International
Journal of Zoology and Applied Biosciences |
ISSN: 2455-9571 |
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Volume 3, Issue 3, pp: xxx-xxx, 2018 |
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Research Article |
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OCCURRENCE OF
OVIDUCAL GLANDS IN TWO TROPICAL MARINE CALANOID COPEPODS PSEUDODIAPTOMUS ANNANDALEI
AND PSEUDODIAPTOMUS SERRICAUDATUS – A NEW REPORT K. Altaff* Department of Marine Biotechnology, AMET University, Chennai-603112, Tamil Nadu, India |
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Article History: Received 04th
May 2018; Accepted 16th May 2018; Published ……. May 2018 |
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The
female reproductive system of the calanoid copepod species shows species
specific variation in organization. Occurrence of oviducal gland in Pseudodiaptomus annandalei and Pseudodiaptomus serricaudatus is reported for the first time in
present study. In the case of P. annandalei, and P. serricaudatus
fertilized eggs undergo embryonic development in an ovisac. In both the
species secretory activity of the oviducal gland synchronizes with the
vitellogenesis and maturation of oocytes, which take place in the
oviduct. The release of secretory
materials from the oviducal gland precedes the release of mature oocytes from
the oviduct, and forms the membranous ovisacs in
which fertilized eggs are deposited.
The oviducal glands of P. annandalei and P. serricaudatus show
resemblance with the oviducal glands of freshwater diaptomids,
Heliodiaptomus viduus
and Sinodiaptomus
(Rhinediaptomus) indicus which suggests a closer phylogenic affinity of
the Pseudiaptomus genus with freshwater diaptomids.
The role of oviducal gland in the female reproductive system of calanoid
copepods is discussed. |
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INTRODUCTION
Copepods
are sexually reproducing animals and sexes are separate. The gonads located in
the cephalosome are typically median in position and unpaired
in free living forms. In females the oviducts arise from the anterior portion
of the ovary and extend back along the side of the body to the genital somite.
The ducts open into a genital antrum. The antra are paired invaginations of the genital sternite that meet at the midline to form a transverse bilobed structure. Seminal receptacles also open into the antra. A variety of glands of unknown functions open into
the antra (Boxshall, 1982). The ovary usually contains previtellogenic oocytes and vitellogenesis takes place when the oocytes are in the
oviducts and diverticulae of oviducts. There are
variations pertaining to the fecundity of copepods which is mostly related to
the reproductive status of the female, food availability and environmental
parameters.
Copepods
constitute important primary consumer in all types of aquatic ecosystems and
play vital role in the energy transfer from primary producers to secondary
consumers. Though many reports are available on the taxonomy and distribution
of planktonic copepods (Kasturirangan, 1963), only few reports available on
their biology and reproduction. Important contributors on female reproductive
system are by Lowe (1935), Fahrenbach (1962), Park (1965), Razouls et al.
(1987), Dharani (1998), Sujatha (2000), Altaff (2003), Zehra (2000), and Gopikrishna (2004). The calanoid copepods have
adopted two different spawning methods of gravid eggs, in the first type fertilized
eggs are freely released in to the medium while in the second type fertilized
eggs are deposited in the egg sac, which is attached to the genital pore until
the nauplii hatch. The adoption of ovisac formation in some of the calanoid
copepods has led to modify the distal region of the oviduct of the females in the
oviducal gland.Occurrence
of oviducal glands was reported in freshwater calanoid copepods, Hemidiaptomus
ingens provinciae and Mixodiaptomus kupelwieseri
(Cuoc et al.,
1989), Heliodiaptomus viduus (Altaff & Chandran, 1994) and Sinodiaptomus
(Rhinediaptomus) indicus (Dharani, 1998).
In this paper occurrence of oviducal glands in two marine species, Pseudodiaptomus annandalei and Pseudodiaptomus serricaudatus and
their role in the formation of egg sac is reported for the first time.
MATERIALS
AND METHODS
Zooplankton
were collected offshore of the Muttukadu and Ennore station. (About 5 nautical miles) using a motor
driven dingy boat. Zooplankton were collected by towing a Bongo net (0.5m
diameter mouth, 2.5m mesh cloth, made of bolting silk 50µm mesh size, which is
fixed with 25cm bottom cup) for nearly half an hour for each sample during
early hours of the day. The samples were fixed using 5% buffered seawater
formalin. Zooplankton was sorted using different mesh sized filter cloth and
different groups of copepods were separated. P. annandalei and P. serricaudatus were identified to species level following
the taxonomic descriptions by Kasturirangan (1963), Huys & Boxshall (1991), Mazzocchi et al. (1995), Toda et al.(1994), Sewell (1999), Conway et al. (2003).
To view the reproductive system in situ,
the method of (Pantin, 1964) was followed.
The mature females of P. annandalei and P. serricaudatus were fixed in 70% ethanol,
transferred to Borax–carmine and stained for 24 hours. The specimens were differentiated
in acid alcohol till outer layer appear transparent and inner structures
pinkish. Then the specimens were dehydrated in 90% ethanol, passed to absolute
ethanol, cleared in xylene and mounted in DPX. To ascertain the correct shape
of the reproductive organs, the borax carmine stained, acid alcohol
differentiated specimens were dissected in a glycerol ethanol mixture under
stereo dissection microscope and then observed under compound microscope. The
different parts of the reproductive system were described following the
terminology by Hopkins (1977) and Dussart & Defaye (1995).
For histology, mature females of both
the species were fixed in aqueous Bouin’s fluid for
12 hours and were washed in tap water for 1 hr. They were dehydrated in 50%,
70%, 90% and absolute ethanol, cleared in xylene, embedded in paraffin wax and
serial sections (cross sections, longitudinal sections, vertical sections and
transverse sections) were taken. The sections were then de paraffinized
in xylene and hydrated in descending series of
ethanol and finally with distilled water, stained with haematoxalin, and counter staining was done with
70% alcoholic eosin and then passed
through 90% ethanol and absolute ethanol. After complete dehydration, xylene
was used for clearing the alcohol and then mounting was done in DPX (Pantin, 1964).
The reproductive system was observed under compound microscope and photomicrographed under different magnifications.
RESULTS
The female reproductive system of P.
annandalei consists of a median ovary a pair of oviducts antrum, seminal receptacle and reproductive pore. Ovary is
an elongate organ lying on the dorsal side of the anterior midgut.
It has a wider anterior end and a narrow as well as rounded posterior end. A
pair of oviducts originates from the anterior end of the ovary and takes a
posterior course and then proceeds laterally through the perivisceral
cavity towards the end of the prosome. The oviducts
enlarge terminally to give rise to oviducal gland which extends into the
genital segment and opens into the antrum (Figure 1).
The antrum in turn opens to the exterior through
female reproductive pore. A pair of spherical seminal receptacle occurs in the
genital segment. In this species fertilized eggs are held in the ovisac where
embryonic development up to naupliar stage takes place. The ovisac of this
animal contains 23 ± 3 eggs. The female reproductive system of
P. serricaudatus also consists of a single
median ovary. A pair of genital ducts which opens through
the lateral sides of the digestive tract to open to the exterior through a
common gonopore on the ventral side of the first urosomal somite (Figure 2).
However, species specific difference is observed in the shape of the ovary and
oviducal glands. The ovary P. annandaleiI is oval in shape while that of P.
serricaudatus has broader center and tapering anterior and posterior
ends. The oviducal glands of P. annandalei show higher elongation than
those of P. serricaudatus.
Occurrence of oviducal glands in marine calanoid copepod is reported for the
first time.
Histology of the posterior region of the
oviduct shows distinct difference with regard to the thickness of its wall and
glandular epithelium. During the process of maturation of oocytes in the
oviducts, the wall of the oviducal gland becomes highly glandular and produces large
quantity of secretory material which is stored in the oval shaped lumen. The
wall of the oviduct is haematoxalin positive whereas
the secretary material in the lumen of the oviduct appears eosin positive. The
lumen leads into a narrow tube which enters into the genital duct and opens
into the antra. The wall of the oviducal gland as it
proceeds towards the posterior end of the prosome
becomes thin and non glandular (Figure 3-5). It is interesting to note that the
secretory activity of the oviducal gland synchronizes with the vitellogenesis
and maturation of oocytes in the oviduct.
In the case of P. serricaudatus also the wall of the oviducal
glands is thicker and glandular than the wall of the oviduct (Figure 6 - 8).
While oocytes undergo vitellogenesis to become gravid, the oviducal glands
produce secretory material and stores in their lumens. When the mature oocytes are released
from the oviduct,
release of secretory materials from the oviducal
gland precedes and forms the membranous ovisac. The fertilized
eggs
are deposited in the ovisac and undergo embryonic
development to become
nauplii.
DISCUSSION
With regard to the reproductive
system, female of calonoid species have a single
median ovary located dorsal to the gut in the posterior part of the cephalosome and first metasomal
somite. Paired oviducts originate from anterolateral part of the ovary and
extend forwards, as diverticula, in to the cephalosome
and backwards on either side of the gut to the urosome.
The oviducts open into a single chamber, the genital antrum.
The genital antrum has paired dorsolaterally
directed pouches, the seminal receptacles in which spermatozoa are stored. The
organization of the female reproductive system shows generalized pattern in
most of the calanoid species (Park, 1965; Corkett & McLaren, 1979; Blades et al., 1984; Razouls et al., 1987; Marshall
& Orr, 2013). Such an
organization of female reproductive system is also observed in both the calanoid
copepod species presently studied. However, variation is observed with regard
to the size and shape of the ovary, the diverticula of the oviduct, and
modification of the posterior region of the oviduct in to a distinct oviducal gland,
structure of the antrum and structure of the seminal
receptacles in different species.
It is
interesting to note that the posterior region of the oviduct occupying the
distal region of prosome is modified into oviducal
gland in P. annandalei and P. serricaudatus. This gland is quite
conspicuous and distended compared to other regions. The proximal spherical
shape and narrow distal region even though common for both P.
annandalei and P. serricaudatus, specific variation is observed with
regard to the shape of the gland in these species. Such an oviducal gland is
not being described in any other marine calanoids copepod. Nevertheless,
occurrence of such an oviducal gland is reported in some of the freshwater
calanoids copepods. In the case of H. ingens provinciae and M. kupelwieseri
(Cuoc et al., 1989) described
ultrastructure of the posterior region of the oviduct which is highly glandular
in nature. Occurrence of well- developed oviducal gland with an elastic sac in
it was reported for the first time in the planktonic
freshwater diaptomids, H. viduus by Altaff & Chandran (1994). Subsequently,
occurrence of such a gland is also reported in another freshwater diaptomids, S. (R.) indicus by Dharani (1998). The oviducal glands of P. annandalei and
P. serricaudatus show resemblance with the oviducal glands of freshwater
diaptomids. This suggest that a closer phylogenic
affinity of the Pseudiaptomus genus with freshwater diaptomids.
Eggs of copepods are either carried by
the female attached in a mass to the genital opening or laid freely in the
water column. It seems that some of the calanoid copepods produce eggs without
any adhesive material which are broadcasted to the medium individually. There
is difference of opinion regarding the nature of egg sac in different egg brooding
calanoid copepods. In egg carrying Eurytemora velox, Huys & Boxshall (1991) reported that
while spawning the secretions of the outer membrane of eggs glued them in to
the egg mass and the same is attached to the genital segment. Further, they
observed that the egg mass is often called an egg sac, but in calanoids there
is no evidence that the eggs are contained in a membrane. Based on the studies
on the eggs carried by species such as Euchaeta
and Paraeuchaeta (Mauchline, 1998) also reported
that the egg mass is often referred to as an egg sac but there is little
evidence that the eggs are carried in a bag.
Contrary to these observations, (Kosobokova et al., 2007) provided clear
evidence of the presence of enclosing egg sac membranes in the Euchaetidae, Augaptilidae and
several Aetideidae. These observations are in
accordance with the observations by Corkett & McLaren (1969) and Hopkins & Machin (1977) on the presence
of an outer egg sac membrane surrounding the egg masses in Paraeuchaeta norvegica. The studies (Altaff & Chandran, 1994) on freshwater calanoid H. viduus and (Dharani, 1998) on S. (R.) indicus, clearly indicated occurrence of specialized
oviducal glands in the distal part of the oviduct and their role in producing a membranous egg sac. These thick walled and multicellular glands
form an elastic sac within itself filled with secretary material (Altaff & Chandran, 1994). When the oviduct
contained previtellogenic oocytes
the elastic sac was found attached throughout the inner wall of the oviducal
glands. When the oocytes became fully developed, the elastic sac detaches from
the wall of the oviduct and released into the distal part of the oviduct in the
genital segment. After fertilization of the eggs the elastic sac transformed
into an ovisac, in which eggs were enclosed. Histochemical
tests indicated the direct involvement of the elastic sac secretion in the
formation of the ovisac (Altaff & Chandran, 1994). Such a
function could be attributed to oviducal glands of both P. annandalei
and P. serricaudatus.
CONCLUSION
The
female reproductive system of the calanoid species shows species specific
variation in organization of the different regions. Occurrence of oviducal
gland in P. annandalei and P. serricaudatus is reported for the
first time in present study. The secretary activity of the oviducal gland
synchronizes with the vitellogenesis and maturation of oocytes in the oviduct
which enables embryonic development of fertilized eggs in the ovisac. This
brooding strategy of P. annandalei, P. serricaudatus ensures higher survival of the nauplii
compared to the species which broadcast eggs directly to the medium. The
structural and functional resemblances of oviducal glands of P. annandalei,
P. serricaudatus with those of
freshwater diaptomids, H. viduus and S. (R.)
indicus suggest close phylogenic
affinity between them.
ACKNOWLEDGEMENT
This work is supported by
The Department of Ocean Development through a research project.
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