Growth of ornate box turtles was studied by measuring recaptured
turtles in the field, by periodically measuring captive hatchlings and
juveniles, and by measuring growth-rings on the epidermal laminae of
preserved specimens. Studies of growth-rings provided by far the
greatest volume of information on growth, not only for the years in
which field work was done, but for the entire life of each specimen
examined.
It was necessary to determine the physical nature of growth-rings and
the manner in which they were formed before growth could be analyzed.
Examination of epidermal laminae on the shell of a box turtle reveals
that each has a series of grooves--growth-rings--on its surface. The
deeper grooves are major growth-rings; they occur at varying distances
from one another and run parallel to the growing borders of the
lamina. Major growth-rings vary in number from one to 14 or more,
depending on the age of the turtle (Pl. 22). In juvenal turtles and in
young adults, major growth-rings are distinct and deep. Other grooves
on the shell--minor growth-rings--have the same relationship to the
borders of the laminae but are shallower and less distinct than major
growth-rings. One to several minor growth-rings usually occur on each
smooth area of epidermis between major growth-rings. As the shell of
an adult turtle becomes worn, the minor growth-rings disappear and the
major rings become less distinct. Both sets of rings may be completely
obliterated in old turtles but the major rings usually remain visible
until several years after puberty.
In cross section, major growth-rings are V- or U-shaped. The inner
wall of each groove is the peripheral edge of the part of the scute
last formed whereas the outer wall represents the inner edge of the
next new area of epidermal growth. The gap produced on the surface of
the lamina (the open part of the groove) results from cessation of
growth at the onset of hibernation. Minor growth-rings are shallow
and barely discernible in cross-section (Fig. 8). It may therefore be
understood that growth-rings are compound in origin; each ring is
formed in part at the beginning of hibernation and in part at the
beginning of the following growing season.
The few publications discussing growth in turtles express conflicting
views as to the exact mode of growth of epidermal laminae. Carr
(1952:22) briefly discussed growth of turtle scutes in general and
stated that eccentric growth results from an entirely new laminal
layer forming beneath, and projecting past the edges of the existing
lamina. Ewing (1939) found the scutes of _T. carolina_ to be the
thickest at the areola and successively thinner in the following eight
annual zones of growth; parts of scutes formed subsequent to the ninth
year varied irregularly in thickness. He stated that epidermal growth
took place at the margins of the laminae rather than over their entire
under-surfaces.
It is evident that the mode of scutular growth described by Carr
(_loc. cit._) applies to emyid turtles that shed the epidermal laminae
more or less regularly (for example, _Chrysemys_ and _Pseudemys_). In
these aquatic emyids a layer of the scute, the older portion,
periodically becomes loose and exfoliates usually in one thin,
micalike piece; since the loosened portion of the scute corresponds in
size to the scute below, it must be concluded that a layer of
epidermis is shed from the entire upper surface of the scute,
including the area of new epidermal growth. Box turtles ordinarily do
not shed the older parts of their scutes; the areola and successively
younger portions of the lamina remain attached to the shell until worn
off. The appearance of a single unworn scute, especially one of the
centrals or the posterior laterals, closely resembles a low, lopsided
pyramid.
Examination of parasagittal sections of scutes revealed that they were
composed of layers, the number of layers varying with the age of the
scute. A scute from a hatchling consists of one layer. A scute that
shows a single season of growth has two layers; a new layer is added
in each subsequent season of growth. Stratification is most evident in
the part of the scute that was formed in the first three or four
seasons and becomes increasingly less distinct in newer parts of the
scute. It may further be understood that scutes grow in the manner
described by Carr (_loc. cit._).
When the epidermal laminae are removed, a sheet of tough, pale grayish
tissue remains firmly attached to the bones of the shell beneath. This
layer probably includes, or consists of, germinal epithelium.
Contrasting pale and dark areas of the germinal layer correspond to
the pattern of markings on the scute removed.
[Illustration: FIG. 8. The second central scute from a juvenal
_T. o. ornata_ (KU 16133) in its third full season of growth.
A) Entire scute from above (A-- 2A1/2); dashed line shows portion
removed in parasagittal section. B) Diagonal view of section
removed from scute in "A" (A-- 4-3/8, thickness greatly
exaggerated) showing layers of epidermis formed in successive
seasons of growth. Each layer ends at a major growth-ring
(M 1-3) that was formed during hibernation; minor growth-rings
(m), formed in the course of the growing season, do not result
from the formation of a new layer of epidermis. Note the
granular texture of the areola (a); the smooth zone between the
areola and M1 shows amount of growth in the season of
hatching.]
Growth of epidermal laminae is presumably stimulated by growth of the
bony shell. As the bone grows, the germinal layer of the epidermis
grows with it. When growth ceases at the beginning of hibernation, the
thin edges of the scutes are slightly down-turned where they enter the
interlaminal seams (Fig. 8). When growth is resumed in spring, the
germinal layer of the epidermis, rather than continuing to add to the
edge of the existing scute, forms an entirely new layer of epidermis.
The new layer is thin and indistinct under the oldest part of the
scute but becomes more distinct toward its periphery. Immediately
proximal to the edge of the scute, the new layer becomes greatly
thickened, and, where it passes under the edge, it bulges upward,
recurving the free edge of the scute above. At this time the formation
of a major growth-ring is completed. The newly-formed epidermis,
projecting from under the edges of the scute, is paler and softer than
the older parts of the scute; the presence or absence of areas of
newly formed epidermis enables one to determine quickly whether a
turtle is growing in the season in which it is captured. There is
little actual increase in thickness of the scute after the first three
or four years of growth. The epidermal laminae are therefore like low
pyramids only in appearance. This appearance of thickness is enhanced
by the contours of bony shell which correspond to the contours of the
scutes.
Minor growth-rings differ from major growth-rings in appearance and in
origin. Ewing (_op. cit._: 91) recognized the difference in appearance
and referred to minor growth-rings as "pseudoannual growth zones."
Minor growth-rings result from temporary cessations of growth that
occur in the course of the growing season, not at the onset of
hibernation. They are mere dips or depressions in the surface of the
scute. The occurrence of minor growth-rings indicates that
interruptions in growth of short duration do not result in the
formation of a new layer of epidermis. Slowing of growth or its
temporary cessation may be caused by injuries, periods of quiescence
due to dry, hot, or cold weather, lack of food, and possibly by
physiological stress, especially in females, in the season of
reproduction. Minor growth-rings that lie immediately proximal to
major growth-rings (Pl. 22, Fig. 2), are the result of temporary
dormancy in a period of cold weather at the end of a growing season,
followed by nearly normal activity in a warmer period before
winter-long hibernation is begun. Cagle (1946:699) stated that sliders
(_Pseudemys scripta elegans_) remaining several weeks in a pond that
had become barren of food would stop growing and develop a growth-ring
on the epidermal laminae; he did not indicate, however, whether these
growth-rings differ from those formed during hibernation.
In species that periodically shed scutes a zone of fracture develops
between the old and new layers of the scute as each new layer of
epidermis is formed, and the old layer is shed. Considering reptiles
as a group, skin shedding is of general occurrence; the process in
_Pseudemys_ and _Chrysemys_ differs in no basic respect from that in
most reptiles. Retention of scutes in terrestrial emyids and in
testudinids is one of many specializations for existence on land.
Retention of scutes protects the shell of terrestrial chelonians
against wear. Some box turtles were observed to have several scutes of
the carapace in the process of exfoliation but no exfoliation was
observed on the plastron. Exfoliation ordinarily occurred on the
scutes of the carapace that were the least worn; the exfoliating
portion included the areola and the three or four oldest (first
formed) layers of the scute. The layer of scute exposed was smooth and
had yellow markings that were only slightly less distinct than those
on the portion that was exfoliating.
Wear on the shell of a box turtle reduces the thickness of scutes, as
does the shedding of scutes in the aquatic emyids mentioned. It is
noteworthy that any of the layers in the scute of a box turtle can
form the cornified surface of the scute when the layers above it wear
away or are shed.
It is uncertain whether turtles that have ceased to grow at a
measurable rate continue to elaborate a new layer of epidermis at the
beginning of each season. Greatly worn shells of ornate box turtles,
particularly those of the subspecies _luteola_, have only a thin layer
of epidermis through which the bones of the shell and the sutures
between the bones are visible. I suspect that, in these old
individuals, the germinal layer of the epidermis does not become
active each year but retains the capacity to elaborate new epidermis
if the shell becomes worn thin enough to expose and endanger the bone
beneath it. The germinal layer of old turtles loses the capacity to
produce color.
Major growth-rings constitute a valuable and accurate history of
growth that can be studied at any time in the life of the turtle if
they have not been obliterated. They are accurate indicators of age
only as long as regular growth continues but may be used to study
early years of growth even in turtles that are no longer growing.
Minor growth-rings, if properly interpreted, provide additional
information on growing conditions in the course of each growing
season.
Nichols (1939a: 16-17) found that the number of growth-rings formed in
marked individuals of _T. carolina_ did not correspond to the number
of growing seasons elapsed; he concluded that growth-rings were
unreliable as indicators of age and that box turtles frequently
skipped seasons of growth. Woodbury and Hardy (1948:166-167) and
Miller (1955:114) came to approximately the same conclusion concerning
_Gopherus agassizi_. It is significant that these workers were
studying turtles of all sizes and ages, some of which were past the
age of regular, annual growth. Cagle's review of the literature
concerning growth-rings in turtles (1946) suggests that, in most of
the species studied, growth-rings are formed regularly in individuals
that have not attained sexual maturity but are formed irregularly
after puberty.
Cagle's (_op. cit._) careful studies of free-living populations of
_Pseudemys scripta_ showed that growth-rings, once formed, did not
change in size, that the area between any two major growth-rings
represented one season of growth, and that growth-rings were reliable
indicators of age as long as the impression of the areola remained on
the scutes studied. Cagle noted decreasing distinctness of
growth-rings after each molt.
The relative lengths of the abdominal lamina and the plastron remain
approximately the same throughout life in _T. ornata_. Measurements
were made of the plastron, carapace, and abdominal lamina in 103
specimens of _T. o. ornata_ from Kansas and neighboring states. The
series of specimens was divided into five nearly equal groups
according to length of carapace. Table 3 summarizes the relationship
of abdominal length to plastral length, and of carapace length to
plastral length. The mathematical mean of the ratio, abdominal
length/plastral length, in each of the four groups of larger-sized
turtles, was not significantly different from the same ratio in the
hatchling group. The relative lengths of carapace and plastron are not
so constant; the carapace is usually longer than the plastron in
hatchlings and juveniles, but shorter than the plastron in adults,
especially adult females.
TABLE 3.--The Relationship of Length of Abdominal Scute to
Plastral Length, and of Plastral Length to Length of Carapace,
in 103 Specimens of _T. o. ornata_ Arranged in Five Groups
According to Length of Carapace. The Relative Lengths of
Abdominal Scute and Plastron are not Significantly Different in
the Five Groups. The Plastron Tends to be Longer than the
Carapace in Specimens of Adult or Nearly Adult Size.
===============+=========+===========================+==================
| | Length of abdominal |Individuals having
| | as a percentage of | plastron longer
LENGTH | Number | length of plastron | than carapace
OF CARAPACE | of | |
|specimens|----------------+----------+------+-----------
| |Mean A+-[sigma]m | Extremes |Number|Percentage
---------------+---------+----------------+----------+------+-----------
Less than | | | | |
50 mm. | 23 | 18.3A+-.498 |13.7-20.3 | 7 | 38.5
(Juveniles) | | | | |
---------------+---------+----------------+----------+------+-----------
50 to 69 mm. | 20 | 17.8A+-.303 |15.2-20.2 | 8 | 40.0
(Juveniles) | | | | |
---------------+---------+----------------+----------+------+-----------
70 to 100 mm. | 20 | 17.9A+-.445 |14.3-20.6 | 15 | 75.0
(Subadults) | | | | |
---------------+---------+----------------+----------+------+-----------
More than | | | | |
100 mm. | 20 | 17.8A+-.236 |16.4-20.6 | 13 | 65.0
(Adult males) | | | | |
---------------+---------+----------------+----------+------+-----------
More than | | | | |
100 mm. | 20 | 18.8A+-.510 |15.1-25.7 | 19 | 95.0
(Adult females)| | | | |
---------------+---------+----------------+----------+------+-----------
The length of any growth-ring on the abdominal lamina can be used to
determine the approximate length of the plastron at the time the
growth-ring was formed. Actual and relative increases in length of the
plastron can be determined in a like manner. For example, a
seven-year-old juvenile (KU 3283) with a plastron 74.0 millimeters
long had abdominal growth-rings (beginning with areola and ending with
the actual length of the abdominal) 5.9, 7.8, 9.5, 10.7, 12.0, 12.5,
14.3, and 14.9 millimeters long. Using the
[AB ABA╣]
proportion, [-- = -- ], where AB is the abdominal length, PL the
[PL X ]
plastral length, ABA╣ the length of any given growth-ring, and X the
plastral length at the time growth-ring ABA╣ was formed, the plastral
length of this individual was 29.3 millimeters at hatching, 38.8 at
the end of the first full season of growth, and 47.2, 53.2, 59.6,
62.1, and 71.0 millimeters at the end of the first, second, third,
fourth, fifth, and sixth seasons of growth, respectively. The present
length of the abdominal (14.9 mm.) indicates an increment of three
millimeters in plastral length in the seventh season, up to the time
the turtle was killed (June 25). This method of studying growth in
turtles was first used by Sergeev (1937) and later more extensively
used by Cagle (1946 and 1948) in his researches on _Pseudemys
scripta_. Because the plastron is curved, no straight-line measurement
of it or its parts can express true length. Cagle (1946 and 1948)
minimized error by expressing plastral length as the sum of the
laminal (or growth-ring) lengths. This method was not possible in the
present study because growth-rings on parts of one or more laminae
(chiefly the gulars and anals) were usually obliterated by wear, even
in young specimens. It was necessary to express plastral length as the
sum of the lengths of forelobe and hind lobe.
The abdominal lamina was selected for study because of its length
(second longest lamina of plastron), greater symmetry, and flattened
form. Although the abdominal is probably subject to greater, over-all
wear than any other lamina of the shell, wear is even, not localized
as it is on the gulars and anals.
In instances where some of the growth-rings on an abdominal lamina
were worn but other rings remained distinct, reference to other, less
worn lamina permitted a correct interpretation of indistinct rings.
Abdominal laminae were measured at the interlaminal seam; since the
laminae frequently did not meet perfectly along the midline (and were
of unequal length), the right abdominal was measured in all specimens.
Growth-rings on the abdominal laminae were measured in the manner
shown in Plate 22.
Data were obtained for an aggregate of 1272 seasons of growth in 154
specimens (67 females, 48 males, and 39 of undetermined sex, chiefly
juveniles). Averages of calculated plastral length were computed in
each year of growth for specimens of known sex (Figs. 9 and 10) and
again for all specimens examined. Annual increment in plastral length
was expressed as a percentage of plastral length at the end of the
previous growing season (Fig. 11). Increment in plastral length for
the first season of growth was expressed as a percentage of original
plastral length because of variability of growth in the season of
hatching; growth increments in the season following hatching are,
therefore, not so great as indicated in Figure 11.