Field observations of North America’s eastern box turtle (Terrapene carolina carolina)
 |
William Belzer Box Turtle Conservation Trust 304 East Bissell Avenue Oil City, PA 16301-2004 USA |
Mistaken presumptions about box turtle population dynamics
When I was a young child, 60 years
ago, I routinely saw eastern box turtles crossing the rural roads in my home
state of Pennsylvania, USA. Not uncommonly, a crushed one would be seen on the
road bed. Such sightings seemed to me to be an integral part of summer’s
backdrop in southeastern Pennsylvania where I grew up; ‘something that would
always be there. My naïve assumptions back then were that a box turtle’s lifespan
was perhaps 10-15 years, that the turtles had the “common sense” to move out
and find safer habitat when road and other construction invaded their
territories, and that the road-kills I saw (or the “pets” that were so often
taken from woodlands by children a generation ago) were inconsequential losses
in the broader picture of this species’ long-term welfare. The color patterns
found among Terrapene carolina carolina are stunningly varied 
(Figs. 1-10) That, and their unusually flexible hinge,
which permits the closed plastron to completely seal appendages within the
shell (Figs.11 & 12), make them attractive to pet collectors. I had assumed
that individual adults lost from a population would steadily get replaced by successive
generations of abundant juveniles. Alas, all my youthful notions (as I was
eventually to learn) were wrong.
Eastern box turtles can live well beyond 100 years.
In the West Tisbury woods of Martha’s Vineyard island, Massachusetts, USA, there lived (and probably still lives) a female eastern box turtle over 150 years of age. Her shell bore carved initials and dates from 1861, 1881, 1932 and 1955. In the 19th & early-20th centuries it was a common, but ignorant, notion that a turtle’s shell was an inert sheathe, not the living layers of dermal and epithelial structures (akin to our finger’s nail bed) that it actually is. Carving initials into box turtle shells was a common practice, mistakenly assumed to be painless and harmless to the turtle. The repeatedly-inscribed West Tisbury box turtle was seen by Tom Hodgson (pers. comm.) in 2006 and photographed. Seventeen years earlier, in 1989, his (then, 9-year-old) daughter, Lucy, had seen and photographed it. A 1989 article (Lovewell, 1989) in the Vineyard Gazette (a Martha’s Vineyard newspaper) featured photographs and interviews with Lucy, local historians, and the (then, 57-year-old) man who had carved the 1932 initials. When Lovewell wrote his article, he was unaware that 57 years earlier his newspaper had published an article (Anonymous, 1932) about this same turtle. That 1932 investigation included an interview with the man who carved the 1881 initials when he was 14 years old, and whose family had known two of the young men who, just before going off to die in the U.S. Civil War, carved two of the several sets of 1861 initials and dates. The female was already an adult when those dates were carved in 1861. By the early twenty-first century, various amateur historians (including Tom Hodgson) had compared the 1932 and 1989 photographs, interviewed people linked to the initials, and authenticated the evidence for this turtle’s long life.
Other such ultracentenarian, carved box turtles have been intermittently found in their habitats over spans of more than a century (e.g., see p.430-431 in Ditmars, 1934; p.292 & Plate XII in Oliver, 1955; Graham & Hutchison, 1969; National Park Service, 2005). Likewise, researchers who have monitored box turtle populations over many decades (e.g., Stickel, 1978; Hall & al., 1999; Miller, 2001) have documented very old box turtles who are repeatedly found alive, still using their habitual haunts, over those long spans.
Box turtles have high “site fidelity”
Eastern box turtles tend to spend their long lives in the same habitat. Field studies spanning a half century or more have found specific box turtles still living in their native habitat, re-using favored nesting, hibernation, hydration and feeding sites (Stickel, 1989; Hall & al., 1999; Schwartz & al., 1984; Miller, 2000). If displaced, most box turtles try to return home. Their homing capability is not very successful outside 400-800 m of their home range (Lemkau, 1970; Posey, 1979; deRosa & Taylor, 1982). Many individuals display remarkable consistency in their use of selective sites for specific purposes. For example, we have monitored one male eastern box turtle via radio telemetry for 12 years, and counting. Each fall, in 11 of those years, he has returned the long distance from his summer habitat (about 800 m to the SE) to dig his hibernaculum within a few meters, sometimes exactly in the center, of the site in which he hibernated the winter before. In his one “off” year, he was heading northwest for his usual hibernation site during fall when premature, sustained, cold weather overtook him, prompting him to dig his hibernaculum 70 m shy (to the SE) of his habitual site. A female, which we have monitored for 10 years, always spends her summers within a small 0.2 ha area amid a cluster of windfalls. She leaves that home base each June in order to trek uphill to a corn field about 600 m away where she nests, thereafter returning to her windfall.
When habitat becomes fragmented by
roads or other construction, resident box turtles do not abandon their home
range; they continue to travel between their habitual nesting, hibernating, and
other sites. Such ongoing movements over their
traditional routes will likely bring them to harm from automobile traffic and
other human activities introduced by the “opening” of their habitat. With
habitats now so fragmented, many box turtles (where populations have not
already been extirpated) reach Veterinary and Animal Rehabilitation Clinics with
terrible injuries suffered when traversing zones used by humans. The
remarkable skill in such clinics has saved some, but certainly not all, of the
victims (Figs. 13-15).
Box turtle eggs and hatchlings suffer high mortality in natural habitats
Box
turtle nests are frequently ravaged by predators (Harless & Morlock, 1989; Ernst
et al., 1994; Dodd, 2001; Flitz & Mullin, 2006). At one study site in
northwestern PA, we recorded nearly 100% predation of box turtle nests (2002,
unpubl. data). Eggs in nests that are not attacked can die from climatic
extremes (Hallgren-Scaffidi, 1986; Zeiller, 1994; Tucker & al., 1997;
Tucker & Packard, 1998; Belzer, 2002). Any hatchlings that do emerge are almost
as vulnerable as eggs; their small, soft-shelled bodies (Figs. 16 -17) offer easy meals for an array of insects, amphibians,
reptiles, birds, and mammals (Madden,1975; Hallgren-Scaffidi, 1986; Ernst &
al., 1994; Dodd,2001; Belzer & al., 2002). Not until a juvenile is half
grown (250-300 g) do its survival prospects improve to that of an adult (Yahner,
1974; Murphy, 1976).
Reproductive capability comes slowly to a wild box turtle
Growth rates vary considerably with environmental conditions. In wild habitat, any hatchlings that do manage to escape death can take more than a decade before they grow to mating size (Ernst & al., 1994; Dodd & Dreslik, 2008; cf, http://www.hsus.org/web-files/PDF/hsus_turtle_report_2005.pdf ).
Not only do wild female box turtles take many years to begin laying eggs, but their small clutches often include infertile eggs (e.g. see Belzer, 2002).
In a species like the box turtle, loss of very few adults is a significant blow to a population’s stability
Given the species’ delayed sexual maturity, low reproductive potential, high juvenile mortality, and lack of compensatory reproductive responses to make up for population declines (cf., Brooks, 1997; Crouse, 1999; Heppell & al., 1999; see literature survey in Belzer, 2002), an adult box turtle must remain in its habitat for a full, long life if it is to contribute to its population’s continuation (cf., Congdon & al., 1993; Crouse, 1999; Musick, 1999). Removing adults strikes at the heart of box turtle population stability. A female box turtle can produce eggs as long as she lives (Miller, 2001), and probably needs her eight or more decades of egg production to actually leave behind a survivable adult replacement before her eventual death. Ron Nussbaum (in Yeoman, 2002) highlighted that peculiarity in their population dynamics as follows: "... what (should) a conservationist do with this information? Well, you would make sure the adults survive (in their native population)...". Very small losses (just one or two extra adults each year) can result in a gradual but inexorable (if imperceptible, in the short-term) decline toward extirpation (Doroff & Keith, 1990; Reed & al., 2002).
This recognition eluded many policy makers because "Long lived species (like box turtles) are particularly vulnerable because the very longevity of older individuals introduces a delay in management response... this matter of perception (makes) this a serious problem... persistent older stages mask declines in (juvenile) recruitment until the problem is well advanced…” (Crouse, 1999). Unlike box turtles, “most of the animals we try to protect such as deer, rabbits, and quail, are relatively short-lived (and produce numerous viable young)…” (Yeoman, 2002), life-history attributes which enable those animals to rebound from population losses.
We are now realizing that proactive conservation practices for box turtles are needed while resident densities are still high. Our own field work indicates that it may be nearly impossible to rebuild a decimated box turtle population (Belzer & Seibert, 2007b). This emerging understanding of box turtle population dynamics that accrued from relatively recent studies of living populations is supported by archaeological findings. Eighteenth century Iroquois in the western New York region of North America used box turtles for various cultural practices. The steady removal of adults eventually depleted regional box turtle populations, so that the Iroquois eventually had to switch to snapping turtles as a substitute in ceremonial and other uses (Adler, 1970). Now, with more than 200 years to recover in the remote, extensive habitat of those western NY locales, box turtle populations have not returned.
In 1994, recognition of the threats to Terrapene populations prompted The Convention on International Trade in Endangered Species (CITES) to add box turtles to Appendix II of its protection against collecting for international trade. Domestic collecting and trade, however, continued to be legal in many states within the U.S. through the late twentieth century. Increasingly, U.S. states are now adopting more aggressive conservation regulations for their native turtles (e.g., see “legal issues” section at http://www.petfinder.com/shelters/MD148.html ). Our 15 years of field work {see below}, however, suggest that these long over-due conservation measures have come too late to prevent the slow disappearance of many already-depauperated populations.
Naïve ideas about how to reverse population declines
At age 40, after decades far from my home state, I was hired by the Biology Department at Clarion University in the northwestern region of Pennsylvania. I was excited about my return to Pennsylvania and the prospect of re-experiencing walks through forests populated with box turtles and other wildlife I’d grown up loving during the summers of my youth. But after my first few years back, I’d seen not a single box turtle. When I asked older residents about the dearth of local box turtles, I generally got the reply: “Oh yes, when I was a kid I saw lots of them, but I haven’t seen any in quite a few years.” I wondered if the decline was peculiar to this northern corner of the state, and so I visited the southeastern Pennsylvania sites where box turtles had been very common during my childhood. I found that there, too, only a relatively few relicts remained in the once-flourishing populations.
Box turtles were in trouble; they were disappearing from their traditional haunts. And so I decided that, as an avocation, I would try to develop strategies that could rebuild dwindling or extirpated populations. I didn’t expect that it would be difficult. My naïve notion was that I’d simply go to areas that had lots of box turtles, collect some, release them in forests surrounding my University, and in just a few years I’d once again see my old friends (if only juveniles, at first) wandering summer’s local woodlands. Fortunately, before attempting such a misguided idea, I learned that my vague plans were terribly ignorant, and would be antithetical to my goal of improving this species’ chances for survival.
When I spoke to Robert Cook (then a graduate student who had spent many years of field work on a box turtle repatriation project in New York state), he warned me that relocated box turtles are not prone to settle into new habitat. He had found (Cook, 1996) a high emigration rate from his 400 ha study site in New York's Gateway National Recreation area. {See Belzer, 1997; Belzer,1999a; and Belzer & Steisslinger, 1999 for other important environmental risks and considerations involved in relocating turtles.}
Bob Cook’s experiences helped me
develop a more rational plan to try to rebuild disappearing box turtle
populations. Bob had found that 50% of his released turtles either died or dispersed
beyond the boundaries of his expansive research sanctuary during their first 5
years or so. I predicted that a relocated turtle, whose movements are monitored
with radio telemetry (Fig. 18), could be
encouraged to adopt a new habitat if it were repeatedly retrieved, and returned
to the sanctuary core, whenever it ventured outside sanctuary boundaries. We
found, however, that even when retrieved numerous times across a span of many
years, and provided offerings of favorite foods and mates in the sanctuary core
when retrieved (in hopes of getting the turtle to associate the sanctuary with
needed resources), many turtles did not adopt homes within sanctuaries of 80 ha
and 200 ha (Belzer, 1999b; Belzer &
Seibert, 2007b). After 15 years of field work, we now estimate that a sanctuary
size of over 800 ha is needed in order to accommodate the dispersal of released
turtles (Belzer & Seibert, 2007b). Klemens (1999)
had speculated that native turtles need sanctuaries greater than 400 ha; Gibbs
& Shriver (2003) estimated a 1000 ha minimum. We anticipate that we will
see even greater dispersal among our relocated turtles as more years pass, and our
estimate for minimum sanctuary size will need upward revision.
What I originally envisioned to be a casual project, that would meet with success after perhaps 5 years of field work, turned out to be a daunting, unending undertaking. It now occupies the vast majority of my time (enabled by my retirement from teaching), and requires the full-time efforts of a salaried field associate and numerous volunteers. Rebuilding just one self-sustaining box turtle population (if it doesn’t finally prove impossible) might well take a century of effort and perhaps $1,000,000 USD in expenditures.
Other findings from our field studies can be found on-line (http://www.chelonian.org/ttn/archives/ttn6/pp17-26.shtml ; http://www.chelonian.org/ttn/archives/ttn5/pp8-9.shtml ; lhttp://www.boxturtlesintrouble.org/abstracts.html ) and in print (e.g., Belzer, 2009; Belzer & Seibert, 2007a; Belzer & Seibert, 2009; Belzer & al., 2007; Johnson & al., 2008). I will focus the remainder of this article on a few surprises” (to me) about box turtles that emerged during our years of observing them in their natural habitat.
Males need to see females in order to find them
During our early field observations, I began to notice that even “alpha” males (i.e., ones who consistently and energetically courted and mated with any females that we carried to them) walked past motionless females, who were still in their overnight ”forms” or otherwise hidden from his sight. However, if I were to prod the female with a long branch, so as to create some motion, the passing male would abruptly look back toward her, and then rapidly approach and begin to court. This (astonishing, to me) observation suggested that the males of this species are unaware of the presence of a female (even nearby ones) unless they actually SEE them! Often, motion by the female is necessary to attract his attention (Belzer, 2002).
We conducted many different types of experiment to test this hypothesis that males use close-range visual cues, not distant signals, to find females. All tests supported the hypothesis (Belzer, 1999c; Belzer, 2002; Belzer & Seibert, 2009). For example, if 100% of the habitat’s females are penned behind an opaque fence for weeks or months at a time, the free-ranging males in the habitat fail to gravitate toward the pen (Belzer, 1999c; Belzer & Seibert, 2009). However, when we tested the proclivity of such males to mate, by periodically placing one inside the pen, he immediately moved to and courted the first passing female he saw. Without seeing the females, the males were evidently oblivious of their presence. Continuous thread trails (some spanned 5 consecutive days) for males living very close to the pen, when all females were confined inside, revealed that even the nearest neighboring males are not attracted by the aggregation of females hidden behind the fence (Belzer & Seibert, 2009).
When we placed a female only 10 cm from a male’s head, but hidden behind a low (12 cm high) visual barrier, males never became aware of the female’s presence (Belzer 2002; Belzer & Seibert, 2009). But when we lifted the barrier so the male could see the female, he energetically rushed to her and began courtship (Belzer, 2002).
When we tested rehabilitated males who had lost vision in only one eye, we found that the males failed to notice females on their blind side (even when the females were within a few centimeters of their hind leg) but actively chased and courted females on their sighted side (Belzer & Seibert, 2009).
The fact that males do not remotely discover prospective mates has important implications for conserving this species. As a population’s density declines, mating opportunities and population recruitment also decline. This insight partially explains the severe impact on population stability that losing adults has.
Ailing box turtles tend to incessantly soak in water
Another surprising bit of behavior we noticed was that our box turtles, when they were feeling ill, tended to soak incessantly (for weeks or months at a time), even before overt signs of illness were evident. Before starting my field studies, I had read field reports (Penn & Pottharst, 1940; Madden, 1975) of unusual individual box turtles that remain in, and even hibernate under, water. Thus, when I occasionally noticed an individual who was always in water I presumed it was one of those unusual individuals. I was to learn otherwise.
During most of the late summer and fall of 1996, I consistently found one of our males sitting on the bed of a creek, in virtually the same spot, never above the water line. I was worried by this odd behavior and so I periodically lifted him out of the water for inspection. He would rapidly close his shell when lifted out of the water and looked healthy, so I assumed he must be one of those rare box turtles that supposedly prefer to stay under water. When cold weather arrived in the fall, he moved a short distance downstream to a shallow tributary, in whose mud he dug to hibernate. In early spring of 1997 I found him on the bank, only one meter from his hibernation site, recently deceased and with his toes gnawed off. There were no signs on his shell or head to indicate that he’d been killed by a predator. I speculated that the foot damage came from small carrion feeders who found him after his death from unknown causes (perhaps depleted nutritional stores) shortly after his emergence from hibernation. I didn’t associate the previous season’s aquatic behavior with this later demise, but I now believe his submersion during the preceding summer and fall signified some undetected chronic illness or parasitism that finally claimed his life following the rigors of a winter’s hibernation. In the summer of 1997 one of our females spent her entire summer near the middle of a very shallow swamp. She made small moves within the swamp and if I dropped some cantaloupe or other dietary treat near her she moved to the food and ate heartily. And so I believed she was in good health. But I finally slogged out to lift her out of the water for inspection. She had a badly swollen joint. Veterinary exam found that a predator or sharp inanimate object had damaged the joint many weeks before. The ensuing, protracted inflammation irreversibly damaged the joint, leaving it useless.
Her case, later field experiences, and numerous subsequent infirmary observations indicate that “unusual” eastern box turtles who remain in water for long periods are struggling with an injury or disease (even if otherwise asymptomatic). Indeed, we now use such incessant-soaking-behavior as the alert that a turtle is probably in the early stages of illness and needs to be closely monitored. If the turtle’s appetite remains robust, and it can achieve behavioral fever in its wild habitat, it often gradually resolves its illness in situ. But if the soaking turtle’s appetite diminishes, we immediately evacuate it to our infirmary to provide a thermal gradient and regular changes of warm soaking-water. That simple intervention is sometimes sufficient to enable its immune system to return it, if only gradually, to full health; but if the underlying illness worsens and finally presents recognizable signs of respiratory or other infection, we begin systemic antibiotic treatment with the fluroquinolone, Enrofloxacin (BaytrilTM, 227mg/ml, Bayer Corporation, Animal Health Division, Shawnee, Kansas, USA). We give a subcutaneous injection (dose = 5 mg enrofloxacin per kg of body weight) in a foreleg on each of the first two or three days of therapy, followed by 10-11 additional doses given every other day.
Besides using incessant-soaking-behavior as a sign of oncoming illness, we now also use it as a good indicator of when an animal has fully recovered from a presenting illness. Antibiotic therapy can eliminate obvious signs of disease even before the animal has completely recovered. So long as the animal continues to soak incessantly and/or has poor appetite, we do not release it back into its habitat. This period of post-therapeutic convalescent soaking can last for several to many weeks. But allowing the extended convalescence to run its full course (signaled by the animal finally climbing out of its soaking bowl by its own volition, and not resuming its soaking behavior) has enabled our treated animals to avoid relapse, and to enjoy indefinite periods of robust health, back in their wild habitat.
Ranavirus is a newly-recognized cause of sudden die-offs in natural turtle populations
During our first ten years (1993-2003)
of field work, we became familiar with common box turtle illnesses like
respiratory, optic, nasal and otic infections (Fig. 19). We were impressed by the box turtle’s durability and ability to
survive protracted periods of illness (e.g. see Belzer, 2008). Even when illness
was not discovered for many weeks, with infection well advanced, therapeutic intervention
generally enabled the turtle’s full recovery. But in August of 2003, we began
to encounter box turtles in our study site who were alert, mobile and in
apparent good health one day, but 4-8 days later were dead; or moribund with
eyelids sealed shut, gaping mouth with caseous coating, and almost no muscle
tone. We’d never imagined (let alone encountered) a disease that could kill a
box turtle so rapidly. Thirteen individuals (about 20% of the study-site’s population)
died before October’s chill arrived and induced the survivors to dig
underground for winter. Our previously reliable antibiotic, heat and soaking
treatments did nothing to slow the rapid demise of turtles afflicted with this
“sudden death plague” that emerged late in the 2003 season. Pathology
Laboratories at several University and State agencies could not identify the
primary pathogen – they found only disparate, opportunistic, secondary infectious
agents. Toxicology screens were negative.
Finally, when we consulted the Veterinary College at the U of Florida, in Gainesville, Florida, USA, the cause of the mysterious deaths was identified. Dr. April Johnson, working in the Laboratory of Dr. Elliott Jacobson, and using recently developed DNA probes, had identified Ranavirus (from the family, Iridoviridae) in tissue samples archived from unexplained turtle die-offs in the past. Her evidence suggested that this virus was the causative pathogen for those puzzling die-offs (Johnson et al., 2004; Johnson et al., 2008). When I described the signs and rapid morbidity/mortality occurring in our Pennsylvania population, Dr. Jacobson speculated that Ranavirus might well be the etiologic pathogen, and requested dead specimens for necroscopy and PCR-tests. Indeed, their DNA probes confirmed their suspicion (http://www.deserttortoise.org/abstract/abstracts2004/2004abs27.html).
2003 had been an exceptionally wet summer in northwestern Pennsylvania. It followed several previous summers of drought. Ranavirus is carried by various amphibians (Johnson et al, 2008) and Jacobson speculated that the proliferation of temporary ponds across our study site during the heavy rains of 2003 might have fostered an amphibian population explosion, with some of them carrying the virus as they dispersed from their natal pools following metamorphosis later in the season.
None of the turtles who survived to hibernate in the fall of 2003 died during their winter hibernation. Tests by Dr. Johnson, and colleague April Childress, in spring 2004, revealed that dead amphibians in our habitat indeed carried the virus, but that our surviving turtles had not developed antibodies to the virus. Evidently, the virus kills box turtles so rapidly (via its massive damage to liver, kidney, lung and other organs) that an infected individual has too little time to develop immunity before it is killed by the disease.
Our 2004 season saw more deaths (but only 5) from the virus. As was the pattern in 2003, the deaths did not start till late in the season. 2005 also saw this pattern: Ranavirus deaths not starting till late in the season. The 2005 population loss was still lower (4 individuals). 2006 saw only 2 deaths; and 2007 saw no deaths.
Given the fact that an immunologic response had not developed within our population’s surviving turtles, we don’t know how to interpret the steady decline in deaths over the 5 year period. Perhaps surviving individuals are genetic variants with a “natural” immunity provided by virally-incompatible cell receptors; perhaps viral abundance has steadily declined in the habitat’s vector populations. Laboratory experiments have not yet elucidated the mode of this virus’s transmission in natural habitats. Although intramuscular injection of the virus produced the systemic disease seen in the wild, the hypothesis that systemic disease emerges in wild turtles via an oral or intestinal route (following ingestion of infected amphibians) failed to gain experimental support (Johnson, 2007).
Our study population is uniquely situated to contribute future insight into the natural history of this viral plague; it is the only one to date in which movements of all turtles before, during, and after the viral outbreak in a natural habitat are known. Our long-term telemetric monitoring of the population’s turtles for our repatriation studies (Belzer 1999b; Belzer & Steisslinger 1999) ensures that we’ll continue to gather such information.
Our growing understanding of population dynamics and threats for this species shows that strong conservation measures that protect habitat and prevent removal of resident adults must be started while a box turtle population’s density is still high. We are learning that box turtle recovery and remediation projects are costly, tenuous and quite possibly futile. Waiting until a population is in obvious decline (or even on the verge of extinction), before initiating aggressive conservation measures, has succeeded for some relatively short-lived and reproductively prolific animals, but that strategy will not work for species like Terrapene.
ACKNOWLEDGMENTS
I am grateful to Sandy & Collin Barnett of the Mid-Atlantic Turtle & Tortoise Society, to Cynthia Meisner of the Vineyard Gazette staff, and to Tom Hodgson of West Tisbury, Massachusetts for information about the ultracentenarian box turtle in West Tisbury woods, Martha’s Vineyard.
I thank Bob Tronzo and Wildlife Works, Inc for the photograph used in Fig. 15.
Figures: (Figs. 1-10), (Figs.11 & 12), (Figs. 13-15), (Figs. 16-17) (Fig. 18), (Fig. 19)
LITERATURE CITED
Adler, K. 1970. The influence of prehistoric man on the distribution of the box turtle. Annals of the Carnegie Museum 41:263-280.
Anonymous. 1932. Box turtle preserves record of Civil War. P.1, In 17 June issue of Vineyard Gazette, Vineyard Gazette, Inc., Edgartown, Massachusetts, USA.
Belzer, W. 1997. Box turtle conservation issues. Reptile and Amphibian Magazine 49:32-35.
Belzer, B. 1999a. Repatriation criteria. Box Turtle Research and Conservation Newsletter 8:2-3.
Belzer, B. 1999b. Home range establishment by translocated eastern box turtles. Box Turtle Research and Conservation Newsletter 8:3-7 and 20-22.
Belzer, B. 1999c. Sexual proclivity among translocated male T. c. carolina. Box turtle research & conservation newsletter 8:8-9.
Belzer, B. 2002. A nine-year study of eastern box turtle courtship with implications for reproductive success and conservation in a translocated population. Turtle and Tortoise Newsletter 6:17-26.
Belzer, W.R. 2008. Spontaneous resolution of aural abscesses in the Eastern Box Turtle (Terrapene carolina carolina). Journal of Herpetological Medicine & Surgery 18:64-66.
Belzer, B., & M.B. Steisslinger. 1999. The Box Turtle: Room with a View on Species Decline. The American Biology Teacher 61:510-513.
Belzer, W.R., & S. Seibert. 2007a. Variable production of annual growth rings by juvenile chelonians. Turtle and Tortoise Newsletter 11:10-13.
Belzer, W., & S. Seibert. 2007b. Long term movement histories for headstarted juvenile, and translocated adult and juvenile Eastern Box Turtles in NW Pennsylvania sanctuaries. Third Box Turtle Conservation Workshop, November 9 - 10, 2007, Londontown Public House and Gardens, Edgewater, Maryland, USA. Retrieved June 15, 2008 from http://www.boxturtlesintrouble.org/abstracts.html
Belzer, W.R., & Seibert. 2009. How do male box turtles find mates? Turtle and Tortoise Newsletter 13:11-21.
Belzer, W.R., S. Seibert, and B. Atkinson. 2002. Putative chipmunk predation of juvenile eastern box turtles. Turtle and Tortoise Newsletter 5:8-9.
Belzer, W.R., A. Belzer & S. Seibert. 2007. Soil temperature and nest site selection by the eastern box turtle, Terrapene corolina corolina. Turtle and Tortoise Newsletter. 10: 10-15.
Brooks, R.J. 1997. Dynamics of a northern population of snapping turtles: How can long-lived species be conserved? Pp. 31-38, In T.F. Tyning (Ed.), Status and Conservation of Turtles in the Northeastern United States. Massachusetts Audubon Society, Serpent's Tale publishing, Lanesboro, MN. 53 pp.
Congdon, J.D., Dunham, A.E. & van Loben Sels, R.C. 1993. Delayed sexual maturity and demographics of Blanding’s turtles (Emydoidea blandingii): implications for conservation and management of long-lived organisms. Journal of Conservation Biology 7:826-833.
Cook, R.P. 1996. Movement and ecology of Eastern box turtles repatriated to human habitat. Box Turtle Research & Conservation Newsletter 5:8.
Crouse, D.T. 1999. The consequences of delayed maturity in a human-dominated world. Pp.195-202, In A. Musick (Ed.). Life in the Slow Lane: Ecology and Conservation of Long-lived Marine Animals. American Fisheries Society Symposium #23, American Fisheries Society, Bethesda, MD. 260 pp.
deRosa, C.T. & D.H. Taylor. 1982 A comparison of compass orientation mechanisms in three turtles (Trionyx spinifer, Chrysemys picta and Terrapene carolina) . Copeia 1982: 394-399
Ditmars, R.L. 1936. The Reptiles of North America: A Review of the Crocodilians, Lizards, Snakes, Turtles and Tortoises of the United States and Northern Mexico. Doubleday and Company, Inc. New York, NY. 476 pp.
Dodd, Jr., C.K. 2001. North American Box Turtles: A Natural History. University of Oklahoma Press, Norman, OK. 1231 pp.
Dodd, Jr., C.K. & M.J. Dreslik (2008) Habitat disturbances differentially affect individual growth rates in a long-lived turtle. Journal of Zoology 275:18-25.
Doroff, A.M., & L.B. Keith. 1990. Demography and ecology of an ornate box turtle (T. ornata) population in south-central Wisconsin. Copeia 1990:387-399.
Ernst, C.H., J.E. Lovich, & R.W. Barbour. 1994. Turtles of the United States and Canada. Smithsonian Institution Press, Washington, D.C. 578 pp.
Flitz, B.A., & S.J. Mullin. 2006. Nest-site selection in the eastern box turtle, Terrapene carolina carolina, in Illinois. Chelonian Conservation and Biology 5:309-312.
Gibbs, J. P. & W. G. Shriver. 2002. Estimating the effects of road mortality on turtle populations. Conservation Biology 16: 1647-1652.
Graham, T., & V.H. Hutchison. 1969. Centenarian box turtles. International Turtle and Tortoise Society Journal 3:25-29.
Hall, R.J., P.F.P. Henry, & C.M. Bunck. 1999. Fifty-year trends in a box turtle population in Maryland. Biological Conservation 88:165-172.
Hallgren-Scaffidi, L. 1986. Habitat, home range and population study of the eastern box turtle (Terrapene carolina). M.S. Thesis. University of Maryland, College Park, MD. 82 pp.
Harless, M., & H. Morlock. 1989. Turtles: Perspectives and Research. Robert E. Krieger Publishing Company, Malabar, Florida. 695 pp.
Heppell, S.S., L.B. Crowder, & T.D. Menzel. 1999. Life table analyses of long-lived marine species with implications for conservation and management. Pp. 137-148, In J.A. Musick (Ed.), Life in the Slow Lane: Ecology and Conservation of long-lived Marine Animals. American Fisheries Society Symposium #23, American Fisheries Society, Bethesda, MD.
Johnson, A.J., J.F.X. Wellehan, A.P. Pessier, T. Norton, W.R. Belzer, J.W. Brooks, R. Wagner, N.L. Stedman, J. Spratt, & E.R. Jscobson. 2004. Iridovirus infections of turtles and tortoises. Pp. 11-12, In C.K. Baer (Ed.), Proceedings: Health and Conservation of Captive and Free-ranging Wildlife Populations—a joint conference, American Association of Zoo Veterinarians, San Diego, California, 28 August–3 September.
Johnson, A.J., A.P. Pessier & E.R. Jacobson. 2007. Experimental transmission and induction of Ranaviral disease in western ornate box turtles (Terrapene ornata ornata) and red-eared sliders (Trachemys scripta elegans) . Veterinary Pathology 44:285-297
Johnson, A.J., A.P. Pessier, J.F.X. Wellehan, A. Childress , T.M. Norton, N.L. Stedman, D.C. Bloom, W. Belzer, V.R. Titus, R. Wagner, J. Brooks, J. Spratt, & E.R. Jacobson. 2008. Ranavirus infection of free-ranging and captive box turtles and tortoises in the United States. Journal of Wildlife Diseases 44:851-863.
Klemens, M.W. 1999. Landscape conservation: Implications for the protection and management of reptiles and amphibians. In Symposium Abstracts: Conservation and Ecology of Turtles of the Mid-Atlantic Region, 30-31 October, 1999. National Wildlife Visitor Center, Patuxent Research Refuge, Laurel, MD
Lemkau, P.J. 1970. Movements of the box turtle, Terrapene c. carolina (Linnaeus) in unfamiliar territory. Copeia. 1970: 781-783.
Lovewell, M.A. 1989. Is she the oldest? Box turtle isn’t telling. P.3, In 18 August issue of The Vineyard Gazette, Vineyard Gazette, Inc., Edgartown, Massachusetts, USA.
Madden, R.C. 1975. Home range, movements, and orientation in the eastern box turtle Terrapene carolina carolina. PhD. Dissertation. City University of New York. 217 pp.
Miller, J.K. 2000. Suburban sprawl and the three-toed crawl: a demographic population study of the three-toed box turtle across 35 years of land-use change. M.S. Thesis. University of Idaho, Moscow, Idaho. 95pp.
Miller, J.K. 2001. Escaping senescence: demographic data from the three-toed box turtle (Terrapene carolina triunguis). Experimental Gerontology 36:829-832.
Murphy, J. 1976. The natural history of the box turtle. Bulletin of the Chicago Herpetological Society 11:2-47
Musick, J.A. 1999. Ecology and conservation of long-lived marina animals. Pp. 2-20, In J.A. Musick (Ed). Life in the Slow Lane: Ecology and Conservation of long-lived Marine Animals. American Fisheries Society Symposium #23, American Fisheries Society, Bethesda, MD. 260 pp.
National Park Service, U.S. Department of the Interior. 2005 (9 March). Centenarian Turtle Found In Park. {Reissue of 23 October, 2002 Press Release}. Retrieved January 29, 2008 from http://www.nature.nps.gov/headlines/102302.cfm
Oliver, J.A. 1955. North American Amphibians and Reptiles. D. Van Norstrand Company. New York, NY. 359 pp.
Penn, G. H., Jr. & K. E. Pottharst. 1940. The reproduction and dormancy of Terrapene major in New Orleans. Herpetologica 2:25-29
Posey, M.H. 1979. A study of the homing instinct in Terrapene c. carolina in Maryland. Bulletin of the Maryland Herpetological Society. 15:139-140.
Reed, R.N., J. Congdon, & J.W. Gibbons. 2002. The alligator snapping turtle (Macrochelys {Macroclemys} temminckii}: A review of ecology, life history, and conservation, with demographic analysis of the sustainability of take from wild populations. A report to Division of Scientific Authority, United State Fish & Wildlife Service. published by University of Georgia, Savannah River Ecology Laboratory, Drawer E. Aiken, S.C. USA. 17pp.
Schwartz, E.R., C.W. Schwartz, & A.R. Kiester. 1984. The Three-Toed Box Turtle in Central Missouri, Part II: a Nineteen-Year Study of Home Range, Movements and Population. Missouri Department of Conservation Terrestrial Series #12, Jefferson City, MO. 30pp.
Smith, H.M. 1958. Total regeneration of the carapace in a box turtle. Turtox News 36:234-237.
Stickel, L.F. 1978. Changes in a box turtle population during three decades. Copeia 1978:221-225.
Stickel, L. F. 1989. Home range behavior among box turtles (Terrapene c. carolina) of a bottomland forest in Maryland. Journal of Herpetology 23:40-44.
Tucker, J.K., & G.C. Packard. 1998. Overwinter survival by hatchling Sliders (Trachemys scripta) in west-central Illinois. Journal of Herpetology 32:431-434.
Tucker, J.K., F.J. Janzen, & G.L. Paukstis. 1997. Response of embryos of the red-eared turtle (Trachemys scripta elegans) to experimental exposure to water-saturated substrates. Chelonian Conservation and Biology 2:345-351.
Yahner, R.H. 1974. Weight change, survival rate and home range change in the box turtle, Terrapene carolina. Copeia 1974:546-548.
Yoeman. B. 2002. Can turtles live forever? Discover, June 2002:61-66.
Zeiller, D. 1994. So You Like Turtles. Self-published, 88 Norman Place, Tenafly, NJ. 58 pp.
This is an English language publication of an article originally published in the journal Cheloniens 2008 12:12-25.
Published online by the Philadelphia Herpetological Society with permission of author and publisher.