Skip to main content
Top
Published in: Brain Structure and Function 2/2004

01-05-2004 | Original Article

Histological organization of roe deer testis throughout the seasonal cycle: variable and constant components of tubular and interstitial compartment

Authors: J. Schön, F. Göritz, J. Streich, S. Blottner

Published in: Brain Structure and Function | Issue 2/2004

Login to get access

Abstract

Seasonally regulated breeding in roe deer, Capreolus capreolus, is associated with significant changes in testis mass, structure and function. This study has quantified seasonal changes of morphometric parameters and cellular composition in roe deer testis parenchyma. Tissue samples were collected bimonthly during a complete annual cycle. Morphometric parameters of seminiferous tubules were measured and the number of different cell types was counted using a computer-aided image-analyzing system. A scheme of eight tubular epithelium stages for active spermatogenesis was devised according to the spermatid development. Stage I is characterized by the occurrence of new round spermatids, stage IV by spermiation and stage VIII by the meiotic division of spermatocytes. The average diameter of seminiferous tubules varied between 88.4±3.6 µm (February) and 216.8±9.2 µm (June). Also numbers of spermatogonia, spermatocytes and spermatids per tubule cross-section showed considerable seasonal changes. In December and February the germinative epithelium mainly consists of Sertoli cells and spermatogonia. In February, the first differentiated spermatogonia enter meiosis, and in April even spermatids occasionally occur, which reach their highest numbers during the rut in August. Both the expansion and the proportion of tubular and interstitial compartment change seasonally and result in differing cell densities. Assuming numerically constant populations of Sertoli cells and interstitial cells during the entire year, the hypothetical cell numbers per mm2 of the tubular and interstitial areas were calculated for the seasonally variable total areas of tissue cross-sections. The concordance of these theoretical values with measured cell densities provided evidence that the total numbers of Sertoli cells, as well as interstitial cells, remain really constant throughout the seasonal cycle. The exact quantification of variable and constant components provides basic data for characterization of cell type and stage-specific processes of spermatogenesis.
Literature
go back to reference Amann RP (1970) Sperm production rates. In: Johnson AD, Gomes WR, Vanemark NL (eds) The Testis, vol. 1. Academic Press, New York, pp 433–482 Amann RP (1970) Sperm production rates. In: Johnson AD, Gomes WR, Vanemark NL (eds) The Testis, vol. 1. Academic Press, New York, pp 433–482
go back to reference Ariyaratne HBS, Mendis-Handagama SMLC (2000) Changes in the testis interstitium of Sprague Dawley rats from birth to sexual maturity. Biol Reprod 62:680–690 Ariyaratne HBS, Mendis-Handagama SMLC (2000) Changes in the testis interstitium of Sprague Dawley rats from birth to sexual maturity. Biol Reprod 62:680–690
go back to reference Bartke A, Sinha Hikim AP, Russell LD (1996) Leydig cell structure and function in seasonal breeders. In: Payne AH, Hardy MP, Russel LD (eds) The Leydig Cell. Cache River Press, Vienna, IL, pp 431–450 Bartke A, Sinha Hikim AP, Russell LD (1996) Leydig cell structure and function in seasonal breeders. In: Payne AH, Hardy MP, Russel LD (eds) The Leydig Cell. Cache River Press, Vienna, IL, pp 431–450
go back to reference Berg KA, Paulenz H, Ropstad E (1998) The spermatogenic cycle in the silver fox (Vulpes vulpes): frequency of the different stages prior to and during the breeding season. Int J Androl 21:377–382PubMed Berg KA, Paulenz H, Ropstad E (1998) The spermatogenic cycle in the silver fox (Vulpes vulpes): frequency of the different stages prior to and during the breeding season. Int J Androl 21:377–382PubMed
go back to reference Berndtson WE (1977) Methods for quantifying mammalian spermatogenesis: a review. J Anim Sci 44:818–833PubMed Berndtson WE (1977) Methods for quantifying mammalian spermatogenesis: a review. J Anim Sci 44:818–833PubMed
go back to reference Berndtson WE, Desjardins C (1974) The cycle of the seminiferous epithelium and spermatogenesis in the bovine testis. Am J Anat 140:167–180PubMed Berndtson WE, Desjardins C (1974) The cycle of the seminiferous epithelium and spermatogenesis in the bovine testis. Am J Anat 140:167–180PubMed
go back to reference Blanco-Rodriguez J, Martinez-Garcia C (1996) Spontaneous germ cell death in the testis of the adult rat takes the form of apoptosis: re-evaluation of cell types that exhibit the ability to die during spermatogenesis. Cell Prolif 29:13–31PubMed Blanco-Rodriguez J, Martinez-Garcia C (1996) Spontaneous germ cell death in the testis of the adult rat takes the form of apoptosis: re-evaluation of cell types that exhibit the ability to die during spermatogenesis. Cell Prolif 29:13–31PubMed
go back to reference Blottner S, Hingst O, Meyer HHD (1996) Seasonal spermatogenesis and testosterone production in roe deer (Capreolus capreolus). J Reprod Fertil 108:299–305CrossRefPubMed Blottner S, Hingst O, Meyer HHD (1996) Seasonal spermatogenesis and testosterone production in roe deer (Capreolus capreolus). J Reprod Fertil 108:299–305CrossRefPubMed
go back to reference Böhme G, Pier C (1986) Ordnungskriterien für den Zyklus des Epithels der Tubuli seminiferi, nach Untersuchungen beim Kater (Felis catus). Berl Münch Tierärztl Wschr 99:232–236 Böhme G, Pier C (1986) Ordnungskriterien für den Zyklus des Epithels der Tubuli seminiferi, nach Untersuchungen beim Kater (Felis catus). Berl Münch Tierärztl Wschr 99:232–236
go back to reference Bronson FH, Heidemann PD (1994) Seasonal regulation of reproduction in mammals. In: Knobil E, Neill JD (eds) The physiology of reproduction. Raven Press, New York, pp 541–583 Bronson FH, Heidemann PD (1994) Seasonal regulation of reproduction in mammals. In: Knobil E, Neill JD (eds) The physiology of reproduction. Raven Press, New York, pp 541–583
go back to reference Foreman D (1997) Seminiferous tubule stages in the prairie dog (Cynomys ludovicianus) during annual breeding cycle. Anat Rec 247:355–367CrossRefPubMed Foreman D (1997) Seminiferous tubule stages in the prairie dog (Cynomys ludovicianus) during annual breeding cycle. Anat Rec 247:355–367CrossRefPubMed
go back to reference Franca LR, Russell LD (1998) The testis of domestic animals. In: Martinez F, Regadera J (eds) Male Reproduction. A Multidisciplinary Overview. Churchill, Madrid, pp 197–219 Franca LR, Russell LD (1998) The testis of domestic animals. In: Martinez F, Regadera J (eds) Male Reproduction. A Multidisciplinary Overview. Churchill, Madrid, pp 197–219
go back to reference Gentile R, Scisciola V, Lenti M, Passantino G (1989) Ulteriori osservazioni e considerazioni sul ciclo biologico e riproduttivo del capriolo (capreolus capreolus). Boll Soct Biol Sper 65:631–638 Gentile R, Scisciola V, Lenti M, Passantino G (1989) Ulteriori osservazioni e considerazioni sul ciclo biologico e riproduttivo del capriolo (capreolus capreolus). Boll Soct Biol Sper 65:631–638
go back to reference Göritz F, Quest M, Wagener A, Faßbender M, Broich A, Hildebrandt TB, Hofmann RR, Blottner S (2003) Seasonal timing of sperm production in roe deer: interrelationship between changes in ejaculate parameters, morphology and function of testis and accessory glands. Theriogenology 59:1487–1502CrossRefPubMed Göritz F, Quest M, Wagener A, Faßbender M, Broich A, Hildebrandt TB, Hofmann RR, Blottner S (2003) Seasonal timing of sperm production in roe deer: interrelationship between changes in ejaculate parameters, morphology and function of testis and accessory glands. Theriogenology 59:1487–1502CrossRefPubMed
go back to reference Griswold MD (1995) Interactions between germ cells and Sertoli cells in the testis. Biol Reprod 52:211–216PubMed Griswold MD (1995) Interactions between germ cells and Sertoli cells in the testis. Biol Reprod 52:211–216PubMed
go back to reference Griswold MD (1998) The central role of Sertoli cells in spermatogenesis. Sem Cell Develop Biol 9:411–416CrossRef Griswold MD (1998) The central role of Sertoli cells in spermatogenesis. Sem Cell Develop Biol 9:411–416CrossRef
go back to reference Hardy MP, Mendis-Handagama SMLC, Zirkin BR, Ewing LL (1987) Photoperiodic variation of Leydig cell numbers in the testis of the golden hamster: a possible mechanism for their renewal during recrudescence. J Exp Zool 244:269–276PubMed Hardy MP, Mendis-Handagama SMLC, Zirkin BR, Ewing LL (1987) Photoperiodic variation of Leydig cell numbers in the testis of the golden hamster: a possible mechanism for their renewal during recrudescence. J Exp Zool 244:269–276PubMed
go back to reference Hochereau-de Reviers MT, Lincoln GA (1978) Seasonal variation in the histology of the testis of the red deer, Cervus elaphus. J Reprod Fert 54:209–213 Hochereau-de Reviers MT, Lincoln GA (1978) Seasonal variation in the histology of the testis of the red deer, Cervus elaphus. J Reprod Fert 54:209–213
go back to reference Johnson L, Matt KS, Bartke A, Nguyen HB, Le HT (1987) Effect of photoperiod on the size of the Leydig cell population and the rate of recruitment of Leydig cells in adult Syrian hamsters. Biol Reprod 37:727–738PubMed Johnson L, Matt KS, Bartke A, Nguyen HB, Le HT (1987) Effect of photoperiod on the size of the Leydig cell population and the rate of recruitment of Leydig cells in adult Syrian hamsters. Biol Reprod 37:727–738PubMed
go back to reference Johnson L, Varner DD, Roberts ME, Smith TL, Keillor GE, Scrutchfield WL (2000) Efficiency of spermatogenesis: a comparative approach. Anim Reprod Sci 60–61:471–480 Johnson L, Varner DD, Roberts ME, Smith TL, Keillor GE, Scrutchfield WL (2000) Efficiency of spermatogenesis: a comparative approach. Anim Reprod Sci 60–61:471–480
go back to reference Kerr JB (1992) Spontaneous degeneration of germ cells in normal rat testis: assessment of cell types and frequency during the spermatogenic cycle. J Reprod Fert 95:825–830CrossRef Kerr JB (1992) Spontaneous degeneration of germ cells in normal rat testis: assessment of cell types and frequency during the spermatogenic cycle. J Reprod Fert 95:825–830CrossRef
go back to reference Kierszenbaum AL (1994) Mammalian spermatogenesis in vivo and in vitro: a partnership of spermatogenic and somatic cell lineages. Endocrine Rev 15:116–134CrossRef Kierszenbaum AL (1994) Mammalian spermatogenesis in vivo and in vitro: a partnership of spermatogenic and somatic cell lineages. Endocrine Rev 15:116–134CrossRef
go back to reference Marchlewsaka-Koij A, Kruczek M (1988) Seasonal variation in testicular activity of roe deer (Capreolus capreolus). Folia Biol (Warszawa) 36:119–126 Marchlewsaka-Koij A, Kruczek M (1988) Seasonal variation in testicular activity of roe deer (Capreolus capreolus). Folia Biol (Warszawa) 36:119–126
go back to reference Mendis-Handagama SMLC, Ewing LL (1990) Sources of error in the estimation of Leydig cell numbers in control and atrophied mammalian testes. J Microsc 159:73–82PubMed Mendis-Handagama SMLC, Ewing LL (1990) Sources of error in the estimation of Leydig cell numbers in control and atrophied mammalian testes. J Microsc 159:73–82PubMed
go back to reference Munoz EM, Fogal T, Dominguez S, Scardapane L, Guzman J, Cavicchia JC, Piezzi RS (1998) Stages of the cycle of the seminiferous epithelium of the viscacha (Lagostomus maximus maximus). Anat Rec 252:8–16CrossRefPubMed Munoz EM, Fogal T, Dominguez S, Scardapane L, Guzman J, Cavicchia JC, Piezzi RS (1998) Stages of the cycle of the seminiferous epithelium of the viscacha (Lagostomus maximus maximus). Anat Rec 252:8–16CrossRefPubMed
go back to reference Munoz EM, Fogal T, Dominguez S, Scardapane L, Piezzi RS (2001) Ultrastructural and morphometric study of the Sertoli cell of the viscacha (Lagostomus maximus maximus) during the annual reproductive cycle. Anat Rec 262:176–185CrossRefPubMed Munoz EM, Fogal T, Dominguez S, Scardapane L, Piezzi RS (2001) Ultrastructural and morphometric study of the Sertoli cell of the viscacha (Lagostomus maximus maximus) during the annual reproductive cycle. Anat Rec 262:176–185CrossRefPubMed
go back to reference Ortavant R, Courot M, Hochereau-de Reviers MT (1977) Spermatogenesis in domestic mammals. In: Cole HH, Cupps PT (eds) Reproduction in domestic animals, 3rd edn. Academic Press, New York, pp 203–227 Ortavant R, Courot M, Hochereau-de Reviers MT (1977) Spermatogenesis in domestic mammals. In: Cole HH, Cupps PT (eds) Reproduction in domestic animals, 3rd edn. Academic Press, New York, pp 203–227
go back to reference Pawar HS, Wrobel KH (1991) The Sertoli cell of the water buffalo (Bubalis bubalis) during the spermatogenic cycle. Cell Tissue Res 265:43–50 Pawar HS, Wrobel KH (1991) The Sertoli cell of the water buffalo (Bubalis bubalis) during the spermatogenic cycle. Cell Tissue Res 265:43–50
go back to reference Pelletier R-M (1986) Cyclic formation and decay of the blood-testis barrier in the mink (Mustela vison): a seasonal breeder. Am J Anat 175:91–117PubMed Pelletier R-M (1986) Cyclic formation and decay of the blood-testis barrier in the mink (Mustela vison): a seasonal breeder. Am J Anat 175:91–117PubMed
go back to reference Pier C (1985) Der Samenepitehlzyklus des Katers (Felis catus). Thesis, Free University of Berlin Pier C (1985) Der Samenepitehlzyklus des Katers (Felis catus). Thesis, Free University of Berlin
go back to reference Robaire B (1999) Fifty years of insight into the seminiferous epithelium: A tribute to Yves W. Clermont. In: Gagnon C (ed) The male gamete. From Basic Science to Clinical Applications. Cache River Press, Vienna, IL, pp 1–4 Robaire B (1999) Fifty years of insight into the seminiferous epithelium: A tribute to Yves W. Clermont. In: Gagnon C (ed) The male gamete. From Basic Science to Clinical Applications. Cache River Press, Vienna, IL, pp 1–4
go back to reference Roelants H, Schneider F, Göritz F, Streich J, Blottner S (2002) Seasonal changes of spermatogonial proliferation in roe deer, demonstrated by flow cytometric analysis of c-kit receptor, in relation to follicle-stimulating hormone, luteinizing hormone and testosterone. Biol Reprod 66:305–312PubMed Roelants H, Schneider F, Göritz F, Streich J, Blottner S (2002) Seasonal changes of spermatogonial proliferation in roe deer, demonstrated by flow cytometric analysis of c-kit receptor, in relation to follicle-stimulating hormone, luteinizing hormone and testosterone. Biol Reprod 66:305–312PubMed
go back to reference Russell LD, Ettlin RA, Sinha Hikim AP, Clegg ED (eds) (1990) Histological and Histopathological Evaluation of the Testis. Cache River Press, Clearwater Russell LD, Ettlin RA, Sinha Hikim AP, Clegg ED (eds) (1990) Histological and Histopathological Evaluation of the Testis. Cache River Press, Clearwater
go back to reference Schlatt S, Meinhardt A, Nieschlag E (1997) Paracrine regulation of cellular interactions in the testis: factors in search of function. Eur J Endocrinol 137:107–117PubMed Schlatt S, Meinhardt A, Nieschlag E (1997) Paracrine regulation of cellular interactions in the testis: factors in search of function. Eur J Endocrinol 137:107–117PubMed
go back to reference Semperé AJ, Mauget R, Mauget C (1998) Reproductive physiology of roe deer. In: Andersen R, Duncan P, Linnel JDC (eds) The European roe deer: the biology of success. Scand Uni Press, Oslo, pp 161–188 Semperé AJ, Mauget R, Mauget C (1998) Reproductive physiology of roe deer. In: Andersen R, Duncan P, Linnel JDC (eds) The European roe deer: the biology of success. Scand Uni Press, Oslo, pp 161–188
go back to reference Sharpe M (1994). Regulation of spermatogenesis. In: Knobil E, Neill JD (eds) The physiology of reproduction, 2nd edn. Raven Press, New York, pp 1363–1434 Sharpe M (1994). Regulation of spermatogenesis. In: Knobil E, Neill JD (eds) The physiology of reproduction, 2nd edn. Raven Press, New York, pp 1363–1434
go back to reference Sharpe RM, McKinnell C, Kivlin C, Fisher JS (2003) Proliferation and functional maturation of Sertoli cells, and their relevance to disorders of testis function in adulthood. Reproduction 125:769–784CrossRefPubMed Sharpe RM, McKinnell C, Kivlin C, Fisher JS (2003) Proliferation and functional maturation of Sertoli cells, and their relevance to disorders of testis function in adulthood. Reproduction 125:769–784CrossRefPubMed
go back to reference Short RV, Mann T (1966) The sexual cycle of a seasonally breeding mammal, the roebuck (Capreolus capreolus). J Reprod Fert 12:337–351 Short RV, Mann T (1966) The sexual cycle of a seasonally breeding mammal, the roebuck (Capreolus capreolus). J Reprod Fert 12:337–351
go back to reference Sinha Hikim AP, Bartke A, Russell LD (1988A) The seasonal breeding hamster as a model to structure-function relationships in the testis. Tissue Cell 20:63–78CrossRefPubMed Sinha Hikim AP, Bartke A, Russell LD (1988A) The seasonal breeding hamster as a model to structure-function relationships in the testis. Tissue Cell 20:63–78CrossRefPubMed
go back to reference Sinha Hikim AP, Bartke A, Russell LD (1988B) Morphometric studies on hamster testes in gonadally active and inactive states. Light microscope findings. Biol Reprod 39:1225–1237PubMed Sinha Hikim AP, Bartke A, Russell LD (1988B) Morphometric studies on hamster testes in gonadally active and inactive states. Light microscope findings. Biol Reprod 39:1225–1237PubMed
go back to reference Sinha Hikim APS, Hikim IS, Amador AG, Bartke A, Woolf A, Russell LD (1991) Reinitiation of spermatogenesis by exogenous gonadotropin in a seasonal breeding mammal, the woodchuck (Marmota monax). Am J Anat 192:194–213PubMed Sinha Hikim APS, Hikim IS, Amador AG, Bartke A, Woolf A, Russell LD (1991) Reinitiation of spermatogenesis by exogenous gonadotropin in a seasonal breeding mammal, the woodchuck (Marmota monax). Am J Anat 192:194–213PubMed
go back to reference Skinner MK (1991) Cell-cell interactions in the testis. Endocrine Reviews 12:45–77PubMed Skinner MK (1991) Cell-cell interactions in the testis. Endocrine Reviews 12:45–77PubMed
go back to reference Stieve H (1950) Anatomisch-biologische Untersuchungen über die Fortpflanzungstätigkeit des europäischen Rehes (Capreolus capreolus). Z Mikr anat Forschg 55: 427–528 Stieve H (1950) Anatomisch-biologische Untersuchungen über die Fortpflanzungstätigkeit des europäischen Rehes (Capreolus capreolus). Z Mikr anat Forschg 55: 427–528
go back to reference Suswillo RFL, Watson PF (1990) A new light microscopy classification of spermatogenesis in the bull and the boar applicable to tissues processed for electron microscopy. Anat Histol Embryol 19:326–339PubMed Suswillo RFL, Watson PF (1990) A new light microscopy classification of spermatogenesis in the bull and the boar applicable to tissues processed for electron microscopy. Anat Histol Embryol 19:326–339PubMed
go back to reference Swierstra EE (1966) Structural composition of Shorthorn bull testes and daily spermatozoa production as determined by quantitative testicular histology. J Anim Sci 46:107–119 Swierstra EE (1966) Structural composition of Shorthorn bull testes and daily spermatozoa production as determined by quantitative testicular histology. J Anim Sci 46:107–119
go back to reference Ueno H, Mori H (1990) Morphometrical analysis of Sertoli cell ultrastructure during the seminiferous epithelial cycle in rats. Biol Reprod 43:769–776PubMed Ueno H, Mori H (1990) Morphometrical analysis of Sertoli cell ultrastructure during the seminiferous epithelial cycle in rats. Biol Reprod 43:769–776PubMed
go back to reference Wagener A, Blottner S, Göritz F, Streich WJ, Fickel J (2003) Differential changes in expression of a and b FGF, IGF-1 and -2, and TGF-α during seasonal growth and involution of roe deer testis. Growth Factors 21:95–102PubMed Wagener A, Blottner S, Göritz F, Streich WJ, Fickel J (2003) Differential changes in expression of a and b FGF, IGF-1 and -2, and TGF-α during seasonal growth and involution of roe deer testis. Growth Factors 21:95–102PubMed
go back to reference Wrobel K-H, Keßler M, Schimmel M (1993) Quantitative evaluations of the tubular epithelium in the testis of the Fallow deer (Dama dama). Reprod Dom Anim 28:1–13 Wrobel K-H, Keßler M, Schimmel M (1993) Quantitative evaluations of the tubular epithelium in the testis of the Fallow deer (Dama dama). Reprod Dom Anim 28:1–13
go back to reference Wrobel K-H, Reichold J, Schimmel M (1995) Quantitative morphology of the ovine seminiferous epithelium. Ann Anat 177:19–32 Wrobel K-H, Reichold J, Schimmel M (1995) Quantitative morphology of the ovine seminiferous epithelium. Ann Anat 177:19–32
go back to reference Yu Z, Guo R, Ge Y, Ma J, Guan J, Li S, Sun X, Xue S, Han D (2003) Gene expression profiles in different stages of mouse spermatogenic cells during spermatogenesis. Biol Reprod 69:37–47PubMed Yu Z, Guo R, Ge Y, Ma J, Guan J, Li S, Sun X, Xue S, Han D (2003) Gene expression profiles in different stages of mouse spermatogenic cells during spermatogenesis. Biol Reprod 69:37–47PubMed
go back to reference Zayed AE, Hifny A, Abou-Elmagd A, Wrobel KH (1995) Seasonal changes in the intertubular tissue of the camel testis (Camelus dromedarius). Ann Anat 177:199–212 Zayed AE, Hifny A, Abou-Elmagd A, Wrobel KH (1995) Seasonal changes in the intertubular tissue of the camel testis (Camelus dromedarius). Ann Anat 177:199–212
go back to reference Zirkin BR (1993) Regulation of spermatogenesis in the adult mammal: gonadotropins and androgens. In: Desjardins C, Ewing LL (eds) Cell and molecular biology of the testis. Oxford Uni Press, pp 166–188 Zirkin BR (1993) Regulation of spermatogenesis in the adult mammal: gonadotropins and androgens. In: Desjardins C, Ewing LL (eds) Cell and molecular biology of the testis. Oxford Uni Press, pp 166–188
Metadata
Title
Histological organization of roe deer testis throughout the seasonal cycle: variable and constant components of tubular and interstitial compartment
Authors
J. Schön
F. Göritz
J. Streich
S. Blottner
Publication date
01-05-2004
Publisher
Springer-Verlag
Published in
Brain Structure and Function / Issue 2/2004
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-004-0385-2

Other articles of this Issue 2/2004

Brain Structure and Function 2/2004 Go to the issue