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Applying the systems approach to urban development
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Braz. J. Biol. vol.69 no.1 S?o Carlos fev. 2009
http://dx.doi.org/10.-00021
Histological
and histochemical analysis of the gonadal development of males and females of
Armases rubripes (Rathbun 1897) (Crustacea, Brachyura, Sesarmidae)
histol&gica e histoqu&mica do desenvolvimento gonadal de machos
e f&meas de Armases rubripes (Rathbun, 1897) (Crustacea, Brachyura,
Sesarmidae)
Santos, CM.I,
; Lima, GV.II; Nascimento, AA.I;
Sales, A.I; Oshiro, LMY.III
ILaborat&rio
de Histologia e Embriologia, Instituto de Veterin&ria, Universidade Federal
Rural do Rio de Janeiro - UFRRJ, Rod. BR 465, Km 07, CEP , Serop&dica,
RJ, Brazil
IIP&s-gradua&&o em Biologia Animal, Universidade
Federal Rural do Rio de Janeiro - UFRRJ, Serop&dica, RJ, Brazil
IIIEsta&&o de Biologia Marinha, Universidade Federal
Rural do Rio de Janeiro - UFRRJ, Rua Sereder, s/n, Itacuru&&,
CEP , Mangaratiba, RJ, Brazil
The objective of
this study was to provide information on the histological characteristics of
the gonads of male and female Armases rubripes crabs, and to try to establish
a relationship between the microscopic and macroscopic stages previously identified.
Thirty-six crabs were collected by hand between February 2003 and January 2004
in banks of Spartina alterniflora on Sahy Beach in Mangaratiba, Rio de
Janeiro state, Brazil. The histological analysis of the ovaries of A. rubripes
demonstrated a gradual process of development of the oocytes. According to their
cellular characteristics, five types of cells were distinguished: oogonia, oocyte
I, oocyte II, oocyte III and oocyte IV. The ovaries showed four stages during
gonadal activity: stage I (rudimentary), stage II (developing or maturing),
stage III (developed or mature) and stage IV (resting). The results of the histochemical
analyses showed that the ovaries vary according to the gonad development stage.
The histological aspect of one section of the male gonad was always the same
in all of the seminiferous tubules, where the lumen of these tubules always
contained spermatozoa and/or spermatids. It was not possible to characterize
the three stages of gonad development in the males. This agrees with previous
reports in the literature. However, in the females there was a relationship
between the gonad stages distinguished macroscopically and the results obtained
through the histological and histochemical analysis, due to the presence of
different cell types, as well as the lysis process and reabsorption of the oocytes
in spent females.
crab, gonadal development, histochemistry, Sesarmidae.
O objetivo deste
estudo foi fornecer informa&&es sobre as caracter&sticas
histol&gicas das g&nadas de machos e de f&meas de Armases
rubripes, tentando estabelecer uma rela&&o entre os est&gios
microsc&picos e os macrosc&picos anteriormente identificados.
Foram coletados manualmente 36 caranguejos, durante o per&odo de fevereiro
de 2003 a janeiro de 2004, em bancos de Spartina alterniflora na praia
do Sahy Mangaratiba, Estado do Rio de Janeiro. A an&lise histol&gica
dos ov&rios de A. rubripes demonstrou um processo gradual de desenvolvimento
dos o&citos. De acordo com sua caracter&stica celular, cinco tipos
de c&lulas foram distinguidos: ovog&nias, o&cito I, o&cito
II, o&cito III, o&cito IV. Os ov&rios revelaram quatro
est&gios de atividade gonadal: est&gio I (rudimentar), est&gio
II (em desenvolvimento ou em matura&&o), est&gio III (desenvolvido
ou maduro), est&gio IV (desovada). Os resultados das an&lises
histoqu&micas permitem afirmar que os ov&rios variam de acordo
com o est&gio de desenvolvimento gonadal. O aspecto histol&gico
de uma sess&o de g&nada masculina & sempre o mesmo em todos
os t&bulos semin&feros, onde o l&men deste t&bulo
sempre cont&m espermatoz&ides e/ou esperm&tides. N&o
foi poss&vel a caracteriza&&o de tr&s est&gios
de desenvolvimento gonadal em machos, conforme descrito previamente na literatura.
Entretanto, em f&meas, houve uma rela&&o entre os est&gios
gonadais distinguidos macroscopicamente e os resultados obtidos atrav&s
da an&lise histol&gica e histoqu&mica, devido &
presen&a de diferentes tipos celulares, assim como processo de lise e
reabsor&&o dos o&citos em f&meas desovadas.
Palavras-chave:
caranguejo, desenvolvimento gonadal, histoqu&mica, Sesarmidae.
1. Introduction
Armases rubripes
(Rathbun, 1897) is a small crab that is widely dispersed in varying environments.
It is usually found in the tropics and subtropics of Central and South America,
from Nicaragua to the River Plate (between Uruguay and Argentina) (Cap&toli
et al., 1977; Melo, 1996). In Brazil, it is commonly found in the South and
Southeast regions, inhabiting mangrove and restinga ecosystems, as well as the
axils of bromeliads and the lower portions of rivers (Fischer et al., 1997;
Teixeira and S&, 1998; Lima et al., 2006).
According to Hartnoll
(1974), the consecutive changes observed during gonadal development are important,
because besides enabling an estimate of physiological sexual maturity (Oshiro
et al., 1999; Silva and Oshiro, 2002a, Cobo and Fransozo, 2003), they permit
detailed visualization of the reproductive cells (Dumont and D'Incao, 2004).
Furthermore, these modifications are indispensable to characterize the reproductive
dynamics and to manage adaptations for the preservation and/or commercial exploitation
of the populations.
The reproductive
cycle of crustaceans has been widely studied, mainly of those species that have
commercial value or ecological potential (Reigada and Negreiro-Franzoso, 1999;
Pinheiro and Franzoso, 2002; Castiglioni and Negreiros-Fransozo, 2006). There
are several studies describing the morphological aspects of the gonads, such
as the morphological and histochemical aspects of the gonad of Macrobrachium
rosenbergii (Moraes, 1995); the histochemical aspects of the testis and
vas deferens of Goniopsis cruentata (Garcia and Silva, 2006); spermatogenesis
and formation of the spermatophore in the vas deferens of Chionoecetes opilio
(Sainte-Marie and Sainte-Marie, 1999); morphology and histology of the male
reproductive system of the mangrove land crab Ucides cordatus (Castilho
et al., 2007) and the stages of the reproductive cycle and anatomical changes
occurring in the spermatic cells (Bawab and El Sherief, 1988).
In A. rubripes,
Lima and Oshiro (2006) described some aspects of the reproductive biology and
characterized macroscopic aspects of the four stages of gonad development of
females (immature, intermediate, developed and resting) and three stages of
males (immature, intermediate and developed).
Because of the
scarcity of information on the morphological aspects of crab gonads, particularly
of the Sesarmidae family, the present work aims to contribute to the knowledge
of the histological and histochemical characteristics of the male and female
gonads of A. rubripes and to establish a relationship between the microscopic
and macroscopic stages previously described in the literature.
2. Material
and Methods
Thirty-six specimens
of A. rubripes were collected by hand (15 males, 15 females and 6 juveniles)
between February 2003 and January 2004, in Spartina alterniflora banks
on Sahy Beach, Mangaratiba, Rio de Janeiro State, Brazil (22& 56' S and
44& 01' W) (). After
capture, all of the specimens were stored in polystyrene boxes and taken to
the Marine Biology Laboratory at Rio de Janeiro Federal Rural University (UFRRJ),
where they were kept in aquariums under constant aeration. In the laboratory,
the animals were sexed and identified according to morphotype (Lima and Oshiro,
2006). All crabs were cold-anesthetized and killed at -20 &C during 15 minutes.
The gonads were quickly dissected and fixed in Bouin's solution for eight hours.
The tissues were dehydrated in increasing concentrations of ethanol, cleared
in xylol and soaked in paraffin in order to make 5 µm thick histological
cuts with a microtome. Later, each cut was stained using hematoxylin and eosin
(HE), Gomori Trichrome, periodic acid-Schiff (PAS) and Alcian blue (AB) pH 2.5,
following the protocol of Junqueira and Junqueira (1983).
The gonads were
analyzed through transversal and longitudinal sections. Photomicrographs were
taken using an Olympus® microscope (CH30) and a Nikon®
digital camera (Colpix 4300).
3. Results
3.1. Characterization
of the female gonad
The female reproductive
system is a bilaterally symmetrical, H-shaped structure in the antero-lateral
portion of the cephalothorax, composed of ovaries, which run to the posterior,
joined by a transversal commissure in the antero-lateral portion of the cephalothorax,
gonoducts () and a
specialized dilation of the gonoduct, known as the spermatheca.
The cells that
constitute the ovaries are of three main types: oogonia, oocytes in different
stages of development and follicle cells.
Oogonia are small,
oval or rounded cells with a spherical nucleus occupying almost the entire cell,
and the cytoplasm is intensely basophilic (). Oocytes come from developing oogonia and are classified into four distinct
cell types according to development, characterized by previtellogenesis and
vitellogenesis. These four types are:
Oocytes I (oI)
are characterized by having a basophilic cytoplasm and for being larger than
oogonia, round and for having a spherical nucleus. These cells are varied in
size and found in the proliferation zone ().
Oocytes II (oII)
are much larger than oocytes I, round or polygonal, have a strongly basophilic
cytoplasm, a large, oval nucleus, and peripheral nucleoli ().
Oocytes III (oIII)
are characterized by the presence of yolk vesicles in the cytoplasm and are
slightly acidophilous in routine preparations ().
Oocytes IV (oIV)
(vitellogenic) possess a varied shape (mostly polyhedral). The nucleus is difficult
to visualize because the cell is filled with vacuoles and granules of yolk characterized
by a strongly acidophilous mass ().
The follicle cells
are found around the oocytes and are responsible for supplying nutrients. They
have elongated nuclei that when compressed by vitellogenic oocytes acquire a
squamous aspect ().
Microscopic analysis
of the ovaries revealed four stages of gonadal activity: stage I (rudimentary),
stage II (developing or maturing), stage III (developed or mature) and stage
IV (resting).
3.1.1. Stage
I - Rudimentary
There is a central
proliferation zone where oogonia divide intensely, followed by oocytes that
are covered by follicle cells. Oocytes I (oI) occupy a more peripheral portion
of the gonad. These oocytes demonstrate a negative reaction to PAS and positive
to AB methods.
3.1.2. Stage
II - Developing or maturing
This stage can
be subdivided into two phases. The first is previtellogenesis and the second
vitellogenesis.
3.1.3. Phase
I - Previtellogenesis
There was a central
proliferation zone: oocytes I and II predominated, whose coloration was basophilic
using both the HE and Gomori T oocytes III (previtellogenic)
appeared, which is characteristic of this phase ().
3.1.4. Phase
II - Vitellogenesis
The oocytes could
be observed in intense vitellogenesis, with their granules very visible, and
a concentration of yolk in the cytoplasm. The nucleus of these oocytes lost
their rounded form, since the concentration of vitellus in the cytoplasm totally
or partially covered the nucleus. In this phase, a concentration of oocytes
II and III however, the oocytes in vitellogenesis (oIV) formed
the thickest zone of the parenchyma. The epithelium was reduced to one layer
of flat follicle cells around oocytes III and IV. The PAS method revealed an
intense coloration of oocytes IV located in the peripheral portion of the gonad,
indicating the presence of neutral glycosaminoglycans in this yolk. However,
the reaction was negative to PAS and positive to AB in the germinative zone
where the oocytes in initial development were found ().
3.1.5. Stage
III - Developed or mature
The germinative
zone appears in dispersed points of the gonad and is compressed by the mature
acidophilous oocytes (). There is no visualization of conjunctive tissue, and the ovarian capsule
is very thin and breaks open easily if compressed, releasing mature oocytes.
Oocytes II and III are found in small quantities, while oocytes IV occupy almost
the entire organ. With histochemical techniques, only neutral glycosaminoglycans
were evidenced in oocytes IV by the positive reaction to PAS.
3.1.6. Stage
IV - Resting
Microscopic examination
shows an ovary in the phase of total disorganization or reorganization. The
remaining oocytes, in different phases of maturation, are found in the process
of lysis and reabsorption (). The oogonia and basophilic oocytes reappear, representatives of the
proliferation zone formerly compressed by the mature oocytes from stage IV.
3.2. Characterization
of the male gonad
The inner part
of the male reproductive system of A. rubripes is bilaterally symmetrical,
located in the antero-lateral portion of the cephalothorax and consists of testes
connected by a testicular commissure (), vas deferens and ejaculatory ducts ().
Each testis is
formed by a whitish interwoven tubule located on the dorsal portion of the hepatopancreas,
extending anterodorsally on the cephalotorax.
The testes are
tubular organs, formed by lobules, where spermatogenesis takes place. They are
surrounded by a simple squamous epithelium that encloses each testicular lobule
(). These lobules
are formed by different germinative lineage cells, such as spermatogonia, spermatocytes,
spermatids and spermatozoa.
The formation of
spermatozoids starts in a peripheral region of the testicular lobule, called
the germinative zone, where the spermatogonias are located, while the cells
in a more advanced stage of development are found in groups called testicular
cysts (). In
the germinative zone, the reaction to the histochemical tests was negative,
but positive for the testicular cysts.
Microscopic analysis
revealed that the spermatogonias were cube-shaped, with indistinct cytoplasm,
an oval or elongated nucleus and were strongly stained by hematoxylin, giving
them a strong basophilic aspect.
The spermatocytes
have a relatively small, indistinct cytoplasm and a voluminous spherical or
slightly elongated nucleus that is larger than that of the spermatogonias. The
cytoplasm is small and acidophilous, increasing its extension according to the
cell development. These cells are very frequent in the germinative epithelium
and many are found in division.
On the wall of
the germinative epithelium and in the lumen of the cyst, the spermatids undergo
substantial morphological changes. These changes are more evident in the nucleus,
which is initially spherical and then becomes elliptical in the advanced phase.
The spermatozoids
are formed from the process of cell differentiation, which results in the appearance
of an acrosomal vesicle in the vicinity of the nucleus. The nucleus gradually
extends around the acrosomal vesicle and surrounds almost all of the vesicle
area when spermiogenesis is completed. At the end of this process there is a
cell whose nucleus is peripheral, with the acrossome located in the central
The vas deferens
consists of a tubule with various diameters that connects the posterior testicular
region to the ejaculatory duct in the posterior part of the abdomen. It is subdivided
in form and function into three different portions.
The first portion
of the vas deferens, known as the proximal vas deferens (PVD), is covered by
a simple cubic epithelium that becomes cylindrical in its most distal region.
Mature spermatozoids, without the presence of a spermatophore, are present in
the lumen of this tubule ().
The middle vas
deferens (MVD) originates in the posterior region of the pair of PVD, located
in the mediodorsal region of the cephalothorax. The tube is broader and can
be differentiated from the PVD by the presence of variable-sized eosiniphilic
granules in the vessel lumen (). The MVD is lined internally with a simple squamous epithelium and harbors
numerous ovoid spermatophores when immersed in a PAS-reactive substance, indicating
the presence of neutral glycosaminoglycans (). The distal portion of the vas deferens (DVD) originates in the final
portion of the MVD and is characterized by a large number of evaginations in
the duct walls.
The DVD is located
ventrally to the cephalothorax and is lined internally with a simple cubic epithelium.
The fluid secreted by this portion was viscous and translucent and reacted strongly
positive to staining with AB, showing the presence of sulfated and carboxylated
glycosaminoglycans (). The presence of spermatophores in its lumen is infrequent in relation
The histological
aspect of one section of the gonad was always the same in all of the seminiferous
tubules. The lumen of these tubules always contained spermatozoa and/or spermatids.
4. Discussion
Sexual maturity
in brachyurans has been determined in various ways, based on analyses of morphological
maturity, relative growth criteria and physiological and functional maturity
(Sampedro et al., 1999; Litulo, 2005).
In this study,
the histological analysis of the ovaries of A. rubripes demonstrated
a gradual process of development of the oocytes. According to their cellular
characteristics, five types of cells were distinguished: oogonia, oocyte I,
oocyte II, oocyte III and oocyte IV.
In Ucides cordatus
females, three stages of gonadal development were identified - developing, mature
or developed, and resting (Dalabona and Silva, 2005). However, most authors
divide microscopic gonadal development into five stages (immature, rudimentary,
incipient maturation, mature and resting) (Vogt et al., 1989; Medina et al.,
1996; Pal&cios et al., 1999).
The gonadal stages
of the Portunus pelagicus females were classified according to the morphological
characteristics of the carapace: soft-shelled females, in which two development
stages were recognized (virgin and copulated females); and hard-shelled females,
with six stages (copulated, ripe - late April, ovigerous - May, ripe - August,
ovigerous - September, non-breeding) (Bawab and El-Sherief, 1988).
In this work it
was possible to identify four histologically distinct gonadal development stages
in the ovaries of A. rubripes: I (rudimentary), II (developing or maturing),
III (developed or mature) and IV (resting). This classification has also been
observed for Macrobrachium acanthurus (Carvalho and Pereira, 1981).
The stage I (rudimentary)
ovaries of A. rubripes are characterized by the occurrence of a central
proliferation zone followed by oogonia and type I oocytes toward the periphery
of the gonad. This has also been observed for M. acanthurus (Carvalho
and Pereira, 1981). Dumont and D'Incao (2004) observed changes in the ovaries
from stage I (immature) to stage II (incipient maturation) regarding the increase
in cell size and cell weight and the start of the production of yolk.
The results here
indicate that stage II (developing or maturing) corresponded to the progression
of gametogenesis, presenting the characteristic aspect of growth and maturation
of the oocytes. In this stage, previtellogenesis and vitellogenesis are designated,
under macroscopic observation, as intermediary A and B, respectively by Lima
et al. (2006).
In the previtellogenesis
phase the basophilic cytoplasm evident in the oocytes II diminish gradually
as the vitellus accumulates in the cytoplasm, becoming acidophilous in the oocytes
in vitellogenesis. According to Raven (1961), this basophilic cytoplasm is especially
important for the increase of the protoplasm, but not for the formation of the
vitellus, justifying the change in staining affinity.
In the vitellogenic
phase of A. rubripes, oocytes are in intense vitellogenesis and there
is a large concentration of oocytes III and appearance of some oocytes IV. Carvalho
and Pereira (1981) divided this vitellogenic phase according to its macroscopic
characteristics into initial and advanced. The initial vitellogenic phase is
characterized by turgidity, distention in the length of the ovary and beginning
of the central proliferation zone with persistence of the germinative epithelium.
The advanced vitellogenic phase is characterized by large ovaries, covering
almost the entire stomach, with persistence of the germinative zone compressed
by oocytes in vitellogenesis.
In the penaeidae
Artemesia longinaris, stage II was considered incipient maturation based
on statistical analysis of the diameter of the oocytes. Females in this stage
were considered reproductive (Quintero and Gracia, 1998).
Stage III (developed
or mature) was characterized by the ovary being almost totally occupied by oocytes
in advanced-type IV vitellogenesis. These oocytes are large and rich in yolk.
The follicle cells, evident around the oocytes in the previtellogenic stage,
flatten, probably due to the tension exercised by the greatly distended oocytes
over them. This has also been observed in other decapods (King, 1948; Kessel,
1968). Raven (1961) and Beams and Kessel (1963) reported that the oocytes remove
the material, or part of it, from these cells to form the yolk.
Stage IV (resting)
is characterized by the total post-elimination of the oocytes. In this phase,
there is ovarian regeneration (with reabsorption), oocyte lysis and proliferation
of the cellular elements of the connective tissue. This was also reported in
Palaemon paucidens (Kamiguchi, 1971) and Artemesia longinaris
(Christiansen and Scelzo, 1971). This phase may be a source of error in the
macroscopic classification since it is similar to stage I, where the ovary is
also difficult to visualize. Microscopic analysis, however, eliminates the possibility
of error in these stages.
The results of
the histological and histochemical analyses here allowed affirming that the
ovaries vary according to gonadal development stage. The processes of sexual
maturation, in view of the observed modifications, allowed the establishment
of four development stages, thus enabling a correlation between the macroscopic
characteristics observed in the previous work carried out by Lima and Oshiro
(2006) and the microscopic characteristics observed in this work.
The reproductive
system of A. rubripes males consists of paired testes, vas deferens and
ejaculatory ducts and is similar to the reproductive system generally described
for other brachyurans (Krol et al., 1992; Lima, 1995; Garcia and Silva, 2006;
Castilho et al., 2007).
The testes are
formed by seminiferous tubules and, like most Decapoda, the spermatogonia are
located in the most peripheral portion of this tubule (Mota-Alves and Tom&,
1966; Nagao and Munehara, 2003).
The spermatids
and the spermatozoa are difficult to distinguish. The spermatozoa do not present
a spiny process, as has been reported for other brachyura (Nath, 1937; Pillai,
At the end of spermatogenesis,
the sexual cells are transported to the vas deferens, where the spermatic cells
are encapsulated, forming spermatophores (Hinsch and McKnight, 1988; Sainte-Marie
and Sainte-Marie, 1999).
In A. rubripes,
the vas deferens was divided into three distinct regions, as has been reported
in other crabs (Hinsch and Walker, 1974; Johnson, 1980). However, other studies
characterize two (Garcia and Silva, 2006), four (Hinsch and McKnight, 1988)
and eight (Manj&n-Cabeza and Evenness, 2000) regions. Different criteria
and different microscopic and macroscopic foci may account for this diversity
(Garcia and Silva, 2006).
Castilho et al.,
(2007) characterized the PVD by the presence of a cylindrical epithelium, spermatozoids
in the lumen and absence of spermatophores, a result also observed here.
The medial portion
of the vas deferens (MVD) is known for its secretory activity (Silva and Garcia,
2006). Binford (1913) and Cronin (1947) observed that a secretion of substances
that allows the coiling and storage of the spermatophore occurs in the PVD.
Hinsch and McKnight
(1988) also attributed the start of the formation of the spermatophore and the
production of the seminal fluid to this region. Sainte-Marie and Sainte-Marie
(1999) characterized two amorphous substances in C. opilio, suggesting
the existence of two different types of seminal fluids. These authors also suggested
that the complete development of the spermatozoon occurs only inside the spermatheca.
In A. rubripes,
we observed spermatohores immersed in a secretion positive to the PAS technique,
a result similar to that found in Ucides cordatus by Castilho et al.,
2007. This PAS-positive secretion can induce spermiogenesis when present in
large quantities (Sainte-Marie and Sainte-Marie, 1999).
The distal vas
deferens is characterized by the presence of invaginations in its wall. The
lumen was filled by a secretion positive to PAS and AB, indicating the presence
of neutral and acidic glycosaminoglycans, respectively.
The results of
the analysis showed that it was not possible to characterize the three gonadal
development stages in males, as described by Lima and Oshiro (2006), since there
is a constant process of gamete production, indicated by the presence of different
spermatogenic lineage cells in the same seminiferous tubules. However, it was
possible to establish a relationship between the gonad stages distinguished
macroscopically by Lima and Oshiro (2006) and our histological results, due
to the presence of different cell types along with the process of lysis and
reabsorption of the oocytes in resting females.
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Received August
Accepted December 3, 2007
Distributed February 28, 2009
Todo o conteúdo deste periódico, exceto onde está identificado, está licenciado sob uma