BIOLOGICAL
CONSERVATION
Biological Conservation 88 (1999) 165±172
Fifty-year trends in a box turtle population in Maryland
Russell J. Hall a,*, Paula F.P. Henry b, Christine M. Bunck c
a
U.S. Geological Survey, Florida Caribbean Science Center, 7920 NW 71 Street, Gainesville, FL 32653, USA
b
U.S. Geological Survey, Patuxent Wildlife Research Center, Laurel, MD 20708, USA
c
U.S. Geological Survey, National Wildlife Health Center, Madison, WI 53711, USA
Received 20 September 1996; received in revised form 22 August 1998; accepted 26 August 1998
Abstract
A survey conducted in 1995 investigated long term declines reported in a population of box turtles Terrapene carolina monitored
each decade since 1945 in bottomland hardwood forest at the Patuxent Wildlife Research Center, Maryland. Methods duplicated
past surveys in most respects, but were supplemented by radiotelemetry and a survey of dominant vegetation. Seventy dierent
turtles were found on the 11.8 ha study area, a decline of >75% since peak populations were recorded in 1955. Searchers were less
ecient in 1995 than in 1945±1975 for a variety of possible reasons. Among turtles recorded, approximately equal numbers persisted from each of the past ®ve decades, with some individuals surviving >70 years. A sex ratio strongly favoring males was ®rst
recorded in 1975 and continued in 1995, but juveniles and subadults were found in greater proportion in 1995 than in any other
survey. Six of nine radio-marked turtles left the bottomland study area and migrated to the adjoining blus to hibernate, suggesting
more extensive movements and perhaps less stable home ranges than formerly thought. Age structure of trees indicated a gradual
change to more shade-tolerant species. Examination of rates of change from survey data suggested that major losses probably
resulted from changes in hydrology that exacerbated ¯ooding in 1972, with recovery only beginning in 1995 and perhaps limited
both by repeated ¯ood events and successional changes in the forest. Slow recovery from losses may indicate that populations of
this species would respond poorly to exploitation. # 1999 Elsevier Science Ltd. All rights reserved.
Keywords: Box turtle; Terrapene; Populations
1. Introduction
Soon after establishment of the US Department of
the Interior's Patuxent Wildlife Research Center in
1939, biologists began wide-ranging studies of many
resident species (Hall, 1988). Beginning in 1942, box
turtles were permanently marked by a standardized
system (Cagle, 1939) and in 1944 Lucille Stickel concentrated research eorts in part of the alluvial ¯oodplain of the Patuxent River that was to serve as the
control area for a study examining eects of applications of the pesticide DDT on populations (Stickel,
1951). Continued emphasis on the population of an 11.8
ha study area led to a comprehensive account of ecology
and behavior of the population (Stickel, 1950). Count
data from Stickel's multi-year study were particularly
complete in 1945, and surveys were repeated in 1955,
1965, and 1975 to examine long term trends in population size. The results (Stickel, 1978) indicated persistence
* Corresponding author. Tel.: +352-378-8181x305; fax: +352-3784956; e-mail: russ_hall@uscs.gov
of some individuals over the three decades of study, but
an overall population decline, despite protection of all
biota throughout the period. Stickel was unsure of reasons for the decline, but speculated that changes in
hydrology resulting from upstream impoundment of the
Patuxent River might be involved. Another less complete survey in 1985 suggested continuing decline
(Hallgren-Scadi, 1986). Additional reports (Stickel,
1989; Stickel and Bunck, 1989) dealt with detailed
aspects of home range and growth. Other studies of box
turtles have extended over decades (e.g. Schwartz et al.
1984; Williams and Parker, 1987), but none approaches
the Patuxent studies in length.
A survey of this box turtle population was conducted
in 1995 to continue surveys conducted in each decade
since 1945 in order to track changes in populations and
update records of persistence of individuals.
Eastern box turtles resemble other terrestrial
chelonians, which are extreme in some aspects of life
history and demography (Germano and Bury, 1994).
Individuals appear sedentary, some occupying the same
c.3 ha home ranges for more than four decades. Adults
0006-3207/99/$Ðsee front matter # 1999 Elsevier Science Ltd. All rights reserved.
PII: S0006 -3 207(98)00107 -4
166
R.J. Hall et al./Biological Conservation 88 (1999) 165±172
are long lived, with some turtles surviving >50 years.
Maturity is late and rates of reproduction are low. Rateconstants of change are low and, despite the unusually
long interval over which data are available on the
Patuxent population, the nature and causes of changes
in populations remain poorly understood. All box turtles of the genus Terrapene were recently included in a
proposed rule (US Fish and Wildlife Service, 1996)
under terms of the Convention on International Trade
in Endangered Species because it was believed that
increasing exploitation for the pet trade might lead to
unsustainable losses from populations.
2. Methods
2.1. Conduct of surveys
Our primary objective was to conduct a survey
resembling as closely as possible those of past decades
(Stickel, 1978) to permit comparison with count data
reported in previous surveys. Additional information on
age structure in the population, individual histories of
turtles marked in past decades, responses of the population to environmental factors, and changes in the
alluvial ¯oodplain forest that has been heavily used by
turtles was sought to help explain the nature, direction,
and causes of change. On the basis of exhaustive studies
spanning several years, Stickel (1950) was able to classify turtles as likely resident turtles, transients, or animals occupying ranges outside the study area. Singleyear surveys in subsequent decades (Stickel, 1978) did
not permit such classi®cation, however, and we followed
her practice of using the total number of turtles observed
on the study area as an index of abundance intended to
detect trends in the population using the area.
Prior surveys relied on frequent systematic searches of
the study area throughout the activity season. While
attempting to replicate past counts, we also used other
techniques to permit evaluation of the error inherent in
the primary survey method. These included conducting
sweep searches, with 10 or more searchers attempting to
cover the entire study area in a single period, and
attachment of radio transmitters to a subset of turtles
found to estimate the eciency of searches in detecting
animals present. Information on age, sex, location, and
behavior of turtles found was recorded. Standardized
methods for measuring, marking, and recording data on
Patuxent box turtles developed in the 1940s were followed with only minor modi®cations.
Individuals can be aged reliably from growth rings on
scutes for about the ®rst 20 years of life (Ewing, 1939;
Stickel and Bunck, 1989), and recaptures can extend
known ages by decades. Turtles with 10 or fewer growth
lines are here regarded as juveniles, those with 11±20 as
subadults, and those with 21 or more lines as adults;
data are not available to correlate these categories with
the onset of reproductive maturity, but animals with
fewer than 21 growth lines rarely had secondary sexual
characters fully developed and could not reliably be
identi®ed as to sex.
Locational data were reported with reference to the
330 foot (100.56 m) US Geological Survey (USGS) grid
system established in 1940 and marked with permanent
monuments. Investigators resurveyed the study area in
1993 and 1994, relocating permanent grid markers and
replacing or refurbishing intermediate sight reference
markers at &33.5 m intervals. Data on the occurrence
and identity of turtles on the study area were collected,
and repeated locations were used to evaluate residency
status.
The study area (Stickel, 1950) and adjacent areas in
the alluvial ¯oodplain of the Patuxent River were the
focus of surveys, but as in past studies, data collected on
box turtles from other locations on the Patuxent Wildlife Research Center were routinely recorded to supplement and help evaluate data from the study area.
2.2. Information on environmental change
A survey of dominant vegetation of the study area
begun in the Fall of 1994 and completed in 1995 was
undertaken to better understand environmental change.
A modi®ed point-quarter methodology (Cottam and
Curtis, 1956) was employed. Points were located at the
intersections of the 33.5 m grid lines used to subdivide
the study area, and at each point the species and diameter at breast height (dbh) of the closest tree >10 cm
in dbh were recorded, as were these data and the distance from the central tree of the closest tree in each of
the four sectors of the compass. Data were used to calculate relative frequency, relative density, and relative
dominance of each species. Available information on
land-use and hydrologic change, including analysis of
USGS data on daily and peak ¯ows of the Patuxent
River at Laurel, was evaluated as it related to turtle
population trends.
3. Results
3.1. Populations and persistence
In all, 103 turtles were recorded a total of 320 times in
searches and radiolocations. Of primary interest in
evaluating population trends were the 70 turtles located
190 times on Stickel's study area in searches extending
from April to November of 1995. Level of searching
eort was comparable to that of previous decades, and
captures tended to con®rm population trends observed
over past decades (Table 1, Fig. 1). Nevertheless, eciency of searches indicated by the mean number of
167
R.J. Hall et al./Biological Conservation 88 (1999) 165±172
Table 1
Eort expended and turtles recorded, 1945±1995
Year
Hours in searches
Days in ®eld
Turtles recorded
Total records
Captures/turtle
1945
1955
1965
1975
1985
1995
257
172
304
236
232
260 a
77
57
81
75
34
69
284
291
230
117
58
70
1002
1184
941
443
87
190 b
3.53
4.07
4.09
3.79
1.50
2.71
a
This total is minimal; it includes eort of primary searchers only and does not include 80 additional hours contributed by relatively inexperienced volunteers.
b
Captures in searches only; does not include radiolocations or captures o the primary study area.
Fig. 1. Numbers and age structure of turtles recorded in six surveys.
Animals reported as juveniles and subadults include all turtles with
fewer than 21 growth rings. Turtles with growth rings near 20 are
adult-sized, but generally lack the full array of secondary sexual characters. Individuals with fewer than ®ve growth rings are seldom seen
on the study area and are represented in the above totals only by two
individuals recorded in 1965 and one recorded in 1975.
captures per turtle was less in 1995 than in the 1945±
1975 surveys. Recaptures (Table 2) seemed to be proportionally distributed among old residents and newly
marked turtles, among young and old turtles, and those
in central and marginal regions of the study area, with
perhaps a slight tendency for old residents with home
ranges near the center of the study area to be recorded
more frequently. Adult males averaged 3.3 captures,
adult females 2.5, and subadults and juveniles combined
averaged 1.6 captures, but the dierences were not statistically dierent in a chi-square analysis of frequencies
(p=0.064). Among 26 animals captured only once, 10
were adult males, 6 were adult females, and 10 were
subadults and juveniles; adult males were most likely
(67%) and females least likely (54%) to be captured
more than once.
Of the 39 previously marked turtles, seven had been
®rst recorded in the 1940s, ®ve in the 1950s, six each in
1960s, 1970s, and 1980s, and eight in the early 1990s.
One apparently old turtle could not be traced to earlier
records owing to shell damage.
Forty-one turtles were judged to be >20 years old,
and eight of these had not been marked previously,
indicating that they were either missed in earlier surveys
or were recent immigrants; three of these turtles were
recorded only once during 1995, suggesting that they
may have been transients.
Age structure and overall population trends (Fig. 1)
indicate little change in adult numbers since 1985, but
apparent increases in the number of turtles estimated to
be <20 years old. These young comprised 22.2% of
populations in 1945±1965, and increased to 32.1% for
Table 2
Distribution of captures in 1995
Number of captures
Number of turtles a
Number previously unmarked
Died during
study
Number with <10
growth lines
Number on
marginal areas
1
2
3
4
5
6
7
8
9
Totals
26
16
11
4
4
4
3
0
2
70
12
11
4
2
0
2
0
±
0
31
1
2
1
5
5
1
0
0
0
0
±
0
11
13
8
5
1
1
2
0
±
1
31
a
4
33 additional turtles recorded on Patuxent but o the study area, 7 of which were bottomland residents and possible transient visitors to the
study area.
168
R.J. Hall et al./Biological Conservation 88 (1999) 165±172
Table 3
Ratios of juveniles and subadults to adult females recorded in surveys
Year
Adult females
Juveniles and
subadults
Number of young
per adult female a
1945
1955
1965
1975
1985
1995
122
119
85
37
12
13
55
78
58
39
17
29
0.45
0.66
0.68
1.05
1.42
2.23
a
These ratios are an index based on observations only. They permit comparisons among dierent surveys, but probably do not accurately represent relative numbers of adult females and immature
turtles in populations; juveniles are rarely observed and almost certainly have greater relative abundance than indicated here.
the 1975±1995 period, reaching a maximum contribution of 41.4% in the 1995 sample. Number of young
recorded per adult female shows a consistent pattern
through time (Table 3). Turtles nearing maturity may be
confused with older individuals which ceased growing
after 17 or 18 distinct growth lines had been laid down.
To conservatively estimate the relative abundance of
young individuals in the population, comparisons were
made using only juveniles with 5±10 growth lines. They
comprised 4.2% of the sample in 1945, 6.2% in 1955,
4.8% in 1965, and 15.7% in 1995.
Known-age turtles, those with fewer than 21 growth
lines at ®rst capture, included only 44 of the 70 turtles
recorded. Minimum ages (Fig. 2) include all available
data, but almost certainly underestimate average ages in
the population because those with 21 or more growth
Fig. 2. Minimum ages of turtles, based on known age turtles possessing fewer than 21 growth rings when ®rst recorded, and known
minimum ages of turtles with 21 or more growth rings when ®rst
recorded. If ages of all turtles were known, numbers in columns would
shift to the right for all categories, beginning with the >20 group.
lines at ®rst capture may have been decades older than
the 21±30 year class. Also, these ®gures may misrepresent recruitment because no turtles <5 years old
were found, continuing a pattern observed in past decades. Among adults recorded, 28 were males and 13
were females, but the probability of captures suggested
by recapture records suggests that the true relative
abundance of females may be greater than indicated by
these numbers.
Individuals observed to have died during the 1995
survey included two old turtles and two relatively young
turtles. A female estimated to be >71 years old died of
injury, possibly caused by a predator, and another
female >65 years old was suspected to have died of heat
exhaustion. The young turtles, estimated to be 9 and 18
years old, died apparently of disease.
Reanalysis of published (Stickel, 1978) and unpublished data on earlier surveys on numbers of adult turtles (Table 4) permitted tracking the persistence of
individuals and some overall comparisons of changes in
the population (Table 5). There were inadequate data
available from 1985, but 1995 data indicated that 77
adults were lost and 17 adults were added between 1975
and 1995. Average persistence rates (Table 5) of all
marked turtles show a slight decline for females in the
1955±1965 interval, and signi®cant losses for both males
and females in the 1965±1975 interval. The rates shown
for the 1975±1995 interval are close to those of the preceeding decade, but they re¯ect losses over an interval
twice as long.
3.2. Eciency of surveys
Radio transmitters were attached to three turtles on 8
June 1995, but appropriate receivers were not available
until 12 August; additional transmitters were attached
on 14 August, 10 September and 13 September. Nine
turtles (5 males, 1 female, and 3 subadults tentatively
identi®ed as males) were initially located by radio signals and then visually sighted 96 times. A primary ®nding was that turtles are far less visible than formerly
assumed; even when the location of an individual could
be narrowed to a few square meters, it often took
observers great eort to sight a turtle that was only
thinly concealed by vegetation or debris. On days when
turtles were known from radiolocations to be in the
open and potentially able to be found, a single searcher
had on the average only slightly more than a 10%
chance of ®nding them in a normal search session without the aid of radio signals. A second ®nding was that
movements appear to be more extensive and more
complex than indicated by past studies of home range
and movements (Table 6). The signal from one radioed
turtle was lost after 6 weeks while the animal was moving away from the study area. Another radio failed after
only 4 weeks, but was recovered 2 weeks later when the
169
R.J. Hall et al./Biological Conservation 88 (1999) 165±172
Table 4
Turtles recorded and persistence of adult turtles; 1945±1995
Year
1945
1955
1965
1975
1995
Cohort
1945
1945
1955
1945
1955
1965
1945
1955
1965
1975
1945
1955
1965
1975
1995
Males
Females
Both sexes
107
122
229
66
62
128
54
57
111
120
119
239
52
32
84
25
17
42
39
36
75
116
85
201
16
13
29
12
3
15
6
6
12
27
15
42
61
37
98
2
3
5
5
2
7
6
0
6
5
1
6
10
7
17
28
13
41
Table 5
Average persistence of all marked adult turtles, 1945±1995, based on the data of Table 4
Interval
1945±1955
1955±1965
1965±1975
1975±1995 a
Males
Females
Both Sexes
0.62
0.51
0.56
0.64
0.41
0.53
0.29
0.26
0.28
0.30
0.16
0.24
a
This is a 20-year period rather than the 10-year periods represented in earlier intervals; calculated average annual persistence rates of adult
turtles are as follow: 1945±1955=0.96; 1955±1965=0.95; 1965±1975=0.93; 1975±1995=0.96.
Table 6
Movements of turtles followed by radiotelemetry
Serial number
Identity
Number of locations
Inclusive dates
Diameter of movements
within home range a (m)
Travel outside home range after
1 October linear distance (m)
1117
1207
1318
1322
1429
1438
2406
2445
2446
Subadult
Adult
Adult
Adult
Adult
Adult
Subadult
Subadult
Adult
18
19
15
22
18
17
6
15
10
6/8±10/9
5/27±10/9
6/30±11/5
6/20±11/5
5/29±10/9
6/8±10/9
8/29±10/6
8/12±10/9
8/12±10/3
85
256
111
174
134
57
151
469
225
390
323
0
0
335
356
0
408
258
a
``Home range'', as used here refers to observed home ranges within the bottomland and does not account for annual migrations to nesting or
hibernation sites.
turtle was found in a visual search. Radios were
removed from six of the remaining turtles on 9 October.
Transmitters were left on two turtles and they were
located until 5 November, when they were in apparent
hibernation sites.
Other information may bear on the eciency of surveys. The number of turtles newly encountered in each
survey year should decline progressively through the
season as more turtles are found, eventually reaching
zero when all turtles have been encountered. Graphing
the occurrence of newly found turtles in each year
against the cumulative number recorded should provide
an estimation of those remaining unrecorded at the end
of the season, and an indirect measure of sampling eciency. Estimates based on this method indicate that
91% of the population was sampled in 1955, 90% in
1965, 86% in 1975, and 92% in 1995. New turtles
showed up erratically in the 1945 survey, and the
resulting graph does not support estimation of the
completeness of sampling. This approach probably does
not lead to a good estimate of total populations owning
to the uncertain number of transient individuals, but
correspondence among years may indicate comparable
eectiveness in sampling.
3.3. Changes in the study area
As in 1945 (Hotchkiss and Stewart, 1947), the forest
of the study area is dominated by two tree species,
tuliptree Liriodendron tulipifera and American beech
Fagus grandifolia. Fifteen other species were recorded,
including in order of decreasing overall importance
Liquidambar styraci¯ua, Ulmus americana, and Fraxinus
americana. But Liriodendron (45.4% of total basal area
in 1994) appears to have reproduced infrequently in
recent decades, whereas Fagus (19.9% of total basal
area in 1994) is reproducing strongly; in time therefore,
the forest may become a nearly pure stand of beech.
Only 24 of 88 (27%) of Liriodendron were <50 cm dbh,
whereas 71 of 83 (86%) of Fagus were smaller trees.
170
R.J. Hall et al./Biological Conservation 88 (1999) 165±172
Moreover, the smallest size class, 10±19 cm dbh,
includes 29 Fagus and only one Liriodendron. Frequent
damage to trees by beavers Castor canadensis in the
vicinity of creeks and sloughs suggests, however, that
succession may be arrested in these parts of the study
area and that limited open areas may be maintained.
Data on peak and daily ¯ows of the Patuxent River at
Laurel, c.10 km upstream from the study area, were
available from beginning of operation of USGS gauging
station 01592500 in late 1944 through 1994. Average
daily ¯ows (recorded as cubic feet per second and here
converted to cubic meters per second ± m3/s) declined
from c. 5 m3/s in the 1945 to 1954 interval to c. 3 m3/s
thereafter, presumably as the result of two upstream
impoundments. Peak ¯ows, which never exceeded 146
m3/s before 1954, reached 330 m3/s on 21 July 1956, 728
m3/s on 22 June 1972 (Hurricane Agnes) and 476 m3/s
on 26 September 1975. Presumably these greater peak
¯ows in later years occurred with massive releases of
stored water from impoundments. Average daily ¯ow
on 18 July 1945 at the peak of the ¯ooding that inundated the study area (Stickel, 1950) was 42.8 m3/s,
whereas the comparable peak ®gure for 22 June 1972
was 364 m3/s. The onset and dissipation of more recent
¯ood events (Fig. 3) seems more abrupt than the 1945
¯ood. The seasonal pattern of peak ¯ows seems to have
changed also; in 1945 through 1954 only three out of 10
years saw peak ¯ows occurring at times (April through
October) when turtles would be expected to be on the
study area, whereas peak ¯ows in 25 of the past 40 years
have occurred during the season when most turtles
would be in the bottomland.
4. Discussion
4.1. Changes in the population
Fewer captures per turtle in 1995 than in 1945±1975
may have re¯ected the relative inexperience of primary
searchers in ®nding turtles, reduced activity during a
record mid-summer drought, lack of ¯exibility to schedule surveys during times of presumed greatest turtle
activity as done in 1975 (Stickel, 1978), reduced visibility due to closure of the forest canopy, or some fundamental change in turtle use of the study area. Young
turtles are generally regarded as less visible and more
dicult to sample than adults, and the fact that 1995
searches revealed more young turtles than earlier surveys suggests that the cause may lie in changes in the
turtle population rather than dierences in the ability of
searchers or in the immediate environmental conditions
during searches.
Despite possible dierences resulting from lower eciency in ®nding turtles or from interpretation of ®eld
data, real declines in numbers of box turtles recorded in
surveys spanning 50 years are evident. Discounting
possible errors in counts, the population in 1995 numbered no more than 23% of the peak population of
1955.
4.2. Eects of altered hydrology and ¯ooding on
populations
Fig. 3. Record of four ¯ood events before (solid line) and since (broken lines) operation of upstream impoundments on the Patuxent
River. The 14±21 July 1945 ¯ood was reported by Stickel (1948, 1950)
to have completely inundated the study area, but to have had only
minor and reversible eects on the turtle population.
De®nitive reasons for changes have been elusive, but
evidence increasingly points to changes in hydrology.
Environmental changes in the surrounding region have
been dramatic, but the Patuxent Center lands in general
and the study area have been protected throughout the
period. Three separate lines of evidence suggest that
population declines have resulted from hydrologic
changes and ¯ooding, especially from the historic ¯ood
occurring in 1972. Available evidence includes: (1)
¯ooding since 1956 and especially in 1972, which has
resulted in daily ¯ows as much as eight times greater
than those observed to have totally inundated the study
area and mildly aected turtles in 1945; (2) severity of
¯ooding and losses of adult turtles were far greater
between 1965 and 1975 than in any other period; (3)
increases in relative numbers of young turtles in the
population since 1975 suggest incipient recovery, or at
least no pattern of decline in productivity.
Stickel (1978) speculated that increased severity and
altered periodicity of ¯oods owing to upstream water
R.J. Hall et al./Biological Conservation 88 (1999) 165±172
171
control might be responsible. She lacked direct evidence
that the massive ¯ooding caused in 1972 by Hurricane
Agnes had lasting eects on the population, and the
¯ood in 1945 that she documented (Stickel, 1948Stickel,
1950) had little eect on resident turtles. Even after the
record 1972 ¯ood some long term resident turtles continued to occupy traditional home ranges, but this ¯ood
was nearly an order of magnitude greater than the 1945
¯ood and almost certainly would have had severe eects
on all turtles present in the ¯oodplain.
Age structure within the population may have dierent interpretations, but seems to support the idea that
losses of turtles, particularly adults, are responsible for
population declines. Our observation of nearly equal
numbers of adults persisting from each of the ®ve decades of study may result either from declining recruitment or changes in survival rates during the period. The
greater proportion of young observed in 1995 than in
other decades may have dierent interpretations, but
suggests strongly that recruitment has not declined dramatically. Adults on the study area may not be the parents of the juveniles and subadults observed with them,
but the simplest explanation for changes over the decades may be changes in the population structure of the
turtles that use the area. The numbers of young turtles
observed in 1995 were 53% of those recorded in 1945
even though overall populations in 1945 exceeded by
fourfold those of 1995. One interpretation might be that
in 1995 the population was growing through increased
recruitment, but it might also indicate changed selective
pressures resulting in losses of adults that would change
population structure regardless of the trajectory of
population size. Assuming that adults and young represent the same population, total numbers of young turtles recorded and ratios of subadults and juveniles
observed relative to observations of adult females
(Table 3) suggest that losses of adults are the problem
and that declining populations are not the result of
decreased recruitment of young.
Stickel (1989), whose evidence suggested that most turtles hibernate within their summer ranges. Combined
with evidence that gravid females migrate to the uplands
for nesting (Stickel, 1989), these new ®ndings suggest
less stability of home ranges than reported earlier. If
some males leave their home ranges once each year, and
females undertake such movements as many as two
times each year, estimates of population density may be
made more dicult. Moreover, turtles with fewer than
®ve growth rings have been observed only three times in
over 3800 captures in all decadal surveys of this area
spanning 50 years, suggesting that very young turtles do
not use the bottomland study area.
4.3. Dierential habitat use among sexes and ages
4.5. Eects of losses on populations
A declining proportion of females over ®ve decades of
study is dicult to interpret, although potential consequences for recruitment seem obvious. Unbalanced
sex ratios in favor of males have been observed in other
box turtle populations (e.g. Dodd et al., 1994), but the
apparent reversal in sex ratio over the decades of surveys at Patuxent seems unique. Stickel (pers. comm.)
suggested that migration to the uplands for nesting may
make females more vulnerable to the regular mowing of
®elds and to progressively increased vehicular trac in
upland areas surrounding the study area as activities at
the Patuxent Center have increased.
Movement of six of nine radio-marked turtles outside
their home ranges in October diers from the ®ndings of
Catastrophic losses resulting from death or permanent displacement of turtles by episodic ¯ooding would
have aected those age classes present on the ¯oodplain,
which are primarily adults and subadults. Evidence
from past surveys (Table 4) indicates reduction of the
breeding population by one-half between 1965 and
1975. Had the trends observed in 1965±1975 continued,
the 1995 population would be only about one-half of
the number recorded. Turtles born in the years immediately following the 1972 ¯ood had only barely reached
adulthood in 1995, and growth of the population may
accelerate gradually as increased numbers of mature
adults join the breeding population. Indications of some
decline by 1965, of slow change in dominant vegetation,
4.4. Eects of vegetation change
Stickel (1978) stated that the forest canopy appeared
not to have closed by 1975, but quantitative data presented here indicate an apparent slow replacement of
the dominant tree species by a much more shade-tolerant species. Schwartz et al. (1984) presented evidence
that populations of the three-toed box turtle, a geographic race of Terrapene carolina, declined in an area
undergoing ecological succession to deciduous forest.
Williams and Parker (1987) found that T. carolina in
Indiana tended to remain in mature forest, but the
population under study declined >50% over a 25 year
period. Research on habitat selection on Long Island
(Madden, 1975) indicated that box turtles shunned both
dense forest and large openings, and concentrated most
activity in forest margins. Similar research on the threetoed subspecies in Arkansas (Reagan, 1974) indicated
seasonal change in habitats selected, with grasslands
selected over forest in cool, moist periods. Changes in
the upland habitats that are demonstrated here to be of
importance to the Patuxent population may have been
more dramatic than those on the ¯oodplain, and could
exert an important eect on those parts of the life cycle
not known from our studies.
172
R.J. Hall et al./Biological Conservation 88 (1999) 165±172
and of reduction of box turtle populations with ecological succession elsewhere suggest that, unless reduced
by major ¯ood events, populations may grow and stabilize at lower levels than those attained in 1955.
Should tentative conclusions about catastrophic loss
of individuals and slow recovery be con®rmed in the
future by gradual recovery and/or continuing losses
from ¯ood events, implications for the conservation of
box turtle populations could be signi®cant. Adler (1969)
argued that prehistoric consumption of box turtles
extirpated populations from large parts of the former
range. The dynamics of long lived vertebrates are highly
sensistive to changes in adult survival. Since their rates
of increase are low, turtles can be expected to recover
very slowly from catastrophic mortality.
Acknowledgements
The Division of Research and the Oce of Inventory
and Monitoring of the National Biological Service made
the study possible, primarily by granting the principal
investigators time o from other duties to work on
the study. The Oce of Scienti®c Authority of the US
Fish and Wildlife Service provided ®nancial support
covering the expenses of a full-time volunteer. Patuxent
Wildlife Research Center provided access to research
sites and buildings during the study. Lucille F. Stickel
provided us with updated summaries of data used in
preparation of her 1978 paper. Numerous volunteers
helped in dierent phases of the study, most notably
Nina Haramis, who participated throughout the study
and Rebecca Raynor of the University of Chicago,
Will Staube of the University of Maryland and Peg
Hall of Gallaudet University, who contributed frequently. Staff at the Upper Mississippi Science Center
and the California Science Center of the National Biological Service generously loaned radiotelemetry equipment. Sta at the Patuxent Wildlife Research Center
helped by reviewing study plans, loaning equipment,
providing technical advice, and bringing in turtles found
in their ®eld studies. O.J. Reichman and Lucille Stickel
critically reviewed the manuscript and oered helpful
suggestions.
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