nesting ecology of the eastern box turtle in a fragmented...
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NESTING ECOLOGY OF THE EASTERN BOX TURTLE
(TERRAPENE CAROLINA CAROLINA) IN A FRAGMENTED LANDSCAPE
by
Rebecca Lynn Kipp
A thesis submitted to the Faculty of the University of Delaware in partial fulfillment of the requirements for the degree of Master of Science in Entomology and Applied Ecology
Summer 2003
Copyright 2003 Rebecca Lynn Kipp All Rights Reserved
NESTING ECOLOGY OF THE EASTERN BOX TURTLE
(TERRAPENE CAROLINA CAROLINA) IN A FRAGMENTED LANDSCAPE
by
Rebecca Lynn Kipp
Approved: __________________________________________________________ Jacob L. Bowman, Ph.D. Professor in charge of thesis on behalf of the Advisory Committee Approved: __________________________________________________________ Douglas W. Tallamy, Ph.D. Chair of the Department of Entomology and Wildlife Ecology Approved: __________________________________________________________ Robin W. Morgan, Ph.D. Dean of the College of Agriculture and Natural Resources Approved: __________________________________________________________ Conrado M. Gempesaw II, Ph.D. Vice Provost for Academic Programs and Planning
ACKNOWLEDGMENTS
Many thanks to Dr. Jacob Bowman, who gave me the opportunity to conduct
my Master’s research on turtles and provided much encouragement and assistance
over the past 3 years. I also thank him for reading many revisions of my thesis and
always taking time to help improve my writing. I thank Nathan Nazdrowicz sharing
his knowledge of box turtles and nesting ecology and for being such a great help with
my research. I thank all the undergraduate research assistants who devoted their time
and energy to this project, including Jordona Doughty, Raymond Iglay, Rebekah
Baity, Isabelle Lajoie, Adam Porter, and Christopher Howey. I thank the New London
Veterinary Center for conducting x-rays at a reduced rate in 2001. I thank Tri-State
Bird Rescue and Research for donating the use of their equipment in 2002, and Andrea
Howey for volunteering her time to conduct x-rays. I also thank my committee
members Drs. Roland R. Roth, Donald C. Forester, and Douglas W. Tallamy for
taking the time to serve on my committee.
I thank the Delaware Division of Parks and Recreation for allowing access to
White Clay Creek State Park and waiving park entrance fees. I also thank the
Frederick family for encouraging this research project and allowing us full access to
the Turkey Run property. Funding support was provided by the MacIntire-Stennis
Cooperative Forestry Program.
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Lastly, I thank my parents for helping me pursue my dreams and always
providing their help and encouragement. Without their support, I would not have been
able to take my time in deciding which direction to go with my life. Thanks also to
Kristopher Pickard for spending endless hours in the field, staying up late at night with
nesting turtles, and giving me all the support and encouragement I needed to make it
through the longest 3 years of my life.
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TABLE OF CONTENTS
LIST OF TABLES .......................................................................................................vii LIST OF FIGURES....................................................................................................... ix ABSTRACT .................................................................................................................. xi INTRODUCTION……………………………………………………………………..1
Nest Site Selection………………………………………………………...2
Clutch Frequency………………………………………………………….4
Survivorship……………………………………………………………….5
Objectives…………………………………………………………………6
STUDY AREAS……………………………………………………………………….8
University of Delaware Woodlot………………………………………...12
University of Delaware Webb Farm Woodlot…………………………...15
Turkey Run Property…………………………………………………….17
White Clay Creek State Park…………………………………………….19
METHODS…………………………………………………………………………...22
Capture and Marking…………………………………………………….22
Radiotelemetry…………………………………………………………...23
Nesting…………………………………………………………………...25
Nest Site Selection……………………………………………………….26
Analyses………………………………………………………………….28
RESULTS…………………………………………………………………………….31
Nesting Behavior………………………………………………………...33
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Clutch Size and Frequency………………………………………………36
Nest Site Selection……………………………………………………….40
Nest Success…………………………………………………………..…48
Nest Site Fidelity………………………………………………………...55
Incubation Period and Hatchling Emergence……………………………56
DISCUSSION………………………………………………………………………...58
Nesting Behavior………………………………………………………...59
Clutch Size and Frequency………………………………………………61
Nest Site Selection……………………………………………………….62
Nest Success……………………………………………………………..66
Nest Site Fidelity………………………………………………………...68
Incubation Period and Hatchling Emergence……………………………69
Management Implications……………………………………………….70
LITERATURE CITED……………………………………………………………….73
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LIST OF TABLES
Table 1. Average monthly minimum and maximum temperatures and total monthly precipitation for the 2001 – 2002 field seasons in Newark, Delaware (National Oceanic & Atmospheric Administration 2001, 2002)……..…11
Table 2. A summary of egg-laying behavior for the 2001 – 2002 field seasons for eastern box turtles in 4 populations in northern Delaware………………35 Table 3. A summary of timing of nesting behavior at 39 eastern box turtle nests on
4 study areas in northern Delaware during the 2001 - 2002 field seasons…………………………………………………………………...37
Table 4. Clutch size of eastern box turtles by study area during the 2001 – 2002
field seasons in northern Delaware………………………………………41 Table 5. The relationship of morphometric measurements to clutch size of female
eastern box turtles in northern Delaware during the 2001 – 2002 field seasons…………………………………………………………………...42
Table 6. Distances eastern box turtle females moved (m) during the 2001 and 2002
field seasons at 4 study areas in northern Delaware. Distances moved differed among study sites (F3, 33 = 15.40, P < 0.001)………………..….43
Table 7. Summary of microhabitat characteristics for 39 eastern box turtle nests
and random plots on 4 study sites in northern Delaware during 2001 and 2002. A paired t-test was used to detect differences between nests and random plots……………………………………………………………..49
Table 8. Summary of microhabitat characteristics for 39 eastern box turtle nests at
nesting, 1 month after nesting, and 2 months after nesting in northern Delaware during 2001 – 2002. A repeated measures ANOVA was used to detect differences in variables across time…………………………….....50
Table 9. Eggs hatched for each successful nest in the 2001 – 2002 field seasons during an eastern box turtle study in northern Delaware………………...52
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Table 10. Timing of predation for eastern box turtle nests in northern Delaware for the 2001 – 2002 field seasons…………………………………………..54
Table 11. Estimated incubation length (in days) for eastern box turtle nests in
northern Delaware for the 2001 – 2002 field seasons………….……….57
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LIST OF FIGURES
Figure 1. Aerial photograph (1997) showing proximity of eastern box turtle populations at the University of Delaware Webb Farm Woodlot (top) and University of Delaware Woodlot (bottom) study areas in Newark, Delaware during 2001 - 2002……………………………………….……..9
Figure 2. Aerial photograph (1997) showing proximity of eastern box turtle
populations at Turkey Run Property (top) and White Clay Creek State Park (bottom) study areas in Newark, Delaware during 2001 – 2002…………10
Figure 3. Aerial photograph (1997) of the University of Delaware Woodlot in
Newark, Delaware used during 2001 – 2002 for an eastern box turtle study……..………………………………………………………………...13
Figure 4. Aerial photograph (1997) of the University of Delaware Webb Farm
Woodlot in Newark, Delaware used during 2001 – 2002 for an eastern box turtle study………………………………………………………………...16
Figure 5. Aerial photograph (1997) of the Turkey Run Property in Newark, Delaware
used during 2001 – 2002 for an eastern box turtle study………………….18 Figure 6. Aerial photograph (1997) of an interior portion of White Clay Creek State
Park in Newark, Delaware used during 2001 – 2002 for an eastern box turtle study………………………………………………………………...20
Figure 7. The number of gravid eastern box turtles by week for the 2001 and 2002
field seasons in northern Delaware. Data were based on x-ray results and known nesting dates. X-rays were not conducted until the first week of June in 2001……………………………………………………………….32
Figure 8. Range of clutch sizes of female eastern box turtles during the 2001 and 2002 field seasons in northern Delaware……………………………..39 Figure 9. Eastern box turtle nest locations at White Clay Creek in Newark, Delaware
for the 2001 – 2002 field seasons. Circles represent 2001 nests and squares represent 2002 nests………………………………………………………44
Figure 10. Eastern box turtle nest locations at Turkey Run in Newark, Delaware
during the 2001 – 2002 field seasons. Circles represent 2001 nests and squares represent 2002 nests. Circled nests are from a female that nested in the same location in consecutive years………………………………...45
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Figure 11. Eastern box turtle nest locations at Webb Farm in Newark, Delaware during the 2001 – 2002 field seasons in northern Delaware. Circles represent 2001 nests and squares represent 2002 nests. Circled nests are from a female that nested in the same location in consecutive years…..…46
Figure 12. Eastern box turtle nest locations at the UD Woodlot in Newark,
Delaware during the 2001 – 2002 field seasons. Circles represent 2001 nests and squares represent 2002 nests. Circled nests are from a female that nested in the same location in consecutive years. Nest in upper left- hand corner is shown with an arrow……………………………………...47
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ABSTRACT
A paucity of information is available on the nesting ecology of the eastern box
turtle (Terrapene carolina carolina). Specifically, minimal research has been
conducted on nest site selection and how it relates to nest success. I investigated all
aspects of nesting ecology (nesting behavior, nest site selection, clutch size and
frequency, nest success, and nest site fidelity) and compared them among 4 study
sites: 3 with varying degrees of disturbance and 1 interior forest area. I used
radiotelemetry to relocate female box turtles in order to determine their reproductive
status throughout the nesting seasons in 2001 and 2002. Using x-ray photography of
38 radio transmittered females, I determined the presence and number of eggs. Thirty-
two females were gravid at least once during my study and egg retention varied from a
minimum of 7 – 26 days. The earliest documented nesting date was 27 May and the
latest was 11 July. Gravid females moved long distances to nest (up to 450 m), and
females in the interior forest moved more than 3 times farther than those at other study
areas. I monitored gravid females to observe nesting behavior and mark nest sites.
Clutch size ranged from 1 – 9 eggs, and was positively related to female body size.
Out of a sample of 57 gravid females, I marked and monitored 39 nests to determine
nest fate. Females most often nested in areas with an open canopy, sun exposure for
part of the day, and in close proximity to a forest edge. Nest sites had less canopy
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cover and a lower percentage of grass and forbs than random sites, whereas exposure
to sunlight and percentages of vines, woody vegetation, woody debris, organic litter,
and other life forms, did not affect nest site selection. Similar numbers of nests were
successful (n = 12), had inviable eggs (n = 13), or were depredated (n = 11).
Percentage of successful nests was greatest at the most fragmented areas (50%, 45%,
31%), whereas success at the interior forest area was less than 1%. Two study sites
with moderate disturbance produced more hatchlings each than either the interior
forest site or the most disturbed site. Incubation periods ranged from 67 – 105 days.
Although the nesting period lasted from late May to early July, hatchlings emerged
during the same time period in September. Since nests in more fragmented areas were
more likely to be at roadside edges or in agricultural cropland, females may nest in
unsuitable areas when other suitable habitat is not available. My data suggest that
fragmented forest areas contain box turtle populations with limited choices for nesting,
which could eventually affect recruitment and population stability.
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INTRODUCTION
Long-lived vertebrates, such as turtles, generally share the life history traits of
delayed sexual maturity and extended longevity (Congdon et al. 1993), which have
advantages and disadvantages. Females become sexually mature at a larger size,
permitting a selective advantage for larger eggs and possibly greater fecundity (Brooks et
al. 1991). Delayed sexual maturity may result in females producing either more or higher
quality offspring (Congdon and van Loben Sels 1993). Larger body size also reduces the
predation risk on adults (Brooks et al. 1991). Additionally, larger females should have a
lower metabolic cost for their weight and be able to reproduce with a lower risk of energy
depletion. Because box turtles have a long juvenile growth period, this species may be
vulnerable to increased juvenile mortality. However, box turtles lay small clutches with
large eggs, which should result in larger hatchling size and increased hatchling and
juvenile survivorship (Tucker et al. 1978). Stable populations cannot be maintained
without concurrent survivorship of reproductive-age adults and a reasonable survivorship
rate of both hatchlings and juveniles (Congdon et al. 1993).
Box turtle populations have declined throughout their range because of
agricultural development, road mortality, collection for the pet trade, and habitat
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alteration (Warwick 1993, Belzer 1997). Box turtle habitat has become increasingly
fragmented by roads, agricultural development, and urban development. Fragmentation
alters the biological and physical components of the ecosystem. Changes in the
environment are manifested in decreased vegetation cover, causing increased solar
radiation, and higher soil temperatures, which promotes desiccation and reduces foraging
opportunities for box turtles (Saumure and Bider 1998). The effects of changing
environmental conditions, such as habitat loss, may influence reproductive potential and
cause a species to decline. In order to maintain reasonable population sizes, habitat must
be available in continuous areas large enough to provide habitat for box turtles and
support a population. If sufficient nesting habitat does not exist within a box turtle’s
home range, then nesting may occur in locations where eggs or hatchlings will not
survive.
Nest Site Selection
Box turtle nesting usually occurs from May through July (Ernst et al. 1994). Most
nests are dug in the evening, with the nest excavation process beginning at approximately
1700 to 1900 hours and continuing for 2 - 4 hours (Allard 1948, Congello 1978, Dodge et
al. 1978). Nests are normally located in open, cleared, elevated patches of sandy or loam
soil where the sun can penetrate through the foliage during daylight hours (Congello
1978, Ernst et al. 1994) and may be located outside a female’s home range (Stickel 1950,
Stickel 1989). Little research has addressed nest site selection and whether females will
travel beyond their home range to find a suitable nesting location.
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Thermal cues, interspecific competition, vegetational cover, and human
disturbances may influence nest site selection (Wang and Cheng 1999). Nest site
selection (e.g., nest placement and soil characteristics) can influence the hatching success
of each nest as well as the reproductive viability of the entire population (Allard 1948,
Roosenburg 1996, Wang and Cheng 1999). Incubation length is dependent on soil
temperature, which may be influenced by air temperature, amount of shade, soil type, and
rainfall (Allard 1948). Clutches incubated at lower temperatures (22.5 – 27.0° C)
produce mostly males, whereas clutches incubated at ≥28.5 °C produce mainly females
(Ernst et al. 1994). Ewert and Nelson (1991) discovered that the sex ratio was 73% male
at 22.5°C, 96% male at 25°C, and 81% male at 27°C, while no males were produced at
30°C. Therefore, nest site selection is important for determining incubation length and
the sex ratio of a clutch.
Certain environmental characteristics such as surface temperature, ground
temperature, and vegetation cover are correlated with nest success, so females should nest
at sites exhibiting these parameters (Morjan and Valenzuela 2001). Females may
discriminate among a variety of nest sites to choose 1 with specific thermal
characteristics (Roosenburg 1996). Janzen (1994) hypothesized that females may use
solar exposure to predict nest temperatures. Once nesting is complete, the condition of
the developing eggs is subject to stochastic weather patterns, exposure, soil type, and
vegetation (Gutzke et al. 1987). The soil type in which the nest occurs is an important
characteristic of nest site selection since the depth of the topsoil layer may fluctuate
during egg development (Montevecchi and Burger 1975). Vegetational cover also plays
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an important role in nest site selection. Females may use vegetation cover at nest
initiation as a cue to predict the long-term temperature of the nest site (Janzen and
Morjan 2001). If agronomic crops or open fields surround a fragmented forest area,
vegetational cover would be absent or minimal and may provide for inappropriate nesting
sites, because concentrated or extended periods of direct sunlight could cause nest
dessication or alter hatchling sex ratios. Thus, females may use nest site selection to alter
sex ratio of hatchlings, as Roosenburg (1996) suggested.
Stickel (1989) documented female box turtles extending their home ranges from
bottomland forests to nest in drier upland areas and returning to the same nesting area
each year. Gravid female yellow-margined box turtles (Cuora flavomarginata) left an
interior forest area and moved to the forest edge or open areas during the nesting season
(Lue and Chen 1999). Snapping turtles (Chelydra serpentina) demonstrated strong nest
site fidelity, even if they had to travel long distances under rugged conditions (Loncke
and Obbard 1977, Obbard and Brooks 1980). Since box turtles can also travel long
distances to nesting sites, we can assume that they are capable of complex navigation like
snapping turtles. Therefore, research to determine if females will travel outside their
home range to nest and if living in a forest fragment will affect nest site selection is
warranted. Additionally, if females are choosing unsuitable nesting sites, will they show
nest site fidelity and return to the same location to nest annually?
Clutch Frequency
An important aspect of box turtle nesting ecology is clutch frequency. Most
species of box turtles lay 1 - 7 clutches annually (Dodd 2001). Clutch frequency is
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variable with the annual number of clutches ranging from 1 - 2 in the eastern box turtle
(Terrapene carolina carolina; Ernst et al. 1994). Captive three-toed box turtles
(Terrapene carolina triunguis) laid 2 - 6 clutches per year (Messinger and Patton 1995),
while Florida box turtles (Terrapene carolina bauri) lay from 0 - 3 clutches per year
(Dodd 1997). More than 1 clutch per season would be beneficial due to low rates of nest
success and the possibility of some eggs being infertile (Congello 1978, Dodge et al.
1978). Annual clutch frequency can affect population stability and should be
investigated in fragmented landscapes.
Survivorship
In many turtle populations, survivorship of eggs, hatchlings, and juveniles is low. Predation and weather cause low hatchling recruitment (Brooks et al. 1991). Probability
of nest predation is a function of the probability of a potential predator searching the area
and ease of nest location (Brooks et al. 1991). Additionally, turtle nests are subjected to
greater predation during and after rainfall events (Congdon et al. 1987). Eggs are
depredated by badgers (Taxidea taxus), skunks (Mephitis mephitis), foxes (Urocyon
cinereoargenteus, Vulpes vulpes), raccoons (Procyon lotor), crows (Corvus spp.), and
snakes (Cemophora coccinea, Heterodon spp., Lampropeltis spp.), as well as destroyed
by inclement weather (Ernst et al. 1994). Crows, vultures (Cathartes aura, Coragyps
atratus), Mississippi kites (Ictinia mississippiensis), barn owls (Tyto alba), and snakes
(Agkistrodon contortrix, A. piscivorus, Coluber constrictor) have been documented
preying on hatchlings and young juveniles (Ernst et al. 1994).
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Adult box turtle mortality results from natural and human induced factors.
Raccoons, skunks, coyotes (Canis latrans), dogs (C. familiaris), foxes, and sudden
climactic changes are known to cause adult mortality (Ernst et al. 1994). Adult female
mortality rate is another important aspect of box turtle nesting ecology and might be
exacerbated by forest fragmentation. Females forced to select alternative nesting sites
may increase their mortality probability by where they select to travel or lay their eggs.
Females may have to cross roads or travel through developed areas or agricultural land to
find appropriate nesting locations. These movements may increase adult female
mortality caused by automobiles or farm machinery (Saumure and Bider 1998). Gibbs
and Shriver (2002) indicated that road mortality was a component of habitat
fragmentation for terrestrial and semiterrestrial turtles, thereby contributing to their
decline. Nieuwolt (1996) documented a tendency of western box turtles (Terrapene
ornata luteola) to use a dirt road within her study site to do most of their movement.
When roads fragment box turtle habitat, the likelihood of turtles being killed by
automobiles or collected as pets increases dramatically (Doroff and Keith 1990).
Empirical evidence is needed to determine the effect of fragmentation on female
survivorship.
Objectives
A paucity of research exists on how box turtles living in fragmented landscapes
choose nest sites. By doing a comparative study on nest site selection, I documented how
females chose nesting sites when limited land areas were available and success of nests at
these sites. I collected empirical evidence to determine if nesting success changed due to
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undesirable nesting conditions (i.e., in a forest fragment) and if adult populations also
suffered as a result. My objectives were to investigate nesting ecology of eastern box
turtles in a fragmented landscape (including clutch size and frequency, length of
incubation, distances traveled to nest, and nest site fidelity), to determine if fragmentation
affected nesting behaviors (site selection, digging, egg deposition, and concealment), to
determine if fragmentation affected nest site selection of eastern box turtles, and to
determine if fragmentation affected nest success of eastern box turtles.
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STUDY AREAS
I conducted my research on 4 study sites, including 3 forest fragments and 1
interior forest area in northern Delaware. The University of Delaware Woodlot and
University of Delaware Webb Farm Woodlot were small, isolated forest fragments
located on the University of Delaware campus in Newark, Delaware in New Castle
County (Figure 1). The Turkey Run property was moderately isolated, fragmented, and
adjacent to contiguous forested areas of White Clay Creek State Park, whereas the
interior forest area was within White Clay Creek State Park (Figure 2). Both sites were
located approximately 8 km north of the University of Delaware sites in New Castle
County.
The temperature during the study period (May to October 2001 and 2002) ranged
from -2 – 20˚C and 46 – 88˚C for mean minimum and maximum temperatures,
respectively (Table 1). During the 2001 nesting season (May to October), the mean
minimum and maximum temperatures were 15.5˚C and 26.1˚C, respectively. The mean
minimum and maximum temperatures were 15.6˚C and 26.9˚C, respectively, during the
2002 nesting season. Northern Delaware experienced a drought throughout the summer
of 2001, with precipitation below normal by at least 5 cm (D. J. Leathers, Delaware State
Climatologist, personal communication). These dry conditions may have influenced nest
8
Figure 1. Aerial photograph (1997) showing proximity of eastern box turtle populations at the University of Delaware Webb Farm Woodlot (top) and University of Delaware Woodlot (bottom) study areas in Newark, Delaware during 2001 – 2002.
9
Figure 2. Aerial photograph (1997) showing proximity of eastern box turtle populations at Turkey Run Property (top) and White Clay Creek State Park (bottom) study areas in Newark, Delaware during 2001 – 2002.
10
Table 1. Average monthly minimum and maximum temperatures and total monthly precipitation for the 2001 – 2002 field seasons in Newark, Delaware (National Oceanic & Atmospheric Administration 2001, 2002).
Minimum Temp.1
Maximum Temp.2
Precipitation3
May 2001
11.6
22.6
13.56
June 2001 17.5 28.0 10.87 July 2001 17.4 27.8 6.02
August 2001 20.1 30.2 6.68 September 2001 13.1 24.3 6.53
October 2001 7.2 20.3 1.85 November 2001 3.9 16.9 2.51 December 2001 1.0 10.7 4.95
January 2002 -1.3 7.7 6.91 February 2002 -1.6 9.8 1.09
March 2002 1.5 12.2 10.29 April 2002 7.2 19.1 5.74 May 2002 10.4 22.3 8.64 June 2002 16.7 27.5 12.57 July 2002 19.7 30.8 3.56
August 2002 19.8 31.1 5.16 September 2002 15.1 26.4 8.69
October 2002 8.7 17.4 15.62
1 Minimum average monthly temperature (ºC) 2 Maximum average monthly temperature (ºC) 3 Total monthly precipitation (cm)
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site selection and ultimately, nest success.
University of Delaware Woodlot
Turtles in the UD Woodlot were isolated from other turtle populations and were
never documented leaving the areas directly adjacent to the woodlot. A 2.4-m high
chain-link fence surrounded the perimeter of the woodlot; however, multiple holes along
the bottom of the fence allowed turtles to easily enter and exit the woodlot (Niederriter
2000). Since the woodlot was completely surrounded by a fence with a locked gate, only
University of Delaware researchers had access to the interior of the woodlot for research
purposes. Webb Farm, located approximately 1 km northeast of the UD Woodlot, was
separated by a series of agricultural fields and a 2-lane highway (Figure 1).
The woodlot (16-ha forest fragment) was bordered on 3 sides by roads (Figure 3).
A dirt road to the north separated the woodlot from cornfields (east) and a small orchard
(west). Grassy areas along the edge of the woodlot and throughout the orchard were
mowed a few times a month and maintained at a height of 5 – 10 cm. Turtles
occasionally crossed the dirt road and moved into the orchard. A lightly traveled, paved
road to the west separated the woodlot from athletic fields and a parking lot. Turtles
occasionally crossed this road, but no appropriate habitat existed west of the road. The
grassy area along the entire western edge of the woodlot was maintained at a height of 5
– 10 cm. A 4-lane highway to the south paralleled the southern edge of the woodlot,
separated by a narrow dirt road and an old fence surrounded by an area of edge habitat
adjacent to the road. Two turtles often moved into this edge habitat and stayed there for
much of the active season. This highway had a high curb (20 cm) and appeared to be a
12
Figure 3. Aerial photograph (1997) of the University of Delaware Woodlot in Newark, Delaware used during 2001 – 2002 for an eastern box turtle study.
13
barrier to turtle movement. A small, infrequently mowed meadow was located in the
northeast corner of the woodlot and often used by 2 females. An athletic field formed the
southeastern border, and an alfalfa field the upper east side of the woodlot. A few turtles
used the edge areas adjacent to the athletic field, but rarely moved into the field except to
reach the edge habitat along the 4-lane highway. Turtles used the alfalfa field during my
study, and we documented 4 mortalities during mowing of this field from 2000 to 2002.
Most of the UD Woodlot was over 130-year-old second growth, whereas the eastern and
southern portions contained 70-year-old second growth (Gorman and Roth 1989).
Common tree species were white oak (Quercus alba), swamp white oak (Q. bicolor),
chestnut oak (Q. prinus), red oak (Q. rubra), black oak (Q. velutina), pin oak (Q.
palustris), mockernut hickory (Carya tomentosa), pignut hickory (C. glabra), tulip poplar
(Liriodendron tulipifera), sweet gum (Liquidambar styraciflua), and red maple (Acer
rubrum) (Gorman and Roth 1989). The understory was dominated by poison ivy
(Toxicodendron radicans), viburnums (Viburnum spp.), pepperbush (Clethra alnifolia),
spicebush (Lindera benzoin), greenbriar (Smilax spp.), and multiflora rose (Rosa
multiflora).
The UD Woodlot contained a small box turtle population that had been studied in
some capacity for the past 37 years. During 1965, 65 turtles were captured and marked
by notching the carapace. Incidental turtle captures were documented and turtles marked
during 1966 - 1998 by researchers studying other fauna in the woodlot. A study in 1999
monitored spatial use of the box turtle population (Niederriter 2000).
14
University of Delaware Webb Farm Woodlot
This 12-ha forest fragment was isolated from other turtle populations (Figure 1)
and all turtles captured in this area stayed within the confines of Webb Farm. This area
was subjected to agricultural management in the cornfields, but no mowing occurred
anywhere on the study area. Inhabitants of the local neighborhoods, mainly children,
occasionally used the forested area of Webb Farm on the eastern side. This woodlot was
a forested area with an open meadow along the southern border where turtles spent most
of their time during the active season. Webb Farm was bordered by a welded wire fence
and cow pastures along the western edge (Figure 4). Horse pastures bordered the
southern edge, but were separated from Webb Farm by a stream and a welded wire fence.
Two cornfields bordered the northwestern portion of Webb Farm and were plowed once a
year. A small meadow was located between the forest edge and the cornfield, and turtles
often moved into this area. A 2-lane, heavily traveled highway along the northwestern
border was separated from Webb Farm by a 2-m high chain-link fence. A small, wooded
area existed directly across the highway from Webb Farm, but turtles were never
documented moving into this area. A residential development bordered the lower east
edge of Webb Farm, but was separated from the woodlot by fences bordering the
backyard of each house. Along the upper east edge of Webb Farm was an adjacent small,
forested area that backed up to the housing development.
The overstory consisted of red and white oaks, red maple, tulip poplar, black gum
(Nyssa sylvatica) (Bartlett 1991) and black cherry (Prunus serotina). The understory
included poison ivy, viburnums, greenbriar, and multiflora rose. Common plants in the
15
Figure 4. Aerial photograph (1997) of the University of Delaware Webb Farm Woodlot in Newark, Delaware used during 2001 – 2002 for an eastern box turtle study.
16
meadow were sedges (Carex spp.), grasses, ragweed (Ambrosia trifida), goldenrod
(Solidago spp.), poison ivy, greenbriar, and buttonbush (Cephalanthus occidentalis).
Turkey Run Property
The Turkey Run site was a privately owned, 13-ha forest fragment with mowed
pathways and open fields fragmenting the forested area (Figure 5). Turkey Run was
adjacent to the property owner’s house to the east and another property to the south,
which was bordered on 2 sides by White Clay Creek State Park. A paved road was
parallel to the northern edge of the property. Across the paved road were individual
houses that backed up to various housing developments. Hay fields, owned and managed
by White Clay Creek State Park, bordered the entire western edge of Turkey Run.
The overstory consisted of oak species, tulip poplar, and dogwood (Cornus
floridanus), with an understory primarily composed of multilflora rose and autumn olive
(Elaeagnus umbellata). Several fields were part of Turkey Run, and were connected by
various open, grassy areas and wide pathways throughout the study site.
Turtles captured at Turkey Run often moved into adjacent forested habitats such
as White Clay Creek State Park, including the interior forest area for this study (Figure
2). Although Turkey Run was a fragmented area, there was sufficient contiguous forest
habitat surrounding the study area so that turtles could easily move into other areas, and
were sometimes documented off the study site.
Box turtles on the Turkey Run property were marked with notches from 1993 –
2000 for a research study. Turkey Run was frequently disturbed by human interference,
17
Figure 5. Aerial photograph (1997) of the Turkey Run Property in Newark, Delaware used during 2001 – 2002 for an eastern box turtle study.
18
primarily the mowing of open, grassy areas and pathways several times a year.
White Clay Creek State Park
A 15-ha interior forest area was selected within White Clay Creek State Park
(Figure 6). The site was a forested area completely surrounded by protected, forested
land, but was bordered by a lightly traveled road on park property with a low speed limit
and was at least 200 m from any field. This area provided a comparison of a natural
forested area to fragmented areas. Turtles captured within our study area did not always
remain on this area and a few turtles relocated to areas outside of White Clay Creek
entirely. Turtles captured at White Clay Creek were also found on the Turkey Run
property, specifically females during the nesting season. Turkey Run was connected to
White Clay Creek via a 500 m, forested corridor, enabling turtles to move between these
areas (Figure 2).
Common overstory species were red maple, tulip poplar, American sycamore
(Platanus occidentalis), black walnut (Juglans nigra), and dogwood. The understory
consisted of multiflora rose, autumn olive, spicebush, and Chinese privet (Ligustrum
sinense). Wet lowland areas were common along a stream, including a small cypress
swamp near the center of the study area, which was dominated by bald cypress
(Taxodium distichum) and skunk cabbage (Symplocarpus foetidus). Several upland,
grassy areas were present and turtles often stayed in these areas for extended time
periods.
The study area within White Clay Creek State Park was relatively undisturbed by
human presence. Traffic on the park road was minimal, with a speed limit of 15 mph.
19
Figure 6. Aerial photograph (1997) of an interior portion of White Clay Creek State Park in Newark, Delaware used during 2001 – 2002 for an eastern box turtle study.
20
Park rangers patrolled the park by vehicle and on foot. A park trail was present inside the
eastern border of the study area. The park was used year-round for hiking, jogging, dog-
walking, and biking, mainly on the wide, dirt pathway that made up the park trail.
21
METHODS
My study was part of a larger study investigating eastern box turtle ecology in a
fragmented landscape. The overall study focused on population ecology, determination
of home ranges, macrohabitat and microhabitat use, movement rates, and nesting
ecology. All methods not specific to nesting were conducted as part of the overall project
and were standardized. Hereafter I use “we” to designate when data were collected by
others and myself. All capture and handling procedures were approved by the University
of Delaware Institutional Care and Use Committee (#1083).
Capture and Marking
We located box turtles using random searches and accidental encounters from
March 2001 to November 2002. For each turtle captured, we recorded capture location,
sex, age, and morphometric measurements, and we marked previously unmarked turtles.
Morphometric measurements included the height, length, and width of the carapace,
length and width of the plastron, and body mass. Using digital calipers, we measured
straight carapace length from the first marginal scute to the last marginal scute, straight
carapace width at the articulation of the second and third vertebral scutes, and carapace
height at the third or fourth vertebral scute (Boucher 1999). We measured plastron length
along the midline (anterior and posterior of the hinge) and plastron width at the hinge.
22
All measurements were recorded to the nearest millimeter, and all turtles were weighed to
the nearest gram with a Pesola® scale. We determined gender using secondary sexual
characteristics. Concave plastrons, strongly curved hind claws, and long, thick tails
identified males (Stuart and Miller 1987, Ernst et al. 1994). Males usually have a red or
orange iris, but this characteristic is not a completely reliable feature (Stuart and Miller
1987). The female carapace is more domed; the plastron is flat or convex; and the hind
claws are shorter, narrower, and straighter (Ernst et al. 1994). Also, females tend to have
a yellowish brown iris (Ernst et al. 1994). We classified all turtles <110 mm in length or
<10 annuli as juveniles and did not sex them, because they lacked secondary sexual
characteristics of adults (Schwartz and Schwartz 1974).
We marked all turtles for individual identification by notching the carapace with a
metal file using the marking system described by Cagle (1939). This method involved
filing a unique combination of notches to make permanent marks on marginal scute(s).
We filed no more than 2 notches in a scute and did not mark scutes proximal to the
carapace bridge. This system allows for identification at recapture and does not harm the
turtle (Cagle 1939).
Radiotelemetry
Each turtle was captured in the field, transported to the laboratory in a cloth bag,
and kept in a bucket. We used epoxy to attach 26.5-g radio transmitters (164 – 165 MHz;
Advanced Telemetry Systems, Isanti, Minn.) to a costal scute so as not to hinder normal
activity and behavior. Scute margins where growth occurs were not covered with epoxy,
since it can inhibit growth. To allow the epoxy to harden and ensure proper transmitter
23
placement, we kept the turtles overnight and duct taped the transmitter in place. We
released turtles the following day at the capture location. Boarman et al. (1998)
documented that radio transmitters can be attached without causing shell deformities,
predator attraction, or mating disruption. Transmitters had duty cycles of 11 hours on/13
hours off and an 1100-day battery life. We attached transmitters to the first 10 males and
10 females captured at each study area, except for the UD Woodlot, where we attached
radiotransmitters to all turtles located (12-16 across the course of the study).
We located transmittered turtles 5 times a week during the active season (May 15
- October 15), 3 - 5 times a week from October 15 – December 15 when activity
decreased, and once a week throughout the winter hibernation period (December 15 -
May 15). We located radio transmittered turtles by homing with a handheld receiver
(Telonics TR-2 in 2001 [Telonics, Inc., Mesa, Ariz.]; ICOM IC-R10 in 2002 [Icom
America Inc., Bellevue, Wash.]) and an Adcock antenna (metal in 2001, rubber in 2002).
We staggered radiolocations throughout the day to observe activity patterns and
behaviors at varying times of day.
Data collection for recaptured turtles, including radiolocated turtles, included time
and date of capture, location, and activity and behavior at first sighting. We made
observations to minimize stress on turtles without hindering normal activity or causing
any variation from routine behavior. We georeferenced each location using a Global
Positioning System (GPS) unit (Geo-Explorer III, Trimble Navigation Ltd., Sunnyvale,
Calif.). We recorded activity at first sighting of each turtle with the classifications used
by Boucher (1999): walking, basking, feeding, mating, resting, or resting form. We
24
recorded any additional data concerning hibernation, aggression, interaction or close
proximity to another turtle, and any nesting behaviors.
Nesting
During the nesting season, I x-rayed females approximately every 10 days in 2001
and every 7 days in 2002 to determine if they were gravid and the number of eggs
present. In 2001 and occasionally in 2002, we collected turtles the day before x-raying,
kept them overnight in the laboratory, and released them the same morning after x-
raying. In 2002, after x-raying, we returned all turtles to the capture location that day.
We transported females to the laboratory in cloth bags. To prevent spreading diseases
among study sites, we kept turtles in partitioned, plastic containers by study area. In
2001, x-rays were taken at a local veterinary center. In 2002, x-rays were taken at a
wildlife rehabilitation clinic.
We monitored gravid females each evening (approximately 1900 - 2100 in 2001
and 1700 - 2100 in 2002) until the turtle was seen nesting or the next x-ray showed that
eggs were no longer present. Once nesting behavior was established, I recorded time of
first observation of nest initiation behavior (i.e., when the female began to dig), as well as
soil temperature and ambient temperature posterior to the turtle. I also recorded the time
egg deposition began, and I removed eggs temporarily to record wet egg mass, length,
and diameter, when possible. I only collected these egg measurements for the first few
nests; at which point, I decided it was too difficult to remove the eggs from the nest
without disturbing the female. I documented clutch size for comparison with x-ray data.
During egg deposition, I deposited a HOBO® temperature logger (Onset Technology Inc.,
25
Santa Cruz, Calif.) into the nest among the eggs when possible. This data logger
recorded nest temperature every 4 hours. I recorded time of nest completion (i.e., when
the nest was concealed), along with soil and ambient temperature posterior to the turtle. I
marked the nest for relocation by recording the coordinates using a GPS, marking the
nearest tree with flagging, and taking a compass bearing and distance from the tree to the
nest. I also marked the nest with a permanent marker in the ground placed next to the
nest, an 8.9 x 1.3 cm piece of PVC pipe with a galvanized metal bolt inside the pipe,
which was hammered into the ground near the nest location. The purpose of the metal
bolt was for nest relocation with a metal detector in case the permanent marker was
obscured or removed. A 38-cm vinyl stake wire flag (6.4 x 8.9 cm) was placed next to
the permanent marker. Observing or marking nests does not influence the risk of
predation (Tinkle et al. 1981, Condgon et al. 1983).
Nest Site Selection
I assessed nest site selection by measuring microhabitat characteristics of each
nest site and comparing them to a random plot. I measured 6 microhabitat variables:
ambient temperature, substrate temperature, relative humidity, overall canopy cover,
ground cover, and the estimated time that sunlight reached the nest. I measured canopy
cover using a spherical densiometer (Lemmon 1956) and used a Daubenmire frame
(Daubenmire 1959) to estimate ground cover (e.g., bare ground, rock, organic litter,
woody debris, grass, forb, vine, woody vegetation). I recorded canopy cover
measurements monthly (28 - 33 days) after the initial measurements until 3 months from
the time of nesting. Using a clinometer, I estimated time that sunlight reached the nest. I
26
measured angles to the top vegetation on the azimuth of the rising and setting sun. The 2
angles were subtracted from 180°, resulting in the arc in which sunlight would reach to
the nest.
I selected random plots by traveling in a random direction (1 - 360°) and distance
(1 - 100 m) from the original nest. I used a computer-generated random numbers table
that was prepared before my field study began. If the random plot chosen was not of the
same macrohabitat, a second random plot was sampled. I selected the second random
plot in the same manner as the first, except selection continued until a plot was selected
within a similar macrohabitat. At random plots, I recorded the same variables as those
collected at nest sites when nest site data were collected.
After a nest was established, I checked for disturbances 2 to 3 times per week and
recorded any observations. I documented any evidence of depredation above the ground
level and removed eggshells and temperature loggers at that time. After the first
hatchling emergence annually, I checked nests daily, when possible, for signs of
hatchling emergence in undestroyed nests. In 2001, wire mesh covers were secured over
nests with imminent hatchling emergence (a small hole on the nest surface indicates
hatchlings have “pipped”). Wire covers were used when practical to retain hatchlings
inside the cover as previously documented by Christens and Bider (1987). I checked
these nests twice a day and removed the covers as soon as hatchlings reached the ground
surface. I marked hatchlings found inside wire mesh covers or found at any nest site with
notches in marginal scutes (Cagle 1939), kept the individuals overnight, and released
them at the nest site. Since hatchling shells were too soft to file notches into the shell, I
27
used small scissors to “clip” the shell in a triangular fashion to form each notch. I
assessed nesting success using the number of depredated nests, the number of inviable
nests, and the number of nests with hatchlings that emerged from the nest. A hatched
nest was determined by a small hole on the surface of the nest, at which time nests were
monitored daily for hatchling emergence. If hatchlings emerged before this hole could be
observed, hatching was obvious by examining the fragments of eggshell. Although
overwintering of hatchlings in the nest has been observed only by Madden (1975), I did
not excavate nests in 2001 until the spring after the nesting season (May 2002) to prevent
disturbing overwintering hatchlings. Since I did not observe overwintering the first year
of my study, I excavated nests in October of 2002 after most hatchling emergence had
been established. I excavated nests to count the number of inviable eggs and the number
of dead hatchlings.
Analyses
Stickel (1950) documented female box turtles moving long distances to nesting
sites, but no nesting research has been conducted in fragmented areas. The amount of
fragmentation may affect the distance that females must travel to locate suitable nesting
sites, so I calculated the kernal home range estimates for the nesting season (May 15 –
July 15) and calculated distance from the center of the home range to the nesting site. I
compared the distance females moved during the nesting season among study sites using
an analysis of variance (ANOVA; Peterson 1985). To investigate differences among
28
study sites, I used a Fisher’s Protected Least Significant Difference (LSD) mean
separation test (Peterson 1985).
In order to determine if clutch size differed among study sites, I compared the
clutch size of each nest among study sites using an ANOVA (Peterson 1985). Clutch size
was initially based on radiographs and confirmed at time of nesting. Because maternal
body size is often related to measures of reproductive output (Tucker 1999), I regressed
carapace length, width, and height, plastron length, posterior plastron length, volume as
measured by carapace length x width x height, volume as measured by plastron length x
width x height, and volume as measured by posterior plastron length x width x height, on
clutch size to determine the relationship of morphometric measurements to clutch size
(Sokal and Rohlf 1995).
To determine if turtles selected nest sites based on microhabitat characteristics, I
compared nest sites versus random plots with respect to percent of ground cover (bare
ground, grass, forb, vine, woody vegetation, woody debris, organic litter, and other
ground cover [e.g., rocks or litter]), canopy cover, and estimated time sunlight reached
the nest using a paired t-test (Sokal and Rohlf 1995). Since eastern box turtles have
temperature-dependent sex determination, nest site selection may affect sex ratio;
therefore, the temperature of the nest over time is important. Eggs within the nest
incubate underground for a period of 2 – 3 months, during which time microhabitat
variables at the nest site are changing and influencing nest temperature. In order to
determine if microhabitat characteristics changed during incubation, I compared the same
29
microhabitat characteristics at time of nesting, 1 month after nesting, and 2 months after
nesting using a repeated measures ANOVA (Peterson 1985).
I compared the proportion of nests with known fates (hatched, inviable, and
depredated) between years using a log-likelihood ratio Chi-square (Sokal and Rohlf
1995) to detect differences in nest fate between years. To determine if microhabitat
characteristics affected nest fate (hatched, inviable, and depredated nests), I compared
microhabitat characteristics (relative humidity, ambient and substrate temperature,
percent of each life form, canopy cover, and estimated time sunlight reached the nest)
using an ANOVA (Peterson 1985). Because nest temperature can influence both sex
ratio and viability of a nest, I used the average of 6 HOBO® data logger readings per day
to estimate mean daily temperatures. I compared mean daily temperatures of successful
and inviable nests using an ANOVA and used an LSD mean separation test to investigate
differences when detected (Peterson 1985).
30
RESULTS
I monitored 35 and 36 females in 2001 and 2002, respectively, although the same
turtles were not always included in both years. X-rays were conducted from 4 June - 5
July 2001 and from 24 May – 28 June 2002 (Figure 7). Female box turtles were gravid
from May – July of 2001 (n = 29, 81%) and 2002 (n = 23, 64%). Due to practical
problems in the field, all possible nests were not documented during this research study
(2001 = 47%, 2002 = 12%). In 2001, the first x-ray was not conducted until 4 June, so
some turtles were likely missed altogether, especially for females that produced 2 clutches.
In 2002, the first x-ray was conducted 24 May, and the first turtle nested 27 May, so it’s
possible that turtles could even have been missed in 2002 as well. Many nests were
missed for turtles that were known to be gravid, either because there were not enough
researchers to check turtles at all study areas throughout the evening or because the turtles
nested at a different time of day. In both years, 2 different turtles had 2 clutches within the
nesting season. Some turtles retained eggs longer than others; the minimum time range
was 7 - 26 days. However, these are minimum estimates of egg retention since eggs could
have developed before the x-ray when eggs were first discovered. Nesting activity was
observed from 6 June to 5 July 2001 and 27 May to 11 July 2002. Of the 39 marked nests,
most (n = 34) were located in open fields or
31
0
5
10
15
20
25
Number of gravid turtles
Mayweek
3
Mayweek
4
Juneweek
1
Juneweek
2
Juneweek
3
Juneweek
4
Julyweek
1
Julyweek
2Weekly x-ray results
20012002
Figure 7. The number of gravid eastern box turtles by week for the 2001 and 2002 field seasons in northern Delaware. Data were based on x-ray results and known nesting dates. X-rays were not conducted until the first week of June in 2001.
32
meadows with no direct canopy cover, 4 were located at roadside edges, and 1 was in an
open, elevated area within an interior forest (White Clay Creek).
Nesting Behavior
I documented infrequent weather events during nesting. On 4 occasions, the sky
was overcast when nesting occurred. On 2 occasions, it rained 1 – 2 hours prior to
nesting activity. On 4 occasions, rain occurred during nesting activity for either all or
part of the nesting process. However, on the other 28 occasions (72% of nesting
occurrences), rain events (overcast sky, rain, or stormy weather) were not associated with
nesting behaviors.
The nesting behavior of 30 females was observed in whole or part during the 2001
and 2002 nesting seasons. The nesting process consisted of nest site selection, digging,
egg deposition, and nest concealment. One female (0014) was observed in the early
stages of nest site selection, poking her nose in the dirt, as if “smelling” a good nest
location. This turtle “smelled” a number of locations before settling on a location to dig.
In most cases, the time spent finding a suitable nest site was not observed, and turtles
were already digging when located by the observers. Once a turtle initiated digging,
turtles either abandoned the nest site or successfully completed the nest.
Two turtles were documented abandoning a nest site and starting a new nest near
the previous attempt in the same night. One turtle (3010), despite missing the end of a
back foot, alternated feet when digging as observed for all other turtles. This turtle
abandoned a nest site in both 2001 and 2002 and then began a new nest <1 m from the
original nest site within 2 hours of starting the first nest. In both years, the turtle
33
successfully completed the nest. Another turtle (0014) abandoned a nest site after 4
hours of digging and began a new nest approximately 7 cm from the original nest site,
abandoning this nest site after an additional 5 hours of digging. This turtle eventually
nested on the following night. For some abandoned nest sites, the turtle had reached a
rock (n = 6) or thick roots (n = 4) that could not be removed from the hole. In other
cases, the cause for abandonment was unknown (n = 22). It took anywhere from 10
minutes to 8 hours for a turtle to decide to abandon a nest, digging either all or part of the
time. Females were documented abandoning 1 - 4 nests on different nights before
ultimately laying their eggs. Nest abandonment was common with 20 females
documented abandoning a nest site at least once (11 in 2001, 9 in 2002).
Laying time ranged from 9 – 58 minutes (Table 2). Once a turtle started laying
her eggs, in almost all cases she laid all of the eggs in her clutch. On 1 occasion a turtle
(1015) was observed digging for 3 hours with only a shallow depression as a hole, laid 1
egg (clutch size = 6) on the ground surface, and then attempted to cover the “nest” with
no results. The remaining 5 eggs were laid at another time. On another nesting occasion,
this same turtle laid 5 eggs in the nest cavity, became disoriented by turning in a different
direction, and moved off the nest, laying 1 egg on the ground surface; then, she found her
way back to the hole and laid the last egg in the nest cavity. One turtle (1017) dug 2
separate holes with the right and left foot. The dirt wall separating the 2 holes eventually
collapsed, making for an unusually large nest cavity with a bridge in the middle. This
turtle laid her eggs on the right side of the hole, but could not find the eggs
34
Table 2. A summary of egg-laying behavior for the 2001 – 2002 field seasons for eastern box turtles in 4 populations in northern Delaware.
Turtle No.
Nesting Date
Laying Time1
Clutch Size
Covering Time2
2011
8-Jun-01
33
4
2047 8-Jun-01 58 6 3019 10-Jun-01 ~19 5 98 2004 11-Jun-01 26 3 3010 12-Jun-01 ~56 7 23 2008 14-Jun-01 ~20 3 11 3014 15-Jun-01 ~13 6 ~43 2014 15-Jun-01 12 2 27 3003 17-Jun-01 ~13 4 24 1015 26-Jun-01 9 4 2011 27-May-02 25 5 1015 1-Jun-02 17 5 1010 4-Jun-02 24 6 1013 6-Jun-02 14 4 1005 10-Jun-02 13 5 3012 11-Jun-02 16 3 2008 12-Jun-02 9 3 2020 12-Jun-02 13 6 1017 16-Jun-02 28 3 0001 19-Jun-02 24 5 2014 19-Jun-02 19 4 2017 20-Jun-02 9 2 3014 25-Jun-02 30 2 3020 27-Jun-02 11 8
1 The total amount of time it took for a female to lay her eggs, when observed from the first egg to the last egg (minutes). 2 The amount of time it took for the covering process to take place, when observed from start to finish (minutes). Covering time was not observed in 2002.
35
to position them with her left foot, so this nesting process took much longer than usual
(7+ hours). On another occasion, a turtle (2020) laid 6 out of 7 eggs, with the last 2 eggs
remaining on the ground surface, as the hole was too small for all of the eggs. The 1
remaining egg was apparently “dropped” at a later date or nesting occurred at another
time of day, since another nesting occurrence was never observed.
In 2001, I tried to quantify the entire nesting process by observing the turtle until
she walked away from the nest after concealment when possible (Table 3). I found that
most turtles stayed at the nest site or about 1 m from the nest site in a resting position and
did not immediately walk away from the nest. Therefore, in 2002, after a turtle was
found covering a nest, I documented the initial time of nest concealment and left the
turtle.
Clutch Size and Frequency
Clutch size was initially based on radiographs and confirmed when possible at the
time of egg deposition. In all but 1 case, accurate clutch size was determined from the
radiographs. The only case when the x-ray estimate of clutch size was not correct
occurred when I counted 7 eggs on the x-ray and the turtle laid 8. In 1 case an odd-
shaped egg was viewed on the radiograph and again observed as the turtle laid her eggs
(3014). This egg was smaller than other eggs and almost spherical in shape. It did not
develop and was deemed inviable. Similarly, smaller yolkless eggs were documented by
Congello (1978) and Madden (1975). Clutch size ranged from 1 - 9 eggs for 53 clutches
determined using x-rays, with a mean clutch size of 4.6 (SE = 0.23; Figure 8). The mean
clutch sizes were similar between years (2001, mean = 4.7, SE = 0.31; 2002, mean = 4.4,
36
Table 3. A summary of timing of nesting behavior at 39 eastern box turtle nests on 4 study areas in northern Delaware during the 2001 - 2002 field seasons.
Turtle
Date
Digging1
Laying2
Covering3
Total Time4
2011
8-Jun-01
1940
0425
0630
11 2047 8-Jun-01 2015 0110 0512 9 2020 10-Jun-01 1940 2215 3 3019 10-Jun-01 2030 2242 0053 4.5 2004 11-Jun-01 1919 2044 3010 12-Jun-01 2010 2244 2359 4 1010 13-Jun-01 2015 2210 2 2008 14-Jun-01 1956 2300 2336 4 3014 15-Jun-01 1945 2140 2243 3 2014 15-Jun-01 2010 2314 0003 4 0014 16-Jun-01 1916 0242 7 3002 16-Jun-01 1950 2205 3003 17-Jun-01 2040 2120 1020 21-Jun-01 2000 2150 1015 26-Jun-01 2026 2110 1010 1-Jul-01 2028 1021 6-Jul-01 1950 2130 2207 3 2011 27-May-02 2037 0150 0224 6 1008 30-May-02 1905 2020 1015 1-Jun-02 1922 2137 2218 3 1010 4-Jun-02 2020 2141 2211 2 1014 5-Jun-02 1942 2100 3003 5-Jun-02 1920 2102 2111 2 0014 6-Jun-02 1900 0040 0056 6 1013 6-Jun-02 2000 2218 1005 10-Jun-02 1848 2144 2207 4 3012 11-Jun-02 2032 0024 2008 12-Jun-02 1921 2227 2020 12-Jun-02 1942 2214 2304 3 1017 16-Jun-02 1952 0255 7+ 0001 19-Jun-02 2022 2425
37
Table 3 (continued)
2014
19-Jun-02
2029
0047
0129
5
2017 20-Jun-02 2004 0030 3011 24-Jun-02 1935 2230 2302 4 3014 25-Jun-02 2041 2238 3010 25-Jun-02 2127 2358 2 3020 27-Jun-02 2050 0100 0118 5 1013 3-Jul-02 1959 2126 2142 2 0014 11-Jul-02 2025 2330 2344 3
1 Time of first observation of digging (EST). In almost all cases, the turtle was digging before the observer found the turtle. 2 Time of first observation of laying; e.g., when the first egg was laid or an estimate based on timing of subsequent eggs. 3 Time of first observation of covering the nest. 4 An estimate of the minimum total time (hours) it took for the entire nesting process to occur.
38
01234567
Frequency of clutch size
1 2 3 4 5 6 7 8 9Clutch size
20012002
Figure 8. Range of clutch sizes of female eastern box turtles during the 2001 and 2002 field seasons in northern Delaware.
39
SE = 0.33; t51 = 0.60, P = 0.553). Clutch size did not differ among study sites
(F3, 49 = 0.53, P = 0.666; Table 4). For all turtles gravid in both years of the study (n =
19), clutch size decreased in 5 turtles and increased in 10 turtles in the subsequent
reproductive season, with a difference of 1 - 4 eggs. Clutch size remained the same in 4
turtles. One turtle that was not gravid in 2001 was gravid in 2002, and 3 turtles that were
gravid in 2001 were not gravid in 2002. Seven females were not gravid in either 2001 or
2002. All morphometric measurements were positively related to clutch size except
carapace height (Table 5). The significant morphometric measurements explained 11 –
22% of the variation in clutch size (Table 5).
Nest Site Selection
Female box turtles moved 9 - 529 m to find a nesting location. Distances moved
differed among study areas (F3, 33 = 15.40, P = < 0.001; Table 6). Females at White Clay
Creek moved >3 times farther to nest than females at the other 3 study areas. At White
Clay Creek, females mostly moved long distances to nest in open fields, approximately 1
– 6 m from the forest edge (Figure 9). Only 1 female nested in an interior forest area
with an open canopy. Turkey Run turtles mainly used fields on the study area, also
nesting 1- 6 m from the forest edge (Figure 10). Webb Farm turtles chose to nest either
in the meadow or in the cornfield, with 1 turtle nesting at the edge of a 2-lane highway
(Figure 11). At the UD Woodlot, where open fields were available in the form of
agricultural or sports fields, the 2 females documented nesting did not move to these
areas (Figure 12). Instead, 1 female nested on a grassy strip between the curb and edge
habitat at the edge of a 4-lane highway on 3 separate occasions (once in 2002, twice in
40
Table 4. Clutch size of eastern box turtles by study area during the 2001 – 2002 field seasons in northern Delaware.
Area
n
Mean
SE
Minimum
Maximum
UD Woodlot
6
4.2
0.60
2.0
6.0
Turkey Run
11
4.4
0.66
2.0
9.0
White Clay
15
5.0
0.41
2.0
8.0
Webb Farm
21
4.5
0.31
1.0
7.0
Total
53
4.6
0.23
1.0
9.0
41
Table 5. The relationship of morphometric measurements to clutch size of female eastern box turtles in northern Delaware during the 2001 – 2002 field seasons.
R2
F1, 51
P
Carapace width
0.22
3.82
<0.001
Volume as measured by plastron length x carapace width x carapace height
0.21
3.63
<0.001
Plastron length
0.20
3.61
<0.001
Volume as measured by posterior plastron length x carapace width x carapace height
0.19
3.46
0.001
Volume as measured by carapace length x carapace width x carapace height
0.17
3.24
0.002
Posterior plastron length
0.16
3.17
0.003
Carapace length
0.11
2.54
0.014
Carapace height
0.04
1.55
0.128
42
Table 6. Distances eastern box turtle females moved (m) during the 2001 and 2002 field seasons at 4 study areas in northern Delaware. Distances moved differed among study sites (F3, 33 = 15.40, P < 0.001).
Area
n
Mean
SE
Minimum
Maximum
LSD1
Turkey Run
8
35.2
5.98
9.4
55.1
B
Webb Farm
13 66.0 13.22 12.1 175.5 B
UD Woodlot
4 86.8 66.28 9.2 284.9 B
White Clay
12 336.9 42.25 33.6 529.1 A
1 Areas with the same letters for the LSD did not differ.
43
Figure 9. Eastern box turtle nest locations at White Clay Creek in Newark, Delaware for the 2001 – 2002 field seasons. Circles represent 2001 nests and squares represent 2002 nests.
44
Figure 10. Eastern box turtle nest locations at Turkey Run in Newark, Delaware during the 2001 – 2002 field seasons. Circles represent 2001 nests and squares represent 2002 nests. Circled nests are from a female that nested in the same location in consecutive years.
45
Figure 11. Eastern box turtle nest locations at Webb Farm in Newark, Delaware during the 2001 – 2002 field seasons in northern Delaware. Circles represent 2001 nests and squares represent 2002 nests. Circled nests are from a female that nested in the same location in consecutive years.
46
Figure 12. Eastern box turtle nest locations at the UD Woodlot in Newark, Delaware during the 2001 – 2002 field seasons. Circles represent 2001 nests and squares represent 2002 nests. Circled nests are from a female that nested in the same location in consecutive years. Nest in upper left-hand corner is shown with an arrow.
47
2002). The other female nested twice in 1 nesting season in a small meadow in 1999
(Niederitter 2000) and, in 2002, made many attempts before nesting in front of a
university building in an area maintained for plants.
The percentage of vines, woody vegetation, woody debris, organic litter, and
other ground cover, and estimated time sunlight reached the nest did not affect nest site
selection (Table 7). Random sites had greater canopy cover than nesting sites (Table 7).
Grass and forbs were more abundant at random sites, whereas bare ground was more
abundant at nest sites (Table 7). The same microhabitat variables were observed just
after nesting occurred, 1 month after nesting, and 2 months after nesting. The percentage
of grass, forbs, vines, and other ground cover, and estimated time sunlight reached the
nest did not change at the nest sites during incubation (Table 8). The percentages of
organic litter and woody debris increased during incubation, whereas the percentage of
bare ground at nest sites decreased slightly during incubation (Table 8). The percentage
of canopy cover almost doubled during incubation (Table 8). Woody vegetation was not
considered because it was biologically insignificant in this analysis.
Nest Success
Of 39 nests that I monitored (17 in 2001, 22 in 2002), 12 (31%) were considered
successful (if ≥1 hatchling emerged from the nest; 2001 = 24%, 2002 = 36%), 13 (33%)
were inviable (eggs did not develop within the nest; 2001 = 41%, 2002 = 27%), 11 (28%)
were destroyed by predators (2001 = 24%, 2002 = 32%), 2 (5%) were destroyed by
machinery (1 in a cornfield, 1 in a cow pasture), and the fate of 1 nest (Nest 12; 2.6%)
was unknown. Nest 12 (in 2001) was monitored through the fall with no sign of
48
Table 7. Summary of microhabitat characteristics for 39 eastern box turtle nests and random plots on 4 study sites in northern Delaware during 2001 and 2002. A paired t-test was used to detect differences between nests and random plots. Nest Random Plot ———————— ———————— Variables mean SE mean SE t38 P Bare ground1 23 3.44 9 3.31 4.18 <0.001 Grass1 23 2.83 33 4.65 -2.03 0.049 Forb1 24 2.50 32 3.85 -2.57 0.014 Vine1 1 0.25 0 0.13 1.36 0.183 Woody vegetation1 0 0.00 0 0.38 -1.00 0.324 Woody debris1 1 0.44 1 0.44 -0.17 0.864 Organic litter1 27 2.80 24 3.53 0.90 0.371 Other1 1 0.59 0 0.26 1.18 0.244 Canopy cover2 26 4.03 37 5.34 1.98 0.056 Sunlight3 126 4.55 126 6.14 -0.10 0.921 1 percentage observed using a Daubenmire frame 2 estimated using a spherical densiometer 3 the estimated amount of time direct sunlight reached to the nest
49
Table 8. Summary of microhabitat characteristics for 39 eastern box turtle nests at nesting, 1 month after nesting, and 2 months after nesting in northern Delaware during 2001 – 2002. A repeated measures ANOVA was used to detect differences in variables across time. Nesting4 1 month5 2 months6
———— ———— ———— Variables mean SE mean SE mean SE F2, 37 P Bare ground1 23 3.44 15 2.20 15 2.11 5.13 0.010 Grass1 23 2.83 19 2.68 21 3.08 1.16 0.324 Forb1 24 2.50 25 2.41 24 2.68 0.35 0.706 Vine1 1 0.25 1 0.47 2 0.78 3.11 0.566 Woody vegetation1 0 0.00 0 0.00 0 0.00 Woody debris1 1 0.44 1 0.50 1 0.48 8.52 0.006 Organic litter1 27 2.80 37 3.56 36 3.37 5.21 0.010 Other1 1 0.59 2 1.17 2 1.29 0.63 0.538 Canopy cover2 26 4.03 36 4.64 47 5.84 7.86 0.001 Sunlight3 126 4.55 128 4.48 129 4.09 2.23 0.122 1 percentage observed using a Daubenmire frame 2 estimated using a spherical densiometer 3 the estimated amount of time direct sunlight reached to the nest 4 date of actual nesting event 5 1 month after nesting 6 2 months after nesting
50
hatchling emergence and thought to be inviable, but further data were not collected since
the nest site could not be relocated in spring 2002. The proportion of nests of known fate
(hatched, inviable, depredated) did not differ between years (x22 = 1.26, P = 0.533).
Of the 12 successful nests (mean total eggs = 4.5, SE = 0.45), most (83%, n = 10;
mean hatched eggs = 4.1, SE = 0.42) had all their eggs hatch. The number of eggs
hatched per nest varied among study areas (Table 9). Turkey Run had 21/23 eggs hatch
and emerge from the nest, Webb Farm had 19/19 hatched eggs, UD Woodlot had 6/6
hatched eggs, and White Clay Creek had 3/6 hatched eggs. As reported earlier, 1 turtle at
Turkey Run laid 6 eggs and left 2 remaining on the ground surface because they did not
fit in the nest. Another female at White Clay Creek laid 6 eggs, with 3 hatching and 3
inviable. Half the nests (50%) at the UD Woodlot were successful (n = 4), 45% of nests
at Webb Farm were successful (n = 13), 31% of nests at Turkey Run were successful (n =
11), and 0.1% of nests at White Clay Creek were successful (n = 11).
For successful nests, the temperature ranged from 23.4ºC - 27.3ºC (mean = 24.8,
SE = 0.35). For inviable nests, the temperature ranged from 22.0ºC - 26.8ºC (mean =
23.8, SE = 0.40). The temperature of successful and inviable nests differed marginally
(F1, 20 = 3.45, P = 0.078). I did not detect a difference among successful nests, inviable
nests, or nests destroyed by predators for relative humidity (F2, 33 = 1.55, P = 0.227),
ambient temperature (F2, 33 = 0.40, P = 0.671), substrate temperature (F2, 33 = 0.15, P =
0.864), bare ground (F2, 33 = 0.29, P = 0.753), grass (F2, 33 = 2.32, P = 0.114), forb (F2, 33 =
1.67, P = 0.204), vine (F2, 33 = 0.97, P = 0.391), woody debris (F2, 33 = 0.98, P = 0.387),
organic litter (F2, 33 = 0.01, P = 0.991), other ground cover (F2, 33 = 0.76, P = 0.474),
51
Table 9. Eggs hatched for each successful nest in the 2001 – 2002 field seasons during an eastern box turtle study in northern Delaware.
Turtle ID
Year
Study Area
Total clutch
size
Eggs hatched
2020
2001
Turkey Run
6
6
2008 2001 Turkey Run 3 3 3014 2001 White Clay 3 6 1021 2001 Webb Farm 7 7 2011 2002 Turkey Run 5 5 0014 2002 UD Woodlot 4 4 1013 2002 Webb Farm 4 4 1005 2002 Webb Farm 5 5 2008 2002 Turkey Run 3 3 2020 2002 Turkey Run 4 6 1013 2002 Webb Farm 3 3 0014 2002 UD Woodlot 2 2
52
canopy cover (F2, 33 = 0.08, P = 0.924), or estimated time sunlight reached the nest (F2, 33
= 1.51, P = 0.2350).
Predation was an important cause of nest failure, mainly at White Clay Creek (n =
6) and Webb Farm (n = 4). One nest was depredated in a field at Turkey Run in 2002;
however, 3 turtles nested in the same field in 2001 with no predation. Two turtles that
nested near their 2001 nest site in 2002 had their nests depredated in both years. UD
Woodlot nests were not subject to predation during this study. Estimated dates of
predation varied greatly within a season, with some nests being depredated just after
nesting and some 2 - 3 months after nesting (Table 10). Predation was never directly
observed by any of the researchers. Based on my personal observations and on my
general knowledge of box turtle life history, nests depredated at Turkey Run, White Clay
Creek, and Webb Farm were most likely depredated by raccoons, skunks, opossums, or
foxes.
Of the 13 nests that were inviable, some were in locations that did not hatch in
2001 but did hatch in 2002. Two turtles chose nests in different locations in 2001 and
2002, but in both years the eggs were inviable. In most cases, a nest had all eggs hatch or
all eggs inviable. In 5 different nests, 1 egg hatched while the remaining eggs were
inviable. These nests were not considered successful since no turtles actually survived
and emerged from their nests. In 3 nests, 1 fully developed hatchling was found dead in
the nest, partially inside the eggshell. In 2001, 2 nests with inviable eggs were excavated
in May of 2002 and 1 live hatchling was found trapped in each nest. I did not assume
that either hatchling overwintered in the nest by choice because in both cases thick roots
53
Table 10. Timing of predation for eastern box turtle nests in northern Delaware for the 2001 – 2002 field seasons.
Nest
Turtle
Nesting Date
Predation Date
No. of Days
4
3019
10-Jun-01
5-Jul-01
26
6 3010 12-Jun-01 11-Jul-01 30 7 1010 13-Jun-01 4-Aug-01 53 15 1015 26-Jun-01 3-Aug-01 39 2 1008 30-May-02 4-Sep-02 98 3 1015 1-Jun-02 22-Jul-02 52 10 3012 11-Jun-02 18-Jun-02 8 15 2014 19-Jun-02 21-Aug-02 64 17 3011 24-Jun-02 29-Jun-02 6 19 3010 25-Jun-02 5-Jul-02 11 20 3020 27-Jun-02 19-Sep-02 85
54
surrounded the nest cavity, preventing the turtle from emerging. These nests were not
considered successful; because without my assistance, I do not believe either turtle would
have emerged from the nest and survived.
Nests at Webb Farm were subject to disturbance by farm machinery. One nest in
2001 was located in a cornfield and destroyed by a tractor (Nest 14), while a nest in 2002
was located in the cow pasture and was destroyed during subsoiling of the pasture (Nest
13). One nest (Nest 8) in 2002 was located at the edge of the cornfield at Webb Farm and
just missed being destroyed by a tractor when the corn was plowed. Plowing occurred on
17 September, which was about the time hatching would have occurred. This nest had
approximately an extra 13 cm of topsoil directly above the nest location after plowing
occurred; but despite the extra barrier, hatchlings emerged from the nest.
Nest Site Fidelity
For all females where 2 nests were documented for the same turtle (n = 11), most
females (n = 8, 73 %) showed nest site fidelity. A few other females in my study that
were known to be gravid moved long distances in both 2001 and 2002 to the same field.
However, nests were not documented in both years, so these were not included. Females
moved 4.5 – 295.0 m (mean = 111.6, SE = 31.80) from their 2001 to their 2002 nest
locations. Some turtles’ nests between years were within 1 m of each other, but the
accuracy of our GPS unit prevented me from detecting differences that were <10 m.
Three turtles nested within 1 m of their 2001 nest location in 2002 based on personal
observations. Some turtles moved a great distance (up to 286 m) to nest in the same field
in both years, but not necessarily in the same exact location. Females with 2 clutches
55
within a nesting season tended to nest in the same area (e.g., within the same field or
meadow). One turtle that nested on a mowed path at Turkey Run in 2001 also nested on
a nearby dirt path in 2002. Turtles at Webb Farm that nested in the meadow in 2001 also
nested in the meadow in 2002. Most turtles from Turkey Run and White Clay Creek
nested in open fields in both years, either in the same field or a different field.
Incubation Period and Hatchling Emergence
The incubation period ranged from 67 to 105 days, with a mean of 89.5 days (SE
= 3.90; Table 11). The earliest and latest hatchings were 38 days apart. Hatchlings
emerged from 2 September through 23 September (Table 11). Regardless of actual
nesting date, hatchlings emerged on similar dates in September. All captured hatchlings
had a visible scar from the yolk sac and a caruncle (egg tooth).
56
Table 11. Estimated incubation length (in days) for eastern box turtle nests in northern Delaware for the 2001 – 2002 field seasons.
Nest
Turtle No.
Nesting Date
Hatching Date
Incubation
Length1
3
2020
10-Jun-01
16-Sep-01
98
8 2008 14-Jun-01 16-Sep-01 94
9 3014 15-Jun-01 21-Sep-01 98
17 1021 6-Jul-01 15-Sep-01 71
1 2011 27-May-02 2-Sep-02 98
7 0014 6-Jun-02 9-Sep-02 95
9 1005 10-Jun-02 23-Sep-02 105
11 2008 12-Jun-02 3-Sep-02 83
12 2020 12-Jun-02 19-Sep-02 99
21 1013 3-Jul-02 17-Sep-02 76
22 0014 11-Jul-02 16-Sep-02 67
1 The number of days from the nesting date to the first observation of hatching.
57
DISCUSSION
Nesting ecology in the eastern box turtle is not well understood because little
research has been conducted to observe nesting behaviors or to document general nesting
ecology. My study represents the largest investigation, to date, of natural nests to be
marked and documented for the eastern box turtle. Only a few studies have looked
specifically at eastern box turtle reproduction and nesting, and these have been mostly for
captive or collected turtles (Ewing 1933, Allard 1948, Dodge et al. 1978, Stuart and
Miller 1987). Congello (1978) observed 29 nesting turtles in both a captive enclosure
and in the wild, with half of the eggs being collected for incubation. More thorough
nesting data have been collected for other box turtle species. Nieuwolt-Dacany (1997)
used x-ray techniques to determine that 72 of 124 western box turtles were gravid, but
nests were not marked or monitored. Ornate box turtle (Terrapene ornata) nests were
monitored by both Temple (1987) and Doroff and Keith (1990). Temple (1987) marked
nests for 16 nesting females and monitored nest fates to determine predation rates near
ecological edges. Doroff and Keith (1990) conducted a study similar to mine, monitoring
37 females with radiotelemetry and observing 16 marked nests.
58
Nesting Behavior
Much of my study was conducted during a record drought, so I was unable to
corroborate a correlation between precipitation and nesting activity. In previous studies,
other researchers (Allard 1948, Congello 1978) have observed that nesting events were
correlated with rain events. Allard (1948) documented nesting often coincided with
thunderstorms or rain showers, and Congello (1978) substantiated that nesting activity
was associated with periods of storm activity, but independent of air temperature.
Congello (1978) often observed nesting behavior before, during, or after a rainstorm; and
periods with multiple nestings corresponded to periods of wet weather. Most nesting
occurred on days with substantial rainfall that followed several dry days in the Gulf Coast
box turtle (Terrapene carolina major) (Jackson 1991).
Gravid females often move long distances to open habitat during the nesting
season (Stickel 1950, Williams and Parker 1987, Stickel 1989). Female yellow-margined
box turtles exhibited different movement patterns based on their reproductive status, with
gravid females moving to open areas during the nesting season and non-reproductive
females staying in forested areas (Lue and Chen 1999). Stickel (1950) was the first to
document females extending their home ranges by traveling long distances to nest. Her
study area was a 12-ha bottomland forest within a mostly wooded 1,072-ha wildlife
refuge (Stickel 1950), which is comparable to the 15-ha interior area of White Clay Creek
State Park (1,369 ha total). Her females moved 457 – 695 m to nest in drier, warmer
upland areas (Stickel 1989); whereas White Clay Creek females moved 151 – 451 m to
nest, aside from the 1 female that nested in an interior forest area (33 m). Williams and
59
Parker (1987) reported that 4 females in a 72.9-ha upland forest moved approximately
450 m from their home range into open field habitats to lay their eggs. Movement to an
open area to nest is common for many turtle species and was documented for all but 1
female in my study. Lue and Chen (1999) documented that yellow-margined box turtles
selected well-sunlit nesting sites in open fields adjacent to vegetated forest areas, and
most female three-toed box turtles laid eggs in open areas that received direct sunlight
during a portion of the day (Messinger and Patton 1995). Turtles in my study also
selected nest sites receiving direct sunlight for part of the day.
In my study, females frequently abandoned nest sites. Females often abandoned
more than 1 nest in a night, and more commonly, abandoned multiple nests over a period
of a few days before nesting. Messinger and Patton (1995) also documented that female
three-toed box turtles abandoned nest sites several times before laying their eggs. Nests
were abandoned because of an immovable object in the nest, for no observable reason, or
due to hard rainstorms (Congello 1978, Messinger and Patton 1995). In my study, the
reason for abandonment was largely unknown; however, in some cases, it was due to
roots or rocks in the nest cavity. Unlike Messinger and Patton (1995), I did not find that
hard rainstorms discouraged turtles from continuing a nest. I observed 3 occurrences of
turtles that nested in a rainstorm. The turtles laid their eggs in the nest and attempted to
cover the nest despite the difficulties of digging in mud.
When females did not abandon nests, they often exhibited behaviors associated
with nest completion. During the course of my study, I documented similar nesting
behaviors to Allard (1948), Congello (1978), and Messinger and Patton (1995) for box
60
turtle species. Females excavated flask-shaped nest cavities whose depth was determined
by how far the female could reach into the hole with her hind legs and still remove dirt.
Dirt was removed from the nest cavity by alternating the hind legs to scoop out dirt.
When preparing to lay an egg, the turtle stretches her legs out and lifts up her body to
position the egg directly over the hole of the nest cavity. Just before laying, the turtle
pulls her head inside of the shell, while keeping the legs extended. Some turtles laid eggs
continuously, while others positioned each egg, alternating the hind feet after laying the
egg. All turtles positioned the eggs in the nest after egg deposition was completed before
covering the nest. I noted that females began covering nests within a few minutes after
laying the last egg and did not reach for the dirt recently excavated from the nest cavity.
Instead, the female reached forward with her hind feet and raked grass and leaf litter from
the ground surface into the nest cavity, followed by treading and tamping the earth with
the hind legs and knees to pack down the soil.
Clutch Size and Frequency
Clutch size in my study (1 – 9 eggs) was similar to previous research (1 – 8 eggs)
on eastern box turtles (Allard 1948, Congello 1978, Dodge et al. 1978, Stuart and Miller
1987). Individual turtles did not reproduce every year in a yellow-margined box turtle
population (Chen and Lue 1999), a western box turtle population (Nieuwolt-Dacany
1997), or an ornate box turtle population (Doroff and Keith 1990); however, in Legler’s
(1960) study on the eastern box turtle, all females oviposited annually, some with 2
clutches in 1 year. During my study, 19 females (58%) were gravid in both 2001 and
2002; and 4 females had 2 clutches within a nesting season.
61
Iverson (1977) documented a positive correlation between clutch size and body
size. Many studies have examined this correlation, but few have involved box turtle
species. A significant, positive correlation between clutch size and maternal size
(carapace length, height, width, and plastron length) was documented by Tucker (1999),
whereas Congdon and Gibbons (1985) documented that clutch size was negatively
correlated with maternal size (plastron length). For the western box turtle, clutch size
was positively correlated with maternal body size (carapace length and width, and body
mass; Nieuwolt-Dacany 1997). My results corroborated those of Tucker (1999) and
Niewolt-Dacany (1997), since I documented all female morphometric measurements
except carapace height were positively related to clutch size (Table 6). My results are not
surprising; given that as body size increases, a female would have a larger capacity for
eggs. In areas with good habitat quality, females would have the benefit of sufficient
resources in which to feed and reproduce. These areas should produce females with
larger body sizes, and therefore, larger clutches with higher quality eggs (Congdon and
Gibbons 1990). Once an area has been fragmented, the habitat quality and resources
would decrease, eventually causing a decrease in female body size and a decrease in
clutch size. Over time, the size and number of clutches would lead to lower recruitment
and underdevelopment in adult body size, affecting the entire population.
Nest Site Selection
Aside from choosing an open area in which to nest, it is not known how females
select nest sites or which environmental cues they are using. Once a female has moved to
an open area, the method by which she chooses a nest site may be related to ground-
62
nuzzling. Ground-nuzzling in female turtles is described as a behavior whereby the head
and ventral side of the neck are pressed to the ground surface before a nest site is chosen
(Morjan and Valenzuela 2001). I observed similar behavior by 1 female in the early
stages of choosing a nest site, although it has not been previously documented for the
eastern box turtle. Similar behavior was documented for captive three-toed box turtles
(Messinger and Patton 1995). This behavior is a widespread occurrence and has been
documented in species of Chelonidae (n = 4), Testudinidae (n = 1), Pelomedusidae (n =
1), and Emydidae (n = 12) and was significantly associated with nesting in painted turtles
(Chrysemys picta; Morjan and Valenzuela 2001). Morjan and Valenzuela (2001)
speculated that this behavior was also associated with nest site philopatry.
In species with temperature-dependent sex determination, identifying how
females choose a thermal cue when nesting for an incubation period that continues weeks
after the nesting event is an enigma (Janzen and Morjan 2001). Females would have to
predict the temperature of the nest cavity based on amount of canopy cover, solar
exposure, and amount of vegetation shading the nest site for 2 – 3 months following
nesting. However, nest temperatures fluctuate depending on nest depth and microhabitat
of the nest site (Wilson 1998). For example, nests with more overstory vegetation cover
tend to be cooler than nests with less cover (Weisrock and Janzen 1999). Some
researchers have suggested that females must choose nest sites to predict a specific sex
ratio if nest site selection is to be effective for successful reproduction (Janzen 1994,
Roosenburg 1996). However, it is more reasonable to assume that females are choosing
63
nest sites that would maintain sufficient temperatures throughout incubation to be
successful and have hatchlings emerge.
Vegetational cover at the nest site might be the most reliable mechanism for
females to choose nest sites since it is relatively constant (Janzen 1994) and is highly
correlated with the thermal environment (Vogt and Bull 1984). However, habitat
alteration can also have an effect on vegetational cover and therefore, nest temperatures.
Mowing changed the vegetational cover for nests throughout the incubation period at
some of the fragmented areas (UD Woodlot and Turkey Run), as well as for nests laid by
White Clay Creek females in mowed fields that were off the study site. Since I did not
investigate differences in microhabitat among study sites, I cannot speculate as to
whether this had an effect on nest success. Vegetational cover at nest sites has also been
correlated to the sex ratio of hatchlings in other species of turtles (Vogt and Bull 1984,
Janzen 1994, Roosenburg 1996). Vegetational cover at time of nesting in painted turtles
predicted mean temperatures in July (when sex ratio was determined) based on the
amount of shade at the nest location (Weisrock and Janzen 1999). Since it is unknown at
what time during incubation sex ratio is determined, I could not determine if vegetational
cover affected sex ratios in nests.
Solar exposure has been suggested as a mechanism for nest site selection (Janzen
1994). In order for eggs to develop at the appropriate incubation temperature, they need
to be maintained at sufficient temperatures based on surrounding environmental
conditions (Wilson 1998). Since larger turtle species can generally dig deeper nests, they
should construct nests in microhabitats with minimal surrounding vegetational cover so
64
that sun exposure is maximized at the nest site (Wilson 1998). For the three-toed box
turtle, Reagan (1972) documented that all nests shared the same characteristics. Nests
were located in low, grassy vegetation with scattered forbs, excavated 5 – 8 m from the
forest edge and constructed on flat terrain (Reagan 1972). My nests showed similar
characteristics. Reagan (1972) postulated that these locations had exposure to moderate
warming from the sun with no direct drying effects of wind due to the proximity to the
forest edge. Congello (1978) also documented that nests occurred in cleared areas where
sunlight could penetrate through leafy foliage during daylight hours. My results support
these findings, because all but 1 of my nests were located in open areas with considerable
sun exposure.
Nest site selection has been defined as the placement of eggs by females at sites
that differ from random sites in a defined area (Wilson 1998). In my analysis, random
sites had more canopy cover than nest sites, which implies that females are seeking out
open areas in which to nest. Based on locations available, most turtles chose to nest in
open areas near a forest edge. I documented that the amount of time sunlight reached to
the nest did not change over time, and half of ground cover variables (grass, forb, vine,
and other) did not change at the nest site over time. This suggests that females chose nest
sites where nest temperature remained stable; therefore, females should be able to use
microhabitat characteristics as cues to estimate incubation temperatures. Janzen and
Morjan (2001) concluded that females consistently preferred nest sites with particular
quantities of overstory vegetation cover. Canopy cover almost doubled throughout the
incubation period, which would have a direct effect on nest temperature. When a nest is
65
excavated, females essentially destroy the surrounding vegetation and excavate excessive
soil, reducing canopy cover and increasing the amount of bare ground at the nest site.
Therefore, it is understandable that canopy cover would double from the time of nesting.
In certain areas, the canopy cover greatly increased, depending on nest location. In the
Webb Farm meadow, field grasses grew steadily over the incubation period since no
mowing occurred in that area; and in the cornfield at Webb Farm, canopy cover increased
until the corn was plowed, which was right around the time of hatching.
Nest Success
Although nests were most successful at the most fragmented areas, the UD
Woodlot and Webb Farm, some successful nests were located at roadside edges. Since
hatchlings were not tracked after emergence, there are no data to show whether they
moved toward the road. Also, since predation was common at Webb Farm, it is possible
that the hatchlings did not survive to adulthood. Only a third of the nests were successful
at Turkey Run, mostly due to nest inviability. Despite my predictions that White Clay
Creek would be the area with the most recruitment, only 1 nest was successful because
nests were subjected to predation and inviability. The number of eggs per nest that
hatched, with hatchlings emerging from the nest, indicated that the most productive study
areas were Turkey Run and Webb Farm. White Clay Creek and UD Woodlot had very
few hatchlings emerging. Turkey Run and Webb Farm had extensive areas of early
successional habitat, which provided better nesting habitat and, therefore, better nest
success.
66
Temple (1987) suggested that nest predation is inversely related to the distance
between the nest and an ecological edge. Since many predators on turtle eggs inhabit
edge habitats, an increase in predator abundance would occur for nests near ecological
edges (Temple 1987). Almost all documented nests for this study occurred near forest
edges. I hypothesize that observed differences in predation rates among study areas were
attributable to variation in the habitat quality for predators or predator abundance. Poor
nesting success may be a result of turtles being forced to nest in fragments of habitat,
rather than having a choice in a more extensive continuous tract of habitat (Temple
1987).
Snow (1982) documented relatively constant predation rates throughout a nesting
season, while other researchers have suggested that predation decreases as nest age
increases (Tinkle et al. 1981, Congdon et al. 1983). I documented predation occurring
throughout the incubation period (Table 11) in accordance with Snow’s (1982) data.
Nests with inviable eggs occurred at all study areas. Inviable eggs located in
areas with a closed canopy have been associated with incubation temperatures too low for
embryonic development to be completed (Congdon et al. 1987). The 1 nest in the interior
forest area of White Clay Creek did contain inviable eggs. Most inviable nests were
located in open, sunlit areas such as the meadow at Webb Farm, in fields at Turkey Run,
and in fields adjacent to White Clay Creek State Park. Although I expected the opposite
to be true, the temperature was actually lower for inviable nests than for successful nests.
I expected the temperature to be greater at nests with inviable eggs, because I predicted
these nests would have temperatures too high for the developing eggs and the eggs would
67
be desiccated. Nests with inviable eggs had temperatures ranging from 22.0 – 26.8ºC,
and the typical range for male-biased nests was 22.5 - 27ºC (Ernst et al. 1994). However,
nests with eggs that hatched had a temperature range of 23.4 – 27.3ºC, which is only a
slightly higher range than those that did not hatch. Both hatched eggs and inviable eggs
had a temperature range well within the documented range for both males and females. I
cannot explain why, in some cases, only 1 egg within the nest hatched while the rest were
inviable, or why half the eggs in 1 nest hatched. I can only speculate that the successful
eggs were the uppermost eggs in the nest and, therefore, had the highest incubation
temperature.
The specific time frame for when sex ratios are determined in box turtle nests is
not known. Because I was unable to determine the sex of hatchlings when they emerged
from the nest, I have no way of knowing if nests were male-biased or female-biased; and
although I cannot predict sex ratio, the temperature data for both inviable and successful
nests did not exhibit a daily mean temperature high enough to produce females (Ewert
and Nelson 1991).
Nest Site Fidelity
Nest site fidelity has been documented for many turtle species, with the most
extensive research having been done on sea turtles. Stickel (1989) documented several
females returning to the same nesting area each year, some even observed in the same
location during a nesting season after a span of 6 - 32 years. One female was
documented nesting 20 m from her previous nest site in consecutive years (Stickel 1989).
Madden (1975) also established nest site fidelity in successive years in all but 1 case.
68
Three females at White Clay Creek traveled across a deep valley out to an open field in
both 2001 and 2002 to nest. One female at White Clay Creek crossed the park road and
traveled up a steep slope to the same field in both 2001 and 2002. There must be some
environmental cue or cues that are attractive to these turtles in order for them to expend
energy traveling such great distances to nest in the same location each year. Obbard and
Brooks (1980) suggest that if females find what they perceive to be a suitable nesting site
early in their reproductive lives that they would remain faithful to it in the future. Many
females in my study preferred nesting sites (i.e., areas where >1 turtle nested or areas
where females showed nest site fidelity) that were not areas with successful nests due to
either predation or inviability. In both 2001 and 2002, predation occurred at nests in
similar locations; and several turtles that nested near their 2001 nest site in 2002 had their
nests predated in both years. Congdon and colleagues (1983) documented that most
Blanding’s turtles (Emydoidea blandingi) demonstrated fidelity to a certain nesting area.
Similarly, I documented nest site fidelity for most females in my study. Valenzuela and
Janzen (2001) documented that females demonstrated fidelity to geographic areas within
a nesting beach and to microhabitat vegetation cover. In examining where most of my
turtles chose to nest, they appear to be seeking grassy areas with an open canopy cover
near a forest edge. This was not true for all turtles, but seemed to be the preferred type of
nesting area for most females.
Incubation Period and Hatchling emergence
A fairly wide range of incubation periods exists within eastern box turtles.
Incubation periods from Ewing (1933; 80 – 103 days), Allard (1948; 69 –136 days),
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Dodge et al. (1978; 51 – 81 days), and Stuart and Miller (1987; 77 – 80 days) were
consistent with my data (67 – 105 days). Hatchlings emerged within a narrow time range
in both years whether eggs were laid early or late in the nesting season, even when
nesting occurrences were well over a month apart (Table 11). A turtle (0014) with 2
clutches within a nesting season nested 10 June and 11 July, and the difference in
incubation time was considerable (28 days); yet hatchlings emerged from both nests
within a 1-week period of each other. This indicates that perhaps incubation times are
actually around the minimum range documented, and turtles that emerge at the maximum
time range are already fully developed well before emergence. Dodd (2001) suggested
that the warmer the incubation temperature, the shorter the incubation length would be;
so perhaps eggs laid later in the summer would have consistently higher temperatures
than those laid in May or early June and would develop with a shorter incubation time.
Management Implications
It is important to understand which environmental cues turtles use to select nest
sites because of the consequences for embryos and hatchlings. In order to identify habitat
needs of a particular species, like the eastern box turtle, areas associated with high rates
of nest success need to be identified. Development in areas that were once contiguous
forested areas causes habitat modification that can influence turtle movements and nest
site selection (Lue and Chen 1999). Knowing the number of females that reproduce each
year is important to estimating the fecundity of a population (Congdon et al. 1987). More
females reproducing annually increases the chance for a greater number of successful
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nests. Fecundity estimates are critical for developing management strategies and
conservation models (Congdon et al. 1987).
Although White Clay Creek had the lowest nest success of all the study areas, we
only sampled a small portion of the turtle population throughout White Clay Creek State
Park. The total population appears to be stable, based on the mark-recapture data
(Nathan Nazdrowicz, unpublished data). Turkey Run also appears to have a healthy
population based on the large number of turtles captured, including many juveniles,
despite turtle mortalities from mowing and the low nest success documented in my study.
Webb Farm had a larger turtle population than expected with many juveniles, so
recruitment seems to be satisfactory for this population. Almost half of the nests at Webb
Farm proved to be successful, including nests located in agricultural fields. There were
only 4 females at the UD Woodlot and 1 of these did not reproduce during my study. A
second turtle excavated 3 nests at the edge of a 4-lane highway, a third nested on
university property near buildings, and a fourth was never documented nesting. Although
2 out of 4 nests were successful, the eggs hatched near the road, quite a distance from the
forest edge of the UD Woodlot; so chances for hatchling survival may be low. With the
low population number at this study area and poor nesting habitat available, this
population could be extirpated in the near future.
In areas where mowing is prevalent (UD Woodlot and Turkey Run), maintaining
grass at an increased height would help prevent turtle mortalities. The same management
strategy could be applied to agricultural equipment used to maintain the alfalfa fields at
the UD Woodlot and the cornfields at Webb Farm. Nest site selection is not a variable
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that can be adjusted since it is the female’s choice, but providing quality areas that would
be attractive to nesting females is an option. I believe that, if available, females at Webb
Farm and the UD Woodlot would choose to nest in open fields like those available to
Turkey Run and White Clay Creek turtles. This type of habitat could be available if not
for the agricultural fields surrounding these areas; additionally, grass on athletic fields
adjacent to the UD Woodlot is maintained at such a low height that I do not think they
would be attractive to nesting females, even though they are open fields. Based on my
results, future research would be necessary to determine a sound management strategy for
each study area.
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