Spermatozoa ultrastructure in Sciaenidae and Polynemidae (Teleostei:Perciformes) with some consideration on Percoidei spermatozoa ultrastructure

Tissue and Cell 37 (2005) 177–191

Spermatozoa ultrastructure in Sciaenidae and Polynemidae (Teleostei:Perciformes) with some consideration on Percoidei spermatozoa ultrastructure P. Gusm˜ao-Pompiani a , C. Oliveira b , I. Quagio-Grassiotto b,∗ a

Universidade Estadual do Mato Grosso do Sul—Unidade de Ensino de Coxim, Rua Pereira Gomes, 355 Coxim, MS, CEP 79400-000, Brazil b Depto. de Morfologia, Instituto de Biociˆ encias, Universidade Estadual Paulista—UNESP, Botucatu, SP, CP 510, CEP 18618-000, Brazil Received 13 July 2004; received in revised form 8 December 2004; accepted 22 December 2004 Available online 7 March 2005

Abstract Spermatozoa ultrastructure was studied in five marines (Paralonchurus brasiliensis, Larimus breviceps, Cynoscion striatus, Micropogonias furnieri, Menticirrhus americanus, Umbrina coroides, Stellifer rastrifer), and one freshwater (Plagioscion squamosissimus) species of Sciaenidae and one species of Polynemidae (Polydactylus virginicus). The investigation revealed that, in all species, spermatozoa display a round head, a nucleus containing highly condensed, filamentous chromatin clusters, no acrosome, a short midpiece with a short cytoplasmic channel, and a flagellum showing the classic axoneme structure (9 + 2) and short irregular lateral fins. In Sciaenidae, the spermatozoa are type II, the flagellar axis is parallel to the nucleus, the lateral nuclear fossa is double arched, the centriolar complex is outside the nuclear fossa, the proximal centriole is anterior and perpendicular to the distal centriole, and no more than ten spherical (marine species) or elongate (freshwater species) mitochondria are observed. Polynemidae spermatozoa are of the intermediate type with the flagellar axis eccentric to the hemi-arc-shaped nucleus, and exhibit no nuclear fossa, the centriolar complex close to the upper nuclear end, the proximal centriole lateral and oblique to the distal centriole, and one large ring-shaped mitocondrion. The data available show that no characteristic is exclusively found in the spermatozoa of members of the Sciaenidae family when compared to other Percoidei with type II spermatozoa. However, three characteristics were exclusively found in Polynemidae: (1) the hemi-arched nucleus; the positioning of the centrioles; and (2) the ring-shaped mitocondrion. The interrelationships between Sciaenidae and Polynemidae as well as between these two families and other Percoidei are herein discussed. © 2005 Elsevier Ltd. All rights reserved. Keywords: Ultrastructure; Sperm; Fish; Teleostei; Sciaenidae; Polynemidae

1. Introduction Perciformes is the most diverse of all fish orders with 20 suborders, 150 families, and at least 6900 species (Greenwood et al., 1966; Gosline, 1968; Nelson, 1994). It was not cladistically defined, and is almost certainly a gradual and unnatural assemblage, clearly polyphyletic (Lauder and Liem, 1983). In a phylogenetical review of Percomorpha, Perciformes has been described as probably paraphyletic (Johnson and Patterson, 1993). The hypotheses about limits ∗

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and/or interrelationships among Perciformes proposed since Greenwood et al. (1966) have led to classificatory changes in two or three of the suborders of Perciformes and in about two-thirds of the 70 families of Percoidei (Johnson, 1993). Percoidei, the largest and most diverse of the perciform suborder (Lauder and Liem, 1983) is divided into three superfamilies that contain 71 families (Greenwood et al., 1966). The superfamily Percoidea congregates a paraphyletic group formed by 65 families, which are mostly very similar and poorly separated from one another (Lauder and Liem, 1983; Nelson, 1994). Sciaenidae, one of the largest Percoidei families, includes about 78 genera and 287 described species (Nelson, 1994). It

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is considered one of the most important families in the suborder Percoidei because of the number of its species that have been described, as well as wide geographic distribution and importance in fishery. The fish of this family inhabit marine coastal, estuarine and freshwaters in tropical and temperate regions of the world. Six genera are restricted to freshwater, four of them endemic and widely distributed across South America (Nelson, 1994; Casatti, 2003). A study conducted by Sasaki (1989), demonstrated the monophyly of the Sciaenidae family on the basis of 21 synapomorphies and the absence of relationships between this family and the other Percoidei families. However, Johnson (1993) demonstrated that many of the synapomorphies identified by Sasaki (1989) were not unique among percoids or sciaenids—in fact, five of them were shared with the polynemids. Though recognizing that further investigations were desirable, Johnson (1993) suggested that Sciaenidae and Polynemidae were sister-groups, and recommended the inclusion of both families in a superfamily, Polymenoidea. The Polynemidae family comprises seven genera and 33 species that dwell marine and brackish waters in all tropical and subtropical seas (Nelson, 1994). According to Johnson (1993), Polynemidae, Mugilidae and Sprhyraenidae have frequently been placed together in a single suborder even though Greenwood et al. (1966) assigned them to separate suborders. Johnson added that Rosen (1964) discounted a close relationship between these three families and atherinomorphs, but did not resolve the question of their relationship. Nelson (1994) included the polynemids in the Percoidei suborder. Ultrastructural studies of the spermatozoa of many fish species have shown that the organization of the spermatic organelles is very conservative in the members of a same family or subfamily (Baccetti et al., 1984; Mattei, 1991; Jamieson, 1991; Burns et al., 1998; Abascal et al., 2002; Quagio-Grassiotto et al., 2003). Sperm characteristics are likely to be very useful in the identification of the relationship patterns among families (Jamieson, 1991). Furthermore the ultrastructural characters of spermatozoa seem to be the kind of data that can be well combined with usual morphologic characters, in phylogenetic analyses. The study of Mattei (1991), that includes 24 new descriptions, analyzes the ultrastructure of spermatozoa in 36 species pertaining to 25 families of the suborder Percoidei. The families analyzed by this author were Acropomatidae, Apogonidae, Carangidae, Centracanthidae, Centrarchidae, Centropomidae, Cepolidae, Chaetodontidae, Echeneidae, Emmelichthyidae, Ephippididae, Gerreidae, Haemulidae, Kuhlidae, Lutjanidae, Malacanthidae, Monodactylidae, Mullidae, Percichthyidae, Percidae, Pomatomidae, Priacanthidae, Sciaenidae, Serranidae, and Sparidae. The study of Jamieson (1991), with one new description, adds six other species to this total. Recent studies of the suborder Percoidei have led to new hypotheses about the relationship among some families, which resulted in the reallocation of some genera (Johnson,

1993). Therefore, an update of the classification of the families analyzed by Mattei (1991) and Jamieson (1991) becomes necessary. Thus, the species Nannoperca oxleyana, described by Marshall (1989—apud Jamieson, 1991) as pertaining to the Kuhlidae family, is now allocated in the family Percichthyidae (Johnson, 1984; Nelson, 1994); the species Parakuhlia boulangeri (=Parakuhlia macrophthalmus), described by Mattei (1991) as also pertaining to the Kuhlidae family, is today in the family Haemulidae; Synagrops microlepsis, described by Mattei (1991) as pertaining to the family Percichthydae, is now in the family Acropomatidae; Morone punctata, described by Mattei (1991) as pertaining to the family Percichthydae, is now placed in the family Moronidae; and Drepane africana, described by Mattei (1991) as pertaining to the family Ephippididae, is now in the family Drepaneidae (Johnson, 1993; Nelson, 1994). Consequently spermatozoa believed to belong to the families Kuhliidae and Ephippididae actually pertain to the families Moronidae and Drepaneidae. The representative species of the family Polynemidae whose spermatozoa were described by Mattei (1970, 1991), as pertaining to the suborder Polynemoidei is now included in the suborder Percoidei (Nelson, 1994). Descriptions of the sperm structure in several Percoidei species have shown that the structure of spermatozoa varies within some families (Jamieson, 1991; Mattei, 1991). The recent descriptions of the structure of spermatozoa in Apogonidae (Lahnsteiner, 2003); Carangidae (Lahnsteiner and Patzner, 1998; Maricchiolo et al., 2002); Moronidae (Saperas et al., 1993); Mullidae (Saperas et al., 1993; Lahnsteiner and Patzner, 1995, 1998; Gwo et al., 2004b); Sciaenidae (Gusm˜ao et al., 1999; Gwo and Arnold, 1992), Sparidae (Gwo et al., 1993, 2004a; Gwo, 1995; Lahnsteiner and Patzner, 1995, 1998), and Serranidae (Gwo et al., 1994; Garc´ıa-D´ıaz et al., 1999) have added new information and confirmed the heterogeneity of the spermatozoa of this suborder. However, most part of this documentation is available only in the form of schematic drawings. In spite of the vast number of families of Percoidei in which spermatozoa are documented, the use of the sperm characters in phylogenetic analyses is not yet feasible because the schematic drawings available do not provide ultrastructural details of most cell organelles. In the same way the lack of detailed documentation about spermatozoa structure for many Percoidei species prevents a fine comparison of the structures presents in different species. Considering the proposal of monophyly in the family Sciaenidae (Sasaki, 1989), and the possibility that Sciaenidae and Polynemidae may belong to a natural group (Johnson, 1993), spermatozoa of seven species pertaining to seven different Sciaenidae marine genera, one species of a freshwater Sciaenidae, and one species of Polynemidae were analyzed and the resulting data was compared with all the data available on the suborder Percoidei. The analyses were conducted with the purpose of identifying ultrastructural spermatozoon characters that could be use-

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ful to a better understanding of the relationships among the Percoidei.

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3. Results 3.1. Sciaenidae sperm

2. Materials and methods Adult male specimens of marine fish were collected in Ubatuba, northern coast of S˜ao Paulo, Brazil (between 23◦ 20 S–23◦ 35 S and 44◦ 50 W–45◦ 14 W), employing a commercial fishing boat equipped with two “double-ring” nets. The marine specimens collected were: Paralonchurus brasiliensis, Larimus breviceps, Cynoscion striatus, Micropogonias furnieri, Menticirrhus americanus, Umbrina coroides, Stellifer rastrifer, of the family Sciaenidae; and Polydactylus virginicus, of the family Polynemidae. The Sciaenidae freshwater species, Plagioscion squamosissimus, was collected from the Volta Grande Reservoir, Cemig, Minas Gerais, Brazil (48◦ 25 /47◦ 35 W and 19◦ 57 /20◦ 10 S). Where this species was introduced some years ago. One to five specimens of each species were analyzed, making a total of 47 specimens. Following sacrifice, gonad fragments were fixed in 2% glutaraldehyde and 4% paraformaldehyde in 0.1 M Sorensen phosphate buffer, pH 7.4, overnight. The material was postfixed in the dark for 2 h in 1% osmium tetroxide in the same buffer, contrasted in block with aqueous solution of 5% uranyl acetate for 2 h, dehydrated in acetone, embedded in araldite, and sectioned and stained with a saturated solution of uranyl acetate in 50% alcohol and lead citrate. Electron micrographs were obtained using a Phillips—CM 100 transmission electron microscope.

Sperm ultrastructure was very similar in the different Sciaenidae species investigated. Only small differences were observed among the samples (Table 1). Spermatozoa were of the type II (sensu—Mattei, 1970) and showed a spherical head with an ovoid nucleus containing highly condensed filamentous clusters of chromatin interspersed by electron lucent areas, and no acrosome (Figs. 1 , 6 , 11 , 16 , 21 , 26 , 31 , 36). Sometimes, as in S. rastrifer and in P. brasiliensis, the nucleus showed a large electron lucent area opposite to the nuclear fossa (Figs. 1 a nd 21). The nuclear fossa was double-arched, lateral and shallow, except in P. brasiliensis where the double arc was deep and narrow. The centriolar complex was outside the nuclear fossa. The proximal centriole was anterior and perpendicular to the distal centriole (Figs. 1 , 6 , 11 , 16 , 21 , 26 , 31 , 36, 38). In general in the Sciaenidae species the centrioles are coated by a sleeve of homogeneous electron dense material and have many stabilization structures. The proximal end of the distal centriole is covered by a complete or incomplete cap of homogeneous electron dense material (Figs. 1 , 6 , 16 , 21, 22 , 26 , 38). Proximal and distal centrioles are fastened each other by microfibrils. The microfibrils interconnect the electron dense cap of the distal centriole with an electron dense plate in the lateral side of the proximal centriole. Others microfibrils connect the lateral side of the distal centriole to another plate of electron dense material that lies close to nuclear envelope at the nuclear fossa. No stabilization structures

Table 1 Spermatozoa characteristics observed in Sciaenidae and Polynemidae Characteristics

Sciaenidae

Spermatozoa type Head form Nucleus form Presence of large electron lucent area in the nucleus Chromatin

Type I Spherical Ovoid Absent Highly condensed filamentous clusters

Nuclear fossa

Double arched, lateral and shallow

Centriolar complex

Outside of the nuclear fossa

Relative position of the centrioles Centriolar stabilization structures Position of flagellum axis Midpiece

Proximal centriole anterior and perpendicular to the distal Conspicuous

Exceptions in Sciaenidae

Polynemidae

Present in P. brasiliensis and S. rastrifer

Intermediate Spherical Hemi-arc Absent

Double arched, lateral, deep and narrow P. brasiliensis

Close to the upper end of the nucleus Proximal centriole lateral and oblique to the distal Not so conspicuous

Parallel to the nucleus Short with a short cytoplasmic channel and some tubular vesicles

Mitochondria number, size and shape Intratubular differentiations

No more than 10, large and spherical

Fins

Short and irregular

Present

Highly condensed filamentous clusters Absent

No more than 10, elongate and fused P. squamosissimus Absent in P. squamosissimus and C. striatus

Eccentric to the nucleus Short with a short cytoplasmic channel and no tubular vesicles One, large and ring-shaped Absent Short and irregular

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Figs. 1–5. Stellifer rastrifer spermatozoon. (Fig. 1) Spermatozoa longitudinal section (bar: 0.37 ␮m). (Fig. 2) Spermatozoon cross section (bar: 0.35 ␮m). (Fig. 3) Midpiece cross section (bar: 0.25 ␮m). (Fig. 4) Flagellum cross section (bar: 0.15 ␮m). (Fig. 5) Flagellum longitudinal section (bar: 0,6 ␮m).

are detected between the nuclear envelope and the proximal centriole, or between the plasmic membrane and the distal end of the distal centriole (Figs. 1 , 6 , 11 , 16 , 21, 22 , 26 , 31 , 36, 38). The distal centriole, differentiated into the axoneme basal body, extended from the nuclear fossa to the initial segment of the cytoplasmic channel. The flagellum axis was parallel to the nucleus (Figs. 1 , 6, 7 , 11 , 16 , 21 , 26 , 31 , 36, 38). The midpiece was short, had some tubular cisternae and a short cytoplasmic channel. No more than ten large spherical (marine species) or elongate (freshwater species, P. squamosissimus) mitochondria surrounded the initial portion of the axoneme and were separated from it by the cytoplasmic channel (Figs. 2, 3 , 7, 8 , 12, 13 , 17, 18 , 22, 23 , 27, 28 , 32, 33 , 37, 39). In the transition zone between the basal body and the axoneme, the basal plate showed nine peripheral doublets and no central microtubules (Figs. 2, 3 , 23 , 27 , 32 , 37). The flagellum exhibited the classic axoneme structure (9 + 2). Intratubular differentiations (ITD—sensu Mattei, 1988), i.e. septa in microtubule A of the peripheral doubles 1, 2, 5

and 6 (Figs. 4 , 9 , 14 , 19 , 24 , 29), were observed, except in C. striatus and P. squamosissimus (Figs. 34 a nd 40). The flagellum membrane was distant from the axoneme and had irregular short fins (Figs. 5 , 10 , 15 , 20 , 25 , 30 , 35 , 41). 3.2. Polynemidae sperm In the Polynemidae P. virginicus, spermatozoa were of an intermediate type, between Mattei’s type I and type II (1970). Its head was spherical with a hemi-arched nucleus containing highly condensed filamentous clusters of chromatin interspersed by electron lucent areas, and no acrosome (Table 1). The nuclear fossa was also absent (Fig. 42). The centriolar complex is close to the upper end of the nucleus, with the proximal centriole lateral and oblique to the distal centriole. The distal centriole, differentiated into the axoneme basal body, was very long and extended from the nuclear fossa to the initial portion of the cytoplasmic channel. The flagellum axis was eccentric to the nucleus (Figs. 42 and 44).

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Figs. 6–10. Umbrina coroides spermatozoon. (Figs. 6 and 7) Spermatozoa longitudinal section (Fig. 6—bar: 0.25 ␮m; Fig. 7—bar: 0.38 ␮m). (Fig. 8) Midpiece cross section (bar: 0.18 ␮m). (Fig. 9) Flagellum cross section (bar: 0.24 ␮m). (Fig. 10) Flagellum longitudinal section (bar: 0.36 ␮m).

The centrioles are coated by a sleeve of homogeneous electron dense material. In the proximal end the distal centriole, the sleeve is short, and forms an incomplete cap. The proximal and distal centrioles are laterally fastened each other by microfibrils. No additional stabilization structures are detected between the nuclear envelope and the centrioles or the plasmic membrane and the distal end of the distal centriole (Figs. 42 and 44). The short midpiece had no tubular cisternae and showed a short cytoplasmic channel (Figs. 42 and 44). In the midpiece, close to the nucleus, one single, large, ring-shaped mitocondrion surrounded the initial portion of the axoneme and was separated from it by the cytoplasmic channel (Figs. 43 and 45). In the transition zone between the basal body and the axoneme, the basal plate showed nine peripheral doublets and no central microtubules (Fig. 42). The flagellum contained the classic axoneme structure (9 + 2). Intratubular differentiations (sensu Mattei, 1979) were not present (Fig. 43). The flagellum membrane had irregular short fins (Figs. 46 and 47).

4. Discussion Mattei (1970) suggests that in Teleostei spermiogenesis may result in two basic spermatozoon types: type I and type II, with an intermediate type between them. This classification is based on whether nuclear rotation, occurs or not during spermiogenesis. The spermatozoon, an aquasperm, has no acrosome, a head usually containing a spherical nucleus a midpiece of variable size with or without a cytoplasmic channel, and one or two long flagella (Jamieson, 1991; Mattei, 1991). When nuclear rotation occurs, the flagellum becomes perpendicular and medial to the nucleus, and spermatozoa are of the type I. If no nuclear rotation occurs, the flagellum remains parallel to the nucleus, and spermatozoa are of the type II. Nuclear rotation, however, may be incomplete. In this case, the flagellum is eccentric to the nucleus, and spermatozoa are of an intermediate type between types I and II (Mattei, 1970). In Perciformes, and also in Percoidei, all these spermatozoa types are present with type II being the most frequent (Jamieson, 1991; Mattei, 1991). Type II spermatozoa

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Figs. 11–15. Menticirrhus americanus spermatozoa. (Fig. 11) Spermatozoon longitudinal section (bar: 0.37 ␮m). (Fig. 12) Spermatozoon cross section (bar: 0.3 ␮m). (Fig. 13) Midpiece cross section (bar: 0.4 ␮m). (Fig. 14) Flagellum cross section (bar: 0.22 ␮m). (Fig. 15) Flagellum longitudinal section (bar: 0.36 ␮m). A: axoneme; B: basal plate; C: centriolar cap; D: distal centriole; F: flagellum; L: electron lucent nuclear area. M: mitochondria; N: nucleus; P: proximal centriole; S: centriolar sleeve; asterisk: cytoplasmic channel; black arrowhead: centriolar stabilization structures; white double arrow: nuclear fossa.

was found in 29 of the 41 families of Perciformes studied by Mattei (1991) who named this type of spermatozoa the type perciforms. In the nucleus of Percoidei spermatozoa, the chromatin is either homogeneous and highly condensed or formed by highly condensed heterogeneous clusters (Jamieson, 1991; Mattei, 1970, 1991—schematic drawings). The final chromatin condensation depends of the type of nuclear proteins associated to the DNA (Saperas et al., 1993) and of results from different condensation processes during the spermiogenesis. In the nucleus of the spermatids of the Mullidae, Upeneus prayensis = Pseudoupeneus prayensis (Boisson et al., 1969; Mattei, 1970—schematic drawings) and Mullus surmuletus (Saperas et al., 1993), the gradual chromatin condensation results in a final homogeneous and highly condensed mass. In the Haemulidae, Parapristipoma octolineatum (Mattei, 1970—schematic drawings), the Centrarchidae, Lepomis macrochirus (Sprando and Russel, 1988), the Percichthyidae, actually Moronidae, Dicentrararchus labrax

(Saperas et al., 1993), and the Sciaenidae, P. squamosissimos (Gusm˜ao et al., 1999), small chromatin granules gradually increase and give origin to highly electron dense, condensed, heterogeneous clusters interspersed by electron lucent areas. 4.1. Percoidei type II spermatozoa Sciaenidae (Mattei, 1991—schematic drawing; Gwo and Arnold, 1992; Gusm˜ao et al., 1999; this paper) have type II spermatozoa. Among Percoidei, type II spermatozoa are found in 19 of the families investigated by Mattei (1970, 1991—schematic drawings), including Serranidae (Jamieson, 1991; Gwo et al., 1994), Centropomidae (Leung, 1987—apud Jamieson, 1991), Percichthyidae (Leung, 1987—apud Jamieson, 1991), Moronidae (Saperas et al., 1993) and Carangidae (Lahnsteiner and Patzner, 1998; Maricchiolo et al., 2002). The type of the spermatozoa found in Centropomidae is still controversial. Leung (1987—apud Jamieson, 1991) describes the spermatozoa of the species

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Figs. 16–20. Micropogonias furnieri spermatozoon. (Fig. 16) Spermatozoon longitudinal section (bar: 0.53 ␮m). (Fig. 17) Spermatozoon cross section (bar: 0.4 ␮m). (Fig. 18) Midpiece cross section (bar: 0.32 ␮m). (Fig. 19) Flagellum cross section (bar: 0.19 ␮m). (Fig. 20) Flagellum longitudinal section (bar: 0.69 ␮m).

Lates calcifer as being of the intermediate type. By analyzing the Jamieson’s Fig. 15.14 (1991, p. 174) it seems that that L. calcifer spermatozoa are better described as type II. According to Mattei (1991—schematic drawings), spermatozoa of the species Lates niloticus are of the type II. In Sciaenidae (Gwo and Arnold, 1992; Gusm˜ao et al., 1999; this paper) and in the other Percoidei with type II spermatozoa, such as Haemulidae (Mattei, 1970—schematic drawings); Serranidae (Jamieson, 1991; Gwo et al., 1994), Centropomidae (Leung, 1987—apud Jamieson, 1991), Percichthyidae (Leung, 1987—apud Jamieson, 1991) and Moronidae (Saperas et al., 1993), the chromatin forms highly electron dense condensed clusters interspersed by electron lucent areas. The only exception is the family Carangidae (Mattei et al., 1979; Lahnsteiner and Patzner, 1998; Maricchiolo et al., 2002) that exhibits homogeneous and highly condensed chromatin in a finely granular pattern. Mattei’s schematic drawings (1991) do not provide information about chromatin condensation. The nuclear fossa is shallow and laterally positioned in Sciaenidae spermatozoa (Mattei, 1991—schematic draw-

ings; Gwo and Arnold, 1992). In this study, the nuclear fossa was also found to be lateral. In addition, it was observed to be shallow and double-arched in the majority of the Sciaenidae species analyzed, with the exception of P. brasiliensis whose fossa exhibits two deep and thin projections into the nucleus. In Serranidae (Jamieson, 1991; Gwo et al., 1994), Centropomidae (Leung, 1987—apud Jamieson, 1991), Moronidae (Saperas et al., 1993), Carangidae (Maricchiolo et al., 2002) and the other Percoidei with type II spermatozoa (Mattei, 1970, 1991—schematic drawings; Mattei et al., 1979), the nuclear fossa is not deep. In the Percichthyidae family, the nuclear fossa is deep in Macculochella peeli, of an intermediary depth in Macculochella macquariensis, and shallow in Macquaria ambigua and Macquaria australasica (Leung, 1987—apud Jamieson, 1991). In spite of the expressive differences in the nuclear fossa length described in the family Percichthyidae (Leung, 1987—apud Jamieson, 1991) in the Fig. 151.15, shown by Jamieson (1991), the nuclear fossa is very similar to the Sciaenidae (this paper). In Sciaenidae (Mattei, 1991—schematic drawings; Gwo and Arnold, 1992; Gusm˜ao et al., 1999; this paper), the cen-

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Figs. 21–25. Paralonchurus brasiliensis spermatozoon. (Fig. 21) Spermatozoon longitudinal section (bar: 0.37 ␮m). (Fig. 22) Spermatozoon cross section (bar: 0.3 ␮m). (Fig. 23) Midpiece cross section (bar: 0.3 ␮m). (Fig. 24) Flagellum cross section (bar: 0.19 ␮m). (Fig. 25) Flagellum longitudinal section (bar: 0.36 ␮m).

triolar complex is outside the nuclear fossa, have many stabilization structures, the proximal centriole is anterior, medial and perpendicular to the distal centriole, and the distal centriole is very long. This type of centriolar organization is found in all the other Percoidei families with type II spermatozoa that were studied by Mattei (1970, 1991—schematic drawings), including Moronidae (Saperas et al., 1993) and Carangidae (Maricchiolo et al., 2002). However, in Serranidae (Jamieson, 1991; Gwo et al., 1994), Centropomidae (Leung, 1987—apud Jamieson, 1991), and Percichthyidae (Leung, 1987—apud Jamieson, 1991), the proximal centriole is anterior, oblique and slightly lateral to the distal centriole. A long distal centriole is observed in the Percoidei families with type II spermatozoa, except the Carangidae (Mattei et al., 1979; Maricchiolo et al., 2002). In the families reviewed and/or documented by Mattei (1970, 1991—schematic drawings), including Sciaenidae, the midpiece is short, has a short cytoplasmic channel, and no cytoplasmic sheath. This study, Gusm˜ao et al. (1999), Gwo and Arnold (1992), confirmed Mattei’s schematic drawing

of Sciaenidae (1991) and others confirmed his drawings of Serranidae (Jamieson, 1991; Gwo et al., 1994; Garc´ıa-D´ıaz et al., 1999), Centropomidae (Leung, 1987—apud Jamieson, 1991) and Moronidae (Saperas et al., 1993) spermatozoa. In the fish of the family Percichthyidae, genus Macquaria there was a long cytoplasmic channel whose final two-thirds were surrounded by a long and straight cytoplasm sheath (Leung, 1987—apud Jamieson, 1991). Another exception is Carangidae that exhibit a mid-sized cytoplasmic channel (Mattei et al., 1979; Maricchiolo et al., 2002). The Percoidei with type II spermatozoa generally have about five spherical mitochondria (Jamieson, 1991; Mattei, 1991—schematic drawings). The same occurs in the marine Sciaenidae (Mattei, 1991—schematic drawings; Gwo and Arnold, 1992; this paper). However, a detailed observation of Gusm˜ao et al. (1999) pictures, show that in the freshwater Sciaenidae, P. squamosissimus, mitochondria are elongate and may be fused to each other (present paper). In Centropomidae (Leung, 1987—apud Jamieson, 1991) Serranidae (Jamieson, 1991; Gwo et al., 1994), Moronidae (Saperas et al., 1993)

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Figs. 26–30. Larimus breviceps spermatozoon. (Fig. 26) Spermatozoon longitudinal section (bar: 0.32 ␮m). (Fig. 27) Spermatozoon cross section (bar: 0.27 ␮m). (Fig. 28) Midpiece cross section (bar: 0.32 ␮m). (Fig. 29) Flagellum cross section (bar: 0.28 ␮m). (Fig. 30) Flagellum longitudinal section (bar: 0.36 ␮m). A: axoneme; B: basal plate; C: centriolar cap; D: distal centriole; F: flagellum; L: electron lucent nuclear area. M: mitochondria; N: nucleus; P: proximal centriole; S: centriolar sleeve; asterisk: cytoplasmic channel; black arrowhead: centriolar stabilization structures; white double arrow: nuclear fossa.

and Carangidae (Maricchiolo et al., 2002) mithocondria follow the general pattern described by Mattei (1991). In Percichthyidae (Leung, 1987—apud Jamieson, 1991), as in P. squamosissimus (this paper), mitochondria are elongate and may be fused to each other. Mattei (1991) considers intratubular differentiations (ITD), a septum in the A microtubule of doublets 1, 2, 5 and 6 as a characteristic of perciform spermatozoa of the type II. Although ITD are present in the axoneme of many Percoidei families, and apparently in some Sciaenidae (Gwo and Arnold, 1992; this paper), they are not found in P. squamosissimus (Gusm˜ao et al., 1999) and in C. striatus (this paper). They are also absent in Serranidae (Gwo et al., 1994). The flagellum membrane may show one or more lateral projections, or fins, of variable length (Mattei, 1988). In the families with type II spermatozoa, the flagellum membrane displays irregular short fins in Sciaenidae (Gwo and Arnold, 1992; Gusm˜ao et al., 1999; this paper); one long fin in the Percichthyidae Macculochella spp., and two fins in Macquaria

spp. (Leung, 1987—apud Jamieson, 1991). The Serranidae, P. leopardus (Gwo et al., 1994) and the Centropomidae L. calcarifer (Leung, 1987—apud Jamieson, 1991), also show two fins. 4.2. Percoidei intermediate spermatozoa type Spermatozoa of the intermediate type, that display a flagellum eccentric to the nucleus, are found in the Polynemidae, Galeoides decadactylus (Mattei, 1970—schematic drawings) and P. virginicus (present paper). They also occur in the Percichthyidae, N. oxleyana (Marshall, 1989—apud Jamieson, 1991), and in Serranus scriba, Serranidae (Garc´ıaD´ıaz et al., 1999). Even though spermatozoa type is the same in these species, nuclear shape is very different in these families. While in the Polynemidae (Mattei, 1970—schematic drawings; this paper), the nucleus shows the shape of a hemiarc, in N. oxleyana, Percichthyidae (Marshall, 1989—apud Jamieson, 1991) and in S. scriba, Serranidae (Garc´ıa-D´ıaz

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Figs. 31–35. Cynoscion striatus spermatozoon. (Fig. 31) Spermatozoon longitudinal section (bar: 0.62 ␮m). (Fig. 32) Spermatozoon cross section (bar: 0.27 ␮m). (Fig. 33) Midpiece cross section (bar: 0.32 ␮m). (Fig. 34) Flagellum cross section (bar: 0.19 ␮m). (Fig. 35) Flagellum longitudinal section (bar: 0.49 ␮m).

et al., 1999) it is spherical with an eccentric depression, the nuclear fossa. In these families, heterogeneous chromatin condensation occurs in the Polynemidae (Mattei, 1970—schematic drawings; this paper) and in N. oxleyana, Percichthyidae (Marshall, 1989—apud Jamieson, 1991). In the Serranidae, S. scriba (Garc´ıa-D´ıaz et al., 1999) chromatin is homogenously condensed. Polynemidae (Mattei, 1970, 1991—schematic drawings; this paper) have no nuclear fossa while in N. oxleyana, Percichthyidae (Marshall, 1989—apud Jamieson, 1991) and S. scriba, Serranidae (Garc´ıa-D´ıaz et al., 1999), the nuclear fossa is eccentric and of intermediary depth. In the family Polynemidae (Mattei, 1970—schematic drawings; this paper), the proximal centriole is lateral and oblique to the distal centriole, and both are located close to the upper end of the nucleus. The centriolar stabilization structures are not so conspicuous in the family Polynemidae (this paper). In N. oxleyana, Percichthyidae (Marshall, 1989; apud Jamieson, 1991), the proximal centriole is anterior and perpendicular in relation to the distal centriole, and both are

partially inside the nuclear fossa. No information about the Serranidae, S. scriba (Garc´ıa-D´ıaz et al., 1999) is available. In Polynemidae (Mattei, 1970—schematic drawings; this paper) and Centropomidae (Leung, 1987—apud Jamieson, 1991), the midpiece is short and has a very short cytoplasmic channel. In N. oxleyana, Percichthyidae (Marshall, 1989—apud Jamieson, 1991) the midpiece is long and has a long cytoplasmic channel with a long and thin cytoplasm sheath surrounding its final two-thirds. The illustrations of the spermatozoa of the S. scriba, Serranidae available (Garc´ıaD´ıaz et al., 1999) are not conclusive but the midpiece seems to be long and have a long cytoplasmic channel. The Polynemidae, P. virginicus, has a single, large, ringshaped mitocondrion separated from the initial portion of the flagellum by the cytoplasmic channel (this paper). In N. oxleyana, Percichthyidae (Marshall, 1989; apud Jamieson, 1991) and in the Serranidae, S. scriba (Garc´ıa-D´ıaz et al., 1999), mitochondria are spherical, and no more than three or four in number. The axoneme of Polynemidae spermatozoa shows no ITD (this paper). Furthermore, no information about their occur-

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Figs. 36–41. Plagioscion squamosissimus spermatozoon. (Fig. 36) Spermatozoon longitudinal section (bar: 0.37 ␮m). (Fig. 37) Spermatozoon cross section (bar: 0.35 ␮m). (Fig. 38) Centriolar complex (bar: 0.28 ␮m). (Fig. 39) Midpiece cross section (bar: 0.31 ␮m). (Fig. 40) Flagellum cross section (bar: 0.2 ␮m). (Fig. 41) Flagellum longitudinal section (bar: 0.4 ␮m).

rence in Percoidei families with spermatozoa type of the intermediate type has been reported. Although not detected in the Polynemidae, G. decadactylus (Mattei, 1970—schematics drawings), the flagellum membrane of P. virginicus (this paper), has very short irregular fins. On the other hand, the Percichthyidae, N. oxleyana (Marshall, 1989—apud Jamieson, 1991) shows two long fins that are absent in the Serranidae, S. scriba (Garc´ıa-D´ıaz et al., 1999). 4.3. Percoidei type I spermatozoa Type I spermatozoa are found in the Percoidei pertaining to the families Mullidae (Boisson et al., 1969; Mattei, 1970—schematic drawings; Saperas et al., 1993; Lahnsteiner and Patzner, 1998; Gwo et al., 2004b), Centracanthidae (Carrillo and Zanuy, 1977—apud Jamieson, 1991; Mattei, 1991—schematic drawings), Centrarchidae (Baccetti et al., 1987; Sprando and Russel, 1988), Sparidae (Gwo et al., 1993; Lahnsteiner and Patzner, 1995; Gwo et al.,

2004a), and the Serranidae of the Serranus genus, except in S. scriba (Garc´ıa-D´ıaz et al., 1999). The type of the spermatozoa found in the species Serranus cabrilla is also controversial. The spermatozoa of this species are described as being type II by Mattei (1991—schematic drawings), but, the analysis of Fig. 2, presented by Garc´ıa-D´ıaz et al. (1999, p. 505), suggests that S. cabrilla spermatozoa are better described as being type I. Apogonidae spermatozoa, structurally of the type I, differ from those of all other Percoidei as they are biflagellate (Mattei and Mattei, 1984; Lahnsteiner, 2003). In all these families the shape of the nucleus varies widely. In the nucleus, the chromatin is homogenously condensed in Sparidae (Gwo et al., 1993, 2004a; Lahnsteiner and Patzner, 1995), in Mullidae (Lahnsteiner and Patzner, 1998; Gwo et al., 2004b) and in the biflagellate Apogonidae (Mattei and Mattei, 1984; Lahnsteiner, 2003). In Centrarchidae (Sprando and Russel, 1988), the chromatin forms highly condensed electron dense clusters interspersed by electron lucent areas while in the Serranidae of the genus Serranus,

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Figs. 42–47. Polydactylus virginicus spermatozoon. (Fig. 42) Spermatozoon longitudinal section (bar: 0.33 ␮m). (Fig. 43) Spermatozoon cross section (bar: 0.33 ␮m). (Fig. 44) Centriolar complex (bar: 0.27 ␮m). (Fig. 45) Midpiece cross section (bar: 0.15 ␮m). (Fig. 46) Flagellum cross section (bar: 0.27 ␮m). (Fig. 47) Flagellum longitudinal section (bar: 0.33 ␮m). A: axoneme; B: basal plate; C: centriolar cap; D: distal centriole; F: flagellum; L: electron lucent nuclear area. M: mitochondria; N: nucleus; P: proximal centriole; S: centriolar sleeve; asterisk: cytoplasmic channel; black arrowhead: centriolar stabilization structures; white double arrow: nuclear fossa.

except in S. scriba (Garc´ıa-D´ıaz et al., 1999), the final condensed chromatin exhibits fine granules. The depth of the nuclear fossa varies in the families with type I spermatozoa. It is deep in Mullidae (Boisson et al., 1969; Mattei, 1970, 1991—schematic drawings; Saperas et al., 1993; Lahnsteiner and Patzner, 1998; Gwo et al., 2004b), Sparidae (Mattei, 1970, 1991—schematics drawings; Gwo et al., 1993; Lahnsteiner and Patzner, 1995; Gwo et al., 2004a) and Centracanthidae (Carrillo and Zanuy, 1977—apud Jamieson, 1991; Mattei, 1991—schematic drawings). It is intermediary in Centrarchidae (Sprando and Russel, 1988), and in the Serranidae, S. scriba (Garc´ıa-D´ıaz et al., 1999). On the other hand, the biflagellate Apogonidae (Mattei and Mattei, 1984; Lahnsteiner, 2003) shows a shallow, double arched nuclear fossa. Apparently, in all the families with type I spermatozoa, the centriolar complex is located inside the nuclear fossa. In Mullidae (Boisson et al., 1969; Mattei, 1970, 1991—schematic

drawings; Saperas et al., 1993; Lahnsteiner and Patzner, 1998; Gwo et al., 2004b), the proximal centriole is anterior and coaxial in relation to the distal centriole. The same occurs in Centracanthidae (Carrillo and Zanuy, 1977—apud Jamieson, 1991), while in Sparidae the proximal centriole is anterior and perpendicular, or slightly oblique in relation to the distal centriole (Mattei, 1970, 1991; Gwo et al., 1993; Lahnsteiner and Patzner, 1995; Gwo et al., 2004a). In the biflagellate Apogonidae, the centrioles are located outside the nuclear fossa and parallel to each other; both differentiate into basal bodies and give origin to the flagella (Mattei and Mattei, 1984; Lahnsteiner, 2003). Both the centrioles are fastened by many stabilization structures (Gwo et al., 1993; Gwo, 1995; Lahnsteiner and Patzner, 1995; Gwo et al., 2004a). In the families Mullidae (Boisson et al., 1969; Mattei, 1970, 1991—schematic drawings; Saperas et al., 1993; Lahnsteiner and Patzner, 1998; Gwo et al., 2004b), Centracanthidae (Carrillo and Zanuy, 1977—apud Jamieson,

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1991) and Sparidae (Mattei, 1970, 1991—schematic drawings; Gwo et al., 1993; Lahnsteiner and Patzner, 1995; Gwo et al., 2004a), the midpiece is short and has a short cytoplasmic channel. Apogonidae also has a short midpiece with a short cytoplasmic channel that is shared by the two flagella (Mattei and Mattei, 1984; Lahnsteiner, 2003). In the Percoidei families with type I spermatozoa, mitochondria are generally spherical and variable in number. They are about five in the Mullidae (Boisson et al., 1969; Mattei, 1970, 1991—schematic drawings; Saperas et al., 1993; Lahnsteiner and Patzner, 1998; Gwo et al., 2004b), one or two in the Sparidae (Mattei, 1970, 1991—schematic drawings; Gwo et al., 1993; Lahnsteiner and Patzner, 1995; Gwo et al., 2004a) and only one in the Centracanthidae (Carrillo and Zanuy, 1977—apud Jamieson, 1991). On the other hand, the biflagellate Apogonidae exhibits about ten spherical mitochondria (Mattei and Mattei, 1984; Lahnsteiner, 2003). There is no information about the occurrence of ITD in the flagellum axoneme of these families. However, two symmetrical fins are observed in the Mullidae, Mullus barbatus (Lahnsteiner and Patzner, 1995, 1998), and one fin in the Sparidae, Diplodus sargus, Boops boops (Lahnsteiner and Patzner, 1995, 1998) while in the Mullidae, Psedoupeneus prayensis, Paraupeneus spilurus (Boisson et al., 1969; Mattei, 1970, 1991—schematic drawings; Gwo et al., 2004b), in the Sparidae, Acanthopagrus genus, Pagrus major and Rhabdosargus sarba (Gwo et al., 1993; Gwo, 1995; Gwo et al., 2004a) and in Centracanthidae (Carrillo and Zanuy, 1977—apud Jamieson, 1991) the flagellum membrane seems to have no fins. 4.4. Some consideration on Perciformes spermatozoa ultrastructure In the family Sciaenidae, the sperm ultrastructure shows a consistent homogeneity (Table 1). The members of this family share with each other and with the other Percoidei that have type II spermatozoa the following characteristics: heterogeneous chromatin condensation; generally shallow and double-arched nuclear fossa; proximal centriole anterior and perpendicular to the distal centriole; centrioles outside the nuclear fossa and close to the nucleus; short midpiece and short cytoplasmic channel; no more than ten spherical or elongate mitochondria and irregular short fins. This similarity among the spermatozoa of the Sciaenidae family agrees with the monophyly proposed for the group (Sasaki, 1989) and supports the hypotheses that in species of a same family the sperm organelles have the same distribution (Baccetti et al., 1984; Burns et al., 1998; Abascal et al., 2002; QuagioGrassiotto et al., 2003). However, the similarity of sperm structure among the families that have the same type of spermatozoa may indicate a closer relationship among them. The major differences in sperm structure are found in the families Carangidae, Percichthyidae and Serranidae, mainly in S. scriba. Johnson (1993) suggests that the Percoidei families Carangidae, Nematitistiidae, Coryphaenidae, Rachycen-

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tridae, and Echeneididae could be recognized as the suborder Carangoidei. Some species formerly recognized in the Percichthyidae, as M. punctata and Dicentrarchus labrax, are now allocated in the family Moronidae (Johnson, 1984). According Johnson (1993), Percichthyidae are polyphyletic, but the family Serranidae, as redefined by Gosline (1966), is a natural assemblage. Curiously, the spermatozoa of the Percichthyidae species of the genus Macquaria (Leung, 1987—apud Jamieson, 1991) are very similar to those of the Mugilidae, Lisa aurata (Brusl´e, 1981; Eiras-Stofella et al., 1993). Although the Sciaenidae analyzed share with the Polynemidae the chromatin condensation pattern, type of midpiece and presence of short irregulars fins, they clearly differ in spermatozoa type, shape of the nucleus, position of the centrioles in relation to the nucleus, position of the centriole in relation to each other, centriolar stabilization structures, length of the distal centriole, and the shape and number of the mitochondria. Johnson (1993) considered Polynemidae as pertaining to the suborder Polynemoidei and believed that Sciaenidae and Polynemidae were sister-groups and recommended the inclusion of both these families in a superfamily Polynemoidea. The ultrastructural study of the spermatozoa does not corroborate Johnson’s proposal (1993) of the close relationship between these two families. In the families with type I spermatozoa, the similarity between the spermatic structure of Centracanthidae and Sparidae agrees with Johnson’s hypotheses of 1981 that Centracanthidae is the sister group of the Sparidae. Akazaki (1962) considers Sparidae, Nemapteridae, Pentapodidae, and Lethrinidae closely related and joined these families in the spariforms group. On the other hand, the heterogeneity of the sperm structures observed among the families with type I spermatozoa agrees with the idea that the suborder Percoidei is polyphyletic (Johnson, 1993). The description of the ultrastructure of spermatozoa of other Perciformes suborders such as Scombroidei (Abascal et al., 2002) and Trachinoidei (Lahnsteiner and Patzner, 1996) instigate the research and discussion about the phylogenetic potential of the spermatozoa ultrastructural characters to solve the pattern of relationship among members of the order Perciformes. There are many similarities among some spermatozoa of these suborders and some families of Percoidei. For example, the spermatozoa of the Scombroidei, Thunnus thynnus (Abascal et al., 2002) are very similar to those of the marine Sciaenidae (present paper) as well as the spermatozoa of the Trachinoidei, Trachinus draco (Lahnsteiner and Patzner, 1996) are very similar to the Serranidae, Epinephelus mabaricus and Plectropomus leopardus (Jamieson, 1991; Gwo et al., 1994).

Acknowledgments We would like to thank the Electron Microscopy Laboratory of IBB-UNESP for allowing us the use of their facilities and to Ricardo Macedo Corrˆea e Castro for the

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taxonomic identification of the species. Funding was provided by Centro de Aquicultura—UNESP (CAUNESP) and Fundac¸a˜ o para o Amparo da Pesquisa do Estado de S˜ao Paulo (FAPESP).

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