Ultrastructure of the spermatozoon of Bothriocotyle sp. (Cestoda: Bothriocephalidea), a parasite of Schedophilus velaini (Sauvage, 1879) (Perciformes: Centrolophidae) in Senegal

The mature spermatozoon of Bothriocotyle sp. is filiform and tapered at both extremities. It possesses 2 axonemes of unequal length, showing the 9 + "1" pattern of Trepaxonemata. The anterior extremity exhibits a crest-like body. Thereafter, the crest-like body disappears, and the first axoneme is surrounded by a ring of cortical microtubules (about 27 units) that persist until the appearance of the second axoneme. This ring of cortical microtubules is characteristic only for species of Bothriocephalidea and represents a very useful phylogenetic character. The spermatozoon cytoplasm is slightly electron-dense and contains numerous electron-dense granules of glycogen in several regions. The anterior and posterior extremities of the spermatozoon lack cortical microtubules. The posterior extremity of the spermatozoon of Bothriocotyle sp. possesses a nucleus and a disorganized axoneme, which also characterizes spermatozoa of the Echinophallidae studied to date.     

Ultrastructural study of spermiogenesis and the spermatozoon of the proteocephalidean cestode Barsonella lafoni de Chambrier et al., 2009, a parasite of the catfish Clarias gariepinus (Burchell, 1822) (Siluriformes, Clariidae)

Spermiogenesis in the proteocephalidean cestode Barsonella lafoni de Chambrier et al., 2009 shows typical characteristics of the type I spermiogenesis. These include the formation of distal cytoplasmic protrusions forming the differentiation zones, lined by cortical microtubules and containing two centrioles. An electron-dense material is present in the apical region of the differentiation zone during the early stages of spermiogenesis. Each centriole is associated to a striated rootlet, being separated by an intercentriolar body. Two free and unequal flagella originate from the centrioles and develop on the lateral sides of the differentiation zone. A median cytoplasmic process is formed between the flagella. Later these flagella rotate, become parallel to the median cytoplasmic process and finally fuse proximodistally with the latter. It is interesting to note that both flagellar growth and rotation are asynchronous. Later, the nucleus enlarges and penetrates into the spermatid body. Finally, the ring of arching membranes is strangled and the young spermatozoon is detached from the residual cytoplasm.The mature spermatozoon presents two axonemes of the 9 + ‘1’ trepaxonematan pattern, crested body, parallel nucleus and cortical microtubules, and glycogen granules. Thus, it corresponds to the type II spermatozoon, described in almost all Proteocephalidea. The anterior extremity of the gamete is characterized by the presence of an apical cone surrounded by the lateral projections of the crested body. An arc formed by some thick and parallel cortical microtubules appears at the level of the centriole. They surround the centriole and later the first axoneme. This arc of electron-dense microtubules disorganizes when the second axoneme appears, and then two parallel rows of thin cortical microtubules are observed. The posterior extremity of the male gamete exhibits some cortical microtubules. This type of posterior extremity has never been described in proteocephalidean cestodes. The ultrastructural features of the spermatozoon/spermiogenesis of the Proteocephalidea species are analyzed and compared.     

Ultrastructure of the spermatozoon of Anomotaenia quelea (Mettrick, 1961) (Cestoda,Cyclophyllidea, Dilepididae), an intestinal parasite of Quelea quelea (Aves,Ploceidae) in Senegal

The mature spermatozoon of Anomotaenia quelea exhibits an apical cone of electron-dense material and two helicoidal crest-like bodies. The apical cone near its base is surrounded by a lucent cytoplasm and a spiraled layer of cortical microtubules. The crest-like bodies are of different lengths, spiraled and make an angle of 30–40° to the hypothetical spermatozoon axis. The axoneme is of the 9 + ‘1’ trepaxonematan pattern and is surrounded by a periaxonemal sheath of electron-dense material. The cytoplasm contains in regions III and IV numerous electron-dense granules situated between the periaxonemal sheath and the cortical microtubules. The posterior extremity of the spermatozoon of A. quelea exhibits a nucleus and a disorganized axoneme and cortical microtubules. This type of posterior extremity of the mature spermatozoon has never been described previously in a Dilepididae. Similarly, two crest-like bodies have not been observed before in a dilepidid cestode.     

Ultrastructure of the spermatozoon of Anomotaenia quelea (Mettrick, 1961) (Cestoda,Cyclophyllidea, Dilepididae), an intestinal parasite of Quelea quelea (Aves,Ploceidae) in Senegal

The mature spermatozoon of Anomotaenia quelea exhibits an apical cone of electron-dense material and two helicoidal crest-like bodies. The apical cone near its base is surrounded by a lucent cytoplasm and a spiraled layer of cortical microtubules. The crest-like bodies are of different lengths, spiraled and make an angle of 30–40° to the hypothetical spermatozoon axis. The axoneme is of the 9 + ‘1’ trepaxonematan pattern and is surrounded by a periaxonemal sheath of electron-dense material. The cytoplasm contains in regions III and IV numerous electron-dense granules situated between the periaxonemal sheath and the cortical microtubules. The posterior extremity of the spermatozoon of A. quelea exhibits a nucleus and a disorganized axoneme and cortical microtubules. This type of posterior extremity of the mature spermatozoon has never been described previously in a Dilepididae. Similarly, two crest-like bodies have not been observed before in a dilepidid cestode.     

Spermiogenesis and the spermatozoon ultrastructure of Robphildollfusium fractum (Digenea: Gyliauchenidae), an intestinal parasite of Sarpa salpa (Pisces: Teleostei)

Spermiogenesis in Robphildollfusium fractum begins with the formation of a differentiation zone containing: two centrioles, each bearing striated rootlets, nucleus, several mitochondria and an intercentriolar body constituted by seven electron-dense layers. The two centrioles originate two free flagella growing orthogonally to the median cytoplasmic process. Later, the free flagella rotate and undergo proximodistal fusion with the median cytoplasmic process. Nuclear and mitochondrial migrations occur before this proximodistal fusion. Finally, the young spermatozoon detaches from the residual cytoplasm after the constriction of the ring of arched membranes. The spermatozoon of R. fractum exhibits two axonemes of different length of the 9 + ‘1’ trepaxonematan pattern, nucleus, two mitochondria, two bundles of parallel cortical microtubules, external ornamentation of the plasma membrane, spine-like bodies and granules of glycogen. Additionally, a shorter axoneme, which does not reach the nuclear region, the presence of an electron-dense material in the anterior spermatozoon extremity and the morphologies of both spermatozoon extremities characterize the mature sperm of R. fractum.     

Spermatological characters of the pseudophyllidean cestode Bothriocephalus scorpii (Müller, 1776)

Spermiogenesis of Bothriocephalus scorpii (Cestoda, Pseudophyllidea) includes an orthogonal development of two flagella, followed by a flagellar rotation and a proximo-distal fusion with the median cytoplasmic process. The fusion occurs at the level of four attachment zones. The presence of dense material in the apical region of the differentiation zone in the early stage of spermiogenesis appears to be a characteristic feature for the Pseudophyllidea. The mature spermatozoon possesses two axonemes of 9+"1" pattern of the Trepaxonemata, nucleus, cortical microtubules, electron-dense granules and crested body. The anterior part of the gamete exhibits a centriole surrounded by electron-dense tubular structures arranged as incomplete spiral. When the crested body disappears, the electron-dense tubular structures are arranged into a ring encircling the axoneme. The electron-dense tubular structures and their arrangement appear to be a specific feature for the clade "Bothriocephalidea". The organization of the posterior extremity of the gamete with the nucleus is described for the first time in the Pseudophyllidea.     

Ultrastructure of the spermatozoon of the digenean Cricocephalus albus (Kuhl & van Hasselt, 1822) Looss, 1899 (Platyhelminthes, Pronocephaloidea, Pronocephalidae), parasite of “the hawksbill sea turtle” Eretmochelys imbricata (Linnaeus, 1766) in Senegal

The mature spermatozoon of Cricocephalus albus is filiform, tapered at both ends and shows the following features: 2 axonemes of different lengths presenting the 9 + “1” trepaxonematan pattern, 2 bundles of parallel cortical microtubules, a mitochondrion and a nucleus. Nevertheless, the particularity of the spermatozoon of C. albus is its anterior extremity with an apical electron-dense material associated with extramembranar ornamentation, a cytoplasmic dorsolateral expansion and spine-like bodies. To our knowledge, such an anterior extremity of the spermatozoon has not previously been described from a species of the superfamily Pronocephaloidea. Our study provides new data on the mature gamete of C. albus in order to improve our understanding of the pronocephaloidean phylogenetic relationships.     

Ultrastructural characteristics of the mature spermatozoon of the digenean Sclerodistomum italicum (Stossich, 1893) (Hemiuroidea,Sclerodistomidae) intestinal parasite of Hypocanthus amia (Teleostei,Carangidae)

The mature spermatozoon of Sclerodistomum italicum is filiform, tapered at both ends and shows the following features: 2 axonemes of the 9 + “1” pattern of the Trepaxonemata, mitochondrion, nucleus and parallel cortical microtubules. The specific features of the spermatozoon of S. italicum include the simultaneous presence of two types of extramembranous ornamentations, the presence of short cortical microtubules in the anterior part of the spermatozoon and the presence of only one bundle of cortical microtubules in the median part of the spermatozoon. Thus far these structures are known only in the Hemiuroidea. The presence of filamentous ornamentation in the anterior extremity of the spermatozoon has not previously been described in the Sclerodistomidae. Similar to spermatozoa of other hemiuroideans, S. italicum lack spine-like bodies described in spermatozoa of many digenean taxa. The posterior extremity of the spermatozoon exhibits the same ultrastructural characteristics typical of the Hemiuroidea.     

Spermiogenesis and spermatozoon ultrastructure of the davaineid cestode Raillietina micracantha (Fuhrmann, 1909)

Miquel, J., Torres, J., Foronda, P. and Feliu, C. 2010. Spermiogenesis and spermatozoon ultrastructure of the davaineid cestode Raillietina micracantha. — Acta Zoologica (Stockholm) 91 : 212–221 The spermiogenesis and the ultrastructural organization of the spermatozoon of the davaineid cestode Raillietina micracantha are described by means of transmission electron microscopy. Spermiogenesis begins with the formation of a zone of differentiation containing two centrioles. One of the centrioles develops a free flagellum that later fuses with a cytoplasmic extension. The nucleus migrates along the spermatid body after the proximodistal fusion of the flagellum and the cytoplasmic extension. During advanced stages of spermiogenesis a periaxonemal sheath and intracytoplasmic walls appear in the spermatids. Spermiogenesis finishes with the appearance of two helicoidal crested bodies at the base of spermatids and, finally, the narrowing of the ring of arched membranes detaches the fully formed spermatozoon. The mature spermatozoon of R. micracantha is a long and filiform cell, tapered at both ends, which lacks mitochondria. It exhibits two crested bodies of different lengths, one axoneme of the 9 + ‘1’ pattern of trepaxonematan Platyhelminthes, twisted cortical microtubules, a periaxonemal sheath, intracytoplasmic walls, granules of glycogen and a spiralled nucleus. The anterior extremity of the spermatozoon is characterized by the presence of an electron‐dense apical cone and two spiralled crested bodies while the posterior extremity of the male gamete exhibits only the axoneme and an electron‐dense posterior tip.     

Spermatozoon ultrastructure of Gyliauchen sp. (Digenea: Gyliauchenidae), an intestinal parasite of Siganus fuscescens (Pisces: Teleostei)

The ultrastructure of the mature spermatozoon of Gyliauchen sp., a parasite of the dusky rabbitfish Siganus fuscescens, was studied by transmission electron microscopy. The spermatozoon possesses two axonemes of the 9+"1" pattern of Trepaxonemata, four attachment zones, one mitochondrion, a nucleus, cortical microtubules, external ornamentation of the plasma membrane, and spine-like bodies. The main characteristics of this spermatozoon are the presence of one mitochondrion, spine-like bodies not associated with the external ornamentation, and a posterior extremity of type 3 that is characterized by the following sequence: posterior extremity of the nucleus then posterior extremity of the second axoneme. Numerous other ultrastructural features are also discussed and compared to the digenean spermatology literature. This is the first study of a member of the Gyliauchenidae and the fourth within the Lepocreadioidea. The results show that many ultrastructural characters are variable within this superfamily and could be useful for phylogeny.     

Ultrastructural characters of the spermatozoon of the digenean Hypocreadium caputvadum Kacem et al., 2011 (Lepocreadioidea: Lepocreadiidae), an intestinal parasite of Balistes capriscus in Tunisia

The ultrastructural organization of the spermatozoon of the digenean Hypocreadium caputvadum (Lepocreadioidea: Lepocreadiidae) is described. Live digeneans were collected from Balistes capriscus (Teleostei: Balistidae) from the Gulf of Gabès, Tunisia (Eastern Mediterranean Sea). The mature spermatozoon of H. caputvadum shows several ultrastructural characters such as two axonemes of different lengths exhibiting the classical 9 + “1” trepaxonematan pattern, a nucleus, two mitochondria, granules of glycogen, external ornamentation of the plasma membrane and two bundles of parallel cortical microtubules. Moreover, in the anterior extremity, the second axoneme is partly surrounded by a discontinuous and submembranous layer of electron-dense material. Our study provides new data on the spermatozoon of H. caputvadum in order to improve the understanding of phylogenetic relationships in the Digenea, particularly in the superfamily Lepocreadioidea. In this context, the electron-dense material surrounding one of the axonemes in the anterior spermatozoon extremity constitutes the unique distinguishing ultrastructural character of lepocreadioideans, and it is present in spermatozoa of lepocreadiids, aephnidiogenids and gyliauchenids.     

Spermiogenesis and spermatozoon ultrastructure of the dilepidid cestode Molluscotaenia crassiscolex (von Linstow, 1890), an intestinal parasite of the common shrew Sorex araneus

Marigo, A.M., Bâ, C.T. and Miquel, J. 2011. Spermiogenesis and spermatozoon ultrastructure of the dilepidid cestode Molluscotaenia crassiscolex (von Linstow, 1890), an intestinal parasite of the common shrew Sorex araneus. —Acta Zoologica (Stockholm) 92 : 116–125. Spermiogenesis in Molluscotaenia crassiscolex begins with the formation of a differentiation zone containing two centrioles. One of the centrioles develops a flagellum directly into the cytoplasmic extension. The nucleus elongates and later migrates along the spermatid body. During advanced stages of spermiogenesis, a periaxonemal sheath appears in the spermatid. Spermiogenesis finishes with the appearance of a single helicoidal crested body at the base of the spermatid and, finally, the narrowing of the ring of arched membranes causes the detachment of the fully formed spermatozoon. The mature spermatozoon of M. crassiscolex exhibits a partially detached crested body in the anterior region of the spermatozoon, one axoneme, twisted cortical microtubules, a periaxonemal sheath, and a spiralled nucleus. The anterior spermatozoon extremity is characterized by the presence of an electron‐dense apical cone and a single spiralled crested body, which is attached to the sperm cell in the anterior and posterior areas of region I, whereas in the middle area it is partially detached from the cell. This crested body is described for the first time in cestodes. The posterior extremity of the male gamete exhibits only the disorganizing axoneme. Results are discussed and compared particularly with the available ultrastructural data on dilepidids sensu lato.     

Ultrastructure of Spermiogenesis and the Spermatozoon of Mathevotaenia herpestis(Cestoda), Intestinal Parasite of Atelerix albiventrisin Senegal

Spermiogenesis in M. herpestisbegins with the formation of a differentiation zone which contains two centrioles associated with an electron–dense, finely granular material. This granular material very quickly becomes striated, a median cytoplasmic extension forms, one of the centrioles becomes laterally oriented in a cytoplasmic bud and the other gives rise to a flagellum. After the migration of the nucleus, a helicoidal crested–like body forms, then the old spermatid separates from the residual cytoplasm. The mature M. herpestisspermatozoon exhibits an apical cone of electron–dense material, a crested–like body and cortical microtubules which are electron–dense centred and spiralized except at their posterior extremity where they are parallel to the spermatozoon axis. The axoneme is of the 9 + ‘1’ pattern. It reaches the posterior extremity of the gamete where the cytoplasm is very electron–dense. The presence of centrioles flanked by ‘striated roots’ has never, to our knowledge, been reported in a platyhelminth. Likewise, a nucleus with an annular cross–section and unevenly distributed electron–dense peri–axonemal material has never been described in a cestod.     

The ultrastructural characters of the mature spermatozoon of Opechona bacillaris (Molin, 1859) (Digenea,Lepocreadiidae) a parasite of Scomber colias Gmelin, 1789 (Scombridae) off the coast of Dakar (Senegal)

This study presents the ultrastructure of the mature spermatozoon of Opechona bacillaris, a digenean belonging to the family Lepocreadiidae. The sperm cell of O. bacillaris exhibits the general pattern described in most of the Lepocreadioidea: two axonemes of the 9 + ‘1’ pattern of the Trepaxonemata, mitochondria, a cortical mitochondrion, a nucleus, electron‐dense material in the anterior extremity of the spermatozoon, external ornamentation of the plasma membrane with associated spinelike bodies, and granules of glycogen. However, particularities of O. bacillaris are the simultaneous presence in the anterior extremity of the spermatozoon of the electron‐dense material, a mitochondrion, and the absence of cortical microtubules. In the Lepocreadiidae, we describe for the first time in O. bacillaris spinelike bodies associated with the external ornamentation of the plasma membrane and two mitochondria. The first mitochondrion is moniliform and composed of a mitochondrial cord with joined mitochondrial bulges. The second mitochondrion shows a regular form. The posterior tip of the spermatozoon has only singlets to owing to the disorganization of the second axoneme and granules of glycogen as occurs in Hypocreadium caputvadum, the other studied species of the family Lepocreadiidae.     

Ultrastructural study of the male gamete of Pleurogonius truncatus Prudhoe, 1944 (Platyhelminthes, Digenea, Pronocephalidae) parasite of Eretmochelys imbricata (Linnaeus, 1766)

In Pronocephaloidea, the spermatozoa of only two species have been studied today. Because of this, we present in this work data concerning to a third specie, Pleurogonius truncatus Prudhoe, 1944. The mature spermatozoon of P. truncatus possesses two axonemes with the 9+"1" pattern typical of Trepaxonemata, mitochondrion, nucleus, parallel cortical microtubules, spinelike bodies, cytoplasmic expansion and an external ornamentation of the plasma membrane. A particularity of the spermatozoon of P. truncatus is in the ultrastructure of the anterior spermatozoon extremity with only cortical microtubules and ornamentation of the plasma membrane. This type of anterior extremity has never been described until today in Pronocephaloidea. On the other hand, the ultrastructure of the posterior extremity of the spermatozoon confirms that already described in Pronocephalidae.     

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

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一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]。     

Sperm characters of the digenean Nephrotrema truncatum (Troglotrematidae): a kidney parasite of Crocidura russula (Soricidae) and their phylogenetic significance

ABSTRACT

Spermatological characteristics of the troglotrematid digenean Nephrotrema truncatum, a parasite of the shrew Crocidura russula, have been investigated by means of transmission electron microscopy. The ultrastructural study reveals that the mature spermatozoon of N. truncatum exhibits many ultrastructural characters previously described in most gorgoderoideans. These are two axonemes of the 9+‘1‘ trepaxonematan pattern, four attachment zones, a lateral expansion, an external ornamentation of the plasma membrane associated with spine-like bodies and cortical microtubules, and in the posterior part of the anterior spermatozoon region, two bundles of parallel cortical microtubules with the maximum number located in the anterior part of the spermatozoon, a nucleus, two mitochondria, and granules of glycogen. The obtained results are compared with those of other digeneans, particularly the Gorgoderoidea. The sperm cells gorgoderoideans are of type IV, characterised by a 9+‘1‘ pattern of axonemes, the presence of an external ornamentation associated with cortical microtubules and located in the posterior area of the anterior extremity, the presence of two bundles of cortical microtubules, the maximum number of cortical microtubules located in the anterior region of the spermatozoon, and the presence of generally two mitochondria. However, dicrocoeliids and troglotrematids have spermatozoa with ornamentation of the plasma membrane and lateral expansions.     

Ultrastructure of the Spermatozoon of Avitellina centripunctata(Cestoda,Cyclophyllidea), a Parasite of the Small Intestine of Cattle in Senegal

The Avitellina centripunctataspermatozoon is filiform, tapered at both ends and lacks mitochondria. The anterior extremity exhibits an apical cone and a crested–like body 150–200 nm thick. The axoneme is surrounded by a fine layer of lucent cytoplasm and a sheath of electron–dense material. The cytoplasm is slightly electron–dense at the anterior tip of the apical cone and in region IV of the spermatozoon. Over the rest of the gamete it is subdivided into numerous electron–lucent compartments by irregularly spaced walls. The nucleus is electron–dense. It interposes itself between the cortical microtubules which are all electron–dense centred and spiralized along their whole length. An apical zone containing spiralized microtubules, cortical microtubules which are all electron–dense centred and stop before reaching the posterior extremity of the nucleus, as well as the subdivision into cavities by intracytoplasmic proteinaceous material, have never been described before in a cestod. Moreover, the crested–like body of Avitellina centripunctatais the thickest of those which have been described to date in the cestods.     

Ultrastructure of the spermatozoon of Parachristianella trygonis Dollfus, 1946 (Trypanorhyncha: Eutetrarhynchidae)

The ultrastructural organization of the mature spermatozoon of the trypanorhynch cestode Parachristianella trygonis is described by transmission electron microscopy. The spermatozoon is a long and filiform cell, tapered at both ends, lacking both mitochondrion and crested bodies. Its cytoplasm contains 2 axonemes of the 9+'1' pattern of the Trepaxonemata longitudinally displaced, parallel cortical microtubules, the nucleus and glycogen in form of both alpha-glycogen rosettes and beta-glycogen particles. The anterior extremity of the spermatozoon is characterized by the presence of an arclike row of up to 10 parallel cortical microtubules that partially surround the first axoneme. The present study emphasizes the ultrastructural similarity between mature spermatozoa of all 4 trypanorhynchs that have been studied to date. Nevertheless, several features, i.e., the characteristics of spermatozoa extremities, the absence of crested bodies, and the possible presence of an arclike layer of cortical microtubules, need a more thorough analysis or confirmation in some of these species.