Int'l J. Mol. Zoo., 2013, Vol.3, No.8, 32-41
http://ijmz.sophiapublisher.com
Research Article
Open Access
Morphometric and Histoarchitectural Changes in the Ovary of Pteropus
giganteus (Brunnich) During Various Phases of Reproductive Cycle
A.V. Dorlikar1 , A.A. Dhamani2 , P.N. Charde1 , A.S. Mohite1
1. P.G. Department of Zoology and Research Academy, Sevadal College for Women, Nagpur-440009, India
2. P.G. Department of Zoology and Research Academy, N.H.College, Bramhapuri- 441206, India
Corresponding authors email: [email protected]
Int'l J. Mol. Zoo., 2013, Vol.3, No.8 doi: 10.5376/ijmz.2013.03.0008
Received: 14 Sep., 2013
Accepted: 17 Oct., 2013
Published: 23 Oct., 2013
Copyright: © 2013, Dorlikar. This is an open access article published under the terms of the Creative Commons Attribution License, which permits unrestricted use,
distribution, and reproduction in any medium, provided the original work is properly cited.
Preferred citation for this article:
Dorlikar et al., 2013, Morphometric and Histoarchitectural Changes in the Ovary of Pteropus giganteus (Brunnich) During Various Phases of Reproductive
Cycle, Int'l J. Mol. Zoo., Vol.3, No.8, 32-41 (doi:10.5376/ijmz. 2013. 03.0008)
Abstract The present study was undertaken to know the morphometrical and histological changes in ovary during various
reproductive phases in Pteropus giganteus giganteus. The ovaries were fixed in alcoholic Bouin’s fixative for histological
examination. Diameter, surface area and volume of each ovary were calculated. Morphometric study of both the ovaries revealed that,
there is no significant morphostructural difference between the left and right ovary during all stages of reproductive cycle except
pregnancy. The result indicates significant changes in (P≤ 0.01) in ovarian diameter, surface area and volume during oestrous and
early pregnancy. However non significant changes have been reported during other stages of reproductive cycle. The significant
increase in (P≤ 0.01) diameter, surface area and volume of corpus luteum has also been observed during early pregnancy to mid
pregnancy. Thus the findings of this study provide baseline data for the ovarian morphometric analysis of chiroptera.
Keywords Pteropus giganteus giganteus; Morphometric analysis; Chiroptera; Ovary
leave their roost for foraging at dusk and continue
feeding until prior to the dawn that is showing the
nocturnal habit, so most active during the night hours
(Kunz and Diaz, 1995). Out of 18 families of living
bats (Hill and Smith, 1988) eight families had been
reported in India. The megabats feed mainly on fruit,
flowers, nectar and pollen. Thus megabats play a
major role in pollination and seed dispersal (Walker
and Molur, 2003; Stephenraj et al., 2010; Ul-Hassan et
al., 2010). These bats are vital to the survival of
rainforests and play crucial role in rejuvenation of the
entire ecosystem (Cox et al., 1992). Thus, the
Angiosperm's biodiversity of forest can be directly
correlated with the population of bats. Due to such
ecological and environmental requirement of this
megabat, management and conservation needs a special
attention. Unfortunately little is known regarding its
reproductive aspects, which may be needed for
management and conservation in future. Ovaries play
crucial role in reproductive physiology due to its role in
oogenesis and synthesis of steroid and peptide hormones.
Thus the aim of this work is to understand the
reproductive biology of Pteropus giganteus giganteus by
studying the histology and morphometrical changes in
ovary during various reproductive phases.
1 Introduction
Pteropus giganteus giganteus presents a seasonally
monoestrous and polygynous pattern of reproduction
(Marshall, 1947). The reproductive cycle of Pteropus
giganteus giganteus exhibits mainly the five stages in
their sex cycle. A period of sexual quiescence - from
July to August, Oestrus and Fertilisation-from last
week of August to first week of September,
Preganacy-from Mid September to late February or
first week of March, Parturation - During the first
week of March and Lactation - from first week of
March to July. This bat has gestation period of
140-150 days. The different strategies had been
developed for successful reproduction in many species
of bats. These were delayed ovulation in Plecotus
townsendii, delayed implantation in Fischer’s pygmy
fruit bat, Haplonycteris ficheri (Heidmann, 1989) and
sperm storage in Pipistrellus kuhlii (Sharifi et al.,
2004). Knowledge of reproductive asymmetry and
unilateral pregnancy in Chiroptera is due to Wimsatt
(1979). Megabats are strictly nocturnal; the only
exceptions had been reported were Samoan flying fox
(Pteropus samoensis) and the Trogen fruit bat
(Pteropus tonganus) which were active during day and
night (Utzurrum, 2002). Pteropus giganteus giganteus
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2 Material and Methods
2.3 Statistical analysis
Statistical analysis was performed to determine the
significant changes in ovarian diameter, surface area
and volume of the ovary during the different phases of
the reproductive cycle. Mean, Standard error, Standard
deviation, Variance and ANOVA with post-hoc Tukey
HSD test were calculated using Statistical Package for
Social Sciences (SPSS 10.0).
2.1 Collection of Specimens
Pteropus giganteus giganteus (Brunnich) is an Indian
megachiropteran bat of pteropidae family commonly
known as Indian flying fox. A colony of 50 to 500
individuals had been observed on the large tree of
Ficus bengalensis near the water reservoir at
Padmapur village. All the specimens used during
entire study period were obtained from natural
populations from feeding site at Padmapur village
near Armori. [Longitude 20°22' North and latitude
79°48' East (Dist-Chandrapur, Maharashtra)]. The
specimens were collected from December 2008 up to
December 2010 in such a way that entire reproductive
cycle was represented. Feeding sites were identified
by the examination of guano of the Pteropus
giganteus giganteus. Five specimens were collected
during each reproductive stage. Complete reproductive
cycle of Pteropus giganteus giganteus had been
studied and anoestrous, oestrous, early pregnancy, mid
pregnancy, parturation and lactation stages were
confirmed by the histological examination of uterus
and ovaries, morphological examination of mammary
glands and breeding behavior at roosting site.
3 Results
3.1 Ovarian morphometric analysis
Non-significant increase in diameter, surface area and
volume of both the ovaries has been observed during
lactation to anaoestrous and anaoestrous to
prooestrous (Table 1 and Table 2). However significant
increase in diameter, surface area and volume of both
the ovaries has been observed during prooestrous to
oestrous (Table 1 and Table 2). During pregnancy one
of the ovaries shows corpus luteum, indicating that
ovulation has been occurred in this ovary and another
undergoes regression. Thus out of six reproductive
asymmetry patterns reported in chiroptera,
Pteropus giganteus giganteus exhibited a pteropid
pattern
of
the
reproductive
asymmetry.
Non-significant increase in diameter, surface area and
volume has been observed in ovary from which
ovulation has been occurred during oestrous to early
pregnancy (Table 1). From early pregnancy to
mid-pregnancy, this ovary showed non significant
increase in diameter whereas significant (P<0.05)
increase in surface area and volume (Table 3). At the
termination of pregnancy and start of lactation
significant decrease in diameter, surface area and
volume has been reported in the ovary from which
ovulation has been occurred (Table1). However,
another ovary, referred as regressed ovary, showed
significant decrease in diameter, surface area and
volume from oestrous to early pregnancy (Table 2).
As the pregnancy proceeds, significant decrease in
diameter has been observed during mid-pregnancy
in regressed ovary. Non significant decrease in
surface area and volume has been noted in regressed
ovary from early pregnancy to mid pregnancy
(Table 3). At the termination of pregnancy and start
of lactation significant increase in diameter, surface
area and volume has been reported in the regressed
ovary (Table 2). Significant increase in diameter,
surface area and volume of corpus luteum has also
been reported during early pregnancy to mid
pregnancy (Table 3).
2.2 Morphometric analysis
Mature live animals were brought to the laboratory and
anesthetized with ether and killed by decapitation. The
ovaries were fixed in alcoholic Bouin’s fixative solution
and serially sectioned (thickness-5µm). Ovarian sections
were stained with hematoxylin-eosin (Humason, 1979).
Histological sections of right and left ovaries were used
to calculate the diameter of the ovary. The ovaries and
corpus luteum were assumed to be spherical. Ovarian
and corpus luteum diameter was measured (a) and the
diameter at right angles to this (b) (Wiliams, 1977). The
diameter (D) was calculated using the following
equation:
Diameter (D) (mm) =
ab
The mean diameter (D) for each ovary and corpus
luteum was calculated. This was then converted to an
ovarian and corpus luteum volume and surface area
using the following equations:
4
Volume of ovary/Corpus luteum (mm3) = 3
⎧⎪ D ⎫
π⎨ ⎬
⎪⎩ 2 ⎭
3
Surface area of ovary/Corpus luteum (mm2) = 4πr2
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Table 1 Comparison of diameter, surface area and volume of right ovary in Pteropus giganteus giganteus during different stages of
life cycle
Reproductive status
Diameter (mm)
Std.Dev.
Surface Area (mm2)
Anaoestrous
a
2.90±0.05
0.12
26.60±1.07
Prooestrous
3.07±0.05a
0.12
29.8±1.06a
Volume (mm3)
Std.Dev.
N
2.4
12.93±0.79
a
1.77
05
2.39
15.32±0.81a
1.82
05
b
b
a
Std.Dev.
b
0.16
69.75±2.19
4.90
54.86±2.56
5.73
05
Early pregnancy Ovary 4.84±0.04b
0.08
73.66±1.22b
2.73
59.48±1.48b
3.31
05
0.16
32.63±1.43ac
3.21
17.57±1.14ac
2.56
05
Oestrous
4.71±0.07
with corpus luteum
Lactation
3.22±0.07ac
Note: Mean ± S.E. Values with the same superscripts letters are not statistically significant different at (P < 0.01)
Table 2 Comparison of diameter, surface area and volume of left ovary in Pteropus giganteus giganteus during different stages of life cycle
Reproductive status Diameter (mm)
Anaoestrous
a
2.88±0.11
Prooestrous
3.10±0.07a
Surface Area (mm2)
Std.Dev.
N
4.72
12.85±1.50
3.36
05
3.42
15.74±1.18a
2.64
05
0.10
71.68±1.48
b
3.31
57.10±1.77
b
3.97
05
0.09
10.24±0.48c
1.08
3.08±0.21c
0.49
05
0.23
29.66±2.07a
4.63
15.30±1.61a
3.62
05
0.26
26.37±2.11
a
0.17
30.30±1.53a
Oestrous
4.77±0.04
b
Early pregnancy
1.80±0.04c
3.06±0.10a
Std.Dev.
Volume (mm3)
a
Std.Dev.
Regressed Ovary
Lactation
Note: Mean ± S.E. Values with the same superscripts letters are not statistically significant different at (P < 0.01)
3.2 Histological changes in ovary
3.2.1 Development of Graffian follicle
Development of graffian follicle starts from primordial
follicle. Primordial follicles were composed of an
immature oocyte surrounded by a single layer of
flattened granulosa cells (Figure 1).
Figure 2 Primary follicle, hematoxylin-eosin stain. (N-Nucleus;
O-Oocyte; PF-Primary follicle)
Figure 1 Primordial follicle, hematoxylin-eosin stain. (PRFPrimordial follicle)
Primary follicles consist of an oocyte surrounded by
one to two layers of cuboidal granulosa cells
(Figure 2 and Figure 3).
Primary follicles develop into secondary follicles
referred as small preantral follicle, which comprised
of two to four layers of granulosa cells (Figure 4).
Figure 3 Primary follicle, hematoxylin-eosin stain.
(GC-Granulosa cell; N-Nucleus; O-Oocyte; PF-Primary
follicle)
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antrum and separated by two or three layers of
cumulus cells. Ovum is attached to the granulosa cells
only at one site forming the cumulus oophorus. Cells
of carona radiata were in contact of follicular antrum.
Thecal layer was present towards the outer side of
basement membrane, which was composed of 3-4
layers of cells. Theca layer could be distinguished into
theca externa and theca interna (Figure 8).
Figure 4 Bilaminar Secondary follicle, hematoxylin-eosin stain.
(GC-Granulosa cell; SF-Secondary follicle; VM-Vitelline
Membrane)
Graffian follicles which possess more than two granulosa
layers, could be termed as multilaminar follicles.
In successive development small preantral follicle
becomes large preantral follicle that had four to six to
layers of cuboidal granulosa cells. In large preantral
follicles, ovum was surrounded by zona pellucida and
four to six layers of granulosa cells (Figure 5).
Figure 6 Vesicular follicle showing vesicular spaces, hematoxylineosin stain. (N-Nucleus; O-Oocyte; VF-Vesicular follicle;
VS-Vesicular space; VM-Vitelline Membrane)
Figure 5 Multilaminar follicle, hematoxylin-eosin stain.
(N-Nucleus; O-Oocyte; PAF-Preantral follicle; VM-Vitelline
Membrane; ZP-Zona pellucida)
Figure 7 Antral follicle showing antral cavity, hematoxylineosin stain. (FA-Follicular antrum; GC-Granulosa cell; O-Oocyte)
As follicle attains maturity oocyte appears to lie in
free antral cavity (Figure 9 and Figure 10).
Development of large preantral follicle results in the
formation of vesicular follicle (Figure 6). Vesicular
follicle comprised of vesicular spaces that appeared in
the closely packed cuboidal granulosa cells. Granulosa
cells start to congregate towards one side to form the
antral space and antrum start to develop in the follicle.
Thus graffian follicle was refered as antral follicle
(Figure 7). Antral follicle was characterized by the
development of follicular antrum and more than five
layers of cuboidal granulosa cells. Oocyte was
surrounded by thick zona pellucida. The oocyte was
pushed to one side of the follicle by developing
All graffian follicles do not attain the maturity. Some
of these follicles undergo the phenomenon of atresia.
Graffian follicles undergo process of atresia by
nuclear pyknosis and nuclear karyorrhexis (Figure 11
and Figure 12).
3.2.2 Histoarchitectural changes in the ovary
During anoestrous phase both ovaries showed peripheral
cortex having cluster of primordial follicles as well as
several follicles in the various stages of maturation;
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Figure 11 Multilaminar follicle showing atresia. The nuclear
pyknosis and nuclear karyorrhexis is clearly visible, hematoxylineosin stain. (NK-Nuclear karyorrhexis; NP-Nulear pyknosis)
Figure 8 Part of antral follicle showing cumulus oophorus. The
primary oocyte is attached to zona granulosa by cumulus
oophorus, hematoxylin-eosin stain. (CR-Carona radiata;
CO-Cumulus oophorus; FA-Follicular antrum; O-Oocyte;
VM-Vitelline Membrane; ZP-Zona pellucida)
Figure 12 Antral follicle showing atresia, hematoxylin-eosin
stain. (NP-Nuclear pyknosis)
Figure 9 Preovulatory Graafian follicle. The primary oocyte
floats freely within the follicular antrum, hematoxylin-eosin
stain. (CR-Carona radiata; FA-Follicular antrum; GC-Granulosa
cell; O-Oocyte; VM-Vitelline Menbrane; ZP-Zona pellucida)
Figure 13 Transverse section of ovary during anoestrous phase,
hematoxylin-eosin stain. (AF-Atretic follicle; PF-Primary
follicles; PRF-Primordial follicle; TA-Tunica albuginea;
ZP-Zona pellucida)
Figure 10 Preovulatory Graafian follicle. hematoxylin-eosin
stain. (CR-Carona radiata; FA-Follicular antrum; GC-Granulosa
cell; O-Oocyte)
During proestrous both the ovaries become active and
ovarian cortex showed numerous primordial follicles
as well as primary, secondary, vesicular and tertiary
follicle with developing follicular antrum (Figure 14).
Increased number of bilaminar and multilaminar
follicles were reported.
with primordial, primary, secondary, preantral and
antral follicles were observed in both the ovaries
(Figure 13). Few atretic follicles have been also reported.
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ovary (Figure 16, Figure 17 and Figure 18). During
early pregnancy corpus luteum appeared active and
secretory. The luteal cells were relatively large with
rounded nucleoli and abundant eosinophillic cytoplasm.
The entire gland appeared to be well supplied with
blood vessels (Figure 19 and Figure 20). By late
pregnancy the luteal cells appeared smaller with
smaller nucleoli and the corpus luteum becomes
infiltered with connective tissue and leucocytes.
Another ovary undergoes the regressed stage. In
regressed ovary the atretic follicles can be seen and
only primordial follicles can be observed after
conceiving the pregnancy and in later stages ovary
undergoes complete regression showing only cluster
of primordial follicles within the ovary (Figure 21).
Figure 14 Transverse section of ovary during proestrous phase,
hematoxylin-eosin stain. (FA-Follicular antrum; PF-Primary
follicles; PRF-Primordial follicle; SF-Secondary follicle
ATF-Antral graffian follicle)
During oestrous both the ovaries show similar pattern
(Figure 15). Abundance of all types of follicles in
various stages of development was observed.
Characteristically primordial follicles and primary
oocyte were congregated at periphery of the cortex
and intermingled with stromal cells. As the follicles
matured from primary to antral state, they appeared to
migrate from more cortical positions towards medulla.
Larger antral follicles lie close to the periphery of the
ovary. Very early antral and atretic follicles were
reported in both the ovaries.
Figure 16 Transverse section of ovary during early pregnancy
showing extrovert type of corpus luteum, hematoxylin-eosin
stain. (AF-Atretic follicle; CL-Corpus luteum)
Figure 15 Transverse section of ovary during oestrous phase,
hematoxylin-eosin stain. (AF-Atretic follicle; ATF-Antral follicle)
During pregnancy ovary showed presence few
bilaminar, multilaminar and other follicles in the stage
of atresia. Within the ovary from where ovulation
occurs showed presence of single extrovert type
corpus luteum which persists up to mid pregnancy and
then regresses. Significant increase in size of corpus
luteum occurs from early to mid pregnancy. At mid
pregnancy corpus luteum occupies 2/3rd portion of the
Figure 17 Transverse section of ovary of during mid pregnancy.
70% of the area of the ovary is occupied by the extrovert type
of corpus luteum, hematoxylin-eosin stain. (CL-Corpus luteum)
During lactation both the ovaries were similar in size.
Histologically ovarian cortex showed numerous
primordial follicles intermingled with stroma towards
periphery. Primordial, unilaminar, bilaminar and few
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Figure 21 Transverse section of regressed ovary during
pregnancy, hematoxylin-eosin stain. (PRF-Primordial follicle)
Figure 18 Extrovert Corpus luteum, hematoxylin-eosin stain.
(CL-Corpus luteum)
Figure 22 Transverse section of ovary during lactation,
hematoxylin-eosin stain. (PR-Primary follicle; PRF-Primordial
follicle)
Figure 19 Magnified portion of corpus luteum during early
pregnancy showing large and small luteal cells, hematoxylineosin stain. (BV-Blood vessel; LLC-Large luteal cell;
SLC-Small luteal cell)
giganteus exhibits mainly five stages of development
(Type 1 to type 5). Gopalkrishna et al. (1974) and
Krishna and Dominic (1980) had observed the
development of garffian follicles in bat Scotophilus
heathi. Lundy et al. (1999) had classified the ovine
graffian follicles on the basis of morphometric
characteristics. Comparing the results of the study of
development of graffian follicle, it can be concluded
that process of development of graffian follicle in
Pteropus giganteus giganteus has similarity with other
mammalian species. Histology of ovary had been
studied in various species of Indian bats viz.
Cynopterus sphinx, Rhinopoma kinneri, Megaderma
lyra lyra, Hipposideros bicolor (Gopalkrishna and
Moghe, 1960). Rasweiler (1988) had noted the
interstitial gland cells in the ovary of Molossus ater
which were concerned with the secretion of
progesterone. Reproductive asymmetry had been
described by Wimsatt (1979) and explained the
complete sinistral dominance of ovary in megaderma
pattern, contra lateral dominance in miniopterus
Figure 20 Magnified portion of corpus luteum during mid
pregnancy showing large and small luteal cells,
hematoxylin-eosin stain. (BV-Blood vessel; LLC-Large luteal
cell; SLC-Small luteal cell)
multilaminar follicles were observed in both the
ovaries but none of the ovaries showed antral or
mature follicle (Figure 22).
4 Discussion
Development of graffian follicle in Pteropus giganteus
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pattern, dextral dominance in molossid pattern, strong
tendancy for right and left ovaries to ovulate
alternately in successive cycle in phyllostomid pattern,
ovulation may occurs from either ovary with nearly
equal frequency in myotis pattern and non random
alternation of ovulations between right and left ovaries
in successive cycles in pteropid pattern. In Pteropus
giganteus giganteus neither ovary is dominant. Both
the ovaries contain a variety of follicular types and
ovulation can occur from any of these ovaries. Only
single ovary is functional during each pregnancy cycle
and other undergoes regression. Such pteropid pattern
has been observed in Pteropus giganteus giganteus.
Marshall (1947, 1949, 1953) in Pteropus giganteus,
Ramkrishna (1950) in Cynopterus sphinx, Gopalkrishna
(1964, 1969) and Gopalkrishna and Choudhary (1977)
in Rousettus leschenaulti, Gopalkrishna and Murthy
(1960) in Taphozous longimanus, Matthews (1941) in
Nycteris luteola and Nycteris hispida, Rasweiler (1972)
in Glossophaga soricina, de Bonilla and Rasweiler
(1974) in Carollia perspicillata, Quintero and
Rasweiler (1974) in Desmondus rotundus, Rasweiler
(1977) in Noctilio albiventris had reported alternation
of ovulation between ovaries in successive pregnancy
which is similar to that found in Pteropus giganteus
giganteus. After ovulation, the corpus luteum was
formed from the cellular components of the ovarian
follicle, the granulosa and theca cells (Rodgers et al.,
1983). The granulosa cells do not divide after
ovulation, but they increase in size and undergo
morphological changes (Auletta and Flint, 1988).
Corpus luteum consists of two types of luteal cells
small and large luteal cells. This finding is in
agreement with the findings of Christensen and Gillim
(1969) and Niswender et al. (1985). The large luteal
cells are derived from the granulosa cells while small
luteal cells are derived from thecal cells (Rodgers et
al., 1983). Gopalkrishna and Badwaik (1998) had
studied the growth of the corpus luteum in relation to
gestation in Rousettus leschenaulti, Rinopoma
microphyllum (kinneri), Megaderma lyra lyra,
Rhinoplophus rouxi, Hipposideros fulvus fulvus,
Hipposideros speoris and Pipistrellus ceylonicus
chrysothrix and reported the intraovarian corpus
luteum in which corpus luteum remains within ovary
and progressively enlarges in R. leschenaulti and
Pipistrellus ceylonicus chrysothrix, pedunculated
corpus luteum in Rhinoplophus rouxi and extrovert
corpus luteum in Megaderma lyra lyra, Hipposideros
fulvus fulvus and H. speoris. Heideman (1989) had
observed the corpus luteum in the Fischer’s pygmy
fruit bat Haplonycteris fischeri and revealed that
corpus luteum was always ipsilateral to reproductive
duct carrying the newly ovulated ovum conceptus.
Anand kumar (1965) in Rhinopoma kinneri,
Gopalkrishna and Bhatia (1983) in Hipposideros
speoris, Sapkal and Bhandarkar (1984) and Seraphim
(2002) in Hipposideros lankadiva had observed the
extrovert type of corpus luteum. Only single extrovert
type of corpus luteum has been observed in Pteropus
giganteus giganteus. Corpus luteum persists till mid
pregnancy and now placenta takes over the function of
production of progesterone to maintain successful
pregnancy thus corpus luteum gets regressed.
The results of morphometric study of ovaries presents
no morphostructural difference between the left and
right ovary. Rani and Devi (2011) in human, Flamini
et al. (2009) in viscacha, Belloa et al. (2012) in
African zebu cattle and Ofusori (2011) in African tree
pangolin have noted the morphometric changes in the
ovaries. Morphometric analysis does not reflect any
significant difference when the data were compared.
Hence both the ovary could be the principal sex organ
of reproduction in Pteropus giganteus giganteus.
Thus results demonstrate that the ovulation in the
left ovary and the right ovary is alternate and none
of the ovary showed dominance over other like in
other pteropid bats.
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Table 3 Comparison of ovarian diameter in Pteropus giganteus giganteus during pregnancy
Reproductive status and Ovary
type
Ovarian Diameter Std.
(mm)
Dev.
Diameter of Corpus Std.
luteum (mm)
Dev.
Surface Area of Std.
Ovary (mm2)
Dev.
Volume of
Ovary (mm3)
Std.
Dev.
Surface Area of Corpus Std.
luteum (mm2)
Dev.
Volume of Corpus Std.
luteum (mm3)
Dev.
N
Early pregnancy Ovary with
corpus luteum
Early pregnancy Regressed Ovary
Mid pregnancy Ovary with
corpus luteum
Mid pregnancy Regressed Ovary
4.84±0.04a
0.08
1.17±0.07a
0.16
73.66±1.22a
2.73
59.48±1.48a
3.31
4.38±0.53a
1.19
0.88±0.15a
0.35
05
1.80±0.04b
5.01±0.06a
0.09
0.13
None
2.57±0.07b
0.16
10.24±0.48b
78.89±1.95c
1.08
4.37
3.08±0.21b
65.95±2.46c
0.49
5.51
None
20.91±1.20b
2.69
None
9.03±0.78b
1.74
05
05
1.54±0.03c
0.06
None
-
7.45±0.30b
1.95
1.91±0.11b
2.46
None
-
None
-
05
41