Theriogenology
Volume 73, Issue 8 , Pages 1104-1115 , May 2010

Semen cryopreservation in the Indian rhinoceros (Rhinoceros unicornis)

  • M.A. Stoops

      Affiliations

    • Center for Conservation and Research of Endangered Wildlife, Cincinnati Zoo and Botanical Garden, Cincinnati, OH 45220, USA
    • Corresponding Author InformationCorresponding author. Tel.: +1 513 569 8224; fax: +1 513 569 8213.
  • ,
  • M.W. Atkinson

      Affiliations

    • The Wilds, Cumberland, OH 43732, USA
  • ,
  • E.S. Blumer

      Affiliations

    • The Wilds, Cumberland, OH 43732, USA
  • ,
  • M.K. Campbell

      Affiliations

    • Center for Conservation and Research of Endangered Wildlife, Cincinnati Zoo and Botanical Garden, Cincinnati, OH 45220, USA
  • ,
  • T.L. Roth

      Affiliations

    • Center for Conservation and Research of Endangered Wildlife, Cincinnati Zoo and Botanical Garden, Cincinnati, OH 45220, USA

Received 3 September 2009 ,Revised 5 January 2010 ,Accepted 5 January 2010.

References 

  1. Stoops MA, DeChant CJ, Pairan RD, Campbell MK, Blumer ES, Bateman HL, et al. Development of techniques for successful artificial insemination in the Indian rhinoceros (Rhinoceros unicornis). In: Proc Am Assoc Zoo Vet. 2007;183
  2. Hermes R, Goritz F, Saragusty J, Sos E, Molnar V, Reid CE, et al. First successful artificial insemination with frozen-thawed semen in rhinoceros. Theriogenology. 2009;71:393–399
  3. O’Brien JK, Roth TL. Post-coital sperm recovery and cryopreservation in the Sumatran rhinoceros (Dicerorhinus sumatrensis) and application to gamete rescue in the African black rhinoceros (Diceros bicornis). J Reprod Fertil. 2000;118:263–271
  4. Roth TL. A review of the reproductive physiology of rhinoceros species in captivity. Int Zoo Yearbook. 2006;40:130–143
  5. Williams KR, Dyche WK, Brinder J, Molteno F, van der Lanken M, Armstrong DL, et al. Longevity in vitro and glycerol toxicity of epididymal sperm recovered from a white rhinoceros (Ceratotherium simum). Theriogenology. 1995;43:353
  6. Lubbe K, Smith RL, Bartels P, Godke RA. Freezing epidiymal sperm from white rhinoceroses (Ceratotherium simim) treated with different cyrodiluents. Theriogenology. 1999;51:288
  7. Lubbe K, Bartels P, Kilian I, Friedmann Y, Godke RA. Comparing motility and morphology of horse, zebra and rhinoceros epididymal spermatozoa when cyropreserved with two different cryodiluents stored at 4°C. Theriogenology. 2000;53:338
  8. Hermes R, Hildebrandt TB, Blottner S, Walzer C, Silinski S, Patton ML, et al. Reproductive soundness of captive southern and northern white rhinoceroses (Ceratotherium simum simum, C.s. cottoni): evaluation of male genital tract morphology and semen quality before and after cyropreservation. Theriogenology. 2005;63:219–238
  9. Reid CE, Hermes R, Blottner S, Goeritz F, Wibbelt G, Walzer C, et al. Split-sample comparison of directional and liquid nitrogen vapour freezing method on post-thaw semen quality in white rhinoceroses (Ceratotherium simum simum and Ceratotherium simum cottoni). Theriogenology. 2009;71:275–291
  10. Hlavacek G, Pagan O, Steck B. In: International studbook for the greater one-horned or Indian rhinoceros Rhinoceros unicornis Linne’ 1758—14th Ed. Zoo Basel, Switzerland; 2007. p. 8-10.
  11. Merenlender AM, Woodruff DS, Ryder OA, Kock R, Vahala J. Alloenzyme variation and differentiation in African and Indian rhinoceroses. J Hered. 1989;80:377–382
  12. Zschokke S, Baur B. Inbreeding, outbreeding, infant growth, and size dimorphism in captive Indian rhinoceros (Rhinoceros unicornis). Can J Zool. 2002;80:2014–2023
  13. Zschokke S, Studer P, Baur B. Past and future breeding of the Indian rhinoceros in captivity. Int Zoo News. 1998;45:261–276
  14. Samper JC, Morris CA. Current methods for stallion semen cyropreservation: a survey. Theriogenology. 1998;49:895–903
  15. Bergeron A, Manjunath P. New insights towards understanding the mechanisms of sperm protection by egg yolk and milk. Mol Reprod Dev. 2006;73:1338–1344
  16. Bedford SJ, Graham JK, Amann RP, Squires EL, Pickett BW. Use of two freezing extenders to cool stallion spermatozoa to 5°C with and without seminal plasma. Theriogenology. 1995;43:939–953
  17. Bedford SJ, Jasko DJ, Graham JK, Amann RP, Squires EL, Pickett BW. Effect of seminal extenders containing egg yolk and glycerol on motion characteristics and fertility of stallion spermatozoa. Theriogenology. 1995;43:955–967
  18. Braun J, Hochi S, Oguri N, Sato K, Torres-Boggino F. Effect of different protein supplements on motility and plasma membrane integrity of frozen-thawed stallion spermatozoa. Cyrobiol. 1995;32:487–492
  19. Wilhelm KM, Graham JK, Squires EL. Comparison of the fertility of cryopreserved stallion spermatozoa with sperm motion analyses, flow cytometric evaluation, and zona-free hamster oocyte pentration. Theriogenology. 1996;46:559–578
  20. Crockett EC, Graham JK, Bruemmer JE, Squires EL. Effect of cooling of equine spermatozoa before freezing on post-thaw motility: preliminary results. Theriogenology. 2001;55:793–803
  21. Roth TL, Stoops MA, Atkinson MW, Blumer ES, Campbell MK, Cameron KN, et al. Semen collection in rhinoceroses (Rhinoceros unicornis, Diceros bicornis, Ceratotherium simum) by electroejaculation with a uniquely designed probe. J Zoo Wildlife Med. 2005;36:617–627
  22. Howard JG, Bush M, Wildt DE. Semen collection, analysis and cyropreservation in nondomestic mammals. In:  Marrow DA editors. Current Therapy in Theriogenology. Philadelphia: WB Saunders Co; 1986;p. 1047–1053
  23. Martin JC, Klug E, Gunzel AR. Centrifugation of stallion semen and its storage in large volume straws. J Reprod Fertil. 1979;(Suppl. 27):47–51
  24. Roth TL, Bush LM, Wildt DE, Weiss RB. Scimitar-horned oryx (Oryx dammah) spermatozoa are functionally competent in a heterologous bovine in vitro fertilization system after cyropreservation on dry ice, in a dry shipper, or over liquid nitrogen vapor. Bio Reprod. 1999;60:493–498
  25. Parrish JJ, Susko-Parrish JL, Critser ES, Eyestone WH, First NL. Bovine in vitro fertilization with frozen-thawed semen. Theriogenology. 1986;25:591–600
  26. Munro CJ, Lasley BL. Non-radiometric methods for immunoassay of steroid hormones. In:  Albertson BD,  Haseltine FP editor. Non-radiometric Assays: Technology and Application in Polypeptide and Steroid Hormone Detection. New York: Alan R. Liss; 1988;p. 289–329
  27. Ginther OJ. Ultrasonic imaging and animal reproduction: horses. Wisconsin: Equiservices Publishing; 1995;pp. 311–34
  28. Schaffer N, Beehler B, Jeyendran RS, Balke B. Methods of semen collection in an ambulatory greater one-horned rhinoceros (Rhinoceros unicornis). J Zoo Biol. 1990;9:211–221
  29. Rajamannan AHJ, Zemjanis R, Ellery J. Freezing and fertility studies with stallion semen. In: Proc VI Inter Congr Anim Reprod and Art Insem. 1968;2:1601
  30. Pickett BW, Faulkner LC, Seidel GE, Berndtson WE, Voss JL. Reproductive physiology of the stallion. VI. Seminal and behavioral characteristics. J Anim Sci. 1976;43:617–625
  31. Card C. Cellular associations and the differential spermiogram: making sense of stallion spermatozoal morphology. Theriogenology. 2005;64:558–567
  32. Van Eldik P, van der Waaij E, Ducro B, Kooper A, Stout T, Colenbrander B. Possible negative effects of inbreeding on semen quality in Shetland pony stallions. Theriogenology. 2006;65:1159–1170
  33. Brown JL, Bellem AC, Fouraker M, Wildt DE, Roth TL. Comparative analysis of gonadal and adrenal activity in the black and white rhinoceros in North America by noninvasive endocrine monitoring. Zoo Biol. 2001;20:463–485
  34. Kretzschmar P, Ganslober U, Dehnhard M. Relationship between androgens, environmental factors and reproductive behavior in male white rhinoceros (Ceratotherium simum simum). Hormones and Behav. 2004;45:1–9
  35. Christensen BW, Troedsson MHT, Young LJ, Oliva M, Penfold LM. Effects of sociosexual environment on serum testosterone in captive male African rhinoceros. Theriogenology. 2009;71:1105–1111
  36. Clay CM, Squires EL, Amann RP, Nett TM. Influences of season and artificial photoperiod on stallions: pituitary and testicular responses to exogenous GnRH. J Anim Sci. 1989;67:763–770
  37. McDonnell SM. Stallion behavior and endocrinology: what do we really know?. In: Proc Amer Assoc Equi Pract. 1995;41:18–29
  38. Endo H, Yamada TK, Nakamuta N, Tanemura K, Kurohmaru M, Hayashi Y. Testicular morphology of a greater Indian rhinoceros (Rhinoceros unicornis). J Vet Med Sci. 1996;58:937–940
  39. Silva AR, Cardoso RCS, Uchoa DC, Silva LDM. Quality of canine semen submitted to single or fractionated glycerol addition during the freezing process. Theriogenology. 2003;59:821–829
  40. Watson PF. The causes of reduced fertility with cyropreserved semen. Ani Repro Sci. 2000;60–61:481–492
  41. Vidament M, Daire C, Yvon JM, Doligez P, Bruneau B, Magistrini M, et al. Motility and fertility of stallion semen frozen with glycerol and/or dimethyl formamide. Theriogenology. 2002;58:249–251
  42. Moore AI, Squires EL, Bruemmer JE, Graham JK. Effect of cooling rate and cryoprotectant on the cryosurvival of equine spermatozoa. J Equi Vet Sci. 2006;26:215–218
  43. Scherzer J, Fayrer-Hosken RA, Aceves M, Hurley DJ, Ray LE, Jone L, et al. Freezing equine semen: the effect of combinations of semen extenders and glycerol on post-thaw motility. Aust Vet J. 2009;87:275–279
  44. Ball BA, Vo A. Osmotic tolerance of equine spermatozoa and the effects of soluble cryoprotectants on equine sperm motility, viability and mitochondrial membrane potential. J Androl. 2001;22:1061–1069
  45. Parks JE, Lynch DV. Lipid composition and thermotropic phase behavior of boar, bull, stallion and rooster sperm membranes. Cryobiol. 1992;29:255–266
  46. Cristanelli MJ, Amann RP, Squires EL, Pickett BW. Effects of egg yolk and glycerol levels in lactose-EDTA-egg yolk extender and of freezing rate on the motility of frozen-thawed stallion spermatozoa. Theriogenology. 1985;24:681–686

PII: S0093-691X(10)00031-2

doi: 10.1016/j.theriogenology.2010.01.011

Theriogenology
Volume 73, Issue 8 , Pages 1104-1115 , May 2010