Advertisement

Recent Advances and Prospects in Germplasm Preservation of Rare and Endangered Species

  • Pierre ComizzoliEmail author
  • William V. Holt
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 753)

Abstract

Fertility preservation strategies using cryopreservation have enormous potential for helping sustain and protect rare and endangered species, especially to assist managing or ‘rescuing’ the genomes of genetically valuable individuals. However, wide-scale applications are still limited by significant physiological variations among species and a sheer lack of fundamental knowledge about basic reproductive traits as well as in germplasm cryobiology. Cryo-studies have been conducted in more species (mainly vertebrates) in the recent years but a vast majority still remains un-studied. Semen cryopreservation represents the most extensive effort with live births reported in more and more species after artificial insemination. Oocyte freezing remains challenging and unsuccessful in wild species and will require more research before becoming a standard procedure. As an alternative to fully grown gametes, gonadal tissue preservation has become a promising option in vertebrates. Yet, more fertility preservation options are necessary to save species so a change in strategy might be required. It is worthwhile thinking beyond systematic characterizations and considering the application of cutting edge approaches to universally preserve the fertility of a vast array of species.

Keywords

Cryopreservation Spermatozoa Oocytes Embryos Testis Ovary 

References

  1. Adams SL, Tervit HR, McGowan LT, Smith JF, Roberts RD, Salinas-Flores L, Gale SL, Webb SC, Mullen SF, Critser JK. Towards cryopreservation of Greenshell mussel (Perna canaliculus) oocytes. Cryobiology. 2009;58:69–74.PubMedGoogle Scholar
  2. Alvarez-Rodriguez M, Alvarez M, Borragan S, Martinez-Pastor F, Holt WV, Fazeli A, de Paz P, Anel L. The addition of heat shock protein HSPA8 to cryoprotective media improves the survival of brown bear (Ursus arctos) spermatozoa during chilling and after cryopreservation. Theriogenology. 2013;79:541–50.PubMedGoogle Scholar
  3. Arav A, Natan D. Directional freezing of reproductive cells and organs. Reprod Domest Anim. 2012;47 Suppl 4:193–6.PubMedGoogle Scholar
  4. Banno Y, Nagasaki K, Tsukada M, Minohara Y, Banno J, Nishikawa K, Yamamoto K, Tamura K, Fujii T. Development of a method for long-term preservation of Bombyx mori silkworm strains using frozen ovaries. Cryobiology. 2013;66:283–7.PubMedGoogle Scholar
  5. Ben-Nun IF, Montague SC, Houck ML, Tran HT, Garitaonandia I, Leonardo TR, Wang YC, Charter SJ, Laurent LC, Ryder OA, Loring JF. Induced pluripotent stem cells from highly endangered species. Nat Meth. 2011;8:829–31.Google Scholar
  6. Billard R, Zhang TT. Techniques of genetic resource banking in fish. In: Watson PF, Holt WV, editors. Cryobanking the genetic resource: wildlife conservation for the future? London: Taylor and Francis; 2001. p. 145–70.Google Scholar
  7. Blanco JM, Long JA, Gee G, Donoghue AM, Wildt DE. Osmotic tolerance of avian spermatozoa: influence of time, temperature, cryoprotectant and membrane ion pump function on sperm viability. Cryobiology. 2008;56:8–14.PubMedGoogle Scholar
  8. Blanco JM, Long JA, Gee G, Wildt DE, Donoghue AM. Comparative cryopreservation of avian spermatozoa: benefits of non-permeating osmoprotectants and ATP on turkey. Anim Reprod Sci. 2011;123:242–8.PubMedGoogle Scholar
  9. Boutelle S, Lenahan K, Krisher R, Bauman KL, Asa CS, Silber S. Vitrification of oocytes from endangered Mexican gray wolves (Canis lupus baileyi). Theriogenology. 2011;75:647–54.PubMedGoogle Scholar
  10. Cleary M, Shaw JM, Jenkin G, Trounson AO. Influence of hormone environment and donor age on cryopreserved common wombat (Vombatus ursinus) ovarian tissue xenografted into nude mice. Reprod Fertil Dev. 2004;16:699–707.PubMedGoogle Scholar
  11. Comizzoli P, Wildt DE. On the horizon for fertility preservation in domestic and wild carnivores. Reprod Domest Anim. 2012a;47 Suppl 6:261–5.PubMedCentralPubMedGoogle Scholar
  12. Comizzoli P, Wildt DE. Centrosomal functions and dysfunctions in cat spermatozoa. Centrosome research. In: Schatten H, editor. The centrosome. Totowa, NJ: Humana; 2012b. p. 49–58.Google Scholar
  13. Comizzoli P, Wildt DE, Pukazhenthi BS. Effect of 1,2-propanediol versus 1,2-ethanediol on subsequent oocyte maturation, spindle integrity, fertilization and embryo development in vitro in the domestic cat. Biol Reprod. 2004;71:598–604.PubMedGoogle Scholar
  14. Comizzoli P, Wildt DE, Pukazhenthi BS. Impact of anisosmotic conditions on structural and functional integrity of cumulus-oocyte complexes at the germinal vesicle stage in the domestic cat. Mol Reprod Dev. 2008;75:345–54.PubMedCentralPubMedGoogle Scholar
  15. Comizzoli P, Songsasen N, Wildt DE. Protecting and extending fertility for females of wild and endangered mammals. Cancer Treat Res. 2010;156:87–100.PubMedCentralPubMedGoogle Scholar
  16. Comizzoli P, Songsasen N, Hagedorn M, Wildt DE. Comparative cryobiological traits and requirements for gametes and gonadal tissues collected from wildlife species. Theriogenology. 2012;78:1666–81.PubMedGoogle Scholar
  17. Critser JK, Agca Y, Woods E. Cryopreservation of immature and mature gametes. In: De Jonge CJ, Barratt CLR, editors. Assisted reproductive technology: accomplishment and new horizons. Cambridge: Cambridge University Press; 2002. p. 144–66.Google Scholar
  18. Crosier AE, Pukazhenthi BS, Henghali JN, Howard J, Dickman AJ, Marker L, Wildt DE. Cryopreservation of spermatozoa from wild-born Namibian cheetahs (Acinonyx jubatus) and influence of glycerol on cryosurvival. Cryobiology. 2006;5:169–81.Google Scholar
  19. Crowe JH, Oliver AE, Tablin F. Is there a single biochemical adaptation to anydrobiosis? Integ Comp Biol. 2002;42:497–503.Google Scholar
  20. Crowe JH, Crowe LM, Wolkers WF, Oliver AE, Ma X, Auh J-H, Tang M, Zhu S, Norris J, Tablin F. Stabilization of dry mammalian cells: lesions from nature. Integ Comp Biol. 2005;45: 810–20.Google Scholar
  21. Czarny NA, Rodger JC. Vitrification as a method for genome resource banking oocytes from the endangered Tasmanian devil (Sarcophilus harrisii). Cryobiology. 2010;60:322–5.PubMedGoogle Scholar
  22. Dunlop CE, Telfer EE, Anderson RA. Ovarian stem cells-potential roles in infertility treatment and fertility preservation. Maturitas. (2013). pii: S0378-5122(13)00128-X. doi: 10.1016/j.maturitas.2013.04.017.
  23. Dyce PW, Liu J, Tayade C, Kidder GM, Betts DH, Li J. In vitro and in vivo germ line potential of stem cells derived from newborn mouse skin. PLoS One. 2011;6:e20339.PubMedCentralPubMedGoogle Scholar
  24. Ehmcke J, Schlatt S. Animal models for fertility preservation in the male. Reproduction. 2008;136:717–23.PubMedGoogle Scholar
  25. Fickel J, Wagener A, Ludwig A. Semen cryopreservation and the conservation of endangered species. Eur J Wildlife Res. 2007;53:81–9.Google Scholar
  26. Gilmore JA, McGann LE, Ashworth E, Acker JP, Raath JP, Bush M, Critser JK. Fundamental cryobiology of selected African mammalian spermatozoa and its role in biodiversity preservation through the development of genome resource banking. Anim Reprod Sci. 1998;53: 277–97.PubMedGoogle Scholar
  27. Gosalvez J, Lopez-Fernandez C, Fernandez JL, Gouraud A, Holt WV. Relationships between the dynamics of iatrogenic DNA damage and genomic design in mammalian spermatozoa from eleven species. Mol Reprod Dev. 2011;78:951–61.PubMedGoogle Scholar
  28. Gourdon JC, Travis AJ. Spermatogenesis in ferret testis xenografts: a new model. Comp Med. 2011;61:145–9.PubMedCentralPubMedGoogle Scholar
  29. Graves-Herring JE, Wildt DE, Comizzoli P. Retention of structure and function of the cat germinal vesicle after air-drying and storage at suprazero temperature. Biol Reprod. 2013;88:139.PubMedCentralPubMedGoogle Scholar
  30. Hermes R, Göritz F, Saragusty J, Sós E, Molnar V, Reid CE, Schwarzenberger F, Hildebrandt TB. First successful artificial insemination with frozen-thawed semen in rhinoceros. Theriogenology. 2009;71:393–9.PubMedGoogle Scholar
  31. Hildebrandt TB, Roellig K, Goeritz F, Fassbender M, Krieg R, Blottner S, Behr B, Hermes R. Artificial insemination of captive European brown hares (Lepus europaeus PALLAS, 1778) with fresh and cryopreserved semen derived from free-ranging males. Theriogenology. 2009;72:1065–72.PubMedGoogle Scholar
  32. Holt WV. Germplasm cryopreservation in elephants and wild ungulates. In: Watson PF, Holt WV, editors. Cryobanking the genetic resource: wildlife conservation for the future? London: Taylor and Francis; 2001. p. 319–48.Google Scholar
  33. Holt WV. Who needs cytoplasm? Genomic preservation for the 21st century. Biol Reprod. 2013;88:1–2.Google Scholar
  34. Holt WV, Penfold LM, Johnston SD, Temple-Smith P, McCallum C, Shaw J, Lindemans W, Blyde D. Cryopreservation of macropodid spermatozoa: new insights from the cryomicroscope. Reprod Fert Dev. 2000;11:345–53.Google Scholar
  35. Holt WV, Penfold LM, Watson PF. Cryopreservation of lagomorphs gametes and embryos. In: Watson PF, Holt WV, editors. Cryobanking the genetic resource: wildlife conservation for the future? London: Taylor and Francis; 2001. p. 319–48.Google Scholar
  36. Holt WV, Abaigar T, Watson PF, Wildt DE. Genetic resource banks for species conservation. In: Holt WV, Pickard A, Rodger JC, Wildt DE, editors. Reproductive sciences and integrated conservation. Cambridge: Cambridge University Press; 2003. p. 2–20.Google Scholar
  37. Honaramooz A. Cryopreservation of testicular tissue in current frontiers in cryobiology edited by Igor I. Katkov. New York: InTech; 2012.Google Scholar
  38. Howard JG, Wildt DE. Approaches and efficacy of artificial insemination in felids and mustelids. Theriogenology. 2009;71:130–48.PubMedGoogle Scholar
  39. Howard JG, Marinari PE, et al. Black-footed ferret: model for assisted reproductive technologies contributing to in situ conservation. In: Holt WV, Pickard AR, Rodger JC, Wildt DE, editors. Reproductive science and integrated conservation, vol. 8. Cambridge: Cambridge University Press; 2003. p. 249–66.Google Scholar
  40. Huang Y, Li DS, et al. Factors affecting the outcome of artificial insemination using cryopreserved Spermatozoa in the Giant Panda (Ailuropoda melanoleuca). Zoo Biol. 2012a;31:561–73.PubMedGoogle Scholar
  41. Huang Y, Zhang H, et al. Relationship of the estrogen surge and multiple mates to cub paternity in the Giant Panda (Ailuropoda melanoleuca): implications for optimal timing of copulation or artificial insemination. Biol Reprod. 2012b;87:111–7.Google Scholar
  42. Inoue D, Fujimoto T, Kawakami Y, Yasui GS, Yamaha E, Arai K. Vitrification of primordial germ cells using whole embryos for gene-banking in loach, Misgurnus anguillicaudatus. J Appl Ichthyol. 2012;28:919–24.Google Scholar
  43. Isachenko V, Maettner R, Petrunkina AM, Mallmann P, Rahimi G, Sterzik K, Sanchez R, Risopatron J, Damjanoski I, Isachenko E. Cryoprotectant-free vitrification of human spermatozoa in large (up to 0.5 mL) volume: a novel technology. Clin Lab. 2011;57:643–50.PubMedGoogle Scholar
  44. Isayeva A, Zhang T, Rawson DM. Studies on chilling sensitivity of zebrafish (Danio rerio) oocytes. Cryobiology. 2004;49:114–22.PubMedGoogle Scholar
  45. Jewgenow K, Wiedemann C, Bertelsen MF, Ringleb J. Cryopreservation of mammalian ovaries and oocytes. Intl Zoo Yrbk. 2011;45:124–32.Google Scholar
  46. Johnson LA, Weitze KF, Fiser P, Maxwell WMC. Storage of boar semen. Anim Reprod Sci. 2000;62:143–72.PubMedGoogle Scholar
  47. Johnston SD, Holt WV. Germplasm conservation in marsupials. In: Watson PF, Holt WV, editors. Cryobanking the genetic resource. Wildlife conservation for the future? London: Taylor and Francis; 2001. p. 203–25.Google Scholar
  48. Johnston SD, Satake N, et al. Osmotic stress and cryoinjury of koala sperm: an integrative study of the plasma membrane, chromatin stability and mitochondrial function. Reproduction. 2012;143:787–97.PubMedGoogle Scholar
  49. Kawakami Y, Saito T, Fujimoto T, Goto-Kazeto R, Takahashi E, Adachi S, Arai K, Yamaha E. Technical note: viability and motility of vitrified/thawed primordial germ cell isolated from common carp (Cyprinus carpio) somite embryos. J Anim Sci. 2012;90:495–500.PubMedGoogle Scholar
  50. Kim S, Lee Y, Yang H, Kim YJ. Rapid freezing without cooling equilibration in canine sperm. Anim Reprod Sci. 2012;130:111–8.PubMedGoogle Scholar
  51. Kiso WK, Brown JL, Siewerdt F, Schmitt DL, Olson D, Crichton EG, Pukazhenthi BS. Liquid semen storage in elephants (Elephas maximus and Loxodonta africana): species differences and storage optimization. J Androl. 2011;32:420–31.PubMedGoogle Scholar
  52. Kobayashi T, Takeuchi Y, Takeuchi T, Yoshizaki G. Generation of viable fish from cryopreserved primordial germ cells. Mol Reprod Dev. 2007;74:207–13.PubMedGoogle Scholar
  53. Kouba AJ, Vance CK. Applied reproductive technologies and genetic resource banking for amphibian conservation. Reprod Fertil Dev. 2009;21:719–37.PubMedGoogle Scholar
  54. Lee S, Iwasaki Y, Shikina S, Yoshizaki G. Generation of functional eggs and sperm from cryopreserved whole testes. Proceedings of the National Academy of Sciences of the United States of America. 2013;110:1640–45.Google Scholar
  55. Leibo SP, Songsasen N. Cryopreservation of gametes and embryos of non-domestic species. Theriogenology. 2002;57:303–26.PubMedGoogle Scholar
  56. Lermen D, Blömeke B, Browne R, Clarke A, Dyce PW, Fixemer T, Fuhr GR, Holt WV, Jewgenow K, Lloyd RE, Lötters S, Paulus M, Reid GM, Rapoport DH, Rawson D, Ringleb J, Ryder OA, Spörl G, Schmitt T, Veith M, Müller P. Cryobanking of viable biomaterials: implementation of new strategies for conservation purposes. Mol Ecol. 2009;18:1030–3.PubMedGoogle Scholar
  57. Lindeberg H, Aalto J, Amstislavsky S, Piltti K, Järvinen M, Valtonen M. Surgical recovery and successful surgical transfer of conventionally frozen-thawed embryos in the farmed European polecat (Mustela putorius). Theriogenology. 2003;60:1515–25.PubMedGoogle Scholar
  58. Liu J, ChengKM SFG. Fundamental principles of cryobiology and application to ex situ conservation of avian species. Avian Biol Res. 2013a;6:187–97.Google Scholar
  59. Liu J, Song Y, Cheng KM, Silversides FG. Production of donor-derived offspring from cryopreserved ovarian tissue in Japanese quail (Coturnix japonica). Biol Reprod. 2010;83:15–9.PubMedGoogle Scholar
  60. Liu J, Cheng KM, Silversides FG. Production of live offspring from testicular tissue cryopreserved by vitrification procedures in Japanese quail (Coturnix japonica). Biol Reprod. 2013b;88:124.PubMedGoogle Scholar
  61. Locatelli Y, Hendriks A, Vallet JC, Baril G, Duffard N, Bon N, Ortiz K, Scala C, Maurel MC, Mermillod P, Legendre X. Assessment LOPU-IVF in Japanese sika deer (Cervus nippon nippon) and application to Vietnamese sika deer (Cervus nippon pseudaxis) a related subspecies threatened with extinction. Theriogenology. 2012;78:2039–49.PubMedGoogle Scholar
  62. Mazur P, Leibo SP, Seidel Jr GE. Cryopreservation of the germplasm of animals used in biological and medical research: importance, impact, status and future directions. Biol Reprod. 2008;78: 2–12.PubMedGoogle Scholar
  63. McClean R, Zee YP, et al. Cryopreservation of kangaroo spermatozoa using alternative approaches that reduce cytotoxic exposure to glycerol. Cryobiology. 2008;57:304–7.PubMedGoogle Scholar
  64. McEvoy TG, Coull GD, Broadbent PJ, Hutchinson JS, Speake BK. Fatty acid composition of lipids in immature cattle, pig and sheep oocytes with intact zona pellucida. J Reprod Fertil. 2000;118:163–70.PubMedGoogle Scholar
  65. Mochida Y, Takemura Y, Kanda T, Horie Y. Fertilized eggs obtained from transplantation of frozen ovaries and parthenogenesis in combination with artificial insemination of frozen semen of the silkworm, Bombyx mori. Cryobiology. 2003;46:153–60.PubMedGoogle Scholar
  66. Molinia FC, Rodger JC. Pellet-freezing spermatozoa of two marsupials: the tammar wallaby, Macropus eugenii, and the brushtail possum, Trichosurus vulpecula. Reprod Fertil Dev. 1996;8:681–4.PubMedGoogle Scholar
  67. Nayernia K, Nolte J, Michelmann HW, Lee JH, Rathsack K, Drusenheimer N, Dev A, Wulf G, Ehrmann IE, Elliott DJ, Okpanyi V, Zechner U, Haaf T, Meinhardt A, Engel W. In vitro-differentiated embryonic stem cells give rise to male gametes that can generate offspring mice. Dev Cell. 2006;11:125–32.PubMedGoogle Scholar
  68. Nelissen EC, Van Montfoort AP, Coonen E, Derhaag JG, Geraedts JP, Smits LJ, Land JA, Evers JL, Dumoulin JC. Further evidence that culture media affect perinatal outcome: findings after transfer of fresh and cryopreserved embryos. Hum Reprod. 2004;27:1966–76.Google Scholar
  69. O’Brien JK, Robeck TR. Development of sperm sexing and associated assisted reproductive technology for sex preselection of captive bottlenose dolphins (Tursiops truncatus). Reprod Fertil Dev. 2006;18:319–29.Google Scholar
  70. Paris MC, Snow M, Cox SL, Shaw JM. Xenotransplantation: a tool for reproductive biology and animal conservation? Theriogenology. 2004;61:277–91.PubMedGoogle Scholar
  71. Penfold LM, L Monfort S, Wolfe BA, Citino SB, Wildt DE. Reproductive physiology and artificial insemination studies in wild and captive gerenuk (Litocranius walleri walleri). Reprod Fertil Dev. 2005;17:707–14.PubMedGoogle Scholar
  72. Pickard AR, Holt WV. Cryopreservation as a supporting measure in species conservation. In: Benson E, Fuller B, Lane N, editors. Not the frozen zoo! Life in the frozen state. Baton Rouge, LA: CRC Press; 2004. p. 393–413.Google Scholar
  73. Pope CE, Gómez MC, Dresser BL. In vitro production and transfer of cat embryos in the 21st century. Theriogenology. 2006;66:59–71.PubMedGoogle Scholar
  74. Pope CE, Gómez MC, Kagawa N, Kuwayama M, Leibo SP, Dresser BL. In vivo survival of domestic cat oocytes after vitrification, intracytoplasmic sperm injection and embryo transfer. Theriogenology. 2012;77:531–8.PubMedGoogle Scholar
  75. Pukazhenthi B, Spindler R, Wildt D, Bush LM, Howard J. Osmotic properties of spermatozoa from felids producing different proportions of pleiomorphisms: influence of adding and removing cryoprotectant. Cryobiology. 2002;44:288–300.PubMedGoogle Scholar
  76. Pukazhenthi BS, Lapiana F, Padilla L, Santiestevan J, Coutinho da Silva M, Alvarenga M, Wildt DE. Improved sperm cryopreservation in the critically endangered Przewalski's horse (Equus ferus przewalskii) using different cryoprotectants. Biol Reprod. 2010;83:675.Google Scholar
  77. Pukazhenthi BS, Togna GD, Padilla L, Smith D, Sanchez C, Pelican K, Sanjur OI. Ejaculate traits and sperm cryopreservation in the endangered Baird's tapir (Tapirus bairdii). J Androl. 2011;32:260–70.PubMedGoogle Scholar
  78. Rall WF, Fahy GM. Ice-free cryopreservation of mouse embryos at −196°C by vitrification. Nature. 1985;313:573–5.PubMedGoogle Scholar
  79. Riesco MF, Robles V. Cryopreservation causes genetic and epigenetic changes in Zebrafish genital ridges. PLoS One. 2013;8:e67614.PubMedCentralPubMedGoogle Scholar
  80. Ringleb J, Waurich R, Wibbelt G, Streich WJ, Jewgenow K. Prolonged storage of epididymal spermatozoa does not affect their capacity to fertilise in vitro-matured domestic cat (Felis catus) oocytes when using ICSI. Reprod Fertil Dev. 2011;23:818–25.PubMedGoogle Scholar
  81. Roache M. The action plan for threatened Australian macropods. Sydney, NSW: WWF-Australia – World Wide Fund for Nature (formerly World Wildlife Fund); 2011.Google Scholar
  82. Robeck TR, O'Brien JK. Effect of cryopreservation methods and precryopreservation storage on bottlenose dolphin (Tursiops truncatus) spermatozoa. Biol Reprod. 2004;70:1340–8.PubMedGoogle Scholar
  83. Robeck TR, Gearhart SA, Steinman KJ, Katsumata E, Loureiro JD, O'Brien JK. In vitro sperm characterization and development of a sperm cryopreservation method using directional solidification in the killer whale (Orcinus orca). Theriogenology. 2011;76:267–79.PubMedGoogle Scholar
  84. Rossato M, Balercia G, Lucarelli G, Foresta C, Mantero F. Role of seminal osmolarity in the reduction of human sperm motility. Int J Androl. 2002;25:230–5.PubMedGoogle Scholar
  85. Saint Jalme M, Lecoq R, Seigneurin F, Blesbois E, Plouzeau E. Cryopreservation of semen from endangered pheasants: the first step towards a cryobank for endangered avian species. Theriogenology. 2003;59:875–88.PubMedGoogle Scholar
  86. Salinas-Flores L, Adams SL, Lim MH. Determination of the membrane permeability characteristics of Pacific oyster, Crassostrea gigas, oocytes and development of optimized methods to add and remove ethylene glycol. Cryobiology. 2008;56:43–52.PubMedGoogle Scholar
  87. Santymire RM, Marinari PE, Kreeger JS, Wildt DE, Howard J. Sperm viability in the black-footed ferret (Mustela nigripes) is influenced by seminal and medium osmolality. Cryobiology. 2006;53:37–50.PubMedGoogle Scholar
  88. Saragusty J. Genome banking for vertebrates wildlife conservation. In: Katkov I, editor. Current frontiers in cryobiology. New York: InTech; 2012. p. 293–368. 574 p.Google Scholar
  89. Saragusty J, Arav A. Current progress in oocyte and embryo cryopreservation by slow freezing and vitrification. Reproduction. 2011;141:1–19.PubMedGoogle Scholar
  90. Saragusty J, Gacitua H, King R, Arav A. Post-mortem semen cryopreservation and characterization in two different endangered gazelle species (Gazella gazella and Gazella dorcas) and one subspecies (Gazella gazelle acaiae). Theriogenology. 2006;66:775–84.PubMedGoogle Scholar
  91. Saragusty J, Hildebrandt TB, Behr B, Knieriem A, Kruse J, Hermes R. Successful cryopreservation of Asian elephant (Elephas maximus) spermatozoa. Anim Reprod Sci. 2009;115:255–66.PubMedGoogle Scholar
  92. Sato T, Katagiri K, Yokonishi T, Kubota Y, Inoue K, Ogonuki N, Matoba S, Ogura A, Ogawa T. In vitro production of fertile sperm from murine spermatogonial stem cell lines. Nat Commun. 2011;2:472.PubMedGoogle Scholar
  93. Schook MW, Wildt DE, Weiss RB, Wolfe BA, Archibald KE, Pukazhenthi BS. Fundamental studies on the reproductive biology of the endangered Persian onager (Equus hemionus onager) result in first wild equid offspring from artificial insemination. Biol Reprod. 2013;89:41.PubMedGoogle Scholar
  94. Seki S, Kouya T, Tsuchiya R, Valdez Jr DM, Jin B, Koshimoto C, Kasai M, Edashige K. Cryobiological properties of immature zebrafish oocytes assessed by their ability to be fertilized and develop into hatching embryos. Cryobiology. 2011;62:8–14.PubMedGoogle Scholar
  95. Silva RC, Costa GM, Lacerda SM, Batlouni SR, Soares JM, Avelar GF, Böttger KB, Silva Jr SF, Nogueira MS, Andrade LM, França LR. Germ cell transplantation in felids: a potential approach to preserving endangered species. J Androl. 2012;33:264–76.PubMedGoogle Scholar
  96. Songsasen N, Comizzoli P. A historic overview of embryos and oocyte preservation in the world of mammalian in vitro fertilization and biotechnology. In: Borini A, Coticchio G, editors. Preservation of human oocytes. London: Informa Healthcare; 2009. p. 1–11.Google Scholar
  97. Songsasen N, Ratterree MS, VandeVoort CA, Pegg DE, Leibo SP. Permeability characteristics and osmotic sensitivity of rhesus monkey (Macaca mulatta) oocytes. Hum Reprod. 2002;17: 175–84.Google Scholar
  98. Songsasen N, Woodruff TK, Wildt DE. In vitro growth and steroidogenesis of dog follicles are influenced by the physical and hormonal microenvironment. Reproduction. 2011;142:113–22.PubMedCentralPubMedGoogle Scholar
  99. Songsasen N, Comizzoli P, Nagashima J, Fujihara M, Wildt DE. The domestic dog and cat as models for understanding the regulation of ovarian follicle development in vitro. Reprod Domest Anim. 2012;47 Suppl 6:13–8.PubMedCentralPubMedGoogle Scholar
  100. Spallanzani L. Opuscoli de fisice animale e vegetabile opuscola. II. Observatione e sperienze intorno ai vermicelli spermatici dell' homo e degli animali. Modena. (1776).Google Scholar
  101. Stoops MA, Bond JB, Bateman HL, Campbell MK, Levens GP, Bowsher TR, Ferrell ST, Swanson WF. Comparison of different sperm cryopreservation procedures on post-thaw quality and heterologous in vitro fertilisation success in the ocelot (Leopardus pardalis). Reprod Fertil Dev. 2007;19:685–94.PubMedGoogle Scholar
  102. Stoops MA, Atkinson MW, Blumer ES, Campbell MK, Roth TL. Semen cryopreservation in the Indian rhinoceros (Rhinoceros unicornis). Theriogenology. 2010;73:1104–15.PubMedGoogle Scholar
  103. Sturmey RG, Leese HJ. Energy metabolism in pig oocytes and early embryos. Reproduction. 2003;126:197–204.PubMedGoogle Scholar
  104. Sunderam S, Kissin DM, Flowers L, Anderson JE, Folger SG, Jamieson DJ, Barfield WD. Assisted reproductive technology surveillance – United States, 2009. MMWR Surveill Summ. 2012;61:1–23.PubMedGoogle Scholar
  105. Swanson WF. Application of assisted reproduction for population management in felids: the potential and reality for conservation of small cats. Theriogenology. 2006;66:49–58.PubMedGoogle Scholar
  106. Swanson WF. Laparoscopic oviduct embryo transfer and artificial insemination in felids – challenges, strategies and successes. Reprod Dom Anim. 2012;47 Suppl 6:136–40.Google Scholar
  107. Tharasanit T, Manee-In S, Buarpung S, Chatdarong K, Lohachit C, Techakumphu M. Successful pregnancy following transfer of feline embryos derived from vitrified immature cat oocytes using 'stepwise' cryoprotectant exposure technique. Theriogenology. 2011;76:1442–9.PubMedGoogle Scholar
  108. Thompson JG, Allen NW, McGowan LT, Bell AC, Lambert MG, Tervit HR. Effect of delayed supplementation of fetal calf serum to culture medium on bovine embryo development in vitro and following transfer. Theriogenology. 1998;49:1239–49.PubMedGoogle Scholar
  109. Thongtip N, Mahasawangkul S, Thitaram C, Pongsopavijitr P, Kornkaewrat K, Pinyopummin A, Angkawanish T, Jansittiwate S, Rungsri R, Boonprasert K, Wongkalasin W, Homkong P, Dejchaisri S, Wajjwalku W, Saikhun K. Successful artificial insemination in the Asian elephant (Elephas maximus) using chilled and frozen-thawed semen. Reprod Biol Endocrinol. 2009;7:75.PubMedCentralPubMedGoogle Scholar
  110. Travis AJ, Kim Y, Meyers-Wallen V. Development of new stem cell-based technologies for carnivore reproduction research. Reprod Domest Anim. 2009;44 Suppl 2:22–8.PubMedCentralPubMedGoogle Scholar
  111. Verma R, Holland MK, Temple-Smith P, Verma PJ. Inducing pluripotency in somatic cells from the snow leopard (Panthera uncia), an endangered felid. Theriogenology. 2012;77:220–8.PubMedGoogle Scholar
  112. Waimey KE, Duncan FE, Su HI, Smith K, Wallach H, Jona K, Coutifaris C, Gracia CR, Shea LD, Brannigan RE, Chang RJ, Zelinski MB, Stouffer RL, Taylor RL, Woodruff TK. Future directions in oncofertility and fertility preservation: a report from the 2011 oncofertility consortium conference. J Adolesc Young Adult Oncol. 2013;2:25–30.PubMedCentralPubMedGoogle Scholar
  113. Watanabe H, Asano T, Abe Y, Fukui Y, Suzuki H. Pronuclear formation of freeze-dried canine spermatozoa microinjected into mouse oocytes. J Assist Reprod Genet. 2009;26:531–6.PubMedCentralPubMedGoogle Scholar
  114. Watson PF. Artificial insemination and the preservation of semen. In: Lamming G, editor. Marshall's physiology of reproduction, vol. 2. London: Churchill Livingstone; 1990. p. 747–869.Google Scholar
  115. Watson PF, Holt WV. Cryobanking the genetic resource; wildlife conservation for the future? London: Taylor and Francis; 2001.Google Scholar
  116. Watson PF, Kunze E, Cramer P, Hammerstedt RH. A comparison of critical osmolality and hydraulic conductivity and its activation energy in fowl and bull spermatozoa. J Androl. 1992;13:131–8.PubMedGoogle Scholar
  117. Wiedemann C, Zahmel J, Jewgenow K. Short-term culture of ovarian cortex pieces to assess the cryopreservation outcome in wild felids for genome conservation. BMC Vet Res. 2013;9:37.PubMedCentralPubMedGoogle Scholar
  118. Wildt DE, Rall WF, Critser JK, Monfort SL, Seal US. Genome resource banks: ‘living collections’ for biodiversity conservation. BioScience. 1997;47:689–98.Google Scholar
  119. Wildt DE, Ellis S, Janssen D, Buff J. Toward more effective reproductive science in conservation. In: Holt WV, Pickard A, Rodger JC, Wildt DE, editors. Reproductive sciences and integrated conservation. Cambridge: Cambridge University Press; 2003. p. 2–20.Google Scholar
  120. Wildt DE, Comizzoli P, Pukazhenthi B, Songsasen N. Lessons from biodiversity – the value of nontraditional species to advance reproductive science, conservation and human health. Mol Reprod Dev. 2010;77:397–409.PubMedCentralPubMedGoogle Scholar
  121. Wishart GJ. The cryopreservation of germplasm in domestic and non-domestic birds. In: Watson PF, Holt WV, editors. Cryobanking the genetic resource. Wildlife conservation for thye future? London: Taylor and Francis; 2001. p. 179–200.Google Scholar
  122. Wolfe BA, Wildt DE. Development to blastocysts of domestic cat oocytes matured and fertilized in vitro after prolonged cold storage. J Reprod Fertil. 1996;106:135–41.PubMedGoogle Scholar
  123. Woods EJ, Benson JD, Agca Y, Critser JK. Fundamental cryobiology of reproductive cells and tissues. Cryobiology. 2004;48:146–56.PubMedGoogle Scholar
  124. Yamauchi Y, Shaman JA, Ward WS. Non-genetic contributions of the sperm nucleus to embryonic development. Asian J Androl. 2011;13:31–5.PubMedCentralPubMedGoogle Scholar
  125. Yang CR, Miao DQ, Zhang QH, Guo L, Tong JS, Wei Y, Huang X, Hou Y, Schatten H, Liu Z, Sun QY. Short-term preservation of porcine oocytes in ambient temperature: novel approaches. PLoS One. 2010;5:e14242.PubMedCentralPubMedGoogle Scholar
  126. Yasui GS, Fujimoto T, Sakao S, Yamaha E, Arai K. Production of loach (Misgurnus anguillicaudatus) germ-line chimera using transplantation of primordial germ cells isolated from cryopreserved blastomeres. J Anim Sci. 2011;89:2380–8.PubMedGoogle Scholar
  127. Yavin S, Arav A. Measurement of essential physical properties of vitrification solutions. Theriogenology. 2007;67:81–9.PubMedGoogle Scholar
  128. Zee YP, Holt WV, Gosalvez J, Allen CD, Nicolson V, Pyne M, Burridge M, Carrick FN, Johnston SD. Dimethylacetamide can be used as an alternative to glycerol for the successful cryopreservation of koala (Phascolarctos cinereus) spermatozoa. Reprod Fertil Dev. 2008;20:724–33.PubMedGoogle Scholar
  129. Zee YP, Lopez-Fernandez C, et al. Evidence that single-stranded DNA breaks are a normal feature of koala sperm chromatin, while double-stranded DNA breaks are indicative of DNA damage. Reproduction. 2009;138:267–78.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  1. 1.Smithsonian Conservation Biology Institute, National Zoological ParkWashington, DCUSA
  2. 2.Academic Department of Reproductive and Developmental MedicineUniversity of SheffieldSheffieldUK

Personalised recommendations