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Tissue and Cell 38 (2006) 303–310

Ovarian follicle growth in the catfish Iheringichthys labrosus(Siluriformes: Pimelodidae)

J.E. Santos a,b, G.E.V. Padilha b, O. Bomcompagni-Junior b,G.B. Santos b, E. Rizzo a, N. Bazzoli a,b,∗

a Department of Morphology, Institute of Biological Sciences, Federal University of Minas Gerais, Brazil,P.O. Box 486, 30 161-970 Belo Horizonte, Minas Gerais, Brazil

b Graduate Programme on Vertebrate Zoology, Catholic University of Minas Gerais, 30 535-610 Belo Horizonte, Minas Gerais, Brazil

Received 8 April 2006; received in revised form 13 July 2006; accepted 27 July 2006Available online 22 September 2006

bstract

The morphofunctional organisation of the female reproductive system, the oocyte growth and the follicular envelope ultrastructure weretudied by the first time in the catfish Iheringichthys labrosus from Upper Parana River basin, Southeastern Brazil, in order to contributeo the knowledge of the reproductive behaviour strategies of this species. As in other Neotropical freshwater siluriforms, the ovaries are ofhe cystovarian type, the oocytes develop in an asynchronous pattern and mature oocytes are released in clusters in the ovarian lumen, beingransported through the oviduct to the urogenital papilla. During the primary growth, nuclear material is transported to the ooplasm, forminghe yolk nucleus, where proliferate membranous organelles. The onset of the zona radiata formation occurs during the late perionucleolartage with the deposition of the outer layer. At the vitellogenic stage, this envelope reaches 6.35 ± 0.84 �m of thickness, being constitutedy three distinct layers crossed by pore-canals containing oocyte and follicular cells processes. Cytochemical analyses evidence neutrallycoproteins in cortical alveoli, yolk globules and zona radiata. Follicular cells with squamous shape during the primary growth acquire

ynthetic activity at the secondary growth, reaching 37.82 ± 4.72 �m in height at the mature vitellogenic follicles. These cells accumulateulphated polysaccharides in large electron-lucent vesicles during the vitellogenic stage which are possibly secreted to form a mucous coat athe egg surface. These evidences suggest that I. labrosus may have adhesive eggs as also detected in other Neotropical freshwater Siluriformes.

2006 Elsevier Ltd. All rights reserved.

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eywords: Iheringichthys labrosus; Follicular cell; Oocyte; Jelly coat; Zon

. Introduction

Siluriformes exhibit large morphological and behaviouraliversities, inhabiting rivers, lagoons, reservoirs and smalltreams in the tropical regions, especially in South America,frica and Southeast Asia. The family Pimelodidae, with ca.00 species, constitutes a heterogeneous group with at leasthree monophyletic assemblages: Pimelodinae, Rhamdiinae

nd Pseudopimelodinae (de Pinna, 1998). The Pimelodinaeheringichthys labrosus (Lutken, 1874) is a non-migratorypecies with 27 cm of maximum body length, reproduces

∗ Corresponding author. Tel.: +55 31 3319 4269; fax: +55 31 3319 4938.E-mail address: bazzoli@pucminas.br (N. Bazzoli).

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040-8166/$ – see front matter © 2006 Elsevier Ltd. All rights reserved.oi:10.1016/j.tice.2006.07.002

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long the year in reservoirs of the Southeastern Brazil,resenting multiple spawning, reproductive peak synchro-ised with the rainy season and no parental care behaviourAgostinho and Julio Jr., 1999; Santos et al., 2004).

In non-mammalia vertebrates, the oogenesis has been fre-uently divided in two phases: a prolonged growth whenhe oocytes are arrested at diplotene of the first meioticivision, and a maturational phase, when occurs the meio-is resumption and full-grown oocytes become apt to fer-ilization (Nagahama et al., 1995). The primary growth,

onadotrophin-independent, is characterised by the perin-cleolar oocytes originated from the oogonia, which keeproliferating for renewing the oocyte stock in adult femalesJalabert, 2005). During the secondary growth, occurs the

304 J.E. Santos et al. / Tissue and Cell 38 (2006) 303–310

Figs. 1–4. Organisation of the female reproductive system of I. labrosus. (1) Resting ovaries and oviduct (arrow) (×2.4). (2) Histological section of restingo s lamels vitellof

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varies with initial (O1) and late (O2) perinucleolar oocytes in the ovigerouection of maturing ovary with predominance of previtellogenic (O3) andollicular cells (FC) and thin connective theca (×96).

ormation of the cortical alveoli and the vitellogenesis undernfluence of gonadotrophins (Selman and Wallace, 1989;yler and Sumpter, 1996; Patino and Sullivan, 2002).

Unlike the mammals, the female reproductive system isighly variable among the teleosts, reflecting the wide rangef reproductive patterns and the different strategies of devel-

pment. Despite the diversity, the ovaries have a basic generaltructure in the most gonochoristic species, with oviger-us lamellae projecting into the ovarian lumen, which isirectly connected to the oviduct and then to genital papilla, a

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lae (×50). (3) Mature ovaries and oviduct (arrow) (×2.4). (4) Histologicalgenic (O4) oocytes. Follicular envelope constituted by zona radiata, high

ystovarian-type organisation (Helfman et al., 2000). In con-rast, ovaries of sturgeons and bowfin of the genus Amia asell as salmonids show ovigerous lamellae opening on theody cavity, where mature oocytes are directly released atvulation. Such pattern is known as gymnovarian-type, andhe oocytes of these species can remain stocked for some time

efore spawning (Helfman et al., 2000; Jalabert, 2005).

In spite of the common ovarian structure, the follicles mor-hology varies according to reproductive behaviour patterns,eing similar among species belonging to the same taxo-

J.E. Santos et al. / Tissue and Cell 38 (2006) 303–310 305

Figs. 5–10. Ultrastructure of the oogenesis in I. labrosus during the primary growth. (5) Oogonium with few condensed chromatin and a very developednucleolus, mitochondria, nuage and annulate lamellae (×6600). (6) Follicular envelope constituted by squamous follicular cells (FC), basement membrane(BM) and thin connective theca (T) with fibroblast-like cells. Microvilli (arrow) of oocytes project to the follicular cell during initial perinucleolar stage(×11200). (7) Deposition of the electron-dense material of the zona radiata (ZR) among the microvilli (arrow) of the oocyte during the late perinucleolar stage.The follicular cells (FC) show cisterns of endoplasmic reticulum and developed connective theca (T) (×16700). (8) Transference of electron-dense materialfrom nucleus (N) to ooplasm (O) (×12650). (9) Initial formation of the yolk nucleus (×14320). (10) Proliferation of membranous organelles in the yolk nucleusduring the late perinucleolar stage (×12540).

306 J.E. Santos et al. / Tissue and Cell 38 (2006) 303–310

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omic group (Bazzoli, 1992). During the folliculogenesis,here are remarkable morphological changes in the nucleusnd cytoplasm of the oocyte as well as in the zona radiata,ollicular cells and thecal layer (Grier, 2000). The eggs ofhe several siluriforms present a layer with gelatinous aspect,elly coat, covering the zona radiata, and this envelope mighte related to the egg capability to adhere to the substrateRizzo et al., 2002).

The present study was intended to analyse the morpho-unctional organisation of the female reproductive system of. labrosus, the oocyte growth and follicle envelopes duringhe gonadal maturation, in order to provide knowledge of thetrategies of reproductive behaviour of this species in wildnd also as a probable biological model among the Siluri-ormes.

. Materials and methods

A total of 125 adult females of I. labrosus (8.1–24.0 cmf standard length and 9.7–204.0 g of body weight) wereaptured bimonthly during 1998 in the Furnas reservoir20◦40′S; 46◦19′W), located in Grande River, Southeasternrazil. The fish were dissected, and anatomical relations of

he ovaries with other organs of the body cavity were estab-ished. The body weight (BW), gonadal weight (GW) and theonadossomatic index (GSI = 100 GW BW−1) were deter-ined for each specimen.Samples of the ovaries were fixed in Bouin’s solution

or 8–12 h, embedded in paraffin or in glycol-methacrylatelastic resin, sectioned at 3–5 �m thickness and stained withematoxylin-eosin or with 1% toluidine blue-sodium borateolution for histological analyses. Thicknesses of the zonaadiata, height of the follicular cells and oocytes diame-er were determined using a micrometric ocular coupled toight microscopy (Mean ± S.D.). During each stage of oocyteevelopment, 100 cells of the oogenic lineage were measured,sing 10–15 histological sections.

The followed histochemical techniques were used for theetection of carbohydrates and proteins (Pearse, 1985): peri-dic acid-Schiff (PAS), Alcian blue (AB) at pH 2.5 and pH.5 and ninhydrin-Schiff (NS). For lipid detection, ovariesragments were fixed in 10% formalin, cut at 10 �m thick-ess in a cryostat, and submitted to reactions of the Sudan

lack B and Nile blue sulphate.

Fragments of ovaries in different gonadal maturationtages were fixed in 2.5% glutaraldehyde in 0.1 M phos-hate buffer at pH 7.3 for 8–10 h a 4 ◦C. The post-fixation

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igs. 11–16. Ultrastructure of the follicular envelope in I. labrosus during the seche pore-canals and evident layers. Cuboidal follicular cells (FC) has characteristicsrevitellogenic stage: (Z1) inner zona radiata; (Z2) middle zona radiata; (Z3) ou×10140). (13) During the vitellogenic stage, large vacuoles (*) with electron-lucidells (FC). The zona radiata (ZR) is more compacted (×8140). (14) During late vitelf the follicular cells (×3950). (15) PAS-positive reaction at the zona radiata (ZR)ositive reaction at the follicular cells (FC) in AB pH 0.5 (×220).

ell 38 (2006) 303–310 307

as performed in 1% osmium tetroxide with 1.5% potas-ium ferrocyanide during 30 min. Following, the specimensere embedded in epon-araldite plastic resin, the ultra-thin

ections were contrasted using uranyl acetate and lead citratend examined to the transmission electron microscope.

. Results

The ovaries of I. labrosus are paired, saculiform organs,ttached dorsally to the body cavity by the mesovarium,stablishing anatomical relations with the swim bladder andhe kidneys dorsally and with the intestine ventrally. Left andight ovaries join at the caudal portion forming the commonvarian duct that communicates with the genital papilla. Inhe ovaries, folds of the germinal epithelium and connec-ive tissue towards the ovarian lumen form the ovigerousamellae, where oogonia nests originate oocytes which goingnto the meiotic prophase. The volume and the colorationf the ovaries change during the gonad maturation. Rest-ng ovaries are thin, whitish, and translucent cords, withSI = 0.62 ± 0.44 and presenting oogonia nests and perin-cleolar oocytes in the ovigerous lamellae (Figs. 1 and 3).ature ovaries are yellowish, have increased volume withSI = 4.55 ± 2.22 and predominance of vitellogenic oocytes

Figs. 2 and 4).The oocyte growth and the follicular envelopes were anal-

sed according to histological and ultrastructural characteris-ics of the nucleus, ooplasm and surrounding follicular layers:

Oogonia (diameter of 14.83 ± 3.69 �m): precursor cellsf the oogenic lineage form nests which originate oocytesn the ovigerous lamellae. They are rounded cells, have aucleus with finely granular chromatin, a single prominentucleolus, cytoplasm with mitochondria, free ribosomes andnnulate lamellae associated to light vesicles with lamellartructures (Fig. 5).

Early perinucleolar oocytes (106.03 ± 10.73 �m): theyresent a strongly basophilic cytoplasm and a central vesicu-ous nucleus with several peripheral nucleoli. The follicularnvelope is formed by a layer of squamous follicular cells, aasal membrane and a thin connective theca. Short microvillif the oocyte project towards the follicular cells (Fig. 6).

Late perinucleolar oocytes (169.87 ± 17.40 �m): theyave a finely granular basophilic cytoplasm, vesiculous

ucleus and several nucleoli closed to the nuclear envelope.he formation of the zona radiata (2.38 ± 0.21 �m thick-ess) initiates with the deposition of the outer layer. Theollicular cells (4.60 ± 1.27 �m thickness) acquire charac-

ondary growth. (11) Transversal section of the zona radiata (ZR) showingof protein synthesis (×5660). (12) Zona radiata shows three layers during

ter zona radiata. Vacuoles (*) appear in cytoplasm of the follicular cellsmaterial accumulate progressively in the apical cytoplasm of the follicular

logenic phase, the large vacuoles (*) are in coalescence filling the cytoplasmand PAS-negative reaction at the follicular cells (FC) (×220). (16) Highly

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eristic of synthesis activity, the basal membrane is thin andhe theca presents fibroblast-like cells (Fig. 7). During thistage, occur the transference of electron-dense material fromhe nucleus to the ooplasm (Fig. 8) to form the yolk nucleushich show association with cytoplasmic organelles in for-ation (Figs. 9 and 10). This structure is initially located

ear the nucleus, then migrates progressively to the corticaloplasm and at last disperses.

Previtellogenic oocytes (338.13 ± 29.05 �m): The baso-hilic nature of the cytoplasm gradually diminishes with thencrease in the diameter of the oocytes and cortical alveolire formed in the peripheral ooplasm. The nucleus is central,nd the several nucleoli remain closed to the nuclear enve-ope. The zona radiata (3.66 ± 0.61 �m thickness) is crossedy pore-canals containing oocyte microvilli which interactith the follicular cells (Fig. 11). It has three layers: anuter electron-lucent layer, a thin middle layer and a thicklectron-dense internal layer (Fig. 12). The cuboidal follicu-ar cells (7.73 ± 2.07 �m height) present synthesis organellesnd large electron-lucent vesicles accumulated at the apicalytoplasm (Figs. 11 and 12).

Vitellogenic oocytes (566.08 ± 54.04 �m): these cells pre-ent round acidophilic yolk globules occupying mostoplasm, cortical alveoli closed the oocyte membrane andcentral or eccentric nucleus. The zona radiata (6.35 ±

.84 �m thickness) has a more developed inner layer, theore-canals are thinner and a finely granular material iseposited into the vacuoles of the follicular cells (Fig. 13).uring late vitelogenic stage, high prismatic follicular cells

37.82 ± 4.72 �m height) have ooplasm full of electron-ucent vesicles in coalescence (Fig. 14).

Cytochemical reactions indicated the presence of neutrallycoproteins in the zona radiata as demonstrated by positiveeactions to PAS and NS (Fig. 15). The follicular cells weretrongly AB-positive in both pH 2.5 and 0.5 (Fig. 16) indi-ating the presence of acidic polysaccharides-rich in sulphateadicals. Acid hydrolysis followed by AB pH 2.5 excludedhe presence of sialic acid in the follicular cells. Cortical alve-li, yolk globules and follicular cells were also PAS-positive.he yolk globules also contained neutral lipids as showed byositive reactions to Sudan black B and Nile blue sulphate.

. Discussion

Although several studies have examined the structuralrganisation of the male reproductive system, little empha-is has been ascribed to the cellular and molecular aspectsf the female reproduction in Neotropical freshwater Siluri-ormes, being this knowledge essential for comprehensionf the reproductive strategies of the species. In I. labro-us, despite the unusual structural pattern of the testes, the

emale reproductive system exhibit common morphologicalrganisation similar to most species with external fertiliza-ion, with ovaries of cystovarian type, which are anatomi-ally related to swim bladder and kidneys dorsally into the

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ell 38 (2006) 303–310

oelomic cavity as was also detected in Pimelodus maculatusOliveira-Junior, 2002), Conorynchos conirostris (Ribeiro,002), Pseudoplatystoma corruscans (Brito and Bazzoli,003) and Lophiosilurus alexandri (Barros, 2006). However,ytochemical and ultrastructural analyses show variationsmong the siluriforms, mainly in the follicular envelopes dur-ng the secondary oocyte growth, reflecting adaptations forhe egg development in different habitats.

Oogenesis in I. labrosus follows the general pattern ofeleosts, with the proliferation of oogonia from the germinalpithelium and the oogonia differentiating in oocytes aftereveral mitotic divisions (Grier, 2000). Perinucleolar oocytesre found during all gonadal maturation acting as reservetock for next reproductive cycle (Selman and Wallace,989). The electron-dense materials transported from theucleus to the ooplasm contain ribonucleoproteins that formhe yolk nucleus, where membranous organelles proliferateTyler and Sumpter, 1996; Patino and Sullivan, 2002).

The previtellogenic oocytes of I. labrosus are charac-erised by the presence in the ooplasm of cortical alveoli thatontain neutral glycoproteins corroborating previous studiesBazzoli and Godinho, 1994). The glycoproteins of the cor-ical alveoli have endogenous origin with the participation ofhe rough endoplasmic reticulum and the Golgi complex ofhe oocyte in their formation (Selman and Wallace, 1989).hese substances are released into the perivitelline spaceuring fertilisation acting in the mechanism of blockage toolyspermy (Tyler and Sumpter, 1996; Micale et al., 1999).

The vitellogenesis is an important stage of the develop-ent, when the oocytes accumulate nutrients for the embryo

evelopment (Kayaba et al., 2001). In the present studyas registered about 70% increase of the oocyte diam-

ter during the secondary growth. According to Selmannd Wallace (1989), the deposition of yolk proteins con-ributes with 80–90% of the dry weight of the ovary, beinghe main responsible for the oocyte growth. In I. labrosus,olk was stored in granules or globules until the end ofhe oocyte maturation, exhibiting no fusion or liquefactionf their contents. The proteolysis and the fusion of yolklobules to form a vitellogenic fluid mass make the eggsransparent, a characteristic of marine species that presentreovulatory hydration (Selman and Wallace, 1989; Tylernd Sumpter, 1996). In teleosts, it has been demonstratedhat vitellogenin is synthesised in the liver in response tostradiol-17ß are released into the blood and then trans-orted to the ovary (Matsubara and Sawano, 1995). The vitel-ogenin is a phospholipoglycoprotein with high molecular

ass, which is incorporated into oocytes during the matu-ation and cleaved proteolytically into smaller yolk proteinsJalabert, 2005), justifying the positive reactions to PAS, NS,udan black B and Nile blue sulphate in the yolk globulesf I. labrosus.

As in other vertebrates, the oocyte is surrounded by theona radiata and follicle envelope that consist of follicularells and theca separated by a basal membrane. The zonaadiata contains neutral glycoproteins that, depending on

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he species, can be associated with acidic polysaccharidesBazzoli, 1992). In the catfish I. labrosus, the zona radi-ta contains only neutral glycoproteins as also registered forther pimelodids as P. corruscans and L. alexandri (Bazzoli,992; Rizzo et al., 1998). The zona radiata is complex, gen-rally formed by two layers crossed by pore-canals that arelled by the microvilli of the oocytes or processes of the fol-

icular cells (Selman and Wallace, 1989). These microvillietermine formation and orientation of the pore-canals of theona radiata (Giulianini and Ferrero, 2000). In I. labrosus theuter layer of the zona radiata is formed during late perin-cleolar stage, by the deposition of electron-dense materialetween the microvilli of the oocytes and the follicular cells.uring the vitellogenic stage, the zona radiata is constitutedy three distinct layers. The middle layer is the most electron-ense as also observed in other species (Cruz-Hofling andruz-Landim, 1989; York et al., 1993). The thickness and

tructure of the zona radiata may reflect adaptations to differ-nt ecological conditions. Therefore, pelagic eggs of marinepecies tend to have a thinner envelope than demersal fresh-ater ones (Stehr and Hawkes, 1979).Several structures are found in the egg surface of neotrop-

cal teleosts: filaments, globules, villi, knobs, fibrillar net,dhesive disc and jelly coat (Rizzo and Godinho, 2003). Inhe vitellogenic oocytes of I. labrosus a finely granular mate-ial was observed into the vacuoles of the follicular cells. Thisaterial appear to be similar to the jelly coat found in the sil-

riform Silurus glanis (Abraham et al., 1993), that undergoeshemical alterations after spawning to allow the eggs adher-nce among them and to substrate (Laale, 1980).

The follicular cells originate from the germinal epithe-ium when prefollicular cells emit processes that surround theocytes in meiotic division (Grier, 2000). The basic structuref the ovarian follicle is established when the prefollicularells and the basal membrane completely surround the oocytet late pachytene or early diplotene (Patino and Sullivan,002). The morphology of follicular cells is variable, depend-ng on the species and oocyte development stage (Bazzoli,992). In I. labrosus, these cells were squamous during therimary growth of the oocyte, cuboidal in the previtellogenictage and at last high prismatic during vitellogenesis. Duringhe secondary growth, the follicular cells acquire organellesf synthesis and glycidic molecules rich in sulphate radicalsccumulate progressively in the electron-lucent vesicles ofhe cytoplasm. Since that these molecules are characteristic ofhe cell surface, mediating the cell-extracellular matrix inter-ctions in vertebrates (Alberts et al., 2002), then the resultsf the present study indicate that the catfish I. labrosus mayave adhesive eggs similar to other Neotropical freshwateriluriforms as L. alexandri.

cknowledgements

The authors are grateful to the staff of the Furnas Hydro-iology and Fishery Station (Furnas Centrais Eletricas S/A)

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ell 38 (2006) 303–310 309

or the assistance during the collection of the fishes, to thelectron Microscopy Centre CEMEL/UFMG and the Brasil-

an Research Foundations: CNPq, FAPEMIG and FIP–PUCinas for financial support.

eferences

braham, M., Hilge, V., Riehl, R., Iger, Y., 1993. Muco-follicle cells of thejelly coat in the oocyte envelope of the sheatfish (Silurus glanis L.). J.Morphol. 217, 37–43.

gostinho, A.A., Julio Jr., H.F., 1999. Peixes da bacia do alto rio Parana.In: Lowe-Mcconnell, R. (Ed.), Estudos ecologicos de comunidades depeixes tropicais. Traducao: Vazzoler, A.E.A.M., Agostinho, A.A., Cun-nighan, P.: EDUSP, Sao Paulo, pp. 375–400.

lberts, B., Johnson, A., Lewis, J., Raff, M., Roberts, K., Walter, P., 2002.The Molecular Biology of the Cell, fourth ed. Garland Publishing, NewYork, p. 1463.

arros, M.D.M., 2006. Morfologia gonadal e gametogenese de Lophiosil-urus alexandri Steindachner, 1877 (Siluriformes: Pseudopimelodidae)do rio Santo Antonio, bacia do rio Doce, Joanesia, Minas Gerais, Brasil.Dissertacao (Mestrado em Zoologia de Vertebrados)—Programa de Pos-graduacao em Zoologia de Vertebrados da PUC Minas, Belo Horizonte,62 pp.

azzoli, N., 1992. Ovogenese em peixes teleosteos neotropicais de aguadoce. Tese (Doutorado em Ciencias)—Instituto de Ciencias Biologicas,Universidade Federal de Minas Gerais, Belo Horizonte, 182 pp.

azzoli, N., Godinho, H.P., 1994. Cortical alveoli in oocytes of freshwaterneotropical teleost fish. Boll. Zool. 61, 301–308.

rito, M.F.G., Bazzoli, N., 2003. Reproduction of the surubim catfish Pseu-doplatystoma coruscans (Pisces, Pimelodidae) in the Sao Francisco river,Pirapora region, Minas Gerais, Brazil. Arq. Bras. Med. Vet. Zootec. 55(5), 624–633.

ruz-Hofling, M.A., Cruz-Landim, C., 1989. Electron microscopic studieson the development of the chorion of Astyanax bimaculatus (Teleostei:Characidae). Zool. Jb. Anat. 119, 241–249.

e Pinna, M.C.C., 1998. Phylogenetic relationships of Neotropical Silu-riformes (Teleostei: Ostariophysi): Historical Overview and synthesisof hypotheses. In: Malabarba, L.R., Reis, R.E., Vari, R.P., Lucena,Z.M.S., Lucena, C.A.S. (Org.), Phylogeny and classification of Neotrop-ical fishes. Porto Alegre: EDIPUCRS, pp. 279–330.

iulianini, P.G., Ferrero, E.A., 2000. Ultrastructural aspects of the ovarianfollicle and egg envelope of the sea-grass goby Zosterisessor ophiocelus(Osteichthyes, Gobiidae). Ital. J. Zool. 68, 29–37.

rier, H.J., 2000. Ovarian germinal epithelium and folliculogenesis in thecommon snook, Centropomus undecimalis (Teleostei: Centropomidae).J. Morphol. 243, 265–281.

elfman, G.S., Collette, B.B., Facey, D.E., 2000. Teleosts at last I: Bony-tongues through Anglerfishes. In: The diversity of fishes. Blackwell,Massachusetts, pp. 221–243.

alabert, B., 2005. Particularities of reproduction and oogenesis in teleostfish compared to mammals. Reprod. Nutr. Dev. 45, 261–279.

ayaba, T., Takeda, N., Adachi, S., Yamauchi, K., 2001. Ultrastructure of theoocytes of the Japanese eel Anguilla japonica during artificially inducedsexual maturation. Fisheries Sci. 67, 870–879.

aale, H.W., 1980. The perivitelline space and egg envolopes of bony fishes:a review. Copeia 2, 210–226.

atsubara, T., Sawano, K., 1995. Proteolytic cleavage of vitellogenin andyolk proteins during vitellogenin uptake and oocyte maturation in barfinflounder (Verasper moseri). J. Exp. Zool. 272, 34–45.

icale, V., Maricchiolo, G., Genovese, L., 1999. The reproductive biology

of the amberjack, Seriola dumerilli (Risso, 1810). I. Oocyte developmentin captivity. Aquac. Res. 30, 349–355.

agahama, Y., Yoshikuni, M., Yamashita, M., Tokumoto, T., Katsu, Y., 1995.Regulation of the oocyte growth and maturation in fish. Curr. Top. Dev.Biol. 30, 103–145.

3 e and C

O

P

P

R

R

R

R

S

S

S

TRev. Fish Biol. Fish. 6, 287–318.

10 J.E. Santos et al. / Tissu

liveira-Junior, R.L., 2002. Analise comparativa da reproducao do mandi-amarelo, Pimelodus maculatus Lacepede, 1803 (Pisces, Pimelodidae) emdois trechos do rio Sao Francisco, MG. Dissertacao (Mestrado em Biolo-gia Celular)—Departamento de Morfologia, curso de pos-graduacao emBiologia Celular, UFMG, Belo Horizonte, MG, 43 pp.

atino, R., Sullivan, C.V., 2002. Ovarian follicle growth, maturation, andovulation in teleost fish. Fish Physiol. Biochem. 26, 57–70.

earse, A.G.E., 1985. Histochemistry: theoretical and applied. ChurchillLivingstone, London, p. 1055.

ibeiro, D.C.J., 2002. Biologia reprodutiva do pira Conorhynchosconirostris Valenciennes, 1840 (Pisces: Pimelodidae) do rio Sao Fran-cisco, regiao de Pirapora, Minas Gerais. Dissertacao (Mestrado emZoologia de Vertebrados)—Programa de Pos-graduacao em Zoologiade Vertebrados da PUC Minas, Belo Horizonte, 60 pp.

izzo, E., Moura, T.F.C., Sato, Y., Bazzoli, N., 1998. Oocyte surface in

four teleost fish species postspawning and fertilization. Braz. Arch. Biol.Technol. 41 (1), 37–48.

izzo, E., Sato, Y., Barreto, B.P., Godinho, H.P., 2002. Adhesiveness andsurface patterns of eggs in neotropical freshwater teleosts. J. Fish Biol.61, 615–632.

Y

ell 38 (2006) 303–310

izzo, E., Godinho, H.P., 2003. Superfıcie de ovos de peixes Characiformese Siluriformes, pp. 115–132. In: Godinho, H.P., Godinho, A.L. (Org.),Aguas, peixes e pescadores do Sao Francisco das Minas Gerais. PUCMinas, Belo Horizonte, 458 pp.

antos, J.E., Bazzoli, N., Rizzo, E., Santos, G.B., 2004. Reproduction of thecatfish Iheringichthys labrosus (Lutken) (Pisces, Siluriformes). Revtabras. Zool. 21 (2), 193–200.

elman, K., Wallace, R.A., 1989. Cellular aspects of oocyte growth inteleosts. Zool. Sci. 6, 211–231.

tehr, C.M., Hawkes, J.W., 1979. The comparative ultrastructure of theegg membrane and associated pore structure in the starry flounder,Platichthys stellatus (Pallas), and pink salmon, Oncorhynchus gorbuscha(Walbaum). Cell Tissue Res. 202 (3), 347–356.

yler, C.R., Sumpter, J.P., 1996. Oocyte growth and development in teleosts.

ork, S.W., Patino, R., Thomas, P., 1993. Ultrastructural changes in fol-licle cell-oocyte associations during development and maturation ofthe ovarian follicle in atlantic croaker. Gen. Comp. Endocrinol. 92,402–418.