Most of the morphological characteristics distinguishing box turtles
from other North American emyid turtles, the most notable of which is
the movable plastron, are modifications that have evolved as a result
of selectional pressures favoring adaptation to more or less
terrestrial existence. Similar adaptations have arisen independently
in several branches of the emyid stock (see introduction). The genus
_Terrapene_ seems to have departed farther from a generalized emyid
form than have other kinds of box-turtle-like chelonians. In a
morphological sense, _Terrapene ornata_ is clearly the most
specialized member of its genus now occurring in the United States
(my own studies have revealed that populations in western Mexico now
referred to as _T. klauberi_ and _T. nelsoni_ are as specialized as
_T. ornata_ in some respects but more generalized in others). The
present ecological study has demonstrated that _T. ornata_ is
specialized in habits as well as in structure. It is concluded that
these specializations (of more generalized and perhaps more primitive
conditions as, for example in _T. carolina_) constitute adaptation for
terrestrial existence in open, semiarid habitats. These adaptations in
_T. ornata_ have resulted, in a few instances, in unique habits and
structures; however, in most instances the adaptations have produced
slight but recognizable changes that are definable only by degree of
difference from other species of box turtles.
The closable shell of box turtles is of obvious survival value in
providing protection for the soft parts of the body. In most of the
species of _Terrapene_, the lobes of the plastron completely close the
openings of the shell; closure is so tightly effected in some
individuals that it is difficult to insert the blade of a knife
between the adpressed margins of carapace and plastron. In _T. ornata_
nevertheless, both lobes of the plastron are deficient on their
lateral margins; four narrow openings remain when the lobes are drawn
shut. Emargination of the plastron has occurred at the places where
the limbs rub against it during locomotion. This reduction of the
plastron permits the body to be held off the ground during forward
locomotion and seemingly permits a generally freer range of movement
for the limbs. The possible disadvantages of an imperfectly closable
shell seem to be compensated for by increased mobility. Reduction of
the plastron is correlated with a general lightening of the shell,
probably associated with the increased vagility of this species.
Lightening of the shell is evident also in the relatively thin,
loosely articulated bony elements. Shells of adult _T. ornata_ that
are old and weathered, or macerated (unless they are partly
co-ossified because of injury), can nearly always be disarticulated
with ease, whereas the bony elements in the shells of adult _T.
carolina_ (all races) are nearly always co-ossified or separable only
after prolonged maceration.
The relatively low, flattened shell of _T. ornata_ is an adaptation
associated with the tendency to seek shelter in the limited space of
earthen forms, burrows, or small natural cavities in the course of the
warm season and to burrow more deeply into the ground in winter.
_Terrapene ornata_ is, in fact, the only species of the genus that may
be considered an habitual burrower. Individuals of _T. carolina_ tend
to seek shelter in the warm season by making forms in dense vegetation
or by digging into yielding substrata such as mud or humus, although
they may burrow deeply into the earth in winter. Extreme weakness or
absence of the middorsal keel of _T. ornata_ seems to be a
modification associated with burrowing habits and general adaptation
to terrestrial life; the keel is similarly reduced in testudinids.
Retention of epidermal laminae (as opposed to regular exfoliation of
the older parts of scutes) occurs in all box turtles, in several other
groups of terrestrial emyids, and in testudinids. The phenomenon is
here considered to be a specialization of scute shedding--developed in
terrestrial and semiterrestrial chelonians--that provides additional
protection to the shell against wear and minor injuries.
General shortening of digits--the result of reduction in number of
phalanges as well as in their length, and to a lesser degree the
shortening of metapodial elements--has occurred in several groups of
chelonians with terrestrial tendencies (the opposite--lengthening of
phalanges and metapodials, and hyperphalangy--has occurred in certain
groups that are highly aquatic). The pes of box turtles has remained
relatively unchanged in this respect; a few phalanges on the lateral
digit have been lost (especially in three-toed forms), but little
reduction in length has occurred. The chief modification of the pes is
a general narrowing brought about by the tendency of the digits to be
crowded together, one on top of the other, rather than spread in a
horizontal plane. Considerably more modification is seen in the manus
of _Terrapene_. Phalangeal formulae (expressing the number of
phalanges from the first digit outward) range from 2-3-3-3-2
(primitive in _Terrapene_) to 2-3-3-2-2 in the races of _carolina_ and
have the same range in the species of eastern Mexico. Extreme
reduction in number (2-2-2-2-2) as well as general shortening of
phalanges occurs in _T. ornata_. The formula is the same in the one
specimen of _T. klauberi_ that has been skeletonized. This
modification of the forelimb in _T. ornata_ has produced a more rigid,
stronger manus that is well adapted to the requirements of burrowing
and to locomotion over unyielding substrata. Shortening of the manus
(and, to a lesser extent, the pes) has been accompanied by reduction
and loss of interdigital webbing. It is noteworthy that _T. ornata_
has achieved the same reduction in number of phalanges as _Gopherus_,
which displays the extreme of specialization in this respect among
North American turtles. The manus in _T. ornata_ is not shortened so
much as in _Gopherus_.
The first toe in males of _T. ornata_ is uniquely widened, thickened,
and inturned. Males of some other species of _Terrapene_ have greatly
enlarged rear claws, some of which turn slightly inward, but none has
the flexed first toe hooklike as it is in _ornata_ (a modified first
toe, resembling that described for _T. ornata_, has been observed in a
live male of _T. klauberi_ [now KU 51430] since the preparation of
this manuscript). In males of _T. ornata_ the penultimate phalanx of
the first toe has a normal, vertical articular surface on its proximal
end. However, the distal articular surface (when viewed from the
distal end of the phalanx) has its axis rotated away from the vertical
plane approximately 45 degrees in a counterclockwise direction. As the
foot is pronated and extended, and as the digits are flexed, there is
a concomitant inward rotation of the first metatarsal at its proximal
joint; this rotation, combined with the divergent planes of the
articulating surfaces on the penultimate phalanx, cause the ungual
phalanx to be flexed at right angles to the inner side of foot, in a
plane perpendicular to that of the other toes (Fig. 21).
The precise function of the modified first toe of males is unknown,
although it is reasonably safe to assume that the modification is
closely associated with clasping during coition. In the matings that I
observed, the inturned first claw of the male secured a hold on the
female's rump or just beneath her legs, whereas the remaining three
toes gripped the edge of her plastron. The combined hold, on shell and
skin, clearly affords the male a more secure position during coitus
(whether the female clasps his legs with hers or not) than would a
hold on skin or shell alone. Possibly intromission can be maintained
in this position even when the female is attempting to escape. In
males the plastron is less concave in _T. ornata_ than in _T.
carolina_. Furthermore, males of _T. ornata_ are, on the average,
smaller than females, whereas the reverse is true in _T. carolina_.
Possibly the ability of the male to secure an especially firm grip on
the female enhances the probability of small males mounting and
inseminating larger females, whereas successful matings might
otherwise be limited to pairs in which the male was the larger member.
It is worthy of note that turtles of the genus _Terrapene_ are
seemingly the only North American emyids that carry out the entire
process of mating on land; other, semiterrestrial emyids (for example,
_Clemmys insculpta_ and _Emydoidea blandingi_) return to water for
actual coition, although the precoital behavior sometimes occurs on
land.
Nearly all gradations from a fully developed zygomatic arch to a
greatly reduced arch can be observed in skulls of the various species
of _Terrapene_ (Fig. 2) (Taylor, 1895:586, Figs. 2-7). The highest
degree of reduction is achieved in _T. ornata_ and _T. klauberi_, both
of which lack the quadratojugal bone and have no zygomatic arch
whatever (except for an occasional, poorly defined anterior vestige
formed by the postfrontal, the jugal, or both). Reduction of the
zygoma clearly represents modification of a more generalized, complete
arch. As yet there is no clear evidence that reduction of the
zygomatic arch is of adaptive value. It is noteworthy, however, that
similar reduction of the arch has occurred independently in a number
of emyid and testudinid groups, nearly all of which have terrestrial
or semiterrestrial habits. Although discussion of phyletic lines in
_Terrapene_ is beyond the scope of this report, I tentatively suggest
that reduced zygomatic arches have arisen independently in more than
one group of _Terrapene_ and that similar reduction of the arch in two
species of the genus does not necessarily indicate an especially close
relationship of such species.
In a recent survey of cloacal bursae in chelonians, Smith and James
(1958:88) reported _T. ornata_ and _T. mexicana_ to be among the few
emyids that lacked these structures; in the opinion of the authors
(_op. cit._:94) cloacal bursae evolved in chelonians that required an
accessory respiratory organ for long periods of quiescence
(hibernation or aestivation) under water, and were secondarily lost in
terrestrial forms that hibernated on land. The assumption is a
reasonable one, at least in regard to emyids and testudinids. Lack of
cloacal bursae in _T. ornata_ and in all testudinids, can be
correlated with the completely terrestrial habits of those turtles.
Cloacal bursae seem to be vestigial in the species of _Terrapene_
possessing them and to be of little or no use as respiratory
structures (except perhaps in _T. coahuila_).
In most of the species of _Terrapene_ the carapace has a pattern of
pale markings on a darker background; however, unicolored individuals
are the rule in certain populations (for example, at the western edge
of the range of _T. carolina_ and in _T. ornata luteola_) and occur as
occasional variations in other populations (in _T. yucatana_, _T.
mexicana_, and, throughout the range of _T. carolina_, albeit more
commonly in the southeastern part of the range). Personal observation
of interspecific and ontogenetic variation of color patterns of box
turtles has convinced me that a basic pattern of more or less linear
radiations is the one from which all other patterns (including spots,
blotches, rosettes, and the unicolored condition) can be derived, and,
that the radial pattern is generalized and primitive for _Terrapene_
(possibly for all emyids and testudinids as well). In the light of
this conclusion, the radial pattern of _T. ornata_ may be considered
generalized. I suspect, however, that the pattern of a living species
most closely approaching that of the primitive ancestral stock of
_Terrapene_ is the pattern of fine, wavy, dark radiations (on a paler
background) present in young examples of _T. coahuila_.
Box turtles in general have lower reproductive potentials (as
indicated by fewer eggs and longer prepuberal period) than do most
aquatic emyids. This low potential seems to be compensated for by a
lower rate of postnatal mortality (especially in adults) due to the
protection afforded by the closable shell and the ability to recover
from serious injury. _Terrapene o. ornata_ and _T. c. carolina_ are
the only box turtles the life histories of which are known well enough
to permit significant comparison. The reproductive potentials of _T.
o. ornata_ and _T. c. carolina_ seem to be much the same.
[Illustration: PLATE 15]
Aerial photograph of Damm Farm (July, 1954).
Numbers and letters on photograph denote the following:
1. Main pasture with subdivisions
a to c, respectively, northwest corner area,
house pond area, and southern ravine area;
2. Wooded area; and,
3. Cultivated area.
[Illustration: PLATE 16]
FIG. 1. A water-filled ravine in the northern part of the
pasture at the Damm Farm (June 28, 1958). The subdivision of
the pasture referred to in text as "northwest corner area" can
be seen sloping into the ravine from the west (left
background).
FIG. 2. A cow path leading southward away from a ravine, at the
Damm Farm (June 28, 1958). Ornate box turtles used such paths
as routes of travel in the course of their daily activities.
[Illustration: PLATE 17]
FIG. 1. Grassland on crest of hill at Damm Farm with
northeastern corner of main pasture in background (June 29,
1958).
FIG. 2. A bare area along the rock fence at northern edge of
pasture at Damm Farm. Ornate box turtles could nearly always be
found foraging in cow dung here and in similar areas along
other fences (June 28, 1958).
[Illustration: PLATE 18]
FIG. 1. A ravine in the southern part of the pasture at the
Damm Farm (June 28, 1958). Small springs at the heads of such
ravines produced marshy conditions at their bottoms and
provided drinking water, in the form of shallow pools, for box
turtles for at least part of the year. Banks of ravines
provided suitable sites for the construction of nests and
forms.
FIG. 2. A mulberry tree on the bank of a ravine near northern
edge of Damm pasture (June 28, 1958). Box turtles frequented
the area beneath the tree when fruit fell to the ground in June
and July. The ravine shown here filled with water after being
dammed in June, 1956.
[Illustration: PLATE 19]
Representative stages in the spermatogenic cycle of
_T. o. ornata_ (all specimens obtained in Douglas County,
Kansas, 1955).
FIGS. 1 to 5, respectively, are sections of seminiferous tubules
obtained on May 17, June 14, July 15, Aug. 31, and Oct. 4.
FIG. 6: seminiferous tubule of immature male (plastral length,
88 mm.), six years old, obtained on June 30.
FIG. 7: section of epididymis from mature male obtained on
April 17, three days after turtle emerged from hibernation;
mature sperm form a continuous dark mass in center of
epididymis.
FIG. 8: sperm in uterine portion of oviduct of female obtained on
April 18, 1954.
Figs. 1 to 6 and 8 were photographed A-- 430, and were enlarged
1.4 times. Fig. 7 was photographed A-- 35, and was enlarged
1.4 times.
[Illustration: PLATE 20]
FIG. 1. Left ovary of mature female, prior to ovulation,
May 15, 1956 (A-- 1).
FIG. 2. Fresh corpus luteum, June 2, 1956 (A-- 4A1/2).
FIG. 3. Testes of mature male, August 31, 1955 (A-- 1).
FIG. 4. Testes of mature male, April 14, 1956 (A-- 2).
FIG. 5. Left ovary of subadult female (seven years old, plastral
length, 114 mm.) that would have matured in approximately one
year (A-- 1A1/2).
FIG. 6. Left ovary of juvenal female (11 years old, plastral length,
95 mm., A-- 1A1/2).
[Illustration: PLATE 21]
FIG. 1. A trial nest cavity excavated by a gravid _T. o. ornata_
at the Damm Farm on June 8, 1956. The cavity was situated at
the edge of a grassy area on the upper rim of a ravine
embankment. Twelve-inch ruler shows scale.
FIG. 2. A depression, resulting from an old post-hole, showing
the openings made by three box turtles as they left their
hibernacula in April, 1956 (photographed May 15, 1956).
Twelve-inch ruler shows scale.
[Illustration: PLATE 22]
FIG. 1. Right abdominal lamina (A-- 2A1/2) of a four-year-old
juvenal male showing method of measuring growth-rings. The
last growth-ring (4) was formed at the end of the 1954 growing
season. The first growth-ring (H) marks the end of the season
of hatching (1950). The umbilical scar (U) is faintly visible.
The growth-zone for 1955 (specimen captured June 23) is just
beginning to show in interlaminal seam.
FIG. 2.
_Left_--Right abdominal lamina (A-- 2) of subadult female, eight
years old. The last growth-zone was formed in 1954. Note
the relatively small growth increments in 1952 and 1953.
The growth-zone for 1955 (date of capture, May 8) is not
yet visible. This specimen grew more in the season of
hatching (1946) than the specimen shown above in Fig. 1.
_Right_--Interpectoral seam (A-- 3) of adult male showing
slowness of growth in later life. The widest growth-zone
seen here was formed in the tenth year and is followed by
four zones too narrow to measure accurately. It is uncertain
whether this specimen was still growing in the year it was
captured (1923).
[Illustration: PLATE 23]
Ontogenetic change in color and markings of carapace. Radial
markings begin to develop at the onset of epidermal growth.
Markings are sharply defined in juveniles and young adults but
may be obscured in later life by the encroachment of dark
ground color or by wear on the shell.
Figures are as follows:
_Upper left_--Hatchling (A-- 1A1/2);
_Upper right_--Juvenile (A-- 1), one year old;
_Lower left_--Juvenile (A-- 1), one year old;
_Lower left_--Female (A-- 7/16) showing typical adult markings;
_Lower right_--Adult male (A-- A1/2showing blotched pattern
resulting from wear on shell.
[Illustration: PLATE 24]
Ontogenetic change in color and markings of plastron. Dark
markings on plastra of hatchlings are unbroken. Dark radiations
appear when epidermal growth begins.
Figures are as follows:
_Upper left_--Hatchling (A-- 1A1/2);
_Upper right_--Juvenile (A-- 1);
_Lower left_--Female (A-- 7/16) showing typical adult markings;
_Lower right_--Adult male (A-- A1/2) showing the effect of wear
on markings. Plastra of old individuals are sometimes solid
yellow. Note the break in the plastron that has healed and
filled with ligamentous tissue.
[Illustration: PLATE 25]
Ontogenetic change and sexual dimorphism in shape, color, and
markings of head and neck. Females retain much of the juvenal
pattern of spots and blotches. In males, the top and sides of
the head become greenish or bluish and markings are obscured.
FIGS. 1 and 3. Lateral and dorsal views of hatchling (A-- 3A1/2);
FIGS. 2 and 4. Lateral and dorsal views of juvenile (A-- 2);
FIGS. 5 and 6. Adult female (A-- 1);
FIGS. 7 and 8. Adult male (A-- 1) showing relatively wider and more
truncated snout in this sex.
[Illustration: PLATE 26]
FIG. 1. A foraging station next to a rock fence at the Damm
Farm (June 28, 1958). The box turtle in foreground was in the
act of tearing apart a pile of partially dried cow dung to
obtain dung insects.
FIG. 2. A depression (A-- A1/2) made by a foraging box turtle in a
pile of partially dried cow dung (June 28, 1958). Similar
"sign" of box turtles was found in cow dung everywhere on the
pasture at the Damm Farm.
[Illustration: PLATE 27]
FIG. 1. Thread-laying device ("trailer") taped to the carapace
of an adult female _T. o. ornata_. The squares of tape on the
sides are to keep the bent-over ends of the wire axle from
catching on vegetation (A-- A1/2).
FIG. 2. A dermal pocket ("cyst") removed from an adult
_T. ornata_ and cut open to show two larval bot flies
(_Sarcophaga cistudinis_) (A-- 2, May 15, 1956).
[Illustration: PLATE 28]
FIGS. 1-3. Stages in courtship of _T. o. ornata_: male pursuing
female and biting her shell; male lunging at female in attempt
to mount; and, male just after mounting female (A-- A1/4).
FIG. 4. _T. o. ornata_ smelling food (A-- 1).
FIG. 5. _T. o. ornata_ in attitude of alertness after detecting
intruder (A-- 3/8).
FIG. 6. Tracks of _T. o. ornata_ in muddy ravine (A-- 1/8) (June 5,
1956).
[Illustration: PLATE 29]
FIG. 1. A small, nearly-healed, injury on the carapace of an
adult _T. o. ornata_ (A-- 2). Note regenerated epidermis at
bottom of depression and two pieces of dead bone ("splinter
scars") at upper right margin of depression.
FIG. 2. Injured area on the carapace of a juvenal _T. o. ornata_
(A-- 3) with dead bone removed and laid to the right, exposing
regenerating epidermis in its early stages.
FIG. 3. Anterior edge of carapace (held away with forceps) of
specimen of _T. carolina_ (KU 51461, Gulf Co., Florida) that
had been badly burned (A-- 8/9). Nearly all the scutes of the
shell had fallen off and large pieces of dead bone could be
pulled away, exposing a gnarled mass of regenerating bone and
epidermis.
FIG. 4. A fracture that has healed and joined the tibia (upper bone)
to the fibula in a specimen of _T. o. ornata_ (KU 1877, A-- 3A1/2).
[Illustration: PLATE 30]
_Top_: A shell of _T. o. ornata_ (A-- A1/2) as it was found at the
Damm Farm June 1, 1956. A serious injury (probably resulting
from burns) had exposed a large area of dead bone on the
carapace.
_Center_: Same shell with some of scutes removed.
_Bottom_: Same shell with dead bone removed to expose
regenerating epidermis and bone. Note that the injury involved
several of the neural bones; the turtle probably died as a
result of this injury but not before regeneration was
approximately one-half completed.
_Terrapene ornata_ seems to concentrate its breeding season (laying,
incubation, and hatching of eggs) more nearly in the middle of the
warm season than does _T. c. carolina_. This concentration probably is
an adaptation for breeding in open habitats where, under environmental
temperatures less equable than in forest, eggs would develop more
rapidly and hatch sooner but would be less able to survive winter
temperatures.
Males of _T. o. ornata_ become sexually mature when younger and
smaller than females and rarely grow as large as females. Nichols
(1939a:20) indicated the reverse to be true of _T. c. carolina_;
Nichols further indicated that growth continued some six to eight
years after puberty. Most individuals of _T. o. ornata_ attain maximum
size within two to three years after puberty.
Although it is difficult to be certain about the adaptive value of
color and pattern, it seems that in box turtles, as in many other
kinds of animals, patterns and colors most nearly blending with those
of the habitat have some selective value in providing concealment from
enemies. The pattern of linear radiations in _T. o. ornata_ closely
resembles the patterns formed by light passing through grasses and
associated vegetation and camouflages the turtle. In a similar manner,
partial or complete loss of radial markings in _T. o. luteola_ seems
to provide concealment in habitats where vegetation is sparse and
where blending with the substrate is of survival value. The patterns
of blotches and broken radiations in most of the subspecies of _T.
carolina_ likewise provide camouflage by tending to match patterns
formed by the light passing through a leafy canopy.
Although ornate box turtles are omnivorous, they probably depend on
insects as a dietary staple. In years when preferred kinds of insects
were unusually abundant, the turtles grew more than in other years. A
large proportion of the insects eaten is obtained by foraging in or
near dung. Alteration of the dung community--at least in a physical
sense, but presumably also by influencing the successional stages of
the dung biota--is one of the few evident effects of box turtles on
the environment. Although certain kinosternids (Carr, 1952:93), emyids
(Deraniyagala, 1939:257; Loveridge and Williams, 1957:198), and
testudinids (Loveridge and Williams, _op. cit._:247) eat mammalian
feces, _T. ornata_ is seemingly the only chelonian that habitually
seeks its staple diet in dung. The habit seems to be yet another
specialization for terrestrial existence. The carnivorous habits of
_T. ornata_ reverse the general trend toward omnivorous and
herbivorous habits in other turtles that have become partly (emyids)
or wholly (testudinids) terrestrial.
It seems remarkable that none of the species of true tortoises
occurring in the grasslands of the world has developed insectivorous
habits or utilized the unique food niche (in regard to dung-foraging)
filled by ornate box turtles in the Great Plains; tortoises are, as
far as is known, strictly herbivorous. The ranges of _Gopherus_ and
_Terrapene_ are now almost mutually exclusive and the two kinds do not
compete with each other for food in the few places where they occur
together. It is known, however, that box turtles (_T. longinsulae_,
_ornata_-like, earliest known box turtle) and true tortoises (genera
_Testudo_ and _Gopherus_, see Williams, 1950:25-26, Fig. 2) occurred
together in what is now the Great Plains in early Pliocene times and
probably for some time before and after this. Assuming that food
habits of fossil representatives of these genera were somewhat like
the habits of recent representatives, ornate box turtles may have
developed insectivorous habits at a time when other food niches were
filled by herbivorous tortoises. Box turtles possibly survived
subsequent changes in habitat that made it impossible for populations
of large tortoises to exist in the Great Plains.