JOURNAL OF CRUSTACEAN BIOLOGY, 29(4): 458-465, 2009
MORPHOLOGY OF TESTIS AND VAS DEFERENS IN THE XANTHOID CRAB, ERIPHIA VERRUCOSA
(FORSKÅL, 1775) (DECAPODA: BRACHYURA)
Melike Erkan, Yasemin Tunali, Hüsamettin Balkis, and Elsa Oliveria
(ME, correspondence, [email protected]; YT; HB) Department of Biology, Faculty of Sciences, Istanbul University, 34134,
Vezneciler, Istanbul, Turkey;
(EO) Laboratory of Cell Biology, Institute Biomedical Sciences Abel Salazar, University of Porto, Porto, Portugal
ABSTRACT
The anatomy of the male reproductive organs of the brachyuran crab Eriphia verrucosa is presented, with a detailed analysis of the
histology and histochemistry of the regional structure of the testis and vas deferens. The H-shaped testis is subdivided into three distinct
parts: anterior, intermediate and posterior. The vas deferens is continuous with the posterior part of the testis, ends at the gonopore, and is
subdivided into three distinct regions: proximal, medial and distal. The anterior part of the testis exhibits convoluted lobules including
seminiferous tubules. Whereas the intermediate part of the testis has a simple columnar epithelium, the posterior part of the testis has a
simple squamous epithelium. In the proximal and medial regions of the vas deferens, there is a simple cubic epithelium, while in the
distal region of the vas deferens there is a high columnar epithelium. Spermatophores are first formed in the convoluted proximal region
of the vas deferens and are encapsulated by mainly protein secretions in the distal region. These results suggest that the testis and vas
deferens of Eriphia show similarity to the testis and vas deferens of other brachyuran crabs except for some slight differences. During
formation of the spermatophores in the vas deferens the spermatozoa are prepared for successful fertilization.
KEY WORDS: Brachyura, crab, spermatophores, testis, vas deferens
DOI: 10.1651/08-3114.1
1995) and Diogenes pugilator (Roux, 1829) (Manjón-Cabeza
and Garcia Raso, 2000).
Spermatophore morphology has also been studied for a
number of decapod crustaceans, including the crab species
Carcinus maenas (Linnaeus, 1758) (Spalding, 1942),
Callinectes sapidus (Cronin, 1947; Johnson, 1980), Scylla
serrata (Forskål, 1775) (Uma and Subramoniam, 1979),
Chionoecetes opilio (Beninger et al., 1988) Portunus
pelagicus (Linnaeus, 1758) (El-Sherief, 1991) and Ucides
cordatus (Leite, 2002), the lobster species Panulirus
laevicauda (Lima, 1995), and the hermit crab species
Diogenes pugilator (Manjón-Cabeza and Garcia Raso,
2000), Micropagurus acantholepis (Stimpson, 1858)
(Tudge and Lemaitre, 2004), Loxopagurus loxochelis
(Moreira, 1901) (Scelzo et al., 2004), Coenobita perlatus
(Edwards, 1837), Coenobita clypeatus (Fabricius, 1787)
(Tudge and Lemaitre, 2006) and Calcinus laevimanus
(Randall, 1840) (Litulo et al., 2006).
The anatomy and histological structure of the male
reproductive tract of Eriphia verrucosa (Forskål, 1775), a
crab from the Black Sea with important commonly
preferable food supply and endangered (EFT, 2004) is
described here for the first time. Specific regional
histological and histochemical characteristics of the ducts
suggest that in this species the vas deferens also participates
in sperm maturation and spermatophore formation.
INTRODUCTION
The reproductive cycle of crustaceans is under hormonal
control, and it is also influenced by external factors such as
photoperiod, temperature, salinity and diet. Some crustaceans
breed only once in their lifetime (monocyclic), whereas
others breed several times a year (polycyclic) (Tomikawa and
Watanabe, 1992; Barnabé, 1994). The male reproductive
organs of most malacostracans, including decapods, are
found in the cephalothorax or thorax and in decapods; it is
composed of paired testes and genital ducts. Each genital duct
consists of a collecting tube, a vas deferens, and an
ejaculatory duct (Krol et al., 1992). When spermatogenesis
is complete, gametes are transported from the testis to the vas
deferens through the collecting tube (Hinsch and Walker,
1974). In the vas deferens spermatozoa then become
encapsulated to form spermatophores (Hinsch and Mcknight,
1988; Saint-Marie and Saint-Marie, 1999).
Only a few studies have described the histological
structure of the male reproductive tract in brachyuran crabs.
These examples include Callinectes sapidus (Rathbun, 1896)
(Cronin, 1947; Johnson, 1980), Portunus sanguinolentus
(Herbst, 1783) (Ryan, 1967), Libinia emarginata (Leach,
1815) (Hinsch and Walker, 1974), Chionoecetes opilio
Fabricius, 1788 (Beninger et al., 1988; Sainte-Marie and
Sainte-Marie, 1999; Benhalima and Moriyasu, 2000) and
Ucides cordatus (Linnaeus, 1763) (Leite, 2002). Testis and
vas deferens morphology have been described for several
other species of decapod crustaceans such as Panulirus argus
(Latreille, 1804) and Panulirus guttatus (Latreille, 1804)
(Talbot and Summers, 1978), Scyllarus chacei Holthuis, 1960
(Hinsch and Mcknight, 1988), Thenus orientalis (Lund, 1793)
(Burton, 1995), Panulirus laevicauda (Latrelli, 1817) (Lima,
MATERIALS AND METHODS
Twelve specimens of adult male Eriphia verrucosa (mean carapace length:
80 mm) were collected from 1 to 5 m depth in the Bay of Karaburun
(Black Sea) in Turkey. Once in the laboratory, the animals were killed by
cold treatment (5 min at 220uC). After lifting away the dorsal carapace,
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ERKAN ET AL.: TESTIS AND VAS DEFERENS OF ERIPHIA VERRUCOSA
the testes and vasa deferentia were dissected under a stereomicroscope and
fixed with Bouin’s solution for 12 h at 20uC and placed in 70% ethanol.
After dehydration through an ethanol series, cleared in xylene, and finally
embedded in paraffin. The sections were cut at 5 mm thickness, placed
onto microscope slides and stained with hematoxylin-eosin and Masson’s
Trichrome stain for histological observation under light microscopy and
with Alcian Blue-PAS for differentiating acid mucopolysaccharides and
neutral mucopolysaccharides, respectively (Pearse, 1960).
Each vas deferens is made of a convoluted tubular duct,
through which spermatozoa pass from the collecting tube of
the testis to the gonopore, where they are discharged
through a small papilla at the base of the last thoracic leg
P5. The vas deferens is formed by secretory epithelium
surrounded by connective tissue and histologically shows
three distinct regions: proximal, medial and distal. The
proximal and medial region of the vas deferens is lined by a
simple cubic epithelium, with lobate nuclei, and exhibits a
lumen filled with PAS-positive and Bromephenol Blue
positive material (Fig. 3A, B).
Spermatophores are formed initially in the proximal vas
deferens and develop in the medial and distal vas deferens.
The distal vas deferens is made of an extremely convoluted
duct which is filled with PAS-positive and Bromephenol
Blue positive material in the lumen (Fig. 3C) and is lined
by high columnar epithelium with lobate nuclei reinforced
by a larger amount of connective tissue and muscle
(Fig. 3D). The material in the lumen of entire vas deferens
is not stained with Alcian Blue. Spermatophores, which are
mainly oval shape in E. verrucosa, are formed when
spermatozoa transfer from the testis to the distal vas
deferens. They are enveloped by a capsule in the distal part
of the vas deferens (Fig. 3E), which is stained with
Bromephenol Blue (Fig. 3F), but is not stained with Alcian
Blue and gives a PAS negative reaction (Fig. 3E). There is
no evidence for a spermatophore capsule in the proximal
and medial vas deferens (Fig. 3B).
RESULTS
DISCUSSION
The male reproductive organ of Eriphia verrucosa is a
paired, H-shaped organ that lies just beneath the dorsal
carapace and above the hepatopancreas (Fig. 1). It is covered
by a thin capsule made up of a simple squamous epithelium
and a dense connective tissue layer (Fig. 2A), and it extends
posteriorly into the vas deferens. The testes are tubular and
can be subdivided into three histologically distinct parts:
anterior, intermediate and posterior. The anterior part of the
testes is composed of a convoluted seminiferous tubule
surrounded by hemal sinuses. Germinal cells develop to
spermatogonia only at one side of the periphery of the
seminiferous tubule. The seminiferous tubules are lined
externally by a simple squamous epithelium (Fig. 2A).
Whereas spermatogonia appear associated with a single
Sertoli cell in this region (Fig. 2B), the spermatocytes
present in the center of seminiferous tubules (Fig. 2A) are
carried by collecting duct to the intermediate part of the
testis. The Sertoli cells are distinguishable from the
spermatogonia, because their nuclei are more basophilic
and appear smaller than that of the spermatogonia. The
collecting duct is made up of a ciliated cubic epithelium at
the anterior part of testis, whereas the intermediate part of
the testis consists of a collecting duct lined by simple
columnar epithelium and its lumen is filled with homogenous material which gives a PAS-positive reaction and when
stained with Bromephenol Blue. Only mature spermatids are
found within the collecting duct (Fig. 2C). The posterior part
of the testis, which is connected to the vas deferens, is lined
by a simple squamous epithelium (Fig. 2D, 2E).
The external morphology of the testes varies among
decapods. In Eriphia verrucosa, the testes are located fairly
centrally within the carapace and form a paired H-shaped
organ. An H-shaped testicular morphology was also
previously described in other brachyuran crabs such as
the blue crab Callinectes sapidus, the snow crab Chionoecetes opilio, the red-clawed mangrove tree crab Goniopsis
cruentata (Latreille, 1802) and the mangrove crab Ucides
cordatus (Johnson, 1980; Beninger et al., 1988; Garcia and
Silva, 2006; Castilho et al., 2008, respectively). Generally,
the testes of decapods are covered by a capsule made up of
an outer epithelial layer and an inner connective tissue
layer (King, 1948; Bell and Lightner, 1988). In Eriphia
verrucosa, the testis is covered by a capsule made up of a
simple squamous epithelium and a thin layer of dense
connective tissue. A fibrous layer, rich in collagen fibers in
the testicular capsule was observed in the blue crab
Callinectes sapidus (Johnson, 1980), the mangrove crab
Ucides cordatus (Leite, 2002), the mangrove tree crab
Goniopsis cruentata (Garcia and Silva, 2006), the penaeid
shrimp Penaeus setiferus (Linnaeus, 1767) (King, 1948)
and the spiny lobster Panulirus laevicauda (Lima, 1995).
As in Eriphia verrucosa, many other decapods also have
a testis composed of multiple lobes surrounded by hemal
sinuses (Bell and Lightner, 1988; Sokolowicz et al., 2007).
These include the shrimp Penaeus trisulcatus (Leach,
1815), the spiny lobster Panulirus penicillatus (Olivier,
1791), the Hawaiian red lobster Enoplometopus occidentalis (Randall, 1840), and the golden deep sea crab Geryon
Fig. 1. Dorsal view of Eriphia verrucosa (carapace length: 85 mm).
Hepatopancreas (HP), gills (G), paired H-shaped testis (T) and vas
deferens (VD).
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JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 29, NO. 4, 2009
Fig. 2. Hematoxylin and eosin stained sections of the testis of Eriphia verrucosa. A, General view of the anterior part of testis, showing the germinal
epithelium (GE) and the seminiferous tubules (asterix) containing spermatocytes (ST) in the lumen and are covered by a capsule (arrow). B, Germinal
epithelium showing spermatogonia (SG) with adjacent single Sertoli cell (SC). C, General view of the intermediate part of testis showing the lumen
contains spermatids (SD) embedded in homogenous material (HM). D, General view of the posterior part of testis showing the lumen contains spermatids
(SD) intermingled with homogenous material (HM). E, The posterior part of the testis is lined by a simple squamous epithelium (SE), containing
spermatids (SD).
ERKAN ET AL.: TESTIS AND VAS DEFERENS OF ERIPHIA VERRUCOSA
461
Fig. 3. Hematoxylin and eosin stained (A-E) and bromephenol stained (F) vas deferens of Eriphia verrucosa. A, Transition of cross section from proximal
to medial vas deferens. The lumen is filled with secretion (S) and shows early spermatophore (asterix). B, The medial region is lined by a simple cubic
epithelium (CE) has and spermatophores embedded in secretion (S). C, General view of distal vas deferens showing convoluted columnar epithelium (CC),
secretion in the lumen (S). D, At the end of the vas deferens distal region has considerably high columnar epithelium (CC) with high secretion activity and
striated muscles (M) are scattered beneath the columnar epithelium. E, Late spermatophore containing mature spermatids (SD) surrounded by a capsule
(arrowhead) embedded in secretion (S). F, The capsule is stained with Bromephenol Blue (arrowhead), mature spermatids (SD), secretion (S).
fenneri Manning and Holthuis, 1984 (Heldt, 1938;
Matthews, 1951; Haley, 1984; Hinsch, 1988, respectively).
The testes of Callinectes sapidus, Geryon maritae Manning
and Holthuis, 1981 and Ranina ranina (Linnaeus, 1758)
also exhibit multiple testicular lobes, consisting of highly
convoluted seminiferous tubules (Cronin, 1947; Johnson,
1980; Melville-Smith, 1987; Minagawa et al., 1994).
The germinal epithelium in Eriphia verrucosa is restricted
to the convoluted anterior part of the testis. It is formed by
spermatogonia and adjacent single Sertoli cells that change
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JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 29, NO. 4, 2009
into germ cysts encapsulated by multiple Sertoli cells with
the spermatocytes in the center. Once spermatids are formed,
they are transported to a common duct lined by a simple
cubic ciliated epithelium and then to the central part of the
testis. The latter shows a simple columnar epithelium with
polysaccharide secretions filling the lumen. In other
brachyurans, Sertoli cells are observed to line the seminiferous tubules, whereas a germinal layer of spermatogonia
develop at one side of the seminiferous tubule periphery as in
E. verrucosa (Krol et al., 1992). The spermatogonia of E.
verrucosa could be distinguished by their large nuclei and
being adjacent to each other. Spermatocytes were observed in
the lumen of the seminiferous tubules at different stages of
meiosis, whereas further down the seminiferous tubules,
spermatids were recognized by their smaller dense nuclei, as
in other brachyurans (Krol et al., 1992; Nagao and Munehara,
2003).
The vas deferens of Eriphia verrucosa is divided into three
regions, proximal, medial and distal. According to different
criteria (Garcia and Silva, 2006), the vas deferens may be
composed of two parts, as in Scyllarus chacei (Hinsch and
Mcknight, 1988), four parts, as in Goniopsis cruentata
(Garcia and Silva, 2006), or ten parts, as in Diogenes
pugilator (Manjon-Cabeza and Garcia Raso, 2000), with
varying functions depending on the species (McLaughlin,
1983). It is thus very possible that the regional differences
found in the vas deferens of different species may be related
to the type of spermatophore produced.
The vas deferens in Eriphia verrucosa is composed of a
tubular duct, convoluted in some sections, through which
spermatozoa pass from the posterior part of the testis to the
gonopore. The role of the vas deferens is spermatophore
formation (Cronin, 1947; Johnson, 1980) and the initial part
of the proximal vas deferens is termed the ‘‘vas efferens’’
by Cronin (1947) and is composed of highly variable
epithelium. The proximal vas deferens is composed of
simple columnar epithelium in Callinectes sapidus (Cronin,
1947) and in the reef lobster Enoplometopus occidentalis
(Haley, 1984), but it is composed of cubic epithelium in
Eriphia verrucosa. The proximal vas deferens of Eriphia
verrucosa showed a difference from Callinectes sapidus
(Cronin, 1947), and Ucides cordatus (Castilho et al., 2008)
by not having muscle cells.
The entire vas deferens secretes one type of substance in
Eriphia verrucosa which was identified on the basis of
same staining properties. This substance is stained with
Bromephenol Blue and gives a PAS-positive reaction, but
is not stained with Alcian Blue. These results suggest that
the secretion is a neutral mucopolysaccharide and mucoprotein. Garcia and Silva (2006) suggested that the vas
deferens in Goniopsis cruentata, had two types of secretion
which are rod-shaped glycoproteins and polysaccharides, as
evidenced by the positive reaction to staining with PAS and
Alcian Blue. According to Castilho et al. (2008) the vas
deferens in Ucides cordatus has evaginations filled with a
secretion positive to PAS reaction, indicating the presence
of polysaccharides.
In the distal vas deferens of decapods the spermatophore
is surrounded by a capsule which is composed of acellular
material (Dudenhausen and Talbot, 1982; Anilkumar et al.,
1999). According to Subromoniam (1991, 1993) this
capsule is made of a protein-bound mucopolysaccaride
material in decapod crustaceans. Since the capsule stains
with Bromephenol Blue, but does not stain with Alcian
Blue and gives a PAS- negative reaction in E. verrucosa
this shows that it consists of mainly protein material (Mazia
et al., 1953). However, Anilkumar et al. (1999) have
suggested that brachyuran spermatophores are enveloped in
a material which is composed of a protein-bound
mucopolysaccharide. On the contrary, the envelope of the
spermatophore is composed of PAS-positive material in
Goniopsis cruentata (Garcia and Silva, 2006). The layer of
muscle cells and the enlarged connective tissue layer
beneath the epithelium of the distal region of the vas
deferens in Eriphia verrucosa suggest that muscle contraction serves to move the spermatophores and mix the
epithelial secretions with sperm along the vas deferens; as
in Libinia emerginata and Ucides cordatus (Hinsch and
Walker, 1974; Castilho et al., 2008).
In decapod crustaceans, sperm maturation, spermatophore
formation, as well as seminal fluid production and storage for
nourishment were described to take place in the vas deferens
before ejaculation occurred (Hinsch and Walker, 1974;
Burton, 1995; Tirelli et al., 2007). The length and coiling
of the vas deferens might thus serve to increase the effective
surface area for secretory, absorptive and storage functions
(Adiyodi and Anilkumar, 1988). Perhaps the secretion is
lubricant to aid the passage of the spermatophores as has
previously been suggested by Greenwood (1972) and Tudge
(1999). For this, several decapods have a fold in the wall of
the vas deferens called a typhlosole. In the spiny lobster
Panulirus sp., the typhlosole is located in the enlarged distal
part of the vas deferens and secretes the matrix that
encapsulates the spermatophore (Aiken and Waddy, 1980).
These kinds of complex foldings are observed in the distal
region of vas deferens of E. verrucosa.
In decapod crustaceans, spermatophores have been
categorized into three different types. One type of
spermatophore is fragile and the simplest form of
spermatophore found in some brachyuran crabs undergoing
internal fertilization and is stored directly in the genital
duct of the female as seen in E. verrucosa [Cronin (1947) –
Callinectes sapidus; Hinsh and Walker (1974) – Libinia
emerginata and Libinia dubai (Edwards, 1834); Erdman
and Blake (1988) – Geryon fenneri; Perez (1990) – Matuta
lunaris (Forskål, 1775); Beninger et al. (1993), Elner and
Beninger (1995) – Chionoecetes opilio; Anilkumar et al.
(1999) – Metopograpsus messor (Forskål, 1775); LopezGreco et al. (1999) – Chasmagnathus granulata (Dana,
1851); Yosho (2000) – Chionoecetes japonicas (Rathbun,
1932); Yamaguchi (2001) – Uca lacteal (De Haan, 1835);
Pinheiro and Fransozo (2002) – Arenaeus cribrarius
(Lamarck, 1818); Hinsch (2005) – Chaceon fenneri
Manning and Holthuis, 1984; Garcia and Silva (2006) –
Goniopsis cruentata]. The spermatophores are small and
either ellipsoidal or spherical. This type might form the
sperm plug in the seminal receptacle of the female, which
prevents other male sperm from getting into the female
reproductive tract (Cronin, 1947; Ryan, 1967; Hinsch and
Walker, 1974; Krol et al., 1992).
ERKAN ET AL.: TESTIS AND VAS DEFERENS OF ERIPHIA VERRUCOSA
Another type of spermatophore in some brachyuran
crabs, anomurans, and macrurans that undergo external
fertilization has a complex structure since the spermatophores in this group are exposed to external factors and
need to be preserved more while awaiting fertilization
outside the body when compared with these in the former
group (Adiyodi and Anilkumar, 1988; Krol et al., 1992;
Subramoniam, 1995; Anilkumar et al., 1999). This type of
spermatophore is tubular and has several layers made of
acellular material and they are found in the form of an
interrupted column as in Pacifastacus leniusculus (Dana,
1852), Homarus americanus Milne Edwards, 1837, Enoplometopus occidentalis and Panulirus homarus (Linnaeus, 1758) (Kooda-Cisco and Talbot, 1982; Haley, 1984;
Mann, 1984; Radha and Subramoniam, 1985) or units
pinched off the column (Dudenhausen and Talbot, 1982).
The third type of spermatophore is pedunculate and
exists in the whole Anomura except for a few species in the
Hippidae and Aeglidae (Greenwood, 1972; Tirelli et al.,
2007; Tudge, 1999; Tudge and Scheltinga, 2002; Scelzo et
al., 2004).
This study constitutes the first investigation of the male
reproductive system of Eriphia verrucosa, a commercially
harvested species (Dogan et al., 2007). These results imply
that E. verrucosa has similar male reproductive systems to
that found in other brachyurans, consisting of an H-shaped
testis with spermatogenesis taking place in the anterior
testis (Garcia and Silva, 2006). Also the spermatophores
are the simplest type of brachyuran form which may form
the sperm plug in the seminal receptaculum of the females
(Hinsh and Walker, 1974; Tomikawa and Watanabe, 1990).
In addition, determination of the microscopic and histochemical structure of the male reproductive system helps to
better understand the management and rearing in culture of
this species.
ACKNOWLEDGEMENTS
We acknowledge Dr. Christopher Tudge for an earlier review of this
manuscript.
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RECEIVED: 4 November 2008.
ACCEPTED: 3 March 2009.