Idea Transcript
动物学报 49 ( 3) :370～379 , 2003 A ct a Zoologica S i nica
Spermatogenesis , spermiogenesis and spermatozoon in the cestode ( Moniezia expa nsa ) ( Cyclophyllidea , Anoplocephalidae) 3 L I Hai2 Yun ①33 Gerard P. BRENNAN ② David W. HAL TON ② ( ① A ni m al Science College , Sout h Chi na A gricult ural U niversity , Guangz hou 510642 , Chi na) ( ② Medical Biology Cent re , The Q ueen ’s U niversity of Belf ast , Belf ast B T 9 7 BL , U K)
Abstract The processes of spermatogenesis and spermiogenesis , and t he fine structure of t he spermatozoon in t he cyclo2 p hyllidean cestode Moniez ia ex pansa , were examined using a combination of light , scanning and transmission electron mi2 croscopy. Primary spermatogonia were found mainly in t he testes of young proglottids. Primary spermatogonia divided in2 to two secondary spermatogonia and t hereafter incomplete divisions gave rise to 16 primary spermatocytes in t he form of a rosette , wit h all cells sharing a common cytoplasm. Synaptonemal complexes appeared in t he nucleus of t he primary sper2 matocyte and mark t he meiotic prop hase , t he first mature division leading to 32 secondary spermatocytes. Successive sec2 ond mature divisions gave rise to a rosette of 64 spermatids. Spermiogenesis began wit h t he formation of a differentiation zone in t he form of a conical2shaped projection of cytoplasm delimited by a ring of arched membrane. Wit hin t his area , t here were two centrioles and associated spiral rootlets. During spermiogenesis , only one of t he centrioles developed an ax2 oneme t hat grew directly into t he cytoplasmic extension ; t he ot her centriole was aborted. The nucleus elongated and moved into t he cytoplasmic extension. After transformation , t he spermatozoa left t he cytop hore and mature. Any remain2 ing rosettes of spermatids de2differentiated to form an electron2dense residual body. The mature spermatozoon of Moniez ia was filiform , tapered at bot h ends and lacked mitochondria. In cross sections , t he spermatozoon had : ( 1) a plasma mem2 brane and crested2like body ; ( 2) 1 - 4 fields of microtubules beneat h t he plasma membrane. The number of cortical mi2 crotubules varied in different regions ; ( 3) electron2dense granular material in t he cytoplasm ; ( 4) an irregular2shaped nu2 cleus ; ( 5) an axoneme of“9 + 1”pattern lacking a peri2axonemal sheat h. Based on longitudinal sections of t he spermato2 zoon , five regions could be distinguished. Its anterior extremity exhibited an apical cone of electron2dense material , and two crested2like bodies. The cortical microtubles varied in lengt h and follow a 25 - 45 degree helicoidal pat h along t heir lengt hs. They were arranged in 1 - 4 fields in different regions. The axoneme did not reach t he very end of t he anterior extremity ; near t he posterior extremity it formed a free flagellum. The nucleus was arranged in an elongated , compact and irregular cord t hat spirals around t he axoneme. Numerous small electron2dense granules occupied t he cytoplasm in re2 gions Ⅲ to Ⅴ. To t he best of our knowledge , t his is t he first report of a free flagellum in t he spermatozoon of a cestode [ A cta Zoologica S i nica 49 ( 3) : 370 - 379 , 2003 ] . Key words Cestode ( Moniez ia ex pansa) , Spermatogenesis , Spermiogenesis , Spermatozoon , Ultrastructure
扩张莫尼茨绦虫 ( 圆叶目 : 裸头科) 精细胞分化 、 精子形成及精子形态 3 李海云 ①33 Gerard P. BRENNAN ② David W. HAL TON ② ( ①华南农业大学动物科技学院 , 广州 510642) ( ②Medical Biology Centre , The Queen’ s University of Belfast , Belfast B T9 7BL , U K)
Received 28 J une , 2002 , revised 15 Oct . 2002 3 This research was funded by grants from t he National Natural Science Foundation of China (No. 39900109) , t he Natural Science Foundation of Guang Dong (No. 980128) and by t he School of Biology and Biochemistry , Medical Biology Centre , Queen’ s University Belfast , U K.
33 Corresponding aut hor. E2mail : hyli @scau. edu. cn Brief introduction to the f irst author : Female ,Ph. D. Research interests : biology of parasites. ν 2003 动物学报 A cta Zoologica S i nica
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摘 要 本项研究应用光学显微镜 、扫描和透射电子显微镜 , 观察了扩张莫尼茨绦虫的精细胞分化 、精子形成 全过程及精子的精细结构 。扩张莫尼茨绦虫的精细胞分化过程为 : 1) 初级精原细胞主要发生于幼节的睾丸滤泡 中 ; 2) 次级精原细胞发生不完全分裂形成 16 个细胞一簇的初级精母细胞群 , 以共同的中央细胞质相连 ; 3 ) 初 级精母细胞的特征为细胞核中出现联会复合体结构 ; 4 ) 紧接着的第二次成熟分裂 , 产生 64 个由中央细胞质相 连的细胞核较小的精细胞 。精子形成始于精细胞中分化区的形成 , 成熟精子缺乏线粒体 , 具有质膜和冠状体 、1 ～4 个领域排布的质膜下皮层微管 , 细胞质中存在电子致密的颗粒状物质 , 具一个不规则形态的细胞核 , 具有 “9 + 1”类型的轴丝构造 , 缺乏轴丝周围鞘 。从精子的纵切面上可将精子区分为 5 个区段 ( Ⅰ～ Ⅴ区 ) 。在精子 形成过程中 , 中心粒基部出现螺旋形小根结构在寄生虫中为首次报导 ; 成熟精子具有游离鞭毛 , 在绦虫中为首 次发现 [ 动物学报 49 ( 3) : 370～379 , 2003 ] 。 关键词 扩张莫尼茨绦虫 精细胞分化 精子形成 精子 精细结构
M oniez ia ex pansa ( Rudolp hi , 1810 ) has a worldwide dist ribution. It is one of t he largest tape2
ice2cold 4 % glutaraldehyde in cacodylate buffer con2
worms known , measuring up to 6 m in lengt h and
taining 3 % ( w/ v) sucrose p H 714 for 4 h , buffer2
116 cm in widt h , and occurs predominantly in t he in2 testine of sheep , goat s , cattle ( mainly in lambs ,
washed and dehydrated for embedment in JB4 resin. Following polymerisation , sections ( 2 - 4 μm in
kids , calves) and ot her ruminant s. Rat her t han caus2 ing direct stock losses , infection wit h t he worm
t hickness) were cut and air2dried on slides for stain2 ing wit h toluidine blue or periodic acid2Schiff ( PAS) .
brings about indirect losses , such as reduced weight
Ot her samples ( n > 20) were fixed overnight in a 3∶ 1
gain , host malnut rition and anaemia , blockage , di2
mixt ure of 4 % glutaraldehyde and 015 % aqueous os2
gestive dist urbance , and sometimes diarrhoea or con2 stipation. It is especially harmf ul to young animals
mium tet roxide for examination by scanning elect ron microscopy ( SEM ) . Following fixation and several
under 9 mont hs of age.
changes in cacodylate buffer2wash , specimens were
20 ) for light microscopic examination were fixed in
Fecundity is an important characteristic of para2
dehydrated t hrough a graded acetone series , critical2
sites and t his is especially t rue of M oniez ia ex pansa.
point dried in CO2 using an Emscope CPD 750 criti2
The worm has two set s of reproductive organs in each
cal2point dryer and mounted on aluminium st ubs ,
proglottid , and t he mechanism of reproduction is bot h
coated wit h gold/ palladium in an Emitech K550 sput2
of biological interest and of economic significance.
ter2coater and viewed on a J EOL J SM235CF scanning
For t his reason , we conducted an ult rast ruct ural matozoon in M oniez ia ex pansa to provide baseline in2
elect ron microscope at 10 - 15 kV . Finally , samples ( n > 10 ) for t ransmission elect ron microscopy ( TEM) were fixed immediately as for JB4 for 4 - 5
formation on reproductive develop ment in t his worm.
h , followed by two 015 h washes in cacodylate buffer
We hope t hat t he result s will give a better insight into
and stored for 24 h in cacodylate buffer prior to post2
t he worm’s reproductive st rategy and t hus be of value
fixation in 1 % aqueous osmium tet roxide for 2 h.
in population cont rol st udies , as well as provide data
Specimens were t hen dehydrated t hrough an et hanol
st udy of spermatogenesis , spermiogenesis and sper2
of p hylogenetic value.
series and orientated appropriately prior to embed2
1 Materials and met hods
ment in Epon 812 resin. Ult rat hin sections were cut
Adult specimens of M oniez ia ex pansa were col2
and collected on uncoated 2002mesh copper grids , stained wit h alcoholic uranyl acetate ( 15 min ) and
lected f rom t he intestines of sheep slaughtered at La2
aqueous lead cit rate ( 8 min ) , and examined using a
gan abattoir , near Belfast , U K. Worms were placed
J EOL 1002CX elect ron microscope operated at 100
in warm 019 % p hysiological saline and maintained at
kV .
35 - 37 ℃ in a vacuum flask for t ransport to t he labo2 ratory. There t hey were quickly cut into small ( ap2
2 Result s
proximately 015 cm long ) pieces. Specimens ( n >
211 Spermatogenesis and spermiogenesis
372
动 物 学 报
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Primary spermatogonia were most evident in t he
t ure division. Occasionally , two cent rioles arranged at
testes of young proglottids and located at t he perip h2
right angles were found in t he perinuclear cytoplasm.
ery of t he testes. As t he proglottid developed , prima2
Large numbers of
ry spermatogonia divided twice forming secondary and
unattached ribosomes and rough endoplasmic reticu2
tertiary spermatogonia. Tertiary spermatogonia t hen
lum were found t hroughout t he cytoplasm. Element s
underwent incomplete division resulting in an 82celled
of a Golgi apparat us were found at t his stage.
mitochondria , polyribosomes ,
rosette of primary spermatocytes joined at t heir bases by common cytoplasm in t he form of t he cytop hore. The eight primary spermatocytes underwent a syn2 chronous division to form a rosette of 16 secondary spermatocytes. Thirty two spermatids arose by a sec2 ond mat ure division of secondary spermatocytes and t hese subsequently t ransformed into t hread2shaped mat ure spermatozoa. Event ually , t he spermatozoa be2 came detached , leaving t he remaining common cyto2 plasm as a residual body. All of t he gradual t ransi2 tional changes in fine st ruct ure which occured during spermatogenesis in M oniez ia ex pansa were briefly summarized as follows. 21111 Primary spermatogonia ( Fig. 1 : 1 and Plate
Ⅰ: 2 ) Primary spermatogonia were morp hologi2 cally characterised by t heir somewhat irregular shape , and were located at t he perip hery of t he testes. The nucleus was large and generally round , wit h a few clumps of heterochromatin ; t he nucleoplasm was granular. The cytoplasm was relative elect ron2dense and largely occupied by numerous small ovoid mito2
Fig. 1 Diagrammatic interpretation of spermatogenesis and spermiogenesis in the cestode ( Moniezia expa nsa ) 1. Primary spermatogonia 2. Secondary spermatogonia 3. Pri2
chondria , scattered populations of polyribosomes and
mary spermatocyte 4. Secondary spermatocyte 5. Spermatid 6.
ribosomes and linear arrays of sparse endoplasmic
Onset of spermiogenesis showing a differentiation zone , note spiral
reticulum. No evidence of a Golgi apparat us was
rootlets (arrow) 7. Spermiogenesis as seen by light microscopy ,
found at t his stage. 21112 Secondary spermatogonia ( Fig. 1 : 2 and Plate Ⅰ: 2 ) Secondary spermatogonia were dis2 t ributed wit hin t he outer layer of primary spermato2 gonia. Most of t hem were sp herical or elliptical in
showing large numbers of t hread2shaped spermatozoa forming from a rosette of spermatids N : Nucleus n : Nucleolus m : Mitochondrion S : Synaptonemal complex G: Golgi complex GER : Granular endoplasmic reticulum c : Centriole R s : Rosette Am : Arched membrane
was similar to t hat of primary spermatogonia but less
21114 Secondary spermatocytes ( Fig. 1 : 4 and Plate Ⅰ: 1 , 5 ) The body of t he secondary sper2
elect ron2dense.
matocyte was distinguished by t he arrangement of it s
21113 Primary spermatocytes ( Fig. 1 : 3 and Plate Ⅰ: 1 , 3 , 4) Primary spermatocytes were morp ho2
ranged just beneat h t he plasma membrane and perinu2
shape , wit h large round nuclei. Their fine st ruct ure
logically irregular wit h a round nucleus and could be i2
mitochondria in two fields : cortical mitochondria , ar2
dentified by t he presence of a nuclear synaptonemal
clear mitochondria close to t he nuclear envelope. 21115 Spermatids ( Fig. 1 : 5 and Plate Ⅰ: 1 , 6 )
complex , indicating pairing of homologous chromo2
Spermatids were located at t he side of t he rosette wit h
somes during t he meiotic prop hase of t heir first ma2
t heir cytoplasm connected to t he common cytop hore.
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Li Hai2 Yun et al . : Spermatogenesis , spermiogenesis and spermatozoon in t he cestode
373
toplasm. The Golgi apparat us was well developed at
①) , roughly 200 nm - 450 nm in widt h , corre2 sponded to t he anterior ext remity of t he spermato2 zoon . It was capped by an apical cone of elect ron2 dense material wit h an approximate widt h of 250 nm and a lengt h of about 300 nm. This region presented
t his stage , wit h membraneous stacks and associated
two helicoidal crested2like bodies associated wit h t he
vesicles.
subjacent microt ubules. The t hickness of t he crested2
21116 Spermiogenesis ( Fig. 1 : 6 , 7 and Plate Ⅱ: 7 - 10 ) Spermiogenesis began in each spermatid
like bodies decreased gradually towards t he beginning of region Ⅱ. An axoneme of t he“9 + 1”pattern was
wit h t he formation of a differentiation zone , limited
located cent rally but did not reach t he very anterior
by sub2membranous cortical microt ubules , in t he
end. It lacked a peri2axonemal sheat h and was sur2
form of a conical2shaped projection of cytoplasm bor2
rounded by a t hin layer of slightly elect ron2dense cy2
dered by a ring of arched membrane. In t he conical
toplasm. The cortical microt ubules spiralled at an an2
area , t here were two cent rioles and associated spiral
gle of about 25 - 45 degrees to t he longit udinal axis of
rootlet s; t he two cent rioles were at right angles to
t he spermatozoon. In longit udinal sections , and in
each ot her. During spermiogenesis , only one of t he
t he surface layers of t he spermatozoon , cortical micro2
cent rioles develops an axoneme. This grew directly
t ubules formed a discontinuous layer of elect ron2dense
into t he cytoplasmic extension ; t he ot her cent riole
appearance. In cross sections , t hey were arranged in
was aborted. The cortical microt ubules rapidly elon2
They had small , round nuclei located in t he cent re of t he cell bodies , wit h large numbers of mitochondria , polyribosomes , unattached ribosomes and rough en2 doplasmic reticulum dist ributed t hroughout t heir cy2
gated and spiralised. The nucleus underwent consid2
two fields associated wit h t he crest2like bodies. Region Ⅱ ( Fig. 2 : Ⅱ, ②; Plate Ⅱ: 11 , 13 -
erable elongation , became filiform , and moved into
16 : ②) was f rom 450 - 500 nm in breadt h , it lacked
t he cytoplasmic extension. Later , as t he nucleus con2
crest2like bodies but exhibited helically2arranged cor2
tinued it s migration , two crest2like bodies appeared in
tical microt ubules , seen as a continuous layer of dense
t he anterior part of t he spermatid. Concurrently ,
submembranous material , and whose numbers were
elect ron2dense granules condensed and progressively
increased. The axoneme was seated in t he cent ral
dispersed towards t he distal areas of t he spermatid.
area and was surrounded by a fine layer of elect ron2lu2
Towards t he end of spermiogenesis , amorp hous elec2
cent cytoplasm.
t ron2dense material condensesd at t he anterior ex2 origin of t he apical cone of elect ron2dense material
Region Ⅲ ( Fig. 2 : Ⅲ, ③; Plate Ⅱ: 12 , 13 , 15 : ③) was f rom 500 - 700 nm in widt h. It was characterised by t he presence of an axoneme en2
presented in t he anterior end of t he mat ure spermato2
veloped by a t hick layer of elect ron2lucent cytoplasm
zoon. Finally , t he ring of arched membrane narrowed
wit hin which t here were numerous granules of elec2
and const ricted such t hat t he mat ure spermatozoon
t ron2dense material resembling in appearance granules
t remity of t he spermatozoon. This was probably t he
became detached f rom t he residual cytoplasm. The
of glycogen. The cytoplasm was surrounded by spi2
latter remained and condensed as an elect ron2dense
raled cortical microt ubules , as in region Ⅰ. The
residual body.
number of cortical microt ubules were at a maximum
212 Fine structure of the spermatozoon
at t his site. No nucleus was apparent in t his region. Region Ⅳ ( Fig. 2 : Ⅳ, ④; Plate Ⅱ: 11 - 14 ,
Examination of an individual spermatozoon f rom anterior to posterior portion revealed five distinct re2 gions ( Ⅰto Ⅴ) . While no marked topograp hical dis2
16 : ④) was f rom 700 - 500 nm in widt h. This re2
continuities in morp hology between t he five regions
which was coiled in an irregular spiral around t he cen2
were evident using SEM , t hey exhibited distinctive
t ral axoneme. It appeared as a compact cord and
ult rast ruct ural feat ures when viewed by TEM. Region Ⅰ ( Fig. 2 : Ⅰ, ①; Plate Ⅱ: 9 , 11 :
showed a different morp hology in diverse cross2sec2
gion was characterized by t he presence of a nucleus ,
tions. Numerous elect ron2dense granules were dis2
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49 卷
during spermatogonial division in parasitic platy2 helmint hs is still unknown ( Rybicka , 1966 ) . The first detailed st udy on spermatogenesis in M oniez ia was conduced by Child ealy t his cent ury using light microscopy. In t his original st udy , spermatogonial division was interpreted as amitosis. Later , Young claimed t hat spermatogonial division involved“chro2 midial ext rusion ”. The 1960 ’s wit nessed t he int ro2 duction and use of t he elect ron microscope in t he field of parasitology , including ult rast ruct ural st udies of spermatogenesis in cestodes. However , despite t his advance in investigative technology t he nat ure of cell division in t he spermatogonia of cestodes remains un2 clear.
Pashchenko once claimed t hat
in
Tae2
niarhy nchus sagi nat us , spermatogonia divide by bot h
mitosis and amitosis ( Rybicka , 1966 ) . Nonet he2 less , many workers ( including Tian et al . , 1998a , Fig. 2 Schematic of a mature spermatozoon of Moniezia expa nsa , showing f ive distinct regions
( Ⅰ2 Ⅴ or ①2 ⑤) from anterior to posterior
b ; Mahendrasingam et al . , 1989 ; Rosario , 1964 ; Xylander , 1989 ) mentioned t hat mitosis occurs , al2 t hough no clear images of t he mitotic p hases have
Ac : Apical cone Ax : Axoneme cb : Crested2like body cm : Cor2
been presented. We did not find eit her mitosis or
tical microtubules G: Granules of glycogen pm : Plasma mem2
amitosis p hases. The main reason for t his may be t hat
brane N : Nucleus F : Flagellum Pse : Posterior spermatozoon
t he dividing stage is very brief compared wit h t he in2
extremity
terp hase. From a t heoretical point of view , bot h mi2
t ributed around t he axoneme in t he elect ron2lucent cytoplasm. Out side t he cytoplasm , t here was still a layer of spiraled cortical microt ubules , which were ar2 ranged in 2 - 4 fields. Region Ⅴ ( Fig. 2 : Ⅴ, ⑤; Plate Ⅱ: 13 , 14 , 16 : ⑤) was less t han 500 nm in widt h. It corre2 sponded to t he posterior end of t he spermatozoon. In t his region t he axoneme appeared at t he side of t he
tosis or amitosis could occur in cestodes. Mitosis , as previously mentioned , has been recorded in spermato2 gonial division in many animals , especially in verte2 brates and insect s. Cestodes represent part of a large p hylum of lower Bilateria invertebrates , and as such it is possible t hat mitosis takes place in t heir sper2 matoginal divisions. Amitosis occurs mainly in proto2 zoans and has also been found to take place in t he for2 mation of plant microspores ( Han , 2001) . The sper2
spermatozoon in some cross sections , while in ot her
matogenic stage in animal ontogenesis is roughly e2
sections no axonemes could be seen. From all t hese
quivalent to t he protozoan stage in animal p hylogene2
observations , it could be deduced t hat t he axoneme
sis. It is possible , t herefore , t hat amitosis could also
grew out of t he spermatozoon body and formed a f ree
occur in t he spermatogonial divisions of cestodes. To
flagellum.
confirm t his , f urt her detailed st udies are needed.
3 Discussion
312 Spermiogenesis J ustine ( 1998 ) summarized most literat ures on
311 Spermatogenesis
spermiogenesis in
cestodes
and
described
four
It is widely believed t hat mitosis occurs during
spermiogenesis types. Type Ⅰ, wit h two flagella ;
t he process of spermatogonial division in vertebrates
during spermiogenesis t here is flagellar rotation and
and insect s. Whet her mitosis or amitosis takes place
proximo2distal f usion ; occurring in some cestodes of
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Li Hai2 Yun et al . : Spermatogenesis , spermiogenesis and spermatozoon in t he cestode
t he orders : Tet rap hyllidea , Onchobot hriidea , Proteo2 cep halidea , Trypanorhyncha and Pseudop hyllidea ; Type Ⅱ, wit h only one flagellum ; spermiogenesis ac2 companied by flagellar rotation and proximo2distal f u2 sion ; found in some cestodes of t he orders : Tet ra2
375
in region Ⅳinstead of in region Ⅲ, as in t he sperma2 tozoon of Di pyli di u m cani n u m ( Miquel et al . , 1997) , A noplocephaloi des dent ate ( Miquel et al . , 1998) and R aillieti na ( R aillieti na ) t u netensis ( Bg et al . , 1994) .
p hyllidea , Phyllobot hriidae , Caryop hyllidea and some
Spermiogenesis and sperm ult rast ruct ure have
Tet rabot hriidea cestodes wit hout an intercent riolar
been used successf ully as a p hylogenetic character in
body ; Type Ⅲ, wit h only one flagellum ; spermio2
cestodes. Moreover , cytochemical and immunocyto2
genesis involves no flagellar rotation but proximo2dis2
chemical met hods , which could be employed to t race
tal f usion does take place ; claimed to occur in some
metabolic event s during spermatogenesis , could prove
Cyclop hyllidea cestodes ( genera : Nem atot aenia , M at hevot aenia , R aillieti na ) ; Type Ⅳ, wit h only
f ruitf ul in developing new approaches in t he cont rol of
one flagellum ; during spermiogenesis neit her flagellar
parasites.
rotation nor proximo2distal f usion was observed in some cestodes of t he order : Cyclop hyllidea ( Anoplo2
Acknowledgements All of t he work recorded here
cep halidae , Thysaniezia , Hymenolepis , Aporina) .
was undertaken at t he School of Biology and Bio2
reproduction of t his economically important group of
Spermiogenesis in M oniez ia ex pansa is similar
chemist ry , Medical Biology Cent re , Queen’s U niver2
to type Ⅳ, but differs in showing spiral rootlet s at t he bottom of t he two cent rioles ( very different to t he
sity Belfast , U K. Appreciation is extended to George
st riated rootlet s found in t rematodes and in some ot h2
st udent s : L ucinda Campbell , Susan Robert s , Michael
er cestodes ) and might connect to t he nucleus.
Stewart , Liam Halferty and Myles Meaney for t heir
Whet her t hey resemble t he rootlet filament s of cent ri2 oles in protozoans which connect to t he nucleus ( and
kind help .
are t herefore cont rolled by nuclei) is unclear and war2 rant s f urt her st udy. 313 Spermatozoon of Moniezi a expa nsa Concerning t he morp hology of t he spermatozoon in M oniez ia ex pansa. Swiderski ( 1968 ) stated t hat t he spermatozoon is a very elongate , spindle2shaped
McCart ney for technical assistance and to graduate
References Bg , C. T. and B. Marchand , 1992 ∗ tude ultrastructurale sur le spermatozogde de Moniezia ex pansa et M . benedeni ( Cestoda , Cyclophyllidea , Anoplocephalidae ) .
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Com p . ( Paris) 67 : 111 - 115.
Bg , C. T. and B. Marchand 1994 Ultrastructure of t he spermiogen2 esis and t he spermatozoon of Raillieti na ( Raillieti na) t unetensis
cell , twisted in a loose spiral. In our st udy , t he sper2
(Cyclophyllidea , Davaineidae) , intestinal parasite of turtle doves in
matozoon is filiform , it s twisted , loose spiral appear2
Senegal. I nt . J . Parasitol . 24 : 237 - 248.
ance may be caused by t he movement of t he sperma2 tozoon. In our work , at least 37 sections show t he spermatozoon in st raight orientation. Bg et al . ( 1992 ) had shown for t he first time t hat t he exis2 tence of an axoneme which does not reach t he ex2 t remities of t he spermatozoon in M oniez ia ex pansa and M .
benedeni . They divided t he spermatozoon
Han , Y. R. 2001 Molecular Cell Biology , Second Edition. Beijing : Science Press , 505 - 506. J ustine , J . L . 1998 Spermatozoa as phylogenetic characters for t he Eucestoda. J . Parasitol . 84 (2) : 385 - 408. Miquel , J . and B. Marchand 1997 Ultrastructure of t he spermato2 zoon of Di pyli di u m cani nu m ( Cestoda , Cyclophyllidea , Dilepidi2 dae) , intestinal parasite of Canis f amiliaris. Parasitol . Res . 83 : 349 - 355. Miquel , J . and B. Marchand 1998 Ultrastructure of t he spermio2
into five distinct regions and described t he nucleus as
genesis and t he spermatozoon of A noplocephaloi des dentata ( Ces2
appearing in region Ⅲ. We also found t hat t he ax2
toda , Cyclophyllidea , Anoplocephalidae) , an intestinal parasite of
oneme does not extend to t he very anterior end. Moreover , before it reaches t he posterior ext remity , it grows out of t he body of t he spermatozoon in region
Ⅴ and becomes a f ree flagellum. The nucleus appears
Arvicolidae rodents. J . Parasitol . 84 : 1 128 - 1 136. Mahendrasingam , S. , I. Fairweat her and D. W. Halton 1989 Spermatogenesis and t he fine structure of t he mature spermatozoon in t he free proglottis of T rilocularia acant hiaev ulgaris ( Cestoda , Tetraphyllidea) . Parasitol . Res . 75 : 287 - 298.
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Swiderski , Z. 1968 The fine structure of t he spermatozoon of sheep tapeworm , Moniezia ex pansa ( Rud. , 1810 ) Cyclophyllidea , Anoplocephalidea. Zool . Pol . 18 : 475 - 486. Rosario , B. 1964 An electron microscope study of spermatogenesis in cestodes. J . Ult rast ruct . Res . 11 : 412 - 427. Rybicka , K. 1966. Embryogenesis in cestodes. A dv . i n Para2 sitol . 4 : 107 - 186.
Tian , X. , L . Yuan , Y. Li , X. Huo , X. Han , M. Xu , M. L u , J . Dai and L . Dong 1998a Ultrastructural observation on sperma2
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tocytogenesis in taeniid cestodes. Chi . J . Parasitol . Para. Dise. 16 : 209 - 212. Tian , X. , L . Yuan , Y. Li , X. Huo , X. Han , M. Xu , M. L u , J . Dai and L . Dong 1998b Ultrastructural observation on t he transformation of t he spermatozoon in spermatogenesis of taeniid cestodes. Chi . J . Parasitol . Para. Dise. 16 : 269 - 273. Xylander , W. E. R. 1989 Ultrastructural studies on t he reproduc2 tive system of Gyrocotylidea and Amphilinidea ( Cestoda) : sper2 matogenesis , spermatozoa , testes and vas deferens of Gy rocotyle. I nternational J . Parasitol . , 19 : 897 - 905.
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Li Hai2 Yun et al . : Spermatogenesis , spermiogenesis and spermatozoon in t he cestode
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Explanations of plates Plate Ⅰ Transmission elect ron micrograp hs of spermatogenesis in t he cestode ( M oniez ia ex pansa ) 1. Section of testicular follicle , showing cells in different stages of development ×3 032 Scale = 2 μm 2. A part of a follicle showing primary ( Psg) and secondary spermatogonia ( Ssg) × 6 885 Scale = 1 μm 3. Primary spermatocytes ( Psc) showing synaptonemal complex in t he nuclei and centrioles (C) arranged at right angles in t he cytoplasm near t he nu2 cleus of a cell ×6237 Scale = 1 μm 4. High magnification of a synaptonemal complex ×22 000 Scale = 015 μm 5. Secondary spermatocytes ( Ssc) , which are characterized by t he arrangement of mitochondria ( m) , connect to t he common cytophore ×3 611 Scale = 2 μm 6. A cytophore (Cp) . Note t he spematid connected to t he cytophore by a narrow cytoplasmic stalk at bottom right ×5 029 Scale = 2 μm
Plate Ⅱ Transmission elect ron micrograp hs of spermiogenesis and spermatozoa in t he cestode ( M oniez ia ex pansa ) 7. Longitudinal section of a differentiation zone , showing spiral rootlets (arrow) connecting to centrioles and t he presence of spiral cortical microtubules (Cm) ×15 810 Scale = 015 μm 8. Spermiogenesis. Longitudinal section of a differentiation zone , showing an axoneme (Ax) growing out of a centriole (C) directly into t he cytoplas2 mic extension. The nucleus (N) shows a typical conical shape ×17 655 Scale = 015 μm 9. Appearance of crest2like body (Cb) followed by a constriction of t he ring of arched membranes. Amorphous electron2dense material condenses at t he level of anterior extremity of t he spermatozoon forming t he apical cone (Ac) of t he spermatozoon ×25 263 Scale = 015 μm 10. Mature spermatozoa detach from t he residual cytoplasm , which remains in t he testicular follicle as an electron2dense residual body ( Rb) ×4 620
Scale = 2 μm 11. Cross sections of regions Ⅰ: ①, Ⅱ: ② and Ⅳ: ④ ×20 628 Bar = 015 μm 12. Cross sections of regions Ⅲ: ③ and Ⅳ: ④ ×17 778 Bar = 015 μm 13. Cross sections of regions Ⅱ to Ⅴ ( ②- ⑤) ×22 620 Bar = 015 μm 14. Cross sections of regions Ⅳ: ④and Ⅴ: ⑤. Longitudinal sections of regions Ⅳ: ④and Ⅴ: ⑤. Some free flagella ( F) are among ×13 415
Bar = 015 μm 15. Longitudinal sections of regions Ⅱ: ② and Ⅲ: ③ ×11 765 Bar = 1 μm 16. Longitudinal sections of regions Ⅱ: ②, Ⅳ: ④ and Ⅴ: ⑤ ×19 670. Bar = 015 μm Am : Arched membrane Cp : Cytophore m : Mitochondrion N : Nucleus Psc : Primary spermatocyte R : Residual cytoplasm Rb : Residual body Ssc : Secondary spermatocyte Spd : Spermatid S : Spermatozoon
L I Hai2 Yun et al . : Spermatogenesis , spermiogenesis and spermatozoon in t he cestode ( M oniez ia ex pansa ) ( Cyclop hyllidea , Anoplocep halidae)
Explanation at t he end of t he text
Plate Ⅰ
L I Hai2 Yun et al . : Spermatogenesis , spermiogenesis and spermatozoon in t he cestode ( M oniez ia ex pansa ) ( Cyclop hyllidea , Anoplocep halidae)
Explanation at t he end of t he text
Plate Ⅱ