during transmitter attach-
ment in the field. Duration of attachment was restricted in our
field test (Table 1), but given the opportunity, transmitters
would likely have remained attached for longer because no
transmitters detached from snakes. We did not observe
external injuries caused by the subdermal stitch, there were
negligible effects on snake movement and behavior (e.g.,
normal rattling but a few instances of brief snags on debris;
Table 1), and snakes moved easily through dense vegetation.
Snakes demonstrated a high level of tail-maneuverability and
often took care to move their tails and the attachment package
around objects (Supporting InformationVideo S2). One of the
female rattlesnakes gave birth during our study, indicating that
the subdermal stitch method does not disrupt parturition.
During transmitter removal, we noted that the catheter
constricted the tail slightly (<1 mm) and both male snakes
experienced some abrasion of scales under the transmitter, but
there was no exposed tissue, blood, or pus (Fig. S7).
DISCUSSION
There were both positive and negative attributes for all 3
external transmitter attachment methods. The glue-only
method is clearly not feasible for aquatic and semiaquatic
snakes because the glue quickly dissolved in water resulting in
transmitter detachment. Additionally, the glue caused skin
irritation, which resulted in minor injury in some individuals.
The glue-only attachment method may be useful for short-
term studies on terrestrial species, because this method is
inexpensive and simple to accomplish in the field; however, we
do not suggest its use in long-term research. The addition of
tape, in the tape-and-glue attachment method, meant that
transmitters remained attached longer and could withstand
aquatic environments, but it came at thecost of injury and likely
increased stress for snakes by restricting movements and
increasing handling. Furthermore, many of the snakes (59%)
lost their transmitters during shedding, which restricted the
duration and consistency of data collection. Cumulatively,
both the glue-only and tape-and-glue attachment methods
underscore major issues with external transmitter attachment
on snakes: 1) anything adhered to a snake’s skin will likely
irritate it; 2) the snake will likely lose the transmitter while
shedding; and 3) disrupting the shedding cycle to reattach
adhesive-based transmitters will further irritate snake’s skin
and increase handling. Our findings directly support negative
impacts found by other studies that used tape-and-glue to
attach transmitters to snakes (Gent and Spellerberg 1993,
Rathburn et al. 1993, Jellen and Kowalski 2007, Madrid-
Sotelo and Garcıa-Aguayo 2008, Wylie et al. 2011).
In contrast, the subdermal stitch method appeared to be
effective in both lab and field evaluations. Attachment is
practical and can easily be completed in the field during
standard initial processing activities, which minimizes overall
handling time. The transmitter can be easily replaced by
simply removing the transmitter and thread while leaving the
catheter in place. Unfortunately, we had difficulty finding
suitable study snakes during the 2013 field season, which
limited our sample size for the field evaluation of this
method. Small sample sizes notwithstanding, in both the
field and lab, we did not observe any negative effects on snake
health or behavior. Ciofi and Chelazzi (1991) used a similar
external attachment method to study the spatial ecology of
western whip snakes, wherein they described results similar
to ours: 1) snakes did not experience injury or skin irritation;
2) snakes easily shed their skin around the transmitter
package; and 3) snakes exhibited natural behaviors (e.g., the
transmitter did not impair movement, breeding, or habitat
selection). The only issue reported by Ciofi and Chelazzi
(1991) was that the nylon thread broke such that some
transmitters fell off; thereafter, they switched to silk thread
and had no further issues with transmitter detachment. The
subdermal stitch method has also been used to attach
transmitter units to dugites (Pseudonaja affinis) without
any negative effects on the snakes (A. Wolfe, Curtin
University, personal communication). Research on P. affinis
also demonstrated that a package consisting of multiple
components can be attached to snakes using the subdermal
stitch method, allowing concurrent collection of multiple
types of data (e.g., environmental, thermal, or social data).
Based on the findings from other studies in combination
with our results, we assert that the subdermal stitch method
is likely a viable alternative to internal implantation for snake
radiotelemetry studies.
An assumption of any research or conservation study is that
the data collection techniques do not negatively affect the
target species or individuals in a way that compromises data
validity (Frazer 1992, Riley and Litzgus 2013). There is no
doubt that research on snakes, which tend to be secretive
and cryptic animals, has benefited from radiotelemetry.
However, evaluation of radiotransmitter attachment has
shown that there can be adverse effects, including increased
stress (Creel et al. 1997, Suedkamp Wells et al. 2003),
increased energy costs (Pennycuick et al. 1990, Gessaman
et al. 1991, Godfrey et al. 2003), reduced movements
(Olsen et al. 1992, Putaala et al. 1997), altered behavior
(Gervais et al. 2006, Steenhof et al. 2006, Booms et al. 2011),
skewed sex-ratios (Moorhouse and Macdonald 2005),
reduced reproductive success (Livezey 1990, Hubbard
6 Wildlife Society Bulletin 9999()
et al. 1998, Chipman et al. 2007, Reed et al. 2009, Barron
et al. 2010), and even reduced survival (Burger et al. 1991,
Cotter and Gratto 1995, Steenhof et al. 2006, Chipman et al.
2007, McIntyre 2012). In snakes, internal attachment
methods (ingestion and surgery) alter snake behavior, and
negatively affect snake health and fitness (Fitch and Shirer
1971, Lutterschmidt and Reinert 1990, Lentini et al. 2011).
Ours, and other evaluations of external attachment methods
(Wylie et al. 2011), have demonstrated that using adhesive
methods, such as tape-and-glue, does not work in some
habitat types (e.g., aquatic), provides only short-term data,
can result in skin injury, and likely increases stress. The
subdermal stitch method is a promising technique that can be
utilized long-term without injuring snakes or altering their
behavior. More research is required to understand how the
subdermal stitch method may alter snake stress levels and
other aspects of their physiology (e.g., immunological studies
similar to those of Lentini et al. 2011) and confirm that it is
an effective research tool with minimal negative effects. We
hope our study can provide a starting point to stimulate more
detailed, quantitative assessments of snake transmitter
attachment methods, as well as inform the selection and use
of external transmitter attachment methods in snake research
and conservation.
ACKNOWLEDGMENTS
We thank J. E. Baxter-Gilbert, G. Hughes, L. Monck-
Whipp, C. Neufeld, D. Jones, K. Tabondung, R. Maleau,
and numerous volunteers for field assistance. We also
thank the Magnetawan First Nation community for their
support, and J. Hathaway for the use of corn snakes at
Scales Nature Park. Thank you to the Associate Editor,
Dr. Jeanine Refsnider, and 2 anonymous reviewers for
their contributions to this manuscript that greatly
improved it. Financial support for this work came from
Magnetawan First Nation, Laurentian University, Natural
Sciences and Engineering Research Council of Canada,
and Aboriginal Fund for Species at Risk through the
Canadian Federal Government.
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Associate Editor: Refsnider.
SUPPORTING INFORMATION
Additional supporting information may be found in the
online version of this article at the publisher’s website. The
provided supporting information includes additional details
on this study’s materials and methods (with its own literature
cited) and Figures S1–S7. Videos S1 and S2 are provided as
separate files. The figures and videos provide visualizations of
the transmitter methods tested in this study, and our
observations that are described in the manuscript.
8 Wildlife Society Bulletin 9999()
... Snakes possess simple, limbless bodies and regularly shed their skins, posing challenges to attachments that rely on external structures (e.g., limbs, fins, feathers, fur, etc.) or prominently regionalized bodies [25]. Consequently, most snake researchers have opted for surgical implantation [22,23,38] instead of external attachment. However, surgical implantation increases the risk of snake mortality due to anesthesia and possible postoperative infection [24]. ...
... In some cases, transmitter implantation has negatively affected growth and reproductive rates [33]. It has been pointed out that relying on movement and habitat data from snakes implanted with transmitters may be questionable because sick and convalescing individuals may not behave normally [23,29]. ...
... The drawbacks of surgical implantation make the use of temporary external transmitters an attractive alternative for gathering movement data, and researchers have devised numerous techniques to do so (e.g., [23,37,38]). External attachment can reduce handling time and stress and addresses concerns of surgery-induced sickness and convalescence behaviors [23]. ...
Article
Full-text available
Background The advent of telemetry has revolutionized wildlife research in recent decades. For telemetry to be effective, transmitting devices must remain attached to study animals throughout a period of interest and without impacting pertinent behaviors. Surgical implantation remains the most common method used to attach transmitters to snakes, but concerns about the effects of transmitter implantation on snake health and behavior have motivated many researchers to opt for external transmitter attachments. Despite the increasing use and diversification of external transmitter attachment techniques in snake research, to date there have been no comprehensive reviews examining the methods, efficacies, and adverse impacts reported in the literature. We therefore conducted a systematic review of past research involving external attachment of transmitters on wild snakes. We extracted data from relevant studies to determine whether and how snake traits and transmitter attachment details correlated with efficacy and likelihood of adverse effects. Results The 54 cases that met inclusion criteria covered 33 species and 3 families. External attachment was biased toward smaller-bodied snakes (median = 186 g), although larger snakes had longer retention durations. Adverse impacts were reported in 37% of studies (n = 20), and included altered behavior and movement, skin wounds at the attachment site, and death. Smaller snakes were more likely to exhibit adverse impacts from attached transmitters. Except for caudal attachments in rattlesnakes, attachment method did not have a significant effect on attachment duration. However, attachment method did influence the probability of causing adverse effects, with glue being the most likely to cause negative impacts. Conclusions Externally attaching transmitters to snakes is an increasingly popular alternative to surgical implantation. To provide guidance to researchers considering this approach, we conclude our systematic review with recommendations for attaching external transmitters to snakes. Actions such as minimizing transmitter weight and protrusion, using shorter and stiffer antennas, and using flexible adhesives may help to avoid commonly reported problems. We encourage more consistency in reporting methodological details and results pertaining to efficacy and animal welfare.
... Entre ellas podemos mencionar la colocación externa, adhiriéndolos al tegumento con cinta adhesiva. Esta técnica se recomienda para estudios a corto plazo y cuando el implante no puede ser aplicado, aunque algunas desventajas de esta técnica incluyen la probabilidad de que los radiotransmisores puedan desprenderse al tener contacto con pastizales muy densos o arbustos, o que los movimientos de las serpientes se vean reducidos debido a que quedan atrapadas en dicha vegetación (Reinert y Cundall 1982, Újvári y Korsós 2000, Riley et al. 2017). En otros estudios se ha introducido de manera forzosa por medio de la cavidad oral el radiotransmisor. ...
... Además, este método puede alterar el comportamiento del individuo ya que tienden a moverse menos cuando poseen radiotransmisores en su estómago (Fitch y Shirer 1971). Por otra parte, en estudios donde se han colocado radiotransmisores con pegamento en la piel, las serpientes han mostrado malformaciones de escamas, sangrados leves y además el pegamento se disolvió en agua y se perdieron radiotransmisores (Riley et al. 2017). Si bien en la literatura científica se menciona que el uso externo de radiotransmisores mediante sutura subdérmica es una buena opción con efectos negativos mínimos (Riley et al. 2017, Zdenek et al. 2021, existe la posibilidad de quedar atrapadas en la vegetación y la acumulación de piel mudada en la parte posterior del cuerpo. ...
... Por otra parte, en estudios donde se han colocado radiotransmisores con pegamento en la piel, las serpientes han mostrado malformaciones de escamas, sangrados leves y además el pegamento se disolvió en agua y se perdieron radiotransmisores (Riley et al. 2017). Si bien en la literatura científica se menciona que el uso externo de radiotransmisores mediante sutura subdérmica es una buena opción con efectos negativos mínimos (Riley et al. 2017, Zdenek et al. 2021, existe la posibilidad de quedar atrapadas en la vegetación y la acumulación de piel mudada en la parte posterior del cuerpo. A su vez, Újvári y Korsós (2000) señalan problemas en individuos de pequeño tamaño corporal, donde el comportamiento o movimiento natural del animal puede resultar alterado. ...
Article
Full-text available
Resumen La radiotelemetría se ha convertido en una herramienta valiosa para estudiar la ecología espacial y reproductiva de las serpientes. Diferentes metodologías han sido utilizadas para colocar radiotransmisores en serpientes, incluida la colocación externa con cinta adhesiva, la ingestión forzada y la aplicación de pegamento en la piel, aunque presentan limitaciones y efectos negativos en las serpientes, como la pérdida de los transmisores o la alteración del comportamiento alimentario. En el presente trabajo se presenta el primer caso de implantación de radiotransmisores en la especie Bothrops alternatus en la Argentina. Se utilizaron dos ejemplares de yarará grande B. alternatus capturados de la naturaleza. Se siguió un procedimiento basado en trabajos anteriores con adaptaciones específicas propias para tratar serpientes venenosas. Los ejemplares fueron anestesiados con isoflurano, con soporte de oxígeno durante toda la cirugía. En cada ejemplar se realizó una incisión de 2 cm de longitud, se dividió el músculo y se accedió a la cavidad celómica. El radiotransmisor, previamente esterilizado, se colocó en esta cavidad y su antena se tunelizó bajo la piel hacia la parte superior del cuerpo. Posteriormente, se suturaron los planos musculares y la piel con material estéril. La cirugía fue exitosa en ambos especímenes, con una duración de aproximadamente 30 minutos y una recuperación rápida después de la anestesia. Los radiotransmisores emitieron señales que se captaron a distancias de hasta 500 metros en el campo, lo que permitió rastrear el movimiento de las serpientes durante un período de 10 días. Sin embargo, se observó que la duración de la batería de los transmisores fue menor de lo esperado, lo que limitó el seguimiento a largo plazo. Este trabajo representa una contribución significativa al campo de la radiotelemetría en serpientes en la Argentina, proporcionando un protocolo detallado y exitoso para la implantación de radiotransmisores en serpientes venenosas. Abstract. Radio telemetry has become a valuable tool for studying the spatial and reproductive ecology of snakes. Various methodologies have been used to attach radio transmitters to snakes, including external placement with adhesive tape, forced ingestion, and skin glue application. Still, these methods have limitations and negative effects on snakes, such as transmitter loss or alterations in feeding behavior. This study presents the first case of radio transmitter implantation in the species Bothrops alternatus in Argentina. Two large venomous snakes B. alternatus specimens, were captured from the wild. A procedure was followed based on previous work with specific adaptations for venomous snakes. The specimens were anesthetized with isoflurane and provided with oxygen throughout the surgery. A 2 cm incision was made in each specimen, the muscle was divided, and access to the celomic cavity was obtained. The previously sterilized radio transmitter was placed in this cavity, and its antenna was tunneled under the skin towards the upper body. Subsequently, the muscle layers and skin were sutured with sterile material. The surgery was successful in both specimens, lasting approximately 30 minutes, with rapid recovery post-anesthesia. The transmitters emitted signals detected at distances of up to 500 meters in the field, allowing tracking of the snakes' movements over 10 days. However, it was observed that the transmitter battery life was shorter than expected, limiting long-term monitoring. This work represents a significant contribution to the field of snake radio telemetry in Argentina, providing a detailed and successful protocol for radio transmitter implantation in venomous snakes.
... 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). ...
... 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). ...
... SVL, snout-vent length; BW, body weight; PW, package weight. (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. ...
... Individuals were transported a short distance to a laboratory space and outfitted with radio-transmitters (BD-2, 1.0g, 5 week lifespan; Holohil Systems Ltd., Carp, Ontario). We followed the subdermal stitch attachment method described by Riley et al. (2017) (modified from Ciofi and Chelazzi, 1991) and since used in other studies (Hudson, 2019;Murphy et al., 2021). The subdermal stitch method involves running a subdermal catheter and thread under the subcaudal scales (under tail) and tie the transmitter to the dorsal surface (upper tail) of the snake. ...
... The transmitters and associated attachment materials (catheter, suture) weighed no more than 5% of the total body mass of each snake. Snakes were administered a local anesthetic (1.5 mg/kg of bupicavaine) around the 20 th subcaudal scale 15 minutes prior to the initial transmitter attachment (Riley et al., 2017), and immediately after were administered Baytril and Metacam (Brown et al., 2009). Snakes were monitored for 48 hours prior to release. ...
Article
Full-text available
Studies on habitat selection are central to our understanding of animal ecology and play an important role in the conservation and management of species. However, habitat selection is not necessarily consistent across sectors of populations and failing to understand both similarities and differences between age classes, for instance, may be problematic. Knowledge on habitat use by juvenile vertebrates in general is sorely lacking, particularly for species with precocial offspring, and here we address this gap by describing habitat use by juvenile Western Rattlesnakes ( Crotalus oreganus ). We measured habitat at two scales for radio-telemetered juvenile snakes along active-season movement paths at a site in southern British Columbia, Canada, where seasonal migrations and habitat associations of adult animals have been particularly well studied. Despite the relatively short distances these animals travelled and their diminutive size, we found there was selection for structurally stable cover (e.g., woody debris, shrub, and rock cover) similar to that documented for adult snakes in the same region. Additionally, we tested for differences in microhabitat features at sites used for short-duration (fewer than seven days) and long-duration (seven days or longer) stopovers: we detected negative selection for leaf litter at long-duration stopover sites, but otherwise identified no difference in the microhabitat features associated with these two categories of locations. Overall, this study contributes rare data to our growing understanding of the complexity of habitat requirements for migratory snake species, including northern crotalid vipers, while underscoring the crucial role of habitat selection research across all segments of populations. Comparative data on habitat selection by early-age classes within reptile populations informs conservation planning for the long-term survival of wild populations.
... Rubinoff et al. (1986) and Rubinoff et al. (1988) worked specifically with H. p. platurus, suturing dive tags to the outer skin of 15 individuals off Panama and following them with a hydrophone to trace their movements. Transmitter studies have substantial scientific value, but small sample size may limit inference about the population (Lindberg & Walker, 2007), unnatural behavior can bias data (Fitch & Shirer, 1971), and the methods may negatively impact captured and tagged individuals (Riley et al., 2017;Rudolph et al., 1998;Weatherhead & Blouin-Demers, 2004;Wilson & McMahon, 2006). Thus, to systematically examine the diel-surfacing patterns of H. p. xanthos, we opted for real-time around-the-clock visual observations analyzed with circular statistics. ...
... Transmitters are a common tool for securing activity and spatial data. These devices are typically attached to or implanted in the bodies of anesthetized snakes through surgical methods (as in Rubinoff et al., 1986;Shetty & Shine, 2002;Udyawer et al., 2015) or swallowed (as in Burns & Heatwole, 1998;Weatherhead & Blouin-Demers, 2004) but can have negative impacts on immunity, fecundity, and lifespan (see Riley et al., 2017 for a review). Tag studies are also expensive and sample sizes tend to be small (Lashley et al., 2018), plus resulting changes in behavior can bias results (Fitch & Shirer, 1971). ...
Article
Full-text available
Abstract Diel activity patterns are an important aspect of wildlife ecology and evolution and provide valuable information for conservation and monitoring, yet for many species, activity patterns remain unstudied and may be presumed to mirror related taxa. Here, we describe the distinct diel patterns of an endemic population of venomous sea snakes Hydrophis platurus xanthos inhabiting a narrow range (circa 320 km2) in Golfo Dulce, Costa Rica. To investigate, we conducted a systematic visual survey over five 24‐h cycles and evaluated 339 h of previously obtained sighting data from different studies spanning a decade. While sporadic diurnal surfacing does occur, mostly for respiration, our observations revealed marked crepuscular peaks with regular surfacing through the night. We also report on observed surface behaviors that were also found to vary in frequency at different phases of the photoperiodic cycle. In particular, we show feeding as more common at night. Hydrophis platurus xanthos has developed a circadian rhythm that differs noticeably from its taxonomic parent (H. p. platurus is reported as diurnal across its Indo‐Pacific range), and no congeners have been categorized as crepuscular. Our work thus contributes to the ecological knowledge of this evolutionarily distinct marine elapid and offers insights into the potential role of environmental conditions in shaping animal activity.
... In addition to small terrestrial mammals, tailmount attachment of ABDs has been trialled in reptiles (e.g. Kerr et al. 2004;Romijn et al. 2014;Riley et al. 2017), a semi-aquatic mammal (Rothmeyer et al. 2002), and a variety of avian species (e.g. Woolnough et al. 2004;Le Souëf et al. 2013;Harmata 2016;Yeap et al. 2017) due to the behavioural (e.g. ...
Thesis
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Conservation translocations are becoming an increasingly necessary tool to stem the decline of threatened species globally. The greater bilby (Macrotis lagotis) is a nationally threatened species in Australia. While bilby translocations are expected to contribute to the species’ persistence, the scarcity of information on their behaviour and ecology prevents informed-management. By intensively studying a population of bilbies both prior to, and following reintroduction, and subsequent reinforcements to a fenced sanctuary, I aimed to (1) advance knowledge of bilby behaviour and examine behaviours potentially relevant to fitness (i.e. survival and breeding success), (2) improve ecological knowledge of bilbies within understudied (temperate) climates, and (3) use this knowledge to suggest and develop effective tools for their conservation. Chapter 1 describes the current state of research in applied conservation research, and how increased behavioural data could help address some of the current knowledge gaps for bilby conservation. In Chapter 2, I examined patterns in bilby resource selection, finding that selection changed between seasons and years due to the environmental conditions and resources available. I also found that resource requirements are likely to be behavioural-state dependent and sex-specific. In Chapter 3, I constructed social networks to examine nocturnal proximity of bilbies and concurrent burrow sharing and found that associations were non-random. Expanding on this, in Chapter 4, I found that burrow sharing was likely to help describe breeding strategies, as males strongly avoided other males, and mixed-sex dyads exhibited kin-avoidance when mate choice was more limited. In Chapter 5, I developed a test to screen personality traits in bilbies, finding links between male response to handling and relative breeding success post-release. Lastly, in Chapter 6, I described a method to collect detailed movement data on the bilby, and discussed some of the practical and animal welfare constraints for its application. My thesis provides new insights into the behavioural ecology of the bilby with potential implications for future management of the species. With further translocations necessary for long-term persistence of the bilby, this research is highly relevant to current and future management of this ecologically important species, with potential applications to other similarly at-risk species.
... Juvenile snakes were captured by hand (using snake tongs or hooks) during egress (April-May) at or near hibernacula, with the exception of four individuals captured opportunistically later in the season in their summer range. Individuals were brought back to a laboratory space and outfitted with radio transmitters (BD-2, 1.0 g; Holohil Systems Ltd., Carp, Ontario) following the subdermal stitch attachment method first described by Riley et al. (2017) (modified from Ciofi and Chelazzi 1991) and since used in other studies (Hudson 2019;Murphy et al. 2021). The subdermal stitch method involves running a subdermal catheter and thread under the subcaudal scales and tying the transmitter to the dorsal surface of the snake. ...
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... following Riley et al58 . The transmitter frequencies were set within the 150-151 and 216-217 MHz band. ...
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... In addition to small terrestrial mammals, tail-mount attachment of ABDs has been trialled in reptiles (e.g. Kerr et al. 2004;Romijn et al. 2014;Riley et al. 2017), a semi-aquatic mammal (Rothmeyer et al. 2002), and a variety of avian species (e.g. Woolnough et al. 2004;Le Souëf et al. 2013;Harmata 2016;Yeap et al. 2017) due to the behavioural (e.g. ...
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This outstanding clinical reference provides valuable insights into solving clinical dilemmas, formulating diagnoses, developing therapeutic plans, and verifying drug dosages for both reptiles and amphibians. The information is outlined in an easy-to-use format for quick access that is essential for emergency and clinical situations. Discusses veterinary medicine and surgery for both reptiles and amphibians Features complete biology of snakes, lizards, turtles, and crocodilians Provides step-by-step guidelines for performing special techniques and procedures such as anesthesia, clinical pathology, diagnostic imaging, euthanasia and necropsy, fracture management, soft tissue surgery, and therapeutics Covers specific diseases and conditions such as anorexia, aural abscesses, and digit abnormalities in a separate alphabetically organized section 53 expert authors contribute crucial information to the study of reptiles and offer their unique perspectives on particular areas of study The expansive appendix includes a reptile and amphibian formulary A new full-color format features a wealth of vivid images and features that highlight important concepts and bring key procedures to life 29 new chapters covering diverse topics such as stress in captive reptiles, emergency and critical care, ultrasound, endoscopy, and working with venomous species Many new expert contributors that share valuable knowledge and insights from their experiences in practicing reptile medicine and surgery Unique coverage of cutting-edge imaging techniques, including CT and MRI.
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