Skip to main content

Advertisement

Log in

Landscape genetic evaluation of a tallgrass prairie corridor using the Greater Prairie-chicken (Tympanuchus cupido)

  • Research Article
  • Published:
Landscape Ecology Aims and scope Submit manuscript

Abstract

Context

We studied current functional connectivity along a developing grassland corridor in the Midwestern U.S. and focused on connectivity for Greater Prairie-chickens (Tympanuchus cupido). Greater Prairie-chickens are an area-sensitive species that rely on grasslands and are an indicator species for the tallgrass prairie ecosystem in North America. The coordinated multi-agency Prairie Landscape Conservation Plan is one of the largest planned and implemented conservation corridors in the U.S., making this system ideal to examine factors associated with corridor functionality.

Objectives

We examined landscape functional connectivity and factors that impact genetic structure and gene flow of Greater Prairie-chickens to identify gaps in a planned prairie corridor that is currently being implemented.

Methods

We collected feathers from 81 leks and obtained 31 hunter-harvested wings. We used a landscape genetic approach to evaluate eight hypotheses to explain functional connectivity and examine impacts of land cover and land use on isolation and genetic structure.

Results

Two populations were most supported based on 294 unique genotypes. Functional connectivity was influenced by land use, land cover, and anthropogenic development. Good connectivity exists within the Greater Prairie-chicken range, but improvements along the corridor in the northern portion of the extant range would be beneficial.

Conclusions

We produced geographically specific recommendations as to where land management can potentially achieve the greatest impact. Our results help prioritize areas for ongoing conservation efforts, like prairie acquisition, restoration, and enhancement. Furthermore, identification of factors influencing connectivity in our study can be applied to improve conservation planning elsewhere in the tallgrass prairie ecosystem.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Adkins K (2017) The relationship between grasslands, Conservation Reserve Program (CRP) Enrollments and Greater Prairie-chicken Populations (Tympanuchus cupido pinnatus) in Minnesota. M. S. Thesis, University of Minnesota-Twin Cities, St. Paul, MN

  • Adkins KC, Roy L, Andersen DE, Wright RG (2019) Landscape-scale Greater Prairie-chicken—Habitat Relations and the Conservation Reserve Program. J Wildl Manag (in press)

  • Anderson JR, Hardy CL, Roach JT, Witmer RE (1976) A land use land cover classification system for use with remote sensor data. United States Geological Survey, United States Department of the Interior, United States Government Printing Office, Washington, DC

  • Balkenhol N, Waits LP, Dezanni RJ (2009) Statistical approaches for landscape genetics: an evaluation of methods for linking landscape and genetic data. Ecography 32:818–830

    Article  Google Scholar 

  • Balloux F, Lugon-Moulin N (2002) The estimation of population differentiation with microsatellite markers. Mol Ecol 11(155):165

    Google Scholar 

  • Bateson ZW, Dunn PO, Hull SD, Henschen AE, Johnson JA, Whittingham LA (2014) Genetic restoration of a threatened population of greater prairie-chickens. Biol Conserv 174:12–19

    Article  Google Scholar 

  • Beier P, Noss RF (1998) Do habitat corridors provide connectivity? Conserv Biol 12:1241–1252

    Article  Google Scholar 

  • Bélisle M (2005) Measuring landscape connectivity: the challenge of behavioral landscape ecology. Ecology 86:1988–1995

    Article  Google Scholar 

  • Berkman LK, Nielsen CK, Roy CL, Heist EJ (2013a) Population genetic structure among bobwhite in an agriculturally modified landscape. J Wildl Manag 77:1472–1481

    Article  Google Scholar 

  • Berkman LK, Nielsen CK, Roy CL, Heist EJ (2013b) Resistance is futile: effects of landscape genetic features on gene flow of the northern bobwhite. Conserv Genet 14:323–332

    Article  Google Scholar 

  • Board of Water and Soil Resources (2016) Conservation lands summary. http://www.bwsr.state.mn.us/easements/CLS_Statewide_Summary.pdf. Accessed 27 Apr 2017

  • Bouzat J, Johnson J, Toepfer J, Simpson S, Esker T, Westmeier R (2009) Beyond the beneficial effects of translocations as an effective tool for the genetic restoration of isolated populations. Conserv Genet 10:191–201

    Article  Google Scholar 

  • Bowman TJ, Robel RJ (1977) Brood break-up, dispersal, mobility, and mortality of juvenile prairie chickens. J Wildl Manag 41:27–34

    Article  Google Scholar 

  • Braunisch V, Segelbacher G, Hirzel AH (2010) Modeling functional landscape connectivity from genetic population structure: a new spatially explicit approach. Mol Ecol 19:3664–3678

    Article  PubMed  Google Scholar 

  • Brown JH, Kodrick-Brown A (1977) Turnover rates in insular biogeography: effect of immigration and extinction. Ecology 58:445–449

    Article  Google Scholar 

  • Burnham KP, Anderson DR (1998) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New York

    Book  Google Scholar 

  • Caizergues A, Dubois S, Mondor G, Loiseau A, Ellison LN, Raspluss JY (2001) Isolation and characterization of microsatellite loci in black grouse (Tetrao tetrix). Mol Ecol Notes 1:36–38

    Article  CAS  Google Scholar 

  • Cheng HH, Levin I, Vallejo RL, Khatib H, Dodgson JB, Crittenden LB, Hille J (1995) Development of a genetic map of the chicken with markers of high utility. J Poult Sci 74:1855–1874

    Article  CAS  Google Scholar 

  • Connelly JW, Gratson MW, Reese KP (1998) Sharp-tailed Grouse (Tympanuchus phasianellus). In: Rodewald PG (ed) The birds of North America. Cornell Lab of Ornithology, Ithaca. Retrieved from the Birds of North America: https://birdsna.org/Species-Account/bna/species/shtgro https://doi.org/10.2173/bna.354

  • Cornuet JM, Luikart G (1997) Description and power analysis of two tests for detecting population bottlenecks from allele frequency data. Genetics 144:2001–2014

    Google Scholar 

  • Coulon A, Cosson JF, Angibault JM, Cargnelutti B, Galan M, Morellet N, Petit E, Aulagnier S, Hewison AJM (2004) Landscape connectivity influences gene flow in a roe deer population inhabiting a fragmented landscape: an individual-based approach. Mol Ecol 13:2841–2850

    Article  CAS  PubMed  Google Scholar 

  • Crooks KR, Burdett CL, Theobald DM, King SRB, Di Marco M, Rondinini C, Boitani L (2017) Quantification of habitat fragmentation reveals extinction risk in terrestrial mammals. Proc Nat Acad Sci 114:7635–7640

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cushman SA, McKelvey KS, Hayden J, Schwartz MK (2006) Gene flow in complex landscapes: testing multiple hypotheses with causal modeling. Am Nat 168:486–499

    Article  PubMed  Google Scholar 

  • D’Eon RG, Glenn SM, Parfitt I, Fortin MJ (2002) Landscape connectivity as a function of scale and organism vagility in a real forested landscape. Conserv Ecol 6:10

    Article  Google Scholar 

  • Donnelly JP, Tack JD, Doherty KE, Naugle DE, Allred BW, Dreitz VJ (2017) Extending conifer removal and landscape protection strategies from sage-grouse to songbirds, a range-wide assessment. Rangel Ecol Manag 70:95–105

    Article  Google Scholar 

  • Donovan TM, Welden CW (2002) Spreadsheet exercises in ecology and evolution. Sinauer Associates Inc., Sunderland, p 547

    Google Scholar 

  • Epps CW, Wehausen JD, Bleich VC, Torres SG, Brashares JS (2007) Optimizing dispersal and corridor models using landscape genetics. J Appl Ecol 44:714–724

    Article  Google Scholar 

  • Evett IW, Weir BS (1998) Interpreting DNA evidence: statistical genetics for forensic scientists. Sinauer, Sunderland

    Google Scholar 

  • Fotheringham AS, Brunsdon C, Charlton M (2002) Geographically weighted regression: the analysis of spatially varying relationships. Wiley, West Sussex

    Google Scholar 

  • Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, New York

    Book  Google Scholar 

  • Franklin J (2009) Mapping species distributions: spatial inference and prediction. Cambridge University Press, Cambridge, p 320

    Google Scholar 

  • Getis A, Ord JK (1992) The analysis of spatial association by use of distance statistics. Geogr Anal 24(3):189–206

    Article  Google Scholar 

  • Gilbert-Norton L, Wilson R, Stevens JR, Beard KH (2010) A meta-analytic review of corridor effectiveness. Conserv Biol 24:660–668

    Article  PubMed  Google Scholar 

  • Gregory AJ (2011) Landscape genetics and behavioral ecology of Greater Prairie-chickens (Tympanuchus cupido). PhD. Dissertation, Division of Biology, Kansas State University, Manhattan, KS

  • Guillot G, Santos F, Estoup A (2008) Analysing georeferenced population genetics data with Geneland: a new algorithm to deal with null alleles and a friendly graphical user interface. Bioinformatics 24:1406–1407

    Article  CAS  PubMed  Google Scholar 

  • Haddad N, Hudgens B, Damshen E, Levey D, Orrock J, Tewksbury JJ, Weldon A (2011) Assessing positive and negative ecological effects of corridors. In: Liu J, Hull V, Morzillo A, Wiens J (eds) Sources, sinks and sustainability. Cambridge University Press, Cambridge, pp 475–504

    Chapter  Google Scholar 

  • Haddad NM, Brudvig LA, Clobert J, Davies KF, Gonzalez A, Holt RD, Lovejoy TE, Sexton JO, Austin MP, Collins CD, Cook WM, Damschen EI, Ewers RM, Foster BL, Jenkins CN, King AJ, Laurance WF, Levey DJ, Margules CR, Melbourne BA, Nicholls AO, Orrock JL, Song DX, Townshend JR (2015) Habitat fragmentation and its lasting impact on Earth’s ecosystems. Sci Adv 1:e1500052

    Article  PubMed  PubMed Central  Google Scholar 

  • Haig SM, Bronaugh WM, Crowhurst RS, D’Elia J, Eagles-Smith CA, Epps CW, Knaus B, Miller MP, Moses ML, Oyler-McCance S, Robinson WD, Sidlauskas B (2011) Genetic applications in avian conservation. Auk 128:205–229

    Article  Google Scholar 

  • Halfman DA (2002) Natal dispersal of greater prairie-chickens in Wisconsin. MS Thesis. University of Wisconsin-Stevens Point

  • Hamerstrom FN, Hamerstrom F (1949) Daily and seasonal movements of Wisconsin prairie-chickens. Auk 66:313–337

    Article  Google Scholar 

  • Hamerstrom FN, Hamerstrom F (1973) The prairie chicken in Wisconsin. Wisconsin Department of Natural Resources Technical Bulletin No .64

  • Hanski IK (1998) Metapopulation dynamics. Nature 396:41–49

    Article  CAS  Google Scholar 

  • Hanski I (1999) Metapopulation ecology. Oxford University Press, New York

    Google Scholar 

  • Hartl DL, Clark AG (2007) Principles of population genetics. Sinauer Associates, Inc., Sunderland, p 652

    Google Scholar 

  • Hedrick PW (2005) Genetics of populations. Jones and Bartlett Publishers, Boston

    Google Scholar 

  • Hellerstein D, Malcolm S (2011) The influence of rising commodity prices on the Conservation Reserve Program. USDA, Economic Research Service, Economic Research Report No. 110

  • Herkert JR (2009) Response of bird populations to farmland set-aside programs. Conserv Biol 23:1036–1040

    Article  PubMed  Google Scholar 

  • Homer CG, Dewitz JA, Yang L, Jin S, Danielson P, Xian G, Coulston J, Herold ND, Wickham JD, Megown K (2015) Completion of the 2011 National Land Cover Database for the conterminous United States-representing a decade of land cover change information. Photogrammetric Engineering and Remote Sensing 81(5):345–354

    Google Scholar 

  • Johnson JA (2008) Recent range expansion and divergence among North American prairie-grouse. J Hered 99(2):165–173.

    Article  PubMed  Google Scholar 

  • Johnson JA, Schroeder MA, Robb LA (2011) Greater prairie-chicken (Tympanuchus cupido). In: Poole A (ed) The birds of North America, vol 36. The Cornell Lab of Ornithology, Ithaca

    Google Scholar 

  • Loiselle BA, Howell CA, Graham CH, Goerck JM, Brooks T, Smith KG, Williams PH (2003) Avoiding pitfalls of using species distribution models in conservation planning. Conserv Biol 17:1591–1600

    Article  Google Scholar 

  • Lowe WH, Allendorf FW (2010) What can genetics tell us about population connectivity? Mol Ecol 19:3038–3051

    Article  PubMed  Google Scholar 

  • MacArthur RH, Wilson EO (1967) The theory of island biogeography. Princeton University Press, Princeton

    Google Scholar 

  • Marschner FJ (1974) The original vegetation of Minnesota compiled from U.S. General Land Office survey noted by Francis Marschner [map]. St. Paul, MN: Redrafted from the original by P. J. Burwell and S. J. Haas under the direction of M. L. Heinselman. Northern Central Forest Experiment Station, USDA

  • McRae BH (2006) Isolation by resistance. Evolution 60:1551–1561

    Article  PubMed  Google Scholar 

  • McRae BH, Dickson BG, Keitt TH, Shah VB (2008) Using circuit theory to model connectivity in ecology, evolution, and conservation. Ecology 89:2712–2724

    Article  PubMed  Google Scholar 

  • Miller HJ (2004) Tobler’s first law of spatial analysis. Annals Assoc Am Geogr 94:284–289

    Article  Google Scholar 

  • Minnesota County Biological Survey (2010) Extent of Minnesota’s Native Prairie. 2008. Minnesota Department of Natural Resources, St. Paul, MN

  • Minnesota Prairie Plan Working Group (2011) Minnesota Prairie Conservation Plan. Minnesota Prairie Plan Working Group, Minneapolis, p 55

    Google Scholar 

  • Mönkkönen M, Reunanen P (1999) On critical thresholds in landscape connectivity: a management perspective. Oikos 84:302–305

    Article  Google Scholar 

  • Mussman SM, Douglas MR, Anthonysamy WJB, Davis MA, Simpson SA, Louis W, Douglas ME (2017) Genetic rescue, the Greater Prairie-chicken and the problem of conservation reliance in the Anthropocene. R Soc Open Sci 4:160736. https://doi.org/10.1098/rsos.160736

    Article  Google Scholar 

  • Niemuth ND (2011) Spatially explicit habitat models for prairie grouse. In: Sandercock BK, Martin K, Segelbacher G (eds) Ecology, conservation, and management of grouse. Studies in avian biology, vol 39. University of California Press, Berkeley, pp 3–20

    Google Scholar 

  • Oksanen JF, Guillaume B, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MH, Szoecs E, Maintainer HW (2016) R Package ‘vegan’. CRAN 2016-09-07 14:41:37

  • Oosterhout CV, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Res 4:535–538

    Google Scholar 

  • Paetkau D (2003) An empirical evaluation of data quality in DNA-based population inventories. Mol Ecol 12:1375–1387

    Article  CAS  PubMed  Google Scholar 

  • Paetkau D, Shields GF, Strobeck C (1998) Gene flow between insular, coastal and interior populations of brown bears in Alaska. Mol Ecol 7:1283–1292

    Article  CAS  PubMed  Google Scholar 

  • Peakal R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28:2537–2539

    Article  Google Scholar 

  • Peterjohn BG, Sauer JR (1999) Population status of North American grassland birds from the North American Breeding Bird Survey, 1966-1996. Stud Avian Biol 19:27–44

    Google Scholar 

  • Piertney SB, Dallas JF (1997) Isolation and characterization of hypervariable microsatellites in the red grouse (Lagopus lagopus scoticus). Mol Ecol 6:93–95

    Article  CAS  PubMed  Google Scholar 

  • Piertney SB, Höglund J (2001) Polymorphic microsatellite DNA markers in black grouse (Tetrao tetrix). Mol Ecol Notes 1:303–304

    Article  CAS  Google Scholar 

  • Pimm SL, Raven P (2000) Extinction by numbers. Nature 403:843–845

    Article  CAS  PubMed  Google Scholar 

  • Pither J, Taylor PD (1998) An experimental assessment of landscape connectivity. Oikos 83:166–174

    Article  Google Scholar 

  • Poiani KA, Merrill MD, Chapman KA (2001) Identifying conservation-priority areas in a fragmented Minnesota landscape based on the umbrella species concept and selection of large patches of natural vegetation. Conserv Biol 15:513–522

    Article  Google Scholar 

  • Pritchard JK, Stephans M, Donnelly P (2000) Inference of population structure using multi-locus genotype data. Genetics 155:945–959

    CAS  PubMed  PubMed Central  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Article  Google Scholar 

  • Roy C (2018) 2018 Minnesota Prairie-chicken Population Survey. Minnesota Department of Natural Resources Report, 9 pages. http://files.dnr.state.mn.us/recreation/hunting/prairiechicken/2018-survey.pdf

  • Samson FB, Knopf FL (1994) Prairie conservation in North America. Bioscience 44:418–421

    Article  Google Scholar 

  • Slatkin M (1993) Isolation by distance in equilibrium and non-equilibrium populations. Evolution 47:264–279

    Article  PubMed  Google Scholar 

  • Sork VL, Waits L (2010) Contributions of landscape genetics—approaches, insights, and future potential. Mol Ecol 19:3489–3495

    Article  PubMed  Google Scholar 

  • Spear SF, Balkenhol N, Fortin M, McRae BH, Scribner K (2010) Use of resistance surfaces for landscape genetic studies: considerations for parameterization and analysis. Mol Ecol 19:3576–3591

    Article  PubMed  Google Scholar 

  • Storfer A, Murphy MA, Evans JS, Goldberg CS, Robinson S, Spear SF, Dezzani R, Delmelle E, Vierling L, Waits LP (2007) Putting the ‘landscape’ in landscape genetics. Heredity 98:128–142

    Article  CAS  PubMed  Google Scholar 

  • Stubbs M (2014) Conservation Reserve Program (CRP): status and Issues. Congressional Research Service 7-5700 R42783. pp 20

  • Taylor PD, Fahrig L, Henein K, Merriam G (1993) Connectivity is a vital element of landscape structure. Oikos 68:571–572

    Article  Google Scholar 

  • Taylor SE, Oyler-McCance SJ, Quinn TW (2003) Isolation and characterization of microsatellite loci in greater sage-grouse (Centrocercus urophasianus). Mol Ecol Notes 3:262–264

    Article  CAS  Google Scholar 

  • Tischendorf L, Fahrig L (2000) How should we measure landscape connectivity? Landscape Ecol 15:633–641

    Article  Google Scholar 

  • Vogel JA, Shephard SE, Debinski DM (2015) An unexpected journey: greater Prairie-chicken travels nearly 4,000 km after translocation in Iowa. Am Midl Nat 174:343–349

    Article  Google Scholar 

  • Waples RS (2007) LDNE: a program for estimating effective population size from data on linkage disequilibrium. Mol Ecol Notes 7:167–184

    Google Scholar 

  • Waples RS, Peel LD, Macbeth GM, Tillett BJ, Ovenden JR (2014) NeEstimator v2:re-implementation of software for the estimation of contemporary effective population size (Ne) from genetic data. Mol Ecol Res 14:209–214

    Article  Google Scholar 

  • Washingon Wildlife Habitat connectivity Working Group (WHCWG) (2010) Washington Connected Landscape Project: statewide analysis. Washington Departments of Fish and Wildlife, and Transportation, Olympia, WA. http://wdfw.wa.gov/publications/01324/wdfw01324.pdf. Accessed 12 July 2017

  • Wilcove DS, Rothstein D, Dubow J, Phillips A, Losos E (1998) Quantifying threats to imperiled species in the United States. Bioscience 48:607–615

    Article  Google Scholar 

  • Wildlife Conservation Society—WCS, and Center for International Earth Science Information Network—CIESIN—Columbia University (2005) Last of the Wild Project, Version 2, 2005 (LWP-2): Global Human Footprint Dataset (Geographic). Palisades, NY: NASA Socioeconomic Data and Applications Center (SEDAC). http://dx.doi.org/10.7927/H4M61H5F. Accessed 16 Dec 2015

  • Wilson MC, Chen X, Corlett RT, Didham RK, Ding P, Holt RD, Holyoak M, Hu G, Hughes AC, Jiang L, Laurance WF, Liu J, Pimm SL, Robinson SK, Russo SE, Si X, Wilcove DS, Wu J, Yu M (2016) Habitat fragmentation and biodiversity conservation: key findings and future challenges. Landscape Ecol 31:219–227

    Article  Google Scholar 

  • With KA, Gardner RH, Turner MG (1997) Landscape connectivity and population distributions in heterogeneous environments. Oikos 78:151–169

    Article  Google Scholar 

  • Wright S (1943) Isolation by resistance. Genetics 28:114–138

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wu JG (2013) Key concepts and research topics in landscape ecology revisited: 30 years after the Allerton Park workshop. Landscape Ecol 28:1–11

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank E. Nelson of MNDNR for his assistance early on with project conception and for organizing hunter submissions. We would also like to thank cooperators involved with prairie-chicken surveys and feather collection efforts including MNDNR staff; cooperators with The Nature Conservancy; Minnesota Prairie Chicken Society, and the U.S. Fish and Wildlife Service; and numerous additional volunteers including S. Bommersbach, D. Svedarsky, D. Wells, T. Wolfe, J. Fejszes, K. Spaeth, T. Kucera, J. Forgit, and D. Hedtke. C. Wilson and S. Crosby collected prairie-chicken feathers in 2015. Wildlife Genetics International Lab completed genetic analyses. Finally, we would like to thank the hunters that submitted wings for this study. This project was funded in part by the Wildlife Restoration (Pittman-Robertson) Program Grant W-71-R-4. M. Larson and 4 anonymous reviewers provided helpful comments on this manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Charlotte L. Roy.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 319 kb)

Supplementary material 2 (DOCX 13 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Roy, C.L., Gregory, A.J. Landscape genetic evaluation of a tallgrass prairie corridor using the Greater Prairie-chicken (Tympanuchus cupido). Landscape Ecol 34, 1425–1443 (2019). https://doi.org/10.1007/s10980-019-00862-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10980-019-00862-3

Keywords

Navigation