Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Time within reproductive season, but not age or inbreeding coefficient, affects seminal and sperm quality in the whooping crane (Grus americana)

M. E. Brown A B , S. J. Converse C , J. N. Chandler C , A. L. Crosier B , W. Lynch B , D. E. Wildt B , C. L. Keefer A and N. Songsasen B D
+ Author Affiliations
- Author Affiliations

A Department of Animal and Avian Sciences, 1413 Animal Sciences Center, University of Maryland, College Park, MD 20742, USA.

B Center for Species Survival, Smithsonian Conservation Biology Institute, National Zoological Park, 1500 Remount Road, Front Royal, VA 22630, USA.

C United States Geological Survey, Patuxent Wildlife Research Center, 12100 Beech Forest Road, Laurel, MD 2078, USA.

D Corresponding author. Email: songsasenn@si.edu

Reproduction, Fertility and Development 29(2) 294-306 https://doi.org/10.1071/RD15251
Submitted: 31 May 2014  Accepted: 27 June 2015   Published: 11 August 2015

Abstract

All living whooping cranes (Grus americana) are descended from 16 or fewer birds that remained alive in the early 1940s, a bottleneck that puts the species at potential risk for inbreeding depression. Although AI is commonly used in the management of the captive population of this species, little is known about seminal traits or factors affecting sperm quality in the whooping crane. In the present study, semen samples were collected from 29 adult males (age 3–27 years) during the early (March), mid (April) and late (May) breeding season over 2 consecutive years. The effects of donor age, time within reproductive season and level of inbreeding on seminal characteristics were analysed using regression and information–theoretic model selection. Only time within reproductive season significantly affected seminal traits, with total numbers of spermatozoa and proportions of pleiomorphisms increasing across the season. We conclude that, even with a highly restricted number of founders, there is no discernible influence of inbreeding (at the levels described) on sperm output or quality. Furthermore, although there is variance in seminal quality, the whooping crane produces significant numbers of motile spermatozoa throughout the breeding season, similar to values reported for the greater sandhill crane (Grus canadensis tabida).

Additional keywords: avian, male reproduction, seasonality, spermatozoa.


References

Akaike, H. (1973). Information theory as an extension of the maximum likelihood principle. In ‘Second International Symposium on Information Theory’. (Eds B. Petro and F. Csaki.) pp. 267–281. (Akademiai Kiado: Budapest.)

Allen, T. E., and Grigg, G. W. (1957). Sperm transport in the fowl. Aust. J. Agric. Res. 8, 788–799.
Sperm transport in the fowl.Crossref | GoogleScholarGoogle Scholar |

Archibald, G. W. (1974). Methods for breeding and rearing cranes in captivity. Int. Zoo Yearb. 14, 147–155.

Archibald, G., and Mirande, C. (1985). Population status and management efforts for endangered cranes. In ‘Transactions of the 50th North American Wildlife Natural Resources Conference’. pp. 586–602. (Wildlife Management Institute: Washington, D.C.)

Barone, M. A., Roelke, M. E., Howard, J., Brown, J. L., Anderson, A. E., and Wildt, D. E. (1994). Reproductive characteristics of male Florida panthers: comparative studies from Florida, Texas, Colorado, Latin America, and North American Zoos. J. Mammal. 75, 150–162.
Reproductive characteristics of male Florida panthers: comparative studies from Florida, Texas, Colorado, Latin America, and North American Zoos.Crossref | GoogleScholarGoogle Scholar |

Bates, D., Maechler, M., and Bolker, B. (2012). lme4: linear mixed-effects models using S4 classes. R package version 0.999999–0. Available at: http://CRAN.Rproject.org/package=lme4 [verified 21 July 2015].

Belaire, J., Kreakie, B. J., Keitt, T., and Minor, E. (2014). Predicting and mapping potential whooping crane stopover habitat to guide site selection for wind energy projects. Conserv. Biol. 28, 541–550.
Predicting and mapping potential whooping crane stopover habitat to guide site selection for wind energy projects.Crossref | GoogleScholarGoogle Scholar | 24372936PubMed |

Birkhead, T. R., Fletcher, F., Pellatt, E. J., and Staples, A. (1995). Ejaculate quality and the success of extra-pair copulations in the zebra finch. Nature 377, 422–423.
Ejaculate quality and the success of extra-pair copulations in the zebra finch.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXos1Smu7Y%3D&md5=5d75bf0cf109886130e856e9e8e1bbe0CAS |

Blanco, J. M., Long, J. A., Gee, G., Donoghue, A. M., and Wildt, D. E. (2008). Osmotic tolerance of avian spermatozoa: influence of time, temperature, cryoprotectant, and membrane ion pump function on sperm viability. Cryobiology 56, 8–14.
Osmotic tolerance of avian spermatozoa: influence of time, temperature, cryoprotectant, and membrane ion pump function on sperm viability.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXpt1Kqtg%3D%3D&md5=c04e3cbc2c0c67791ac8a48f96ecf0fbCAS | 18005955PubMed |

Blanco, J. M., Wildt, D. E., Höfle, U., Voelker, W., and Donoghue, A. M. (2009). Implementing artificial insemination as an effective tool for ex situ conservation of endangered avian species. Theriogenology 71, 200–213.
Implementing artificial insemination as an effective tool for ex situ conservation of endangered avian species.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1cjnt1Glsg%3D%3D&md5=5159a7db0e6c80ea51b47dae5adc8de8CAS | 19004491PubMed |

Blanco, J. M., Long, L. A., Gee, G., Wildt, D. E., and Donoghue, A. M. (2011). Comparative cryopreservation of avian spermatozoa: benefits of non-permeating osmoprotectants and ATP on turkey and crane sperm cryosurvival. Anim. Reprod. Sci. 123, 242–248.
Comparative cryopreservation of avian spermatozoa: benefits of non-permeating osmoprotectants and ATP on turkey and crane sperm cryosurvival.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXit1Whs7s%3D&md5=2ff6d559f99e0521c9ad6c70be8a018bCAS | 21277718PubMed |

Blanco, J. M., Long, L. A., Gee, G., Wildt, D. E., and Donoghue, A. M. (2012). Cryopreservation of avian spermatozoa: effects of freezing and thawing rates on turkey and sandhill crane sperm cryosurvival. Anim. Reprod. Sci. 131, 1–8.
Cryopreservation of avian spermatozoa: effects of freezing and thawing rates on turkey and sandhill crane sperm cryosurvival.Crossref | GoogleScholarGoogle Scholar | 22406423PubMed |

Boyce, M. S., Subhash, R. L., and Johns, B. W. (2005). Whooping crane recruitment enhanced by egg removal. Biol. Conserv. 126, 395–401.
Whooping crane recruitment enhanced by egg removal.Crossref | GoogleScholarGoogle Scholar |

Brillard, J. P., and Bakst, M. R. (1990). Quantification of spermatozoa in the sperm-storage tubules of turkey hens and the relation to sperm numbers in the perivitelline layer of eggs. Biol. Reprod. 43, 271–275.
Quantification of spermatozoa in the sperm-storage tubules of turkey hens and the relation to sperm numbers in the perivitelline layer of eggs.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3czjsFeksg%3D%3D&md5=52fa93929dde3bf28f760f40544726e2CAS | 2378938PubMed |

Burnham, K. P., and Anderson, D. R. (2004). Multimodel inference: understanding AIC and BIC in model selection. Sociol. Methods Res. 33, 261–304.
Multimodel inference: understanding AIC and BIC in model selection.Crossref | GoogleScholarGoogle Scholar |

Chen, G., Gee, G., Nicolich, J., and Taylor, J. (2001). The effects of semen collection on fertility in captive, naturally fertile, sandhill cranes. In ‘Proceedings of the Eighth North American Crane Workshop’. (Eds D. H. Ellis and C. H. Ellis.) pp. 185–193. (AlphaGraphics: Tuscon, AZ.)

Converse, S. J., Royal, J. A., and Urbanek, R. P. (2012). Bayesian analysis of multi-state data with individual covariates for estimating genetic affects on demography. J. Ornithol. 152, S561–S572.
Bayesian analysis of multi-state data with individual covariates for estimating genetic affects on demography.Crossref | GoogleScholarGoogle Scholar |

Canadian Wildlife Service and U.S. Fish and Wildlife Service (2009). ‘International Recovery Plan for the Whooping Crane.’ (Recovery of Nationally Endangered Wildlife (RENEW) and US Fish & Wildlife Service: Albuquerque, NM.)

Donoghue, A. M., Howard, J. G., Byers, A. P., Goodrowe, K. L., Bush, M., Blumer, E., Lukas, J., Stover, J., Snodgrass, K., and Wildt, D. E. (1992). Correlation of sperm viability with gamete interaction and fertilization in vitro in the cheetah (Acinonyx jubatus). Biol. Reprod. 46, 1047–1056.
Correlation of sperm viability with gamete interaction and fertilization in vitro in the cheetah (Acinonyx jubatus).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3s%2FgtlylsQ%3D%3D&md5=67a391158b2474b8a654957ee73ba1baCAS | 1391303PubMed |

Donoghue, A. M., Sonstegard, T. S., King, L. M., Smith, E. J., and Burt, D. W. (1999). Turkey sperm mobility influences paternity in the context of competitive fertilization. Biol. Reprod. 61, 422–427.
Turkey sperm mobility influences paternity in the context of competitive fertilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXkslKqtrs%3D&md5=893ad5be3272da683437ed6bdb87b481CAS | 10411522PubMed |

Ellis, D. H., Gee, G. F., and Mirande, C. M. (1996) ‘Cranes: Their Biology, Husbandry, and Conservation.’ (Department of the Interior, National Biological Service: Washington, D.C.)

Fischer, D., Neumann, D., Purchase, C., Bouts, T., Meinecke-Tilmann, S., Wehrend, A., and Lierz, M. (2014a). The use of semen evaluation and assisted reproduction in Spix’s macaws in terms of species conservation. Zoo Biol. 33, 234–244.
The use of semen evaluation and assisted reproduction in Spix’s macaws in terms of species conservation.Crossref | GoogleScholarGoogle Scholar | 24752991PubMed |

Fischer, D., Neumann, D., Wehrend, A., and Lierz, M. (2014b). Comparison of conventional and computer-assisted semen analysis in cockateils (Nymphicus hollandicus) and evaluations of different dosages for artificial insemination. Theriogenology 82, 613–620.
Comparison of conventional and computer-assisted semen analysis in cockateils (Nymphicus hollandicus) and evaluations of different dosages for artificial insemination.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2cfptFarsQ%3D%3D&md5=2822aa501cc81bbdb1c196599f85bbe5CAS | 24985563PubMed |

Fitzpatrick, J. L., and Evans, J. P. (2009). Reduced heterozygosity impairs semen quality in endangered mammals. Biol. Lett. 5, 320–323.
Reduced heterozygosity impairs semen quality in endangered mammals.Crossref | GoogleScholarGoogle Scholar | 19324650PubMed |

Froman, D. P., Feltmann, A. J., Rhoads, M. L., and Kirby, J. D. (1999). Sperm mobility: a primary determinant of fertility in the domestic fowl (Gallus domesticus). Biol. Reprod. 61, 400–405.
Sperm mobility: a primary determinant of fertility in the domestic fowl (Gallus domesticus).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXkslKqtr8%3D&md5=846d9500cadaca5164a8a2f5e248905bCAS | 10411518PubMed |

Gee, G. F. (1983). Crane reproductive physiology and conservation. Zoo Biol. 2, 199–213.
Crane reproductive physiology and conservation.Crossref | GoogleScholarGoogle Scholar |

Gee, G. F., and Temple, S. A. (1978). Artificial insemination for breeding non-domestic birds. In ‘Symposia of the Zoological Society of London 43.’ (Ed. P. F. Watson.) pp. 376. (Academic Press: London.)

Gee, G. F., Bakst, M. R., and Sexton, S. F. (1985). Cryogenic preservation of semen from the greater sandhill crane. J. Wildl. Manage. 49, 480–484.
Cryogenic preservation of semen from the greater sandhill crane.Crossref | GoogleScholarGoogle Scholar |

Gee, G. F., Bertschinger, H., Donoghue, A. M., Blanco, J., and Soley, J. (2004). Reproduction in nondomestic birds: physiology, semen collection, artificial insemination and cryopreservation. Avian Poult. Biol. Rev. 15, 47–101.
Reproduction in nondomestic birds: physiology, semen collection, artificial insemination and cryopreservation.Crossref | GoogleScholarGoogle Scholar |

Glenn, T. C., Stephan, W., and Brayn, M. J. (1999). Effects of population bottleneck on whooping crane mitochondrial DNA variation. Conserv. Biol. 13, 1097–1107.
Effects of population bottleneck on whooping crane mitochondrial DNA variation.Crossref | GoogleScholarGoogle Scholar |

Goodnight, K. F., and Queller, D. C. (1999). Computer software for performing likelihood tests of pedigree relationship using genetic markers. Mol. Ecol. 8, 1231–1234.
Computer software for performing likelihood tests of pedigree relationship using genetic markers.Crossref | GoogleScholarGoogle Scholar |

Guojun, C., Gee, G. F., Nicolich, J. M., and Taylor, J. A. (1998). Investigation into semen characteristics of naturally-fertile pairs in vitro and their correlation with fertility in Florida sandhill crane. J. Forest. Res. 9, 71–76.
Investigation into semen characteristics of naturally-fertile pairs in vitro and their correlation with fertility in Florida sandhill crane.Crossref | GoogleScholarGoogle Scholar |

Hereford, S. G. (1987). Semen volumes and peak production periods for cranes at the international crane foundation. In ‘International Crane Workshop: Proceedings of the 1983 International Crane Workshop’, Bharatpur, India. (Eds G. Archibald and R. F. Pasquier.) pp. 525–534. (International Crane Foundation: Baraboo, WI.)

Holsberger, D. R., Donoghue, A. M., Froman, D. P., and Ottinger, M. A. (1998). Assessment of ejaculate quality and sperm characteristics in turkeys: sperm mobility phenotype is independent of time. Poult. Sci. 77, 1711–1717.
Assessment of ejaculate quality and sperm characteristics in turkeys: sperm mobility phenotype is independent of time.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1M%2FltFSisA%3D%3D&md5=69b0c20ee1f46dfa007831c5e7fecd54CAS | 9835348PubMed |

Howard, J. G., Donoghue, A. M., Johnston, L. A., and Wildt, D. E. (1993). Zona pellucida penetration of structurally abnormal spermatozoa and reduced fertilization in teratospermic cats. Biol. Reprod. 49, 131–139.
Zona pellucida penetration of structurally abnormal spermatozoa and reduced fertilization in teratospermic cats.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3szlslegug%3D%3D&md5=ca8d7ccb884a49e0d5463e180b33d5a4CAS | 8353179PubMed |

Hurvich, C. M., and Tsai, C.-L. (1989). Regression and time series model selection in small samples. Biometrika 76, 297–307.
Regression and time series model selection in small samples.Crossref | GoogleScholarGoogle Scholar |

Jones, K. L., and Nicolich, J. M. (2001). Artificial insemination in captive whooping cranes: results from genetic analyses. Zoo Biol. 20, 331–342.
Artificial insemination in captive whooping cranes: results from genetic analyses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXosVSgu7o%3D&md5=54ebec98927d1e39e63207bcac805c57CAS |

Jones, K. L., Glenn, T. C., Lacy, R. C., Pierce, J. R., Unruh, N., Mirande, C. M., and Chavez-Ramirez, F. (2002). Refining the whooping crane studbook by incorporating microsatellite DNA and leg-banding analysis. Conserv. Biol. 16, 789–799.
Refining the whooping crane studbook by incorporating microsatellite DNA and leg-banding analysis.Crossref | GoogleScholarGoogle Scholar |

Keller, D. L., and Hartup, B. K. (2013). Reintroduction medicine: whooping cranes in Wisconsin. Zoo Biol. 32, 600–607.
Reintroduction medicine: whooping cranes in Wisconsin.Crossref | GoogleScholarGoogle Scholar | 24027128PubMed |

Konovalov, D., Manning, C., and Henshaw, M. (2004). KINGROUP: a program for pedigree relationship reconstruction and kin group assignments using genetic markers. Mol. Ecol. Notes 4, 779–782.

Kuyt, E. (1996). Reproductive manipulation in the whooping crane, Grus americana. Bird Conserv. Int. 6, 3–10.
Reproductive manipulation in the whooping crane, Grus americana.Crossref | GoogleScholarGoogle Scholar |

Lacy, R., Ballou, J., and Pollack, J. (2012). PMx: software package for demographic and genetic analysis and management of pedigreed populations. Methods Ecol. Evol. 3, 433–437.
PMx: software package for demographic and genetic analysis and management of pedigreed populations.Crossref | GoogleScholarGoogle Scholar |

Lake, P. E., and Stewart, J. M. (1978). ‘Artificial Insemination in Poultry.’ Bulletin/Ministry of Agriculture, Fisheries and Food 213. (HMSO: London.)

Lewis, J. C. (1997). Alerting the birds. Endanger. Spec. Bull. 22, 2.

Link, W. A. (2003). Nonidentifiability of population size from capture–recapture data with heterogeneous detection probabilities. Biometrics 59, 1123–1130.
Nonidentifiability of population size from capture–recapture data with heterogeneous detection probabilities.Crossref | GoogleScholarGoogle Scholar | 14969493PubMed |

Łukaszewicz, E., and Kruszyynski, W. (2003). Evaluation of fresh and frozen–thawed semen of individual ganders by assessment of spermatozoa motility and morphology. Theriogenology 59, 1627–1640.
| 12559467PubMed |

Maksudov, G. Y., and Panchenko, V. G. (2002). Obtaining an interspecific hybrid of cranes by artificial insemination and frozen–thawed semen. Biol. Bull. 29, 311–314.
Obtaining an interspecific hybrid of cranes by artificial insemination and frozen–thawed semen.Crossref | GoogleScholarGoogle Scholar |

Marvan, F., Rob, O., and Janecková, E. (1981). Die Klassifikation morphologischer spermienanomalien bei Garten. Zuchthygiene 16, 176–183.

Maximini, L., Fuerst-Walti, B., Gredler, B., and Baumung, R. (2011). Inbreeding depression on semen quality in Austrian dual-purpose Simmental bulls. Reprod. Domest. Anim. 46, e102–e104.
Inbreeding depression on semen quality in Austrian dual-purpose Simmental bulls.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M7itl2ltw%3D%3D&md5=22e036cac8f33bc8583d579ac44344bdCAS | 20546181PubMed |

Møller, A. P. (1988). Testes size, ejaculate quality and sperm competition in birds. Biol. J. Linn. Soc. Lond. 33, 273–283.
Testes size, ejaculate quality and sperm competition in birds.Crossref | GoogleScholarGoogle Scholar |

Monfort, S. L., Brown, J. L., Bush, M., Wood, T. C., Wemmer, C., Vargas, A., Williamson, L. R., Montali, R. J., and Wildt, D. E. (1993). Circannual inter-relationships among reproductive hormones, gross morphometry, behavior, ejaculate characteristics, and testicular histology in Eld’s deer stags (Cervus eldi thamin). J. Reprod. Fertil. 98, 471–480.
Circannual inter-relationships among reproductive hormones, gross morphometry, behavior, ejaculate characteristics, and testicular histology in Eld’s deer stags (Cervus eldi thamin).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2c%2Fhs1WhtQ%3D%3D&md5=9a78c4b36c3e79d2850eacbfb8baee42CAS | 8410813PubMed |

Moore, C. T., Converse, S. J., Folk, M. J., Runge, M. C., and Nesbitt, S. A. (2012). Evaluating release alternatives for a long-lived bird species under uncertainty about long-term demographic rates. J. Ornithol. 152, 339–353.
Evaluating release alternatives for a long-lived bird species under uncertainty about long-term demographic rates.Crossref | GoogleScholarGoogle Scholar |

Mortimer, D. (1994). ‘Practical Laboratory Andrology.’ (Oxford University Press: New York.)

Nesbitt, S. A., Folk, M. J., Spalding, M. G., Schmidt, J. A., Schwikert, S. T., Nicholich, J. M., Wellington, M., Lewis, J. C., and Logan, T. H. (1997). An experimental release of whooping cranes in Florida: the first 3 years. In ‘Proceedings of the Seventh North American Crane Workshop’. (Eds R. P. Urbanek and D. W. Stahlecker.) pp. 79–85. (AlphaGraphics: Tuscon, AZ.)

Nicolich, J. M., Gee, G. F., Ellis, D. H., and Hereford, S. G. (2001). Natural fertility in whooping cranes and Mississippi sandhill cranes at Patuxent Wildlife Research Center. In ‘Proceedings of the Eighth North American Crane Workshop’. (Eds D. H. Ellis and C. H. Ellis.) pp. 170–177. (AlphaGraphics: Tuscon, AZ.)

O’Brien, J. K., and Robeck, T. R. (2014). Semen characterization, seasonality of production, and in vitro sperm quality after chilled storage and cryopreservation in the king penguin (Aptenodytes patagonicus). Zoo Biol. 33, 99–109.
Semen characterization, seasonality of production, and in vitro sperm quality after chilled storage and cryopreservation in the king penguin (Aptenodytes patagonicus).Crossref | GoogleScholarGoogle Scholar | 24395205PubMed |

Omprakash, A. V., Kumararaj, R., Narahari, D., Prasad, A. J., and Sundararsu, V. (1992). Semen characteristics and their correlation with fertility in white leghorn as influenced by semen dilutents. Indian Vet. J. 69, 333–337.

Parks, J. E., Heck, P. W. R., and Hardaswick, V. A. (1986). Cryopreservation of peregrine falcon semen and post-thaw dialysis to remove glycerol. Raptor Res 20, 15–20.

Penfold, L. M., Wildt, D. E., Herzog, T. L., Lynch, W., Ware, L., Derrickson, S. R., and Monfort, S. L. (2000). Seasonal patterns of LH, testosterone, and semen quality in the northern pintail duck (Anas acuta). Reprod. Fertil. Dev. 12, 229–235.
Seasonal patterns of LH, testosterone, and semen quality in the northern pintail duck (Anas acuta).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXisFSks78%3D&md5=d5b6372e74b51860b1f6ce7d3525df91CAS | 11302434PubMed |

Penfold, L. M., Harnal, V., Lynch, W., Bird, D., Derrickson, S. R., and Wildt, D. E. (2001). Characterization of northern pintail (Anas acuta) ejaculate and the effect of sperm preservation on fertility. Reproduction 121, 267–275.
Characterization of northern pintail (Anas acuta) ejaculate and the effect of sperm preservation on fertility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhslSisbo%3D&md5=3064ca0d43e95a13c9a958d509a328ffCAS | 11226051PubMed |

Pukazhenthi, B., Pelican, K., Wildt, D., and Howard, J. G. (1999). Sensitivity of domestic cat (Felis catus) sperm from normospermic versus teratospermic donors to cold-induced acrosomal damage. Biol. Reprod. 61, 135–141.
Sensitivity of domestic cat (Felis catus) sperm from normospermic versus teratospermic donors to cold-induced acrosomal damage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXktFKgur0%3D&md5=ce004339a923110219e2a10235342778CAS | 10377041PubMed |

Pukazhenthi, B. S., Wildt, D. E., and Howard, J. G. (2001). The phenomenon and significance of teratospermia in felids. J. Reprod. Fertil. Suppl. 57, 423–433.
| 1:STN:280:DC%2BD38%2Fmt1Whuw%3D%3D&md5=840bbec912ccec358d7b25728751fe52CAS | 11787186PubMed |

Pukazhenthi, B. S., Neubauer, K., Jewgenow, K., Howard, J., and Wildt, D. E. (2006). The impact and potential etiology of teratospermia in the domestic cat and its wild relatives. Theriogenology 66, 112–121.
The impact and potential etiology of teratospermia in the domestic cat and its wild relatives.Crossref | GoogleScholarGoogle Scholar | 16644003PubMed |

R Core Team (2014). R: a language and environment for statistical computing. (R Foundation for Statistical Computing: Vienna.) Available at: http://www.R-project.org/ [verified 21 July 2015].

Ritland, K. (1996). Estimators for pairwise relatedness and individual inbreeding coefficients. Genet. Res. 67, 175–185.
Estimators for pairwise relatedness and individual inbreeding coefficients.Crossref | GoogleScholarGoogle Scholar |

Roldan, E. R. S., Cassinello, J., Abaigar, T., and Gomendio, M. (1998). Inbreeding, fluctuating asymmetry, and ejaculate quality in an endangered ungulate. Proc. Biol. Sci. 265, 243–248.
Inbreeding, fluctuating asymmetry, and ejaculate quality in an endangered ungulate.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1c7lsVClsg%3D%3D&md5=6d36bf69b0df7a7b2c0c04b101dcaf77CAS |

Ruiz-Lopez, M. J., Evenson, D., Espeso, G., Gomendio, M., and Roldan, E. (2010). High levels of DNA fragmentation in spermatozoa are associated with inbreeding and poor sperm quality in endangered ungulates. Biol. Reprod. 83, 332–338.
High levels of DNA fragmentation in spermatozoa are associated with inbreeding and poor sperm quality in endangered ungulates.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVyrsrrP&md5=d124a38464a76916c1e3fd8391ab7526CAS | 20505170PubMed |

Russman, S. E. (1981) Sperm morphology in the crane. MS Thesis, University of Illinois at Urbana–Champaign.

Smith, D. H. V., Converse, S. J., Gibson, K. W., Moehrenschlager, A., Link, W. A., Olsen, G. H., and Maguire, K. (2011). Decision analysis for conservation breeding: maximizing production for reintroduction of whooping cranes. J. Wildl. Manage. 75, 501–508.
Decision analysis for conservation breeding: maximizing production for reintroduction of whooping cranes.Crossref | GoogleScholarGoogle Scholar |

Sontakke, S. D. (2004). Semen characteristics, cryopreservation, and successful artificial insemination in the blue rock pigeon (Columba livia). Theriogenology 62, 139–153.
Semen characteristics, cryopreservation, and successful artificial insemination in the blue rock pigeon (Columba livia).Crossref | GoogleScholarGoogle Scholar | 15159109PubMed |

Stelzer, G., Schmidt, V., Sobiraj, A., and Krautwald-Junghanns, M.-E. (2009). Spermatozoa characteristics in six psittacine species using light microscopy. Reprod. Domest. Anim. 44, 894–899.
Spermatozoa characteristics in six psittacine species using light microscopy.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3czisFeltw%3D%3D&md5=69e8d576b987bc2b7da4ef9f3c506815CAS | 20456089PubMed |

Stunden, C. E., Bluhm, C. K., Cheng, K. M., and Rajamahendran, R. (1998). Plasma testosterone profiles, semen characteristics, and artificial insemination in yearling and adult captive mallard ducks (Anas platyrhynchos). Poult. Sci. 77, 882–887.
Plasma testosterone profiles, semen characteristics, and artificial insemination in yearling and adult captive mallard ducks (Anas platyrhynchos).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmsFOg&md5=9bfecd8548577bd845bc65cd9720f825CAS | 9628539PubMed |

Trinkel, M., Funston, P., Hofmeyr, M., Hofmeyr, D., Deli, S., Packer, C., and Slotow, R. (2010). Inbreeding and density dependent population growth in a small, isolated, lion population. Anim. Conserv. 13, 374–382.
Inbreeding and density dependent population growth in a small, isolated, lion population.Crossref | GoogleScholarGoogle Scholar |

Umapathy, G., Sontakke, S., Reddy, A., Ahmed, S., and Shivaji, S. (2005). Semen characteristics of the captive Indian white-backed vulture (Gyps bengalensis). Biol. Reprod. 73, 1039–1045.
Semen characteristics of the captive Indian white-backed vulture (Gyps bengalensis).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFGktbzP&md5=19fe93fe1aa3af4e1366548b6507dd86CAS | 16033999PubMed |

Urbanek, R. P., Fondow, L. E. A., Satyshur, C. D., Lacy, A. E., Zimorski, S. E., and Wellington, M. (2006). First cohort of migratory whooping cranes reintroduced to eastern North America: the first year after release. In ‘Proceedings of the Tenth North American Crane Workshop’. (Eds M. J. Folk and S. A. Nesbitt.) pp. 213–223. (Leesburg Printing: Leesburg, FL.)

Waldoch, J., Root, T., Ramer, J., and Proudfoot, J. (2007). Semen collection and characterization in rockhopper penguins (Eudyptes chrysocome chrysocome). J. Zoo Wildl. Med. 38, 13–17.
Semen collection and characterization in rockhopper penguins (Eudyptes chrysocome chrysocome).Crossref | GoogleScholarGoogle Scholar | 17469270PubMed |

Waldoch, J., Root, T., Dubach, J. M., Proudfoot, J., and Ramer, J. (2012). Semen characteristics and artificial insemination in rockhopper penguins (Eudyptes chrysocome chrysocome). Zoo Biol. 31, 166–180.
Semen characteristics and artificial insemination in rockhopper penguins (Eudyptes chrysocome chrysocome).Crossref | GoogleScholarGoogle Scholar | 21538504PubMed |

Wang, J. (2011). COANCESTRY: a program for simulating, estimating, and analysing relatedness and inbreeding coefficients. Mol. Ecol. Resour. 11, 141–145.
COANCESTRY: a program for simulating, estimating, and analysing relatedness and inbreeding coefficients.Crossref | GoogleScholarGoogle Scholar | 21429111PubMed |

White, J. (2000). ‘Management of Captive Whooping Crane (Grus americana) to Improve Breeding Behavior and Success.’ (University of Calgary: Calgary.)

Wildt, D. E., Bush, M., Howard, J. G., O’Brien, S. J., Metzler, D., van Dyk, A., Ebedes, H., and Brand, D. J. (1983). Unique seminal qualityin the South African cheetah and a comparative evaluation in the domestic cat. Biol. Reprod. 29, 1019–1025.
Unique seminal qualityin the South African cheetah and a comparative evaluation in the domestic cat.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2c%2FltlGltA%3D%3D&md5=551f90cee0d5cc591f284a641eb1201cCAS | 6640033PubMed |

Wildt, D., Bush, M., Goodrowe, K., Packer, C., Pusey, A., Brown, J., Joslin, P., and O’Brien, S. (1987). Reproductive and genetic consequences of founding isolated lion populations. Nature 329, 328–331.
Reproductive and genetic consequences of founding isolated lion populations.Crossref | GoogleScholarGoogle Scholar |

Williams, C., and McGibbon, W. H. (1956). The yields of semen among inbred lines and crosses of SC leghorns. Poult. Sci. 35, 617–620.
The yields of semen among inbred lines and crosses of SC leghorns.Crossref | GoogleScholarGoogle Scholar |