Comparative morphology of the gonadal structure related to reproductive strategies in six species of...

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Comparative Morphology of the Gonadal StructureRelated to Reproductive Strategies in Six Species ofNeotropical Catfishes (Teleostei: Siluriformes)

Rafael Magno Costa Melo,1 Fabio Pereira Arantes,2 Yoshimi Sato,3 Jose Enemir dos Santos,1

Elizete Rizzo,2 and Nilo Bazzoli1*

1Ichthyology Department, Graduate Program on Zoology of Vertebrates, Pontifical Catholic University of MinasGerais, Belo Horizonte, Minas Gerais, Brazil2Morphology Department, Institute of Biological Sciences, Federal University of Minas Gerais, Belo Horizonte,Minas Gerais, Brazil3Reproduction Department, Hydrobiology and Fishculture Station of Tres Marias, Tres Marias, Minas Gerais, Brazil

ABSTRACT We studied the relationship between themorphology of the reproductive system and the repro-ductive strategies of six neotropical catfishes using mac-roscopic and microscopic analyses. The reproductive sys-tem of the examined Siluriformes showed diversifiedcharacteristics, but permitted their being groupedaccording to three reproductive strategies: pelagicspawning, demersal spawning, and internally fertilizing.The pelagic spawners Pseudoplatystoma corruscans andConorhynchos conirostris have testes that are character-ized by filiform lobes, absence of testicular secretion,full-grown oocytes of small diameter, thin zona radiata,and cuboidal follicular cells. Pimelodus maculatus ismorphologically distinct from the other two pelagicspawners catfishes due to the presence of testicularsecretion. The demersal spawners Lophiosilurus alexan-dri and Rhinelepis aspera possess homogeneous testicu-lar secretion, large mature oocytes, and columnar follicu-lar cells. The most specialized reproductive system wasobserved in the internally fertilizing Trachelyopterusgaleatus, which possesses a seminal vesicle accessory tothe testes, spermatozoa with elongated nuclei that formspermatozeugmata, and a secretory ovarian lamellarepithelium that is associated with sperm storage. Thereproductive system observed in Neotropical catfishesshowed a relationship associated with the type of fertil-ization and the reproductive strategies of the six speciesstudied. J. Morphol. 272:525–535, 2011. � 2011 Wiley-

Liss, Inc.

KEY WORDS: gonad morphology; secretion; spermato-zeugmata; fertilization type; reproductive strategy

INTRODUCTION

The taxon Siluriformes is represented by 36families and 3,088 known species. They have awide geographical distribution with representationon every continent (Ferraris, 2007). Almost 64% ofthe world’s freshwater siluriform catfishes arefound in South and Central America, 19% occur inAfrica, 15% are present in Europe and SoutheastAsia while only 2% of the species are found inNorth America (Teugels, 1996; Ferraris, 2007).

The adaptive radiation of the South AmericanSiluriformes started during the isolation of SouthAmerica during the Tertiary period (Lowe-McConnell, 1987). The occupation of different eco-logical niches by neotropical catfishes allowed theevolution of diversified morphological patterns(Burguess, 1989; Teugels, 1996), as observedbetween the siluriform families that considered inthis study: Auchenipteridae (driftwood catfishes),Pimelodidae (long-whiskered catfishes), Pseudopi-melodidae (bumblebee catfishes), and Loricariidae(armored catfishes) (Reis et al., 2003). The successthat has been achieved by these catfishes in differ-ent environments is also related to their diversereproductive strategies (Suzuki et al., 2000; Satoet al., 2003; Sato and Godinho, 2004; Godinhoet al., 2009). Several previous studies have dis-cussed the relationship of reproductive strategiesand the morphological characteristics of the repro-ductive systems in Siluriformes (Loir et al., 1989;Meisner et al., 2000; Rizzo et al., 2002; Mazzoldiet al., 2007; Spadella et al., 2008).

The male reproductive system of siluriformmales is morphologically diverse; many siluriformfamilies present testes with digitiform lobes (Loiret al., 1989; Meisner et al., 2000; Santos et al.,2001; Guimaraes-Cruz and Santos, 2004; Lopeset al., 2004), whereas others have compact testeswithout lobes (Loir et al., 1989; Mazzoldi et al.,

Contract grant sponsors: CNPq, FAPEMIG, and FIP PUC Minas.

*Correspondence to: Nilo Bazzoli, Programa de Pos-Graduacaoem Zoologia de Vertebrados, PUC Minas-Av. Dom Jose Gaspar, n500-30535-610, Belo Horizonte-MG, Brazil. E-mail: bazzoli@pucminas.br

Received 16 March 2010; Revised 6 August 2010;Accepted 1 November 2010

Published online 18 January 2011 inWiley Online Library (wileyonlinelibrary.com)DOI: 10.1002/jmor.10931

JOURNAL OF MORPHOLOGY 272:525–535 (2011)

� 2011 WILEY-LISS, INC.

2007). In some catfish families, the testes presentspermatogonia distributed along the cranial andcaudal regions (Guimaraes-Cruz and Santos, 2004;Lopes et al., 2004). In others families, the caudalregion of the testes contains seminal vesicles orsecretory cells without spermatogenic activity thathave secretory and/or storage functions (Legendreet al., 1996; Meisner et al., 2000; Santos et al.,2001). Some species in the families Auchenipteri-dae and Scoloplacidae exhibit internal fertilizationassociated with modifications to the spermatozoonand the reproductive system (Burns et al., 2002;Spadella et al., 2008; Parreira et al., 2009).

Catfish females show some morphological varia-tion in their reproductive systems (Suzuki et al.,2000; Bazzoli, 2003). In general, the vitellogenicoocytes of neotropical Siluriformes, when comparedto those from other teleost orders, present commoncharacteristics such as a thin zona radiata, colum-nar follicular cells, and a jelly coat surroundingthe released eggs (Rizzo et al., 2002; Bazzoli,2003). The histological, histometrical, and histo-chemical variations of the ovarian follicles can beassociated with the different reproductive strat-egies used by catfishes (Suzuki et al., 2000; Santoset al., 2006; Barros et al., 2007).

This present study compares the morphologicalcharacteristics of the testes and ovaries of six neo-tropical catfish species in relation to their repro-ductive strategies.

MATERIALS AND METHODS

Six species (Fig. 1) belonging to four families of Siluriformeswere captured using gillnets between August 2004 and July2008, at the Tres Marias Reservoir (18–208 S; 44–468 W) and atthe Sao Francisco River (17820045@ S; 44856055@ W), in the SaoFrancisco River basin, southeastern Brazil. The fishes werehandled according to the procedures indicated in the Guidelinesfor Animal Experimentation established by the BrazilianCollege for Animal Experimentation (COBEA). Only those that

were sexually mature and in reproductive condition wereselected for this study. Species name, number of specimen perspecies, the ranges of total length (LT), and body mass (MB) aregiven in Table 1 together with data on the reproductive strat-egies of the species with the respective references.

After dissection, the fresh testes and ovaries were photo-graphed and macroscopically analyzed regarding their shape,coloration, and presence of accessory structures. For microscopicanalysis, fragments from the cranial and caudal regions of 77testes and 74 ovaries were fixed in Bouin’s solution for 8 to12 h, embedded in paraffin, cut into 3–5 lm thick sections, andstained with haematoxylin-eosin and Gomori’s trichrome. Inhistological slides, the diameters of 50 vitellogenic oocytes frommature ovaries of each species and the thickness of their sur-rounding layers (zona radiata and follicular cells) were meas-ured using an ocular micrometer ruler attached to an ocularlight microscope.

To determine the histochemical content of proteins and car-bohydrates in the testicular secretions, the zona radiata andthe follicular cells of the vitellogenic oocytes from matureovaries, the following histochemical techniques were used(Pearse, 1985): periodic acid Schiff (PAS), Alcian blue (AB)pH 2.5 and pH 0.5, and hydrolysis with HCl 0.1 M (8 h at608C) for the extraction of sialic acid followed by PAS andAB pH 2.5.

RESULTSMale Reproductive System

Remarkable morphological differences wereobserved among the mature testes of the species.All testes had a continuous central portion fromwhich lobes of varied morphology originated(Fig. 2). Testicular projections in the form of fili-form lobes were found in Trachelyopterus galeatus,Pimelodus maculatus, Pseudoplatystoma corrus-cans, Lophiosilurus alexandri, and Conorhynchosconirostris (Fig. 2a–c). In Rhinelepis aspera, thetesticular lobes were folded (Fig. 2d). In the cra-nial region, the testes of T. galeatus had lobes thatwere longer and thinner and of whitish coloura-tion, whereas in the caudal region seminal vesiclesoccurred with thicker and shorter lobes of pink col-ouration (Fig. 2a).

Fig. 1. Species of catfishes examined with the respective total length: (a) Trachelyopterusgaleatus (18.5 cm). (b) Pimelodus maculatus (24.6 cm). (c) Pseudoplatystoma corruscans (123.2cm). (d) Lophiosilurus alexandri (46.4 cm). (e) Rhinelepis aspera (45.5 cm). (f) Conorhynchosconirostris (67.3 cm).

526 R.M.C. MELO ET AL.

Journal of Morphology

Histologically, the seminiferous tubules from themature testes of the examined species showed ger-minal compartments that communicate with eachother, forming a highly branched system and anas-tomosed tubular system (Fig. 3a–f). The testes ofP. corruscans and C. conirostris exhibited sperma-togenic activity throughout entire length (Fig.4a,b), whereas in T. galeatus, P. maculatus, L.alexandri, and R. aspera, spermatogenic activitywas observed only in the cranial region and secre-tory activity in the caudal region (Fig. 4c,d). Inthese species, the spermatogenic activity was notobserved in the caudal region of the testes. A glob-ular acidophilic secretion associated with sperma-tozoa was detected in the lumen of the secretorytubules and in the spermatic duct of the caudalregion of testes in P. maculatus (Fig. 4c–e). Thissecretion reacted positively to the PAS and AB pH2.5 and 0.5 techniques, indicating the presence ofneutral glycoproteins as well as carboxylic andsulphated acid glycoconjugates. A homogeneousacidophilic secretion associated with spermatozoawas detected in the secretory tubules of the caudalregion of testes in T. galeatus, L. alexandri, and R.aspera (Fig. 4f), which reacted positively to thePAS technique, indicating the presence of neutralglycoproteins. In the testes of P. corruscans and C.conirostris, there was no secretion observed. In P.maculatus, P. corruscans, L. alexandri, R. aspera,and C. conirostris, the heads of the spermatozoawere rounded (Fig. 4g), whereas in T. galeatuswith internal fertilization the head of the sperma-tozoon was elongated (Fig. 4h).

Female Reproductive System

The mature ovaries of the catfishes analyzedhad yellowish coloration with different hues andwere sacciform in shape (Fig. 5). A digitiform pro-tuberance was observed in the cranial region ofthe ovary of C. conirostris (Fig. 5d). In reproduc-tive females, the vitellogenic oocytes had distinctmorphological and histometric characteristics,with the largest full-grown oocytes being inL. alexandri and the smallest in P. corruscans (Ta-ble 2). Vitellogenic oocytes with cuboidal follicularcells were observed in P. maculatus, P. corruscans,and C. conirostris (Fig. 6b). Columnar follicularcells occurred in the other species (Fig. 6a,c). Ellip-tical yolk globules were observed in the vitello-genic oocytes of R. aspera (Fig. 6c). In the otherspecies, yolk globules were spherical as in T. galea-tus and P. corruscans (Fig. 6a,b). The thickest zonaradiata was observed in R. aspera (Fig. 6c), andthe tallest follicular cells were found in T. galeatus(Table 2 and Fig. 6a). The histochemical content ofthe zona radiata and the follicular cells variedamong the Siluriformes studied (Table 2). In theovaries of the catfishes analyzed, no remarkable

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GONAD MORPHOLOGY OF NEOTROPICAL CATFISHES 527

morphological differences were detected among thecranial and caudal regions.

In the lumen of the mature and partiallyspawned ovaries of T. galeatus, folds of the cuboi-dal epithelium from the ovarian lamellae wereobserved containing packed spermatozoa (Fig. 6d).These spermatozoa were found arranged in paral-lel with nuclei strongly associated with eachother and inserted in the apical portion of the epi-thelial cells, characteristic of spermatozeugmata(Fig. 6d,e). The spermatozeugmata were alwaysfound in compact packages stored in the epithelialfolds (Fig. 6d,e). Free and dissociated spermatozoafound inside the female reproductive tract werealways surrounded by a strongly PAS acidophilicsecretion, which contained neutral glycoproteins(Fig. 6e,f).

DISCUSSIONMorphology of the Testes

Filiform or folded lobes of varied morphologywere observed in the testes of the Siluriformes

species examined. Filiform lobes also occur incatfishes from the families Ictaluridae (Sneedand Clemens, 1963), Clariidae (Siscar, 1970),Bagridae (Loir et al., 1989), Auchenipteridae(Meisner et al., 2000; Mazzoldi et al., 2007),Pimelodidae (Santos et al., 2001; Lopes et al.,2004), and Pseudopimelodidae (Barros et al.,2007). Testes in some catfish families are charac-terized by the absence of filiform projections,having elongated testes, as in the families Arii-dae, Helogeneidae, and Callichthyidae (Loiret al., 1989; Mazzoldi et al., 2007), or lobes witha folded aspect, as in the loricarid R. aspera(present study). The seminal vesicles observed inthe caudal region of the testes in T. galeatushave also been reported in catfishes from thefamilies Clariidae, Heteropneustidae, Auchenip-teridae, and Callichthyidae (Siscar, 1970; Loiret al., 1989; Meisner et al., 2000; Mazzoldi et al.,2007) and in acanthomorphs in the familiesBlenniidae, Batrachoididae, and Gobiidae (Rich-tarski and Patzner, 2000; Barni et al., 2001;Mazzoldi et al., 2005).

Fig. 2. Macroscopic characteristics of mature testes of Siluriformes: (a) Filiform lobes and seminal vesicle in the testis of Trache-lyopterus galeatus. (b) Filiform lobes in the testis of Pseudoplatystoma corruscans. (c) Filiform lobes in the testis of Lophiosilurusalexandri. (d) Folded lobes in the testis of Rhinelepis aspera. Fi, filiform lobes; Sv, seminal vesicle; Sd, spermatic duct; Fo, foldedlobes; Cr, cranial; Cd, caudal regions.

In all of the catfish species studied, the testeshave anastomosing seminiferous tubules, a charac-ter of the Siluriformes order and also more ances-tral teleosts (Grier, 1993; Parenti and Grier, 2004).In these fish, the seminiferous tubules are highlybranched and form anastomoses along the entirelength of the testes. In contrast, testes of neote-leosts possess branched lobules that do terminateblindly at the testis’ periphery (Parenti and Grier,2004).

The secretory activity of the testes in Siluri-formes has been attributed to specialized struc-tures or to specific testicular regions (Meisner

et al., 2000; Santos et al., 2001; Guimaraes-Cruzand Santos, 2004; Mazzoldi et al., 2007). In thisstudy, during the reproductive period and immedi-ately after spermiation, an acidophilic secretion,associated with the spermatozoa, was observed inthe secretory tubules in the caudal region of thetestes of T. galeatus, P. maculatus, L. alexandri,and R. aspera. In T. galeatus, this secretion origi-nated in the seminal vesicles, which have both se-cretory and storage functions (Meisner et al., 2000;Parreira et al., 2009). In the species P. maculatus,L. alexandri, and R. aspera, which do not possessseminal vesicles, the origin of the secretion can be

Fig. 3. Transversal sections of Siluriformes testes stained with haematoxylin-eosin (a–f),showing anastomosis in the seminiferous (a, b, c, d, f) and secretory (e) tubules: (a) Trachelyop-terus galeatus. (b) Pimelodus maculatus. (c) Pseudoplatystoma corruscans. (d) Lophiosilurusalexandri. (e) Rhinelepis aspera. (f) Conorhynchos conirostris. Scale bars (a–f) 5 100 lm.

Fig. 4. Transversal sections of Siluriformes testes stained with haematoxylin-eosin (a–h): (a) Lobes and spermatic duct full ofspermatozoa in the mature testis of Conorhynchos conirostris. (b) Detail of spermatogenic cells in the germinal epithelium of theseminiferous tubules of C. conirostris. (c) Acidophilic globular secretion associated with spermatozoa in the lumen of the secretorytubules of the caudal region of partially spent testis of Pimelodus maculatus. (d) Detail of the secretory cells in the epithelium ofthe secretory tubules of P. maculatus. (e) Detail of globular secretion in the spermatic duct of the caudal region of testis of P. macu-latus. (f) Homogeneous acidophilic secretion associated with spermatozoa in the lumen of the secretory tubules of the caudal regionof partially spent testis of Rhinelepis aspera. (g) Lumen of the seminiferous tubules full of rounded-head spermatozoa (inset 1) inthe cranial region of the mature testis of Lophiosilurus alexandri. (h) Lumen of the seminiferous tubules full of elongated-headspermatozoa (inset 2) in the cranial region of the mature testis of Trachelyopterus galeatus. Fi, filiform lobes; Sd, spermatic duct;Spc, spermatogenic cells; Sz, spermatozoa; S, secretion; Sc, secretory cells. Scale bar (a, b, c, e, f, g, h) 5 100 lm; Scale bar (d) andInset (1, 2) 5 500 lm.

attributed to secretory cells located in the epithe-lium of the testes’ caudal region, as has also beenobserved in the catfishes Iheringichthys labrosus,P. maculates, and L. alexandri (Santos et al., 2001;Guimaraes-Cruz and Santos, 2004; Barros et al.,2007). Through histochemical reactions, glycopro-teins and glycoconjugates were detected in thetesticular secretions of the studied catfishes. Thepresence of these compounds suggests that thesesecretions can have similar functions to the secre-tions produced by the seminal vesicles of someother teleosts, which are involved in the matura-tion and nutrition of the spermatozoa and play a

role in fertilization (Lahnsteiner et al., 1990;Mazzoldi et al., 2005; Chowdhury and Joy, 2007).

In general, fishes with external fertilization haveaquasperm with a spherical or ovoid head and areconsidered evolutionarily ancestral (Jamieson, 1991).Fishes with internal fertilization have spermatozoawith elongated head, as observed in catfishes of thefamily Auchenipteridae (Loir et al., 1989; Meisneret al., 2000; Parreira et al., 2009). Our observationsconfirmed such relationships, where spermatozoawith spherical heads occurred in the external fertil-izers P. maculatus, P. corruscans, L. alexandri, R.aspera, and C. conirostris. In T. galeatus, a species

Fig. 5. Macroscopic characteristics of mature ovaries of Siluriformes: (a) Sacciform ovaries ofTrachelyopterus galeatus. (b) Sacciform ovaries of Lophiosilurus alexandri. (c) Sacciform ovariesof Pimelodus maculatus. (d) Sacciform ovaries with cranial diverticulum of Conorhynchosconirostris.

TABLE 2. Histometrical and histochemical characteristics of vitellogenic oocytes of the Neotropical catfishes analyzed: mean 6 S.E.oocyte diameter (OD), thickness and histochemical content of the zona radiata (ZR), and follicular cells (FC)

Species

Histometry Histochemistry

OD (lm) ZR (lm) FC (lm) ZR FC

T. galeatus 813.8 6 91.4 1.2 6 0.3 98.4 6 7.6 NGP NGP 1 GPSP. maculatus 496.1 6 65.3 1.7 6 0.6 25.4 6 5.2 NGP 1 CGC NGP 1 SGCP. corruscans 488.6 6 53.1 1.2 6 0.4 18.8 6 2.9 NGP 1 CGC NGP 1 SGCL. alexandri 1505.8 6 197.1 1.5 6 0.5 38.9 6 4.3 NGP NGP 1 CGCR. aspera 956.2 6 182.7 4.8 6 1.0 52.3 6 9.1 NGP NGP 1 CGCC. conirostris 523.3 6 66.0 1.8 6 0.4 29.8 6 5.7 NGP 1 CGC NGP 1 SGC

NGP, neutral glycoproteins; GPS, glycoproteins rich in sialic acid; CGC, carboxylic acid glycoconjugates; SGC, sulphated acid glyco-conjugates.

with internal fertilization, spermatozoa wereobserved having elongated heads which are organizedinto compact packages of spermatozeugmata. In inter-nally fertilizing teleosts, nuclear elongation of thespermatozoa facilitates their passage through the lob-ular gonopodium of the males and into the labyrinthicstructures of the females, in addition to facilitatingformation of the spermatozeugmata (Jamieson, 1991;Burns and Weitzman, 2005). The spermatozeugmatain Trachelyopterus lucenai and Auchenipterus nucha-

lis are associated with the secretion from the epithe-lial cells in the seminal vesicles, whose function is tointegrate and maintain the spermatozeugmata pack-ages (Burns et al., 2002; Mazzoldi et al., 2007).

Morphology of the Ovaries

In all the species examined, the female repro-ductive system had an anatomical organization asfound in most teleosts. The paired ovaries are of

Fig. 6. Transversal sections of Siluriformes ovaries stained with haematoxylin-eosin (a, c, d, e, f) and Gomori’s Trichromic (b): (a)Detail of the vitellogenic oocyte of Trachelyopterus galeatus, showing spherical yolk globules, cortical alveoli with large vesicles, thin zonaradiata, columnar follicular cells, and conjunctive theca. (b) Detail of the vitellogenic oocyte of Pseudoplatystoma corruscans, showingspherical yolk globules, thin zona radiata, and cuboidal follicular cells. (c) Detail of the vitellogenic oocyte of Rhinelepis aspera, showing el-liptical yolk globules, cortical alveoli with small vesicles, thick zona radiata, and columnar follicular cells. (d) Spermatozeugmata packagesinserted in the apical portion of the cuboidal epithelium folds in the mature ovaries of T. galeatus. (e) Spermatozeugmata stored in the ovar-ian epithelium and dissociated spermatozoa surrounded by acidophilic secretion in the mature ovaries of T. galeatus. (f) Dissociated sper-matozoa surrounded by abundant ovarian secretion of T. galeatus. Yg, yolk globules; Ca, cortical alveoli; Zr, zona radiata; Fc, follicular cells;T, theca; E, ovarian epithelium; Szg, spermatozeugmata; Vo, vitellogenic oocyte; Sz, spermatozoa; S, secretion. Scale bars (a–f)5 200 lm.

the cystovarian type, in which the ovarian lumenis continuous with the gonoduct located where theoocytes reach the external environment (Naga-hama, 1983; Bazzoli, 2003). The coloration of thevitellogenic oocytes from the studied catfishes isyellowish with their hue varying among the spe-cies. The same coloration pattern was observed ineight Siluriformes species with the exception ofPseudopimelodus charus, which have greenoocytes (Sato et al., 2003). The yellow coloration ofthe oocytes is probably due to the presence ofcarotenoid pigments, which include endogenousoxygen sources to be used when the respiratorysystem is inefficient in obtaining exogenous oxygen(McElman and Balon, 1980).

Variations in the egg diameter can be related tothe different reproductive strategies of the fishes(Suzuki et al., 2000; Kolm and Ahnesjo, 2005).The diameter of the full-grown oocytes variedamong the siluriforms analyzed, being largest inL. alexandri and smallest in P. corruscans. Themigratory species P. corruscans, P. maculates, andC. conirostris, with smaller full-grown oocytes,have high absolute fecundity, non-adhesive eggs,and do not display parental care, whereas thenon-migratory species L. alexandri and R. aspera,with larger vitellogenic oocytes, have low fecun-dity, adhesive eggs, and exhibit parental care(Rizzo et al., 2002; Sato et al., 2003; Godinhoet al., 2009).

The thickness of the zona radiata in teleosts canreflect adaptations to different ecological conditions(Fausto et al., 2004; Santos et al., 2006); demersaleggs tend to have a thicker zona radiata than pe-lagic eggs to avoid injury to the developing embryo(Stehr and Hawkes, 1979; Riehl, 1996). Rhinelepisaspera has demersal eggs and spawns on rockysubstrates where the eggs can incur abrasion (Satoet al., 2003). This species has vitellogenic oocyteswith a thick zona radiata, as has also beenobserved in some loricariid catfishes (Suzuki et al.,2000). Lophiosilurus alexandri also has demersaleggs, but this species spawns on sandy substrates(Sato et al., 2003; Barros et al., 2007). Conse-quently, its eggs are subject to a less physical dam-age and have thinner zona radiata compared to R.aspera. The species P. maculatus, P. corruscans,and C. conirostris spawns at the surface of thewater and their pelagic eggs disperse freely down-stream (Sato and Godinho 2004; Godinho et al.,2007). These species also have thin zona radiata.

The morphology of the follicular cells is vari-able depending on the species and the stage ofoocyte’s development (Suzuki et al., 2000; Baz-zoli, 2003). Normally, columnar follicular cellssurrounding vitellogenic oocytes have greatersynthesizing capacity (Favaro et al., 2005; San-tos et al., 2006). This is probably related to theirability to synthesize mucosubstances that aretransferred to the surface of the zona radiata,

aiding in the egg’s adhesiveness and facilitatingparental care, as has been observed in the catfishesSilurus glanis and L. alexandri (Abraham et al.,1993; Barros et al., 2007). In fact, during this studythe tallest follicular cells were observed in the vitel-logenic oocytes of T. galeatus, L. alexandri, and R.aspera, which have adhesive eggs and parentalcare. Regarding T. galeatus, the results of thisstudy and the information available in literatureare not sufficient enough to state that the speciesexhibits parental care.

In the mature ovaries of the catfishes examined,the histochemical analyses of the zona radiata andthe follicular cells showed differences in contentbetween migratory and non-migratory catfishes.The neutral glycoproteins associated with thecarboxylic acid glycoconjugates found in the follic-ular cells of the non-migratory L. alexandri andR. aspera can form mucosubstances that are trans-ferred to the zona radiata, conferring adhesivenessto the eggs, as observed in other Neotropicalcatfishes (Favaro et al., 2005; Santos et al., 2006;Barros et al., 2007).

In this study, spermatozeugmata packages wereobserved stored in narrow and complex folds of thecuboidal lamellar epithelium in T. galeatusfemales. In Siluriformes, internal fertilization wasobserved only in the families Auchenipteridae andScoloplacidae (Loir et al., 1989; Meisner et al.,2000; Burns et al., 2002; Mazzoldi et al., 2007;Spadella et al., 2008; Parreira et al., 2009). Thespermatozeugmata stored in the epithelial cellslining ovarian lamellae of the mature and partiallyspawned ovaries of T. galeatus may represent animportant strategy to maintain the viability of thespermatozoa for long periods. Meisner et al. (2000)state that these spermatozoa can remain in theovaries for 6 months in T. lucenai. The abundantacidophilic secretion observed in the ovarianlumen of T. galeatus, during the reproductiveperiod, appears to be secreted by ovarian lamellarepithelium, as reported in the teleosts Syngnathusscovelli (Begovac and Wallace, 1987) and Alcich-thys alcicornis (Koya et al., 1995). This secretionwas always detected associated with free sperma-tozoa inside the female’s reproductive tract ofT. galeatus. Histochemical analyses revealed thepresence of neutral glycoproteins in this secretion,which due to their chemical nature, may possiblyact as an energy source for the spermatozoa(Chowdhury and Joy, 2007).

In conclusion, the morphological specializationsin males are superimposed upon the constancy of acommon testis type, regardless of external mor-phology, where the germinal compartment is com-posed to anastomosing tubules in all of the speciesexamined. Comparison of reproductive characters,including gonad morphology of males and females,among six species of catfishes reveals a clear rela-

tionship between fertilization type and reproduc-tive strategy.

ACKNOWLEDGMENTS

The authors wish to thank the technicians atthe Tres Marias Hydrobiology and FishcultureStation (CODEVASF) for their assistance duringthe collection of biological material, the laboratorytechnician Rogerio Silva Matos for the preparationof the histological slides, and two anonymousreferees for the review and improve of the manu-script.

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Comparative morphology of the gonadal structure related to reproductive strategies in six species of...

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