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Graduate School Form 9(Revised 10107)
PURDUE UNIVERSITYGRADUATE SCHOOL
ThesislDissertation Acceptance
This is to certify that the thesis/dissertation prepared
By Andrea F. Currylow
Entitled Effects of Forest Management on the Ecology and Behavior of Eastern Box Turtles
For the degree of Master of Science
is not to be regarded as confidential.
To the best ofmy knowledge and as understood by the student in the Research Integrity andCopyright Disclaimer (Graduate School Form 20), this thesis/dissertation adheres to the provisions ofPurdue University's "Policy on Integrity in Research" and the use ofcoX
~ //"orp~,--D is
This thesis [Z]Major Professor
-~~2h~~:;::::==--- or --::---c::--:-::--,..,....,..---xamining Committee Department Thesis Fonnat Advisor
EFFECTS OF FOREST MANAGEMENT ON THE ECOLOGY AND BEHAVIOR OF
EASTERN BOX TURTLES
A Thesis
Submitted to the Faculty
of
Purdue University
by
Andrea F. Currylow
In Partial Fulfillment of the
Requirements for the Degree
of
Master of Science
May 2011
Purdue University
West Lafayette, Indiana
ii
ACKNOWLEDGEMENTS
I thank my graduate committee, Dr. Patrick Zollner and Brian MacGowan, for
considerate direction both in the field and academically as well as offering many detailed
and helpful reviews of manuscripts. I especially thank Dr. Rod Williams, my major
advisor, for affording me the opportunity to work on and develop this project. He has
also been gracious enough to support my pursuits of additional projects stemming from
this one. I am grateful to him for being so thoughtful and helpful as an advisor and
sometimes, a therapist. I would also like to thank the graduate students in PFEN G004
who through sharing office space and coffee breaks, offered help through every issue and
all the questions, but most importantly, offered friendship. For all this, I will always be
grateful.
I would like to thank my loving parents, Gary and Fran Curry, who have always been
there for me with support and inspiration. My fiancée, Michael Tift, deserves many
thanks for enduring the struggles with me as we both undertook the challenges of
graduate school nearly an entire continent apart.
Finally, I would like to thank the changing members of Williams’ lab group and
multitude of field technicians who, without them, none of this could have been possible.
Thank you for your hard work and, for many of you, your friendship.
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TABLE OF CONTENTS
Page
LIST OF TABLES ...............................................................................................................v
LIST OF FIGURES ........................................................................................................... vi
ABSTRACT ..................................................................................................................... viii
CHAPTER 1: SHORT-TERM FOREST MANAGEMENT EFFECTS ON A LONG-LIVED ECTOTHERM ....................................................................................................1
Abstract .......................................................................................................................1 Introduction .................................................................................................................2 Methods.......................................................................................................................4
Study Area ............................................................................................................4 Forest Management Design and Sampling ...........................................................4 Landscape-Scale Analyses ....................................................................................6 Local-Scale Analyses ............................................................................................8
Results .........................................................................................................................9 Landscape-Scale Effects .......................................................................................9 Local-Scale Effects .............................................................................................11
Discussion .................................................................................................................12 Landscape-Scale Effects – home ranges and thermal ecology ...........................13 Local-Scale Effects – movement and edge effects .............................................15 Conservation Implications ..................................................................................17
Acknowledgements ...................................................................................................17 Literature Cited .........................................................................................................19 Appendix 1 ................................................................................................................35
CHAPTER 2: HIBERNAL THERMAL ECOLOGY OF EASTERN BOX TURTLES WITHIN A MANAGED FOREST LANDSCAPE .......................................................36
Abstract .....................................................................................................................36 Introduction ...............................................................................................................37
Study Area ..........................................................................................................39 Methods.....................................................................................................................40
Turtle Monitoring................................................................................................40 Experimental Design and Habitat Monitoring ....................................................40
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Page Analyses ..............................................................................................................41
Results .......................................................................................................................42 Box Turtle Thermal Behavior .............................................................................43 Microclimates of Forests vs. Clearcuts ...............................................................45
Discussion .................................................................................................................46 Management Implications ...................................................................................50
Acknowledgements ...................................................................................................50 Literature Cited .........................................................................................................51 Appendix 2 ................................................................................................................63 Appendix 3 ................................................................................................................65 Appendix 4 ................................................................................................................68
PUBLICATION .................................................................................................................70
v
LIST OF TABLES
Table Page
Table 1. Pre-harvest (Pre-harv.; 2007-2008) and post-harvest (Post-harv.; 2009-2010) home ranges of female and male Eastern Box Turtles. The associated management class (Mngmnt Class) is listed and home ranges were calculated by biennial Minimum Convex Polygons (MCP) and 95% kernel isopleths. Only the 95% kernel isopleths areas are listed here, as they are the only relevant comparisons to 100% MCP. ................................................................................................................27
Table 2. Least Squares Means (LS Mean) Tukey-Kramer post-hoc pairwise comparisons connecting letters report of monthly environmental temperatures (Tmin, Tmax, Tmean) during 2009-2010 within four habitat types (clearcut openings, group selection openings, harvest-adjacent forest, and forested control). Habitat types at each level not connected by the same letter are significantly different. .....................................................................................................................28
Table 3. Published studies involving home range estimates from native populations of T. carolina. .................................................................................................................33
Table 4. Number and location of temperature dataloggers in harvest openings (H) and forested habitats (F). Slope aspect (NW, SE, etc.) represents the slope for which the logger was assigned or that the overwintering turtle chose. .................................56
Table 5. Mean body temperatures (Tb) and standard errors for all turtles at hibernation (Hib) and emergence (Emerg). “Unknown” slopes indicate turtles did not select hibernacula by the final tracking date. The 12 turtles associated with hibernaculum Thermal Profile Stakes. ..............................................................................................57
Table 6. Mean Thermal Profile Stake temperatures (°C) and standard error from all depths combined during hibernation and emergence thermal periods. Temperatures are separated by habitat types (forests, hibernacula, and clearcuts) and by slope aspects. Starred (*) values are significantly different (P < 0.05 and Δ°C > 1) from each other/others across habitat types for associated thermal period and slope aspect. Total mean values are reported for each habitat type at the bottom of the table. .....................................................................................................58
vi
LIST OF FIGURES
Figure Page
Figure 1. Regional and local map of the study area in south-central Indiana. a) The location of the study area in Indiana relative to the continental US. b) The nine study sites spanning Morgan, Monroe, and Brown Counties in IN. Polygon colors represent management classes (clearcuts = medium grey, group selections = dark, controls = light) ..........................................................................................................26
Figure 2. Scatter plot of daily distances traveled by Eastern Box Turtles (steplengths; y-axes) by ground temperature (Tg in °C; x-axes). All 2007-10 steplengths in meters per day by ground temperature (a.) and the log-transformed steplength by ground temperature (b.). Pre-harvest (2007-08) steplength in meters per day by ground temperature (c.) and post-harvest (2009-10; d.). Plots show 95% (black ellipse) and 50% (grey ellipse) density ellipses around points and histogram densities along plot boarders. Darkened areas represent the peak of activity temperatures (22-26°C; thermal optimum) in these data. ..........................................29
Figure 3. Average steplength (m/day) moved by Eastern Box Turtles each month for both harvest periods (pre-harvest [2007-08] and post-harvest [2009-10]; bars). The average ground temperatures (Tg; °C) recorded at turtle location each harvest period are also plotted (lines). ....................................................................................30
Figure 4. Mean monthly temperature maxima (Tmax), mean (Tmean), and minima (Tmin) over two years (2009-2010) by habitat type (clearcut openings, group selection openings, harvest-adjacent forest (Harv. Adjacent), and forested control) (a). Maxima, means, and minima monthly Eastern Box Turtle body temperatures (Tb) for the same period (b). ......................................................................................31
Figure 5. Mean Eastern Box Turtle body temperatures (Tb) in degree Celsius (C) with relation to timber harvest proximity over the active season months for post-harvest years (2009-10 combined). Starred bars represent significantly different mean temperatures during that month. .................................................................................32
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Figure Page
Figure 6. Study Site Map. Map of Indiana with study area in Morgan, Monroe, and Brown Counties outlined (inset) and the six study sites (3 clearcut treatment sites and 3 control sites) as part of the Hardwood Ecosystem Experiment in south-central Indiana. All radiotelemetered turtle hibernacula are indicated as dark dots. 59
Figure 7. TPS Setup and Arrangement. Schematic of thermal profile stakes (TPS) with temperature loggers affixed at 10-cm increments (not to scale). The TPS recorded the microclimate through the hibernal season (hibernation and emergence periods). Temperatures collected from temperature loggers at each depth were matched to turtle temperatures (Tb) in order to inform the depth to which turtles hibernated and when they emerged (verified by radiotelemetry) (a). A subset of TPS and turtle hibernacula physical locations with relation to the management types (clearcut treatment and control) (b). ..........................................................................................60
Figure 8. Hibernation Temperatures. Mean hibernacula temperatures recorded by week at various depths (+10, 0, -10, -20, &-30) and mean turtle body temperatures. Figure illustrates the point of inversion (between 23 February and 7 Mar 2010), demarcating the hibernation period (weeks 2 through 17) and emergence period (weeks 18 through 22). See text for details and further description. .........................61
Figure 9. Habitat Temperatures by Depth. Mean location TPS temperatures (°C) by depth (centimeters) during the hibernation and emergence periods. Temperatures found at hibernacula and forests were not significantly different at varying depths. However, temperatures found in treatments were significantly colder (hibernation period) or warmer (emergence period) at nearly all depths. ......................................62
viii
ABSTRACT
Currylow, Andrea F. M.S., Purdue University, May 2011. Effects of Forest Management on the Ecology and Behavior of Eastern Box Turtles. Major Professor: Rod N. Williams.
Declines in long-lived and geographically widespread forest animals, such as the case
with Eastern Box Turtles (Terrapene carolina carolina), warrants investigation. Despite
declines, this species’ ability to endure in a range of available habitat and its
physiological ties to environmental flux make it ideal for study of habitat use and
selection amid anthropogenic disturbances. For my thesis work, I focused on
investigating the ecology and behavior of Eastern Box Turtles following timber harvests.
As part of the Hardwood Ecosystem Experiment, I used nine experimental forest
management sites to investigate the effects of clearcut harvest openings and group
selection harvest openings on box turtles. I used standard homing radiotelemetry to
collect GPS location, morphometric, temperature, and behavior data on 50 adult Eastern
Box Turtles. I conducted the majority of this work during the active seasons (May –
October) but during the winter of 2010 I investigated the hibernal thermal ecology within
clearcut harvest openings. Combined with the radiotelemetry data previously collected
on these turtles from 2007-08, I was able to measure the effects of the harvests by
analyses of movement parameters and temperatures. I found that timber harvests had no
effect on the typical measurement of home range size, 100% Minimum Convex Polygons
(MCP), however the MCPs here are 33% larger than any other published report for this
species. Additionally, I found that turtles decreased the daily distances they traveled by
approximately 30%, but their thermal optima increased by 8% following the harvests.
Microclimates inside the timber harvests were significantly warmer (29%) in the summer
and colder (31%) in the winter than forested habitats, effectively excluding many animals
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from consistently using them. Instead of leaving the harvested areas, however, turtles
continued to use them differently. During the active season, box turtles used the edges of
harvest areas apparently for behavioral thermoregulation and possibly for foraging.
Turtles that used the harvest areas maintained 9% higher body temperatures during the
active season than those that did not. During the winter, turtles generally burrowed to 10
cm for overwintering, but depth varied by slope and gender. I found that the depth
influenced the emergence timing, which was also correlated with a soil-surface
temperature inversion. A single female turtle that hibernated in a group-selection harvest
opening had an estimated burrowing depth of nearly 30 cm to maintain her hibernal body
temperature. Moreover, I estimated the annual survival rate (96.2%) of box turtles in our
population, the first for the Midwest.
The investigation of ecological mechanisms underlying species declines has become
paramount in conservation literature. Simply reporting the extirpation of populations
without testing mechanistic causes does little to promote conservation management.
Herein, I investigated temporal thermal habitat availability, habitat use, thermal behavior,
survival, and intersexual differences among Eastern Box Turtles within the framework of
a managed forest setting.
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CHAPTER 1: SHORT-TERM FOREST MANAGEMENT EFFECTS ON A LONG-
LIVED ECTOTHERM
Abstract
Timber harvesting has been shown to have both positive and negative effects on
forest dwelling species. I examined the immediate effects of timber harvests (clearcuts
and group selection openings) on ectotherm behavior, using the Eastern Box Turtle as a
model. I monitored the movement and thermal ecology of 50 adult box turtles using
radiotelemetry from May-October for two years prior to, and two years following
scheduled timber harvests in the Central Hardwoods Region of the U.S. Box turtle
annual home ranges (7.45 ha, 100% MCP) did not differ in any year or in response to
timber harvests, but were 33% larger than previous estimates (range 0.47-187.67 ha).
Distance of daily movements decreased post-harvest (from 22 m ± 1.2 m to 15 m ± 0.9
m) whereas thermal optima increased (from 23 ± 1°C to 25 ± 1°C). Microclimatic
conditions varied by habitat type, but monthly average temperatures were warmer in
harvested areas by as much as 13°C. Turtles that used harvest openings were exposed to
extreme monthly average temperatures (~40°C). As a result, turtles made shorter and
more frequent movements in and out of the harvest areas while maintaining 9% higher
body temperatures.. This experimental design coupled with radiotelemetry and
behavioral observation of a wild ectothermic population prior to and in response to
anthropogenic habitat alteration is the first of its kind. Our results indicate that in a
relatively contiguous forested landscape, small-scale timber harvests have modest effects
on the short-term behavior of box turtles. Ultimately, the results of this research can
benefit the conservation and management of temperature-dependent species by informing
effects of timber management across landscapes.
2
Introduction
Study of habitat alteration through direct and indirect anthropogenic episodes such as
reduction of forest habitats and changing climate is becoming increasingly frequent. The
understanding of how these changes affect the physiology and behavior of native fauna is
vital to the preservation of diversity. Timber harvesting is likely one of the most
prominent land uses affecting forest wildlife (Peterman & Semlitsch 2009). Forest
management practices change the vegetative structure and local temperature, which may
affect community structure and function (Renken et al. 2004). Environmental flux also
has a greater effect on movements and behavior of poikilotherms than for homeothermic
species (Allard 1935; Bayless 1984). In response, timber harvests have been implicated
as a possible cause for worldwide herpetofaunal declines (Gibbons et al. 2000; Pechmann
et al. 1991; Wake 1991). As a result, management of our eastern hardwood forests has
become a balancing act between timber production and ecological conservation.
While some data suggest that heavily logged areas are associated with moderate
increases in bird and reptile diversity (Fredericksen et al. 2000), it is not clear whether
this can be considered a general trend for all taxa. Timber harvesting has the potential to
affect multiple facets of how ectotherms utilize available habitat both directly and
indirectly. Canopy openings may create basking sites or allow herbaceous mass to
flourish and provide basilar food sources (Perison et al. 1997). Edge effects of openings
and access roads have been shown to influence habitat resources into the forest interior at
varying distances (Cadenasso & Pickett 2001; Delgado García et al. 2007; Donovan et al.
1997). Because variation in resources such as vegetation and invertebrate prey occur,
daily movements and annual home range sizes may readily expand, contract, or shift in
response to this variation. Moreover, the behavior, physiology, and even fitness of
ectotherms are strongly affected by temperature fluctuations (Cunnington et al. 2009;
Huey & Kingsolver 1989). Temperature dictates ectothermic habitat use based on the
animals thermal optima (i.e., the temperature at which movement activity is maximal;
Huey & Kingsolver 1989) which in turn alters behavior (Bradshaw & Holzapfel 2007;
Fox et al. 2003).
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Recent attempts to assess the effects of timber harvests on many ectothermic species
often suffer from the lack of replication or comparable pre-harvest data (e.g. Goldstein et
al. 2005; McLeod & Gates 1998). Furthermore, the majority of these herpetofaunal
studies have focused on the harvest effects on amphibian populations (e.g. Hocking &
Semlitsch 2008; Peterman & Semlitsch 2009; Rittenhouse & Semlitsch 2009;
Rittenhouse et al. 2009; Semlitsch et al. 2009), while relatively little is known about the
impacts on reptile populations. However, the existing data suggest reptiles are not only
sensitive to habitat perturbations, but that the impacts are more pervasive and severe than
for amphibians (Gibbons et al. 2000). Negative impacts to reproductive adult reptiles,
such as long-lived, K-selected turtles, can devastate entire populations (Brooks et al.
1991; Gibbs & Shriver 2002). Box turtles, which are among the longest lived of all
reptiles, are geographically widespread throughout the eastern forests, yet they are
sensitive to environmental disturbances that affect local habitat features (Currylow et al.
2011; Dodd 2001; MacGowan et al. 2004). Widespread population declines have
sparked interest in the conservation of this species. While basic data exist on the habitat
requirements of box turtles, many studies were conducted at a single location and did not
empirically assess responses to changing habitat or microenvironmental conditions.
The investigation of ecological mechanisms underlying species declines has become
paramount in conservation literature. Simply reporting the extirpation of populations
without testing mechanistic causes does little to promote conservation management.
Herein, I investigated temporal thermal habitat availability, habitat use, thermal behavior,
and intersexual differences among Eastern Box Turtles (Terrapene carolina carolina)
within the framework of a managed forest setting. The overarching goals of this study
were to examine ectothermic response to timber harvesting at both the landscape and
local scales. At the landscape scale, our specific goals were to assess effects of various
timber harvest regimes on habitat use, thermal environments, and turtle thermal ecology.
At the local level, our specific goals were to investigate edge effects of timber harvests on
box turtle thermoregulatory behavior, movement metrics (frequency of movement and
steplength), and observed behavior.
4
Methods
Study Area
The research was conducted within approximately 35,000 hectares of Morgan-
Monroe State Forest (MMSF) and Yellowwood State Forest (YSF) in Morgan, Monroe,
and Brown Counties, Indiana (Figure 1a). From the years 1860 through 1910, the
forestland was characterized by routine burning and cutting for cattle grazing. At the turn
of the 20th century, the state of Indiana began purchasing the land and establishing these
State Forests. Now, MMSF and YSF boundaries are shared, forming a relatively
contiguous forested habitat characterized by hills and ravines of hardwood, deciduous
forests with scattered gravel access roads. This is an oak-hickory dominated forest, with
the majority of canopy species being Quercus spp., such as Q. montnana (chestnut oak),
and Carya cordiformis and C. ovata (butternut and shagbark hickory; Summerville et al.
2009). These State Forests are managed for multiple-uses including recreation,
education, research, and timber harvesting.
Forest Management Design and Sampling
Our research is part a long-term (100-yr), landscape-scale (spanning 31 linear
kilometers and 3,601 hectares) timber and wildlife research collaborative designed for the
study of ecological and social impacts of various silvicultural methods typically
employed in the Midwest (Hardwood Ecosystem Experiment). In 2007, I identified nine
study sites of approximately 400-ha, each assigned to one of three forest management
classes in a randomized complete block design (Figure 1b). The management classes
included two 2.72 – 4.43-ha clearcuts, eight 0.15 – 2.55-ha group selection openings, and
forested controls. The timber harvests were implemented on equal numbers of
southwest- and northeast-facing slopes over the winter of 2008-09 within the center 90-ha
of each study site. The remaining 300+ hectares at each site remained intact to serve as
refugia and maintain species diversity.
To determine the effects of timber harvests on T. c. carolina, I collected GPS location
and habitat use data before timber harvests (pre-harvest; 2007-08) and after harvests
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(post-harvest; 2009-10). I initially located adult box turtles by meandering-transect
visual encounter surveys. Upon capture, I assigned a unique ID number and marked each
turtle using a triangle file along the marginal scutes following a modified Cagle scheme
(Cagle 1939; Ernst et al. 1974; Ferner 2007), recorded morphometrics, and affixed a
transmitter (model RI-2B Holohil Systems, Ltd., Ontario, Canada) to the carapace.
Where possible, sex ratios and numbers of turtles were equally divided among sites and
management classes. I subsequently radio-tracked (homing) turtles 2-3 times per week
during the active seasons (May through October). For each tracked location, I recorded
GPS coordinates, date, ground temperature, elevation, and during the post-harvest years I
also recorded observed activity classifications (resting, eating, mating, basking, walking,
etc.).
To monitor the thermoregulatory behavior of turtles post-harvest, I affixed iButton
temperature dataloggers (model DS1921G-F5#, Maxim Integrated Products, Inc.,
Sunnyvale, CA) to the carapace of each of the tracked turtles in May 2009. Since
carapacial temperature measurements have been shown to correlate well with deep body
temperatures (Bernstein & Black 2005; Congdon et al. 1989; do Amaral et al. 2002;
Peterson 1987), I used the dataloggers to represent each turtle’s body temperature (Tb).
Temperature datalogger and transmitter weight combined was usually no more than 5%
(max 20 g) of the animal’s total body weight. Dataloggers recorded temperatures every
45 minutes during the active season (May-October).
To assess the available thermal habitats in harvest areas versus uncut forests, I
measured ambient temperature using temperature dataloggers affixed to stakes, 10 cm
from soil surface (at approximately T. c. carolina carapace height). I randomly placed
these ‘environmental dataloggers’ at four sample locations within each of the nine study
sites for a total of 36 individual thermal locations. In each clearcut management site, two
environmental dataloggers were randomly deployed inside clearcuts and two in the
adjacent forests (between 100 m and 500 m from the nearest harvest edge; harvest-
adjacent forest). In each group selection management site, four dataloggers were
randomly deployed inside harvest openings. In each control site, four dataloggers were
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randomly deployed in forested habitats. This blocked design resulted in equal numbers
of environmental dataloggers inside harvest openings (n=18) and in forested areas (n=18)
representing the four habitat types (clearcut opening, group selection opening, harvest-
adjacent forest, and forested control). To eliminate the effect of slope aspect on
temperature logged, I used equal numbers of southwest- and northeast -facing slopes. I
deployed all temperature loggers from May 2009 to October 2010 for a total of 75 weeks.
I programmed dataloggers to record temperatures every 45 minutes to match the
carapacial dataloggers described above.
Landscape-Scale Analyses
Home range estimation
I used multiple analyses to examine how various timber-harvesting regimes affect
behavior at landscape- and local-scales. To describe landscape-scale effects of timber
harvests on box turtles, I used all turtle location data across all nine study sites throughout
the forested landscape. To characterize spatial land use in our population of box turtles, I
created a point layer in ArcGIS 9 (version 9.3.1; ESRI 2009) using the GPS location data
and calculated 100% Minimum Convex Polygons (MCP) with the Hawth’s Analysis
Tools extension (Beyer 2004) for each turtle in each year, thus creating annual MCP
home ranges. I standardized all annual MCP home ranges by the number of GPS
locations and log-transformed them for normality.
I used a generalized linear mixed model to test annual MCP home ranges for
differences among sites using a crossover design and the PROC GLMMIX command in
SAS (SAS Institute Inc. 2007) with a first-order autoregressive covariance structure. I
compared all the pre-harvest data then “crossed over” to the post-harvest control
comparisons. In my initial model, site, year, and the interaction of site and year were
fixed effects and turtle ID nested in site was a random effect. By analyzing data in this
cross-over fashion, I could verify that control sites were representative of pre-harvest
conditions (i.e., site explained very little variation). I grouped sites by management class
(clearcut, group selection, and control) for all subsequent analyses and evaluated their
7
effects in the pre- and post-harvest data using a full factorial generalized linear mixed
model (GLMM) with unbounded variance components in JMP (SAS Institute Inc. 2008).
I used year, sex, management class, and their interactions as fixed effects and turtle ID
nested in year as a random effect (to account for repeated measures of individual turtles)
to find any differences in annual MCP home ranges with relation to harvests. To detect
significant differences across effect levels, I used post-hoc Least Squares Means
(LSMeans) Tukey-Kramer pairwise comparisons, which adjusts significance for multiple
comparisons.
Year-to-year variation in movements and habitat use is common (often due to
variation in resources such as vegetation and invertebrate prey; Dodd 2001; Schwartz et
al. 1984; Stickel 1989), therefore I used biennial (two-year) intervals as indices of longer-
term home range sizes and core use areas. These biennial intervals corresponded to the
two pre-harvest years and two post-harvest years (hereafter “harvest periods”). To assess
differential habitat utilization due to timber harvests, I used biennial MCPs and kernel
estimates (ArcGIS Home Range Tools [HRT] extension; Rodgers et al. 2005) for each
turtle between harvest periods. I chose to use kernel estimates for further comparisons to
other habitat use studies (Worton 1989) but also continued to calculate MCPs because it
has been argued they they better represent herpetofaunal habitat use (Row & Blouin-
Demers 2006). I calculated 50-, 90-, and 95-percent kernel isopleths (percent volume
contour) of utilization distributions using the fixed kernel method with least squares cross
validation (LSCV) for pre- and post-harvest. For both biennial MCP and kernels, I used
a GLMM to test for differences in pre- and post-harvest area measurements (log-
transformed) caused by the fixed effect of harvest period (with turtle ID nested as a
random effect to control for re-sampling error).
Movement and thermal ecology
Turtles may not only adjust their annual home ranges in response to harvests, but vary
their movement activity (i.e. move farther distances within their home range or move
more frequently). For this analysis, I calculated the Euclidian distance between GPS
locations for each turtle in ArcGIS using the HRT extension then calculated steplength
8
(average estimated distances by day). To test whether harvest period had an effect on
steplength, I log-transformed these data and fitted a full factorial unbounded GLMM with
harvest period, sex, management class, and their interactions as fixed effects and turtle ID
nested in harvest period as a random effect. Then to examine the thermal ecology of T. c.
carolina in relation to the timber harvests, I tested for correlation between the log-
transformed steplength data and ground temperature (Tg; recorded when turtles were
radio-located). I also used these data to find the thermal optima (the temperature at
which movement activity is maximal) across harvest periods.
Thermal habitats
To test for changes in available thermal habitat, I used differences in ambient
temperature among habitat types within sites. I summarized the temperature time series
data from each of the 36 environmental dataloggers into three variables - monthly
temperature maxima (Tmax), monthly temperature minima (Tmin), and monthly
temperature mean (Tmean) using R (R Development Core Team 2009). I used unbounded
GLMM in JMP to test for significant Tmin, Tmax, and Tmean differences caused by habitat
type, month, and their interaction as fixed effects and individual datalogger ID nested in
month as the random effect. I used LSMeans Tukey-Kramer post-hoc comparisons to
detect significant differences in Tmin, Tmax, and Tmean between months.
Local-Scale Analyses
To determine the thermal effects of harvests on box turtle behavior, I first
characterized the thermoregulatory behavior of our entire population. I examined the
max, mean, and min Tb to find the range of selected temperatures for each month. I
correlated observed behavior at the time of each GPS location in relation to Tb. I used a
GLMM to investigate turtle body temperature (Tb) differences explained by the fixed
effect of observed behavior category with the random effect of turtle ID nested in
behavior. Behavior categories included basking, eating, mating, resting, inverted (found
upside-down), walking, and buried.
9
To investigate local-scale harvest edge use and activity, I examined the actual harvest
openings and their associated edges in combination with GPS location data. I then
created 10- and 50-meter polygon buffers around the harvest boundaries using ArcGIS
Analysis Tools. I tested for differences in the percent of turtle locations within these
three harvest-polygons (inside harvest, 10 m buffer, and within the 50 m buffer) across
harvest periods, again controlling for individual effects using an unbounded GLMM as
described above. I conducted a similar analysis using the Euclidian distances turtles
moved within these harvest-polygons to test for differences in activity (frequency of
movement or daily distance moved).
To determine the edge effects for thermoregulation, I compared Tb of turtles using the
harvests and their edges to the Tb of those same turtles when they were located in the
forests. To investigate edge effects on turtle movement activity, I used Tb to describe the
available thermal habitats in various harvest-polygons. I analyzed harvest edge effects by
categorizing harvest proximity polygons (as above) by inside the harvest, 10 m buffer,
and 50 m buffer from the nearest harvest opening. I also explored Tb within harvest-
polygons by using Tb as the response variable and distance to harvest and month as the
fixed effects. I used unbounded GLMMs and controlled for repeated measures using
turtle ID nested in harvest-polygons as a random effect in each model. Post-hoc
LSMeans Tukey-Kramer pairwise comparisons was performed to detect significant
differences.
Results
Landscape-Scale Effects
I radio-tracked 23-44 T. c. carolina each year (average = 33.5/year), carrying over all
that survived each year and were not lost or censored. Losses due to transmitter failure
were rare (n = 1). Two turtles were separated from their transmitters and censored. Five
turtles died of various causes including predation (n = 1), severe emaciation (n = 1),
suspected disease (n = 2), or failure to emerge from hibernacula (n = 1). Home range
MCPs for the remaining turtles (n = 50; 23♂, 27♀) with > 20 locations per year (avg. =
10
57.34, SD = 19.10, range = 14-79) were calculated for each year and are summarized in
Appendix 1.
I found no difference (P-value = 0.418) in the overall size of T. c. carolina annual
MCP home ranges between all pre-harvest sites and control post-harvest sites, verifying
our experiment used true controls. Annual MCP home ranges (4.10 ha to 11.43 ha) did
not differ among sex, year (2007-10), management class, or any combination of these
factors (all P-values > 0.07). The annual minimum and maximum home range sizes were
0.47 ha and 187.67 ha, respectively. The average MCP for all four years was 9.14 ha for
males and 5.55 ha for females.
Pre-harvest biennial MCP home ranges (18.93 ha, SE = 7.51) were generally larger
than post-harvest (9.09 ha SE = 5.75; Table 1), however, this difference was not
significant (F1, 2.435 = 0.018, P = 0.90). There was much variation in kernel areas by sex
and harvest period (Table 1) For all three kernel isopleths (50-, 90-, and 95%), the home
range areas increased from pre-harvest to post-harvest (all P-values < 0.05). No variation
in biennial home range area was attributed to harvest type (clearcut or group selection) or
sex (all P-values > 0.29).
Movements and thermal ecology
Steplength decreased from pre-harvest to post-harvest (F1, 66.2 = 33.96, P < 0.001) but
there were no differences (all P-values > 0.13) by sex, management class, or any
combination of the three. The percent of steplengths that equaled zero (the percent of
time the turtles did not change position between GPS locations) was 1.83% pre-harvest
and 0.86% post-harvest, meaning the turtles moved more often post-harvest. Steplength
was positively and significantly correlated with ground temperature (R2 = 0.16, P <
0.001; Figure 2a & b). Thermal optimum was found at 22-24°C pre-harvest (Figure 2c)
and 24-26°C post-harvest (Figure 2d). Average steplength during the pre-harvest period
was 22.08 meters (SE = 1.21) and 15.40 meters (SE = 0.88) during the post-harvest
period, with the height of activity varying by month (Figure 3). The thermal optima were
22-24°C during the pre-harvest period and between 24-26°C post-harvest despite the fact
11
that ground temperatures were higher pre-harvest (mean = 24.5°C) than post-harvest
(mean = 22.7°C; F1, 7315 = 140.8, P < 0.001).
Thermal habitats
I processed 388,974 environmental temperatures from 36 locations in four habitat
types (clearcut opening, group selection opening, harvest-adjacent forest, and forested
control) between May 2009 and October 2010. Available temperatures differed at each
level (Tmax, Tmean, and Tmin) for each habitat type, month, and habitat by month
interaction. The interaction term for Tmin was the only non-significant effect (F33, 376.6 =
0.959, P = 0.54) in the model. The strength of the effects varied by month, with the
harvest habitat types (clearcut and group selection openings) more similar to one another
and forested habitat types (harvest-adjacent forest and forested controls) more similar
(Table 2). Habitat type affected Tmax more strongly than others. Explicitly, the range of
temperatures for Tmax was broader between habitats than for Tmin or Tmean especially
during the active period (Figure 4a). Between March and October, Tmax in both harvest
habitat types were significantly warmer (>10°C) than forested habitats (forests Tmax =
24.57°C, SE = 0.73; harvest Tmax = 34.43°C, SE = 0.80; F1, 40.25 = 83.56, P < 0.001). This
difference was most extreme in August when the Tmax in harvest areas averaged 39.98°C
(SE = 0.99) while it was nearly 13°C cooler in forested areas at 27.49°C (SE = 0.88). In
contrast, Tmin and Tmean differences remained within 3°C between habitat types, but
usually less than 2°C for these months.
Local-Scale Effects
I recorded and processed 494,548 body temperatures among 50 turtles between May
2009 and October 2010. The maximum, mean, and minimum Tb varied by month (Figure
4b). Tb was highly correlated with Tg (R2 = 0.71, P < 0.001). Behavioral categories were
correlated with Tb over the post-harvest period, but explained very little of the variation
(R2 = 0.08, P < 0.001). Post-hoc analysis revealed significant Tb differences in basking,
walking, resting, and being underground behaviors. Behaviors associated with higher Tb
(24-27°C) included basking and mating. Behaviors generally associated with lower Tb
(22-23C°) included resting, inverted, walking, and eating, but post-hoc analysis revealed
12
that these were not significantly different than mating. When Tb decreased to an average
of 13.8°C, the turtles were generally buried underground (near the hibernation season).
I found no significant difference in number of turtle locations between the harvest
periods within harvest-polygons. While the pre-harvest Euclidian distances within the
designated harvest boundaries and their edges did not differ from 2007 to 2008, the
averages were significantly different from post-harvest Euclidian distances in each
polygon (F1, 516.5 = 32.45, P < 0.001). Inside the harvest boundaries, post-harvest
Euclidian distances were shorter (11.26 m, SE = 1.66) compared to pre-harvest Euclidian
distances of 22.91 m (SE = 2.83). A similar trend was found within edge polygons where
post-harvest Euclidian distances (14.45 m, SE = 1.27) were smaller than pre-harvest
(23.60 m, SE = 2.10).
Body temperatures did not vary among management classes (F2, 40.72 = 1.624, P =
0.21) but were different among months (F6, 294.7 = 1087.334, P < 0.001; Figure 5).
However, turtles found within the harvest openings maintained 9% higher Tb overall than
those found in the forest/harvest edge or forest interior (F2, 73.24 = 8.135, P < 0.001).
Body temperatures within 50 meters of the harvest edges were lower (21.72°C, SE =
0.35) than farther inside the forest (22.22°C, SE = 0.21) and harvests (23.91°C, SE =
0.44).
Discussion
Recent literature has shown that timber harvesting can have both positive and
negative effects on forest dwelling species. Here I investigated the effect of various
harvest openings on an ectotherm, the Eastern Box Turtle. Using an experimental design
and a variety of approaches, I demonstrate that in a relatively contiguous forested
landscape, timber harvests have little effect on the short-term annual behavior of box
turtles. However, I did detect a behavioral effect at the local scale where available
microenvironmental temperatures are altered. I also offer further evidence that there is
much variation in the annual behavior and home ranges of T. c. carolina that should be
considered when establishing management strategies for forests and this species.
13
Landscape-Scale Effects – home ranges and thermal ecology
Box turtles will preferentially use certain types of available habitats for
thermoregulation, nesting, and aestivation (Madden 1975; Schwartz & Schwartz 1974).
Home range size of this species likely depends on the quality of available food and other
resources within the habitat (Dodd 2001). Annual MCP home ranges for our adult T. c.
carolina ranged from 0.47 and 187.67 hectares, the upper extreme being much larger than
reports from any other study on this species. Indeed, our average annual home range
estimate of 7.45 ha is more than 33% larger than any other published estimates to date
(Table 3; Bayless 1984; Dolbeer 1969; Donaldson & Echternacht 2005; Hallgren-Scaffidi
1986; Nichols 1939; Quinn 2008; Stickel 1989; Strang 1983; Williams & Parker 1987).
It should be noted that there is a large variance in home range estimates across studies,
which is likely associated with study duration, size, and monitoring method. The most
likely explanation for the large home range size reported here is that my study was
conducted within an expansive, relatively contiguous, and undisturbed habitat. Iglay et
al. (2007) found that turtles in fragmented habitats moved less often than those in
contiguous habitats. To this end, many previous studies were conducted within relatively
small and fragmented habitats that likely physically limited home ranges (Table 3).
In this study, I found no differences in either annual or biennial home ranges across
the landscape in association with any of the three management classes (clearcut opening,
group selection opening, or control). This lack of variation was likely due to the fact that
the actual timber harvest openings were relatively small (0.15 – 4.43 ha) in relation to T.
c. carolina home range size and the surrounding contiguous forested habitat. Forest
species often develop different strategies to cope with habitat perturbations. Some
species expand their home ranges in response to forest fragmentation (Hansbauer et al.
2008) while others inhabit territories that contain only small percentages of preferred
habitat or(Andrén 1994). Still other species may gravitate toward mixed-composition
habitat (Andrén 1992). In the current study, the percent of turtle locations within harvest
edges did not change from pre- to post-harvest; suggesting that no such gravitation
occurred. However, the movement parameters I investigated suggested that turtles did
alter their behavior while in proximity to harvest boundaries.
14
In pre-harvest years, turtles tended to move longer distances (i.e., longer steplengths)
than post-harvest years. However, the percent of steplengths that were zero were higher
pre-harvest (1.83% vs. 0.86%). This suggests that although turtles moved shorter
distances and maintained generally smaller home ranges after the harvests were
implemented, they moved more often. These increased short-range movements may be
the result of changes in resources. Turtles in this altered habitat may need to move
frequently for new foraging opportunities as seen with many small mammal and bird
species (Debinski & Holt 2000; Hansbauer et al. 2008). Shorter movements may be a
result of downed slash acting as physical barriers or severe climatic conditions (i.e.,
drought). While it was evident that turtles did reduce movements during drought years,
the cumulative effect on our results is minimal because turtles experienced drought years
during pre-harvest 2007 and post-harvest 2010. Alternatively, behavioral
thermoregulation may explain why turtles regularly moved but remained nearer to the
same locations post-harvest.
Studies of fine-scale temperatures over broad spatial expanses are rare, despite the
fact that temperature is an important factor in the location and activity of species
(Cunnington et al. 2009). A primary effect of the alteration of landscapes is the change in
the microclimate of available habitats (Saunders et al. 1991). I measured these changes
temporally across the landscape using temperature dataloggers. Although there was
annual variation in ambient temperatures, the microclimatic conditions varied
significantly between harvest and forested habitats. The most pronounced period
occurred between May and September for Tmax when differences were often greater than
10°C. These extreme summer temperatures found within harvest areas potentially
exclude many plant and animal species. For example, variation in microclimates has
been shown to affect the germination of emergent herbaceous and woody species
(Breshears et al. 1998). During periods of highest temperatures, Tmax within harvest areas
was often observed to be near the maximum thermal tolerance for most ectotherms
(43°C) effectively reducing the suitability of these areas for T. carolina (34.2°C; Penick
et al. 2002) and other herpetofauna (Blem et al. 1986; Brattstrom 1965; Hutchison et al.
1966; Kroll 1973). Although the current study examines a subset of factors affected by
15
timber harvests, the advantage of this approach is the resulting detailed data of
mechanisms underlying landscape effects (Debinski & Holt 2000). My results suggest
that population-level responses to small-scale timber harvests (which are typical for the
Midwestern U.S.) are minimal.
Local-Scale Effects – movement and edge effects
Ecotones (either natural or man-made) will influence box turtle activity differently
as surface temperature, air temperature, and canopy cover varies across the landscape
(Strang 1983; Weiss 2009). Ecotones at the harvest edges may provide cover by fallen
logs and downed treetops, increased concentration and variety of forage (soft mast plants
and invertebrates), and may facilitate behavioral thermoregulation by providing basking
sites. Although I found no significant difference in the relative number of turtle locations
within the boundary or edges of the harvest areas, I did find differences in the movement
metrics that suggest the turtles use these areas differently. Prior to the harvests, turtles
made longer, scattered movements across would-be harvest areas. Once the harvests
were implemented, the movements across the harvests shortened and were concentrated
along the edges of the harvests. Directed movements, although varied, often would
alternate from the forest to the harvest edge, and frequently would cross logging roads to
do so. Studies on various turtle species have determined that roads bisecting turtle routes
were positively correlated with male biased sex ratios (Gibbs & Shriver 2002; Kipp 2003;
Marchand & Litvaitis 2004; Gibbs & Steen 2005; Steen et al. 2006), population declines
(Shepard et al. 2008), and expanded home range sizes (Nieuwolt 1996). In this study,
two of the sites were bordered by public roads and all sites were adjacent to logging
roads, however, there appeared to be no associations between roads and home ranges.
Anthropogenic effects extend beyond the physical boundary of disturbance. In a
broader definition of habitat, thermal microclimates limit the use of certain areas both
seasonally and spatially. Analyses of the variables that affect ambient temperatures on a
microclimate scale will aide in the understanding of habitat requirements of ectotherms
(Cunnington et al. 2009). In this study, turtles found inside the harvest areas maintained
higher active season body temperatures than those outside the harvests by 10.13%. As
16
expected, basking behavior correlated with higher temperatures. Forested sites located
near roads or open areas such as timber harvests, are found to be generally warmer than
those further away (Cunnington et al. 2009). However, Tb at timber harvest edges were
the lowest during the active period, even lower than in the adjacent forested habitat
suggesting that box turtles were moving between microhabitats for thermoregulation as
seen in other taxa (Adolph 1990; Sepulveda et al. 2008). Turtles within our experimental
openings were exposed to a wide range of temperatures. In a laboratory study, the
specificity of Tb was investigated between T. c. carolina and T. ornata with the finding
that T. c. carolina has less thermal specificity (do Amaral et al. 2002). I routinely found
turtles walking while inside the harvests and document that they do have the ability to
behaviorally adjust to varying temperatures at a fine scale. These adjustments may play
key roles in the physiological requirements of ectotherms throughout ontogeny and in
various physical conditions (e.g., in reptiles, gravid females actively adjust to maintain
higher body temperatures than males; Tozetti et al. 2010).
Open spaces, such as clearcuts, may have less of an effect on larger-bodied species or
those adapted to hot and dry conditions. Canopy cover directly influences light intensity,
which is known to be a critical factor for many reptiles during activity periods (Gould
1957; Rose & Judd 1975; Todd & Andrews 2008). On the other hand, many reptilian
species such as small-bodied snakes are adapted to utilize leaf litter and are likely to be
adversely affected by its removal with associated timber harvests (Todd & Andrews
2008). During the active season, T. c. carolina use leaf litter to create ‘forms’ as cover
(Stickel 1950). T. c. carolina will use these forms throughout the active period as refuge
from the heat, cold, rain, or disturbance (Dodd 2001). In addition to cover, leaf litter
serves as habitat for prey (such as snails, worms, and mushrooms) of box turtles.
Immediately following implementation of harvests, leaf litter is degraded, blown from
these areas, and often leaves large patches of unsuitable bare ground (Enge & Marion
1986). Studies have found that the increased soil temperatures and reduced leaf-litter
cover (which can take decades to return pre-harvest conditions) in previously cut areas
exclude many amphibian species (Crawford & Semlitsch 2008; Petranka et al. 1993). I
found that short term effects such as the loss of leaf litter did not cause box turtles to
17
abandon the area, but rather continue to use it in a different way (such as for
thermoregulation).
Conservation Implications
Merely reporting species declines without determining their mechanistic causes
leaves conservation planners with little recourse. To date, no studies have monitored the
response of an ectotherm’s movement parameters prior to and after discrete
anthropogenic disturbance such as timber harvests. The present study has yielded detailed
data on box turtle habitat use and spatial ecology in a managed forest, but has much
broader implications on multiple forest-dwelling species. In my study, the timber harvest
openings were fairly small (< 5 ha) and were contained in a relatively contiguous and
much larger forest matrix. My results indicate that in a relatively contiguous forested
landscape, small-scale timber harvests have minimal effects on the short-term behavior of
box turtles. However, temperature fluctuations as seen in the current study may affect
seasonal available habitat for other forest-dwelling animals, especially for those with
limited dispersal and thermoregulatory capabilities. Altered microclimates can exclude
animals from harvest areas but also may create desired ecotonal habitats. Considerations
of habitat requirements and contiguity of surrounding refugia habitat and species ability
to recover should be thoroughly considered before timber harvest sizes are determined.
These factors are of particular interest when dealing with long-lived species of
conservation concern.
Acknowledgements
This paper is a contribution of the Hardwood Ecosystem Experiment, a partnership of
the Indiana Department of Natural Resources (IDNR), Purdue University, Ball State
University, Indiana State University, Drake University, and the Nature Conservancy.
Funding for the project was provided by the Indiana Division of Forestry Grant #E-9-6-
A558 and IDNR Division of Fish and Wildlife, Wildlife Diversity Section, State Wildlife
Improvement Grant #E2-08-WDS15. I thank field technicians A. Garcia, A. Hoffman, A.
Krainyk, B. Geboy, B. Johnson, B. Tomson, G. Stephens, H. Powell, J. Faller, J.
MacNeil, K. Creely, K. Lilly, K. Norris, K. Powers, K. Westerman, L. Keener-Eck, L.
18
Woody, M. Baragona, M. Cook, M. Cross, M. Turnquist, M. Wildnauer, N. Burgmeier,
N. Engbrecht, S. Johnson, S. Kimble, S. Ritchie, T. Jedele, and Z. Walker. I also thank
members of the Williams lab group for providing helpful comments on previous versions
of this manuscript. Research activities associated with this project fall under the Purdue
Animal Care and Use Protocols and amendments, PACUC 07-037 and IDNR Scientific
Purposes Licenses 09-0080 & 10-0083.
19
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26
Figure 1. Regional and local map of the study area in south-central Indiana. a) The
location of the study area in Indiana relative to the continental US. b) The nine study
sites spanning Morgan, Monroe, and Brown Counties in IN. Polygon colors represent
management classes (clearcuts = medium grey, group selections = dark, controls = light)
27
Table 1. Pre-harvest (Pre-harv.; 2007-2008) and post-harvest (Post-harv.; 2009-2010)
home ranges of female and male Eastern Box Turtles. The associated management class
(Mngmnt Class) is listed and home ranges were calculated by biennial Minimum Convex
Polygons (MCP) and 95% kernel isopleths. Only the 95% kernel isopleths areas are
listed here, as they are the only relevant comparisons to 100% MCP.
Harvest
Period Sex Mngmnt Class n Biennial MCP Biennial 95% Kernel
Median Mean SE Median Mean SE
Pre-harv. F Clearcut 5 6.80 15.42 10.20 3.57 32.32 28.97
Control 4 3.52 4.54 1.86 3.32 3.37 0.73
GroupSelect 2 10.21 10.21 6.74 4.31 4.31 0.38
M Clearcut 5 2.02 4.63 1.75 2.71 4.34 1.07
Control 4 5.52 83.08 78.41 5.39 14.99 10.63
GroupSelect 7 3.53 5.70 2.81 3.85 4.35 1.11
Summary F All 11 5.27 10.52 4.74 3.94 16.70 13.15
M All 16 3.57 24.71 19.62 4.12 7.01 2.72
Totals 27 3.61 18.93 11.70 3.94 10.96 5.52
Post-harv. F Clearcut 7 2.57 10.56 5.80 1.45 1.85 0.51
Control 8 7.96 9.87 2.81 2.28 5.02 2.91
GroupSelect 9 2.69 5.48 1.89 1.30 1.36 0.23
M Clearcut 7 5.98 11.11 6.30 2.22 49.22 46.96
Control 7 3.65 16.72 13.10 1.59 18.66 17.29
GroupSelect 8 2.32 2.64 0.51 1.66 1.64 0.21
Summary F All 24 4.19 8.42 2.02 1.49 2.72 1.00
M All 22 3.02 9.82 4.57 1.75 22.19 15.69
Totals 46 3.02 9.09 2.40 1.57 12.03 7.57
28
Table 2. Least Squares Means (LS Mean) Tukey-Kramer post-hoc pairwise
comparisons connecting letters report of monthly environmental temperatures (Tmin,
Tmax, Tmean) during 2009-2010 within four habitat types (clearcut openings, group
selection openings, harvest-adjacent forest, and forested control). Habitat types at each
level not connected by the same letter are significantly different.
Level Habitat Type LS Mean
Tmean GroupSelection A 12.4068993
Clearcut A 12.3435027
Control B 11.4761091
Harv.Adjacent B 11.1620106
Tmax GroupSelection A 25.3953822
Clearcut A 24.6201529
Control B 17.7994578
Harv.Adjacent B 17.2141375
Tmin Control A 7.302016
Harv.Adjacent A 7.05775033
Clearcut B 5.99306883
GroupSelection B 5.84889568
29
Figure 2. Scatter plot of daily distances traveled by Eastern Box Turtles (steplengths;
y-axes) by ground temperature (Tg in °C; x-axes). All 2007-10 steplengths in meters per
day by ground temperature (a.) and the log-transformed steplength by ground temperature
(b.). Pre-harvest (2007-08) steplength in meters per day by ground temperature (c.) and
post-harvest (2009-10; d.). Plots show 95% (black ellipse) and 50% (grey ellipse)
density ellipses around points and histogram densities along plot boarders. Darkened
areas represent the peak of activity temperatures (22-26°C; thermal optimum) in these
data.
a.
c.
b.
d.
30
Figure 3. Average steplength (m/day) moved by Eastern Box Turtles each month for
both harvest periods (pre-harvest [2007-08] and post-harvest [2009-10]; bars). The
average ground temperatures (Tg; °C) recorded at turtle location each harvest period are
also plotted (lines).
0
5
10
15
20
25
30
35
40 PreTx
PostTx
TempPreTx
TempPostTx
Pre-harvest
Post-harvest
Tg Pre-harvest
Tg Post-harvest
31
Figure 4. Mean monthly temperature maxima (Tmax), mean (Tmean), and minima
(Tmin) over two years (2009-2010) by habitat type (clearcut openings, group selection
openings, harvest-adjacent forest (Harv. Adjacent), and forested control) (a). Maxima,
means, and minima monthly Eastern Box Turtle body temperatures (Tb) for the same
period (b).
32
0
5
10
15
20
25
April May June July August September October
Figure 5. Mean Eastern Box Turtle body temperatures (Tb) in degree Celsius
(C) with relation to timber harvest proximity over the active season months for post-
harvest years (2009-10 combined). Starred bars represent significantly different
mean temperatures during that month.
33
Tabl
e 3.
Pub
lishe
d st
udie
s inv
olvi
ng h
ome
rang
e es
timat
es fr
om n
ativ
e po
pula
tions
of T
. car
olin
a.
Aut
hors
(Dat
e)
# of
Tur
tles
(# o
f loc
/turtl
e)
Dur
atio
n
of st
udy
Met
hod
Hom
e R
ange
Siz
e
Estim
ate
Loca
tion
(stu
dy si
ze)
Nic
hols
193
9 12
(14)
20
yrs
M
ark-
reca
ptur
e 12
0-20
0 m
dia
m.
Long
Isla
nd, N
Y
Stic
kel 1
950
55 (3
+)
3 yr
s M
ark-
reca
ptur
e &
thre
ad
traili
ng
100
m d
iam
eter
M
aryl
and
(11
ha)
Dol
beer
196
9 ‘m
any’
of 2
70
mar
ked
1 yr
M
ark-
reca
ptur
e 76
.2 m
dia
m.
Tenn
esse
e (8
.9 h
a)
Schw
artz
&
Schw
artz
197
4
239
(4-1
8)
8 yr
s D
og c
aptu
re-r
ecap
ture
&
Rad
iote
lem
etry
1.9
ha
ave.
are
a
(1.2
-10.
2 ha
)
Mis
sour
i (22
ha)
Mad
den
1975
23
(85)
4
yrs
Rad
iote
lem
etry
♀
373
m d
iam
.;
♂ 2
84 m
dia
m.
2.12
ha
ave.
are
a
New
Yor
k
Stra
ng 1
983
8 (3
+)
3 yr
s Th
read
trai
ling
167
m d
iam
. Pe
nnsy
lvan
ia (2
9 ha
)
Schw
artz
&
Schw
artz
198
4
37 (1
1-44
) 19
yrs
D
og c
aptu
re-r
ecap
ture
&
Rad
iote
lem
etry
5.2
ha a
ve. a
rea
(0.6
-10.
7 ha
)
Mis
sour
i (22
ha)
Bay
less
198
4 6
(10+
) 56
day
s
over
2yr
s
Rad
iote
lem
etry
& th
read
traili
ng
213
m d
iam
.
1.25
ha
Virg
inia
(49.
4 ha
)
Will
iam
s &
Park
er 1
987
35 (3
+)
26 y
rs
Mar
k-re
capt
ure
♀ 1
76 m
dia
m.
♂ 1
71 m
dia
m.
Indi
ana
(72.
9 ha
)
34
Aut
hors
(Dat
e)
# of
Tur
tles
(# o
f loc
/turtl
e)
Dur
atio
n
of st
udy
Met
hod
Hom
e R
ange
Siz
e
Estim
ate
Loca
tion
(stu
dy si
ze)
Hal
lgre
n-Sc
affid
i
1986
11 (3
+)
2 yr
s M
ark-
reca
ptur
e &
thre
ad
traili
ng
97 m
dia
m.
0.2
ha a
rea
Mar
ylan
d (1
1.3
ha)
Stic
kel 1
989
103
(3+)
37
yrs
M
ark-
reca
ptur
e 14
5 m
dia
m.
♀ 1
.13
ha a
rea
♂ 1
.2 h
a ar
ea
Mar
ylan
d (1
1 ha
)
Don
alds
on &
Echt
erna
cht 2
005
13(3
0-54
) ~1
50 d
ays
Rad
iote
lem
etry
& th
read
traili
ng
1.88
ha
area
Te
nnes
see
(28
ha)
Qui
nn 2
008
14 (a
v. 6
2)
1 yr
R
adio
tele
met
ry
♀ 4
.0 h
a ar
ea
♂ 6
.7 h
a ar
ea
4.97
ha
ave.
are
a
Con
nect
icut
Cur
rent
Stu
dy
50 (a
v. 3
4-70
/yr)
4
yrs
Rad
iote
lem
etry
♀
5.5
5 ha
are
a
♂ 9
.14
ha a
rea
7.45
ha
4-yr
ave
.
Indi
ana
(35,
000
ha)
35
Appendix 1. Summary of the Eastern Box Turtle annual home ranges at nine study
sites in south-central Indiana from 2007-10. Year, sex, management class (Mngmt
Class), number in group (n), and median, mean, and standard errors of annual home range
(100% Minimum Convex Polygon; MCP) in hectares (ha). For 2007-08, the
management class represents the assigned harvest type prior to harvest implementation.
Year Sex MngmtClass n Median Area Mean Area Std Err
2007 F Clearcut 4 4.76 16.44 12.747
Control 4 1.63 1.62 0.274
GroupSelection 2 2.26 2.26 0.360
M Clearcut 4 1.59 2.03 0.540
Control 4 1.90 34.02 32.289
GroupSelection 5 2.89 3.58 1.032
2008 F Clearcut 5 3.04 3.04 0.568
Control 3 4.77 5.40 2.463
GroupSelection 2 9.28 9.28 7.185
M Clearcut 5 1.97 3.84 1.469
Control 4 4.17 49.50 46.064
GroupSelection 7 1.20 4.31 2.966
2009 F Clearcut 7 2.16 9.77 5.835
Control 7 6.57 6.69 1.712
GroupSelection 7 2.11 3.94 2.025
M Clearcut 6 2.94 3.01 0.664
Control 6 2.48 17.57 15.510
GroupSelection 8 1.85 1.99 0.405
2010 F Clearcut 7 1.64 2.11 0.641
Control 7 2.50 5.38 2.369
GroupSelection 8 2.07 3.48 1.358
M Clearcut 7 2.48 9.02 6.155
Control 7 2.20 2.97 1.041
GroupSelection 8 1.71 2.05 0.345
36
CHAPTER 2: HIBERNAL THERMAL ECOLOGY OF EASTERN BOX TURTLES
WITHIN A MANAGED FOREST LANDSCAPE
Abstract
Box turtles are being extirpated from much of their former range and remaining
populations often live in association with anthropogenically altered habitats. This is
particularly evident at the northern distributional limit of eastern box turtles (Terrapene
carolina carolina) and important over the winter months when their ability to respond to
microclimatic change is limited. Using temperature dataloggers, I studied the hibernal
microclimate of box turtles and associated habitat following timber harvests. I monitored
the body temperatures (Tb) of 38 T. c. carolina and collected detailed air and soil profile
temperatures of 12 box turtle hibernacula, 6 clearcut treatments, and 6 adjacent forested
areas during the hibernal season (winter 2009-10). I was able to partition the hibernal
season into two biologically significant thermal periods: hibernation and emergence. The
mean hibernation Tb averaged (3.28°C, SE = 0.09) and corresponded to an average depth
of 10 cm. Clearcuts were consistently colder (mean = 1.91°C) than forests (mean =
2.68°C) and hibernacula (mean = 2.77°C) during hibernation, but became the warmest
areas during emergence (mean = 9.96°C). I found that in the average clearcut, turtles
could burrow to approximately 20 cm in order to attain the average hibernation Tb or to
approximately 15 cm to attain Tb no different than those overwintering on colder,
northeast-facing slopes in the forest (mean = 2.83°C). Alternatively, I found that
southwest-facing slopes were warmer and if turtles chose to overwinter only in clearcuts
on those slopes, they could remain shallower. All but one turtle overwintered in forested
areas; however, our study suggests that timber harvests offer various microhabitats
exploitable by hibernating box turtles based on soil profile temperatures, slope aspect,
and depth of hibernation.
37
Introduction
Among all threats to the perseverance of wildlife populations, habitat loss and
alteration are considered the most pervasive and deleterious (Fahrig 2003; Gibbons et al.
2000; Lawton et al. 2001; Todd & Andrews 2008). Consequently, practices encouraging
the sustainable use of natural resources such as timber harvesting are increasingly
becoming the focus of conservation study (Fredericksen et al. 2000; Gitzen et al. 2007; Li
et al. 2000; Perison et al. 1997). A variety of vertebrate taxa (including birds, small
mammals, and some herpetofauna) benefit, at least temporarily, from the canopy
openings and clearings created by certain silvicultural techniques (Fredericksen et al.
2000; Goldstein et al. 2005; Semlitsch et al. 2009). However, other taxa (especially
amphibians) have been found to respond negatively to timber harvests (Cushman 2006;
Semlitsch et al. 2009), while many more have not been studied and their response to
timber harvests is not known. Thus, effects of timber harvests can differ both across taxa
and within species based on their changing habitat requirements throughout the year.
Habitat selection occurs during biologically significant events including mating,
nesting, and the selection of overwintering sites (Madden 1975; Spencer & Thompson
2003). While our general knowledge of habitat selection for many species is plentiful for
both mating and nesting events, there is far less information for hibernal season
(overwinter). Moreover, there is a severe dearth of information regarding the impacts on
wildlife associated with silvicultural practices during the hibernal season. For non-
migratory species, hibernal season habitat selection is critical to survival, especially for
poikilotherms whose body temperature is regulated by ambient temperature.
Herpetofauna are particularly affected by habitat alteration in that they must behaviorally
adapt to environmental flux (Johnston & Bennett 1996). Many herpetofaunal species
sustain regular cycles of dormancy to adapt to changing environmental conditions
(Gregory 1982). Cold winter conditions will cause many taxa to retreat to hibernacula
for extended periods (e.g. Squamate spp. up to 8 months, Anuran spp. up to 11 months;
Aleksiuk 1976; Zug et al. 2001). Therefore, as analysis of behavior at these hibernation
sites is equally as important as during the active season. Empirical evaluation of habitat
38
selection during the hibernal season is crucial to gain a more complete picture of the
effects of timber harvests on forest dependent wildlife species.
Eastern box turtles (Terrapene carolina carolina) are a forest-dwelling species
that are declining throughout their range (Dodd 2001; Hall et al. 1999; IDNR 2007;
Stickel 1978; Williams & Parker 1987). This species is protected in most states within its
range and its survival may be compromised by habitat proximity to anthropogenic
disturbances (Currylow et al. 2011). Box turtles select habitats based on a combination
of factors, including cover and temperature (Reagan 1974). Canopy cover influences
temperature by means of regulating light intensity, a factor known to be critical for turtles
during activity periods (Gould 1957; Rose & Judd 1975). Ground and air temperature
play key roles in the activity of box turtles, even in winter months (Congdon et al. 1989).
Eastern box turtles may hibernate for a significant proportion of the year (up to nine
months) however, much in situ work with this species involves only active season
monitoring. The studies that do examine hibernal behavior are often limited by unnatural
settings, do not address thermal environments, or are narrow in scope (few records and
lack of habitat variables such as slope aspect or canopy). Alterations of temperature due
to canopy removal and the concomitant use by box turtles have not been studied during
hibernal seasons.
Thermoregulation is ostensibly an important factor in hibernacula selection and
overwintering behavior in box turtles. Box turtles have a natural mechanism that enables
them to endure sub-zero temperatures when more than 58% of their body fluids are
frozen, with minimal deleterious effects (Costanzo & Claussen 1990). Though T. c.
carolina can survive below freezing temperatures, mortality due to prolonged exposure is
not uncommon (Claussen et al. 1991). Box turtles burrow to avoid extreme temperatures
during the hibernal season (November through April). They may burrow deeper as the
seasonal temperatures decrease (Carpenter 1957). The majority of studies have found T.
carolina to overwinter at an average depth of only five centimeters, and no more than 18
cm (Carpenter 1957; Claussen et al. 1991; Congdon et al. 1989; Dolbeer 1971; Madden
1975; Minton 2001). Depth to which turtles burrow may also depend on slope aspect.
39
Slopes are an important consideration when studying thermal profiles during the hibernal
season because slopes that face the sun low on the horizon will remain warmer than
slopes facing away from the sun. Therefore, it is important to include evaluations of
slope aspect, especially in areas completely exposed such as in timber harvests.
In this study, I expanded upon the limited knowledge pertaining to hibernal
season impacts of timber harvests on a hibernating forest ectotherm. Specifically, I
aimed to investigate whether timber harvested areas offer suitable habitat for
overwintering eastern box turtles. The goals of this study were to: (1) characterize
hibernal thermal behavior of eastern box turtles, (2) determine the available thermal
habitat in timber harvests relative to forests on various slope aspects, and (3) evaluate the
effect of timber harvests on actual and theoretical hibernal habitat use.
Study Area
The study was conducted within approximately 35,000 hectares of Morgan-
Monroe and Yellowwood State Forests in Morgan, Monroe, and Brown Counties,
Indiana. Both forests are characterized by hills and ravines of hardwood, deciduous
forests with scattered timber harvest areas. The majority of canopy species are Quercus
spp., such as montnana (chestnut oak), and Carya cordiformis and C. ovata (butternut
and shagbark hickory; Summerville et al. 2009).
Morgan-Monroe and Yellowwood State Forests are managed for multiple-uses,
including recreation, education, research, and timber harvesting. The study site was
selected because it comprises a relatively contiguous forest and population of free-
ranging box turtles, and timber harvests were recently implemented within the box turtle
habitat as part of the Hardwood Ecosystem Experiment (HEE). The HEE is a long-term
(100-yr), landscape-scale timber and wildlife research and management collaborative
designed for the study of ecological and social impacts of various silvicultural methods.
For our study, I focused on six of the nine HEE study sites, each with similar vegetative
species, slope aspects, and elevations. The six study sites encompass approximately 400
hectares each and were randomly assigned a management type: clearcut treatments (2
40
clearcuts approximately 4-hectares each) or control (no timber removal), each with three
replicates (Figure 6). The clearcuts were implemented over the winter of 2008-09 within
90-hectare centers of each unit to allow the remaining forest to act as buffer areas.
Methods
Turtle Monitoring
To locate hibernaculum sites for hibernal monitoring I used standard
radiotelemetry homing methodology. As part of a concurrent radiotelemetry study, radio
transmitters (Holohil RI-2B, Carp, Ontario, Canada; 14.5 grams each representing less
than 5% of the animal’s total body weight) were epoxied to the carapaces of 38 adult box
turtles (19♂, 19♀) throughout the the HEE sites (Figure 6). I followed turtles until they
were consistently found underground for hibernation (5 November 2009). Initiation of
hibernation was defined as the first date each turtle was consistently observed buried
underground provided that it was subsequently found at that location for at least one
week before regular tracking ceased. To represent the temperatures turtles chose over
time, I affixed temperature dataloggers, accurate to 0.5° Celsius (Thermochron iButtons,
model number DS1921G-F5, Maxim Integrated Products, Inc., Sunnyvale, California,
USA) to each turtle’s carapace prior to hibernation. Carapacial temperature
measurements have been found to correlate well with turtle core body and cloacal
temperatures (Bernstein & Black 2005; Congdon et al. 1989; do Amaral et al. 2002;
Peterson 1987). Temperature dataloggers were set to record turtle body temperatures
(Tb) every 180 minutes throughout the hibernal season. These temperatures were then
aligned with soil thermal profile temperatures (described below) to inform turtle
burrowing depth. These activities were permitted under Purdue Animal Care and Use
Protocols and amendments (PACUC 07-037).
Experimental Design and Habitat Monitoring
To document levels of hibernal microhabitats available to burrowing animals, I
monitored temperatures at multiple soil depths using thermal profile stakes (hereafter:
TPS) at 24 locations throughout the study sites. The TPS consisted of five temperature
41
dataloggers affixed at 10-cm intervals along the length of a 1.3x5x51-cm wooden stake,
and sunk into the forest floor. The profile intervals spanned from 10 cm above soil
surface (in the leaf litter at “turtle height”), at the soil surface (0 cm), and at 10, 20, and
30 cm below the soil surface (Figure 7a). I programmed the temperature dataloggers to
logging intervals of 180 minutes and they recorded soil profile temperatures throughout
the landscape for 22 weeks from 8-November 2009 through 10-April 2010.
For this study, I compared thermal environments between forested habitats
(forests) and clearcut treatments (clearcuts) to evaluate their suitability as box turtle
hibernal habitat. Twelve TPS were placed mid-slope at each of the 4-ha clearcut
treatments (six replicates of “clearcut TPS”) and adjacent forested habitats (six replicates
of “forest TPS”; Table 4). I used ArcGIS to determine the random locations of the TPS
within the designated habitats. I placed the remaining 12 TPS at selected turtle
hibernacula (Figure 7b) to characterize soil profile temperatures where turtles chose to
overwinter. Each of these “hibernacula TPS” replicates were sunk into the forest floor
within 1 m of hibernating turtles, but no closer than 0.33 m to avoid disturbing the turtle.
Hibernating turtles were radio-tracked monthly to ensure consistent proximity to
hibernacula TPS was maintained over the hibernal season. The 12 turtles associated with
hibernacula TPS were selected based on a variety of factors including their association
with clearcuts, sex, slope aspect, and elevation. Hibernacula TPS were divided equally
by sex and active season home range association with clearcuts or controls. Slope aspect
and elevation can significantly affect the amount of penetrating solar radiation, vegetative
cover, precipitation, and consequently, the temperature of a particular location (Holland
& Steyn 1975; Schulze 1975). Thus, replicates of north-to-east- and of south-to-west-
facing slopes were used to the greatest extent possible (Table 4). On all slopes,
elevations were selected to most closely match the average turtle hibernacula
(approximately 260 m).
Analyses
I analyzed thermal data at multiple levels in an attempt to characterize the
hibernal ecology of box turtles and detect specific patterns of temperature in the
42
landscape relative to clearcut and forested habitat. I processed raw logged data using R
version 2.10.1 (R Development Core Team 2009), which is capable of handling and
managing very large datasets, and calculated daily minimum, maximum, and mean
temperatures for all temperature loggers. I analyzed all temperatures weekly to
determine biologically significant periods over the season. Temperatures recorded from
each of the 38 turtles were combined to obtain an average hibernal Tb at which turtles
spend the majority of their time. To determine the depths to which turtles burrow
overwinter, Tb were compared to hibernacula TPS on specific slopes.
Overwintering microclimates throughout the landscape were determined by
various comparisons of the TPS temperatures. I tested for differences in TPS
temperatures at varying depths and slopes for each of the TPS types (clearcut, forest, and
hibernacula) across time. I used restricted maximum likelihood (REML) method for
fitting our mixed model designs for each test. I used temperature logger ID as a repeated
measures random effect with sex, slope, period, depth, and associated location as fixed or
interacting effects, depending on the scenario. Following those analyses, I conducted
Least Squares Means Tukey-Kramer post-hoc pairwise comparisons or Student’s t tests
where appropriate to detect significant differences in mean temperatures. All statistical
analyses were carried out using JMP statistical software (SAS 2008). Values were
considered significant where the P-values were less than 0.05 and differences in mean
temperature values were greater than 1°C (Δ°C > 1).
Results
Over the 22-week period, 191,200 temperatures were recorded on a variety of
slope aspects associated with clearcuts, forests, and turtles. Due to the volume of data,
many of the comparisons were statistically significant; however, the accuracy of the
temperature dataloggers (± 0.5°C) is an additional criterion that must be considered.
Here I report all statistical significance with both of these considerations in mind (i.e. P <
0.05 and Δ°C > 1).
43
Temporal analysis of all TPS temperatures revealed two biologically significant
time periods within the 22-weeks of monitoring: hibernation and emergence. Mean
temperatures of these periods are significantly different (F1, 45 = 1059, P < 0.001, Δ°C =
6.56) and are divided by the time at which inversion of soil and surface temperature
occurs (point of inversion). For example, early in the season the coldest hibernacula
temperatures were found at the surface and progressively warmed at increasing depths
(Figure 8). However, between the 17th and 18th week of monitoring (28 February – 7
March 2010), that trend reversed and the warmest temperatures were found at the surface.
I refer to the thermal period between weeks 2 and 17 as “hibernation” and between weeks
18 and 22 as “emergence” (Figure 8).
Box Turtle Thermal Behavior
All 12 TPS-associated turtles remained within 3 m of their hibernacula TPS (i.e.,
no turtles made significant movements over the hibernation period from their last known
location the previous fall). Most turtles (n = 34) chose hibernacula between 14 October
and 29 October 2009 and the vast majority of turtles (97%) overwintered in forested
habitats. A single female turtle (706F) overwintered within an unmonitored 2.56-ha
harvest opening associated with a separate aspect of the HEE.
Mean hibernation Tb (3.28°) of all turtles differed significantly from emergence
Tb (9.32°C; F1, 72 = 1297, P < 0.001, Δ°C = 6.04; see Appendix ). Turtle 706F
maintained Tb values that were comparable but warmer (ave = 3.72°C) than the mean
hibernation Tb. In addition, the mean depth of hibernation for all turtles averaged slightly
less than 10 cm. Turtles began to decrease their depths and emerge corresponding to
higher temperatures after the point of inversion (28 February – 7 March 2010). While I
found no statistically significant differences in mean Tb between the sexes over the
hibernal season, several trends in those data were observed. Females averaged slightly
warmer Tb (3.34°C) than males (3.22°C) during the hibernation period. Moreover,
differences between sexes were even more striking for the subset of 12 turtles in
monitored hibernacula. Males selected hibernation Tb matching depths just below the
soil surface (2.55°C) with the shallowest overwintering turtle consistently above the soil
44
surface (turtle number 605M, Tb ave = 1.81°C). Monitored females, on the other hand,
chose Tb matching depths at 10 cm (3.51°C) with the deepest burrowing to 20 cm (turtle
number 906F, Tb ave = 4.44°C). These two extreme cases constitute the minimum and
maximum mean hibernation Tb, respectively (see Appendix ).
Eight of the 38 turtles were not used in analyses involving slopes. Four of these
turtles did not meet the criteria for determining if a hibernaculum site was selected before
tracking ceased and four overwintered in flat locations such as hilltops or creek-beds. No
turtles chose to overwinter on north-facing slopes and these slopes were not monitored.
Tb varied somewhat by slope during both hibernation (P = 0.6129) and emergence
periods (P = 0.2623; Table 5). Before the point of inversion at week 17, the overall
warmest slope aspect was southeast (mean at all depths = 3.49°C) and the overall coldest
was northeast (mean at all depths = 2.47°C). Turtles overwintering on these warmer,
southeast-facing slopes did not burrow as deeply as other hibernating turtles, but were
able to remain as warm (mean Tb = 3.31°C). The mean hibernation Tb (3.28°C) was
found just below the surface on southeast-facing slopes (mean=3.06°C at a depth of 0
cm) and was not significantly different from the mean Tb found deeper on most other
slopes (mean = 3.33°C at a depth of 10 cm). Turtles overwintering on colder, northeast-
facing slopes also did not burrow as deeply as most other turtles, but the colder slope
aspect resulted in relatively cold mean Tb (mean = 2.65°C). After the point of inversion,
the warmest slope aspects were south (mean at all depths = 9.28°C) and southwest (mean
at all depths = 9.25°C) while the coldest remained northeast (mean at all depths =
8.29°C). Interestingly, the turtles that hibernated shallowly on both southeast- and
northeast-facing slopes emerged sooner than the average on other slopes. Additionally,
those turtles who overwintered on southwest-facing slopes averaged emergence Tb that
matched soil depths between 0 and 10 cm (Tb mean = 9.00°C, 0 cm = 10.60°C, 10 cm =
8.52°C), suggesting that they were still below the surface during the emergence period
despite those slopes being among the warmest.
45
Microclimates of Forests vs. Clearcuts
The thermal habitat in timber harvested versus forested areas was evaluated by
comparing mean temperatures from TPS within the clearcuts (n = 6), the forest (n = 6),
and at turtle hibernacula (n=12). There was no difference between mean temperatures of
TPS habitat or slope comparisons during the entire 22-week hibernal season (F2, 21 = 1.7,
P = 0.2088, Δ°C = 0.36). However, when separated by hibernation and emergence
periods, the clearcuts maintained more extreme daily temperatures. During hibernation,
the range of temperatures were significantly greatest in clearcuts (F 2, 47 = 9.32, P =
0.0004) meaning these areas were more variable in temperature. However, clearcuts
were consistently colder (mean from all depths = 1.91°C) than forests (mean from all
depths = 2.68°C) and hibernacula (mean at all depths = 2.77°C) during hibernation (F 2, 21
= 9.60, P = 0.0011), but were warmest during emergence (mean from all depths =
9.96°C; F 2, 21.07 = 6.70, P = 0.0056; Table 6). Although ambient (+10 cm) temperatures
during the hibernation period were nearly identical in all locations, comparable soil
temperatures in clearcuts were found approximately 10 cm deeper than in forests and
hibernacula (i.e., clearcut hibernation temperatures at a depth of 10 cm were more similar
to forest hibernation temperatures at 0 cm; Figure 9). It is interesting to note that during
the emergence period, hibernacula locations were generally cooler than other locations at
all depths, and significantly so from treatments on most slopes (see Appendix ).
Slope aspect influenced microclimates in clearcuts and forests (Table 6; see also
Appendix ). During hibernation, southwest-facing slopes in forests were the warmest
overall (mean from all depths = 3.16°C), but during emergence, southwest-facing slopes
in clearcuts became the warmest (mean from all depths = 10.50°C). On average, the
coldest slopes were northeast facing during hibernation (mean from all depths = 2.11°C)
and northwest facing during emergence (mean from all depths = 8.42°C). Nonetheless,
when depth is taken into account, northeast-facing slopes showed the greatest differences
in mean temperatures across habitats (from +10 cm during hibernation at -0.88°C to +10
cm during emergence at 11.02°C; see Appendix ).
46
Discussion
Forest management practices change the vegetative structure and local
environmental conditions, which in turn may alter species use of available habitat
(Renken et al. 2004). Many forest dwelling vertebrates (both endothermic and
poikilothermic alike) will preferentially use certain types of available habitat at different
times throughout the year for thermoregulation, nesting, and dormancy (Madden 1975;
Schwartz & Schwartz 1974). The current study provides key insights into the hibernal
thermal behavior of eastern box turtles and the microclimates of habitats within timber-
harvested areas versus those within adjacent forests.
Several general patterns have emerged from TPS within clearcuts, adjacent
forests, and at turtle hibernacula. First, the emergence of box turtles was correlated with
an inversion of surface and deep soil temperatures. Once the point of inversion occurs,
turtle hibernacula are no longer warmer than soil surface temperatures. Previous studies
attribute rising air, surface, and rough estimates of subsurface temperatures as the triggers
for box turtles to emerge in the spring (Bernstein & Black 2005; Grobman 1990). Our
data suggests proximity to the surface is also a key factor to timing of emergence.
Turtles that burrowed deeper during winter months emerged later in the spring.
Second, nearly all turtles chose hibernacula that were in forested habitats. Only a
single radiotelemetered turtle overwintered within a HEE-associated harvest opening.
The question of whether T. c. carolina will use forest openings such as clearcuts during
the hibernal period is central to this project. It could be argued that few turtles
overwintered within clearcuts because the total area of openings was small relative to that
of forested habitat and thus, not part of the turtles’ normal home range. While the
treatments do represent a relatively small proportion of the overall study site (<1.5%),
associated radiotelemetry data clearly demonstrates that harvest openings are used by
many of these same turtles during the turtle’s active season (averaging 8.2% of their
home ranges; Currylow et al., in prep). Therefore, the lack of overwintering sites within
treatments may reflect habitat selection based on simple energetics.
47
With little leaf litter or canopy cover to buffer harsh weather, the microclimate of
the clearcuts often exhibited temperature extremes that overwintering turtles were
expected to avoid. Freezing temperatures are known to cause mortality in even hearty,
freeze-tolerant taxa such as frogs and salamanders, as well as box turtles (Carpenter
1957; Metcalf & Metcalf 1979; Storey & Storey 1986). During intermittent warm
periods, however, hibernal soil temperatures in clearcuts temporarily increased above
those found in adjacent, uncut forests. Higher soil temperatures mid-winter has been
implicated in the premature emergence and subsequent freezing death of overwintering
turtles (Neill 1948; Schwartz & Schwartz 1974; Ultsch 2006). Nearly all turtles in this
study (37 of the 38) chose hibernacula in forested areas where forest debris such as leaf
litter was noted to be greater than in clearcuts. Dolbeer (1971) noted that turtles selected
areas with a thick mat of leaf litter and rotting logs for hibernacula. Based on soil profile
data among clearcuts and forests, turtles overwintering in a clearcut would need to
burrow an average of 10 additional centimeters to achieve the warmer Tb.
The third general pattern that emerged from temporal analyses of temperatures
was that most turtles chose temperatures of 3.28°C for hibernation. This Tb corresponded
to a depth of approximately 10 cm, which is within the range (5-18 cm) found in other
studies (Carpenter 1957; Claussen et al. 1991; Congdon et al. 1989; Dolbeer 1971;
Madden 1975; Minton 2001). Interestingly, I found that females maintained slightly
warmer Tb than males and generally burrowed deeper throughout hibernation. Many
males burrowed to just below the soil surface with only leaf litter shielding them from
harsh winter weather conditions. It is unclear as to whether this observation is due to
variation caused by slope aspect. One explanation is that certain adult males could be
physiologically more tolerant of the cold, although studies on hatchling turtles showed no
sex differences in cold tolerance (Costanzo et al. 1995; Packard & Janzen 1996). A
blood chemistry panel from a subset of turtles in the present study showed that males
generally had higher freeze-resistant glucose levels than females and that turtle 605M
(who was at the surface for a majority of the hibernal season) had comparable levels to
other males (Kimble et al., unpublished data). In contrast, females undergoing follicle
development may select warmer sites to speed the process or because their increased
48
mass would cause them to recover from freezing temperatures more slowly (Shine 1980).
Despite numerous laboratory studies on freeze tolerance in this species, the reported sex
difference herein is novel and warrants further investigation.
Slope aspect appears to be an important habitat characteristic for many burrowing
animals during the hibernal season. Black Rat Snakes and Eastern Massasauga
Rattlesnakes in Ontario prefer to hibernate on south-facing slopes that remain warmer
and thaw earlier, likely ameliorating the effects of freezing winter temperatures (Harvey
& Weatherhead 2006; Prior & Weatherhead 1996). Similarly, toads in the Pacific
Northwest chose to inhabit south-facing slopes and burrow to just below the frost line
(Bull 2006). Yellow-bellied marmots in Colorado generally choose burrows on either
southwest- or northeast-facing slopes year-round, but choose those with deep, insulating
snow cover overwinter (Svendsen 1976). In contrast, Claussen et al. (1991) found that T
c. carolina in Ohio’s woodlands prefer nearly level ground or west-facing slopes for
hibernacula, but I found no such trend among the 38 turtles in this study. However, I did
observe patterns in the burrowing behavior (depth of hibernacula) depending on the slope
of the selected hibernaculum site. As with the aforementioned studies, many of our
animals burrowed deeper to reach warmer temperatures overwinter. However, the
conflicting behavior I noted on the colder, northeast-facing slopes is an important
observation, as the temperatures available in the clearcuts were overall equally as cold.
The clearcuts did offer temperatures most often used by overwintering turtles, but at
greater depths (depending on slope) than forested areas and hibernacula. Therefore, these
areas could theoretically be inhabited by burrowing animals during the winter months.
Forest floor temperatures have been shown to affect the burrowing activity of
small mammals, amphibians, reptiles, and invertebrates (Byers 1984; Landry-Cuerrier et
al. 2008; Vernberg 1953). Temperatures collected in this study can be used to predict the
hibernal use of clearcuts. If overwintering animals choose to use clearcuts for
hibernaculum sites, they must behaviorally adapt as found in some amphibians (Storey &
Storey 1996). Turtles must burrow twice as deep (20 cm) to attain a mean Tb of 3.28°C,
or tolerate the colder hibernation temperatures of 2.83°C (at 15 cm). Alternatively, they
49
could choose to overwinter in clearcuts only on warmer slopes (such as southwest facing)
and burrow 10 cm to attain the mean hibernation temperature.
Turtle 706F was the only turtle to overwinter in a timber harvest opening. This
female was able to maintain above average hibernation temperature, despite being in an
opening and on a northeast-facing slope. Using the temperatures obtained from TPS that
were placed in other northeast-facing treatment slopes, I determined that this female
would have had to burrow to depths greater than 30 cm to attain her hibernation
temperatures in that habitat. Even the northeast-facing slopes of forested habitats only
offered temperatures comparable to her mean at depths of nearly 20 cm. A comparison
of 706F daily mean temperatures to corresponding TPS suggests this turtle regulated
body temperature by rising to the surface on warmer days and burrowing deeper on
colder days. These depth adjustments are frequently seen in the T. c. triunguis
subspecies, which burrows deeper as winter temperatures decrease (Carpenter 1957; do
Amaral et al. 2002). Still, I did not observe this behavior to such extremes in any of the
12 hibernacula monitored turtles or the remaining 25 turtles until the emergence period.
Data from this and other studies indicate that site fidelity may play a role in
hibernacula selection. Cook (2004) observed that several individuals exhibited
hibernacula site fidelity with inter-hibernacula changes of less than 100 m over
successive years. Analysis of the concurrent radiotelemetry study data of the same turtles
herein indicate that in 2010 turtles chose overwinter locations averaging 123 m from the
2009 site (Appendix C). Most turtles appeared to choose sites within 61 meters of their
2009 hibernacula (median = 41 m, min = 5.8 m, max = 1801 m). Thus, it is unlikely that
turtles would indiscriminately return to the exact location of a previous hibernacula if
habitat alteration made it undesirable. Instead, the animal could choose a more desirable
site adjacent to that location. None of the turtles appeared to choose 2010 overwintering
locations within the treatments, although some were relatively close. Turtle 706F was
last located in 2010 within 16 m of the edge of the harvest opening she hibernated in
previously; and turtle 906F, which was the turtle that maintained the warmest hibernation
temperatures in 2009-10, was within 20 m of a clearcut treatment in October 2010.
50
Management Implications
The data herein suggest that small-scale timber harvests techniques used in the
Midwest have little effect on Eastern Box Turtles during the winter months. The
microclimates available in these timber-harvested habitats are within the range used by
hibernating box turtles, but are generally found at deeper depths. The typical harvest size
(0.5 - 5-ha) is small enough in proportion to animal home ranges that another habitat
could be selected for hibernacula if desired. However, the slope on which the timber
harvest is implemented may have a profound effect on other burrowing animals. A
variety of taxa use south facing slopes for overwintering sites, and I found southwest-
facing slopes to be the warmest over the winter months. Yet, temperatures in clearcuts
were more variable than in forested habitats and this may cause inconsistency in the
warmer temperatures generally offered on south-facing slopes. In contrast, these
temperature fluctuations may make the generally colder and less desirable north-facing
slopes more desirable or at least, more tolerable. If timber harvests are to be
implemented, I suggest they be done over the winter months, remain relatively small, and
placed on a variety of slope aspects to mediate their overall impact on forest-dwelling
wildlife.
Acknowledgements
I would like to thank S. Johnson for her dedicated and hard work in the field. I
would also like to thank the Williams lab group and two anonymous reviewers for review
comments on earlier versions of this manuscript. This paper is a contribution of the
Hardwood Ecosystem Experiment, a partnership of the Indiana Department of Natural
Resources (IDNR), Purdue University, Ball State University, Indiana State University,
Drake University, and The Nature Conservancy. Funding for the project was provided by
the Indiana Department of Forestry Grant #E-9-6-A558 and IDNR Division of Fish and
Wildlife, Wildlife Diversity Section, State Wildlife Improvement Grant #E2-08-WDS15.
Research activities associated with this project fall under the Scientific Purposes Licenses
09-0080 & 10-0083.
51
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56
Tabl
e 4.
Num
ber a
nd lo
catio
n of
tem
pera
ture
dat
alog
gers
in h
arve
st o
peni
ngs (
H) a
nd fo
rest
ed h
abita
ts (F
). S
lope
asp
ect
(NW
, SE,
etc
.) re
pres
ents
the
slop
e fo
r whi
ch th
e lo
gger
was
ass
igne
d or
that
the
over
win
terin
g tu
rtle
chos
e.
Slop
e A
spec
t
N
W
NE
E SE
S
SW
W
N
/A
To
tal
H
FH
FH
FH
FH
F
HF
HF
T
urtle
38
7
1 5
2
4
3
2
6 8
TPS
12
3 2
1
3
2
1
Hib
erna
culu
m T
PS
12
2
3
1
2
1
3
57
Table 5. Mean body temperatures (Tb) and standard errors for all turtles at
hibernation (Hib) and emergence (Emerg). “Unknown” slopes indicate turtles did not
select hibernacula by the final tracking date. The 12 turtles associated with hibernaculum
Thermal Profile Stakes.
Hibernaculum
Slope
# of records Hibernation Tb
Mean (°C) &
SE
Emergence Tb
Mean (°C) & SE
Northeast 7,038 2.83 0.20 8.58 0.22
East 2,346 3.20 0.35 9.20 0.37
Southeast 4,692 3.31 0.25 9.38 0.26
South 3,519 3.21 0.29 9.82 0.30
Southwest 2,346 3.23 0.35 9.00 0.37
West 7,039 3.23 0.20 9.63 0.22
Northwest 8,211 3.52 0.19 9.09 0.20
Flat 4,692 3.34 0.25 9.33 0.26
Unknown 4,692 3.61 0.25 10.11 0.26
Total Hib:34,048
Emerg:10,527
3.28 0.09 9.32 0.09
Select 12 Total H:10,752/E:3,325 3.10 0.16 9.00 0.17
58
Tabl
e 6.
Mea
n Th
erm
al P
rofil
e St
ake
tem
pera
ture
s (°C
) and
stan
dard
err
or fr
om a
ll de
pths
com
bine
d du
ring
hibe
rnat
ion
and
emer
genc
e th
erm
al p
erio
ds.
Tem
pera
ture
s are
sepa
rate
d by
hab
itat t
ypes
(for
ests
, hib
erna
cula
, and
cle
arcu
ts) a
nd b
y sl
ope
aspe
cts.
Star
red
(*) v
alue
s are
sign
ifica
ntly
diff
eren
t (P
< 0.
05 a
nd Δ
°C >
1) f
rom
eac
h ot
her/o
ther
s acr
oss h
abita
t typ
es fo
r ass
ocia
ted
ther
mal
per
iod
and
slop
e as
pect
. To
tal m
ean
valu
es a
re re
porte
d fo
r eac
h ha
bita
t typ
e at
the
botto
m o
f the
tabl
e.
Hib
erna
tion
Em
erge
nce
Slop
e n
For
ests
M
ean
& S
E
Hib
erna
cula
Mea
n &
SE
Cle
arcu
ts
Mea
n &
SE
Fore
sts
Mea
n &
SE
Hib
erna
cula
Mea
n &
SE
Cle
arcu
ts
Mea
n &
SE
NW
11
,736
.
. 2.
68
0.12
.
. .
. 8.
42
0.14
.
.
NE
46
,945
2.
44
0.17
2.
49
0.14
1.
53
0.14
8.
72
0.18
8.
00*
0.15
9.
42*
0.15
E
3,52
8 2.
24
0.10
.
. .
. 9.
20
0.17
.
. .
.
SE
5,85
8 .
. 3.
49
0.06
.
. .
. 8.
60
0.11
.
.
S 11
,734
.
. 2.
92
0.12
.
. .
. 9.
28
0.14
.
.
SW
35,1
79
3.16
0.
32
2.60
0.
45
2.29
0.
26
9.19
0.
33
9.36
0.
46
10.5
0 0.
27
W
23,4
60
2.65
0.
31
2.81
0.
18
. .
8.79
0.
33
9.10
0.
19
. .
Tota
l 13
8,44
0 2.
69
0.17
2.
77
0.12
1.
91
0.17
8.
94
0.18
8.
71
0.12
9.
96*
0.18
59
Figure 6. Study Site Map. Map of Indiana with study area in Morgan, Monroe, and
Brown Counties outlined (inset) and the six study sites (3 clearcut treatment sites and 3
control sites) as part of the Hardwood Ecosystem Experiment in south-central Indiana.
All radio-telemetered turtle hibernacula are indicated as dark dots.
60
Figure 7. TPS Setup and Arrangement. Schematic of thermal profile stakes (TPS)
with temperature loggers affixed at 10-cm increments (not to scale). The TPS recorded
the microclimate through the hibernal season (hibernation and emergence periods).
Temperatures collected from temperature loggers at each depth were matched to turtle
temperatures (Tb) in order to inform the depth to which turtles hibernated and when they
emerged (verified by radiotelemetry) (a). A subset of TPS and turtle hibernacula physical
locations with relation to the management types (clearcut treatment and control) (b).
b.
a.
61
-10-5051015
Temp C
12
34
56
78
910
1112
1314
1516
1718
1920
2122
Figu
re 8
. H
iber
natio
n Te
mpe
ratu
res.
Mea
n hi
bern
acul
a te
mpe
ratu
res r
ecor
ded
by w
eek
at v
ario
us d
epth
s (+1
0, 0
, -10
, -
20, &
-30)
and
mea
n tu
rtle
body
tem
pera
ture
s. F
igur
e ill
ustra
tes t
he p
oint
of i
nver
sion
(bet
wee
n 23
Feb
ruar
y an
d 7
Mar
201
0),
dem
arca
ting
the
hibe
rnat
ion
perio
d (w
eeks
2 th
roug
h 17
) and
em
erge
nce
perio
d (w
eeks
18
thro
ugh
22).
See
text
for d
etai
ls
and
furth
er d
escr
iptio
n.
Hib
erna
tion
Emer
genc
e
Poin
t of
Inve
rsio
n
Tim
e (w
eeks
)
Temperature °C
62
Figure 9. Habitat Temperatures by Depth. Mean location TPS temperatures (°C) by
depth (centimeters) during the hibernation and emergence periods. Temperatures found
at hibernacula and forests were not significantly different at varying depths. However,
temperatures found in treatments were significantly colder (hibernation period) or
warmer (emergence period) at nearly all depths.
Clearcut Forest Hibernacula
63
Appendix 2
Average body temperatures (Tb) of 38 adult eastern box turtles during hibernation and
emergence (sorted by sex, then hibernation temperature). The mean values are totaled at
the bottom of the table. Starred (*) individuals are the select 12 associated with
hibernacula TPS. The four turtles who did not select hibernacula by the time tracking
ceased have “unknown” slopes.
n
Hibernation Tb Emergence Tb
ID# & Sex Slope Mean (°C ) & SE Mean (°C ) & SE
1206F S 1173 2.36 0.12 9.66 0.22
506F E 1173 2.53 0.12 9.17 0.22
800F flat 1173 2.70 0.12 8.74 0.22
1357F* NE 1173 2.79 0.12 7.36 0.22
1403F flat 1173 3.03 0.12 10.09 0.22
714F SW 1173 3.13 0.12 9.27 0.22
1252F SE 1173 3.14 0.12 9.32 0.22
100F SE 1173 3.19 0.12 10.04 0.22
1360F* NW 1173 3.30 0.12 7.07 0.22
1455F* SW 1173 3.32 0.12 8.77 0.22
900F* W 1171 3.35 0.12 9.86 0.22
885F unknown 1173 3.54 0.12 10.69 0.22
503F unknown 1173 3.59 0.12 8.74 0.22
706F NE (in Tx) 1173 3.71 0.12 8.65 0.22
680F NW 1173 3.72 0.12 9.34 0.22
1602F* W 1176 3.78 0.12 9.98 0.22
603F flat 1173 3.83 0.12 8.84 0.22
880F unknown 1173 3.93 0.12 10.53 0.22
906F* S 1173 4.44 0.12 10.25 0.22
605M* NE 1173 1.85 0.12 10.02 0.22
1350M* NE 1173 2.32 0.12 7.66 0.22
64
n
Hibernation Tb Emergence Tb
ID# & Sex Slope Mean (°C ) & SE Mean (°C ) & SE
406M* W 1173 2.58 0.12 9.83 0.22
615M* NW 1173 2.71 0.12 10.28 0.22
806M W 1173 2.78 0.12 9.52 0.22
1100M* S 1173 2.86 0.12 9.46 0.22
704M NE 1173 2.97 0.12 8.60 0.22
402M* SE 1173 3.07 0.12 8.57 0.22
904M W 1173 3.14 0.12 8.77 0.22
500M NE 1173 3.30 0.12 9.29 0.22
1150M NW 1173 3.34 0.12 9.05 0.22
504M unknown 1173 3.42 0.12 10.39 0.22
708M NW 1173 3.67 0.12 8.38 0.22
814M NW 1173 3.75 0.12 9.40 0.22
700M W 1173 3.79 0.12 9.71 0.22
848M flat 1173 3.81 0.12 9.67 0.22
1207M SE 1173 3.86 0.12 9.60 0.22
1253M E 1173 3.86 0.12 9.23 0.22
607M NW 1173 4.09 0.12 10.25 0.22
65
App
endi
x 3
Mea
n te
mpe
ratu
res a
nd st
anda
rd e
rror
s (SE
) rec
orde
d fr
om e
ach
dept
h al
ong
TPS
durin
g th
e hi
bern
atio
n an
d em
erge
nce
perio
ds.
Tem
pera
ture
s are
sepa
rate
d by
stak
e ha
bita
t typ
es (f
ores
ts, h
iber
nacu
la, &
cle
arcu
ts) a
nd b
y sl
ope
aspe
cts.
Sta
rred
(*) v
alue
s are
sign
ifica
ntly
diff
eren
t (P
< 0.
05 a
nd Δ
°C >
1) o
f mea
n va
lues
acr
oss h
abita
ts (f
ores
ts, h
iber
nacu
la, &
cle
arcu
ts) f
or a
ssoc
iate
d
ther
mal
per
iod
(hib
erna
tion/
emer
genc
e), s
lope
asp
ect,
and
dept
h.
H
iber
natio
n E
mer
genc
e
Slop
e D
epth
#
of
Rec
ords
For
ests
M
ean
& S
E
Hib
erna
cula
Mea
n &
SE
Cle
arcu
ts
Mea
n &
SE
Fore
sts
Mea
n &
SE
Hib
erna
cula
Mea
n &
SE
Cle
arcu
ts
Mea
n &
SE
NE
10
9387
-0
.56
0.33
-1
.17
0.27
-0
.80
0.27
11.1
5 0.
52
10.2
5*0.
43
11.7
1*0.
43
0 93
90
0.89
0.33
2.
01*
0.27
0.
800.
279.
88
0.52
8.
37*
0.43
10
.00
0.43
-10
9388
3.
460.
33
3.40
0.27
1.
73*
0.27
7.92
0.
52
7.41
*0.
43
8.77
*0.
43
-20
9390
4.
070.
33
3.94
0.27
2.
77*
0.27
7.41
0.
52
7.08
*0.
43
8.63
*0.
43
-30
9390
4.
330.
33
4.27
0.27
3.
16*
0.27
7.24
0.
52
6.89
*0.
43
7.98
*0.
43
E
10
1176
-0
.81
0.47
.
. .
. 11
.64
0.74
.
. .
.
0 Fa
iled
. .
. .
. .
. .
. .
. .
-10
1176
3.
420.
47
. .
. .
8.07
0.
74
. .
. .
-20
1176
4.
110.
47
. .
. .
7.89
0.
74
. .
. .
-30
Faile
d .
. .
. .
. .
. .
. .
.
SE
10
1172
.
. -0
.22
0.47
.
. .
. 11
.01
0.74
.
.
0 11
72
. .
3.06
0.47
.
. .
. 8.
930.
74
. .
66
H
iber
natio
n E
mer
genc
e
Slop
e D
epth
#
of
Rec
ords
For
ests
M
ean
& S
E
Hib
erna
cula
Mea
n &
SE
Cle
arcu
ts
Mea
n &
SE
Fore
sts
Mea
n &
SE
Hib
erna
cula
Mea
n &
SE
Cle
arcu
ts
Mea
n &
SE
-10
1172
.
. 4.
460.
47
. .
. .
7.96
0.74
.
.
-20
1170
.
. 4.
780.
47
. .
. .
7.55
0.74
.
.
-30
1172
.
. 5.
380.
47
. .
. .
7.51
0.74
.
.
S
10
2346
.
. -0
.33
0.33
.
. .
. 11
.90
0.52
.
.
0 23
46
. .
1.91
0.33
.
. .
. 9.
580.
52
. .
-10
2346
.
. 3.
720.
33
. .
. .
8.83
0.52
.
.
-20
2348
.
. 4.
340.
33
. .
. .
8.24
0.52
.
.
-30
2348
.
. 4.
970.
33
. .
. .
7.87
0.52
.
.
SW
10
7035
-0
.22
0.33
-1
.06
0.47
-0
.22
0.27
11.5
0 0.
52
12.0
00.
74
12.3
00.
43
0 70
35
2.26
*0.
33
0.88
0.47
0.
880.
279.
09*
0.52
10
.60
0.74
11
.31
0.43
-10
7035
4.
340.
33
3.69
0.47
2.
69*
0.27
9.22
0.
52
8.52
*0.
74
9.93
*0.
43
-20
7038
4.
390.
33
4.37
0.47
3.
790.
278.
16
0.52
8.
010.
74
9.65
*0.
43
-30
7036
5.
010.
33
5.14
0.47
4.
290.
277.
97
0.52
7.
710.
74
9.32
*0.
43
W
10
4690
-0
.56
0.47
-0
.80
0.27
.
. 11
.15
0.74
11
.83
0.43
.
.
0 46
93
2.15
0.47
1.
470.
27
. .
9.29
0.
74
9.57
0.43
.
.
-10
4693
3.
450.
47
3.75
0.27
.
. 8.
28
0.74
8.
400.
43
. .
-20
4691
3.
960.
47
4.47
0.27
.
. 7.
85
0.74
7.
940.
43
. .
-30
4693
4.
240.
47
5.14
0.27
.
. 7.
41
0.74
7.
750.
43
. .
67
H
iber
natio
n E
mer
genc
e
Slop
e D
epth
#
of
Rec
ords
For
ests
M
ean
& S
E
Hib
erna
cula
Mea
n &
SE
Cle
arcu
ts
Mea
n &
SE
Fore
sts
Mea
n &
SE
Hib
erna
cula
Mea
n &
SE
Cle
arcu
ts
Mea
n &
SE
NW
10
2342
.
. -0
.80
0.33
.
. .
. 11
.05
0.52
.
.
0 23
49
. .
1.67
0.33
.
. .
. 8.
570.
52
. .
-10
2349
.
. 3.
440.
33
. .
. .
7.71
0.52
.
.
-20
2349
.
. 4.
220.
33
. .
. .
7.53
0.52
.
.
-30
2347
.
. 4.
860.
33
. .
. .
7.26
0.52
.
.
68
Appendix 4
Pairwise comparisons of mean distances between turtle hibernacula since 2007 (‘07) as
part of a radiotelemetry study at the Hardwood Ecosystem Experiment in south-central
Indiana. Turtles often returned to locations used previously but not necessarily
consecutively.
Turtle ID ‘07 to ‘08 ‘07 to ‘09 ‘07 to ‘10 ‘08 to ‘09 ‘08 to ‘10 ‘09 to ‘10
402M 9.22 247.16 41.00 250.24 34.53 234.83
404F 55.00 . . . . .
406M . 3062.80 . . . .
500M . 155.72 146.29 . . 9.43
503F 544.82 55.04 60.03 580.55 354.22 6.40
504M 36.50 54.57 20.12 25.50 36.12 44.28
506F . 12.73 11.05 . . 22.36
603F . 38.08 98.90 . . 75.24
605M . 483.92 398.53 . . 91.02
607M . 42.54 34.01 . . 9.22
615M . . . . . 47.10
680F . . . . . 155.13
700M . . . . . 47.17
704M 39.56 47.27 55.03 10.82 15.65 13.93
706F 88.84 89.99 57.04 5.00 36.06 39.05
708M 45.54 166.00 156.42 132.65 124.48 11.00
787F . . . . . 13.89
800F . 12.04 20.62 . . 18.44
806M . 85.00 87.09 . . 89.05
814M . . . . . 132.62
848M . . . . . 5.83
880F . . . . . 97.05
885F . . . . . 538.03
69
Turtle ID ‘07 to ‘08 ‘07 to ‘09 ‘07 to ‘10 ‘08 to ‘09 ‘08 to ‘10 ‘09 to ‘10
900F . 236.14 227.73 . . 37.58
904M . 69.63 43.01 . . 22.36
906F 200.81 58.05 35.23 230.78 213.56 26.63
908M . 71.70 9.22 . . 23.60
1206F . . . . . 129.31
1207M . . . . . 10.44
1252F . . . . . 8.54
1253M . . . . . 47.43
1350M . . . . . 1800.64
1357F . . . . . 43.01
1360F . . . . . 43.86
1455f . . . . . 264.70
1602F . . . . . 24.70
Average 127.54 277.13 88.31 176.51 116.37 123.06
St. Dev. 178.49 704.67 99.43 205.44 126.37 313.89
Median 50.27 70.67 55.03 132.65 36.12 41.03
PUBLICATION
70
PUBLICATION
71
72
73
74
75
76