Development and evaluation of electroejaculation techniques in the Tasmanian devil (Sarcophilus harrisii)

Article

<< Previous

Contents Vol 24(7)

doi:10.1071/RD12022

Vertebrate Reproductive Science & Technology

	Search




	Advanced Search



	Journal Home

	About the Journal

	Editorial Board

	Contacts



	Content

	Online Early

	Current Issue

	Just Accepted

	All Issues

	Special Issues

	Research Fronts

	Sample Issue



	For Authors

	General Information

	Instructions to Authors

	Submit Article

	Open Access



	For Referees

	Referee Guidelines

	Review Article



	For Subscribers

	Subscription Prices

	Customer Service

	Print Publication Dates

e-Alerts

Subscribe to our email Early Alert or

feeds for the latest journal papers.

Connect with us

Affiliated Societies

RFD is the official journal of the International Embryo Transfer Society and the Society for Reproductive Biology.

Development and evaluation of electroejaculation techniques in the Tasmanian devil (Sarcophilus harrisii)

T. Keeley ^A ^B ^F, M. Harris ^C, P. D. McGreevy ^A, D. Hudson ^C ^D and J. K. O’Brien ^A ^E

^A Faculty of Veterinary Science, Gunn Building (B19), University of Sydney, NSW 2006, Australia.
^B Taronga Conservation Society Australia, Taronga Western Plains Zoo, Obley Road, Dubbo, NSW 2830, Australia.
^C School of Environmental and Life Sciences, Chemistry Building (C218), University of Newcastle, Callaghan, NSW 2308, Australia.
^D Noah’s Ark Veterinary Services, Medowie Shopping Village Ferodale Rd, Medowie, NSW 2318, Australia.
^E SeaWorld and Busch Gardens Reproductive Research Center, 2595 Ingraham Street, San Diego, CA 92109, USA.
^F Corresponding author. Email: zooreproduction@yahoo.com

Reproduction, Fertility and Development 24(7) 1008-1018 http://dx.doi.org/10.1071/RD12022
Submitted: 14 December 2010 Accepted: 30 January 2012 Published: 29 August 2012





	PDF (793 KB) $25



	Export Citation

Print

Abstract

Electroejaculation (EEJ) has been used successfully to collect samples suitable for genome resource banking from a variety of endangered wildlife species. Ejaculates can also be used to evaluate the reproductive potential of individuals and provide information on seminal characteristics to aid in the development of sperm cryopreservation techniques. Electroejaculation techniques used for marsupial and eutherian species were tested on Tasmanian devils (n = 35). Spermic ejaculates were collected in 54% (19/35) of EEJ attempts. Spermic ejaculates were low in volume (3.9 ± 6.5 × 10² µL, range 10–3000 µL) and contained low numbers of spermatozoa (3.3 ± 7.8 × 10³ spermatozoa per ejaculate, range 6–33 000). The osmolality and pH of presumptive urine-free ejaculates were 389 ± 130 mOsm kg^–1 (range 102–566) and 7.0 ± 0.9 (range 6.0–8.0), respectively. Prostatic bodies were observed in 79% (26/33) of ejaculates. Episodic fluctuations in serum testosterone concentrations were not detected during the EEJ procedure (P > 0.05). Increases observed in serum cortisol concentrations during EEJ were less (P < 0.05) than those observed after an adrenalcorticotropic hormone challenge and diurnal variation suggested that cortisol concentrations are greater during the day than at night (P < 0.05). This information can be used to provide range values for the future examination of basic endocrine responses and the adrenal–pituitary axis of this species. This study also demonstrated that spermatozoa-rich devil electroejaculates are more difficult to obtain and poorer in quality than those of other marsupials.

Additional keywords: dasyurid, marsupial, semen collection, spermatozoa.

References

Ball, L. (1976). Electroejaculation. In ‘Applied Electronics for Veterinary Medicine and Animal Physiology’. (Ed. W. R. Klemm) pp. 394–440. (Charles C. Thomas: Springfield, USA.)

Bedford, J. M., Rodger, J. C., and Breed, W. G. (1984). Why so many mammalian spermatozoa – a clue from marsupials? Proc. R. Soc. Lond. B Biol. Sci. 221, 221–233.
| CrossRef | CAS | PubMed |

Bolliger, A. (1942). Spermatorrhoea in marsupials, with special reference to the action of sex hormones on spermatogenesis of Trichosurus vulpecula. J. R. Soc. NSW 76, 86–92.

Bradley, A. J. (1990). Failure of glucocorticoid feedback during breeding in the male red-tailed phascogale, Phascogale calura (Marsupialia: Dasyuridae). J. Steroid Biochem. Mol. Biol. 37, 155–163.
| CrossRef | CAS | PubMed |

Carter, K. K., Chakraborty, P. K., Bush, M., and Wildt, D. E. (1984). Effects of electroejaculation and ketamine-HCl on serum cortisol, progesterone and testosterone in the male cat. J. Androl. 5, 431–437.
| CAS | PubMed |

Cummins, J. M. (1980). Decondensation of sperm nuclei of Australian marsupials: effects of air drying and of calcium and magnesium. Gamete Res. 3, 351–367.
| CrossRef | CAS |

Gilmore, D. P. (1969). Seasonal reproductive periodicity in the male Australian brush-tailed possum (Trichosurus vulpecula). J. Zool. 157, 75–98.
| CrossRef |

Guiler, E. R. (1970). Observations on the Tasmanian devil, Sarcophilus harrisii (Marsupialia: Dasyuridae) II. Reproduction, breeding and growth of pouch young. Aust. J. Zool. 18, 63–70.
| CrossRef |

Hamede, R., McCallum, H., and Jones, M. (2008). Seasonal, demographic and density-related patterns of contact between Tasmanian devils (Sarcophilus harrisii): implications for transmission of devil facial tumour disease. Austral Ecol. 33, 614–622.
| CrossRef |

Hesterman, H. (2008). Reproductive physiology of the Tasmanian devil (Sarcophilus harrisii) and spotted-tailed quoll (Dasyurus maculatus). Ph.D. Thesis, University of Tasmania, Hobart.

Hesterman, H., and Jones, S. M. (2009). Longitudinal monitoring of plasma and faecal androgens in the Tasmanian devil (Sarcophilus harrisii) and the spotted-tailed quoll (Dasyurus maculatus). Anim. Reprod. Sci. 112, 334–346.
| CrossRef | CAS | PubMed |

Hesterman, H., Jones, S. M., and Schwarzenberger, F. (2008). Reproductive endocrinology of the largest dasyurids: characterization of ovarian cycles by plasma and faecal steroid monitoring. Part I. The Tasmanian devil (Sarcophilus harrisii). Gen. Comp. Endocrinol. 155, 234–244.
| CrossRef | CAS | PubMed |

Holt, W., and Pickard, A. R. (1999). Role of reproductive technologies and genetic resource banks in animal conservation. Rev. Reprod. 4, 143–150.
| CrossRef | CAS | PubMed |

Holt, W., Bennett, P. M., and Volobouev, V. (1996). Genetic resource banks in wildlife conservation. J. Zool. 238, 531–544.
| CrossRef |

Hughes, R. L. (1965). Comparative morphology of spermatozoa from five marsupial families. Aust. J. Zool. 13, 533–543.
| CrossRef |

Hughes, R. L. (1976). Reproduction in the male marsupial devil Sarcophilus harrisii with particular reference to the ultrastructure of epididymal spermatozoa. In ‘VIIIth International Congress on Animal Reproduction and Artificial Insemination. Vol. 4’. pp. 908–910. (Wrocławska Drukarnia Naukowa: Krakow, Poland.)

Hughes, R. L. (1982). Reproduction in the Tasmanian devil Sarcophilus harrisii (Dasyuridae, Marsupialia). In ‘Carnivorous Marsupials’. (Ed. M. Archer) pp. 49–63. (Surrey Beatty and Sons: Sydney.)

IUCN (2008). IUCN Red List of Threatened Species. (IUCN Species Survival Commission: Gland, Switzerland.)

Johnston, S. D., McGowan, M. R., Carrick, F. N., Cameron, R. D. A., and Tribe, A. (1994). Seminal characteristics and spermatozoal morphology of captive Queensland koalas (Phascolarctos cinereus adustus). Theriogenology 42, 501–511.
| CrossRef | CAS | PubMed |

Johnston, S. D., Blyde, D., Gamble, J., Higgins, D., Field, H., and Cooper, J. (1997). Collection and short-term preservation of semen from free-ranging eastern grey kangaroos (Macropus giganteus: Macropodidae). Aust. Vet. J. 75, 648–651.
| CrossRef | CAS | PubMed |

Johnston, S. D., O’Callaghan, P. O., McGowan, M. R., and Phillips, N. J. (1997). Characteristics of koala (Phascolarctos cinereus adustus) semen collected by artificial vagina. J. Reprod. Fertil. 109, 319–323.
| CrossRef | CAS | PubMed |

Johnston, S. D., McGowan, M. R., Phillips, N. J., and O’Callaghan, P. O. (2000). Optimal physicochemical conditions for the manipulation and short-term preservation of koala (Phascolarctos cinerus) spermatozoa. J. Reprod. Fertil. 118, 273–281.
| CAS | PubMed |

Johnston, S. M., Blyde, C., Mc, D., Clean, R., Lisle, A., and Holt, W. (2006). An investigation into the similarities and differences governing the cryopreservation success of koala (Phascolarctos cinereus: goldfuss) and common wombat (Vombatus ursinus: shaw) spermatozoa. Cryobiology 53, 218–228.
| CrossRef | CAS |

Jones, S. M., Lockhart, T. J., and Rose, R. (2005). Adaptation of wild-caught Tasmanian devils (Sarcophilus harrisii) to captivity: evidence from physical parameters and plasma cortisol concentrations. Aust. J. Zool. 53, 339–344.
| CrossRef | CAS |

Keeley, T., McGreevy, P. M., and O’Brien, J. K. (2011). Characterization and short-term storage of Tasmanian devil spermatozoa collected post-mortem. Theriogenology 76, 705–714.
| CrossRef | CAS | PubMed |

Keeley, T., McGreevy, P. M., and O’Brien, J. K. (2012). The effects of season and devil facial tumour disease on the reproductive physiology of the male Tasmanian devil (Sarcophilus harrisii). Reprod. Fertil. Dev. 24, 999–1007.
| CrossRef | PubMed |

Kempenaers, B., Peters, A., and Foerster, K. (2008). Sources of individual variation in plasma testosterone levels. Philos. Trans. R. Soc. Lond. B Biol. Sci. 363, 1711–1723.
| CrossRef | CAS | PubMed |

Kravets, F. G., Lee, J., Singh, B., Trocchia, A., Pentyala, S. N., and Khan, S. A. (2000). Prostasomes: current concepts. Prostate 43, 169–174.
| CrossRef | CAS | PubMed |

Lachish, S., Jones, M., and McCallum, H. (2007). The impact of the disease on the survival and population growth rate of the Tasmanian devil. J. Anim. Ecol. 76, 926–936.
| CrossRef | PubMed |

Lachish, S., McCallum, H., and Jones, M. (2009). Demography, disease and the devil: life-history changes in a disease-affected population of Tasmanian devils (Sarcophilus harrisii). J. Anim. Ecol. 78, 427–436.
| CrossRef | PubMed |

Lachish, S., McCallum, H., Mann, D., Pukk, C., and Jones, M. (2010). Evaluating selective culling of infected individuals to control Tasmanian devil facial tumour disease. Conserv. Biol. 24, 841–851.
| CrossRef | PubMed |

Lee, A. K., Bradley, A. J., and Braithwaite, R. W. (1977). Corticosteroid levels and male mortality in Antechinus stuartii. In ‘The Biology of Marsupials’. (Eds B. Stonehouse and D. Gilmore.) pp. 209–220. (The MacMillan Press Ltd.: London.)

Loh, R., Hayes, D., Mahjoor, A., O’Hara, A., Pyecroft, S., and Raidal, S. (2006). The immunohistochemical characterization of devil facial tumour disease (DFTD) in the Tasmanian devil (Sarcophilus harrisii). Vet. Pathol. 43, 896–903.
| CrossRef | CAS | PubMed |

MacCallum, C. (2004). The reproductive biology of the male and female common wombat, Vombatus ursinus: studies towards the development of an artificial insemination protocol. M.Sc. Thesis, University of Queensland, Brisbane.

McDonald, I. R., Lee, A. R., Bradley, A. J., and Than, K. A. (1981). Endocrine changes in dasyurid marsupials with differing mortality patterns. Gen. Comp. Endocrinol. 44, 292–301.
| CrossRef | CAS | PubMed |

Molinia, F. C., and Rodger, J. C. (1996). Pellet-freezing spermatozoa of two marsupials: the tammar wallaby, Macropus eugenii, and the brushtail possum, Trichosurus vulpecula. Reprod. Fertil. Dev. 8, 681–684.
| CrossRef | CAS | PubMed |

Ortiz-de-Montellano, M., Galindo-Maldonado, F., Cavazos-Arizpe, E. O., Aguayo-Arceo, A. M., Torres-Acosta, J. F. J., and Orihuela, A. (2007). Effect of electro-ejaculation on the serum cortisol response of Criollo goats (Capra hircus). Small Rumin. Res. 69, 228–231.
| CrossRef |

Paris, D. B., Taggart, D. A., Shaw, G., Temple-Smith, P. D., and Renfree, M. B. (2005). Birth of pouch young after artificial insemination in the tammar wallaby (Macropus eugenii). Biol. Reprod. 72, 451–459.
| CrossRef | CAS | PubMed |

Pemberton, D. (1990). Social organization and behaviour of the Tasmanian devil, Sarcophilus harrisii. Ph.D. Thesis, University of Tasmania, Hobart.

Pemberton, D., and Renouf, D. (1993). A field study of communication and social behaviour of the Tasmanian devil at feeding sites. Aust. J. Zool. 41, 507–526.
| CrossRef |

Pollock, K., Booth, R., Wilson, R., Keeley, T., Grogan, K., Kennerley, P., and Johnston, S. D. (2010). Oestrus in the Julia Creek dunnart (Sminthopsis douglasi) is associated with wheel-running behaviour but not necessarily changes in body weight, food consumption or pouch morphology. Anim. Reprod. Sci. 117, 135–146.
| CrossRef | CAS | PubMed |

Rodger, J. C. (1976). Comparative aspects of the accessory sex glands and seminal biochemistry of mammals. Comp. Biochem. Physiol. 55B, 1–8.

Rodger, J. C., and Hughes, R. L. (1973). Studies of the accessory glands of male marsupials. Aust. J. Zool. 21, 303–320.
| CrossRef |

Rodger, J. C., and Pollitt, C. C. (1981). Radiographic examination of electroejaculation in marsupials. Biol. Reprod. 24, 1125–1134.
| CAS | PubMed |

Rodger, J. C., and White, I. G. (1975). Electroejaculation of Australian marsupials and analyses of the sugars in the seminal plasma from three macropod species. J. Reprod. Fertil. 43, 233–239.
| CrossRef | CAS | PubMed |

Rodger, J. C., and White, I. G. (1978). The collection, handling and some properties of marsupial semen. Symposium of the Zoological Society of London 43, 289–301.

Rodger, J. C., Cousins, S. J., and Mate, K. E. (1991). A simple glycerol-based freezing protocol for the semen of a marsupial Trichosurus vulpecula, the common brushtail possum. Reprod. Fertil. Dev. 3, 119–125.
| CrossRef | CAS | PubMed |

Rodger, J. C., Paris, D. B. B. P., Czarny, N. A., Harris, M. S., Molinia, F. C., Taggart, D. A., Allen, C. D., and Johnston, S. D. (2009). Artificial insemination in marsupials. Theriogenology 71, 176–189.
| CrossRef | PubMed |

Setiadi, D., Lin, M., and Rodger, J. C. (1997). Post-testicular development of spermatozoa of the tammar wallaby (Macropus eugenii). J. Anat. 190, 275–288.
| CrossRef | PubMed |

Sistina, Y., Lin, M., Mate, K. E., Robinson, E. S., and Rodger, J. C. (1993). The unique stability of the marsupial sperm acrosomal membranes examined by unprotected freeze–thawing and treatment with the detergent Triton X-100. Reprod. Fertil. Dev. 5, 1–14.
| CrossRef | CAS | PubMed |

Sistina, Y., Lin, M., Mate, K. E., and Rodger, J. C. (1993). Induction of the marsupial sperm acrosome reaction in vitro by treatment with diacylglycerols. J. Reprod. Fertil. 99, 335–341.
| CrossRef | CAS | PubMed |

Stafford, K. J., Spoorenberg, J., West, D. M., Vermunt, J. J., Petrie, N., and Lawoko, C. R. O. (1996). The effect of electro-ejaculation on aversive behaviour and plasma cortisol concentration in rams. N. Z. Vet. J. 44, 95–98.
| CrossRef | CAS | PubMed |

Taggart, D. A. (1994). A comparison of sperm and embryo transport in the female reproductive tract of marsupial and eutherian mammals. Reprod. Fertil. Dev. 6, 451–472.
| CrossRef | CAS | PubMed |

Taggart, D. A., and Temple-Smith, P. (1990). Effects of breeding season and mating on total number and distribution of spermatozoa in the epididymis of the brown marsupial mouse, Antechinus stuartii. J. Reprod. Fertil. 88, 81–91.
| CrossRef | CAS | PubMed |

Taggart, D. A., Leigh, C. M., Schultz, D., and Breed, W. G. (1995). Ultrastructure and motility of spermatozoa in macropodid and potoroidid marsupials. Reprod. Fertil. Dev. 7, 1129–1140.
| CrossRef | CAS | PubMed |

Taggart, D. A., Shimmin, G. A., Ratcliff, J. R., Steele, V. R., Dibben, R., Dibben, J., White, C., and Temple-Smith, P. D. (2005). Seasonal changes in the testis, accessory glands and ejaculate characteristics of the southern hairy-nosed wombat, Lasiorhinus latifrons (Marsupialia: Vombatidae). J. Zool. 266, 95–104.
| CrossRef |

Todhunter, R., and Gemmell, R. T. (1987). Seasonal changes in the reproductive tract of the male marsupial bandicoot, Isoodon macrourus. J. Anat. 154, 173–186.
| CAS | PubMed |

Tyndale-Biscoe, C. H., and Renfree, M. B. (1987). ‘Reproductive Physiology of Marsupials’. 476 pp. (Cambridge University Press: Cambridge.)

Walker, S. L., Waddell, W. T., and Goodrowe, K. L. (2002). Reproductive endocrine patterns in captive female and male red wolves (Canis rufus) assessed by faecal and serum hormone analysis. Zoo Biol. 21, 321–335.
| CrossRef |

Wildt, D. E., Meltzer, D., Chakraborty, P. K., and Bush, M. (1984). Adrenal–testicular–pituitary relationship in the cheetah subjected to anaesthesia/electroejaculation. Biol. Reprod. 30, 665–672.
| CrossRef | CAS | PubMed |

Wildt, D. E., Bush, M., O’Brien, S. J., Murray, N. D., Taylor, A., and Marshall Graves, J. A. (1991). Semen characteristics in free-living koalas (Phascolarctos cinereus). J. Reprod. Fertil. 92, 99–107.
| CrossRef | CAS | PubMed |

Wingfield, J. C., and Kitaysky, A. S. (2002). Endocrine responses to unpredictable environmental events: stress or anti-stress hormones? Integr. Comp. Biol. 42, 600–609.
| CrossRef | CAS | PubMed |

Young, K. M., Walker, S. L., Lanthier, C., Waddell, W. T., Monfort, S. L., and Brown, J. L. (2004). Noninvasive monitoring of adrenocortical activity in carnivores by faecal glucocorticoid analyses. Gen. Comp. Endocrinol. 137, 148–165.
| CrossRef | CAS | PubMed |

Subscriber Login

	Username: Password:

Legal & Privacy | Contact Us | Help