The following account of oAÂgenesis is based on examination of
preserved ovaries from 68 mature specimens. The ages of most specimens
were known, inasmuch as the specimens were used in studies of growth
as well as gametogenesis. Other data were obtained from adult females
that were dissected but not preserved, and from immature females.
[Illustration: FIG. 4. Seasonal fluctuations in ovarian weight
in _T. o. ornata_, as determined by examination of 60 specimens
from eastern Kansas.]
Size of ovarian follicles was determined by means of a clear plastic
gauge containing notches 5, 10, 15, 20, and 25 millimeters wide. The
number of follicles within a given size range could be quickly
determined by finding the smallest notch into which the follicles fit.
It was necessary to weigh all ovaries after preservation since some of
them had not been weighed when fresh. Since all ovarian samples were
preserved in the same manner, weights remained relatively the same.
Preserved material was lighter than fresh by an average of 13 per
cent. Follicles less than one millimeter in diameter were not counted.
Corpora lutea and corpora albicantia were studied under a binocular
dissecting microscope. No histological studies were made of the female
reproductive system.
Ovarian follicles and oviducal eggs were recorded separately for the
right and left sides. Each ovary was always kept associated with the
oviduct of the same side, but in some instances it was not recorded
whether the organs were left or right.
Ovaries ordinarily weighed most in October, March, and April, when
most females contained enlarged follicles, and least in August and
September when the supply of enlarged follicles was usually exhausted
(Figs. 4 and 5).
[Illustration: FIG. 5. The seasonal occurrence of enlarged
ovarian follicles in females of _T. o. ornata_, expressed,
For each month, as the percentage of total females that
contained two or more follicles having diameters greater than
15 mm. Total number of females in each of the samples is shown
in parentheses at the top of each bar.]
The ovarian cycle begins in July or August, after ovulation has
occurred. At that time many minute follicles form on the germinal
ridges of the ovaries. On the basis of the material that I examined,
it seems that ovarian follicles either grow to nearly mature size in
the season preceding ovulation and remain quiescent over winter or
grow rapidly in the period of approximately six weeks between spring
emergence and ovulation. Altland (1951:603-5) reported that the former
condition was the usual one in _T. carolina_; he suggested that
possibly some of the enlarged follicles were absorbed during
hibernation.
Examination of yolks of oviducal eggs revealed that follicles mature
when they reach a diameter of 16 to 20 millimeters and a weight of two
to two and one-half grams (Pl. 20, Fig. 1).
The enlarged follicles remaining on the ovaries after ovulation
(excluding those smaller than six mm.) can be grouped according to
diameter as: large (greater than 15 mm.), medium (11 to 15 mm.), and
small (six to 10 mm.). Ten females collected in the period from June 2
to 8, after they had ovulated, all had follicles falling in at least
one of these size groups, and eight had follicles falling in two or
more of the groups. In females having enlarged follicles of more than
one of the size groups, there were several follicles in each of two
groups and no follicles, or only one follicle, in the remaining group.
Enlarged follicles represent future clutches but whether the enlarged
follicles will be ovulated in the same season or in a later season is
questionable.
Evidence found in the present study suggested that at least a few
females lay more than one clutch of eggs per year. Among 34 specimens
obtained in June and July, eight (24 per cent) had corpora lutea (or
easily discernible corpora albicantia) and at least two follicles more
than 15 millimeters in diameter; in three specimens (9 per cent) the
ovaries bore fresh corpora lutea (representing recent ovulations) and
a set of older corpora lutea (representing ovulations that had
occurred several weeks previously). It was thought that each of these
eleven females (33 per cent of sample) had produced or would have
produced two clutches of eggs in the season of its capture. The number
of large follicles present after the first set of ovulations (mean,
3.5) was fewer in most instances than the average clutch-size (see
below), indicating that second clutches are smaller than first
clutches. Smaller second clutches were found also in _T. carolina_
(Legler, 1958).
Further evidence for multiple clutches was the absence of enlarged
ovarian follicles in some females obtained in September. Atretic
follicles, ordinarily orange, brown, or purplish, were observed on the
ovaries of many of the females examined; in most instances, not more
than two follicles of the small or medium size groups were atretic.
Atresia was in no instance great enough to account for the complete
loss of enlarged follicles.
Further study probably will show that many of the females laying in
May and early June lay again before the end of July, and that eggs in
the oviducts of females captured in the latter month frequently
represent second clutches. Under favorable conditions, eggs laid by
the end of July would have a good chance of hatching before the advent
of cold weather in autumn; turtles hatching too late to escape from
the nest could burrow into its sides and probably escape freezing
temperatures.
Cagle's findings concerning _Pseudemys scripta_ (1950:38) and
_Chrysemys picta_ (1954:228-9) suggest that these species lay more
than one clutch per season, at least in the southern parts of their
ranges. Carr (1952) indicated that multiple layings were known in most
species of marine turtles (families Dermochelydae and Chelonidae) and
strongly suspected in other species. Other turtles recorded to have
produced multiple clutches in a single season (based chiefly on
captive specimens or cultured populations) include: the starred
tortoise, _Geochelone elegans_ (Deraniyagala, 1939:287); the Asiatic
trionychid, _Lissemys punctata_ (_op. cit._:304); the diamond-backed
terrapin, _Malaclemys terrapin_ (Hildebrand and Prytherch, 1947:2);
and the Japanese soft-shelled turtle, _Trionyx japonicus_ (Mitsukuri,
1895, cited by Cagle, 1950:38).
There is a marked alternation of ovarian activity in _T. ornata_, one
ovary being more active than its partner in a given season. The less
active ovary is more active than its partner in the following season.
For example, a specimen killed in July had four corpora lutea on the
right ovary and two on the left and there were five enlarged follicles
(of the medium size group), representing the next set of eggs to be
ovulated, four on the left ovary and one on the right. Similar
alternation of ovarian activity was observed, to a greater or lesser
extent, in nearly all of the females examined. Many subadult females
that were approaching their first breeding season (as evidenced by the
presence of large ovarian follicles but no indication of former
ovulation) had but one active ovary. This may account in part for the
tendency of small, young females to lay clutches smaller than average.
One ovary may become senile in old females before its partner does;
this may explain the occasional absence or atrophy of one ovary in
large females that I have examined.
In all the specimens examined, it was evident that ovulation had
occurred or would occur in two successive seasons. Senile or young
females might, however, be expected to skip a laying season if only
one ovary was functioning.
After ovulation, the collapsed follicle assumes a cuplike shape and
becomes a glandular corpus luteum (Pl. 20, Fig. 2). Corpora lutea are
approximately eight millimeters in diameter and are easily discernible
at least until the eggs are laid; they are somewhat less distinct
after preservation. Corpora lutea undergo rapid involution following
oviposition and, after two to three weeks, are little more than small
puckerings on the ovarian epithelium. At this stage they are properly
referred to as corpora albicantia and are discernible only after
careful examination of the ovary under low magnification. Corpora
albicantia remain on the ovary until April of the year following
ovulation but disappear in May and are never present after the new set
of eggs is ovulated. Ovaries of some subadults (that would have laid
first in the season following capture) contained enlarged follicles
and, but for their lack of corpora lutea and corpora albicantia, were
indistinguishable from those of older, fully mature females.
Altland (1951:605-610) gave a histological description of the corpus
luteum of _Terrapene carolina_. Corpora lutea were glandular and
filled with lipoidal material until the eggs were laid. Atresia of
corpora lutea began when eggs were laid, was completed by mid-August,
and was coincident with atresia of large follicles that did not
undergo ovulation. Altland did not describe the gross external
appearance of the corpus albicans.
The corpus luteum of oviparous reptiles seems to be closely associated
with the intrauterine life of the eggs and, in viviparous reptiles, it
may be an important factor in maintaining optimum gestational
environment; however, its functions in all reptiles are poorly
understood (Miller, 1948:200-201).
Information gleaned from records of gravid females and known dates of
nesting suggests that eggs are retained in the oviducts two to three
weeks before laying. Once they are ovulated, the eggs are exposed to
but few hazards until laid; counts of corpora lutea are an accurate
indication of the number of eggs laid. In the gravid females examined
by me, number of corpora lutea on the ovaries was equal, in all but
one instance, to the number of oviducal eggs. In the single instance
in which an extra corpus luteum was found, one egg had probably been
laid before the specimen was captured. The high incidence of
correspondence between counts of corpora lutea and counts of oviducal
eggs indicates also that _T. ornata_ deposits the entire complement of
oviducal eggs at one time, not singly or in smaller groups.
Extrauterine migration of ova, whereby eggs from one ovary pass into
the oviduct of the opposite side, is of common occurrence in _T.
ornata_ and is known to occur also in _T. carolina_, _Chrysemys
picta_, _Emydoidea blandingi_, _Pseudemys scripta_, _Cnemidophorus
sexlineatus_, and in several mammals (Legler, 1958). This ovular
migration may serve to redistribute eggs to the oviducts when the
ovaries are functioning at unequal rates.
The eggs acquire shells soon after they enter the oviducts. No
shell-less eggs were found in oviducts but several specimens of _T.
ornata_ had oviducal eggs, the thin, parchmentlike shells of which
lacked the outer calceous layer; in these specimens the corpora lutea
were fresh, probably not more than two days old. Eggs that had
remained in the oviducts longer had a calceous layer on the outside of
the shell. Eggs having incompletely developed shells were successfully
incubated in the laboratory. Cagle (1950:38) found shelled but
yolkless eggs in the oviducts of several _Pseudemys scripta_ but found
no yolkless eggs in nests. No yolkless eggs were found in specimens of
_T. ornata_ in the course of the present study.
The uterine portion of the oviducts becomes darkened (pale gray to
intense black) in the breeding season. Darkening of oviducts seemed to
coincide with the period when eggs were in the oviducts and it
persisted for a variable length of time after the eggs were laid.
Oviducts of immature females were ordinarily pale.