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373
Herpetological Conservation and Biology 12(2):373–383.
Submitted: 10 December 2016; Accepted: 21 January 2017; Published: 31 August 2017.
Copyright © 2017. Thomas A. Radzio
All Rights Reserved.
Nesting behavior can inuence reproductive
success and ospring quality in oviparous species.
For example, nest-site selection by female turtles can
determine incubation environment and aect embryonic
development, hatching success, and ospring
performance (Wilson 1998; Booth et al. 2013). In
many turtles, nest temperature also determines ospring
sex, which may be important when demographic or
environmental characteristics benet one sex over the
other (Charnov and Bull 1977; Bull and Vogt 1979). In
addition to carefully selecting nest sites, some turtles
camouage nests from predators or actively guard nests
(Hailman and Elowson 1992; Agha et al. 2013 and
references therein). External factors such as nest-site
availability or human disturbance may inuence nesting
behavior (Roosenburg 1991; Johnson et al. 1996), but
conspecic interactions are not thought to interfere with
nesting activities in most turtles (but see Hughes and
Richard 1974; Doody et al. 2009).
Gopher Tortoises (Gopherus polyphemus) inhabit dry
upland areas along the Coastal Plain of the southeastern
United States. Individuals center daily activities on long
(often > 4 m) burrows that they excavate and use for
thermoregulation, predator avoidance, rest, and other
activities (Douglas and Layne 1978). In part because
tortoises spend most of their time at burrows, these
sites also serve as primary locations for mating and
competitive intrasexual interactions (Douglas 1986;
McRae et al. 1981; Diemer 1992; Johnson et al. 2007;
Guyer et al. 2014). Additionally, in many populations,
females often, perhaps predominantly, nest just in front
of burrows in the mound of bare soil referred to as the
burrow apron (Landers et al. 1980; Butler and Hull 1996;
Epperson and Heise 2003; Hammond 2009; Lamb et al.
2013). Gopher Tortoises potentially prefer relatively
sunlit burrow aprons or other warm bare ground areas
as nest sites, but such sites may be less common in areas
where re suppression has allowed dense hardwood
shrubs and small trees to dominate (Diemer 1986;
Diemer and Moore 1993; Averill-Murray et al. 2014).
We investigated the nesting behavior of Gopher
Tortoises in an old-growth forest dominated by an
overstory of Longleaf Pine (Pinus palustris) and a
diverse groundcover community composed of hundreds
)
1,421,3
1Department of Biodiversity, Earth, and Environmental Science, Drexel University, Philadelphia,
Pennsylvania 19104, USA
2Tall Timbers Research Station and Land Conservancy, 13093 Henry Beadel Drive Tallahassee, Florida 32312, USA
3Department of Biology, Drexel University, Philadelphia, Pennsylvania 19104, USA
4Corresponding author, e-mail: tomradzio@hotmail.com
Key Words.—Georgia; Longleaf Pine; nests; reproduction; reptile; social; turtle
374
Radzio et al.—Gopher tortoise nesting behavior.
of native forbs and grasses. Although Gopher Tortoises
have been studied extensively, aspects of their nesting
behavior beyond frequency, seasonal timing, and
location (e.g., cavity construction, egg laying) remain
largely undescribed. Gopher Tortoise behaviors can be
dicult to document due to the tendency of individuals
from many populations to quickly hide in burrows when
approached (Anderson 2001, Thomas Radzio, pers.
obs.). Butler and Hull (1996) briey observed two wild
female Gopher Tortoises digging nest cavities, but both
tortoises abandoned nesting attempts before ovipositing,
apparently in response to researcher presence. The most
complete account of an actual nesting event is for a
single captive individual kept far north of the range of
the species in Connecticut, USA (Keneck 1954).
We used time-lapse video cameras to document
the natural, undisturbed behaviors of nesting Gopher
Tortoises before, during, and after oviposition. Our
observations comprised nesting activity as well as
interactions between tortoises, including gravid females,
at nest sites. This work provides new insights into
tortoise social interactions and how they might inuence
nesting activity in this secretive species.
.—We studied Gopher Tortoise
nesting and conspecic interactions on Wade Tract
(30°45'N, 84°0'W), an 80-ha old-growth ecological
preserve located near Thomasville in southwestern
Georgia, USA. Longleaf Pines, many greater than 200
y old, dominated the upper canopy (Platt et al. 1988).
Ground cover included relatively few bare spots and was
dominated by Wiregrass (Aristida stricta), oak (Quercus
spp.), and other native plants (Christine Ambrose, unpbl.
report). Wade Tract is located within Arcadia Plantation,
a 957-ha area that consists primarily of mature (> 80 y)
Longleaf Pine forest. Wade Tract is managed by Tall
Timbers Research Station using frequent prescribed
re (≤ 2-y return intervals), and surrounding areas of
Arcadia Plantation are burned at similar intervals.
Previous work at Wade Tract reports a site-wide density
of adult tortoises of 0.8 individuals/ha (Guyer et al.
2012). However, adult tortoise densities at locations
within the site where we conducted observations were
higher (Thomas Radzio, unpubl. data).
.—We set time-lapse video cameras
(Plotwatcher Pro, Day 6 Outdoors, Inc., Columbus,
Georgia, USA) to record activity at tortoise burrows
known or thought to potentially contain adult female
tortoises. We attached cameras to wooden stakes and
positioned them to monitor burrow entrances, burrow
aprons, and surrounding areas. We programmed video
cameras to record a time-stamped frame every 5 s during
daylight hours, except for a very small number of days
when we set video cameras to record a frame every 1
s. Tortoises did not appear to respond to the presence
of cameras.
During mid-May to late-June 2013, video cameras
monitored the activities of 10 female tortoises at their
burrows, hereafter referred to as resident tortoises 1–10
that each could be individually identied by the presence
of radio transmitters (used in another study) or unique
shell markings. Resident females were monitored
for 2–33 complete d (median = 20 d; complete day =
video collected from at least 0600–1900, but usually
dawn to dusk; all times reported in Eastern Standard
Time). Additionally, cameras monitored activity at two
other burrows, both occupied by adult males, for 5–11
complete d. We refer to tortoises that appeared at the
burrows of resident tortoises as visitors.
From mid-May to mid-June, we visited tortoise
burrows on most days to search for nests. In general,
we spent little time at individual burrows, allowing
tortoises to engage in natural, undisturbed activity and
behavior throughout most of the day. We rarely dug
into burrow aprons to locate nests, but instead relied on
signs of potential nesting activity such as disturbance to
burrow aprons and presence of fresh soil behind burrow
entrances (Matt Hinderliter, pers. comm.). When we
located a nest, we initially covered it with a small piece
of hardware cloth, buried several cm below the soil
surface, to protect eggs against predators (Radzio et
al. 2017). Only in one of six instances where females
completed a nest on video did we dig in burrow aprons
or install a nest protector during the remaining daylight
period following nesting. In that instance, we partially
excavated the nest and covered it at 1900, more than
3 h after the female completed nesting. Therefore, we
only minimally inuenced nest manicuring activity. In
most cases, we allowed cameras to continue recording
tortoise activity at nest sites for several days following
nest discovery.
.—We viewed video recordings in
GameFinder software (Day 6 Outdoors, Columbus,
Georgia) and scored all nesting attempts, conspecic
visits, and social interactions. We assessed whether
females dug nest cavities and oviposited with their heads
oriented non-randomly relative to burrow entrances
(either facing at least partially toward or at least partially
away from the burrow) using a binomial test. We also
evaluated variation in the time that females spent in
dierent stages of nesting (identied and described
in Results) using a Kruskal-Wallis test. We used this
nonparametric test because sample sizes were too
small to assess assumptions of parametric procedures.
We performed posthoc pairwise comparisons using
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Herpetological Conservation and Biology
Bonferroni-corrected Mann-Whitney U tests. We
conducted statistical analyses in SPSS version 24.0
(IBM Corp. Released 2015. IBM SPSS Statistics for
Mac, Version 24.0.) with α = 0.05.
We describe encounters between nesting tortoises and
conspecics. We also characterized encounters between
females and conspecics outside of obvious nesting
activity, but during the nesting season. To characterize
interactions between females, we determined the
proportion of female-female encounters (multiple
individuals visible at the same time on video) that
included at least one female responding aggressively to
the other. We evaluated aggression at two levels. We
considered an interaction to be aggressive if at least one
female rammed the other. We considered the interaction
potentially aggressive if one female blocked the burrow
entrance. We used the same approach to describe
encounters between females and large juveniles.
To characterize female-male interactions, we
determined the proportion of female-male encounters in
which the male attempted to mate with the female. We
identied male mating behavior to include head bobbing
or mounting attempts. We also calculated the proportion
of female-male encounters and mounts that represented
potentially successful mating attempts. Potentially
successful matings appeared to be distinct from other
mating attempts in that males remained mounted longer,
made deep head thrusts, and dismounted females
voluntarily (Supplemental Video 1). Males left female
burrow areas immediately after potentially successful
mating attempts. We did not assess aggression between
females and males because subtle aggression is dicult
to distinguish from mating activity.
.—Cameras
documented six complete and six abandoned nesting
attempts on Wade Tract by six resident and three visiting
females (n = 9), all commencing between 1009–1736
on 25 May to 13 June 2013 (Table 1). Additionally,
while conducting eldwork, we observed a tenth female
digging a nest cavity on a burrow apron outside of
Wade Tract, but still on Arcadia Plantation in the late
afternoon of 5 June 2013. She abandoned the attempt
before ovipositing, but a nest was laid in the same
location 2 d later. We found no indication of tortoises
laying eggs more than once during the nesting season.
All observed nesting attempts occurred on burrow
aprons, approximately even with to three adult tortoise
body lengths from the back edges of burrow entrances.
. Nesting observations, minimum number of nesting attempts away from own burrow (NA), minimum number of female-female
interactions at potential nesting sites (burrows) 10 d preceding nesting (FFI), and minimum number of conspecic disruptions to nesting
activity (includes disruptions during nest manicuring activity; CD) for individual Gopher Tortoises (Gopherus polyphemus) from a site
in southwestern Georgia, USA, based on video recordings at burrow aprons. Asterisks indicate possible nesting activity away from own
burrow.
Female Nesting Observations NA FFI CD
Resident 1 5 June 2013, 1146–1207: Attempted to nest at own burrow. Abandoned attempt, perhaps
due to approaching rainstorm.
8 June 2013, 1009–1117: Nested successfully at own burrow. Two visiting males
disrupted nest covering and manicuring.
2
Resident 2 7 June 2013, 1550–1622: Abandoned nesting attempt at own burrow. Large root observed
in abandoned cavity.
7-14 June 2013: No further nesting activity at this burrow. Female possibly nested away
from own burrow.
1*
Resident 3 2 June 2013, 1154–1159: Abandoned nesting attempt at own burrow when male visited.
4 June 2013, 1047–1240: Nested at own burrow.
2 1
Resident 4 9 June 2013, 1011: Left own burrow. Tracked to new burrow at 1850 h. Apron of new
burrow contained fresh nest.
1* 1
Resident 6 5 June 2013, 1011–1103: Nested at own burrow. Visiting male disrupted nest manicuring
activity.
2 1
Resident 8 9 June 2013, 1447–1615: Nested at own burrow. 6
Resident 9 7 June 2013, 1344–1441: Nested at own burrow.
Visitor 1 25 May 2013, 1418–1428: Visited male-occupied burrow. Started to nest, but abandoned
attempt.
1 1
Visitor 2 1 June 2013, 1425–1432: Visited Resident Female 8’s burrow while resident was away.
Started nesting, but abandoned attempt.
1 2
Visitor 3 12 June 2013, 1736-1739: Visited Resident Female 2’s burrow. Abandoned nesting
attempt when resident emerged from burrow. Both tortoises abandoned burrow.
13 June 2013, 1440–1545: Returned and nested at vacant burrow.
211
376
Radzio et al.—Gopher tortoise nesting behavior.
Tortoises did not limit nesting activity to their own
burrows. Three visiting females attempted to nest
(three observations) or nested (one observation: after
the resident female left) at burrows of video-recorded
conspecics (Table 1). Resident females also may
have nested at other burrows. One resident female left
her burrow at 1011 on 9 June and was found at 1850
inside another burrow containing a freshly laid nest in
the apron (Table 1). A second video-recorded resident
female abandoned a nesting attempt at her burrow after
hitting a large root, and, based on subsequent camera
observations at her burrow, likely nested elsewhere.
A third video-recorded resident tortoise that nested at
her burrow had only moved to that burrow within the
previous 10 d.
We documented seven females each abandon a
single nesting attempt prior to oviposition, one for
an unknown reason, one perhaps in response to an
approaching rainstorm, and the remainder apparently
in response to a root in the nest cavity (one female),
researcher disturbance (one female), and conspecics
(three females; Table 1). Conspecics also temporarily
disrupted the nesting activities (nest covering and
manicuring) of two females that had oviposited earlier
in the day (Table 1).
.—Nesting could be divided into
ve stages: circling and/or digging a shallow depression,
digging the egg cavity, ovipositing, covering the nest,
and manicuring the nest area. Time spent in dierent
stages diered (H = 25.8, df = 4, P < 0.001; Table 2).
Females exhibited wide variation in the rst nesting
stage, circling and/or digging a shallow depression,
and not all females performed this stage. Four females
initiated nesting by circling on their center axis at the
prospective nest location. Four other tortoises initiated
nesting by both circling and constructing a shallow
depression (Suppl. Video 2). However, one of these
tortoises started one nesting attempt by circling and
digging a shallow depression, but started another
by immediately excavating a nest cavity.
Similarly, a ninth tortoise basked on her burrow apron
for 29 min without changing position and transitioned
directly to excavating a nest cavity in the same location
without first circling or digging a shallow depression
(Supplemental Video 3). Most females lowered
their head to the ground a small number of times
before nesting, but this behavior was minimal during
this stage. Mean time spent circling and/or digging
a shallow depression was 7.0 min (range = 0.0–15.0
min, n = 8: one female excluded because she abandoned
her attempt during this stage; Table 2).
When excavating nest cavities, females faced away
from, rather than toward, burrow entrances more often
than expected by chance (nine of nine facing away;
binomial test: P = 0.004) and used their hindlimbs to
remove soil (Supplemental Video 4). As time progressed,
individuals lifted up slightly on their forelimbs as if to
reach deeper into the cavity with the hindlimbs. In some
instances, females kicked excavated soil into and behind
burrow entrances. Mean time to excavate the nest cavity
was 40.3 min (range = 25.3–59.5 min, n = 6).
After constructing a nest cavity, tortoises oviposited
immediately. All females laid eggs without interruption
while facing away from the burrow entrance.
Ovipositing females pumped their heads in and out of
their shells (Supplemental Video 5). Due to tortoise
and camera positioning, it was only possible to see into
the egg chamber during one oviposition event. In that
instance, the female used a hindlimb multiple times to
manipulate eggs within the nest cavity. Two ovipositing
females exhibited extensive frothy saliva or mucus
discharge from the mouth and nares (Supplemental
Video 6). One of these females also had discharge from
the eyes. Mean time to oviposit was 10.9 min (range =
7.2–16.1 min, n = 6; Table 2).
After ovipositing, females immediately covered
nests. Females initially used their hindlimbs to cover
the eggs, while continuing to face away from the burrow
entrance. Forelimbs remained planted stationary on the
ground from when tortoises initiated cavity excavation
until individuals nearly completed covering the nest
using their hindlimbs, at which point the forelimbs
were employed to nish the task (Supplemental Video
7). Mean time to cover nests was 15.3 min (range =
10.0–22.0 min, n = 6). Initiation of nesting through nal
covering of eggs averaged 73.8 min (range = 52.1–112.6
min, n = 6; Table 2).
After covering nests, females (n = 6) extensively
manicured the nest area, burrow entrance, and
surrounding burrow apron (Supplemental Video 8).
Manicuring females kicked soil and other materials out
of burrow entrances, some of which had accumulated
. Time spent by female Gopher Tortoises (Gopherus
polyphemus) from a site in southwestern Georgia, USA, in each
nesting stage and total time required to construct a nest (excluding
nest manicuring activity). Dierent letters next to mean values
denote signicantly dierent time spent in stages (Bonferroni-
corrected Mann-Whitney U tests, P < 0.05). Manicuring activity
refers to manicuring activity on the day of oviposition and does not
include additional nest manicuring on subsequent days.
Activity Mean (min) Range (min) n
Circling/Digging Depression 7.0 (a) 0.0–15.0 8
Digging Egg Cavity 40.3 (b) 25.3–59.5 6
Oviposition 10.9 (a) 7.2–16.1 6
Covering Egg Cavity 15.3 (a) 10.0–22.0 6
Total Time to Construct Nest 73.8 52.1–112.6 6
Nest Manicuring 150.5 (c) 101.8–207.5 6
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Herpetological Conservation and Biology
during excavation of the nest cavity, and roughed up
soil on the burrow apron using their forelimb claws.
On average, females repeated the behavior of entering
(or partially entering) burrows and kicking soil out 19.7
times (range = 11–30, n = 6 tortoises) and spent about
150.5 min (range = 101.8–207.5 min, n = 6; Table 2)
engaged in manicuring activity during daylight hours
following nesting. Manicuring females also repeatedly
nuzzled the ground (Supplemental Video 8). On average
individuals lowered their noses toward the ground at least
106 times (range = 22–200, n = 6) during manicuring
activities before retreating into burrows by dark. Due
to camera angles, vegetation, and low video frame rate
(0.2 frames/ s), we likely undercounted this behavior.
At least four of six females emerged from burrows much
earlier than usual the morning following nesting and
continued some manicuring activities. Observations
on days following nesting were unavailable for two
females. In one case, we installed protective wire mesh
over the nest (Radzio et al. 2017) soon after it was laid,
and the female left shortly thereafter and did not return.
In the other case, the female overnighted in the burrow
after nesting, but additional video was not recorded at
that burrow.
.—We
documented interactions between nesting females
and conspecics in ve of 12 video-recorded nesting
attempts (n = 6 total interactions, one nesting event
included two interactions). In each instance that the
interaction occurred before eggs were laid (n = 3), the
female abandoned the nesting attempt (Table 1). In
one interaction, a visiting female (Visitor 1) arrived at a
burrow containing a male and immediately began to nest
on the burrow apron, but abandoned the attempt soon
thereafter, apparently when the male emerged (Table
1). Similarly, another female (Resident 3) immediately
abandoned nest site preparation at her burrow when a
male visited (Supplemental Video 9). She nested in the
same location alone 2 d later. A third female (Visitor
3) visited a burrow containing another female and
started to dig a cavity, but abandoned the attempt when
the resident emerged (Fig. 1A–B; Supplemental Video
10). The two tortoises interacted on the burrow apron
before both left the area. On the following day, when
the burrow was vacant, the visiting female returned and
nested. Visiting males disturbed two other females after
they oviposited. A male visited a female (Resident 1)
as she covered her nest and vigorously tried to mate
with her, immediately biting, mounting, and ejaculating/
urinating on her shell. She was unreceptive, and at one
point, the aggressive male overturned in the partially
lled in nest (Supplemental Video 11; Fig. 1C–D).
Later that day, another male visited, and disrupted nest
. Images from time-lapse video camera stations at two Gopher Tortoise (Gopherus polyphemus) burrows in southwestern
Georgia, USA. (A-B; Supplemental Video 10) Female Gopher Tortoise (Visitor 3; left) visits the apron of a burrow containing a female
conspecic (Resident Female 2; right) and starts to excavate a nest cavity. Shortly thereafter, the resident female emerges; the visitor
stops digging; the tortoises interact; and the visitor leaves. Later that day, the resident female also left. On the following day, the visiting
tortoise returned and successfully nested at the vacant burrow. (C-D; Supplemental Video 11) Visiting male aggressively mounting a
female (Resident Female 1) while she attempts to cover or manicure her nest, which she laid minutes before. The male overturned while
attempting to mount the female.
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Radzio et al.—Gopher tortoise nesting behavior.
manicuring activity, but may have successfully mated
with the now more receptive female (Supplemental
Video 1). A male also visited another female (Resident
6) as she manicured a nest she laid earlier in the day
and distracted her from this activity for about 30 min
(Supplemental Video 12; Table 1).
.—Cameras documented 12 visits by females
to female-occupied burrows outside obvious nesting
activity (Table 3). Observations involved at least seven
females. Visiting and resident females interacted in
11 of 12 visits (Table 3). In the lone visit without an
interaction, the resident tortoise remained inside the
burrow out of camera view while the visitor briey
inspected the burrow entrance. Ten of the 11 interactions
involved at least one gravid tortoise (Table 1). Ten
interactions lasted fewer than 20 min. One interaction,
which included overt aggression, involved tortoises
sharing a burrow for at least 2 d.
Six of 11 interactions involved overt aggression in
which at least one female rammed the other tortoise with
her the gular protrusion and/or carapace (Supplemental
Video 13). At least ve females exhibited such overt
aggression toward another female. In three of the ve
remaining interactions without overt aggression, a
female was initially at the surface and positioned itself
(in two instances quite quickly) in the burrow entrance
as if to prevent the other female from entering. In the
remaining two interactions without overt aggression,
a female was already in the burrow entrance, facing
inside, and responded to another female on the burrow
apron either by turning sideways in the burrow entrance
or turning to face completely outward.
.—
Cameras documented 49 visits by males to females (n =
10) at their burrows outside of obvious nesting activity.
A female (n = 9) was at, or emerged to, the surface during
40 of these visits. Males attempted to mate with females
in at least 38 of 40 (95.0%) such encounters (Table 3).
Mating attempts often proceeded by: 1) the male
headbobbing toward (and sometimes biting) the female;
2) the male backing away from a female; 3) if receptive,
the female advancing toward the male; 4) the male
continuing to headbob toward (and sometimes biting)
the female; 5) the female turning around to face away
from the male (and toward the burrow entrance); 6) the
male rapidly mounting the female; 7) the female moving
toward and into the burrow, which would cause the male
to become dislodged or voluntarily dismount before
copulating; and 8) often repeats of this sequence once
the female reemerged from the burrow (Supplemental
video 12). At other times, males initiated mating
attempts by immediately mounting and, sometimes,
biting females. Males regularly mounted females from
ineective copulatory positions, such as from the front
or side of the carapace (Supplemental Video 11). Rapid
mounting often led to ejaculation or urination onto
female carapaces or onto the ground (Supplemental
Video 11). In at least one instance, a male ejaculated or
urinated onto the ground very soon after arriving, before
even mounting the female.
Males mounted females as many as six times per
interaction with obvious mating attempt (mean = 1.8
mounts), but appeared to copulate only in up to ve of
69 (7.2%) total mounting attempts, or ve of 38 (13.2%)
interactions involving obvious mating attempts (Table 3).
In these potentially successful copulations, which were
distributed evenly among ve females, males remained
mounted longer, made deep head thrusts, dismounted
females voluntarily, and left immediately thereafter
(Supplemental Video 1). Similar to ovipositing females,
several males expelled mucus or saliva from their
nares during potentially successful copulation events.
Although male mating attempts often were aggressive,
we did not observe females exhibiting overt aggression
(i.e., ramming, pushing) toward males.
.—
Large juveniles (about 15 cm carapace length) briey
visited burrows containing adult females on ve
occasions. On two occasions, the resident female
emerged from the burrow and rammed the smaller
tortoise (Supplemental Videos 14 and 15). On one
occasion, a large juvenile visited a burrow while
the resident female was inside and a visiting female
was about to initiate a nesting attempt on the burrow
apron. The large juvenile and the visitor interacted,
but the interaction did not include overt aggression
(Supplemental Video 16). On two other occasions, large
juveniles visited burrows containing adults, but the adult
did not emerge from the burrow nor was observed in the
entrance (Table 3).
. Conspecic encounters (multiple individuals observed
together) of Gopher Tortoises (Gopherus polyphemus) from a site
in southwestern Georgia, USA, outside obvious nesting activity,
but during the nesting season. Number of encounters (NE),
encounters with interactions (EI), interactions with aggression
(IA), interactions with mating attempts (IMA), and interactions
with potential matings (IPM; interaction types dened in Materials
and Methods). In six of 11 female-female interactions, at least one
female rammed the other. In each of the ve remaining potentially
aggressive interactions, a female blocked the burrow entrance.
Encounter Type NE EI IA IMA IPM
Female-Female 11 11 6–11 – –
Female-Male 40 39 – 38 5
Female-Large Juvenile 3 3 2 – –
379
Herpetological Conservation and Biology
.—Similar to reports for other
Gopher Tortoise populations (Landers et al. 1980; Butler
and Hull 1996; Epperson and Heise 2003; Hammond
2009; Lamb et al. 2013), females at this site frequently,
perhaps predominantly, nest at burrow aprons. Gopher
Tortoises in Georgia nest up to once annually (Landers
et al. 1980), and at least 6–7 of 10 resident females in
this study exhibited nesting activity at burrow aprons.
We also add to other reports suggesting that females
do not nest exclusively at their burrow aprons but may
select nest sites from among multiple burrows, including
those of juvenile tortoises, and other bare ground areas
(Landers et al. 1980; Lamb et al. 2013; Radzio et al.
2017). Our observations suggest that at least ve females
exhibited nesting activity away from their burrows,
one on two occasions (Table 1). Additionally, another
tortoise that nested at her burrow had only moved to that
burrow within the previous 10 d. Although quantitative
data are limited, tortoises may select among multiple
potential nest sites on the basis of vegetative cover, soil
composition, and thermal environment (Landers et al.
1980; Diemer and Moore 1993; Smith 1995; Lamb et
al. 2013).
In some diurnal turtle species, high daytime
temperatures constrain nesting to night hours and
other cooler times of day (Spotila and Standora 1985).
Video-recorded nesting observations distributed rather
uniformly between 1000 and 1800, but sample sizes
were low. However, cameras did not monitor possible
night activity. Given that females required on average
more than an hour to nest, and that in hot environments
body temperatures of adult Gopher Tortoises can
increase from typical active values (mean = 34.7° C)
to temperatures at which individuals begin to froth (≥
38.0° C) in as little as 10 min (Douglass and Layne
1978), females should avoid nesting in open habitats
during hot weather. In this study, two video-recorded
females secreted large amounts of mucus or frothy saliva
when thrusting their heads in and out of shells during
oviposition. Although it is possible that this discharge
represented a physiological response to thermal stress
(Douglass and Layne 1978; Johnston 1996), we were
unable to unambiguously assess heat loads experienced
by these nesting tortoises. Additionally, discharge may
have reected symptoms of upper respiratory disease
(McLaughlin et al. 2000) or simply represented a feature
of nesting that sometimes occurs in healthy individuals
of this species when they thrust their heads deeply in
and out of their shell during oviposition. Notably, some
males exhibited similar discharge when performing
deep head thrusts during potentially successful mating
attempts.
Gopher Tortoises in this study exhibited many typical
turtle nesting behaviors, including nest site preparation
(Ehrenfeld 1979), but this activity was plastic even
within individuals. Keneck (1954) reported that a
captive Gopher Tortoise began nesting by swinging
its body in a circle and digging a shallow depression
with its forelimbs. We observed similar behavior in
most nesting tortoises, but several times females started
nesting by immediately digging an egg cavity with their
hindlimbs. Females engaged in little to no ground-
nuzzling behavior before starting to nest (Morjan
and Venlenzuela 2001 and references therein), but as
described below, engaged in this behavior extensively
when manicuring the nest area following oviposition.
Typical of most chelonians (but see Kuchling 1993),
individuals in this study used their hindlimbs to both
excavate and initially cover the egg cavity (Ehrenfeld
1979). Tortoises required considerable time to excavate
the nest cavity, but after doing so, immediately laid
eggs, on average within 11 min. By ovipositing quickly
and immediately covering the nest, tortoises may reduce
depredation risk to themselves and their eggs and also
prevent nest substrate from losing excessive moisture.
Unlike as reported for captive Agassiz’s Desert Tortoises
(Gopherus agassizi; Lee 1963) and free-ranging Texas
Tortoises (G. berlandieri; Auenberg and Weaver
1969; Rose and Judd 2014), we did not observe Gopher
Tortoises urinating on nests. However, due to camera
angles and tortoise orientations, we could only see into
the nest cavity in one video.
Tortoises always oriented facing away from burrow
entrances while excavating the nest cavity (Butler and
Hull 1996), ovipositing, and covering eggs. The soil in
front of burrows often slopes down toward the burrow
entrance (Thomas Radzio, pers. obs.). Facing upslope
may allow females to reach deeper into the nest cavity
with their hindlimbs, deposit excavated soil downhill,
and detect potential predators (Butler and Hull 1996)
or visiting conspecics more easily because the head
remains elevated and out of the burrow. This orientation
often also results in excavated soil being scattered
behind the back edge of the burrow entrance, a sign
that can be used by investigators to locate nests (Matt
Hinderliter, pers. comm.).
After covering nests, females manicured nest areas,
perhaps having the eect of reducing egg depredation,
which can be very high in Gopher Tortoise populations
(Landers et al. 1980; Smith et al. 2013). Keneck
(1954) reported that after covering her nest, a captive
Gopher Tortoise “walked back and forth over the nest
area and brushed it lightly with the nails of her front
feet” for a short period. Our observations indicate
that wild females engage in extensive nest manicuring
intermittently throughout the day, or even days,
following nesting and suggest that females also disguise
380
Radzio et al.—Gopher tortoise nesting behavior.
nests by kicking soil out of burrows onto burrow aprons.
All females intermittently kicked soil out of the burrow
and onto the apron throughout the afternoon following
nesting. Using their forelimbs, they also roughed up
soil over a portion of the burrow apron. By excavating
soil from burrows, tortoises can remove material that
accumulated in burrow entrances during nest cavity
excavation and create the visual appearance of a burrow
that has been dug out or cleaned by a tortoise, rather than
one that contains a nest in its apron. It is also possible
that by kicking soil out of burrows, which frequently
contain tortoise feces, tortoises mix in odors from the
burrow to the nest area, and that this may confuse
potential predators that locate turtle nests via olfactory
cues, including volatiles released from disinterred soils
(Buzuleciu et al. 2016). Manicuring females engaged
in extensive ground nuzzling, a common turtle nesting
behavior hypothesized to play a role in nest site selection
either via detection of thermal or olfactory cues (Morjan
and Valenzuela 2001). Therefore, it is notable that
Gopher Tortoises ground nuzzled extensively after,
but very little or not at all before nesting. A recent
study of Painted Turtles (Chrysemys picta) suggests
females can detect nests of conspecics via olfactory
cues (Iverson et al. 2016), and we speculate that
Gopher Tortoises use ground nuzzling behavior and
olfactory senses to guide eorts to disguise nest odors.
Disguising nest odors for even a few days may be
highly benecial because turtle nests may be at greatest
risk of depredation early in incubation (Congdon et al.
1983, 1987). Interestingly, a camera documented a
Gray Fox (Urocyon cinereoargenteus) visit a burrow
apron containing a nest that had been laid fewer than
6 h earlier. The female, who was sitting atop her nest
when the fox arrived, quickly hid inside. The fox left
the burrow seconds later without disturbing the nest.
Although not observed in this study, recent accounts
suggest that some female Gopher Tortoises defend nests
against potential predators (Grosse et al. 2012; Dziadzio
and Smith 2015). Nest defense is also documented in
several western Gopherus species, including ones that
often nest inside burrows (Roberson et al. 1985; Turner
et al. 1986; Agha et al. 2013 and references therein),
where predation risk to defending females might be
limited because large predators cannot enter narrow
burrows.
.—Our observations
suggest that, in addition to abiotic factors (Landers et
al. 1980; Diemer and Moore 1993; Smith 1995; Lamb
et al. 2013), conspecic interactions may directly or
indirectly inuence where individual females nest.
In our study population, approximately one-quarter
to one-half of adult-sized tortoise burrows are used
by an adult tortoise at any given time (Burke 1989;
Guyer et al. 2012), and tortoises spend virtually all of
their nighttime hours and nearly all of their daytime
hours at burrows (unpubl. data). In each of the three
instances where we documented a female attempting
to nest in the presence of a conspecic, the female
abandoned the attempt. It is likely more dicult
for a female to nest at a burrow occupied by an adult
conspecic because as our observations of tortoise
interactions indicate, if the burrow contains a female,
she may be may be aggressively pushed or rammed, or
if it is occupied by a male, she may be aggressively bit
and/or mounted (Douglass 1986; Johnson et al. 2007;
Guyer et al. 2014; this study). Even if she manages
to oviposit, her eggs could be inadvertently trampled
and broken during interactions with the conspecic.
Any of these possibilities could explain why females
abandoned nesting attempts following interactions with
conspecics.
To adversely inuence reproductive success
or ospring phenotype, conspecic constraints on
nesting activity must aect nest characteristics such as
depredation risk or incubation conditions. Although
Gopher Tortoise nests at our site exhibit substantial
variation in hatching success (0–100%) and oviposition-
to-hatchling emergence times (96–128 d; Radzio et al.
2017), potentially reecting underlying variation in
incubation conditions, our data do not assess whether
social interactions aect reproductive outcomes.
However, our observations do suggest that, if Gopher
Tortoises exhibit nest site philopatry, it could be
somewhat obscured by conspecic constraints on where
females nest.
We document apparent burrow competition
involving gravid female tortoises, avoidance responses
by nesting females to male and female conspecics, and
other social interactions outside of nesting in an old-
growth Longleaf Pine forest that suggest movements
and nest-site choices of female Gopher Tortoises may
be inuenced by conspecic interactions. Old-growth
Longleaf Pine forest is hypothesized to be one of the
primary ancestral habitats of Gopher Tortoises (Guyer
and Herman 1997), but Gopher Tortoises inhabit a
variety of environments, including less productive
Longleaf Pine ecosystems and barrier islands where
ground cover is less dense. At a site characterized by
many unvegetated areas, Smith (1995) documented
extensive nesting activity by Gopher Tortoises away
from, but very little at, burrow aprons. Therefore, our
observations may serve as a reference for how social
interactions inuence the nesting ecology of Gopher
Tortoises in a portion of their natural environment,
particularly where tortoises occur in high densities and
nest extensively on burrow aprons.
381
Acknowledgments.—We thank Jaci Smolinsky
and Brent Mills for valuable assistance in the eld.
Tim Mok helped process the video data. Maryann
Fitzpatrick and Wolfgang Nadler graciously shared their
expertise on a variety of technical topics. This work
was funded by a graduate teaching assistantship and a
McLean Fellowship in Ornithology and Environmental
Science from the Department of Biodiversity, Earth, and
Environmental Science at Drexel University. The Wade
Tract Research Fund, Chicago Herpetological Society,
Minnesota Herpetological Society, Western Digital
Foundation, Biology Department at Drexel University,
National Aeronautical and Space Administration, and
Betz Chair Endowment in Environmental Science at
Drexel University provided funding and/or equipment
used in this study. We thank Paddy Wade, the Wade
Family, and the entire sta of Arcadia Plantation,
including Paul Massey, for allowing access to their
property and for their ongoing support of research at the
site. This work was conducted in accordance with the
Drexel University Institutional Animal Care and Use
Committee (protocol number: 19661) and the Georgia
Department of Natural Resources (permit number:
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Herpetological Conservation and Biology
is a Ph.D. candidate within the Department
of Biodiversity, Earth, and Environmental Science at Drexel
University. Much of his current research investigates various
aspects of the thermal ecology of juvenile Gopher Tortoises.
(Photographed by Jaclyn Smolinsky).
heads up the Stoddard Bird Lab at Tall Timbers
Research Station and Land Conservancy. The lab studies
relationships between controlled res and the habitat needs of the
many declining species associated with southern pine forests. The
Lab also is engaged in land conservation eorts that make use of
special programs designed to conserve habitat for rare species on
private lands. Prior to this, Cox worked statewide conservation
recommendations for several rare and imperiled species found in
Florida, including the gopher tortoise. (Photographer unknown).
is an Associate Professor in the
Department of Biodiversity, Earth, and Environmental Science
at Drexel University. His research tends to focus on abiotic
and physiological constraints on the activity and ecology of
(predominantly terrestrial) ectotherms. (Photographed by Tom
Radzio).
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1986. Egg production by the Desert Tortoise
(Gopherus agassizii) in California. Herpetologica
42:93–104.
Wilson, D.S. 1998. Nest-site selection: Microhabitat
variation and its eects on the survival of turtle
embryos. Ecology 79:1884–1892.
