1932

Abstract

Anthropogenic environmental change has led to unprecedented rates of species extinction, presenting a major threat to global biodiversity. Among vertebrates, amphibians have been most severely impacted, with an estimated 41% of species now threatened with extinction. In response to this biodiversity crisis, a moral and ethical obligation exists to implement proactive interventionist conservation actions to assist species recovery and decelerate declines. Conservation breeding programs have been successfully established for several threatened amphibian species globally, aiming to prevent species’ extinction by maintaining genetically representative assurance colonies ex situ while providing individuals for population augmentation, translocation, and reestablishment in situ. Reproductive technologies have enormous potential to enhance the propagation and genetic management of threatened species. In this review, we discuss the role of reproductive technologies in amphibian conservation breeding programs and summarize technological advancements in amphibian hormone therapies, gamete storage, and artificial fertilization.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-animal-020518-115056
2019-02-15
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/animal/7/1/annurev-animal-020518-115056.html?itemId=/content/journals/10.1146/annurev-animal-020518-115056&mimeType=html&fmt=ahah

Literature Cited

  1. 1.  Ceballos G, Ehrlich PR, Barnosky AD, García A, Pringle RM, Palmer TM 2015. Accelerated modern human–induced species losses: entering the sixth mass extinction. Sci. Adv. 1:e1400253
    [Google Scholar]
  2. 2. Int. Union Conserv. Nat. 2017. Table 3a: status category summary by major taxonomic group (animals) Red List of Threatened Species, Version 2017.3 Int. Union Conserv. Nat Gland, Switz: http://cmsdocs.s3.amazonaws.com/summarystats/2017-3_Summary_Stats_Page_Documents/2017_3_RL_Stats_Table_3a.pdf
  3. 3. Int. Union Conserv. Nat. 2017. Table 1: numbers of threatened species by major groups of organisms (1996–2017) Red List of Threatened Species, Version 2017.3 Int. Union Conserv. Nat Gland, Switz: http://cmsdocs.s3.amazonaws.com/summarystats/2017-3_Summary_Stats_Page_Documents/2017_3_RL_Stats_Table_1.pdf
  4. 4.  Phillips K 1990. Where have all the frogs and toads gone? A recent workshop described an apparent decline worldwide of amphibian populations. Bioscience 40:422–24
    [Google Scholar]
  5. 5.  Pounds JA, Crump ML 1994. Amphibian declines and climate disturbance: the case of the golden toad and the harlequin frog. Conserv. Biol. 8:72–85
    [Google Scholar]
  6. 6.  Pechmann JHK, Wilbur HM 1994. Putting declining amphibian populations in perspective: natural fluctuations and human impact. Herpetologica 50:65–84
    [Google Scholar]
  7. 7.  Stuart SN, Chanson JS, Cox NA, Young BE, Rodrigues ASL et al. 2004. Status and trends of amphibian declines and extinctions worldwide. Science 306:1783–86
    [Google Scholar]
  8. 8.  Skerratt L, Berger L, Speare R, Cashins S, McDonald K et al. 2007. Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. EcoHealth 4:125–34
    [Google Scholar]
  9. 9.  Scheele BC, Hunter DA, Grogan LF, Berger L, Kolby JE et al. 2014. Interventions for reducing extinction risk in chytridiomycosis‐threatened amphibians. Conserv. Biol. 28:1195–205
    [Google Scholar]
  10. 10.  Blaustein AR, Han BA, Relyea RA, Johnson PTJ, Buck JC et al. 2011. The complexity of amphibian population declines: understanding the role of cofactors in driving amphibian losses. Ann. N.Y. Acad. Sci. 1223:108–19
    [Google Scholar]
  11. 11.  Gascon C, Collins JP, Moore RD, Church DR, McKay JE, Mendelson JR III 2007. Amphibian Conservation Action Plan London: IUCN SSC Amphib. Spec. Group http://www.amphibians.org/wp-content/uploads/2013/07/ACAP.pdf
  12. 12.  Wren S, Angulo A, Meredith H, Kielgast J, Dos Santos M, Bishop P 2015. Amphibian Conservation Action Plan London: IUCN SSC Amphib. Spec. Group http://www.amphibians.org/publications/amphibian-conservation-action-plan/
  13. 13.  Pritchard DJ, Fa JE, Oldfield S, Harrop SR 2012. Bring the captive closer to the wild: redefining the role of ex situ conservation. Oryx 46:18–23
    [Google Scholar]
  14. 14.  Harding G, Griffiths RA, Pavajeau L 2016. Developments in amphibian captive breeding and reintroduction programs. Conserv. Biol. 30:340–49
    [Google Scholar]
  15. 15.  Griffiths RA, Garcia G, Oliver J 2008. Re-introduction of the Mallorcan midwife toad, Mallorca, Spain. Global Re-Introduction Perspectives: Re-Introduction Case-Studies from Around the Globe PS Soorae, pp. 54–57. Gland Switz: IUCN/SSC Re-Introd. Spec. Group
    [Google Scholar]
  16. 16.  Kouba A, Vance C, Willis E 2009. Artificial fertilization for amphibian conservation: current knowledge and future considerations. Theriogenology 71:214–27
    [Google Scholar]
  17. 17.  Byrne PG, Silla AJ 2010. Hormonal induction of gamete release, and in-vitro fertilisation, in the critically endangered Southern Corroboree frog. Pseudophryne corroboree. Reprod. Biol. Endocrinol. 8:144
    [Google Scholar]
  18. 18.  Kouba AJ, Vance CK 2009. Applied reproductive technologies and genetic resource banking for amphibian conservation. Reprod. Fertil. Dev. 21:719–37
    [Google Scholar]
  19. 19.  Silla AJ, McFadden M, Byrne PG 2018. Hormone-induced spawning of the critically endangered northern corroboree frog. Pseudophryne pengilleyi. Reprod. Fertil. Dev. In press
  20. 20.  Kouba A, Willis E, Vance C, Hasenstab S, Reichling S et al. 2011. Development of assisted reproduction technologies for the endangered Mississippi gopher frog (Rana sevosa) and sperm transfer for in vitro fertilization. Reprod. Fertil. Dev. 24:170
    [Google Scholar]
  21. 21.  Mansour N, Lahnsteiner F, Patzner RA 2011. Collection of gametes from live axolotl, Ambystoma mexicanum, and standardization of in vitro fertilization. Theriogenology 75:354–61
    [Google Scholar]
  22. 22.  Dziminski MA, Roberts JD, Simmons LW 2008. Fitness consequences of parental compatibility in the frog Crinia georgiana. . Evolution 62:879–86
    [Google Scholar]
  23. 23.  Sherman CD, Wapstra E, Uller T, Olsson M 2008. Male and female effects on fertilization success and offspring viability in the Peron's tree frog. Litoria peronii. Austral. Ecol. 33:348–52
    [Google Scholar]
  24. 24.  Silla AJ 2013. Artificial fertilisation in a terrestrial toadlet Pseudophryne guentheri: effect of medium osmolality, sperm concentration and gamete storage. Reprod. Fertil. Dev. 25:81134–41
    [Google Scholar]
  25. 25.  Whitaker BR 2001. Reproduction. Amphibian Medicine and Captive Husbandry KM Wright, BR Whitaker 285–99 Malabar, FL: Krieger
    [Google Scholar]
  26. 26.  Gore AC 2002. GnRH: The Master Molecule of Reproduction New York: Springer
  27. 27.  Hogben L 1930. Some remarks on the relation of the pituitary gland to ovulation and skin secretion in Xenopus laevis. Proc. R. Soc. S. Afr 22:17–18
    [Google Scholar]
  28. 28.  Gurdon JB, Hopwood N 2000. The introduction of Xenopus laevis into developmental biology: of empire, pregnancy testing and ribosomal genes. Int. J. Dev. Biol. 44:43–50
    [Google Scholar]
  29. 29.  Bruehl FS 1952. The development of pregnancy tests. Am. J. Nurs. 52:591–92
    [Google Scholar]
  30. 30.  Brown DD 2004. A tribute to the Xenopus laevis oocyte and egg. J. Biol. Chem. 279:45291–99
    [Google Scholar]
  31. 31.  Lensch MW, Mummery CL 2013. From stealing fire to cellular reprogramming: a scientific history leading to the 2012 Nobel Prize. Stem Cell Rep 1:5–17
    [Google Scholar]
  32. 32.  Jacobs LE, Robertson JM, Kaiser K 2016. Variation in male spermiation response to exogenous hormones among divergent populations of red-eyed treefrogs. Reprod. Biol. Endocrinol. 14:83
    [Google Scholar]
  33. 33.  Kouba AJ, delBarco-Trillo J, Vance CK, Milam C, Carr M 2012. A comparison of human chorionic gonadotropin and luteinizing hormone releasing hormone on the induction of spermiation and amplexus in the American toad (Anaxyrus americanus). Reprod. Biol. Endocrinol. 10:59
    [Google Scholar]
  34. 34.  Rowson AD, Obringer AR, Roth TL 2001. Non‐invasive treatments of luteinizing hormone‐releasing hormone for inducing spermiation in American (Bufo americanus) and Gulf Coast (Bufo valliceps) toads. Zoo Biol 20:63–74
    [Google Scholar]
  35. 35.  Browne R, Seratt J, Vance C, Kouba A 2006. Hormonal priming, induction of ovulation and in-vitro fertilization of the endangered Wyoming toad (Bufo baxteri). Reprod. Biol. Endocrinol. 4:34
    [Google Scholar]
  36. 36.  McDonough CE, Martin MW, Vance CK, Cole JA, Kouba AJ 2016. Frequency of exogenous hormone therapy impacts spermiation in male Fowler's toad (Bufo fowleri). Reprod. Fertil. Dev. 28:995–1003
    [Google Scholar]
  37. 37.  Della Togna G, Trudeau VL, Gratwicke B, Evans M, Augustine L et al. 2017. Effects of hormonal stimulation on the concentration and quality of excreted spermatozoa in the critically endangered Panamanian golden frog (Atelopus zeteki). Theriogenology 91:27–35
    [Google Scholar]
  38. 38.  Silla AJ, Roberts JD 2012. Investigating patterns in the spermiation response of eight Australian frogs administered human chorionic gonadotropin (hCG) and luteinizing hormone-releasing hormone (LHRHa). Gen. Comp. Endocrinol. 179:128–36
    [Google Scholar]
  39. 39.  Uteshev V, Kaurova S, Shishova N, Stolyarov S, Browne R, Gakhova E 2015. In vitro fertilization with hormonally induced sperm and eggs from sharp-ribbed newts Pleurodeles waltl. . Russ. J. Herpetol 22:135–40
    [Google Scholar]
  40. 40.  Silla AJ 2011. Effect of priming injections of luteinizing hormone-releasing hormone on spermiation and ovulation in Günther's toadlet. Pseudophryne guentheri. Reprod. Biol. Endocrinol. 9:68
    [Google Scholar]
  41. 41.  Silla AJ 2010. Effects of luteinizing hormone-releasing hormone and arginine-vasotocin on the sperm-release response of Günther's toadlet. Pseudophryne guentheri. Reprod. Biol. Endocrinol. 8:139
    [Google Scholar]
  42. 42.  Calatayud NE, Gardner N, Shier DM 2016. Captive breeding and reintroduction of the mountain yellow-legged frog (Rana muscosa) Annu. Rep., San Diego Zoo, Inst Conserv. Res. Div. Appl. Anim. Ecol Escondido, CA:
    [Google Scholar]
  43. 43.  Browne RK, Li H, Seratt J, Kouba A 2006. Progesterone improves the number and quality of hormone induced Fowler toad (Bufo fowleri) oocytes. Reprod. Biol. Endocrinol. 4:3
    [Google Scholar]
  44. 44.  Calatayud NE, Langhorne CJ, Mullen AC, Williams CL, Smith T et al. 2015. A hormone priming regimen and hibernation affect oviposition in the boreal toad (Anaxyrus boreas boreas). Theriogenology 84:600–7
    [Google Scholar]
  45. 45.  Michael S, Buckley C, Toro E, Estrada A, Vincent S 2004. Induced ovulation and egg deposition in the direct developing anuran Eleutherodactylus coqui. Reprod. Biol. . Endocrinol 2:6
    [Google Scholar]
  46. 46.  Uteshev VK, Shishova NV, Kaurova SA, Browne RK, Gakhova EN 2012. Hormonal induction of spermatozoa from amphibians with Rana temporaria and Bufo bufo as anuran models. Reprod. Fertil. Dev. 24:599–607
    [Google Scholar]
  47. 47.  Clulow J, Clulow S, Guo J, French AJ, Mahony MJ, Archer M 2012. Optimisation of an oviposition protocol employing human chorionic and pregnant mare serum gonadotropins in the Barred Frog Mixophyes fasciolatus (Myobatrachidae). Reprod. Biol. Endocrinol. 10:60
    [Google Scholar]
  48. 48.  Ogawa A, Dake J, Iwashina Y-k, Tokumoto T 2011. Induction of ovulation in Xenopus without hCG injection: the effect of adding steroids into the aquatic environment. Reprod. Biol. Endocrinol. 9:11
    [Google Scholar]
  49. 49.  Calatayud NE, Mullen AK, Langhorne CJ 2017. Induction of reproductive behaviors by exogenous hormones in captive southern Rocky Mountain boreal toads. Anaxyrus boreas boreas bioRxiv 131763. https://doi.org/10.1101/131763
    [Crossref]
  50. 50.  Trudeau VL, Somoza GM, Natale GS, Pauli B, Wignall J et al. 2010. Hormonal induction of spawning in 4 species of frogs by coinjection with a gonadotropin-releasing hormone agonist and a dopamine antagonist. Reprod. Biol. Endocrinol. 8:36
    [Google Scholar]
  51. 51.  Vu M, Weiler B, Trudeau VL 2017. Time- and dose-related effects of a gonadotropin-releasing hormone agonist and dopamine antagonist on reproduction in the Northern leopard frog (Lithobates pipiens). Gen. Comp. Endocrinol. 254:86–96
    [Google Scholar]
  52. 52.  Uteshev V, Shishova N, Kaurova S, Manokhin A, Gakhova E 2013. Collection and cryopreservation of hormonally induced sperm of pool frog (Pelophylax lessonae). Russ. J. Herpetol. 20:105–9
    [Google Scholar]
  53. 53.  Sherman CD, Sagvik J, Olsson M 2010. Female choice for males with greater fertilization success in the Swedish Moor frog. Rana arvalis. PLOS ONE 5:e13634
    [Google Scholar]
  54. 54.  Sherman CD, Uller T, Wapstra E, Olsson M 2008. Within-population variation in ejaculate characteristics in a prolonged breeder, Peron's tree frog. Litoria peronii. Naturwissenshaften 95:1055–61
    [Google Scholar]
  55. 55.  Vu M, Trudeau VL 2016. Neuroendocrine control of spawning in amphibians and its practical applications. Gen. Comp. Endocrinol. 234:28–39
    [Google Scholar]
  56. 56.  Clulow J, Trudeau VL, Kouba AJ 2014. Amphibian declines in the twenty-first century: why we need assisted reproductive technologies. Reproductive Sciences in Animal Conservation WV Holt, JL Brown, P Comizzoli 275–316 New York: Springer-Verlag
    [Google Scholar]
  57. 57.  Zohar Y, Mylonas CC 2001. Endocrine manipulations of spawning in cultured fish: from hormones to genes. Reproductive Biotechnology in Finfish Aquaculture EM Donaldson 99–136 Amsterdam: Elsevier
    [Google Scholar]
  58. 58.  Conn PM 1986. The molecular basis of gonadotropin-releasing hormone action. Endocrine Rev 7:3–10
    [Google Scholar]
  59. 59.  Ferreira do Nascimento N, da Silva RC, Nogueira Valentin F, do Carmo Faria Paes M, De Stéfani MV, Okada Nakaghi LS 2015. Efficacy of buserelin acetate combined with a dopamine antagonist for spawning induction in the bullfrog (Lithobates catesbeianus). Aquacult. Res. 46:3093–96
    [Google Scholar]
  60. 60.  Brown JL, Morales V, Summers K 2010. A key ecological trait drove the evolution of biparental care and monogamy in an amphibian. Am. Nat. 175:436–46
    [Google Scholar]
  61. 61.  Byrne PG, Roberts JD 2012. Evolutionary causes and consequences of sequential polyandry in anuran amphibians. Biol. Rev. 87:209–28
    [Google Scholar]
  62. 62.  Roberts JD, Byrne PG 2011. Polyandry, sperm competition, and the evolution of anuran amphibians. Adv. Study Behav. 43:1–53
    [Google Scholar]
  63. 63.  Parker GA 1998. Sperm competition and the evolution of ejaculates: towards a theory base. Sperm Competition and Sexual Selection TR Birkhead, AP Møller 3–54 London: Academic
    [Google Scholar]
  64. 64.  Byrne P, Roberts J, Simmons L 2002. Sperm competition selects for increased testes mass in Australian frogs. J. Evol. Biol. 15:347–55
    [Google Scholar]
  65. 65.  Emerson SB 1997. Testis size variation in frogs: testing the alternatives. Behav. Ecol. Sociobiol. 41:227–35
    [Google Scholar]
  66. 66.  Jennions MD, Passmore NI 1993. Sperm competition in frogs: testis size and a “sterile male” experiment on Chiromantis xerampelina (Rhacophoridae). Biol. J. Linn. Soc. 50:211–20
    [Google Scholar]
  67. 67.  Kusano T, Toda M, Fukuyama K 1991. Testes size and breeding systems in Japanese annrans with special reference to large testes in the treefrog, Rhacophorus arboreus (Amphibia: Rhacophoridae). Behav. Ecol. Sociobiol. 29:27–31
    [Google Scholar]
  68. 68.  Prado CPA, Haddad CF 2003. Testes size in leptodactylid frogs and occurrence of multimale spawning in the genus Leptodactylus in Brazil. J. Herpetol. 37:354–62
    [Google Scholar]
  69. 69.  Varriale B, Serino I 1994. The androgen receptor mRNA is up-regulated by testosterone in both the Harderian gland and thumb pad of the frog. Rana esculenta. J. Steroid Biochem. Mol. Biol. 51:259–65
    [Google Scholar]
  70. 70.  Browne R, Clulow J, Mahony M 2001. Short-term storage of cane toad (Bufo marinus) gametes. Reproduction 121:167–73
    [Google Scholar]
  71. 71.  Edwards DL, Mahony MJ, Clulow J 2004. Effect of sperm concentration, medium osmolality and oocyte storage on artificial fertilisation success in a myobatrachid frog (Limnodynastes tasmaniensis). Reprod. Fertil. Dev. 16:347–54
    [Google Scholar]
  72. 72.  Silla AJ, Keogh LM, Byrne PG 2015. Antibiotics and oxygen availability affect the short-term storage of spermatozoa from the critically endangered Booroolong frog. Litoria booroolongensis. Reprod. Fertil. Dev. 27:1147–53
    [Google Scholar]
  73. 73.  Kouba AJ, Vance CK, Frommeyer MA, Roth TL 2003. Structural and functional aspects of Bufo americanus spermatozoa: effects of inactivation and reactivation. J. Exp. Zool. B Mol. Dev. Evol. 295:172–82
    [Google Scholar]
  74. 74.  Browne RK, Clulow J, Mahony M 2002. The short-term storage and cryopreservation of spermatozoa from hylid and myobatrachid frogs. CryoLetters 23:129–36
    [Google Scholar]
  75. 75.  Keogh LM, Byrne PG, Silla AJ 2017. The effect of gentamicin on sperm motility and bacterial abundance during chilled sperm storage in the Booroolong frog. Gen. Comp. Endocrinol. 243:51–59
    [Google Scholar]
  76. 76.  Germano JM, Arregui L, Kouba AJ 2013. Effects of aeration and antibiotics on short-term storage of Fowler's toad (Bufo fowleri) sperm. Aquaculture 396–99:20–24
    [Google Scholar]
  77. 77.  Kouba AJ, Lloyd RE, Houck ML, Silla AJ, Calatayud N et al. 2013. Emerging trends for biobanking amphibian genetic resources: the hope, reality and challenges for the next decade. Biol. Conserv. 164:10–21
    [Google Scholar]
  78. 78.  Holt W, Pickard A 1999. Role of reproductive technologies and genetic resource banks in animal conservation. Rev. Reprod. 4:143–50
    [Google Scholar]
  79. 79.  Shishova N, Uteshev V, Kaurova S, Browne R, Gakhova E 2011. Cryopreservation of hormonally induced sperm for the conservation of threatened amphibians with Rana temporaria as a model research species. Theriogenology 75:220–32
    [Google Scholar]
  80. 80.  Mansour N, Lahnsteiner F, Patzner R 2009. Optimization of the cryopreservation of African clawed frog (Xenopus laevis) sperm. Theriogenology 72:1221–28
    [Google Scholar]
  81. 81.  Beesley SG, Costanzo JP, Lee RE Jr 1998. Cryopreservation of spermatozoa from freeze-tolerant and -intolerant anurans. Cryobiology 37:155–62
    [Google Scholar]
  82. 82.  Sargent MG, Mohun TJ 2005. Cryopreservation of sperm of Xenopus laevis and Xenopus tropicalis. . Genesis 41:41–46
    [Google Scholar]
  83. 83.  Mansour N, Lahnsteiner F, Patzner RA 2010. Motility and cryopreservation of spermatozoa of European common frog. Rana temporaria. Theriogenology 74:724–32
    [Google Scholar]
  84. 84.  Michael SF, Jones C 2004. Cryopreservation of spermatozoa of the terrestrial Puerto Rican frog. Eleutherodactylus coqui. Cryobiology 48:90–94
    [Google Scholar]
  85. 85.  Langhorne CJ, Calatayud NE, Kouba AJ, Feugang JM, Vance CK, Willard ST 2013. 026 cryoconservation: successful sperm cryopreservation and developmental outcomes using endangered North American amphibians. Cryobiology 67:405
    [Google Scholar]
  86. 86.  Della Togna G 2015. Structural and functional characterization of the Panamanian golden frog (Atelopus zeteki) spermatozoa–impact of medium osmolality and cryopreservation on motility and cell viability PhD Diss., Cell Biol. Mol. Genet., Univ. Md College Park, MD:
    [Google Scholar]
  87. 87.  Clulow J, Clulow S 2016. Cryopreservation and other assisted reproductive technologies for the conservation of threatened amphibians and reptiles: bringing the ARTs up to speed. Reprod. Fertil. Dev. 28:1116–32
    [Google Scholar]
  88. 88.  Wolf DP, Hedrick JL 1971. A molecular approach to fertilization: 11. Viability and artificial fertilization of Xenopus laevis gametes. Dev. Biol. 25:348–59
    [Google Scholar]
  89. 89.  Dziminski MA, Roberts J, Simmons LW 2010. Sperm morphology, motility and fertilisation capacity in the myobatrachid frog Crinia georgiana. Reprod. Fertil. . Dev 22:516–22
    [Google Scholar]
  90. 90.  Toro E, Michael SF 2004. In vitro fertilization and artificial activation of eggs of the direct-developing anuran Eleutherodactylus coqui. Reprod. Biol. Endocrinol 2:60
    [Google Scholar]
  91. 91.  Waggener WL, Carroll EJ 1998. A method for hormonal induction of sperm release in anurans (eight species) and in vitro fertilization in Lepidobatrachus species. Dev. Growth Diff. 40:119–25
    [Google Scholar]
  92. 92.  Browne RK, Clulow J, Mahony M, Clark A 1998. Successful recovery of motility and fertility of cryo-preserved cane toad (Bufo marinus) sperm. Cryobiology 37:339–45
    [Google Scholar]
  93. 93.  Cabada MO 1975. Sperm concentration and fertilization rate in Bufo arenarum (Amphibia: Anura). J. Exp. Biol. 62:481–86
    [Google Scholar]
  94. 94.  Levitan DR 1998. Sperm limitation, gamete competition, and sexual selection in external fertilizers. Sperm Competition and Sexual Selection TR Birkhead, AP Møller 175–218 London: Academic
    [Google Scholar]
  95. 95.  Soudakevicz T 1874. Report on progress of pisciculture in Russia. US Comm. Fish Fish. 2:493–513
    [Google Scholar]
  96. 96.  Byrne PG, Simmons LW, Roberts JD 2003. Sperm competition and the evolution of gamete morphology in frogs. Proc. R. Soc. Lond. B Biol. Sci. 270:2079–86
    [Google Scholar]
  97. 97.  Wells KD 2007. The Ecology and Behavior of Amphibians Chicago: Univ. Chicago Press
  98. 98.  Birkhead TR, Hosken DJ, Pitnick SS 2008. Sperm Biology: An Evolutionary Perspective Cambridge, MA: Academic
  99. 99.  Browne R, Kaurova S, Uteshev V, Shishova N, McGinnity D et al. 2015. Sperm motility of externally fertilizing fish and amphibians. Theriogenology 83:1–13.e8
    [Google Scholar]
  100. 100.  Silla AJ, Keogh LM, Byrne PG 2017. Sperm motility activation in the critically endangered Booroolong frog: the effect of medium osmolality and phosphodiesterase inhibitors. Reprod. Fertil. Dev. 29:2277–83
    [Google Scholar]
  101. 101.  O'Brien ED, Krapf D, Cabada MO, Visconti PE, Arranz SE 2011. Transmembrane adenylyl cyclase regulates amphibian sperm motility through protein kinase A activation. Dev. Biol. 350:80–88
    [Google Scholar]
  102. 102.  Byrne PG, Dunne C, Munn AJ, Silla AJ 2015. Environmental osmolality influences sperm motility activation in an anuran amphibian. J. Evol. Biol. 28:521–34
    [Google Scholar]
/content/journals/10.1146/annurev-animal-020518-115056
Loading
/content/journals/10.1146/annurev-animal-020518-115056
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error