Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Wildlife Research Wildlife Research Society
Ecology, management and conservation in natural and modified habitats
RESEARCH ARTICLE

Post-release breeding of translocated sharp-tailed grouse and an absence of artificial insemination effects

Steven R. Mathews A B , Peter S. Coates https://orcid.org/0000-0002-8393-5391 A E , Jennifer A. Fike C , Helena Schneider D , Dominik Fischer D , Sara J. Oyler-McCance C , Michael Lierz D and David J. Delehanty B
+ Author Affiliations
- Author Affiliations

A US Geological Survey, Western Ecological Research Center, Dixon Field Station, 800 Business Park Drive, Suite D, Dixon, CA 95620, USA.

B Department of Biological Sciences, Idaho State University, Pocatello, ID 83209, USA.

C US Geological Survey, Fort Collins Science Center, 2150 Centre Avenue, Building C, Fort Collins, CO 80526, USA.

D Clinic for Birds, Reptiles, Amphibians and Fish, Faculty of Veterinary Medicine, Justus Liebig University Giessen, Giessen, Germany.

E Corresponding author. Email: pcoates@usgs.gov

Wildlife Research 46(1) 12-24 https://doi.org/10.1071/WR18094
Submitted: 2 June 2018  Accepted: 23 August 2018   Published: 21 December 2018

Abstract

Context: Translocation has become a widely used method to restore wildlife populations following extirpation. For some species, such as lekking grouse, which breed at traditional mating grounds, reproduction is linked to culturally established geographic locations. Cultural centres are lost upon extirpation, making restoration into otherwise rehabilitated habitats especially challenging. The process by which species with culturally dependent reproduction sometimes become re-established is poorly understood and merits investigation to improve conservation strategies.

Aims: We reintroduced CSTG to vacant habitat in north-central Nevada, USA, from 2013 to 2017, with concordant goals of promoting females to nest and males to lek. We tested the utility of performing artificial insemination (AI) on females before translocation and we conducted paternity analyses to understand male reproduction.

Methods: We monitored females for the effects of AI on nest initiation, nest survival and egg fertility. We used post-hatch extra-embryonic membranes and other tissues to evaluate paternity of chicks produced at the restoration site.

Key results: Artificial insemination had no effect on female survival or nest initiation, and did not fertilise any eggs within nine sampled clutches (n = 102 eggs). Most paternity was attributable to male residents that had survived for ≥1 year at the restoration site before the arrival of translocated females.

Conclusions: Artificial insemination neither aided nor harmed female reproduction. A small number of translocated, resident adult males sired reproduction following female release.

Implications: The presence of resident males at restoration sites may be more likely to result in post-translocation reproduction than is pre-translocation AI. Restoring CSTG to vacant habitat should focus on translocating females into suitable nesting habitat while simultaneously ensuring that reproductively capable males are available within or adjacent to the nesting habitat.

Additional keywords: conservation ecology, conservation genetics, conservation management, management strategies, population management, radio telemetry, reproductive behaviour, threatened species, wildlife management.


References

Akaike, H. (1973). Information theory and an extension of the maximum likelihood principle. In ‘Proceedings of the Second International Symposium on Information Theory’. (Eds B. N. Petrov and S. Caski.) pp. 27–281. (Akademiai Kaido: Budapest, Hungary.)

Armstrong, D. P., and Seddon, P. J. (2008). Directions in reintroduction biology. Trends in Ecology Evolution 23, 20–25.
Directions in reintroduction biology.Crossref | GoogleScholarGoogle Scholar |

Atamian, M. T., and Sedinger, J. S. (2010). Balanced sex ratio at hatch in a greater sage-grouse (Centrocercus urophasianus) population. The Auk 127, 16–22.
Balanced sex ratio at hatch in a greater sage-grouse (Centrocercus urophasianus) population.Crossref | GoogleScholarGoogle Scholar |

Bakst, M. R. (2011). Physiology and endocrinology symposium: role of the oviduct in maintaining sustained fertility in hens. Journal of Animal Science 89, 1323–1329.
Physiology and endocrinology symposium: role of the oviduct in maintaining sustained fertility in hens.Crossref | GoogleScholarGoogle Scholar |

Bates, D., Maechler, M., Bolker, B., and Walker, S. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 1–48.
Fitting linear mixed-effects models using lme4.Crossref | GoogleScholarGoogle Scholar |

Beehler, B. M., and Foster, M. S. (1988). Hotshots, hotspots, and female preference in the organization of lek mating systems. American Naturalist 131, 203–219.
Hotshots, hotspots, and female preference in the organization of lek mating systems.Crossref | GoogleScholarGoogle Scholar |

Bird, D. M., and Buckland, R. B. (1976). The onset and duration of fertility in the American kestrel. Canadian Journal of Zoology 54, 1595–1597.
The onset and duration of fertility in the American kestrel.Crossref | GoogleScholarGoogle Scholar |

Bird, K. L., Aldridge, C. L., Carpenter, J. E., Paszkowski, C. A., Boyce, M. S., and Coltman, D. W. (2013). The secret sex lives of sage-grouse: multiple paternity and intraspecific nest parasitism revealed through genetic analysis. Behavioral Ecology 24, 29–38.
The secret sex lives of sage-grouse: multiple paternity and intraspecific nest parasitism revealed through genetic analysis.Crossref | GoogleScholarGoogle Scholar |

Birkhead, T. R. (1987). Sperm competition in birds. Trends in Ecology Evolution 2, 268–272.
Sperm competition in birds.Crossref | GoogleScholarGoogle Scholar |

Birkhead, T. R., and Møller, A. P. (1993). Sexual selection and the temporal separation of reproductive events: sperm storage data from reptiles, birds and mammals. Biological Journal of the Linnean Society. Linnean Society of London 50, 295–311.
Sexual selection and the temporal separation of reproductive events: sperm storage data from reptiles, birds and mammals.Crossref | GoogleScholarGoogle Scholar |

Blanco, J. M., Wildt, D. E., Hofle, 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 |

Burnham, K. P., and Anderson, D. R. (2002). ‘Model Selection and Multimodel Inference: a Practical Information-theoretic Approach.’ 2nd edn. (Springer: New York, NY.)

Burrows, W. H., and Quinn, J. P. (1935). A method of obtaining spermatozoa from the domestic fowl. Poultry Science 14, 251–254.
A method of obtaining spermatozoa from the domestic fowl.Crossref | GoogleScholarGoogle Scholar |

Bush, K. L., Vinsky, M. D., Aldridge, C. L., and Pazkowski, C. A. (2005). A comparison of sample types varying in invasiveness for use in DNA sex determination in an endangered population of greater sage-grouse (Centrocercus urophasianus). Conservation Genetics 6, 867–870.
A comparison of sample types varying in invasiveness for use in DNA sex determination in an endangered population of greater sage-grouse (Centrocercus urophasianus).Crossref | GoogleScholarGoogle Scholar |

Caruso, K. J., Cowell, R. L., Meinkoth, J. H., and Klaassen, J. K. (2002). Abdominal effusion in a bird. Veterinary Clinical Pathology 31, 127–128.
Abdominal effusion in a bird.Crossref | GoogleScholarGoogle Scholar |

Ciereszko, A., Dietrich, G. J., Liszewaska, E., Krzywiński, A., and Kobus, A. (2011). Short-term storage and cryopreservation of black grouse and capercaillie semen. European Journal of Wildlife Research 57, 383–388.
Short-term storage and cryopreservation of black grouse and capercaillie semen.Crossref | GoogleScholarGoogle Scholar |

Coates, P. S., and Delehanty, D. J. (2006). Effect of capture date on nest-attempt rate of translocated sharp-tailed grouse Tympanuchus phasianellus. Wildlife Biology 12, 277–283.
Effect of capture date on nest-attempt rate of translocated sharp-tailed grouse Tympanuchus phasianellus.Crossref | GoogleScholarGoogle Scholar |

Coates, P. S., and Delehanty, D. J. (2010). Nest predation of greater sage-grouse in relation to microhabitat factors and predators. The Journal of Wildlife Management 74, 240–248.
Nest predation of greater sage-grouse in relation to microhabitat factors and predators.Crossref | GoogleScholarGoogle Scholar |

Coates, P. S., Stiver, S. J., and Delehanty, D. J. (2006). Using sharp-tailed grouse movement patterns to guide release site selection. Wildlife Society Bulletin 34, 1376–1382.
Using sharp-tailed grouse movement patterns to guide release site selection.Crossref | GoogleScholarGoogle Scholar |

Coates, P. S., Dudko, J. E., Delehanty, D. J., and Casazza, M. L. (2011). Data summary of a Columbian sharp-tailed grouse habitat suitability examination between Idaho and Nevada: United States Geological Survey data summary. US Geological Survey, Dixon, CA.

Connelly, J. W., Gratson, M. W., and Reese, K. P. (1998). Sharp-tailed Grouse (Tympanuchus phasianellus), version 2.0. In ‘The Birds of North America’. (Eds A. F. Poole, F. B. Gill). (Cornell Lab of Ornithology: Ithaca, NY, USA.)

Connelly, J.W., Reese, K.P., and Schroeder, M.A. (2003). Monitoring of Greater Sage-Grouse habitats and populations. College of Natural Resources Experimental Station Bulletin, 80, 1 – 47. University of Idaho, Moscow, Idaho USA. Available at https://sagemap.wr.usgs.gov/docs/grouse_habitat_book.pdf

DeMatteo, K. E., Karagiannis, K. L., Asa, C. S., Macek, M. S., Snyder, T. L., Tieber, A. M., and Parker, P. G. (2004). Semen collection and artificial insemination in the common piping guan (Pipile cumanensis cumanensis): potential applications for cracidae (AVES: Galliformes). Journal of Zoo and Wildlife Medicine 35, 447–458.
Semen collection and artificial insemination in the common piping guan (Pipile cumanensis cumanensis): potential applications for cracidae (AVES: Galliformes).Crossref | GoogleScholarGoogle Scholar |

Dickens, M. J., Delehanty, D. J., and Romero, M. L. (2009a). Stress and translocations: alterations of the stress physiology of translocated birds. Proceedings. Biological Sciences 276, 2051–2056.
Stress and translocations: alterations of the stress physiology of translocated birds.Crossref | GoogleScholarGoogle Scholar |

Dickens, M. J., Delehanty, D. J., Reed, J. M., and Romero, L. M. (2009b). What happens to translocated game birds that ‘disappear’? Animal Conservation 12, 418–425.
What happens to translocated game birds that ‘disappear’?Crossref | GoogleScholarGoogle Scholar |

Dickens, M. J., Delehanty, D. J., and Romero, L. M. (2010). Stress: an inevitable component of animal translocation. Biological Conservation 143, 1329–1341.
Stress: an inevitable component of animal translocation.Crossref | GoogleScholarGoogle Scholar |

Drummer, T. D., Coracelli, R. G., and Sjogren, S. J. (2011). Sharp-tailed grouse lek attendance and fidelity in Upper Michigan. The Journal of Wildlife Management 75, 311–318.
Sharp-tailed grouse lek attendance and fidelity in Upper Michigan.Crossref | GoogleScholarGoogle Scholar |

Emmons, S. R., and Braun, C. E. (1985). Natal dispersal and lek fidelity of sage grouse. The Auk 102, 1023–1028.

Fike, J. A., Oyler-McCance, S. J., Zimmerman, S. J., and Castoe, T. A. (2015). Development of 13 microsatellites for Gunnison sage-grouse (Centrocercus minimus) using next-generation shotgun sequencing and their utility in greater sage-grouse (Centrocercus urophasianus). Conservation Genetics Resources 7, 211–214.
Development of 13 microsatellites for Gunnison sage-grouse (Centrocercus minimus) using next-generation shotgun sequencing and their utility in greater sage-grouse (Centrocercus urophasianus).Crossref | GoogleScholarGoogle Scholar |

Fischer, D., Neumann, D., Wehrend, A., and Lierz, M. (2014). Comparison of conventional and computer-assisted semen analysis in cockatiels (Nymphicus hollandicus) and evaluation of different insemination dosages for artificial insemination. Theriogenology 82, 613–620.
Comparison of conventional and computer-assisted semen analysis in cockatiels (Nymphicus hollandicus) and evaluation of different insemination dosages for artificial insemination.Crossref | GoogleScholarGoogle Scholar |

Giesen, K. M., and Connelly, J. S. (1993). Guidelines for management of Columbian sharp-tailed grouse habitats. Wildlife Society Bulletin 21, 325–333.

Grier, J. W. (1973). Techniques and results of artificial insemination with golden Eagles. Raptor Research 7, 1–12.

Griffith, B., Scott, J. M., Carpenter, J. W., and Reed, C. (1989). Translocation as a species conservation tool: status and strategy. Science 245, 477–480.
Translocation as a species conservation tool: status and strategy.Crossref | GoogleScholarGoogle Scholar |

Gross, W. B., and Siegel, P. B. (1959). Coliform peritonitis of chickens. Avian Diseases 3, 370–373.
Coliform peritonitis of chickens.Crossref | GoogleScholarGoogle Scholar |

Hagen, C. A. and Giesen, K. M. (2005). Lesser Prairie-Chicken (Tympanuchus pallidicinctus), version 2.0. In ‘The Birds of North America’. (Ed. A. F. Poole.) (Cornell Lab of Ornithology: Ithaca, NY, USA.)

Hoffman, C. (1998). Peregrine to soar off endangered species list. Endangered Species Bull 23, 20–21.

Hoffman, R. W., and Thomas, A. E. (2007). ‘Columbian Sharp-tailed Grouse (Tympanuchus phasianellus columbianus): a Technical Conservation Assessment.’ (USDA Forest Service, Rocky Mountain Region: Golden, CO.)

International Association of Fish and Wildlife Agencies (IAFWA) (2002). Economic Importance of Hunting in America. (IAFWA: Washington, DC.) Available at https://buffalo.uwex.edu/files/2011/01/Economic-Importance-of-Hunting-in-America.pdf [verified 10 December 2018]

Johnson, J. A., Schroeder, M. A., and Robb, L. A. (2011). Greater Prairie-Chicken (Tympanuchus cupido), version 2.0. In ‘The Birds of North America’. (Ed. A. F. Poole) (Cornell Lab of Ornithology: Ithaca, NY, USA.)

Kahn, N., St. John, J., and Quinn, T. (1998). Chromosome-specific intron size differences in the avian CHD gene provide an efficient method for sex identification in birds. The Auk 115, 1074–1078.
Chromosome-specific intron size differences in the avian CHD gene provide an efficient method for sex identification in birds.Crossref | GoogleScholarGoogle Scholar |

Kalinowski, S. T., Taper, M. L., and Marshall, T. C. (2007). Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Molecular Ecology 16, 1099–1106.
Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment.Crossref | GoogleScholarGoogle Scholar |

Laake, J. (2013). RMark: an R Interface for Analysis of Capture–Recapture Data with MARK. In ‘AFSC Processed Rep 2013-01’. pp. 25. (Alaska Fisheries Science Center; NOAA; National Marine Fisheries Service; Seattle, WA.)

Lierz, M., Reinschmidt, M., Müller, H., Wink, M., and Neumann, D. (2013). A novel method for semen collection and artificial insemination in large parrots (Psittaciformes). Scientific Reports 3, 2066.
A novel method for semen collection and artificial insemination in large parrots (Psittaciformes).Crossref | GoogleScholarGoogle Scholar |

Longmire, J. L., Gee, G. F., Hardekoph, C. L., and Mark, G. A. (1992). Establishing paternity in whooping cranes (Grus americana) by DNA analysis. The Auk 109, 522–529.

Marshall, T. C., Slate, J., Kruuk, L. E. B., and Pemberton, J. M. (1998). Statistical confidence for likelihood-based paternity inference in natural populations. Molecular Ecology 7, 639–655.
Statistical confidence for likelihood-based paternity inference in natural populations.Crossref | GoogleScholarGoogle Scholar |

Mathews, S. R., Coates, P. S., and Delehanty, D. J. (2016). Survival of translocated sharp-tailed grouse: temporal threshold and age effects. Wildlife Research 43, 220–227.
Survival of translocated sharp-tailed grouse: temporal threshold and age effects.Crossref | GoogleScholarGoogle Scholar |

McKelvey, K. S., and Schwartz, M. K. (2005). DROPOUT: a program to identify problem loci and samples for noninvasive genetic samples in a capture–mark–recapture framework. Molecular Ecology Notes 5, 716–718.
DROPOUT: a program to identify problem loci and samples for noninvasive genetic samples in a capture–mark–recapture framework.Crossref | GoogleScholarGoogle Scholar |

Miller, G. C., and Graul, W. D. (1980). Status of sharp-tailed grouse in North America. In ‘Proceedings of the Prairie Grouse Symposium’. (Eds P.A. Vohs and F.L. Knopf.) pp. 18–28. (Oklahoma State University: Stillwater, OK, USA.)

Neumann, D., Kaleta, E. F., and Lierz, M. (2013). Semen collection and artificial insemination in cockatiels (Nymphicus hollandicus): a potential model for psittacines. Tierarztliche Praxis Kleintiere 41, 101–105.
Semen collection and artificial insemination in cockatiels (Nymphicus hollandicus): a potential model for psittacines.Crossref | GoogleScholarGoogle Scholar |

Nevada Department of Wildlife (NDOW) (2008). ‘Nevada Upland Game Species Management Plan.’ Game Division internal document. (Nevada Department of Wildlife Headquarters: Reno, NV.)

Oyler-McCance, S. J., and St. John, J. (2010). Characterization of small microsatellite loci for use in non invasive sampling studies of Gunnison sage-grouse (Centrocercus minimus). Conservation Genetics Resources 2, 17–20.
Characterization of small microsatellite loci for use in non invasive sampling studies of Gunnison sage-grouse (Centrocercus minimus).Crossref | GoogleScholarGoogle Scholar |

Oyler-McCance, S. J., DeYoung, R. W., Fike, J. A., Hagen, C. A., Johnson, J. A., Larsson, L. C., and Patten, M. A. (2016). Rangewide genetic analysis of lesser prairie-chicken reveals population structure, range expansion, and possible introgression. Conservation Genetics 17, 643–660.
Rangewide genetic analysis of lesser prairie-chicken reveals population structure, range expansion, and possible introgression.Crossref | GoogleScholarGoogle Scholar |

Piertney, S. B., and Dallas, J. F. (1997). Isolation and characterization of hypervariable microsatellites in the red grouse Lagopus lagopus scoticus. Molecular Ecology 6, 93–95.
Isolation and characterization of hypervariable microsatellites in the red grouse Lagopus lagopus scoticus.Crossref | GoogleScholarGoogle Scholar |

Piertney, S. B., and Höglund, J. (2001). Polymorphic microsatellite DNA markers in black grouse (Tetrao tetrix). Molecular Ecology Resources 1, 303–304.

R Core Team (2017). ‘R: a Language and Environment for Statistical Computing.’ (R Foundation for Statistical Computing: Vienna, Austria.) Available at https://www.R-project.org/ [verified 10 December 2018]

Reese, K. P., and Connelly, J. W. (1997). Translocations of sage grouse Centrocercus urophasianus in North America. Wildlife Biology 3, 235–241.
Translocations of sage grouse Centrocercus urophasianus in North America.Crossref | GoogleScholarGoogle Scholar |

Rotella, J. (2017). Nest survival models. In ‘Program MARK, a Gentle Introduction’. 17th edn. (Eds E. G. Cooch and G. C. White.) pp. 17.1–17.9. (Lulu Press, Morrisville, NC, USA)

Saint Jalme, M., Gaucher, P., and Paillat, P. (1994). Artificial insemination of Houbara bustards (Chlamydotis undulata): influence of the number of spermatozoa and insemination frequency on fertility and ability to hatch. Journal of Reproduction and Fertility 100, 93–103.
Artificial insemination of Houbara bustards (Chlamydotis undulata): influence of the number of spermatozoa and insemination frequency on fertility and ability to hatch.Crossref | GoogleScholarGoogle Scholar |

Schneider, H., Fischer, D., Failing, K., Ehling, C., Meinecke-Tillmann, S., Wehrend, A., and Lierz, M. (2018). Investigations on a cryopreservation protocol for long-term storage of psittacine spermatozoa using cockatiel semen as an example. Theriogenology 110, 8–17.
Investigations on a cryopreservation protocol for long-term storage of psittacine spermatozoa using cockatiel semen as an example.Crossref | GoogleScholarGoogle Scholar |

Schroeder, M. A., and Braun, C. E. (1991). Walk-in traps for capturing greater prairie-chickens on leks. Journal of Field Ornithology 62, 378–385.

Segelbacher, G., Paxton, R. J., Steinbruck, G., Trontelj, P., and Storch, I. (2000). Characterization of microsatellites in capercaillie Tetrao urogallus (AVES). Molecular Ecology 9, 1934–1935.
Characterization of microsatellites in capercaillie Tetrao urogallus (AVES).Crossref | GoogleScholarGoogle Scholar |

Selous, E. (1906–1907). Observations tending to throw light on the question of sexual selection in birds, including a day-to-day diary on the breeding habits of the ruff (Machetes pugnax). The Zoologist 4, 201–381.

Siudzińska, A., and Łukaszewicz, E. (2008). Effect of semen extenders and storage time on sperm morphology of four chicken breeds. Journal of Applied Poultry Research 17, 101–108.
Effect of semen extenders and storage time on sperm morphology of four chicken breeds.Crossref | GoogleScholarGoogle Scholar |

Snyder, J. W., Pelren, E. C., and Crawford, J. A. (1999). Translocation histories of prairie grouse in the United States. Wildlife Society Bulletin 27, 428–432.

Sontakke, S. D., Umapathy, G., Sivaram, V., Kholkute, S. D., and Shivaji, S. (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 |

Toepfer J. E. Eng R. L. Anderson R. K. 1990 Translocating prairie grouse: what have we learned? Transactions of the North American Wildlife and Natural Resources Conference 55 569 579

Trimbos, K. B., Broekman, J., Kentie, R., Musters, C. J. M., and de Snoo, G. R. (2009). Using eggshell membranes as a DNA source for population genetic research. Journal of Ornithology 150, 915–920.
Using eggshell membranes as a DNA source for population genetic research.Crossref | GoogleScholarGoogle Scholar |

Vogel, J. A., Shepherd, S. E., and Debinsky, D. M. (2015). An unexpected journey: greater prairie-chicken travels nearly 4000 km after translocation to Iowa. American Midland Naturalist 174, 343–349.
An unexpected journey: greater prairie-chicken travels nearly 4000 km after translocation to Iowa.Crossref | GoogleScholarGoogle Scholar |

Wakkinen, W. L., Reese, K. P., Connelly, J. W., and Fischer, R. A. (1992). An improved spotlighting technique for capturing sage grouse. Wildlife Society Bulletin 20, 425–426.

Walling, C. A., Pemberton, J. M., Hadfield, J. D., and Kruuk, L. E. B. (2010). Comparing parentage inference software: reanalysis of a red deer pedigree. Molecular Ecology 19, 1914–1928.
Comparing parentage inference software: reanalysis of a red deer pedigree.Crossref | GoogleScholarGoogle Scholar |

White, G. C., and Burnham, K. P. (1999). Program MARK: survival estimation from populations of marked animals. Bird Study 46, S120–S138.
Program MARK: survival estimation from populations of marked animals.Crossref | GoogleScholarGoogle Scholar |