Abstract
Landscape heterogeneity can influence animal dispersal by causing a directional bias in dispersal rate, as certain landscape configurations might promote, impede, or prevent movement and gene flow. In forested landscapes, logging operations often contribute to heterogeneity that can reduce functional connectivity for some species. American martens (Martes americana) are one such species, as they are considered specialists of late-seral coniferous forests. We assessed marten gene flow to test the hypothesis that habitat management has maintained landscape connectivity for martens in the managed forests of Ontario, Canada. We genotyped 653 martens at 12 microsatellite loci, sampled from 29 sites across Ontario. We expected that if forest management has an effect on marten gene flow, we would see a correlation between effective resistance, estimated by circuit theory, and genetic distance, estimated by population graphs. Although we found a positive relationship between effective resistance and genetic distance (Mantel r = 0.249, P < 0.001), marten gene flow was better described by isolation by Euclidean distance (Mantel r = 0.410, P < 0.001). Our results suggest that managed forests in Ontario are well connected for marten and neither impede nor promote marten gene flow at the provincial scale.
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References
Berg WE (1982) Reintroduction of fisher, pine marten, and river otter. In: Sanderson GC (ed) Midwest furbearer management. Proceedings of the 43rd midwest fish and wildlife conference, Wichita, Kansas, 1981
Bowman JC, Robitaille J-F (1997) Winter habitat use of American martens Martes americana within second-growth forest in Ontario, Canada. Wildl Biol 3:97–105
Bowman J, Robitaille J-F (2005) An assessment of expert-based marten habitat models used for forest management in Ontario. For Chron 81:801–807
Broquet T, Johnson CA, Petit E et al (2006a) Dispersal and genetic structure in the American marten, Martes americana. Mol Ecol 15:1689–1697
Broquet T, Ray N, Petit E et al (2006b) Genetic isolation by distance and landscape connectivity in the American marten (Martes americana). Landscape Ecol 21:877–889
Buskirk SW, Powell RA (1994) Habitat ecology of fishers and American martens. In: Buskirk SW, Harestad AS, Raphael MG, Powell RA (eds) Martens, sables, and fishers: biology and conservation. Cornell University Press, Ithaca, pp 283–296
Chapin TG, Harrison DJ, Katnik DD (1998) Influence of landscape pattern on habitat use by American marten in an industrial forest. Conserv Biol 12:1327–1337
Crawford NG (2010) SMOGD: software for the measurement of genetic diversity. Mol Ecol Resour 10:556–557
Cushman SA, Landguth EL (2010a) Scale dependent inference in landscape genetics. Landscape Ecol 25:967–979
Cushman SA, Landguth EL (2010b) Spurious correlations and inference in landscape genetics. Mol Ecol 19:3592–3602
Cushman SA, Lewis JS (2010) Movement behavior explains genetic differentiation in American black bears. Landscape Ecol 25:1613–1625
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
Cushman SA, Raphael MG, Ruggiero LF et al (2011) Limiting factors and landscape connectivity: the American marten in the Rocky Mountains. Landscape Ecol 26:1137–1149
Dallas JF, Piertney SB (1998) Microsatellite primers for the Eurasian otter. Mol Ecol 7:1248–1251
Davis CS, Strobeck C (1998) Isolation, variability, and cross-species amplification of polymorphic microsatellite loci in the family Mustelidae. Mol Ecol 7:1776–1778
de Vos A (1951) Overflow and dispersal of marten and fisher from wildlife refuges. J Wildl Manag 15:164–175
Driezen K, Adriaensen F, Rondinini C et al (2007) Evaluating least-cost model predictions with empirical dispersal data: a case study using radio tracking data of hedgehogs (Erinaceus europaeus). Ecol Model 209:314–322
Duffy AJ, Landa A, O’Connell M et al (1998) Four polymorphic microsatellites in wolverine, Gulo gulo. Anim Genet 29:63
Dyer RJ (2009) GeneticStudio: a suite of programs for spatial analysis of genetic-marker data. Mol Ecol Resour 9:110–113
Dyer RJ, Nason JD (2004) Population Graphs: the graph theoretic shape of genetic structure. Mol Ecol 13:1713–1727
Dyer RJ, Nason JD, Garrick RC (2010) Landscape modelling of gene flow: improved power using conditional genetic distance derived from the topology of population networks. Mol Ecol 19:3746–3759
Elkie PC, Hooper G, Carr AP, Rempel RS (1999) Ontario marten analyst and marten1 models: Directions for applying the forest management guidelines for the provision of marten habitat in the northwest region. Ontario Ministry of Natural Resources Northwest Science and Technology, Thunder Bay, Ontario, NWST TM-004
Elkie PC, Gluck M, Boos J, et al. (2009) Science and information in support of the forest management guide for landscapes: package “A” simulations, rationale, and inputs. Ontario Ministry of Natural Resources, Forest Policy Section
Fleming MA, Ostrander EA, Cook JA (1999) Microsatellite markers for American mink (Mustela vison) and ermine (Mustela erminea). Mol Ecol 8:1352–1354
Fuller AK, Harrison DJ (2005) Influence of partial timber harvesting on American martens in north-central Maine. J Wildl Manag 69:710–722
Garroway CJ, Bowman J, Carr D, Wilson PJ (2008) Applications of graph theory to landscape genetics. Evol Appl 1:620–630
Garroway CJ, Bowman J, Holloway GL et al (2011a) The genetic signature of rapid range expansion by flying squirrels in response to contemporary climate warming. Glob Change Biol 17:1760–1769
Garroway CJ, Bowman J, Wilson PJ (2011b) Using a genetic network to parameterize a landscape resistance surface. Mol Ecol 20:3978–3988
Hagmeier EM (1956) Distribution of marten and fisher in North America. Can Field Nat 70:101–148
Hargis CD, Bissonette JA (1997) Effects of forest fragmentation on populations of American marten in the intermountain west. In: Proulx G, Bryant HN, Woodard PM (eds) Martes: taxonomy, ecology, techniques, and management. Provincial Museum of Alberta, Edmonton, Alberta, pp 437–451
Hargis CD, Bissonette JA, Turner DL (1999) The influence of forest fragmentation and landscape pattern on American martens. J Appl Ecol 36:157–172
Holloway GL, Naylor BJ, Watt WR (2004) Habitat relationships of wildlife in Ontario. Revised habitat suitability models for the Great Lakes-St. Lawrence and Boreal East forests. Ontario Ministry of Natural Resources, Science and Information Branch, Southern Science and Information and Northeast Science and Information Joint Technical Report #1
Johnson CA (2008) Mammalian dispersal behaviour and its fitness correlates. Dissertation, University of Guelph
Johnson CA, Fryxell JM, Thompson ID, Baker JA (2009) Mortality risk increases with natal dispersal distance in American martens. Proc R Soc B 276:3361–3367
Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405
Jombart T, Devillard S, Dufour AB, Pontier D (2008) Revealing cryptic spatial patterns in genetic variability by a new multivariate method. Heredity 101:92–103
Jost L (2008) GST and its relatives do not measure differentiation. Mol Ecol 17:4015–4026
Koen EL, Garroway CJ, Wilson PJ, Bowman J (2010) The effect of map boundary on estimates of landscape resistance to animal movement. PLoS One 5(7):e11785
Krohn WB, Elowe KD, Boone RB (1995) Relations among fishers, snow, and martens: development and evaluation of two hypotheses. For Chron 71:97–105
Kyle CJ, Strobeck C (2003) Genetic homogeneity of Canadian mainland marten populations underscores the distinctiveness of Newfoundland pine martens (Martes americana atrata). Can J Zool 81:57–66
Legendre P, Fortin M-J (2010) Comparison of the Mantel test and alternative approaches for detecting complex multivariate relationships in the spatial analysis of genetic data. Mol Ecol Resour 10:831–844
Manel S, Schwartz MK, Luikart G, Taberlet P (2003) Landscape genetics: combining landscape ecology and population genetics. Trends Ecol Evol 18:189–197
Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220
McLaren MA, Thompson ID, Baker JA (1998) Selection of vertebrate wildlife indicators for monitoring sustainable forest management in Ontario. For Chron 74:241–248
McRae BH, Beier P (2007) Circuit theory predicts gene flow in plant and animal populations. Proc Natl Acad Sci USA 104:19885–19890
McRae BH, Shah VB (2009) Circuitscape user’s guide. http://www.circuitscape.org. Accessed Jan 2011
McRae BH, Dickson BG, Keitt TH, Shah VB (2008) Using circuit theory to model connectivity in ecology, evolution, and conservation. Ecology 89:2712–2724
Moran P (1948) The interpretation of statistical maps. J R Stat Soc B 10:243–251
Moran P (1950) Notes on continuous stochastic phenomena. Biometrika 37:17–23
Naylor B, Kaminski D, Bridge S, et al. (1999) User’s guide for OWHAM99 and OWHAMTool (Ver. 4.0). Ontario Ministry of Natural Resources, SCSS Technical Report. no. 54
O’Grady JJ, Brook BW, Reed DH et al (2006) Realistic levels of inbreeding depression strongly affect extinction risk in wild populations. Biol Conserv 133:42–51
Oksanen J, Kindt R, Legendre P et al (2009) Vegan: community ecology package. R package version 1.15-3. http://vegan.r-forge.r-project.org/. Accessed June 2009
Payer DC, Harrison DJ (2003) Influence of forest structure on habitat use by American marten in an industrial forest. For Ecol Manag 179:145–156
Perera AJ, Baldwin DJB (2001) Spatial patterns in the managed forest landscape of Ontario. In: Perera AH, Euler DL, Thompson ID (eds) Ecology of a managed terrestrial landscape: patterns and processes of forest landscapes in Ontario. Ontario Ministry of Natural Resources and UBC Press, Vancouver, British Columbia, pp 74–99
Perez-Espona S, Perez-Barberia FJ, McLeod JE et al (2008) Landscape features affect gene flow of Scottish Highland red deer (Cervus elaphus). Mol Ecol 17:981–996
Peterson RL, Crichton V (1949) The fur resources of Chapleau District, Ontario. Can J Res 27:68–84
Potvin F, Belanger L, Lowell K (2000) Marten habitat selection in a clearcut boreal landscape. Conserv Biol 14:844–857
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
R Development Core Team (2008) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org. Accessed Jan 2011
Raufaste N, Rousset F (2001) Are partial Mantel tests adequate? Evolution 55:1703–1705
Rousset F (2008) GENEPOP’007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Resour 8:103–106
Schwartz MK, Copeland JP, Anderson NJ et al (2009) Wolverine gene flow across a narrow climatic niche. Ecology 90:3222–3232
Shirk AJ, Wallin DO, Cushman SA et al (2010) Inferring landscape effects on gene flow: a new model selection framework. Mol Ecol 19:3603–3619
Short Bull RA, Cushman SA, Mace R et al (2011) Why replication is important in landscape genetics: American black bear in the Rocky Mountains. Mol Ecol 20:1092–1107
Spear SF, Balkenhol N, Fortin MJ et al (2010) Use of resistance surfaces for landscape genetic studies: considerations for parameterization and analysis. Mol Ecol 19:3576–3591
Storfer A, Murphy MA, Evans JS et al (2007) Putting the ‘landscape’ in landscape genetics. Heredity 98:128–142
Taylor PD, Fahrig L, Henein K, Merriam G (1993) Connectivity is a vital element of landscape structure. Oikos 68:571–573
Ter-Mikaelian MT, Columbo SJ, Chen J (2009) Estimating natural forest fire return interval in northeastern Ontario, Canada. For Ecol Manag 258:2037–2045
Thompson ID (2000) Forest vegetation of Ontario: factors influencing landscape change. In: Perera AH, Euler DL, Thompson ID (eds) Ecology of a managed terrestrial landscape: patterns and processes of forest landscapes in Ontario. Ontario Ministry of Natural Resources and UBC Press, Vancouver, British Columbia, pp 30–53
Thompson ID, Colgan PW (1987) Numerical responses of martens to a food shortage in northcentral Ontario. J Wildl Manag 51:824–835
Tully SM (2006) Habitat selection of fishers (Martes pennanti) in an untrapped refugium: Algonquin Provincial Park. Thesis, Trent University, Ontario, Canada
Vincent IR, Farid A, Otieno CJ (2003) Variability of thirteen microsatellite markers in American mink (Mustela vison). Can J Anim Sci 83:597–599
Voigt DR, Baker JA, Rempel RS, Thompson ID (2000) Forest vertebrate responses to landscape-level changes in Ontario. In: Perera AH, Euler DL, Thompson ID (eds) Ecology of a managed terrestrial landscape: patterns and processes of forest landscapes in Ontario. Ontario Ministry of Natural Resources and UBC Press, Vancouver, British Columbia, pp 198–233
Walker CW, Vila C, Landa A et al (2001) Genetic variation and population structure in Scandinavian wolverine (Gulo gulo) populations. Mol Ecol 10:53–63
Wasserman TN, Cushman SA, Schwartz MK, Wallin DO (2010) Spatial scaling and multi-modal inference in landscape genetics: Martes Americana in northern Idaho. Landscape Ecol 25:1601–1612
Watt WR, Baker JA, Hogg DM, et al. (1996) Forest management guidelines for the provision of marten habitat, version 1.0. Ontario Ministry of Natural Resources Forest Management Branch MNR#50908, Queens Printer for Ontario
Williams BW, Scribner KT (2010) Effects of multiple founder populations on spatial genetic structure of reintroduced American martens. Mol Ecol 19:227–240
Williams BW, Gilbert JH, Zollner PA (2007) Historical perspective on the reintroduction of the fisher and American marten in Michigan and Wisconsin. General Technical Report NRS-5. Newtown Square, PA: U.S. Department of Agriculture, Forest Service, Northern Research Station
Acknowledgments
We thank Linda Dix-Gibson and Lynn Landriault for providing marten genetic samples, and Taryne Chong and Vanessa Meunier for lab work. Funding was provided by NSERC (Discovery grants to JB and PJW, and scholarships to ELK and CJG), a Canada Research Chair to PJW, and the Ontario Ministry of Natural Resources. We thank Aaron A. Walpole and Laura M. Thompson for helpful discussions.
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Koen, E.L., Bowman, J., Garroway, C.J. et al. Landscape resistance and American marten gene flow. Landscape Ecol 27, 29–43 (2012). https://doi.org/10.1007/s10980-011-9675-2
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DOI: https://doi.org/10.1007/s10980-011-9675-2