ON THE FORMATION AND REGRESSION OF CORPUS
LUTEUM IN THE NORTHERN FUR SEAL OVARIESKAZUMOTO YOSHIDA, NORIHISA BABA
Far Seas Fisheries Research Laboratory, Shimizu

MACHIKO OYA AND KAZUHIRO MIZUE
Ocean Research Institute, University of Tokyo, Tokyo

ABSTRACT

Corpus luteum and the process of its formation in fur seal ovary, collectedaround the Robben Island in the Okhotsk Sea, were studied. The regressive
phases of follicle and courpus luteum were examined histologically. There are
two kinds of corpus luteum, one is formed inside the vesicular follicle after
ovulation, the other is formed outside the follicle without ovulation. The
former is the true corpus luteum and the latter is the accessory corpus luteum
or corpus atreticum. The function of corpus luteum graviditatis degenerates in
the last stage of pregnancy. Corpus albicans originated from the true corpus
luteum is distinguished from the corpus atreticum clearly. The former exists
for about two years in the ovary and then disappears, but the latter vanishes
shortly.

INTRODUCTION

There are many informations about the mammalian ovaries including human race.
Since the fur seal is a kind of marine mammal but goes ashore during some months
once a year for reproduction, its sexual cycle, age and growth were made clear byvarious authors. But microanatomical studies of the reproductive tracts are stillrather scanty. Craig (1964), Enders et al. (1946), and Pearson and Enders (1951)
report ovarian cycle for seals taken in the eastern Pacific and on the Pribilof Islands
respectively. However, there is no report on the microanalisis of reproductive organs on the Robben and Commander fur seals.
In the field observation of fur seals for the purpose of the stock assessment,
numbers of corpus luteum and corpus albicans are counted, but the disappearing
process of corpus luteum and corpus albicans can not be followed sufficiently by
this method and further the corpus albicans can not be identified from corpus atreticum by macroscopical observation. The disappearing processes of corpus luteum and corpus albicans were not treated sufficiently in the aforesaid reports.
We report in this paper on the corporal cycle in the fur seal ovaries taken in
the seas around Robben Island between July and October 1975.

Sci. Rep. Whales Res. Inst.,

No. 29, 1977, 121-128.

YOSHIDA, BABA, OYA AND MIZUE122

MATERIAL AND METHODThe Fur Seal Section of the Far Seas Fisheries Research Laboratory, JapaneseFisheries Agency, took fur seals in the seas around Robben Island in 1975 for the
purpose of stock assessment and their reproductive tracts were preserved in 10%
formalin after field biological investigation. We have sampled randomly 11 7 pairsof ovaries from these, which consisted of ovaries from 11 immature females, 11
ovulated females for the first time this year, 29 nonpregnant females but ovulated
in preceding breeding season, 23 ovulated females this year but non-ovulated inpreceding breeding season, and 43 pregnant females. These ovaries were weighed
their weight, then sliced to the thickness of about 2 mm, and measured the diameter of corpus luteum in three dimensions, counted the number of corpus albicans,and measured the diameter of the largest Graafian folicle. And then all ovaries
were further sliced into thin sections, embedded in paraffin, and these sections were
stained by compound stain method of Mayer's haematoxylin and eosin, and thenobserved. Age of these fur seals was determined by annual rings in the upper andlower cuspids.
OBSERVATION AND RESULT(1)

Regression offollicle

Section of the pup ovary of about three months after birth is indicated in Plate I-1
which contains many small follicles. Very few follicles among them develop tolarge size and finally ovulated, but many other follicles would be regressed, because it can be seen that there are many corpora atretica and follicles in process of degeneration and contraction. Plate I-2 shows ovary of 2 years of age, immature female, which contains many large follicles and this specimen was collectedin the middle of October. In this investigation mature females had no large follicle in the ovaries at this time of the season, owing to their functional corpus luteum, but in the ovaries of immature females, a number of comparatively large follicles are present, due to the fact that they have no functional corpus. Plate I-3
shows matured ovary of 14 years of age. A functional corpus Iuteum caused byovulation of this reproductive season exist in this section. Since this specimen wascollected towards the end of July, it is not clear whether this is corpus luteum graviditatis or corpus luteum of without gravidity. (Craig, 1964; Enders et al., 1946;
Pearson' and Enders, 1951). In addition there are corpus albicans and corpora
atretica resulted from Graafian follicles in this figure.
Enlarged follicle figure in the process of regression existed in pup ovary of
Plate I-1 is shown in Plate I-4. Oocyte is actualized in this figure but stratum
granulosum begins to degenerate, and in antrum folliculi, a sort of phagocyte
which is usefull for exhaustion are observed in abundance, and the basement membrane transformed to glassy membrane by distortion and increase of thickness.
The former term of vesicular follicle in the progress of development which is similar
to that of the other mammals is shown in Plate II-1. Contraction of the vesicularSci. Rep. Whales Res. Inst.,
No. 29, 1977.

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CORPUS LUTEUM OF FUR SEAL

follicle, the stratum granulosum degeneration in the first place, and then in oocyte
are shown in Plate II-2. In corpus atreticum distortion has occurred and thickened glassy membrane, and in Plate II-3, there are no oocyte and stratum granulosum. This corpus atreticum existed abundantly in ovary and it can be distinguished from corpus albicans resulted from corpus luteum distinctly and it seems
that these corpora atretica vanishes rapidly.
The figure of large vesicular follicle which contracted already is shown in
Plate II-4. The glassy membrane in this figure thicken increasingly than theformer, but it is the same in fundamental structure as corpus atreticum.

(2)

Corpus luteum and its degeneration
The aspect just ruptured to release an ovum from a ripened vesicular follicle
is shown in Plate III- I. In this figure, liquor folliculi and blood are still exist in
antrum folliculi, stratum granulosum along interna of theca folliculi increases the
thickness exceedingly and follicular epithelial cells formed stratum granulosum begin to expand and change to lutein cell in the enlarged figure. It is thought that
fur seal corpus luteum is originated mainly from the cells of stratum granulosumand not from theca interna of folliculi.
TABLE I. CORPUS LUTEUM DIAMETERS IN mm
AFTER OVULATION BY MONTHS

July
AugustSeptember
October

Vertical diameter

Lateral diameter

Height

8.0
10.0
11.3
14.0

7.4
8.7
10.4
12.7

8.5
9. 7

10.5
13.5

The corpus luteum resulted from an ovulation about two months before isshown in Plate III-2, a specimen from mid September. In the fur seal corpus
luteum is contained within the ovary like in many other mammals, though inwhales it is usually protruded from the ovary. Other corpus luteum constituted
around the outside of vesicular follicle, beside formal corpus luteum, is observed in
Plate III-2. Such corpus luteum is not rare in fur seal ovary, like in ovaries ofwhales (Harrison et al. 1972). It seems that the lutein cells of such corpus luteum
are originated from theca follicular cells and perform the same function as formal
one besides suppressing the development of its inside follicle. The lutein cells informal corpus luteum resulted from an ovulation of about three months before areenlarged in Plate IIl-3, a specimen from mid October. This figure shows the mostactive appearance of lutein cells and there are many secretions in the protoplasm ofthese cells and around them. The lutein cells in corpus luteum formed aroundvesicular follicle show the same histological appearance in this season too.
In Table I corpus luteum measurements in three dimensions are arranged in
the order from July to October. The corpus luteum which was formed in earlySci. Rep. Whales Res. Inst.,
No. 29, 1977.

124

YOSHIDA, BABA, OYA AND MIZUE

July by ovulation increases its size during the progress of month and increases its
function gradually, as shown in Table 1 clearly. And no difference in the size of
corpus luteum by ages, from three to twenty years, is noted.
After fur seals went ashore for reproduction and delivered a calf, the ovulation
is taken place within one week. Consequently it might be necessary that the regression of the lutein cells should begin towards the latter of the pregnancy. Craig(1964) describes that the corpus luteum graviditatis of the fur seal in the eastern
Pacific is functional until February and begins to degenerate after that. His description agrees with ours. The histological figure of corpus luteum graviditatisof pregnant animal prior to delivery caught on 10 July is indicated in Plate III-4.
In this figure lutein cells are almost degraded or fallen off and remains are small andnot in complete phase. It is distinct that the aspect of this corpus luteum graviditatis does not perform the secretion, unlikely from the lutein cells in Plate III-3,
and has the connective tissue penetrating into the structure of corpus luteum arborescently. As we have only specimens for four months, from July to October,we can not conclude definitly about the cycle of corpus luteum, but it is thoughtthat the same pattern of corporal cycle of Robben seal, as reported by Craig(1964), would be followed by the eastern Pacific stock of the fur seal.
Table 2 shows the process of regression of the corpus luteum graviditatis, indiameters in three dimensions, from just before delivery to after birth. In spite of
TABLE 2. THE AVERAGE DIAMETER OF CORPUS LUTEUM
IN mm BEFORE AND AFTER PARTURITION

Corpus luteum just before parturition
Corpus luteum after parturition(corpus albicans)

July
AugustSeptember
October

Verticaldiameter

LateraldiameterHeight

18.9
11.2
10.6
8.7
8.6

14.2
10.4
8.7
8.5
7.3

15.5
13.0
10.9
8.9
8.5

the unfunctional lutein cells, the size of this corpus luteum is larger than thatshown in Table 1, so it is concluded that the corpus luteum enlarges continuously
since ovulation. Fur seal fertilized ovum remains free in the lumen of uterine
horns and does not implant for about four months and placentation is establishedafter implantation (Craig, 1964; Enders et al., 1946; Pearson and Enders, 1951).
It seems possible that this phenomenon occurs not only in fur seal but also in all
Pinniped animals (Matthews and Harrison, 1949). The corpus luteum without
pregnancy, or in the case of unfertilization or unimplantation it does not contract
rapidly, unlikely to whales, because it has enough time for contraction until next
reproductive season and contractive process is thought to be same to that of corpus
luteum graviditatis. Pearson and Enders (1951) describes that the fur seal corpus
luteum which has not accompanied by a pregnancy follows even in the latter part ofMarch same phase of corpus luteum graviditatis and this is similar to our result.
The corpus albicans originated from corpus luteum without pregnancy in theSci. Rep. Whales Res. Inst.,
No. 29, 1977.

CORPUS LUTEUM OF FUR SEAL

125

preceding breeding season, and from an animal caught in 6 August, is shown in
Plate IV-2. The size and the stage of degeneration of this corpus albicans is sameto that of Plate IV-1. From Table 2, the corpus luteum graviditatis contracts
rapidly just after whelping, but the pace of contraction become slow after that.
The corpus albicans two months later from the parturition is indicated in Plate
IV-1, in which no lutein cell is observed naturally. And this is a typical corpus
albicans originated from the true corpus luteum and it shows quite different phase,compared with the accessory corpus luteum or corpus atreticum originated fromvesicular follicle. Laws (1958) discusses about the differences between the corpus
albicans resulted from corpus luteum graviditatis and that without pregnancy inwhales, but in the fur seal, there is no difference between both corpora albicantia
from the starting points of ovulations.

Corpus albicans and its degeneration
The corpus albicans disappears within a comparatively short span of time inmost mammals, but in whales the corpus albicans persists in the ovaries throughout
the life. This is thought to be based on the fact that their ovaries are large enoughfor admiting the persistence of all corpora albicantia, but in the fur seal, the ovary
is small and has no core in the center of corpus albicans, unlikely to whales. Accordingly, the disappearing period of corpus albicans is not short in the fur seal,
compared with other mammals. It does not remain, however, in the ovary
throughout the life.
A contracted figure of corpus albicans after one year since parturition is shownin Plate IV-3. Its surrounding parts are torn to pieces and has disappeared andbecame smaller. There are many ovaries in our specimens which have such a
corpus albicans, collected from animals one year after parturition, in which twenty
percent have vanished within one year, and this rate is higher in younger animals
than older. Plate IV-4 shows corpus albicans of an animal taken two years after
partunt10n. Such an old corpus albicans which existed such long time is very seldom in the fur seal. According to our investigations, it is concluded that in the
fur seal corpus albicans vanishes within three years after ovulation, though there
are some individual variations. That is different from the finding of Pearson andEnders (1951) who describe that it disappears before the next ovulation from thesame ovary, which means that the corpus albicans disappears within one year after
parturition.
(3)

REFERENCES
CRAIG, A. M., 1964. Histology ofreproduction and the estrus cycle in the female fur seal, Callorlzinus ursinus.
]our. Firh. Res. Bd. Canada, 21(4):773-811.
ENDERS, R. K., L. P. PEARSON and A. K. PEARSON, 1946. Certain aspects of reproduction in the fur seal.
Anal. Ree., 94 (2): 213-227.
HARRISON, R.J., R. L. BROWNELL Jr. and R. C. BOICE, 1972. Reproduction and gonadal appearances insome odontocetes. Functional Anatomy of Marine Mammals, 1 : 361-429.
LAws, R. M., 1958. Age determination of whales by means of the corpora albicantia. Proc. XVth lnt.
Sci. Rep. Whales Res. Inst.,

No. 29, 1977.

126

YOSHIDA, BABA, OYA AND MIZUECongr. :(',ool., Sect. III : 303-305.
MAITHEWS, L. H., and R.J. HARISON, 1949. Subsurface crypts, oogenesis, and the corpus luteum in theovaries of seals. Nature, 164: 587-588.
PEARSON, A. K., and R. K. ENDERS, 1951. Further observations on the reproduction of the Alaskan fur
seal. Anat. Ree., 111 (4) : 695-711.

Sci. Rep. Whales Res. Inst.,
No. 29, 1977.

CORPUS LUTEUM OF FUR SEALEXPLANATION OF PLATESPLATE I
Fig. 1. X 11.4, Histological section of fur seal pup ovary after three months frombirth. Caught 11 October, 1975.
Fig. 2. x5.7, Histological section of immature fur seal ovary, two years old.
Caught 13 October, 1975.
Fig. 3. x5.7, Histological section of mature fur seal ovary, 14 years old. Caught
31 July, 1975. It contains one functional corpus luteum resulted from this ovulation, one corpus albicans originated from corpus luteum and eight corpora
atretica originated from vesicular follicle.
Fig. 4. X 380, Histological figure of small follicle in the progress of degeneration.
The same ovary of Fig. 1.
PLATE II
Fig. I. X 380, Early stage of vesicular follicle in the process of development, three
years old. Caught 3 September, 1975.
Fig. 2. X 155, Degrading vesicular follicle, five years old. Caught 15 July, 1975.
There is no stratum granulosum already and oocyte is degenerating.
Fig. 3. X 155, Corpus atreticum originated from vesicular follicle, from the same
specimen shown in Fig. 2.
Fig. 4. x51, Corpus atreticum originated from large vesicular follicle, eighteen
years old. Caught 6 August, 1975.
PLATE III
Fig. 1. X 11.4, Ovulated follicle, four years old. Caught 29 July, 1975.
Fig. 2. x5.7, Mature ovary, nineteen years old. Caught 14 September, 1975. In
this section there are two kinds of corpus luteum, one is the formal by ovulation,
the other is formed around the outside of vesicular follicle.
Fig. 3. X 760, Functional lutein cells, fourteen years old. Caught 11 October, 1975.
Fig. 4. X 155, Histological figure of corpus luteum graviditatis just before delivery.
Fourteen years old. Caught 10 July, 1975. It is in the process of degeneration.
PLATE IV
Fig. I. x51, Corpus albicans after about two months from parturition. Seven
years old. Caught 13 September, 1975.
Fig. 2. X 51, Corpus albicans not accompanied by pregnancy passed about thirteenmonths after ovulation. Eighteen years old. Caught 6 August, 1975.
Fig. 3. x51, Corpus albicans originated from corpus luteum graviditatis of about
fourteen months after parturition. Six years old. Caught 28 September, 1975.
Fig. 4. x51, Corpus albicans of about two years after parturition. Fifteen years
old. Caught 3 July, 1975.

Sci. Rep. Whales Res. Inst.,
No. 29, 1977.

127

128

YOSHIDA, BABA, OYA AND MIZUEEXPLANATION OF SYMBOLS IN PLATES
AF
Antrum folliculi
BM Basement membrane
CA
Corpus albicans
CAT Corpus atreticum
CLF Corpus luteum formed around the follicle
CO Cumulus oophorus
FC
Functional corpus luteum
GM Glassy membrane
LC
Lutein cell
LF
Liquor folliculi
N
Nucleus0
OocyteP
Protoplasm
PH
Phagocyte
S
Secretion
SG
Stratum granulosum
TA
Tunica albuginea
TF
Theca folliculi
VF
Vesicular follicle
ZP
Zona pellucida

Sci. Rep. Whales Res. Inst.,
No. 29, 1977.

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