Full text of DOI:10.1163/156854100509150

Nematology, 2000, Vol. 2(3), 285-296
Ultrastructure of sperm development in the free-living marine
nematodes of the family Chromadoridae (Chromadorida:
Chromadorina)
*
1,
2
USHIN
OOMANS
and August C
Vladimir V. Y
1 Institute of Marine Biology, Far East Branch of the Russian Academy of Sciences, Vladivostok 690041, Russia;
2 Universiteit Gent, Instituut voor Dierkunde, K.L. Ledeganckstraat 35, 9000 Gent, Belgium
Accepted for publication: 22 November 1999
Summary –
Spermatogenesis in two species of free-living marine nematodes from the family Chromadoridae (Panduripharynx paciŽca
and Euchromadora robusta) was studied electron-microscopically. The spermatogonia of both species are undifferentiated polygonal
cells with a large nucleus surrounded by a small amount of cytoplasm. In P. paciŽ ca the cytoplasm of spermatocytes contains many Golgi
bodies, cisternae of RER, ribosomes, mitochondria and dense spherical bodies. Filamentous material is accumulated in spermatids,
which contain only mitochondria and a fragmented (or lobed) nucleus devoid of the nuclear envelope. The immature sperm resembles
the late spermatid: its central Ž lamentous area is surrounded by chromatine particles and occasional mitochondria. The immature sperm
plasma membrane forms deep infoldings. Mature spermatozoa from the uterus consist of a small main cell body (MCB) bearing a
prominent pseudopod Ž lled with cytoskeleton Ž laments. The MCB contains a nucleus and mitochondria. Spermatogenesis in E. robusta
(studied only in testes) resembles that described for P. paciŽca, but spermatocytes of E. robusta show much lower metabolic activity
and, as a result, a smaller mass of Ž lamentous material is stored in the spermatids and immature sperm. The spermatozoa of P. paciŽ ca
and the immature sperm of E. robusta have the main ultrastructural features characteristic for nematodes (amoeboid nature, absence
of axoneme, acrosome and nuclear envelope). No aberrant organelles special for many nematode sperm (membranous organelles,
paracrystalline Ž brous bodies and their complexes) were found during sperm development of the chromadorids studied. In this respect
their spermatogenesis differs signiŽ cantly from that in secernents and monhysterids.
Résumé – Ultrastructure du développement du sperme chez les nématodes libres de la famille des Chromadoridae (Chromadorida:
Chromadorina) –
La spermatogenèse a été étudiée en microscopie électronique à transmission chez deux espèces de nématodes
libres marins (Panduripharynx paciŽ ca et Euchromadora robusta) de la famille des Chromadoridae. Les spermatogonies, chez les
deux espèces, sont des cellules indifférenciées avec un grand noyau entouré d’une petite quantité de cytoplasme. Chez P. paciŽca, le
cytoplasme des spermatocytes contient de nombreux corps de Golgi, des cisternae du RER, des ribosomes, des mitochondries et des
corps sphériques denses. Le matériel Ž lamenteux est accumulé dans les spermatides qui contiennent seulement des mitochondries
et un noyau fragmenté (ou lobé) dépourvu d’enveloppe nucléaire. Le sperme immature resemble aux dernières spermatides: son
aire centrale Ž lamenteuse est entourée par des particules de chromatine et quelques mitochondries. La membrane plasmatique du
sperme immature forme des invaginations profondes. Les spermatozoïdes matures, dans l’utérus, sont constitués par un petit corps
cellulaire principal (MCB) portant un pseudopode proéminent rempli de Ž laments de cytosquelette. Le MCB contient un noyau et
des mitochondries. La spermatogenèse chez E. robusta (étudiées seulement au niveau des testicules) ressemble à celle décrite chez
P. paciŽ ca, mais les spermatocytes d’E. robusta sont le siège d’une activité métabolique plus faible et, par conséquent, une masse
plus faible de matériel Ž lamenteux est stockée dans les spermatides et dans le sperme immature. Les spermatozoïdes de P. paciŽ ca
et le sperme immature d’E. robusta ont les mêmes caractéristiques ultrastructurales pour des nématodes (nature amiboïde, absence
d’axonème, d’acrosome et d’enveloppe nucléaire) mais aucune des organelles aberrantes particuliéres à de nombreux spermes de
nématodes (organelles membraneuses, corps Ž breux paracrystallins et leurs complexes) n’ont été identiŽ ées pendant le développement
du sperme chez les Chromadorides étudiés. Par cet aspect, leur spermatogenèse diffère signiŽ cativement de celle des Secernentes et des
Monhysterides.
Keywords –
Euchromadora robusta, Panduripharynx paciŽ ca, spermatogenesis.
* Corresponding author, e-mail: yushinvladimir@hotmail.com
c
®
Koninklijke Brill NV, Leiden, 2000
285

V.V. Yushin & A. Coomans
The nematode sperm are characterised by the absence
of an axoneme, acrosome and nuclear envelope (Foor,
1983; Bird & Bird, 1991). The basic type of nematode
spermatozoon may be described as a bipolar cell with an-
terior pseudopod and posterior main cell body (MCB).
The MCB has a condensed nucleus without nuclear en-
velope surrounded by mitochondria and so called ‘mem-
branous organelles’ (MO), unique organelles, which are
characteristic of most nematode sperm cells and which
open to the surface in mature spermatozoa (Foor, 1983;
Bird & Bird, 1991).
Spermatogenesis and ultrastructure of nematode sperm
has been studied mainly in animal and plant-parasitic
species(Foor, 1983; Bird & Bird, 1991). Publications con-
cerning the sperm structure of free-living marine nema-
todes are limited to seven papers. Five of them deal with
the sperm ultrastructure of the members of the order Eno-
plida (Enoplia) (Wright et al., 1973; Baccetti et al., 1983;
Yushin & Malakhov, 1994, 1998; Turpeenniemi, 1998).
Two papers are devoted to the sperm development in ma-
rine species belonging to the order Monhysterida (Chro-
madoria): Noury-Sraïri et al. (1993) for Sphaerolaimus
hirsutus and Nicholas and Stewart (1997) for Gonionchus
australis. There are no other data concerning the sperm
ultrastructure in Chromadoria, which include mainly free-
living aquatic species of nematodes.
Noury-Sraïri et al. (1993) revealed that spermatogen-
esis in the monhysterid S. hirsutus is close to the pat-
tern of sperm development described in many secernen-
tean species (Foor, 1983). This is true when the develop-
ment of the unique aberrant organelles of nematode sperm
(MO and Ž brous bodies [FB]) is considered. In much the
same way as found in many secernenteans, MO in sper-
matocytes of S. hirsutus derive from the Golgi bodies and
appear as a part of bipartite FB-MO complexes each in-
cluding a crystalline FB associated with membranous cis-
ternae. During spermatogenesis these FB-MO complexes
dissociate into: i) separate MO, which move to the periph-
ery of immature sperm and ii) free FB, which transform
during sperm maturation into ectoplasmic Ž laments of the
cytoskeleton (Noury-Sraïri et al., 1993).
It is interesting to investigate whether or not the se-
cernentean features of spermatogenesis are widespread
amongst Chromadoria. In this paper we describe the de-
velopment of the sperm of two species of free-living
marine nematodes (Panduripharynx paciŽ ca Belogurov,
Dashchenko & Fadeeva, 1985 and Euchromadora robusta
Kulikov, Dashchenko, Koloss & Yuhsin, 1998) both be-
longing to the family Chromadoridae of the order Chro-
madorida. These data are aimed to widen our knowledge
of the spermatogenesis and sperm ultrastructure in Chro-
madoria.
Material and methods
The adult males and females of P. paciŽ ca were col-
lected from silty sand at 1 m depth, the adult males of
E. robusta were extracted from clusters of the bivalve
Crenomytilus grayanus collected at 10 m depth. Both
species were collected at Vostok Marine Biological Sta-
tion of the Institute of Marine Biology (Vladivostok, Rus-
sia) located in Vostok Bay, Sea of Japan.
Live males were cut into pieces each containing a whole
testis. Females of P. paciŽ ca were cut at head and tail
regions to give a piece containing uteri with fertilised
eggs and mature sperm. These specimens were Ž xed for
TEM in 2.5% glutaraldehyde in 0.05 M cacodylate buffer
containing 21 mg/ml NaCl and then postŽ xed in 2%
osmium tetroxide in the same buffer containing 23 mg/ml
NaCl. PostŽ xation was followed by en bloc staining for
12 h in 1% uranyl acetate and then the specimens were
dehydrated in ethanol and acetone series and embedded
in Spurr resin. Thin sections were cut with a Reichert
Ultracut E ultramicrotome, stained with lead citrate and
then examined with a Philips EM 300, JEOL JEM 100B
and JEOL JEM 1010 electron microscopes. The testes
of four males were studied in each species, uteri of
two females of P. paciŽ ca were observed. Thus, the full
cycle of spermatogenesis (up to the mature sperm from
uterus) was studied only in P. paciŽ ca. In E. robusta the
immature sperm from the testes was the Ž nal stage of
sperm development studied.
Results
Males of both species studied (as well as in other
Chromadoridae) have a single (anterior) testis, longitu-
dinal sections through which allows observation of all
the stages of sperm development — from spermatogonia
through immature sperm.
PANDURIPHARYNX PACIFICA
Spermatogonia occur at the distal tip of the testis as
slightly  attened (8 m long, 4 m wide) cells with a
m
m
large irregular nucleus Ž lled with large clumps of chro-
matin (Fig. 1A). The cytoplasm contains mitochondria,
ribosomes, small vesicles and endoplasmic reticulum.
286
Nematology

Spermatogenesis in Chromadoridae
Fig. 1.
Panduripharynx paciŽ ca. A: Spermatogonium; B: Late spermatocyte; C: Late spermatocyte, Ž lamentous material (F) condenses
between outfoldings (ou) of the nuclear envelope (arrowheads). (Abbreviations: Ch = nuclear chromatin; cy = cytoplasm; F = Žlamen-
tous material; fp = Ž lopodia; G = Golgi bodies; i = infoldings of outer membrane; mt = mitochondria; N = nucleus; n = nucleolus;
ou = outfoldings of nuclear envelope; P = pseudopod; RB = residual body; rer = rough endoplasmic reticulum; Scale bar = 1 m.)
m
Vol. 2(3), 2000
287

V.V. Yushin & A. Coomans
The nuclei of spermatocytes are strongly lobed, their
nuclear envelope forms numerous outfoldings deeply pro-
truded into the cytoplasm (Figs 1B, C; 7). The nucle-
oplasm contains patches of chromatin and large nucle-
oli, the cytoplasm comprises many mitochondria, Golgi
bodies, cisternae of rough endoplasmic reticulum (RER),
granular or Ž lamentous spherical bodies and ribosomes.
(Fig. 1C). The late spermatocytes attain a diameter of
The mature spermatozoa (found inside the uteri of the
adult females) are clearly polarised cells (Figs 3B; 7).
They consist of small (only 1-2 m in diam.) MCB
m
bearing a prominent (1-2 m long) pseudopod Ž lled with
m
cytoskeleton Ž laments. The MCB contains the nucleus
and mitochondria, with the latter concentrated mainly at
the base of the pseudopod. Nucleus in the mature sperm
is condensed into a single slightly lobed mass. Plasma
membrane of the mature sperm is without infoldings.
about 12 m.
m
The stage of the spermatid is limited to the period from
the last meiotic division to the detachment of the residual
body (Shepherd, 1981). The spermatids consist of a small
spherical chromatin-containing part connected to the large
residual body by a narrow neck-like cytoplasmic bridge
(Figs 2A, B; 7). The nuclear chromatin in the early sper-
matids is arranged in randomly distributed and intercon-
nected pieces, some of which show Ž lamentous structure
(Fig. 2A). In the late spermatids the nucleus consists of
strongly condensed chromatin particles without any traces
of the nuclear envelope (Fig. 2B).
Several mitochondria, concentrated mostly at the cyto-
plasmic bridge, are the only organelles surrounding the
nuclear chromatin. The cytoplasm of the residual body
is Ž lled with ribosomes, large Golgi bodies, cisternae of
RER, vesicles and clumps of granular material (Fig. 2A,
B).
EUCHROMADORA ROBUSTA
Spermatogonia Ž ll the very distal region of the testis
where mitosis was rarely observed. Spermatogonia are
closely packed cells about 6 m in diam., with 4-5
wide spherical nucleus surrounded by a thin layer of
cytoplasm with ribosomes, mitochondria and transparent
vesicles (Fig. 4A).
m
m
m
Spermatocytes are about 7 m diam. The cytoplasm
m
of late spermatocytes contains mitochondria, occasional
Golgi bodies, cisternae of RER and transparent vesicles
(Figs 4B; 7). No other organelles and inclusions appear in
spermatocytes.
The meiotic telophases during the spermatogenesis of
E. robusta are not fully completed and spermatids develop
in tetrads where four spermatids are shared by a common
residual body. At the Ž nal stages of meiosis, four centres
of the nuclear chromatin condensation with associated mi-
tochondria are formed (Fig. 5A). Later each spermatid
segregates into its own spherical bud connected to the
large residual body (cytophore) by a narrow cytoplasmic
bridge(Figs 5B; 7). Occasional Ž lopodia occur on the sur-
face of the spermatids(Fig. 5B). The process of chromatin
condensation continues and Ž nally small patches are inte-
grated into the solid concave or fragmented nucleus with-
out nuclear envelope (Fig. 6A). Mitochondria immersed
into the Ž lamentous matrix are the only organelles of the
spermatids. The ectoplasm of the late spermatid contains
microtubules, the plasma membrane is arranged into small
outfoldings or Ž lopodia(Fig. 6A). The large residual body
accumulates a mass of ribosomes and numerous cisternae
of RER belonging to the maternal spermatocyte(Fig. 6A).
Immature sperm from the proximal region of the testes
The region of spermatids occupies up to the one third
of the whole length of the testis; this suggests a long
period of spermatid development. This process includes
the growth of the nucleus containing part (from 3.5 to
4-5 m diam.) coinciding with the accumulation of the
m
dense Ž lamentous material. The latter occupies the centre
of the late spermatid shifting the chromatin particles and
mitochondria to the periphery (Fig. 2B).
After detaching from the residual body the central re-
gion of the immature sperm resembles that of the sper-
matid: the central Ž lamentous area is surrounded by chro-
matine particles which seem to be immersed into the Ž la-
mentous matrix (Figs 3A; 7). The peripheral cytoplasm
of the immature sperm contains only occasional mito-
chondria. The sperm plasma membrane is arranged into
deep infoldings which look in some sections like cister-
nae, but all these cisternae are open to the exterior by
‘pores’ (Fig. 3A). Spherical unpolarised immature sperm
are small (about 2.5 m in diam.) rounded cells with
m
slightly irregular contours (Figs 6B, C; 7). The surface
of immature sperm may be arranged into several small
pseudopods with sparse Ž lamentous content, but these
pseudopods do not polarise the cell. It seems that nuclei
of the immature sperm are not uniform in shape. Some
sections demonstrate a cup-shaped form, but on other sec-
4-5 m in diameter devoid of both aberrant (MO and FB)
m
and normal organelles (with exception of mitochondria)
are the Ž nal stage of sperm development in the testes. Ac-
tivation of sperm after insemination changes their struc-
ture signiŽ cantly.
288
Nematology

Spermatogenesis in Chromadoridae
Fig. 2.
Panduripharynx paciŽ ca. A: Early and B: late spermatids are connected to residual body by cytoplasmic bridge (arrowheads),
arrows indicate the cisternae of rough endoplasmic reticulum (For abbreviations see Fig. 1; Scale bar = 1 m).
m
Vol. 2(3), 2000
289

V.V. Yushin & A. Coomans
Fig. 3.
Panduripharynx paciŽ ca. A: Immature sperm (arrowheads: pores connecting outer membrane infoldings with the lumen of
testis); B: Mature (in utero) sperm (For abbreviations see Fig. 1; Scale bar = 1 m).
m
tions the nucleus appears to consist of separate chromatin
particles (Fig. 6B, C). It is conceivable that some of these
sperm nuclei are multilobed. The dense Ž lamentous cy-
toplasm of the immature sperm contains only mitochon-
dria, which are concentrated mainly at the cell periphery
(Fig. 6C). No other organelles (including MO and FB)
were observed in the immature sperm of E. robusta.
out axoneme, acrosome and nuclear envelope around the
strongly condensed nuclear chromatin (Foor, 1983; Bird
& Bird, 1991; Scott, 1996). Sperm of the chromadorids
studied contain only a nucleus and several mitochondria
around it. Mature sperm of P. paciŽ ca stored inside the fe-
male reproductive system are bipolar cells with prominent
pseudopod and compact MCB containing the nucleus and
mitochondria. It is possible, that polarisation and pseudo-
pod formation may occur also in sperm of E. robusta after
their activation in uterus.
Discussion
Other nematode sperm from very different orders, how-
ever, may be more complicated. One of the usual aber-
rant structures appearing in the mature sperm or during
the spermatogenesis of nematodes are MO, FB and their
The spermatozoa of P. paciŽ ca and E. robusta have
the main ultrastructural features characteristics of many
nematodes studied so far: they are amoeboid cells with-
290
Nematology

Spermatogenesis in Chromadoridae
Fig. 4.
Euchromadora robusta. A: Spermatogonium (arrows: thin layer of cytoplasm); B: Late spermatocyte (For abbreviations see
Fig. 1; Scale bar = 1 m).
m
Vol. 2(3), 2000
291

V.V. Yushin & A. Coomans
Fig. 5.
Euchromadora robusta. A: Quartet of spermatids is forming (1, 2 and 3 indicate three of four centres of condensation of nuclear
chromatin [arrowheads] and grouping of mitochondria [mt]); B: Early spermatid connected to residual body (RB) by cytoplasmic
bridge (arrowheads). Note occasional Žlopodia (fp) on the surface of the spermatid. (For abbreviations see Fig. 1; Scale bar: A =
1
m; B = 0,5 m.)
m
m
complexes. These organelle complexes were described in
many nematodes as a necessary component of the differ-
entiating cytoplasm during spermatogenesis(Foor, 1983).
As a rule, the provisory FB-MO complexes appear in the
spermatocytes in the form of membranous vesicles and
cisternae connected with growing paracrystalline FB. The
FB-MO complexes dissociate in the spermatids and give
rise to the free FB (later disintegrated and transformed
into the pseudopod cytoskeleton) and MO, which attach
to the plasma membrane and release their content via
pores (Foor, 1983). This pattern of sperm development
is the usual one for most studied secernentean species
(McLaren, 1973; Shepherd & Clark, 1976; Wolf et al.,
1978; Ugwunna & Foor, 1982; Foor, 1983) and for the
only representative studied from Chromadoria (Noury-
Sraïri et al., 1993).
to some extent the MO of many other nematodes, but we
cannot interpret them as homologous with true MO. The
membrane infoldings in P. paciŽ ca have a distinctly diver-
gent structure and their origin and fate is quite different.
We found them only at the stage of immature sperm, but
usually MO appear as derivatives of Golgi bodies in sper-
matocytes and persist through all the stages of spermio-
genesis including mature sperm from uteri (Foor, 1983;
Bird & Bird, 1991).
Alterations of the basic type of spermatogenesis are
known both for secernentean and adenophorean nema-
todes. Two unusual variations of spermatogenesisin Rhab-
ditia have been described for tylenchids and oxyurids.
In Meloidogyne incognita (Tylenchida) the FB (also the
precursors of pseudopod cytoskeleton) are formed freely
in the cytoplasm of the spermatocytes, no MO were ob-
served (Shepherd & Clark, 1983). The same situation
was described recently in the tylenchid Pratylenchus pen-
etrans (Endo et al., 1998). The Ž nal (in utero) sperm
of this nematode is a bipolar cell with pseudopod and
MCB with the nucleus, mitochondria and remnants of FB.
The chromadorids studied here demonstrate signiŽ cant
deviations from the above mentioned type of sperm or-
ganelle development. Both species have no MO and FB
in all the stages of spermatogenesis. The deep infoldings
of the immature sperm membrane in P. paciŽ ca resemble
292
Nematology

Spermatogenesis in Chromadoridae
Fig. 6.
Euchromadora robusta. A: Late spermatid with strongly condensed nuclear chromatin (arrowheads: cytoplasmic bridge);
B: Immature sperm, section showing a cup-shaped projection of the nucleus; C: Immature sperm, the nucleus on this section looks
like separate chromatin particles (small arrows). (For abbreviations see Fig. 1; Scale bar = 0,5 m.)
m
These spermatozoa resemble the mature sperm of P. paci-
Ž ca. Mention may also be made of Ž lopodia, which were
described in spermatids and sperm of many tylenchids
(Shepherd & Clark, 1983; Cares & Baldwin, 1995; Endo
et al., 1998) and are present in spermatids of the chro-
madorid E. robusta as described above.
The orders of Enoplia show great variability in cyto-
logical events during spermatogenesis. Relatively minor
alterations were described in Enoplus anisospiculus (Eno-
plida), where MO and FB occur during spermatogenesis
and their structure and fate is more or less typical (Yushin
& Malakhov, 1998).
The spermatogenesis of the oxyurid nematode Aspicu-
luris tetraptera proceeds without MO and FB, but its
sperm is not simple in structure and is unique for nema-
todes (Lee & Anya, 1967).
In Xiphinema theresiae (Dorylaimida) the MO and FB
appear in spermatocytes as separate cytoplasmic compo-
nents (Kruger, 1991). Then the MO disappear, but FB
Vol. 2(3), 2000
293

V.V. Yushin & A. Coomans
Fig. 7.
Schematic representation of the sperm development in chromadorid nematodes. A: Panduripharynx paciŽ ca (Spermatocyte [Sc],
note Ž lamentous spherical bodies and outfoldings of the nuclear envelope. Early spermatid is connected to the residual body by the
cytoplasmic bridge [St]. Immature sperm [Is] from testis, nuclear chromatin is immersed into the Ž lamentous matrix, outer membrane
is organised into deep infoldings. Mature bipolar sperm [Ms] from the uterus, the main cell body contains only nucleus and several
mitochondria, pseudopod is Žlled with Žlaments of cytoskeleton); B: Euchromadora robusta. (Sc: with poor synthetic activity; St: with
condensing nucleus is connected to the residual body by cytoplasmic bridge; Is: the set of organelles is reduced to the nucleus and
several mitochondria).
form the peripheral cytoskeleton of the unpolarised sperm
cell.
No FB were observed during the spermatogenesis of
Capillaria hepatica (Trichurida) but the distinctly bipolar
spermatozoa of this nematode are amoeboid and possess
an anterior pseudopod (Neill & Wright, 1973). In the
immature sperm of C. hepatica very simple MO appear
as double membrane-bound vesicles formed by fusion of
small cisternae.
In Gastromermis sp. (Mermithida) the MO-like struc-
tures begin developing from membrane-bound pockets
only in immature spermatozoa (Poinar & Hess-Poinar,
1993). No structures resembling FB were indicated dur-
ing the spermatogenesisof Gastromermis sp., even though
the mature sperm possesses a distinct pseudopod (Foor,
1983).
An extremely simpliŽ ed sperm for Enoplia was de-
scribed in Dioctophyme renale (Dioctophymida) (Foor,
294
Nematology

Spermatogenesis in Chromadoridae
1970, 1983). This polarised sperm has a small pseudopod
but no MO while FB were described in spermatocytes and
spermatids. Moreover, the mature sperm is devoid of mi-
tochondria, which are removed during sperm development
with the cytophore.
Foundation. Authors are grateful to M. Claeys and D. Ba-
turin for the technical assistance.
References
Thus, there are several independent lines of nematode
sperm simpliŽ cation which is manifested in reduction of
typical aberrant organelles — MO and FB. The result
of this trend is illustrated by dioctophymid D. renale
in Enoplia (Foor, 1970, 1983), tylenchid P. penetrans
in Rhabditia (Endo et al., 1998), and two chromadorid
species in Chromadoria (present paper). In this respect
the spermatogenesis of monhysterids which retains all
the phenomena of sperm development in secernents (or
Rhabditia) (Noury-Sraïriet al., 1993; Nicholas & Stewart,
1997) may be referred to as a primitive for Chromadoria.
Despite total absence of FB during spermatogenesis of
P. paciŽ ca the distinct pseudopod Ž lled with Ž laments is
formed in the mature sperm. It means that cytoskeleton
proteins are synthesised in the cell at the stages of sper-
matocytes and spermatids. This is conŽ rmed by signiŽ -
cant metabolic activity of the cells at these stages which
is evidenced by proliferation of the RER and Golgi bod-
ies together with accumulation of dense Ž lamentous ma-
terial. This material Ž lls the central region of the late sper-
matid and transforms into the pseudopod cytoskeleton in
the mature sperm. Pseudopod formation without the in-
termediary condensed stages resembling the FB is not an
unique feature for the sperm studied here since it has been
described in several other nematode species(Lee & Anya,
1967; Neill & Wright, 1973; Foor, 1983; Poinar & Hess-
Poinar, 1993).
The two species of chromadorids studied represent
two different subfamilies of the family Chromadoridae
— Euchromadorinae (E. robusta) and Hypodontholaim-
inae (P. paciŽ ca) (Lorenzen, 1994), but we cannot extend
their pattern of sperm and sperm development throughout
all the order Chromadorida. Light microscopical observa-
tions show great variability of sperm form, size and inter-
nal structure in different groups of the order (Cobb, 1928;
Chitwood & Chitwood, 1977; Riemann, 1983). The ultra-
structural study of this variability can provide the system-
atics of nematodes with new data of phylogenetic value.
ACCETTI
ALLAI
RIMALDI DE IO
ARI
-
B
B
C
, B., D
, A. (1983). The evolution of the nematode spermato-
zoon. Gamete Research 8, 309-323.
, R., G
Z
, S. & M
NARI
IRD
IRD
, J. (1991). The structure of nematodes.
, A.F. & B
San Diego, New York, Boston, London, Sydney, Tokyo &
Toronto, Academic Press, v + 316 pp.
ARES
ALDWIN
, J.G. (1995). Comparative Ž ne struc-
J.E. & B
ture of sperm of Heterodera schachtii and Punctodera chal-
coensis, with phylogenetic implications for Heteroderinae
(Nemata: Heteroderidae). Canadian Journal of Zoology 73,
309-320.
HITWOOD
HITWOOD
, M.B. (1977). Introduction
C
, B.G. & C
to nematology. Baltimore, London & Tokyo, University Park
Press, v + 334 pp.
OBB
C
E
, N.A. (1928). Nemic spermatogenesis. Journal of the
Washington Academy of Sciences 18, 37-50.
NDO
UNKE
ERGIN
, U. & W , W.P. (1998). Spermato-
, B.Y., Z
genesis in the lesion nematode, Pratylenchus penetrans (Ne-
mata, Pratylenchidae). Journal of the Helminthological Soci-
ety of Washington 65, 227-242.
OOR
F
F
K
, W.E. (1970). Spermatozoon morphology and zygote for-
mation in nematodes. Biology of Reproduction Supplements
2, 177-202.
OOR
, W.E. (1983). Nematoda. In: Adiyodi, K.G. & Adiyodi,
R.G. (Eds). Reproductive biology of invertebrates, Vol. 2.
Chichester, USA, John Wiley & Sons, pp. 223-256.
RUGER
DE
W. (1991). Ultrastructure of sperm devel-
, J.C.
opment in the plant parasitic nematode Xiphinema theresiae.
Journal of Morphology 210, 163-174.
EE
NYA
, A.O. (1967). The structure and develop-
L
L
, D.L. & A
ment of the spermatozoon of Aspiculuris tetraptera (Nema-
toda). Journal of Cell Science 2, 537-544.
ORENZEN
, S. (1994). The phylogenetic systematics of free-
living nematodes. London, UK, Ray Society Publications,
162, v + 383 pp.
C
AREN
, D.J. (1973). The structure and the development
M L
of the spermatozoon of Dipetalonema viteae (Nematoda:
Filarioidea). Parasitology 66, 447-463.
EILL
RIGHT
, K.A. (1973). Spermatogenesis in the
N
, B.W. & W
hologonic testis of the trichuroid nematode, Capillaria hepat-
ica (Bancroft, 1893). Journal of Ultrastructure Research 44,
210-234.
Acknowledgements
ICHOLAS
TEWART
, A.C. (1997). Ultrastructure
N
N
, W.L. & S
of Gonionchus australis (Xyalidae, Nematoda). Journal of
Nematology 29, 133-143.
This research was supported by the Russian Foundation
for the Basic Research (grant 96-15-98014), the Univer-
sity of Ghent and the Fellowship support from the Grass
OURY RAÏRI
OURBAULT
USTINE
, N. & J , J.-L.
-S
, N., G
(1993). The development and evolution of actin-containing
Vol. 2(3), 2000
295

V.V. Yushin & A. Coomans
URPEENNIEMI
, T.A. (1998). Ultrastructure of spermatozoa
organelles during spermiogenesis of a primitive nematode.
T
Biology of the Cell 79, 231-241.
in the nematode Halalaimus dimorfus (Nemata: Oxysto-
minidae). Journal of Nematology 30, 391-403.
OINAR
R
ESS OINAR
P
, G.O. J . & H -P , R.T. (1993). The Ž ne
GWUNNA
OOR
, W.E. (1982). Development and
U
, S.C. & F
structure of Gastromermis sp. (Nematoda: Mermithidae)
sperm. Journal of Submicroscopic Cytology and Pathology
25, 417-431.
fate of the membranous organelles in spermatozoa of Ancy-
lostoma caninum. Journal of Parasitology 68, 834-844.
OLF
IRSCH
C NTOSH
, D. & M I , J.R. (1978). Spermato-
W
W
, N., H
IEMANN
R
, F. (1983). Observations on spermatozoa in aquatic
genesis in males of the free-living nematode, Caenorhabditis
elegans. Journal of Ultrastructure Research 63, 155-169.
nematodes. Systematics Association, special volume No 22,
85-93.
RIGHT
OPE
ONES
, W.D. & J , N.O. (1973). The ul-
, K.A., H
COTT
S
S
S
, A.L. (1996). Nematode sperm. Parasitology Today 12,
trastructure of the sperm of Deontostoma californicum, a free-
living marine nematode. Proceedings of the Helminthological
Society of Washington 40, 30-36.
425-430.
HEPHERD
, A.M. (1981). Interpretation of sperm development
in nematodes. Nematologica 27, 122-125.
HEPHERD
USHIN
ALAKHOV
, V.V. (1994). Ultrastructure of
Y
Y
, V.V. & M
LARK
, S.A. (1976). Spermatogenesis
, A.M. & C
sperm cells in the female gonoduct of free-living marine ne-
matodes from genus Enoplus (Nematoda: Enoplida). Funda-
mental and Applied Nematology 17, 513-519.
and the ultrastructure of the sperm and of the male repro-
ductive tract of Aphelenchoides blastophthorus (Nematoda:
Tylenchida, Aphelenchina). Nematologica 22, 1-9.
USHIN
ALAKHOV
, V.V. (1998). Ultrastructure of
, V.V. & M
HEPHERD
LARK
, S.A. (1983). Spermatogene-
S
, A.M. & C
sperm development in the free-living marine nematode Eno-
plus anisospiculus (Enoplida: Enoplidae). Fundamental and
Applied Nematology 21, 213-225.
sis and sperm structure in some Meloidogyne species (Het-
eroderoidea, Meloidogynidae) and a comparison with those in
some cyst nematodes (Heteroderoidea, Heteroderidae). Revue
de Nématologie 6, 17-32.
296
Nematology

Copyright of Nematology is the property of Brill Academic Publishers and its content may
not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's
express written permission. However, users may print, download, or email articles for
individual use.