Artificial fertilization for amphibian conservation: Current knowledge and future considerations

Theriogenology

Volumn 71, Issue 1, 2009, Pages 214-227

  Kouba, A J ^a   Vance, C K ^a,b   Willis, E L ^a  

^a Department of Conservation and Research ^*  (United States)

^b MISSISSIPPI STATE UNIVERSITY   (United States)

Author keywords

Amphibian; Artificial fertilization; Egg; Hormones; Sperm

Indexed keywords

AMPHIBIA; ANIMAL; ARTICLE; ENVIRONMENTAL PROTECTION; FEMALE; FERTILIZATION; MALE; METHODOLOGY; PHYSIOLOGY;

AMPHIBIANS; ANIMALS; CONSERVATION OF NATURAL RESOURCES; FEMALE; FERTILIZATION; MALE;

AMPHIBIA;

EID: 56749173362     PISSN: 0093691X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.theriogenology.2008.09.055     Document Type: Article

References (92)

1. Duellman W.E., and Trueb L. Biology of amphibians (1986), Johns Hopkins University Press Ltd, London, Baltimore, Maryland pp. 13-197
2. Salthe S.N., and Mecham J.S. Reproductive and courtship patterns. In: Lofts B. (Ed). Physiology of the amphibian vol. II (1974), Academic Press, New York 309-521
3. Whitaker B.R. Reproduction. In: Wright K.M., and Whitaker B.R. (Eds). Amphibian medicine and captive husbandry (2001), Krieger Publishing Co., Malabar, FL 285-299
4. Briggs R., and King T.J. Transplantation of living nuclei from blastula cells into enucleated frogs eggs. Proc Natl Acad Sci U S A 38 (1952) 455-463
5. Browne R.K., Seratt J., Vance C.K., and Kouba A.J. Hormonal priming, induction of ovulation and in-vitro fertilization of the endangered Wyoming toad (Bufo baxteri). Reprod Biol Endocrinol 4 (2006) 34
6. Roelants K., Gower D.J., Wilkinson M., Loader S.P., Biju S.D., Guillaume K., et al. Global patterns of diversification in the history of modern amphibians. Proc Natl Acad Sci U S A 104 (2007) 887-892
7. IUCN. 2007 IUCN Red List of Threatened Species. Downloaded on August 1, 2008 (2007). http://www.iucnredlist.org
8. Clark J.A., and May R.M. Taxonomic bias in conservation research. Science 297 (2002) 191-192
9. Stuart S.N., Chanson J.S., Cox N.A., Young B.E., Rodrigues A.S.L., Fischman D.L., et al. Status and trends of amphibian declines and extinctions world-wide. Science 306 (2004) 1783-1786
10. Baille J.E.M., Bennun L.A., Brooks T.M., Butchart S.H.M., Chanson J.S., Cokeliss Z., et al. IUCN red list of threatened species. A global species assessment (2004), IUCN, Gland, Switzerland/Cambridge, UK
11. Williams E.S., Yuill T., Artois M., Fischer J., and Haigh S.A. Emerging infectious diseases in wildlife. Rev Sci Tech 21 (2002) 139-157
12. Pounds A., Carnaval A.C.O.Q., and Corn S. Climate change, biodiversity loss and amphibian declines. In: Gascon C., Collins J.P., Moore R.D., Church D.R., McKay J.E., and Mendelson III J.R. (Eds). Amphibian conservation action plan (2007), IUCN/SSC Amphibian Specialist Group, Gland, Switzerland/Cambridge, UK 64
13. Gascon C, Collins JP, Moore RD, Church DR, McKay JE, Mendelson III JR, editors. Amphibian conservation action plan. IUCN/SSC Amphibian Specialist Group; Gland, Switzerland and Cambridge, UK: 2007. p. 64.
14. Mendelson III JR,Gagliardo R, Andreone F, Buley KR, Coloma L, Garcia G, et al. Captive programs. In:Gascon C, Collins JP, Moore RD, Church DR, McKay JE, Mendelson III JR, editors. Amphibian conservation action plan. IUCN/SSC Amphibian Specialist Group; Gland, Switzerland and Cambridge, UK: 2007. p. 64.
15. Lock B.A. Reproductive surgery in reptiles. Vet Clin North Am Exot Anim Pract 3 (2000) 733-752
16. Menon K.M.J., Munshi U.M., Clouser C.L., and Nair A.K. Regulation of luteinizing hormone/human chorionic gonadotropin receptor expression: a perspective. Biol Reprod 70 (2004) 861-866
17. Kumar T.R. What have we learned about gonadotropin function from gonadotropin subunit and receptor knockout mice?. Reproduction 130 (2005) 293-302
18. Pozzi A.G., Rosemblit C., and Ceballos N.R. Effect of human gonadotropins on spermiation and androgen biosynthesis in the testis of the toad Bufo arenarum (Amphibia, Anura). J Exp Zool A Comp Exp Biol 305 (2006) 96-102
19. Licht P. Induction of spermiation in anurans by mammalian pituitary gonadotropins and their subunits. Gen Comp Endocrinol 20 (1973) 522-529
20. Redshaw M.R. The hormonal control of the amphibian ovary. Am Zool 12 (1972) 289-306
21. Jorgensen C.B. Growth and reproduction. In: Feder M.E., and Burggren W.W. (Eds). Environmental physiology of the amphibians (1992), University of Chicago Press, Chicago and London 439-466
22. Arimura A., Vilchez-Martinez J.A., Coy D.H., Hirotsu Y., and Schally A.V. d-Ala6, Des-Gly-NH210]-LH-RH-ethylamide: a new analogue with unusually high LH-RH/FSH-RH activity. Endocrinology 95 (1974) 1174-1177
23. Michael S.F., Buckley C., Toro E., Estrada A.R., and Vincent S. Induced ovulation and egg deposition in the direct developing anuran Eleutherodactylus coqui. Reprod Biol Endocrinol 2 (2004) 6
24. Waggener W.L., and Carroll Jr. E.J. A method for hormonal induction of sperm release in anurans (eight species) and in vitro fertilization in Lepidobatrachus species. Dev Growth Differ 40 (1998) 19-25
25. Obringer A.R., O'Brien J.K., Saunders R.L., Yamamoto K., Kikuyama S., and Roth T.L. Characterization of the spermiation response, luteinizing hormone release and sperm quality in the American toad (Bufo americanus) and the endangered Wyoming toad (Bufo baxteri). Reprod Fertil Dev 2 (2000) 51-58
26. Roth T.L., and Obringer A.R. Reproductive research and the worldwide amphibian extinction crisis. In: Holt W.V., Pickard A.R., Rodger J.C., and Wildt D.E. (Eds). Reproductive science and integrated conservation (2003), Cambridge University Press, Cambridge, UK 359-374
27. Kouba A.J., Vance C.K., Frommeyer M.A., and Roth T.L. Structural and functional aspects of Bufo americanus spermatozoa: effects of inactivation and reactivation. J Exp Zool 295A (2003) 72-182
28. Wolf D.P., and Hedrick J.L. A molecular approach to fertilization. II. Viability and artificial fertilization of Xenopus laevis gametes. Dev Biol 25 (1971) 348-359
29. Browne R.K., Li H., Seratt J., and Kouba A.J. Progesterone improves the number and quality of hormone induced Fowler toad (Bufo fowleri) oocytes. Reprod Biol Endocrinol 4 (2006) 3
30. Subcommittee on amphibian standards. Committee on standards, National Research Council (Eds.). Amphibians: guidelines for the breeding, care, and management of laboratory animals. Washington, DC: National Academy Press Inc.; 1996. 153 pp. (books.nap.edu/html/amphibian).
31. Johnson C.J., Vance C.K., Roth T.L., and Kouba A.J. Oviposition and ultrasound monitoring of American toads (Bufo americanus) treated with exogenous hormones. Proceedings of the American association of zoo veterinarians meeting (2002) 299-301
32. Rugh R. Experimental embryology: techniques and procedures. 3rd ed. (1965), Burgess Publishing Co., Minneapolis p. 501
33. Kutzler M.A. Estrus induction and synchronization in canids and felids. Theriogenology 68 (2007) 354-374
34. Thatcher W.W., and Santos J.E. Control of ovarian follicular and corpus luteum development for the synchronization of ovulation in cattle. Soc Reprod Fertil Suppl 64 (2007) 69-81
35. Galli-Mainini. Pregnancy test using the male toad. J Clin Endocrinol Metab 7 (1947) 653-658
36. McKinnell R.G., Picciano D.J., and Kriegg R.E. Fertilization and development of frog eggs after repeated spermiation induced by human chorionic gonadotropin. Lab Anim Sci 26 (1976) 932-935
37. Easley K.A., Culley Jr. D.D., Horseman N.D., and Penkala J.E. Environmental influences on hormonally induced spermiation of the bullfrog, Rana catesbeiana. J Exp Zool 207 (1979) 407-416
38. Clulow J., Mahony M., Browne R.K., Pomering M., and Clark A. Applications of assisted reproductive technologies (ART) to endangered amphibian species. In: Campbell A. (Ed). Declines and disappearance of Australian frogs (1999), Environment Australia, Canberra 219-225
39. Limori E., D'Occhio M.J., Lisle A.T., and Johnston S.D. Testosterone secretion and pharmacological spermatozoa recovery in the cane toad. Anim Reprod Sci 90 (2005) 163-173
40. Lipke C, Meinecke-Tillmann S, Meyer W, Meinecke B. Preparation and ultra structure of spermatozoa from Green Poison Frogs, Dendrobates auratus, following hormonal induced spermiation (Amphibia, Anura, Dendrobatidae), Anim Reprod Sci; in press. Available on line June 20, 2008.
41. Norris III D.O. Tropic hormones of the adenohypophysis. In: Norris D.O. (Ed). Vertebrate endocrinology. 3rd ed. (1997), Academic Press, San Diego, CA 125-140
42. Goncharov B.F., Shubravy O.I., Serbinova I.A., and Uteshev V.K. The USSR programme for breeding amphibians, including rare and endangered species. Int Zoo Yb 28 (1989) 10-21
43. Rowson A.D., Obringer A.R., and Roth T.L. Non-invasive treatments of lutienizing hormone-releasing hormone for inducing spermiation in American (Bufo americanus) and Gulf coast (Bufo valliceps) toads. Zoo Biol 20 (2001) 63-74
44. Browne R.K., Clulow J., and Mahony M. Short-term storage of cane toad (Bufo marinus) gametes. Reproduction 121 (2001) 167-173
45. Hollinger T.G., and Corton G.L. Artificial fertilization of gametes from the South African clawed frog, Xenopus laevis. Gamete Res 3 (1980) 45-57
46. Browne R.K., Clulow J., and Mahony M. The short-term storage and cryopreservation of spermatozoa from hylid and myobatrachid frogs. Cryo Lett 23 (2002) 129-136
47. Browne R.K., Davis J., Pomering M., and Clulow J. Storage of cane toad (Bufo marinus) sperm for 6 days at 0 °C with subsequent cryopreservation. Reprod Fertil Dev 14 (2002) 267-273
48. Browne R.K., Clulow J., Mahony M., and Clark A. Successful recovery of motility and fertility of cryopreserved cane toad (Bufo marinus) sperm. Cryobiology 37 (1998) 339-345
49. Beesley S.G., Costanzo J.P., and Lee R.E. Cryopreservation of spermatozoa from freeze-tolerant and intolerant anurans. Cryobiology 37 (1998) 155-162
50. Costanzo J.P., Mugnano J.A., and Wehrheim H.M. Osmotic and freezing tolerance in spermatozoa of freeze-tolerant and -intolerant frogs. Am J Physiol 37 (1998) 713-719
51. Michael S.F., and Jones C. Cryopreservation of spermatozoa of the terrestrial Puerto Rican frog, Eleutherodactylus coqui. Cryobiology 48 (2004) 90-94
52. Sargent M.G., and Mohun T.J. Cryopreservation of sperm of Xenopus laevis and Xenopus tropicalis. Genesis 41 (2005) 41-46
53. Watanabe T., Itoh T., Watanabe A., and Onitake K. Characteristics of sperm motility induced on the egg-jelly in the internal fertilization of the Newt, Cynops pyrrhogaster. Zool Sci 20 (2003) 345-352
54. Sasaki T., Kamimura S., Takai H., Watanabe A., and Onitake K. The activity for the induction of the sperm acrosome reaction localizes in the outer layers and exists in the high-molecular-weight components of the egg-jelly of the newt, Cynops pyrrhogaster. Zygote 10 (2002) 1-9
55. Drevius L.D., and Eriksson H. Osmotic swelling of mammalian spermatozoa. Exp Cell Res 42 (1966) 136-156
56. Inoda T., and Morisawa M. Effect of osmolality on the initiation of sperm motility in Xenopus laevis. Comp Biochem Physiol 88A (1987) 539-542
57. Bernardini G., Andrietti F., Camatini M., and Cosson M.P. Xenopus spermatozoon: correlation between shape and motility. Gamete Res 20 (1988) 165-175
58. Bernardini G., Camatini M., and Cosson M.P. Motility of spermatozoa of Xenopus laevis. Eur J Cell Biol 44 (1987) 24
59. Kouba A.J., Maas A.K., Frommeyer M.A., and Roth T.L. Effects of BSA and energy substrates on toad (Bufo americanus) sperm motility. Theriogenology 55 (2001) 402
60. Twigg J., Fulton N., Gomez E., Irvine D.S., and Aitken R.J. Analysis of the impact of intracellular reactive oxygen species generation on the structural and functional integrity of human spermatozoa: lipid peroxidation, DNA fragmentation, and effectiveness of antioxidants. Hum Reprod 13 (1998) 1429-1436
61. Edwards D.L., Mahony M.J., and Clulow J. Effect of sperm concentration, medium osmolality and oocyte storage on artificial fertilization success in a myobatrachid frog (Limnodynastes tasmaniensis). Reprod Fertil Dev 16 (2004) 347-354
62. Fitzsimmons C., McLaughlin E.A., Mahony M.J., and Clulow J. Optimisation of handling, activation and assessment procedures for Bufo marinus spermatozoa. Reprod Fertil Dev 19 (2007) 594-601
63. Carroll E.J., Wei S.H., and Nagel G.M. Purification, physiochemical characterization and immuno-histochemical localization of a major 11.7 S glycoprotein from the jelly coats of the anuran Lepidobatrachus laevis. Arch Biochem Biophys 284 (1991) 346-351
64. McLaughlin E.W., and Humphries A.A. The jelly envelopes and fertilization of eggs in the Newt, Notophthalmus viridescens. J Morphol 158 (1978) 73-90
65. Katagiri C.H. The participation of toad egg jelly in fertilization. Embryologia 9 (1966) 159-169
66. Elinson R.P. Fertilization of partially jellied and jelly-less oocytes of the frog Rana pipiens. J Exp Zool 176 (1971) 415-428
67. Stewart-Savage J., and Grey R.D. Fertilization of investment-free Xenopus eggs. Exp Cell Res 154 (1984) 639-642
68. Tian J.D., Gong H., Thomsen G.H., and Lennarz W.J. Gamete interactions in Xenopus laevis: identification of sperm binding glycoproteins in the egg vitelline envelope. Cell Biol 136 (1997) 1099-1108
69. Katagiri C.H. The role of oviductal secretions in mediating gamete fusion in the toad, Bufo bufo japonicas. Adv Exp Med Biol 207 (1986) 151-166
70. Ueda Y., Yoshizaki N., and Iwao Y. Acrosome reaction in sperm of the frog, Xenopus laevis: its detection and induction by oviductal pars recta secretion. Dev Biol 243 (2002) 55-64
71. Hedrick J.L., and Nishihara T. Structure and function of the extracellular matrix of anuran eggs. J Electron Microsc Tech 17 (1991) 319-335
72. Vo L.H., and Hedrick J.L. Independent and hetero-oligomeric-dependent sperm binding to egg envelope glycoprotein ZPC in Xenopus laevis. Biol Reprod 62 (2000) 766-774
73. Grey R.D., Working P.K., and Hedrick J.L. Alteration of structure and penetrability of the vitelline envelope after passage of eggs from coelom to oviduct in Xenopus laevis. J Exp Zool 201 (1977) 73-83
74. Katagiri C., Yoshizaki Y., Kotani M., and Kubo H. Analysis of oviductal pars recta-induced fertilizability of coelomic eggs in Xenopus laevis. Dev Biol 210 (1999) 269-276
75. Kubo H., Kawano T., Tsubuki S., Kawashina S., Katagiri C., and Suzuki A. A major glycoprotein of Xenopus egg vitelline envelope, gp41, is a frog homolog of mammalian ZP3. Dev Growth Differ 39 (1997) 405-417
76. Lindsay L.L., Wieduwilt M.J., and Hedrick J.L. Oviductin, the Xenopus laevis oviductal protease that process egg envelope glycoprotein gp43, increase sperm binding to envelopes, and is translated as part of an unusual mosaic protein composed of two protease and several CUB domains. Biol Reprod 60 (1999) 989-995
77. Tian J., Gong H., Thomsen G.H., and Lennarz W.J. Xenopus laevis sperm-egg adhesion is regulated by modifications in the sperm receptor and the egg vitelline envelope. Dev Biol 187 (1997) 143-153
78. Krapf D., Visconti P.E., Arranz S.E., and Cabada M.O. Egg water from the amphibian Bufo arenarum induces capacitation-like changes in homologous spermatozoa. Dev Biol 306 (2007) 516-524
79. Olsen J.H., and Chandler D.E. Xenopus laevis egg jelly contains small proteins that are essential to fertilization. Dev Biol 210 (1999) 401-410
80. Al-Anzi B., and Chandler D.E. A sperm chemoattractant is released form Xenopus egg jelly during spawning. Dev Biol 198 (1998) 366-375
81. Xiang X., Burnett L., Rawls A., Bieber A., and Chandler D. The sperm chemoattractant "allurin" is expressed from the Xenopus oviduct in a hormone-regulated manner. Dev Biol 275 (2004) 343-355
82. Fonovich deSchroeder T.M., Guana L., and Pechen de D'Angelo A.M. Is buffering capacity the principal role of the jelly coat in Bufo arenarum fertilization?. Comp Biochem Physiol 105A (1993) 533-537
83. Reinhart D., Ridgway J., and Chandler D.E. Xenopus laevis fertilisations: analysis of sperm motility in egg jelly using video light microscopy. Zygote 6 (1998) 173-182
84. Ishihara K., Hosono J., Kanatani H., and Katagiri C.H. Toad egg-jelly as a source of divalent cations essential for fertilization. Dev Biol 105 (1984) 435-442
85. Shimoda Y., Kitajima K., Inoue S., and Inoue Y. Isolation, structural determination, and calcium-binding properties of the major glycoprotein present in Bufo japonicus japonicus egg jelly. Eur J Biochem 223 (1994) 223-231
86. Krapf D., Vidal M., Arranz S.E., and Cabada M.O. Characterization and biological properties of L-HGP, a glycoprotein from the amphibian oviduct with acrosome-stabilizing effects. Biol Cell 98 (2006) 403-413
87. Campanella C., Carotenuto R., Infante V., Maturi G., and Atripaldi U. Sperm-egg interaction in the painted frog (Discoglossus pictus): an ultrastructural study. Mol Reprod Dev 47 (1997) 323-333
88. Nakai S., Watanabe A., and Onitaki K. Sperm surface heparin/heparin sulfate is responsible for sperm binding to the uterine envelope in the newt Cynops pyrrhogaster. Dev Growth Differ 41 (1999) 101-107
89. Arranz S.E., and Cabada M.O. Diffusible highly glycosylated protein from Bufo arenarum egg-jelly coat: biological activity. Mol Reprod Dev 56 (2000) 392-400
90. Cabada M.O. Sperm concentration and fertilization rate in bufo arenarum (amphibian:). J Exp Biol 62 (1975) 481-486
91. Toro E., and Michael S.F. In vitro fertilization and artificial activation of eggs of the direct-developing anuran Eleutherodactylus coqui. Reprod Biol Endocrinol 2 (2004) 60
92. Osikowski A. Sperm transport after insemination in the alpine newt (Friturus alpestris, Caudata, Salamandridae). Folia Biol 55 (2007) 101-114