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SociedadEspañoladeMalacología Iberas, 26 (2): 1-14, 2008
Ultrastructural studies on the spermatogenesis of the
African mussel Pernaperna (Bivalvia: Mytilidae)
Estudio ultraestructural de la espermatogénesis del mejillón africano
Pernaperna (Bivalvia: Mytilidae)
Soumya BENOMAR*, Oumkeltoum BELHSEN**, Didier GOUX**,
Michel MATHIEU** andAbdellatifMOUKRIM*1
Recibidoel30-V-2006.Aceptadoel15-1-2008
ABSTRACT
Transmission electrón microscopy of spermiogenesis ¡n gonads of Perno perna (Mytilidae)
was carried out to study the different developmental stages and the structure of mature
sperm. Samples of mussels originated from a population living at Cap Ghir (southwestern
Morocco) and were collected from December 1999 toJune 2000 atseveral periods oftheir
sexual cycle. Numerous acini, surrounded by a connective tissue containing vesicular cells,
constituted the mate gonad of P. perna. Groups ofspermatogonia, spermatocytes, and sper-
matids, interconnected by ¡ntercellular bridges, were found in these acini. Proacrosomal
vesicles and a shortflagellum developed early in spermatogonia. Numerous Sertoli-like cells
were distributed among spermatogonia, nearestthe innerwall ofeach acinus. The reduced
cytoplasm of primary and secondary spermatocytes mainly contained mitochondria and
proacrosomal vesicles. Spermatogenesis consisted of a progressive condensation of the
chromatin and a reduction in size ofthe nucleus, the migration ofthe proacrosomal granule
from the base ofthe nucleus to its apex to become the acrosome, and the elaboraron ofthe
flagellum bythe distal centriole. The nucleus ofthe mature spermatozoon was barrel shaped
and contained a completely condensed chromatin. The funnel shaped acrosome showed
two types ofelectrón-dense materials in the basal and apical parts, and a more lucentzone
in the subacrosomal invagination and the center ofthe premembranoid sleeve. An axial rod
could be observed from the apex ofthe acrosome up to the base ofthe nucleus. The length
of the nucleus in the spermatozoon, the premembranoid sleeve, and the presence of three
types of materials in the acrosome might be additional criterio to sepárate the Moroccan
populations of P. perna from other Mytilidae and, in particular, from those of Mytilus gallo-
provincialiswhich also lives along Moroccan coasts.
RESUMEN
Las gónadas de Perna perna (Mytilidae) se examinaron en microscopía electrónica de
transmisión (TEM) con el fin de estudiar los estadios de desarrollo y la estructura del
esperma maduro. Las muestras de mejillones se originaron de una población asentada en
Cap Ghir (suroeste de Marruecos) y fueron colectadas entre diciembre de 1999 y junio
de 2000 en varios momentos de su ciclo sexual. La gónada macho de P. perna se com-
pone de numerosos ácinos, rodeados por un tejido conectivo que contiene células vesicu-
*LaboratoireSystémesAquatiques,MilieuMarínetContinental,FacultédesSciences,UniversitéIbnZohr,BP
28/S, 80000Agadir, Morocco.
** LaboratoiredeBiologieetde BiotechnologieMarines, FacultédesSciences, UniversitédeCaen, Esplanade
delaPaix, 14032CaenCedex, France.
1Addressreprintrequests.
,
Iberus, 26 (2), 2008
losas. Grupos de espermatogenias, espermatocitos y espermatidias, vinculados por puen-
tes intercelulares, fueron encontrados en estos ácinos. Vesículas proacrosomales y un fla-
gelo corto se desarrollaron temprano en las espermatogonias. Numerosas células tipo Ser-
toli estaban distribuidas en las espermatogonias, ¡unto a la pared interna de cada ácino.
El citoplasma reducido de espermatocitos primarios y secundarios contenía principal-
mente mitocondrias y vesículas proacrosómicas. La espermiogénesis consistió en una pro-
gresiva condensación de la cromatina y reducción del tamaño del núcleo, en la migración
del gránulo proacrosomal desde la base del núcleo hasta su ápice en donde forma el
acrosoma y en la elaboración del flagelo por el centriolo distal. El núcleo de! espermato-
zoo maduro tiene forma de barril y contiene una cromatina completamente condensada.
El acrosoma, en forma de embudo, presenta dos tipos de materiales densos frente a los
electrones de las partes basal y apical y una zona más clara en la invaginación subacro-
somal y en el centro de la manga premembranóide. Una varilla axial se puede observar
entre el ápice del acrosoma y la base del núcleo. La longitud del núcleo del espermato-
zoo, la manga premembraníode y la presencia de tres tipos de material en el acrosoma
pueden resultar criterios adicionales para diferenciar las poblaciones marroquíes de P.
perna de otros Mytilidae y particularmente de aquellas de Mytilus galloprovincialis, que
también vive en la costa marroquí.
KEYWORDS:Pernaperna spermatogenesis,Mytilidae,ultrastructure.
PALABRAS CLAVE:Pernaperna, espermatogénesis,Mytilidae, ultraestructura.
INTRODUCTION
Ln Bivalvia, the morphology of the described by Bernard and Hodgson
spermatozoon gives information on the (1985). By contrast, to our knowledge,
mode of fertilization (in water, or in the there are no published reports on the
mollusc) (Franzen, 1955) and on the first cell stages of spermatogenesis.
systematic position oftaxa (Healy, Keys Therefore, the aim of this work was to
and Daddow, 2000). As the morphol- describe the fine structure of the devel-
ogy of this gamete is well conserved in opmental cell stages which succeeded in
several taxa, it is considered to be a the spermatogenesis of this mussel and,
good indicator of phylogenetic relation- in particular, during the formation of
ships between species, in particular the acrosome, as this organelle has a
when these come cióse to each other direct implication on the fertilization of
(Popham, 1979; Healy et al., 2000). A the oocyte.
goodexampleisthefamilyMytilidae, as As other populations of P. perna live
the characteristics of the spermatozoon worldwide under tropical conditions
vary remarkably between genera (see the review by Hicks, McMahon
(KafanovandDrozdov, 1998). and Ingrao, 2001), it is interesting to
Contrary to studies whichhavebeen detect the variations which may exist in
carried out on the spermatogenesis of the morphology of spermatozoa when
numerous mytilids, little information on they originate from different communi-
the developmental cell stages of the ties of mussels, as the fine structure of
male line in Perna perna is available in these male cells has already been
literature. The fine structure of mature studied in Brazilian (Bourcart et al.,
spermatozoa of this mussel was already 1965) as well as in South African
studied by Bourcart, Lavallard and (Bernardand Hodgson, 1985) popula-
Lubet (1965), or by Bernard and tions of P. perna. Consequently, the
Hodgson (1985), while aspeets of second aimofthis workwas to compare
spermiogenesis in P. perna were first spermatozoon morphologies between
2
:
BENOMARETAL. Spermatogenesis ofPernaperna
:
the abovementioned populations of P. series, the tissues were directly embed-
perna and the Moroccan mussels, as P. ded in Epon resin at 37°C for 60 min
perna is present here at the northern and were subsequently placed at room
limit of its distribution along the temperature during 12 hours for poly-
AtlanticcoastsofAfrica. merization. Semi-thin sections of each
Finally, as the Moroccan mussels are gonad portion were stained at room
abundantly consumedbylocalpeople, a temperature with 0.5% toluidine blue in
project to develop the breeding of this 2.5% Na2CC>3. Ultrathin sections were
mollusc for commercial purposes has collected on copper grids and were
been set up in Morocco (Berraho, stained for 20 min with uranyl acétate,
1998). However, to realize this project, followed by lead citrate for 5 min. Sec-
more detailed information on the local tions were examined using a Siemens
reproduction of P. perna was necessary. 102electrónmicroscope.
Several studies of our team were Thelengthandthewidthofeachcell
already carried out on the growth, stage were also measured (10 cells at
ecology, reproduction, and reserve strat- least per stage). Individual valúes
egy of this species (Id Halla, recorded for each measurement and
Bouhaimi, Zekhnini, Narbonne, eachcellstagewereaveraged.
Mathieu and Moukrim, 1997; Najimi,
Bouhaimi, Daubeze, Zekhnini, Pel-
lerin, Narbonne and Moukrim, 1997; RESULTS
Kaaya, Najimi, Ribera, Narbonne and
Moukrim, 1999; Moukrim, Kaaya, Each gonad was constituted by
Najimi, Roméo and Gnassia-Barelli, many acini, surrounded by connective
2000). The work reported in the present tissue and an external ciliated epithe-
study completes these first papers and lium (Fig. 1A). From the internal wall of
gives information on the development each acinus to the lumen, all develop-
ofthemalelineinthismussel. mental stages were present (Fig. IB).
Groups ofspermatogonia arepositioned
nearest the wall of each acinus, groups
MATERIALSAND METHODS of spermatocytes and spermatids were
located closer to the acinus lumen,
Samples of five male mussels each whereas the flagella of mature sperm
(3-4 cm long, 8-9 g in weight) were col- were confined to the central lumen (Fig.
lected in December 1999, January, IB). All acini emptyed into spermatic
March, June, and July 2000 from the ducts, each being lined by an internal
mid-tide level at Cap Ghir (50 km north ciliated, columnar epithelium. Vesicular
from Agadir town). The choice of these cells, containing two types of granules,
months for mussel sampling was based were distributed within the interacinar
on the different sexual stages observed connectivetissue (Fig. 1A).
by Id Halla et al. (1997) in the same Spermatogonia Two types of sper-
population of P. perna: December (II matogonia (Fig. 2A,B)were observed in
stage), January (IIIAstage), March (IIIB the gonad of P. perna. The A spermato-
and IIIC stages). June (IIIC and IIID gonia (primordial cells) were large cells
stages), and July (IIIC and IIID stages). (16.6 x 5.9 jum in size). Their nucleus
mm
Small portions oímale gonad (1-3 3 was often ovoid (6.3 x 4.0 jum), each
each) were fixed for 60 min in 2% glu- with a single 1.6-jum nucleolus, and
M
taraldehyde (in 0.4 sodium cacody- their translucent cytoplasm contained
late buffer, pH 7.2) at 4°C. The tissue an extensive rough endoplasmic reticu-
M
was then washed in 0.4 cacodylate lum (RER), numerous mitochondria,
buffer (3 x 10 min) and postfixed for 90 and a Golgi apparatus. B spermatogonia
M
min in 1% tetroxide osmium (in 0.4 are smaller cells (7.2 x 3.0 jum) and their
cacodylate buffer) at 4°C. After dehy- nuclei (4.2 x 2.3 jum) had a well-devel-
dration through a gradual ethanol oped euchromatin and sometimes a
3
Iberus, 26 (2), 2008
visible nucleolus. Their dark cytoplasm divided into four stages, from A the
contained numerous mitochondria, RER youngest, to D the oldest. A spermatids
cisternae, and proacrosomal vesicles (Fig. 4A) were irregular in shape (7.4 x
derived from the Golgi complex. These 6.6 |Um) and their round nuclei (4 pm)
B spermatogonia had an irregularly- contained scattered heterochromatin.
shaped membrane and intercellular Grouped mitochondria and proacroso-
bridges were frequently observed. In malvesicles cióseto the Golgiapparatus
some B cells, a short flagellum elabo- couldbe seenintheircytoplasm. B sper-
rated by the distal centriole, at the base matids (Fig. 4B) were smaller (4.1 x 3.2
of the nucleus, could be seen. When the ium) than A cells and their nuclei were
nuclei of B cells underwent metaphase more reduced (2.5 x 1.9 jum), eccentri-
(Fig. 3A), these spermatogonia became cally positioned, and contained a more
smaller (4.6 x 4.1 jum). Numerous condensed heterochromatin. Aproacro-
Sertoli-like cells were distributed among somal granule, resulting from the fusión
spermatogonia, nearest the wall of each of the corresponding vesicles, was
acinus. Each of these elongated (10.5 x present in their cytoplasm. In C sper-
3.0 ¡um) and regularly-shaped cells con- matids (Fig. 4C), the nuclei became
tained an ovoid nucleus with chromatin rounded (2.2 x 1.9 ¡um) and the nuclear
condensed along the nuclear envelope. chromatin was continuously condens-
Numerous cytoplasmic processes in ing, thus showing a patchwork pattern.
contact with cióse spermatogonia could The proacrosomal granule migrated
be observed. The cytoplasm of these from the basal part ofthe nucleus to the
Sertoli-like cells contained numerous cell apex and progressively modified its
electrón-dense inclusions, mitochondria, shape. Its basal part, towards the
several lipid inclusions, and myelin-like nucleus, became flattened, whereas an
figures (Fig. 2A,B, andFig. 3A). invagination in the granule formed the
Spermatocytes The primary sperma- subacrosomal zone, containing a mater-
:
tocytes (Fig. 3B, C) were arranged in ial less electrón-dense than that
groups of 2-4 cells each, with intercellu- observed in the granule. Spherical mito-
lar bridges. When these cells were in chondria set up at the base of the
prophase (pachytene stage), their nuclei nucleus and surrounded the centrioles.
were similar in shape to those ofB sper- The nuclei ofthe oldest spermatids (Fig.
matogonia. However, their nuclear 4D) became elongated, were completely
envelope was thicker, with a clearly condensed, and showed two invagina-
wider perinuclear cisterna. The small tions, the first at the apex ofthe nucleus
size (6.7 x 3.8 pm) of their cytoplasm and the second atitsbase nearthe distal
increased the nucleo-cytoplasmic ratio. centriole. The proacrosomal granule
These cells contained the same progressively became funnel-like and
organelles as described for B spermato- turned into an acrosome containing a
gonia. A short flagellum was often dense material. In several spermatids, a
observed (Fig. 3B, C). premembranoid sleeve was sometimes
The secondary spermatocytes were observed in the apical part of the acro-
scarcely visible, due to the rapidity of some. The flagellum showed gradual
the second meiotic división. These cells structural changes during the differenti-
were irregular in shape (5.7 x 4.3 ¿/m) ation of spermatids. It is elaborated by
andptheir rounded nuclei (a meanof3.3- the distal centriole and was surrounded
3.4 in diameter) contained chro- by a ring of five mitochondria at the
matin forming a dense network at base ofthenucleus. The distal and prox-
metaphase stage. Mitochondria and imal centrioles were situated in perpen-
proacrosomal vesicles were mainly dicularposition(Fig. 4D).
present in their reduced cytoplasm (Fig. Spermatozoa: Inthe5.3pm longhead,
3D). the nucleus (1.35 ji/m in size) wasbarrel-
Spermatids: Their development like and was completelycondensed. The
within the gonad can be arbitrarily very long acrosome was funnel-like
4
BENOMARETAL.: Spermatogenesis ofPernaperna
Figure 1. The male acini ofPernaperna. A: semi-thin section showing vesicular cells in the
interacinar connective tissue. These cells had two types ofgranules and lipid inclusions. B: semi-
thinsection ofanacinuslimitedbyabasallamina. Sertoli-likecellsandspermatogoniaarelocated
along its inner side. Abbreviations, ac: acinus; bl: basal lamina; h: hemocytes; ict: interacinar con-
nective tissue; Li: lipid inclusions; se: Sertoli-like cells; Spc: spermatocytes; Spd: spermatids; Spg:
spermatogonia; Spz: spermatozoa;ve:vesicularcells. Scalebars, 10 pm.
Figura 1. Los ácinos macho de Perna perna. A: sección semifina mostrando células vesiculares en el
tejidoconectivoentreácinos. Estascélulasteníandostiposdegránalosyinclusionesdelípidos. B:sección
semifinadeunácinolimitadoporunalámina basal. CélulastipoSertoliyespermatogoniasestánsitua-
dosensuladointerno. Abreviaturas, ac:ácino; bl: lamina basal;h:hemocitos; ict: tejidoconectivo inte-
racinar; Li: inclusiones de lípidos; se: células tipo Sertoli; Spc: espermatocitos; Spd: espermatidias; Spg:
espermatogonia;Spz:espermatozoos; ve:célulasvesiculares. Escalas, 10jcm.
5
.
Iberas, 26 (2), 2008
Figure 2. Ultrathin sections ofearly (ASpg) and late (B Spg) spermatogonia inPernaperna sepa-
,
rated from each other by cytoplasmic processes ofSertoli-like cells. Intercellular bridges between
spermatogoniaarefrequent.Abbreviations: bl: basallamina;cp: cytoplasmicprocessesofSertoli-like
cells; cy: cytoplasm; da: dense aggregates; de: distal centrioles; fl: flagellum; m: mitochondria; mf:
muscularfibersaroundtheacinus;N: nucleus; nu: nucleolus;pb: intercellularbridgesbetweensper-
matogonia; pv: proacrosomalvesicle;se: Sertoli-likecells; Spg: spermatogonia. Scalebars, 5 pm.
Figura2. Secciones ultrafmasdeespermatogonias tempranas (A Spg)ytardías (BSpg) en Pernaperna,
separadas unas de otrasporextensiones citoplásmicas de células tipo Sertoli. Sonfrecuentes lospuentes
intercelulares entre espermatogonias. Abreviaturas: bl: lamina basal; cp: extensiones citoplásmicas de
células tipo Sertoli; cy: citoplasma; da: agregados densos; de: centriolos distales;fl:flagelo; m: mitocon-
dria; mf:fibras musculares rodeando elácino; N: núcleo; nu: nucléolo;pb:puentes intercelulares entre
espermatogonias;pv: vesículaproacrosomal;se:célulastipoSertoli;Spg:espermatogonia. Escalas, 5pm.
(Rightpage) Figure 3. Ultrathinsections ofspermatogoniaandspermatocytes inPernaperna A: B
spermatogonia in metaphase. B, C: primary spermatocytes (Spcl) in prophase (pachytene stage),
each showing a wide perinuclear cisterna. D: secondary spermatocytes (Spc2). Abbreviations, bl:
basal lamina; cy: cytoplasm; fl: flagellum; m: mitochondria; N: nucleus; nu: nucleolus; pb: inter-
cellular bridges between spermatogonia; pv: proacrosomal vesicle; se: Sertoli-like cells; Spg: sper-
matogonia;wpc:wideperinuclearcisterna. Scalebar, 3 pm.
(Páginaderecha)Figura3. SeccionesultrafinasdeespermatogoniasyespermatocitosdePernaperna.A:
espermatogoniasB en metafase. B, C: espermatocitosprimarios (Spcl) enprofase (estadiopaquiteno),
cada uno mostrando unaamplia cisternaperinuclear. D: espermatocitossecundarios (Spc2). Abreviatu-
ras, bl: lámina basal; cy: citoplasma;fl:flagelo; m: mitocondria; N: núcleo; nu: nucléolo;pb:puentes
intercelularesentreespermatogonias;pv: vesículaproacrosomal;se:célulastipoSertoli;Spg: espermatogo-
nia; wpc:cisternaperinuclearancha. Escalas, 5pm.
ó
BENOMARETAL.: Spermatogenesis ofPernaperna
7
Iberus, 26 (2), 2008
shaped, could reach up to 3.4 pm in of 9 doublets along the periphery and a
length, and contained an axial rod from single central doublet. In this last zone,
the apex to its basal part. Three types of the cytoplasm was strongly reduced,
material couldbeobserved.Anelectron- thus increasing the nucleo-cytoplasmic
lucent zone in the subacrosomal invagi- ratio.
nationand the center ofthepremembra- Abnormal spermatogenesis Giantsper-
:
noid sleeve could be observed, whereas matogonia, each containing 2 to 5 nuclei
two types of electrón-dense materials (Fig. 6A), and binucleated spermato-
were respectively present at the periph- cyteswere oftenfoundinDecember and
ery of the apical part and in the base of March, respectively. In spermatids, lysis
the acrosome, the former material being could affect the cytoplasm or the
denser than the latter. The axial rod nucleus to finally yield to an extremely
passed outside the nucleus, from the condensed nucleus or a thick nuclear
apical to the posterior invaginations envelope, respectively. At the end of
(Fig. 5A).Atthebase ofthenucleus, five spermatogenesis, the acrosome might
spherical mitochondria, of variable size lose its shape, curve, and evenemptyits
(0.5-0.7 jum), surrounded the diplosome material, thus giving an electron-lucent
and constituted the middle piece (Fig. zone (Fig. 6B). Cióse to these abnormal
5B). The two centrioles were situated in cells, cytoplasmic inclusions with lipid
a perpendicular position and showed inclusions and lysosomal membranes
the classic nine triplets of microtubules mightbe seenintheluminaofacini.
(Fig. 5B). Some fibers, originating from
the distal centriole and situated in a
radiating position around it, formed a DISCUSSION
basal píate with the plasma membrane.
Transversal sections of the axonemal Most results on the spermatogenesis
complex of the flagellum (0.3 pin in of P. perna are similar to those noted on
diameter) showed the typical presence the differentiation of male cells in other
(Rightpage) Figure4. UltrathinsectionsofspermiogenesisinPernaperna.A: ayoungspermatid(A
Spd),with fusión ofmitochondriaandaGolgi complexshowingsyntheticactivity. B: aproacroso-
malgranuleandproacrosomalvesicles nearthe Golgi complexin an olderspermatid (B Spd). C: a
C spermatid (C Spd) with its nucleus showing a patchwork aspect. The proacrosomal granule is
migratingto the anteriorapexofthe spermatid. D: an oldestspermatid (D Spd) showingthe total
condensation ofthe nucleus.Theacrosomeis atthecellapex.Abbreviations,A: acrosome; cc: cen-
triolarcomplex; de: distal centrioleattachedto the flagellum; fl: flagellum; G: Golgi complex; gpa:
proacrosomalgranule;ln:nuclearlacunacomposedofheterochromatin;m:mitochondria;N:nucleus;
pb:intercellularbridges;pe:proximalcentriole;pi(whitearrow):posteriorinvaginationofthenucleus;
pv: proacrosomalvesicles; rf: radiatingfibers; sai (white arrowhead): subacrosomal invagination of
thenucleus;vg: Golgianvesicle. Scalebars,A-C: 2pm; D: 1 pm.
(Páginaderecha)Figura4. Seccionesultrafmasdeespermiogénesisen Pernaperna.A: unaespermatidia
joven (A Spd), confusión demitocondriasyun complejode Golgi mostrandoactividadsintética. B: un
granuloproacrosomaly vesículasproacrosomales cerca delcomplejo de Golgi en una espermatidia más
avanzada (B Spd). C: una espermatidia C (CSpd) cuyo núcleo muestra un aspecto en mosaico. El
gránuloproacrosomalesta migrando hacia elápiceanteriordelaespermatidia. D: unaespermatidiade
mayoredad(DSpd) mostrando la condensación totaldelnúcleo. Elacrosomasesitúa en elápicede la
célula. Abreviaciones, A: acrosoma; cc: complejo delcentriolo; de: centriolo distalsujeto alflagelo;fl:
flagelo; G: complejo de Golgi;gpa:gránuloproacrosomal; ln: laguna nuclearcompuestaporheterocro-
matina; m: mitocondria; N: núcleo;pb:puentes intercelulares;pe: centrioloproximal;pi (flecha
blanca): invaginaciónposteriordelnúcleo;pv: vesículasproacrosomales; rf:fibras radiales; sai (cabeza
deflecha blanca): invaginaciónsubacrosomaldelnúcleo; vg: vesículade Golgi. Escalas, A-C:2pm; D:
1pm.
8
BENOMARETAL.: Spermatogenesis ofPernaperna
9
Iberus, 26 (2), 2008
Figure 5. Mature spermatozoa (Spz) ofPernaperna. A: longitudinal section, showing the barrel-like
shaped nucleus and agreatly reduced cytoplasm (doublewhite arrow). B: sagittal section ofmiddle
piece, showing five spherical mitochondria around the diplosome. C: transversal sections offlagella
with nine peripheral doublets and asingle central doublet ofmicrotubules. Abbreviations,A: acro-
some;apa: apicalpartoftheacrosome;ar(whitearrow):axialrod;bpa: basalpartoftheacrosome;cc:
centriolarcomplex;m: mitochondria;ms:pre-membranoidsleeve;N: nucleus;pe:proximalcentriole;
pm: plasmamembrane;tsa: transversalsectionoftheacrosome. Scalebars,A, B: 2pm; C: 0.5 pm.
Figura5. Espermatozoosmaduros (Spz) dePernaperna. A:sección longitudinal, mostrandoelnúcleoen
formadebarrilyuncitoplasmaconsiderablementereducido (dobleflechablanca). B:secciónsagitaldela
partemediana, mostrandocincomitocondriasesféricasalrededordeldiplosoma. C:seccionestransversalesde
flageloscon nuevedobletesperiféricosyunsolodobletecetraldemicrotúbulos. Abreviaturas,A:acrosOma;
apa:parteapicaldelacrosoma;ar (flecha blanca): varillaaxial; bpa:partebasaldelacrosoma; cc: com-
plejodelcentriolo; m: mitocondria; ms: mangapre-membranóide;N: núcleo pe: centrioloproximal;pm:
;
membranaplasmática;tsa:seccióntransversaldelacrosome. Escalas,A, B:2pm;C:0,5pm.
10
