Advertisement

History matters: contemporary versus historic population structure of bobcats in the New England region, USA

Abstract

Habitat fragmentation and genetic bottlenecks can have substantial impacts on the health and management of wildlife species by lowering diversity and subdividing populations. Population genetic comparisons across time periods can help elucidate temporal changes in populations and the processes responsible for the changes. Bobcats (Lynx rufus) are wide-ranging carnivores and are currently increasing in abundance across an expanding range. Bobcat populations in New England have fluctuated in the past century in response to changes in their prey base, harvest pressure, and landscape development. We genotyped contemporary (2010–2017) and historic (1952–1964) bobcats from New England and Quebec, Canada at a suite of microsatellite loci and tested for differences in diversity, effective population size, and gene flow. Over 20 generations separated the sampling periods, and the intervening years were marked by drastic changes in land use and species management regimes. We found a general decrease in genetic diversity and differing population genetic structure through time. Effective population size decreased at the end of the historic period, coincident with a spike in harvest, but rebounded to greater numbers in the contemporary period. Our results suggest that bobcat populations in the region are robust, but development and range dynamics may play a significant role in population structure. Our study also highlights the benefits of a historical perspective in interpreting contemporary population genetic data.

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

Access options

Buy single article

Instant unlimited access to the full article PDF.

US$ 39.95

Price includes VAT for USA

Subscribe to journal

Immediate online access to all issues from 2019. Subscription will auto renew annually.

US$ 99

This is the net price. Taxes to be calculated in checkout.

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

References

  1. Anderson EM, Lovallo MJ (2003) Bobcat and Lynx. In: Feldhamer GA, Thompson BC, Chapman JA (eds) Wild mammals of North America: biology, management, and conservation, 2nd edn. Johns Hopkins University Press, Baltimore, pp 758–786

  2. Anderson CS, Prange S, Gibbs HL (2015) Origin and genetic structure of a recovering bobcat (Lynx rufus) population. Can J Zool 93:889–899

  3. Baigas PE, Squires JR, Olson LE et al (2017) Using environmental features to model highway crossing behavior of Canada lynx in the Southern Rocky Mountains. Landsc Urban Plan 157:200–213

  4. Beerli P (2013) Migrate documentation. Florida State University. http://popgen.sc.fsu.edu/migratedoc.pdf. Accessed 3 March 2018

  5. Beerli P, Felsenstein J (2001) Maximum likelihood estimation of a migration matrix and effective population sizes in n subpopulations by using a coalescent approach. Proc Natl Acad Sci USA 98:4563–4568

  6. Broman DJA, Litvaitis JA, Ellingwood M et al (2014) Modeling bobcat (Lynx rufus) habitat associations using telemetry locations and citizen-scientist observations: are the results comparable? Wildl Biol 20:229–237

  7. Burakowski EA, Wake CP, Braswell B et al (2008) Trends in wintertime climate in the northeastern United States: 1965–2005. J Geophys Res 113:JD009870

  8. Cambridge Systematics, Inc. (1994) New England Transportation Initiative. In: States of CT, ME, MA, NH, RI, VT, and the New England Governor’s conference

  9. Carmichael LE, Clark W, Strobeck C (2000) Development and characterization of microsatellite loci from lynx (Lynx canadensis), and their use in other felids. Mol Ecol 9:2155–2234

  10. Cobben MMP, Verboom J, Opdam PFM et al (2011) Projected climate change causes loss and redistribution of genetic diversity in a model metapopulation of a medium-good disperser. Ecography 34:920–932

  11. Coulon A, Fitzpatrick JW, Bowman R et al (2008) Congruent population structure inferred from dispersal behaviour and intensive genetic surveys of the threatened Florida scrub-jay (Aphelocoma cœrulescens). Mol Ecol 17:1685–1701

  12. Crooks KR (2002) Relative sensitivities of mammalian carnivores to habitat fragmentation. Conserv Biol 16:488–502

  13. Croteau EK, Heist EJ, Nielsen CK (2010) Fine-scale population structure and sex-biased dispersal in bobcats (Lynx rufus) from southern Illinois. Can J Zool 88:536–545

  14. de Meeûs T (2018) Revisiting FIS, FST, Wahlund effects, and null alleles. J Hered 109:446–456

  15. Dray S, Dufour AB (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22:1–20

  16. Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing Structure output and implementing the Evanno method. Conserv Genet Resour 4:359–361

  17. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:2611–2620

  18. Excoffier L, Foll M, Petit RJ (2009) Genetic consequences of range expansions. Annu Rev Ecol Evol Syst 40:481–501

  19. Faircloth BC, Reid A, Valentine T et al (2005) Tetranucleotide, trinucleotide, and dinucleotide loci from the bobcat (Lynx rufus). Mol Ecol Notes 5:387–389

  20. Farrell LE, Levy DM, Donovan T et al (2018) Landscape connectivity for bobcat (Lynx rufus) and lynx (Lynx canadensis) in the Northeastern United States. PLoS ONE 13:e0194243

  21. Foster DR, Motzkin G, Bernardos D, Cardoza J (2002) Wildlife dynamics in the changing New England landscape. J Biogeogr 29:1337–1357

  22. Green RE, Purcell KL, Thompson CM et al (2018) Reproductive parameters of the fisher (Pekania pennanti) in the southern Sierra Nevada, California. J Mammal 99:537–553

  23. Guillot G, Mortier F, Estoup A (2005) GENELAND: a computer package for landscape genetics. Mol Ecol Notes 5:712–715

  24. Hagen SB, Kopatz A, Aspi J et al (2015) Evidence of rapid change in genetic structure and diversity during range expansion in a recovering large terrestrial carnivore. Proc R Soc B 282:20150092

  25. Hansen K (2007) Bobcat: master of survival. Oxford University Press, New York

  26. Hewitt G (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907

  27. Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806

  28. Jombart T, Devillard S, Dufour A-B, Pontier D (2008) Revealing cryptic spatial patterns in genetic variability by a new multivariate method. Heredity 101:92–103

  29. Jorde PE, Ryman N (1995) Temporal allele frequency change and estimation of effective size in populations with overlapping generations. Genetics 139:1077–1090

  30. Kalinowski ST (2005) HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol Ecol Notes 5:187–189

  31. Koen EL, Bowman J, Murray DL, Wilson PJ (2014) Climate change reduces genetic diversity of Canada lynx at the trailing range edge. Ecography 37:754–762

  32. Kosterman MK, Squires JR, Holbrook JD et al (2018) Forest structure provides the income for reproductive success in a southern population of Canada lynx. Ecol Appl 28:1032–1043

  33. Lee EJ, Luedtke JG, Allison JL et al (2010) The effects of different maceration techniques on nuclear DNA amplification using human bone. J Forensic Sci 55:1032–1038

  34. Lee JS, Ruell EW, Boydston EE et al (2012) Gene flow and pathogen transmission among bobcats (Lynx rufus) in a fragmented urban landscape. Mol Ecol 21:1617–1631

  35. Li R, Liriano L (2011) A bone sample cleaning method using trypsin for the isolation of DNA. Leg Med 13:304–308

  36. Li R, Chapman S, Thompson M, Schwartz M (2009) Developing a simple method to process bone samples prior to DNA isolation. Leg Med 11:76–79

  37. Litvaitis JA (1993) Response of early successional vertebrates to historic changes in land use. Conserv Biol 7:866–873

  38. Litvaitis JA (2001) Importance of early successional habitats to mammals in eastern forests. Wildl Soc Bull 29:466–473

  39. Litvaitis JA, Tash JP (2008) An approach toward understanding wildlife-vehicle collisions. Environ Manag 42:688–697

  40. Litvaitis JA, Stevens CL, Mautz WW (1984) Age, sex, and weight of bobcats in relation to winter diet. J Wildl Manag 48:632–635

  41. Litvaitis JA, Tash JP, Stevens CL (2006) The rise and fall of bobcat populations in New Hampshire: relevance of historical harvests to understanding current patterns of abundance and distribution. Biol Conserv 128:517–528

  42. Litvaitis JA, Reed GC, Carroll RP et al (2015) Bobcats (Lynx rufus) as a model organism to investigate the effects of roads on wide-ranging carnivores. Environ Manag 55:1366–1376

  43. Lorimer CG (2001) Historical and ecological roles of disturbance in eastern North American forests: 9000 years of change. Wildl Soc Bull 29:425–439

  44. Luna C (1971) The handbook of transportation in America. Popular Library, New York

  45. Lynch GS, Kirby JD, Warren RJ, Conner LM (2008) Bobcat spatial distribution and habitat use relative to population reduction. J Wildl Manag 72:107–112

  46. Mahard TJ, Litvaitis JA, Tate P et al (2016) An evaluation of hunter surveys to monitor relative abundance of bobcats. Wildl Soc Bull 40:224–232

  47. Martinuzzi S, Stewart SI, Helmers DP et al (2015) The 2010 wildland–urban interface of the conterminous United States. U.S. Department of Agriculture, Forest Service, Northern Research Station. https://doi.org/10.2737/NRS-RMAP-8. Accessed 18 Sep 2015

  48. McRae BH, Beier P, Dewald LE et al (2005) Habitat barriers limit gene flow and illuminate historical events in a wide-ranging carnivore, the American puma. Mol Ecol 14:1965–1977

  49. Menotti-Raymond M, David VA, Lyons LA et al (1999) A genetic linkage map of microsatellites in the domestic cat (Felis catus). Genomics 57:9–23

  50. Menotti-Raymond MA, David VA, Wachter LL et al (2005) An STR forensic typing system for genetic individualization of domestic cat (Felis catus) samples. J Forensic Sci 50:1061–1070

  51. Millions DG, Swanson BJ (2007) Impact of natural and artificial barriers to dispersal on the population structure of bobcats. J Wildl Manag 71:96–102

  52. Nagylaki T (1985) Homozygosity, effective number of alleles, and interdeme differentiation in subdivided populations. Proc Natl Acad Sci USA 82:8611–8613

  53. Ordeñana MA, Crooks KR, Boydston EE et al (2010) Effects of urbanization on carnivore species distribution and richness. J Mammal 91:1322–1331

  54. Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Bioinformatics 28:2537–2539

  55. Peers MJL, Thornton DH, Murray DL (2013) Evidence for large scale effects of competition: niche displacement in Canada lynx and bobcat. Proc R Soc B 280:20132495

  56. Peery MZ, Kirby R, Reid BN et al (2012) Reliability of genetic bottleneck tests for detecting recent population declines. Mol Ecol 21:3403–3418

  57. Piry S, Luikart G, Cornuet J (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503

  58. Poessel SA, Burdett CL, Boydston EE et al (2014) Roads influence movement and home ranges of a fragmentation-sensitive carnivore, the bobcat, in an urban landscape. Biol Conserv 180:224–232

  59. Prange S, Gehrt SD, Wiggers EP (2004) Influences of anthropogenic resources on raccoon (Procyon lotor) movements and spatial distribution. J Mammal 85:483–490

  60. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

  61. R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/. Accessed 1 Jan 2019

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

  63. Reding DM, Bronikowski AM, Johnson WE, Clark WR (2012) Pleistocene and ecological effects on continental-scale genetic differentiation in the bobcat (Lynx rufus). Mol Ecol 21:3078–3093

  64. Reding DM, Carter CE, Hiller TL, Clark WR (2013a) Using population genetics for management of bobcats in Oregon. Wildl Soc Bull 37:342–351

  65. Reding DM, Cushman SA, Gosselink TE, Clark WR (2013b) Linking movement behavior and fine-scale genetic structure to model landscape connectivity for bobcats (Lynx rufus). Landsc Ecol 28:471–486

  66. Reed GC, Litvaitis JA, Callahan C et al (2016) Modeling landscape connectivity for bobcats using expert-opinion and empirically derived models: how well do they work? Anim Conserv 20:308–320

  67. Reid AE (2006) Spatial genetic structure of four bobcat populations in the southeastern US. Dissertation, University of Georgia

  68. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225

  69. Riley SPD, Sauvajot RM, Fuller TK et al (2003) Effects of urbanization and habitat fragmentation on bobcats and coyotes in southern California. Conserv Biol 17:566–576

  70. Riley SPD, Pollinger JP, Sauvajot RM et al (2006) A southern California freeway is a physical and social barrier to gene flow in carnivores. Mol Ecol 15:1733–1741

  71. Riley SPD, Boydston EE, Crooks KR, Lyren LM (2010) Bobcats (Lynx rufus). In: Gehrt SD, Riley SPD, Cypher BL (eds) Urban carnivores: ecology, conflict, and conservation. Johns Hopkins University Press, Baltimore, pp 121–138

  72. Roberts NM, Crimmins SM (2010) Bobcat population status and management in North America: evidence of large-scale population increase. J Fish Wildl Manag 1:169–174

  73. Ruell EW, Riley SPD, Douglas MR et al (2012) Urban habitat fragmentation and genetic population structure of bobcats in coastal southern California. Am Midl Nat 168:265–280

  74. Safner T, Miller MP, McRae BH et al (2011) Comparison of Bayesian clustering and edge detection methods for inferring boundaries in landscape genetics. Int J Mol Sci 12:865–889

  75. Samarasin P, Shuter BJ, Wright SI, Rodd FH (2017) The problem of estimating recent genetic connectivity in a changing world. Conserv Biol 31:126–135

  76. SAS Institute, Inc. (2016) JMP v13.0. SAS Institute, Inc., Cary

  77. Serieys LEK, Lea A, Pollinger JP et al (2014) Disease and freeways drive genetic change in urban bobcat populations. Evol Appl 8:75–92

  78. Seton ET (1925) Lives of game animals: cats, wolves, and foxes. Doubleday, Garden City

  79. Tigas LA, Van Vuren DH, Sauvajot RM (2002) Behavioral responses of bobcats and coyotes to habitat fragmentation and corridors in an urban environment. Biol Conserv 108:299–306

  80. Tucker MA, Böhning-Gaese K, Fagan WF et al (2018) Moving in the Anthropocene: global reductions in terrestrial mammalian movements. Science 359:466–469

  81. U.S. Census Bureau (2018) Quick facts. Retrieved from https://www.census.gov/quickfacts. Accessed 20 Mar 2019

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

  83. Waples RS, Do C (2008) LDNE: a program for estimating effective population size from data on linkage disequilibrium. Mol Ecol Resour 8:753–756. https://doi.org/10.1111/j.1755-0998.2007.02061.x

Download references

Acknowledgements

We thank Patrick Tate at New Hampshire Fish and Game Department, Chris Bernier at Vermont Fish and Wildlife Department, Laura Conlee and Susan McCarthy at Massachusetts Division of Fisheries and Wildlife, Eric Jaccard and Florent Lemieux at Quebec Ministry of Forests, Wildlife, and Parks, Tom Crews, and Randy Shoe for providing samples, as well as Brittaney Buchanan, Amanda Cugno, and Casey Coupe for assistance with sample processing. RPC was supported in part, by a National Science Foundation Graduate Research Fellowship (Grant Number 147766). Partial funding was provided by the New Hampshire Agricultural Experiment Station. This is Scientific Contribution Number 2799. This work is supported by the United States Department of Agriculture National Institute of Food and Agriculture McIntire-Stennis Projects (233076 and 1009906). The microsatellite datasets analyzed for this study are available in the Dryad Repository, https://datadryad.org/resource/doi:10.5061/dryad.t77f1p4.

Author information

Correspondence to Rory P. Carroll.

Additional information

Clark L. Stevens in memoriam.

Publisher’s Note

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

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Carroll, R.P., Litvaitis, M.K., Clements, S.J. et al. History matters: contemporary versus historic population structure of bobcats in the New England region, USA. Conserv Genet 20, 743–757 (2019). https://doi.org/10.1007/s10592-019-01170-8

Download citation

Keywords

  • Temporal genetics
  • Bottleneck
  • Fragmentation
  • Land use change
  • Wildlife management
  • Lynx rufus