Skip to main content
SpringerLink
Log in

Testosterone production and spermatogenesis in free-ranging Eurasian lynx (Lynx lynx) throughout the year

  • Original Paper
  • Published:
European Journal of Wildlife Research Aims and scope Submit manuscript

Abstract

Seasonal variation in reproduction is common in mammals as an adaptation to annual changes in the habitat. In lynx, male reproduction activity is of special interest because female lynxes are monoestric with an unusual narrow (about 1 month) breeding season. In Eurasian lynx, mating occurs between January and April depending on the latitude. To characterize the seasonal pattern of sperm and testosterone production in free-ranging Eurasian lynxes, long-term frozen-stored testis material obtained postmortem from 74 hunted or road-killed lynxes in Sweden was used to analyze annual changes in testis mass, testicular testosterone content, and spermatogenetic activity. Values of most gonadal parameters obtained in subadult lynxes were significantly different from the values observed in adult males. In adult lynxes, a moderate annual fluctuation of gonadal parameters was found which was most profound for testis weight and testicular testosterone concentration reaching highest values in March (median of 2.18 g and 2.67 μg/g tissue respectively). Grouping the data of pre-/breeding (January–April) and postbreeding season (May–September) revealed significant changes in testis weight and testosterone concentration. The relative spermatogenetic activity remained high in postbreeding testes. However, net sperm production decreased according to reduction of testis mass and a tendency to lower cauda epididymal sperm numbers in the postbreeding period was observed. Our results demonstrate that it is possible to analyze the gonadal activity of frozen testis/epididymis tissue postmortem and that male Eurasian lynxes show—opposite to the females—only moderate seasonal changes in their reproductive capacity.

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

Similar content being viewed by others

References

  • Andersen Berg K, Wiger R, Dahl E, Torp T, Farstad W, Krogenaes A, McNeilly AS, Paulenz H, Ropstad E (2001) Seasonal changes in spermatogenic activity and in plasma levels of FSH, LH and testosterone, and the effect of immunization against inhibin in the male silver fox (Vulpes vulpes). Int J Androl 24(5):284–294

    Article  CAS  PubMed  Google Scholar 

  • Axner E, Uhlhorn H, Agren E, Morner T (2009) Reproductive maturation in the male Eurasian lynx (Lynx lynx): a study on 55 reproductive organs collected from carcasses during 2002-2005. Reprod Domest Anim 44(3):467–473. doi:10.1111/j.1439-0531.2008.01130.x

    Article  CAS  PubMed  Google Scholar 

  • Berndtson WE, Jones LS (1989) Relationship of intratesticular testosterone content of stallions to age, spermatogenesis, Sertoli cell distribution and germ cell-Sertoli cell ratios. J Reprod Fertil 85(2):511–518

    Article  CAS  PubMed  Google Scholar 

  • Blottner S, Jewgenow K (2007) Moderate seasonality in testis function of domestic cat. Reprod Domest Anim 42(5):536–540. doi:10.1111/j.1439-0531.2006.00817.x

    Article  CAS  PubMed  Google Scholar 

  • Blottner S, Hingst O, Meyer HH (1996) Seasonal spermatogenesis and testosterone production in roe deer (Capreolus capreolus). J Reprod Fertil 108(2):299–305

    Article  CAS  PubMed  Google Scholar 

  • Blottner S, Schon J, Jewgenow K (2006) Seasonally activated spermatogenesis is correlated with increased testicular production of testosterone and epidermal growth factor in mink (Mustela vison). Theriogenology 66(6–7):1593–1598. doi:10.1016/j.theriogenology.2006.01.041

    Article  CAS  PubMed  Google Scholar 

  • Bronson FH, Heidemann PD (1994) Seasonal regulation of reproduction in mammals. In: Knobil E, Neill JD (eds) The Physiology of Reproduction. Raven, New York, pp 541–583

    Google Scholar 

  • Brown JL (2011) Female reproductive cycles of wild female felids. Anim Reprod Sci 124(3–4):155–162. doi:10.1016/j.anireprosci.2010.08.024

    Article  CAS  PubMed  Google Scholar 

  • Burgess EA, Lanyon JM, Keeley T (2012) Testosterone and tusks: maturation and seasonal reproductive patterns of live, free-ranging male dugongs (Dugong dugon) in a subtropical population. Reproduction 143(5):683–697. doi:10.1530/Rep-11-0434

    Article  CAS  PubMed  Google Scholar 

  • Crosier AE, Marker L, Howard J, Pukazhenthi BS, Henghali JN, Wildt DE (2007) Ejaculate traits in the Namibian cheetah (Acinonyx jubatus): influence of age, season and captivity. Reprod Fertil Dev 19(2):370–382. doi:10.1071/Rd06057

    Article  PubMed  Google Scholar 

  • Fuentes LB, Caravaca N, Pelzer LE, Scardapane LA, Piezzi RS, Guzman JA (1991) Seasonal variations in the testis and epididymis of vizcacha (Lagostomus maximus maximus). Biol Reprod 45(3):493–497

    Article  CAS  PubMed  Google Scholar 

  • Ganan N, Gonzalez R, Sestelo A, Garde JJ, Sanchez I, Aguilar JM, Gomendio M, Roldan ER (2009) Male reproductive traits, semen cryopreservation, and heterologous in vitro fertilization in the bobcat (Lynx rufus). Theriogenology 72(3):341–352. doi:10.1016/j.theriogenology.2009.03.002

    Article  CAS  PubMed  Google Scholar 

  • Ganan N, Sestelo A, Garde JJ, Martinez F, Vargas A, Sanchez I, Perez-Aspa MJ, Lopez-Bao JV, Palomares F, Gomendio M, Roldan ER (2010) Reproductive traits in captive and free-ranging males of the critically endangered Iberian lynx (Lynx pardinus). Reproduction 139(1):275–285. doi:10.1530/REP-09-0259

    Article  CAS  PubMed  Google Scholar 

  • Goeritz 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 among changes in ejaculate parameters, morphology and function of testis and accessory glands. Theriogenology 59(7):1487–1502

    Article  CAS  PubMed  Google Scholar 

  • Goritz F, Neubauer K, Naidenko SV, Fickel J, Jewgenow K (2006) Investigations on reproductive physiology in the male Eurasian lynx (Lynx lynx). Theriogenology 66(6–7):1751–1754. doi:10.1016/j.theriogenology.2006.02.036

    Article  PubMed  Google Scholar 

  • Hasler M, Hothorn LA (2008) Multiple contrast tests in the presence of heteroscedasticity. Biom J 50:793–800

    Article  PubMed  Google Scholar 

  • Hayssen V, Tienhoven AV, Tienhoven AV (1993) Asdell's pattern of mammalian reproduction. A compendium of species-specific data. Cornell University, Ithaca

    Google Scholar 

  • Henriksen HB, Andersen R, Hewison AJM, Gaillard J-M, Bronndal M, Jonsson S, Linnell JDC, Odden J (2005) Reproductive biology of captive female Eurasian lynx, Lynx lynx. Eur J Wildl Res 51(3):151–156

    Article  Google Scholar 

  • Hikim AP, Hikim IS, Amador AG, Bartke A, Woolf A, Russell LD (1991) Reinitiation of spermatogenesis by exogenous gonadotropins in a seasonal breeder, the woodchuck (Marmota monax), during gonadal inactivity. Am J Anat 192(2):194–213. doi:10.1002/aja.1001920208

    Article  CAS  PubMed  Google Scholar 

  • Jewgenow K, Songsasen N (2014) Reproduction and advances in reproductive studies in carnivores. In: Holt WV, Brown JL, Comizzoli P (eds) Reproductive sciences in animal conservation—progress and prospects. Springer

  • Jewgenow K, Goeritz F, Neubauer K, Fickel J, Naidenko SV (2006) Characterization of reproductive activity in captive male Eurasian lynx (Lynx lynx). Eur J Wildl Res 52(1):34–38. doi:10.1007/s10344-005-0002-6

    Article  Google Scholar 

  • Kaneko K, Akiya Y, Sato H, Tanaka A, Aoki H, Miyoshi M, Abukawa T, Mochizuki M, Kawakami S (2005) Seasonal influence on testicular function of male raccoons, Procyon lotor. J Reprod Dev 51(4):477–482

    Article  PubMed  Google Scholar 

  • Konietschke F, Brunner E, Hothorn LA (2012) Rank-based multiple test procedures and simultaneous confidence intervals. Electron J Stat 6:738–759

    Article  Google Scholar 

  • Kvam T (1990) Ovulation rates in European lynx, Lynx lynx (L.), from Norway. Mamm Biol 55(5):315–320

    Google Scholar 

  • Kvam T (1991) Reproduction in the European lynx, Lynx lynx. Mamm Biol 56(3):146–158

    Google Scholar 

  • Lermen D, Blomeke B, Browne R, Clarke A, Dyce PW, Fixemer T, Fuhr GR, Holt WV, Jewgenow K, Lloyd RE, Lotters S, Paulus M, Reid GM, Rapoport DH, Rawson D, Ringleb J, Ryder OA, Sporl G, Schmitt T, Veith M, Muller P (2009) Cryobanking of viable biomaterials: implementation of new strategies for conservation purposes. Mol Ecol 18(6):1030–1033. doi:10.1111/j.1365-294X.2008.04062.x

    Article  PubMed  Google Scholar 

  • Lincoln GA (1989) Seasonal aspects of testicular function. In: Burger H, de Kretser D (eds) The Testis. Raven, New York, pp 329–386

    Google Scholar 

  • Minter LJ, DeLiberto TJ (2008) Seasonal variation in serum testosterone, testicular volume, and semen characteristics in the coyote (Canis latrans). Theriogenology 69(8):946–952. doi:10.1016/j.theriogenology.2008.01.010

    Article  CAS  PubMed  Google Scholar 

  • Moss AM, Clutton-Brock TH, Monfort SL (2001) Longitudinal gonadal steroid excretion in free-living male and female meerkats (Suricata suricatta). Gen Comp Endocrinol 122(2):158–171. doi:10.1006/gcen.2001.7622

    Article  CAS  PubMed  Google Scholar 

  • Okuyama MW, Shimozuru M, Takahashi N, Fukui D, Nakamura R, Tsubota T (2012) Seasonal changes in spermatogenesis and peripheral testosterone concentration in raccoons (Procyon lotor) in Hokkaido. J Vet Med Sci 74(6):727–732

    Article  CAS  PubMed  Google Scholar 

  • Preston BT, Stevenson IR, Lincoln GA, Monfort SL, Pilkington JG, Wilson K (2012) Testes size, testosterone production and reproductive behaviour in a natural mammalian mating system. J Anim Ecol 81(1):296–305. doi:10.1111/j.1365-2656.2011.01907.x

    Article  PubMed  Google Scholar 

  • Raynaud J, Muller K, Schradin C (2012) Experimental increase of testosterone levels in free-ranging juvenile male African striped mice (Rhabdomys pumilio) induces physiological, morphological, and behavioral changes. Gen Comp Endocrinol 178(1):108–115. doi:10.1016/j.ygcen.2012.04.028

    Article  CAS  PubMed  Google Scholar 

  • Roelants H, Schneider F, Goritz 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(2):305–312

    Article  CAS  PubMed  Google Scholar 

  • Spano M, Evenson DP (1993) Flow cytometric analysis for reproductive biology. Biol Cell 78(1–2):53–62

    Article  CAS  PubMed  Google Scholar 

  • Spindler RE, Wildt DE (1999) Circannual variations in intraovarian oocyte but not epididymal sperm quality in the domestic Cat. Biol Reprod 61(1):188–194

    Article  CAS  PubMed  Google Scholar 

  • Swanson WF, Brown JL, Wildt DE (1996) Influence of seasonality on reproductive traits of the male Pallas' cat (Felis manul) and implications for captive management. J Zool Wildl Med 27(2):234–240

    Google Scholar 

  • Tsubota T, Howell-Skalla L, Nitta H, Osawa Y, Mason JI, Meiers PG, Nelson RA, Bahr JM (1997) Seasonal changes in spermatogenesis and testicular steroidogenesis in the male black bear Ursus americanus. J Reprod Fertil 109(1):21–27

    Article  CAS  PubMed  Google Scholar 

  • Welbergen JA (2011) Fit females and fat polygynous males: seasonal body mass changes in the grey-headed flying fox. Oecologia 165(3):629–637. doi:10.1007/s00442-010-1856-1

    Article  PubMed  Google Scholar 

  • Wildt DE, Brown JL, Swanson WF (1998) Cats. In: Knobil E, Neill JD (eds) Encyclopedia of Reproduction, vol 1. Academic, San Diego, pp 497–510

    Google Scholar 

Download references

Acknowledgments

We thank Christiane Franz, Katrin Paschmionka and Marlies Rohleder for their excellent technical assistance. We also thank the staff of the Necropsy Division and Jessica Åsbrink, SVA, for their help with the postmortem examinations and sample collection. This work was supported by the German Ministry of Education and Research (BMBF Number 033 L046).

Author information

Authors and Affiliations

  1. Leibniz-Institut für Zoo- und Wildtierforschung, Alfred-Kowalke-Str. 17, 10315, Berlin, Germany

    Karin Müller, Stephanie Koster, Johanna Painer, Martin Dehnhard & Katarina Jewgenow

  2. Department of Pathology and Wildlife Diseases, National Veterinary Institute (SVA), 751 89, Uppsala, Sweden

    Arne Söderberg & Dolores Gavier-Widèn

  3. Department of Biomedical Sciences and Veterinary Public Health, Swedish University of Agricultural Sciences (SLU), Uppsala, Sweden

    Dolores Gavier-Widèn

  4. Department of Medical Statistics, University Medical Center Göttingen, Humboldtallee 32, 37073, Göttingen, Germany

    Edgar Brunner

  5. Arbeitsgruppe Reproduktionsbiologie, Leibniz-Institut für Zoo- und Wildtierforschung, PF 700430, 10324, Berlin, Germany

    Karin Müller

Authors
  1. Karin Müller
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stephanie Koster
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Johanna Painer
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Arne Söderberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Dolores Gavier-Widèn
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Edgar Brunner
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Martin Dehnhard
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Katarina Jewgenow
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Karin Müller.

Additional information

Communicated by C. Gortázar

Karin Müller and Stephanie Koster contributed equally to the work.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Müller, K., Koster, S., Painer, J. et al. Testosterone production and spermatogenesis in free-ranging Eurasian lynx (Lynx lynx) throughout the year. Eur J Wildl Res 60, 569–577 (2014). https://doi.org/10.1007/s10344-014-0821-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10344-014-0821-4

Keywords

Search

Navigation