Skip to main content
SpringerLink
Log in

The structure of spermatogenic cysts and number of Sertoli cells in the testes of Bombina bombina and Bombina variegata (Bombinatoridae, Anura, Amphibia)

  • Original Paper
  • Published:
Zoomorphology Aims and scope Submit manuscript

Abstract

Spermatogenesis in amphibians occurs inside spermatogenic cysts formed by Sertoli cells (SCs). SCs do not constitute a permanent population and their number increases during spermatogenic cycle and ontogeny. The number of SCs per cyst is strongly correlated with the number of germ cells in the same cyst and with the cyst volume. The number of germ and Sertoli cells and cyst volumes are species-specific and increase along with age. The mean number of primary spermatocytes per one Sertoli cell (efficiency) was the same, irrespective of age and species. Late spermatids are not attached to the Sertoli cells and do not form bundles as in other amphibians. The number of primary spermatocytes inside a cyst was the yield of several mitotic cycles of a single primary spermatogonium (stem cell) and its descendants, i.e., secondary spermatogonia. In adult Bombina bombina, the majority of cysts contained germ cells after 6–8 cycles, in juveniles after 4–6 cycles, and in adult Bombina variegata after 5–7 cycles. The mean numbers of SCs per cyst were 27.4 ± 9.9 in adult B. bombina, 6.42 ± 2.32 in adult B. variegata, and 7.1 ± 2.33 in juvenile B. bombina. The number of primary spermatocytes per one SC (SC efficiency) in B. bombina in adults was 6.5 ± 2.2, in juveniles 9.0 ± 4.2, and in adult B. variegata 7.40 ± 2.96. Spermatogenesis in Bombinatoridae is exceptional owing to the lack of intimate contact between SCs and germ cells.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Abercrombie M (1946) Estimation of nuclear population from microtome sections. Anat Rec 94:239–247

    Article  CAS  PubMed  Google Scholar 

  • Atherton RW (1974) A gradient analysis of spermatogenesis in the toad Bufo woodhousei Girard (1854). Herpetologica 30:240–244

    Google Scholar 

  • Báo SN, Dalton GC, de Oliveira SF (1991) Spermiogenesis in Odontophrynus cultripes (Amphibia, Anura, Leptodactylidae): ultrastructural and cytochemical studies of proteins using E-PTA. J Morphol 207:303–314

    Article  Google Scholar 

  • Bergman M, Greven H, Schindelmeiser J (1983) Observations on the blood-testis barrier in a frog and salamander. Cell Tissue Res 232:189–200

    Article  Google Scholar 

  • Burgos MH, Vitale-Calpe R (1967a) The fine structure of the Sertoli cell-spermatozoan relationship in the toad. J Ultrastruct Res 19:221–237

    Article  CAS  PubMed  Google Scholar 

  • Burgos MH, Vitale-Calpe R (1967b) The mechanism of the spermiation in the toad. Am J Anat 120:227–252

    Article  Google Scholar 

  • Cavicchia JC, Moviglia GA (1983) The blood–testis barrier in the toad (Bufo arenarum Hensel): a freeze-fracture and lanthanum tracer study. Anat Rec 205:387–396

    Article  CAS  PubMed  Google Scholar 

  • Clermont Y, Perey B (1957) Quantitative study of the cell population of the seminiferous tubules in mature rat. Am J Anat 100:241–267

    Article  CAS  PubMed  Google Scholar 

  • De Rooij DG (2001) Proliferation and differentiation of spermatogonial stem cells. Reproduction 121:347–354

    Article  PubMed  Google Scholar 

  • Exbrayat JM (2009) Spermatogenesis and male reproduction system in Gymnophiona. In: Ogielska M (ed) Reproduction of amphibians. Science Publishers, Enfield, pp 125–152

    Google Scholar 

  • Falconi R, Dalpiaz D, Zaccanti F (2004) Ultrastructural aspects of gonadal morphogenesis in Bufo bufo (Amphibia, Anura). 1. Sex differentiation. J Exp Zool A Comp Exp Biol 301A:378–388

    Article  Google Scholar 

  • Ferreira A, Mehanna M, Prado CP (2008) Morphologic and morphometric analysis of testis of Pseudis limellum (Cope, 1862) (Anura, Hylidae) during the reproductive cycle in the Pantanal, Brazil. Biocell 32:185–194

    PubMed  Google Scholar 

  • Folliot R (1979) Ultrastructural study of spermiogenesis of the anuran amphibian Bombina variegata. In: Fawcett DW, Bedford JM (eds) The Spermatozoon. Urban and Schwarzenberg, Baltimore-Munich, pp 333–339

    Google Scholar 

  • Furieri P (1975) The peculiar morphology of the spermatozoon of Bombina variegata (L.). Monit Zool Ital 9:185–201

    Google Scholar 

  • Gramapurohit NP, Shanbhag BA, Saidapur SK (2000) Pattern of gonadal sex differentiation, development, and onset of steroidogenesis in the frog, Rana curtipes. Gen Comp Endocrinol 119:256–264

    Article  CAS  PubMed  Google Scholar 

  • Grier HJ (1993) Comparative organization of the Sertoli cells including the Sertoli cell barrier. In: Russell LD, Griswold MD (eds) The Sertoli Cell. Cache River Press, Clearwater, pp 703–739

    Google Scholar 

  • Haczkiewicz K, Rozenblut-Kościsty B, Ogielska M (2017) Prespermatogenesis and early spermatogenesis in frogs. Zoology. pii: S0944-2006(16)30125–8. doi:10.1016/j.zool.2017.01.003

  • Kalt MR (1976) Morphology and kinetics of spermatogenesis in Xenopus laevis. J Exp Zool 195:393–407

    Article  CAS  PubMed  Google Scholar 

  • Karnovsky MJ (1965) A formaldehyde–glutaraldehyde fixative of high osmolarity for use in electron microscopy. J Cell Biol 27:137A

    Google Scholar 

  • Leal MC, Cardoso ER, Nóbrega RH, Batlouni SR, Bogerd J, França LR, Schulz RW (2009) Histological and stereological evaluation of zebrafish (Danio rerio) spermatogenesis with an emphasis on spermatogonial generations. Biol Reprod 81:177–187

    Article  CAS  PubMed  Google Scholar 

  • Lee J-H, Kwon J-K (2005) Sperm ultrastructure of Bombina orientalis. Korean J Electron Microsc 35:1–11

    Google Scholar 

  • Lofts B (1964) Seasonal changes in the functional activity of the interstitial and spermatogenetic tissues of the green frog, Rana esculenta. Gen Comp Endocrinol 4:550–562

    Article  CAS  PubMed  Google Scholar 

  • Lofts B (1974) Reproduction. In: Lofts B (ed) Physiology of the amphibia. Academic Press, New York, pp 107–218

    Chapter  Google Scholar 

  • Lopez K (1989) Sex differentiation and early gonadal development in Bombina orientalis (Anura: Discoglossidae). J Morphol 199:299–311

    Article  Google Scholar 

  • Manochantr S, Sretarugsa P, Wanichanon C, Chavadej J, Sobhon P (2003) Classification of spermatogenic cells in Rana tigerina based on ultrastructure. Sci Asia 29:241–254

    Article  Google Scholar 

  • Matta SLP, Vilela DAR, Godinho HP, França LR (2002) The goitrogen 6-n-propyl-2-thiouracil (ptu) given during testis development increases Sertoli and germ cell numbers per cyst in fish: the tilapia (Oreochromis niloticus) model. Endocrinology 143:970–978

    Article  CAS  PubMed  Google Scholar 

  • McClusky LM (2012) Coordination of spermatogenic processes in the testis: lessons from cystic spermatogenesis. Cell Tissue Res 349:703–715

    Article  CAS  PubMed  Google Scholar 

  • Miething A (1990) Intercellular bridges between germ cells in the immature golden hamster testis: evidence for clonal and non-clonal mode of proliferation. Cell Tissue Res 262:559–567

    Article  CAS  PubMed  Google Scholar 

  • Obert HJ (1976) Die Spermatogenese bei der Gelbbauchunke (Bombina variegata variegata L.) im Verlauf der järlichen Aktivitatatsperiode und die Korrelation zur Paarungsrufaktivität (Discoglossidae, Anura). Z Mikrosk Anat Forsch 90:908–924

    CAS  PubMed  Google Scholar 

  • Ogielska M, Bartmańska J (2009) Spermatogenesis and male reproductive system in Anura. In: Ogielska M (ed) Reproduction of amphibians. Science Publishers, Enfield, pp 34–99

    Google Scholar 

  • Oliveira C, Vicentini CA (1998) Anatomical description of the Scinax fuscovarius fat bodies and testes (Anura, Hylidae). Biociências 6:79–88

    Google Scholar 

  • Oliveira C, Zanetoni C, Zieri R (2002) Morphological observations on the testes of Physalaemus cuvieri (Amphibia, Anura). Rev Chil Anat 20:263–268

    Article  Google Scholar 

  • Pabijan M, Wandycz A, Hofman S, Węcek K, Piwczyński M, Szymura JM (2013) Complete mitochondrial genomes resolve phylogenetic relationships within Bombina (Anura: Bombinatoridae). Molec Phylog Evol 69:63–74

    Article  CAS  Google Scholar 

  • Parsons GR, Grier HJ (1992) Seasonal changes in the shark testicular structure and spermiogenesis. J Exp Zool 261:173–184

    Article  Google Scholar 

  • Pierantoni R, Cobellis G, Meccariello R, Palmiero C, Fienga G, Minucci S, Fasano S (2002) The amphibian testis as model to study germ cell progression during spermatogenesis. Com Biochem Physiol B, Biochem Mol Biol 132:131–139

    Article  CAS  Google Scholar 

  • Piprek RP, Pecio A, Szymura JM (2010) Differentiation and development of gonads in the yellow-bellied toad, Bombina variegata L. 1758 (Amphibia: Anura: Bombinatoridae). Zool Sci 27:47–55

    Article  PubMed  Google Scholar 

  • Pudney J (1993) Comparative cytology of the non-mammalian vertebrate Sertoli cell. In: Russell LD, Griswold MD (eds) The Sertoli Cell. Cache River Press, Clearwater, pp 611–657

    Google Scholar 

  • Pudney J (1995) Spermatogenesis in nonmammalian vertebrates. Microsc Res Tech 32:459–497

    Article  CAS  PubMed  Google Scholar 

  • Rastogi RK, Iela L (1980) Steroidogenesis and spermatogenesis in anuran Amphibia: a brief survey. In: Delrio G, Brachet J (eds) Steroids and their mechanism of action in non-mammalian vertebrates. Raven Press, New York, pp 131–146

    Google Scholar 

  • Rastogi RK, Iela L, Di Meglio M, Di Matteo L, Minucci S, Izzo-Vitiello I (1983) Initiation and kinetic profiles of spermatogenesis in the frog, Rana esculenta (Amphibia). J Zool 201:515–525

    Article  Google Scholar 

  • Rastogi RK, Bagnara JT, Iela L, Krasovich MA (1988) Reproduction in the Mexican leaf frog, Pachymedusa dacnicolor. IV. Spermatogenesis: a light and ultrasonic study. J Morphol 197:277–302

    Article  Google Scholar 

  • Reed SC, Stanley HP (1972) Fine structure of spermatogenesis in the South African clawed toad Xenopus laevis Daudin. J Ultrastruct Res 41:277–295

    Article  CAS  PubMed  Google Scholar 

  • Rodríguez Y, Segura ML, Jiménez LF, Sanz A, Lara R (2007) Ultrastructure of sexual cells of Eleutherodactylus riparius (Anura: Leptodactylidae). Microsc Acta 16:187–188

    Google Scholar 

  • Rough R (1939) The reproductive processes in the male frog Rana pipiens. J Exptl Zool 80:81–105

    Article  Google Scholar 

  • Rupik W, Huszno J, Klag J (2011) Cellular organisation of the mature testes and stages of spermiogenesis in Danio rerio (Cyprinidae; Teleostei)—structural and ultrastructural studies. Micron 42:833–839

    Article  CAS  PubMed  Google Scholar 

  • Sanz A, Rodríguez Y, Segura ML, Jiménez LF (2007) TEM of Bufo longinasus (Anura: Bufonidae) gonad. Microsc Acta 16:185–186

    Google Scholar 

  • Scheltinga DM, Jamieson BGM (2003) Spermatogenesis and the mature spermatozoa: Form, function and phylogenetic implications. In: Jamieson BGM (ed) Reproductive biology and phylogeny of anura. Science Publisher Inc, Enfield, Plymouth, pp 119–251

    Google Scholar 

  • Schultz RW, Menting S, Bogerd J, França LR, Vilela DAR, Godinho HP (2005) Sertoli cell proliferation in the adult testis—evidence from two fish species belonging to different orders. Biol Reprod 73:891–898

    Article  Google Scholar 

  • Schulz RW, De França LR, Lareyre JJ, Le Gac F, Chiarini-Garcia H, Nobrega RH, Miura T (2010) Spermatogenesis in fish. Gen Comp Endocrinol 165:390–411

    Article  CAS  PubMed  Google Scholar 

  • Sprando RL, Russell LD (1988) Spermiogenesis in the bullfrog (Rana catesbeiana): a study of cytoplasmic events including cell volume changes and cytoplasmic elimination. J Morphol 198:303–319

    Article  CAS  PubMed  Google Scholar 

  • Stanley HP (1966) The structure and development of the seminiferous follicle in Scyliorhinus caniculus and Torpedo marmorata (Elasmobranchii). Z Zellforsch Mikrosk Anat 75:453–468

    Article  CAS  PubMed  Google Scholar 

  • Steinberger A, Steinberger E (1971) Replication patterns of Sertoli cells in maturing rate testis in vivo and organ culture. Biol Reprod 4:84–87

    Article  CAS  PubMed  Google Scholar 

  • Takamune K, Kawasaki T, Ukon S (2001) The first and the second mitotic phases of spermatogonial stage in Xenopus laevis: secondary spermatogonia which have differentiated after completion of the first mitotic phase acquire an ability of mitosis to meiosis conversion. Zoolog Sci 18(4):577–583. doi:10.2108/zsj.18.577

    Article  Google Scholar 

  • Tanimura A, Iwasawa H (1988) Ultrastructural observations on the origin and differentiation of somatic cells during gonadal development in the frog Rana nigromaculata. Dev Growth Differ 30:681–691

    Article  Google Scholar 

  • Tso E (1974) An ultrastructural study on the Sertoli cells in the newt (Trituroides hongkongensis). Acta Zool 55:217–223

    Article  Google Scholar 

  • Uribe MCA (2009) Spermatogenesis and male reproductive system in Urodela. In: Ogielska M (ed) Reproduction of amphibians. Science Publishers, Enfield, pp 100–124

    Google Scholar 

  • Van Oordt PGWJ, Brands F (1970) The Sertoli cells in the testis of the common frog, Rana temporaria. Proc Soc Endocrinol 119 M Meet J Endocrinol 48:100

    Google Scholar 

  • Yazawa T, Yamamoto T, Nakayama Y, Hamada S, Abé S (2000) Conversion from mitosis to meiosis: morphology and expression of proliferating cell nuclear antigen (PCNA) and dmc 1 during newt spermatogenesis. Dev Growth Differ 42:603–611

    Article  CAS  PubMed  Google Scholar 

  • Yi M-J, Lee J-H (2015) Seminiferous epithelium cycle in Bombina orientalis. Dev Reprod 19:1–10

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We would like to thank the staff of the Laboratory of Scanning Electron Microscopy Institute of Zoology, Jagiellonian University for technical assistance with (JEOL JSM 5410 (JEOL, Tokyo, Japan) and Beata Lorenc for valuable help with cell counting. This work was supported by the Polish Ministry of Sciences and Higher Education (Grant Numbers 2020/BW/IZ, 1018/DS/IZ, and 5429/B/P01/2010/38).

Author information

Authors and Affiliations

  1. Department of Evolutionary Biology and Conservation of Vertebrates, University of Wrocław, ul. Sienkiewicza 21, 50-335, Wrocław, Poland

    Beata Rozenblut-Kościsty, Jolanta Bartmańska & Maria Ogielska

  2. Department of Comparative Anatomy, Jagiellonian University, ul. Gronostajowa 9, 30-387, Kraków, Poland

    Rafał Piprek, Anna Pecio & Jacek M. Szymura

Authors
  1. Beata Rozenblut-Kościsty
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rafał Piprek
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Anna Pecio
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jolanta Bartmańska
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jacek M. Szymura
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Maria Ogielska
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Maria Ogielska.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rozenblut-Kościsty, B., Piprek, R., Pecio, A. et al. The structure of spermatogenic cysts and number of Sertoli cells in the testes of Bombina bombina and Bombina variegata (Bombinatoridae, Anura, Amphibia). Zoomorphology 136, 483–495 (2017). https://doi.org/10.1007/s00435-017-0362-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00435-017-0362-y

Keywords

Search

Navigation