MORFOLOGIA

MORPHOLOGICAL CONSIDERATIONS ON THE SEMINIFEROUS

STRUCTURES AND TESTES OF ANURAN AMPHIBIANS:
Bufo crucifer, Physalaemus cuvieri AND Scinaxfuscovarius
Classius de Oliveira I
Aline Cristina Sant' Anna2
Paula Munhoz de Omena3
Lia Raquel de Souza Santos4
Rodrigo ZierP
ABSTRACT
This study describes the testicular anatomy and the general morphology ofthe seminiferous elements
in three species 01' anurans: Bufo crucifer (Wied, \82\), Physalaemus cuvieri (Fitzinger, \826), Scinax
fscovarius (Lutz, 1925). Six samples 01' each species were used and, after a macroscopic examination,
their testes were submitted to microscopic analysis. Anatomically, the testes of those three species had
distinct patterns as to shape, size, and color. An unusual characteristic was the presence of pigment-
containing cells in the testis 01'P cuvieri, showing a dark brown coloration; pigmented cells were present
only in the Bidder's organ 01' B. crucifer; however, this pigmentation did not occur in S. jscovarius. We
described the histological structure and identified a general organization 01' cellular types 01'
spermatogenetic lineage, which were similar among the species. Other morphological aspects 01' the
mal e gonads were compared with species 01' anurans.
Key words: Anura, Bufo cntc/fer, Physalaemus cuvieri, Scinaxjscovarius, testis, spermatogenesis.
RESUMO
Consideraes morfolgicas sobre os testculos e as estruturas seminferas de anfbios anuros: Bufo
crucifer, Physalaemus cuvieri e Scinaxfuscovarius
Este trabalho descreve aspectos anatmicos e apresenta uma caracterizao morfolgica geral dos
elementos seminferos, quanto organizao cstica do epitlio germinativo, de trs espcies de anuros:
Bufo crucifer (Wied, 182\), Physalaemus cuvieri (Fitzinger, \826) e Scinax fuscovarius (Lutz, 1925).
Foram utilizados seis exemplares de cada espcie que, aps as descries macroscpicas, foram subme-
tidos rotina histolgica para anlises microscpicas. Anatomicamente, os testculos dessas espcies
apresentam diferentes padres quanto forma, ao tamanho e colorao. Uma caracterstica que se
destaca a presena de clulas contendo pigmento no testculo de P cuvieri, conferindo a colorao
marrom escura ao rgo, interna e externamente; uma discreta presena de pigmentao ocorre apenas
no rgo de Bidder de B. crucifer; entretanto, nenhuma pigmentao ocorre em S. fuscovarius. Em
relao aos aspectos microscpicos tambm foram analisados, a arquitetura histolgica testicular e os
diferentes tipos celulares da linhagem germinativa e conclui-se que, de modo geral, so muito seme-
lhantes. A partir da anlise do epitlio germinativo cstico desses animais discutimos a formao e o
desenvolvimento dos cistos espermatogenticos em Anura.
Palavras-chave: Anura, Bufo crucifel~ Physalaemus cuvieri, Scinax fuscovarius, testculo, esper-
matognese.
Recebido em: 18.1102; aceito em: 30.04.03.
I Coordenador do Laboratrio de Anatomia Comparativa, Departamento de Biologia, Instituto de Biocincias, Letras e Cincias Exatas (lBILCE) -
UNESP. CEP 15054-000, So Jos do Rio Preto, So Paulo, Brasil - E-mail:classius@bio.ibilce.unesp.br
2 Discente de Cincias Biolgicas, IBILCE. Bolsista PET/SESu-MEC.
) Discente de Cincias Biolgicas, IBILCE.
4 Discente de Cincias Riolgicas, UFMS, Trs Lagoas.
5 Mestrando do Programa de Ps-Graduao em Biologia Animal, IBILCE.
BIOCINCIAS, Porto Alegre, v. 11, n. I, p. 39-46, jun. 2003
40
OLIVEIRA, C de, et aI.
INTRODUCTION
In general, anatomically, in anurans the testes are
rounded, compact and yellowish, They can present
anatomic variations in form and weight according
to the reproductive period (OUELLMAN; TRUEB,
1994), beside other morphofunctional alterations re-
lated to the seasonality of reproduction (LOFTS,
1974), as it was described for some species
(MONTEIRO; PISAN, 1990, 1992; HUANG et aI.,
1997; OLIVEIRA; VICENTINI, 1998),
Histologically, the testes are covered with a thin
capsule ofconnective tissue, the albuginea tunic, with
its traverse for blood vessels, which go to the testicu-
lar parenchyma, Th is parenchyma presents a germ
tissue arranged in seminiferous locules delimited by
a loose connective tissue, however an intratesticu-
lar septa fonnation does not occur (OLIVEIRA;
VICENTINI, 1998),
In vertebrates, the germ tissue is disposed in a
hollow structure - e.g. the seminiferous tubules in the
amniotes, saclike seminiferous ampoules in the cy-
clostomes and urodeles or intermediate structures in
some other groups (HILOEBRANO, 1995), According
to Romer and Parsons (1985), the arrangement of
this tissue, in fish and amphibians, defines some-
what spherical structures, the seminiferous ampoule,
In amphibians, the terminology used for the des-
cription ofthis genninative compartment may change
(GRIER, 1992; OLIVEIRA; VICENTINI, 1998),
However, as a general characteristic of the histologi-
cal architecture of the seminiferous elements in
amphibians, the germ epithelium is organized in
seminiferous locules in Apoda (WAKE, 1969) and
Anura (OUELLMAN; TRUEB, 1994; OLIVEIRA;
VICENTINI, 1998) or in a seminiferous ampoule in
Urodela (HILOEBRANO, 1995).
In the testicular parenchyma, the germ tissue
presents spermatogonias located in the base of the
epithelium, and, in the sequence of cytodifferentiatioil,
spermatocytes, spermatids, and spermatozoa, wh ich
are generally found near the lumen. This epithelium
shows a cystic arrangement, i.e., groups of germ cells
join with the Sertoli cells forming spermatocysts, a
common characteristic in the amphibians (WAKE,
1969; LOFTS, 1974; OLIVEIRA et aI., 2003), as well
as in other anamniotes (GRIER, 1992).
Concerning the morphology of the seminiferous
locules and the cystic arrangement of the germ
epithelium, we can stress the contributions in the
following families: Bufonidae - Nectophrynoides
BIOCIENCIAS, Porto Alegre, v. 11,11. I, p. 39-46, jUI1. 2003
occidentalis (ZUBER- VOGELI; XAVIER, 1966);
Bufo woodhousei (ATHERTON, 1974); B. arenarum
(CAVICCHIA; MOVIGLIA, 1982); B. regularis
(ABOELMAGUID; SABRY, 1987); genus Telmatobius
(MONTERO; PISAN, 1990) and B. melanostictus
(HUANG et aI., 1997); Hylidae - Pachyme-
dusa dacnicolor (RASTOGI et aI., 1988); Hyla
ranki (TABOGA; OOLOER, 1991); H andina
(MONTERO; PISAN, 1992); H japonica (LEE;
KWON, 1992) and Scinax fuscovarius (OLIVEIRA;
VICENTINI, 1998; OLIVEIRA et aI., 2003);
Leptodactylidae - Physalaemus fuscomaculatus
(AOKI et aI., 1969); Caudiverbera caudiverbera
(HERMOSILLA et aI., 1983); Odontophrynus
cultripes (BO et aI., 1991); Bombina bombina
(GOLLMANN et aI., 1993); genus Physalaemus
(AMARAL et aI., 1999) and Physalaemus cuvieri
(OLIVEIRA et aI., 2002).
Thus, we describe some morphological characte-
ristics of the seminiferous locules and testes in three
different anuran species of distinct families. While
analyzing and comparing these aspects in the referred
species, we establ ished a generalized description for
anurans.
MATERIAL AND METHOD
Five adults of each species were used: Bufonidae
- B. crucifer (Wied, ] 82]), Leptodactylidae - P
cuvieri (Fitzinger, 1826), and Hylidae - S fuscovarius
(Lutz, 1925). The specimens were collected in Botu-
catu (So Paulo State - Brazil), between June and
Oecember, when the individuais are easily found in
their natural habitat because they were in the
reproductive activity period.
The animais were dissected and submitted to
morphological studies, after anesthesia with saturation
in ether. The animais were opened through medium
incision exposing the reproductive organs to macros-
copic analyses. After the reduction of the testes in
small pieces, they were immediately immersed in
Bouin fixative solution during 20 hours, washed, and
transferred to 70% ethanol solution. Then, the material
was sent to the histological routine to be dehydrated
in increasing concentration of ethanol, submitted
to tissular cIarification with xylol, and embedded
in paraffin. Sections of 6 mm were stained with
haematoxylin and eosin for histological analyses. The
morphological testicular arrangement was examined
with the light microscopy (Zeiss-Jenaval). The indi-
viduais were appropriately preserved as proof mate-
rial (collectionnumbers: B. crucifer-OZSJRP 6013,
Morphological considerations on the seminiferous . 41
6014,6015,6016,6017,6018; P cuvieri - 6019,6020,
6021, 6022, 6023, 6024; S. fuscovarius - 6004 with
fifteen samples).
RESULTS AND DISCUSSION
In vertebrates like mammals, the testes are com-
prised ofthe albuginea tunic which emits septa, de]i-
miting incomplete, strongly marked lobulations which
shelter the seminiferous tubules (HILDEBRAND,
1995). ln those animais, the tubules are typically
permanent structures which produce sperma-
tozoa during the reproductive period (ROMER;
PARSONS, 1985). To the anurans the structures
containing the germ epithelium are defined as semi-
niferous locules and the testes are not lobulated,
common in many urodeles and apodes (DUELLMAN;
TRUEB, 1994). In the three anuran species analyzed
- B. cruc(fer, P cuvieri, and S.fuscovarius, the testis
do not have septation and the seminiferous unit is also
defined as seminiferous locules, because histologically
they do not show a typical tubular aspect similar to
the mammals (OLIVEIRA; VICENTINI, 1998). In
H ranki the structure was defined as locular-tubule
(TABOGA; DOLDER, 1991).
As established, the species were collected during
the reproductive period, i.e., when the individuais
were in reproductive activity. The spermatogenetic
activity was afterward confirmed by means of analysis
of the histological testicular characteristics. Anato-
mically, there were great differences related to the
color, size, and shape ofthe gonads: B. crucifer had a
cylindric, milk-white testis with pigmented ovarian
tissue at the anterior end, Bidder's organ; P cuvieri
presented ovoid testis with dark brown pigmentation,
including internally; S. fuscovarius had in general
ovoid and milk white testis (Fig. 1). A testicular
pigmentation is also described for P fuscomaculatus
(AOKI et aI., 1969), B. bombina (GOLLMANN et aI.,
1993) and P cuvieri (OLIVEIRA et aI., 2002). These
pigment cells are found in different organs, consti-
tuting an extracutaneous pigmentary system of
unknown function (ZUASTI et aI., 1998). Despite
these interspecific anatomic differences, there are
morphologic similarities in the organ, mainly related
to histological characteristics.
Externally, the gonads show a granular aspect due
to the seminiferous locules, which are observed due
to albuginea tunic transparency. The blood vessels,
which exist in this testicular capsule, are mainly
destined to the parenchyma (Figs. 1 and 2). In these
units, the germ epithelium has cellular groups (cyst
or germ follicles) of ali kinds of cells of sper-
matogenetic lineage. This cystic arrangement is a
common characteristic in the amphibians (WAKE,
1969; LOFTS, 1974; DUELLMAN; TRUEB, ]994;
OLIVEIRA et aI., 2002, 2003). However, it is not an
exclusive one because it occurs in other anamniotes
(GRIER, 1992). Internally, between the seminiferous
units, they have an interlocular tissue composed by
Leydig cells, fibroblasts, blood vessels and some
efferent ductules (Fig. 3).
During the cytodifferentiation, the germ cells are
intimately associated to the Serto]i cells making cyst:
primary (I) spermatogonia, isolatedly and in the
epithelium base; secondary (11) spermatogonia, cysts
with high degree of variation in the cellular popu-
lation, proceeding from mitosis of the previous cells
and, in general, they are observed in the locular
periphery. Primary (I) and secondary (11) sperma-
tocytes and primary or round (I) and secondary or
e]ongated (11) spermatids, all of them present a great
cellular population, variable localization, and pecu-
liar morphologic aspecto Finally, the spermatocysts
arranged in spermatozoon bundles near the central area
of the locule, frequently present free spermatozoa in
the lumen of the seminiferous locule (Figs. 3 and 4).
Except for some characteristics of the cells and
specie-specific cystic arrangement, this description, in
general, occurs in the three species, and it was reported
in a similar way to some species ofthe same families:
Bufonidae - B. arenarum (CAVICCHIA;MOVIGLIA,
1982), B. melanostictus (HUANG et aI., 1997),
B. regularis (ABDELMAGUID; SABRY, 1987),
B. woodhousei (ATHERTON, 1974), N. occidentalis
(ZUBER-VOGELI; XAVIER, 1966) and genus
Telmatobius (MONTERO; PISAN, 1990); Hylidae
- H andina (MONTERO; PISAN, 1992), H
ranki (TABOGA; DOLDER, 1991) P dacnicolor
(RASTOGI et aI., 1988) and S. fuscovarius
(OLIVEIRA; VICENTINI, 1998; OLIVEIRA et
aI., 2003); Leptodactyl idae - C. caudiverbera
(HERMOSILLA et aI., 1983), o. cultripes (BO et
aI., 1991), Pfuscomaculatus (AOKl et aI., 1969) and
P cuvieri (OLIVEIRA et aI., 2002). A common
characteristic between these species is the fact that the
reproductive cyclened as continuous or potentially
continuous, according to the established classification
by LOFTS (1974).
ln the germ epithelium of the analyzed species,
the cystic distribution apparent]y does not follow a
distribution sequence; it is possible to just identify the
BIOCINCIAS, Porto Alegre, v. 11, n. I, p. 39-46, jun 2003
42
OLIVEIRA, C de, et aI.
spermatogonia near to the locule wall and the
spermatozoon bundles, in general, near or in the
locular lumen. This description can also be used to B.
woodhousei (ATHERTON, 1974) and C. caudiverbera
(HERMOSILLA et aI., 1983) for which an aleatory
disposition was also observed.
Concerning formation and development of the
cystic structure, it is reported that the interaction
between the germ cells and Sertoli cells is impor-
tant. This was studied before in other species, like:
B. regularis (ABDELMAGUlD; SABRY, 1987),
C. caudiverbera (HERMOSILLA et aI., 1983),
P dacnicolor (RASTOGI et aI., 1988) and Rana
catesbeiana (SPRANDO; RUSSELL, 1988). Accor-
ding to these authors, thin extensions of cytoplasm of
the Sertoli cells comprise completely the germ cells,
forming a surrounded wall which also emits cyto-
plasmatic process between the cells ofthe cysts.
The Sertoli cells rest on the basal lamina of the
seminiferous tubule (CAVICCHIA; MOVIGLIA,
1982; ABDELMAGUlD; SABRY, 1987; RASTOGI
et aI., 1988), and continue attached to the wall even in
the more advanced stages of the spermatogenesis
(HERMOSILLA et aJ., 1983). With the formation of
the cysts, a compartmentalization is originated with a
fundamental role in the cytodifferentiation, providing
a structural and functional support to the germ cells
(RASTOGI et aI., 1988; BO et aI., 1991).
Therefore, the process starts when the sper-
matogonia - which are involved by the follicular or
Sertoli cells, forming the cyst wall- begin in a division
stage producing their followers, which are also located
in the interior of the structure. This arrangement
will only be altered in the final stages, during the
spermiogenesis, when the cells will pass through an
extraordinary elongation until the formation ofthe tail
and head of the spermatozoon. The Sertoli cells will
sustain the bundles with the heads embedded in their
cytoplasm and the tail will be free and turned to the
lumen of the seminiferous locule (Fig. 4). According
to Sprando and Russel (1988), at this moment the
lumen of the germ cyst joins the Iumen of the
seminiferous 10Cllle. Thus, the spermatozoa will be
released to follow the spermatic path.
Hermosilla et aI. (1983) reported that the germ
cells remain directly or indirectly attached to the locule
wall. For this reason, we suppose that after the
spermatozoa liberation, the Sertoli cell regresses till it
acquires the characteristics of a follicular cell, which
may restart the process as soon as it joins the primor-
dial genn cell. Although this might be a possibility
BlOClNClAS. Porto Alegre, v. lI, n. l, p. 39-46, jun. 2003
concerning these cells, these questions can not be
elucidated by the present study.
Despite the architecture ofthe germ epithelium of
ali mentioned species represents general and typical
model for the anurans, the final germ cell ~ the
spermatozoon - shows a great heterogeneity in the
species. This can be related to phylogenetic aspects
(KWON; LEE, 1995) and to reproductive strategies
ofthe anurans (DUELLMAN; TRUEB, 1994).
Regarding the reproduction, the presence of
developed spermatozoa during ali the reproductive
period suggests a capacity of reproduction occurring
a few times in a single season. Thus, the gametogenic
activity occurs simultaneously in ali the locules;
however, while some seminiferous locules shelter
mainly free spermatozoa, ready to be spread, others
have bigger cellular populations in the previous stages
ofthe cytodifferentiation. This allows for each indivi-
dual and to the population, as a reproductive strategy,
a great chance of success in the appropriate moments
during that only season. Our observations are corro-
borated by Rossa-Feres and Jim (1994), who put
in evidence preferential periods of reproduction,
based on the occurrence of tadpole and male in
vocal ization.
ACKNOWLEDGMENTS
We are grateful to Benedito Rinaldo Cardana (Departamento
de Zoologia - UNESP - Botucatu) for identificaton ofthe species.
to Umberto Jorge Alves de Andrade for schematizing in
translucent tracer paper, to Roberta Faria Fernandes and Prol'. Df.
lvaro Luiz Hattnher (Departamento de Letras Modernas,
UNESP, So Jos do Rio Preto) for the translation into English.
This work was supported by FAPESP (grant n 02/08016-9).
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BIOCINCIAS, Porto Alegre, V. 11, n. I, p. 39-46,jlln. 2003
44
OLIVEIRA, C. de, et a!.
Fig. 1. A. Cylindric testes (1) af B. crucifer with Bidder's argan (arrow) in the cranial extremity
(3,2x). B. Ovaid testes af P. cuvieri with dark brown pigmentatian (6,4x). C. Ovaid testes af
S. fuscovarius unprovide af the pgmentatian (3,2x).
BIOCINCIAS, Porto Alegre, v. 11, n. 1, p. 39-46, jun. 2003
Morphological considerations on the seminiferous ...
45
t
A
t
B
Fig. 2. Testes anatomic aspect of the B. crucifer (A - 7x) and P cuvieri (B - 17x):
testes (t), fat body (I) and Bidder's organ (arrowhead). The pigmentation in P cuvieri
emphasize the units denominated seminiferous locules.
Fig. 3. Histological testicular arrangement in S.fuscovarius. A. interstitial tissue (i) with various Leydig cells, blood capillary (arrowhead)
and efferent ductules (arrow). (H/E, 850x). B. Seminiferous locuIes with the cystic germ epithelium: primary (1) and secondary (2 and 3)
spermatogonia; primary (4), in meiotic division (5) and secondary (6) spermatocytes; secondary spermatids (7); spermatozoa (8). Indicated
also the Leydig (L) and Sertoli (S) cells. (H/E, 680x).
BIOCINCIAS, Porto Alegre, v. 11, n. 1, p. 39-46, jun. 2003
46 OLIVEIRA, C. de, et a!.
Fig. 4. The schematic shows the generalized representation of the cystic germ epithelium for the three species:
1) spermatogonia I; 2) spermatogonia II; 3) spermatogonia II; 4) spermatocytes I; 5) spermatocytes I in division
meiotic; 6) spermatocytes II; 7) spermatocytes II in division meiotic; 8) spermatids I; 9) spermatids II;
10) spermatozoon bundles. The cysts are always connected to the locular wall by the Sertoli cells.
BIOCINCIAS, Porto Alegre, v. 11, n. 1, p. 39-46, jun. 2003