Since 1993 we have conducted long-term
field studies (Belzer and Seibert 2007a) on potential methods to augment recruitment
in eastern box turtle (Terrapene carolina carolina) populations
in northwestern Pennsylvania. We
described our field sites in Belzer and Seibert (2009a). We use head started juveniles (Belzer
and Seibert 2007b) for some aspects
of the investigation. Our first attempts at head starting box turtle hatchlings did little more than
demonstrate how susceptible small
(30-50g) box turtles are to predation (Belzer et al. 2002). Yahner (1974) and Murphy (1976) reported that
after juvenile box turtles surpass
about 250g, they are no more susceptible to predation than are adults. We therefore adopted a modification
(Belzer and Seibert 2007b) of the
indoor headstarting method of Kathy Michell (New York Center for Turtle Rehabilitation and Conservation) which
produces juveniles of approximately
250g within 2 years. This report shares our observations on carapace color development gathered during
our first 7 years of headstarting
box turtle hatchlings.
Color
deficiencies accompany indoor headstarting
During our 2-year indoor headstart protocol
(Belzer and Seibert 2007b), scant
color developed in the juveniles' carapaces. Even after our turtles surpassed 250g and were ready for release,
their carapaces were generally
colored with little more than different shades of tan (Figs.1A, 2A,4A,5A, 6A,7A,8A, 9A,and 10A) and none of the bright yellows common among native eastern box turtles
(Fig. 3). That
color deficiency made us wonder if
other physiological functions (e.g., immunity) were also hindered by our headstarting
conditions. We were relieved to find
that not only were our headstarted juveniles healthy after their first year in the wild (and remain
so to this day, 6 years later, Belzer
and Seibert 2007b), but that their carapaces had started to develop the bright patterns (Figs. 1B,2B,and4B) typical
of this species.
An outdoor
environmental trigger for carapace pigment production
This observation suggested that something
found in the natural habitat, missing
from our headstarting environment, is needed to promote carapace pigment production. Alternatively, maybe carapace
color development in this species
is an age-related phenomenon that begins at about 2 years. Perhaps the start of our juveniles' life in
wild habitat simply coincided with
color development that would have started regardless of environment.
Because our headstarting protocol (Belzer
and Seibert 2007b) varies slightly
from Kathy Michell's, we were able to distinguish between these two hypotheses. Unlike us, Kathy puts her headstarted
juveniles outdoors for the few
summer months at the end of their first winter of indoor rearing, before returning them indoors
for their second year. Her
unpublished photos (pers. comm., December 2008) show that her headstarted box turtles start generating carapace
color when outdoors during their
first year, well before ours (whose first exposure to the outdoors generally begins not till age 2 years).
On-line photos of baby eastern
box turtles, posted by other workers, also document instances of good carapace color appearing before 12 months
(retrieved 15 July 2009 from http://www.aboxturtle.com/box_turtle_hatchling_care.htm),
and before 18 months (retrieved
15 July 2009 fromhttp://boxturtlesite.info/boxbabypics.html).
Pigment production in our juveniles
was evidently artificially delayed. Something in the outdoor habitat triggered their later carapace color
development.
De Vosjoli (1992) states that loss of
color in captive box turtles (T.c.c.) "...can be partially due to a diet lacking in
plant pigments" and that
supplementing the diet with plant pigments helps maintain color. It is unclear if he means skin or shell color.
The manufacturer of Kaytee Land
Turtle Fortified Daily Food®, however, specifically claims that their food contains "...special plant ingredients which provide the nutrients
necessary for excellent shell color..." (retrieved 15 July 2009 from http://www.amazon.com/gp/product/B00068K2AE).
Statements like those suggested
to us that the remarkable color change that we see after our juveniles are released might be due to
their change to a wild diet. But
understanding of carapace pigmentation physiology is rudimentary as noted by Rowe et al. (2006a) who state: "While we cannot rule out dietary influences on color
variation, we know of no instances where variation in dietary composition
has been shown to cause variation in pigmentation
of reptiles". Our findings below agree; they do not support a dietary hypothesis. Rather, they
suggest that sunlight has direct
and localized effects on cells (chromatophores? paracrine cells?), or on pigment precursors, that require
many months before generating the
more distinct yellows and browns, as well as intensification of the black markings, that
eventually appear in the carapaces
of our released juveniles. Although our indoor headstarting light was provided by "full spectrum" (10%
UVB [310 nm]; 50% UVA [360 nm])
LumichromeXX bulbs (Belzer and Seibert 2007b), it evidently failed to replicate sunlight.
A non-dietary
environmental stimulus for carapace color production
All box turtles in our study populations
carry a dome-shaped cap (Figs.1B, 2B,4B, and10C) which
houses the turtle's radiotransmitter (Belzer and Seibert 2009b). We were surprised, when
the first occasion arrived for
us to lift the cap and replace the transmitter on our juveniles, to discover that the cap-shaded portion of each
juvenile's carapace had failed
to produce the color and pattern enhancements appearing in contiguous sun-exposed areas (Figs. 4C, 5B,6B,7B,and10D). The coloration boundaries between sun-exposed and
shaded portions of the carapace
were rather sharply defined. Presumably, a dietary stimulation of color production would have been systemic
and would not have ended at the
sun-exposure border.
These findings argue that the color
which develops in our headstarted juveniles after they enter a natural environment
requires direct exposure to sun,
and is not a systemic aftermath of newly accessed forage.
Sun exposure
will initiate color production in previously-shaded, color deficient, regions of the carapace
As a test of the sun-exposure hypothesis,
we removed the transmitters and
caps from some of our juveniles for a few years to see if the previously shaded zones that were deficient
in pigment would generate color
once they received direct sun. They did, as is seen in Figs. 8B,8C,9D, and10F.
Our finding of deficient pigment production
in shaded regions of carapace might
have been an artifact of some factor, other than shade, associated with the presence of a transmitter
cap. Perhaps dead vegetation (or
even the transmitter) lodged under the cap emitted tannins or other chemicals that stained the
scute to create a misleading appearance
of deficient pigmentation, or exerted direct chemical interference with pigment production. But those
hypotheses would not account for
the delay in pigment generation (particularly during the second year) while our juveniles were indoors,
before a transmitter housing was
ever affixed to the carapace. And they would not seem able to account for the sharp color demarcation
between shaded and exposed regions.
We believe that the direct sunlight hypothesis is a better explanation of available data.
Carapace
pigment is not permanent
The juvenile seen in [Fig.
4 ] is unusual in that he started to produce some (if only a little) yellowish pigment before
he was exposed to sun (Fig. 4A).
Because of that initial coloration, his photo in Fig. 4C reveals that the shaded region under his transmitter
cap subsequently lost that early
pigmentation over a period of 2 years. Belzer (1997) had found that no such color loss occurred
in adults who carried transmitter
housings for as long as 5 years. The situation exhibited by the juvenile in Fig. 4prompted
us to revisit the phenomenon in adult box turtles.
Adult
carapace pigment appears to be more stable than juvenile carapace pigment after it is deprived of sun
Recent examination of adults in our
study populations revealed that
adults do (eventually) suffer some (if relatively slight) color loss in sun-blocked carapace regions. Their color-loss
is very slow, requiring an absence
of sun exposure that approaches a decade, especially in older adults. The relatively young (ca. 20-40 years)
male in Fig. 11 shows
mild, but obvious, carapace color
loss in the region that was shaded by his transmitter housing for 7 years.
Examination of older adults, on the
other hand, found no noticeable
color loss in such shaded zones till after 7 or more years of carrying a transmitter. But by 9 or 10 years without sun,
some of the color had started to
fade. The female in Fig. 12exhibits an almost imperceptible (no?) color loss in her (8-year shaded) first
right pleural area between the
transmitter flaps, when compared to adjacent, non-shaded scutes.
The dorsal regions of the first and
second right pleural scutes of the female in Fig. 13 had been shaded by her transmitter
cap for 10.5 years when this photo
was taken. Examination of those regions shaded by her transmitter cap reveals an almost imperceptible
color loss when compared to the
adjacent, sun exposed, areas of the first vertebral scute and ventral edges of the first and second right
pleural scutes.
The first right pleural scute of the
female shown inFig.
14had been shaded by
her transmitter cap for 12 years. A slight color loss is noticeable in that scute.
Fig. 15shows a different female whose
first right pleural scute had also been shaded by a transmitter cap for 12 years.
The color loss in her case is a
little more noticeable.
Fig. 16 shows a male whose second vertebral
scute had been shaded by his transmitter
cap for 14.5 years. The color loss in that shaded scute is rather slight.
The male in Fig. 17 has been in our telemetered
study population longer than any
other turtle. His second vertebral scute had been shaded by a transmitter housing for 15 years when we took
the photograph. Although the shaded scute exhibits a more obvious
color loss, his color pattern is
still pronounced. When we examined this male a decade earlier (reported in Belzer 1997) we found
no color loss under his transmitter
cap during the first 5 years of shade.
Finding that there is considerable delay
before color starts to fade in
older adults (compared to younger adults and juveniles) suggests to us that if carapace color has developed and has
been well established in an eastern
box turtle carapace for many years, then the pigment has a much longer half-life, after it is blocked from
direct sun, than does the newer
carapace pigment of younger animals.
Cooper and Greenberg (1992), and Rowe
at al. (2006a, 2006b), survey the fragmentary knowledge of physiological and morphological
color changes found in various reptiles.
The mechanisms that they describe involve time spans of minutes to months, and many employ
systemic mediators. The color
changes that we report here for juvenile (80 individuals), as well as adult (30 of which were examined for
this report) box turtles, do not
appear to involve systemic mediators, and fall outside the temporal parameters of mechanisms so far described
for chelonians. Elucidating the cellular
and chemical mediators, and mechanisms, of these slow color changes will likely require
laboratory study.
Acknowledgements
We are deeply indebted to the dozens
of volunteers (too numerous to name here) who kindly headstarted the juvenile box
turtles involved in our field studies.
We thank Kathy Michell for sharing unpublished data. We thank the owners of the large nature sanctuary
where we work for their generous
permission to conduct our studies. Without their enabling these long-term studies within their large land
holding, much of the insight we
are gaining into box turtle biology and ecology would have been impossible. We thank Edward Reindle for
kindly performing high resolution
scans of prints from photographs taken before we had digital cameras. Our long-term field investigations
are enabled by a special scientific
permit first issued to us in 1993 by the Pennsylvania Fish and Boat Commission.
Bibliography
Belzer, W.R. 1997. Observations on superficial
turtle scute condition after prolonged
covering by PC-7
epoxy. Bulletin of the Association of Reptilian and Amphibian Veterinarians 7:7-8.
Belzer, W.R., and S. Seibert. 2007a.
Long term movement histories for
headstarted and translocated adult and juvenile Eastern Box Turtles in NW Pennsylvania sanctuaries. Third Box Turtle
Conservation Workshop, November
9-10, 2007, Patuxent Wildlife Research Center, Laurel, MD. retrieved 15 July 2009 from http://www.boxturtlesintrouble.org/abstracts.html.
Belzer, W.R., and S. Seibert. 2007b.
Variable production of annual growth
rings by juvenile chelonians. Turtle and Tortoise Newsletter 11:10-13.
Belzer, W.R., and S. Seibert. 2009a.
How do male box turtles find mates?
Turtle and Tortoise Newsletter 13:11-21.
Belzer, W., and S. Seibert. 2009b. A
transmitter attachment method for terrestrial turtles, designed to protect the
radio module from mammalian chewing.
Turtle and Tortoise Newsletter 14:18-21.
Belzer, W.R., S. Seibert, and B. Atkinson.
2002. Putative chipmunk predation
of juvenile eastern box turtles. Turtle and Tortoise Newsletter 5:8-9. (Also accessible on-line,
retrieved 15 July 2009 from http://www.chelonian.org/ttn/archives/ttn5/pp8-9.shtml
)
Rowe, J.W., D.L. Clark, and M. Porter.
2006a. Shell color variation of
Midland Painted Turtles (Chrysemys picta
marginata) living in habitats with variable substrate colors. Herpetology
Review 37:293-298.
Rowe, J.W., D.L. Clark, C. Ryan, and
J.K. Tucker. 2006b. Effect of substrate
color on pigmentation in Midland Painted turtles (Chrysemys picta marginata)
and Red-Eared Slider turtles (Trachemys
scripta elegans). Journal of Herpetology 40:358-364.[abstract]
Murphy, J. 1976. The natural history
of the box turtle. Bulletin of the Chicago Herpetological Society 11:2-47
Yahner, R.H. 1974. Weight change, survival
rate and home range change in the
box turtle, Terrapene carolina.
Copeia 1974:546-548.