Abstract
The strength and arrangement of movement barriers can impact the connectivity among habitat patches. Anthropogenic barriers (e.g. roads) are a source of habitat fragmentation that can disrupt these resource networks and can have an influence on the spatial genetic structure of populations. Using microsatellite data, we evaluated whether observed genetic structure of moose (Alces alces) populations were associated with human activities (e.g. roads) in the urban habitat of Anchorage and rural habitat on the Kenai Peninsula, Alaska. We found evidence of a recent genetic subdivision among moose in Anchorage that corresponds to a major highway and associated infrastructure. This subdivision is most likely due to restrictions in gene flow due to alterations to the highway (e.g. moose-resistant fencing with one-way gates) and a significant increase in traffic volume over the past 30 years; genetic subdivision was not detected on the Kenai Peninsula in an area not bisected by a major highway. This study illustrates that anthropogenic barriers can substructure wildlife populations within a few generations and highlights the value of genetic assessments to determine the effects on connectivity among habitat patches in conjunction with behavioral and ecological data.
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References
Alexander SM, Waters NM, Paquet PC (2005) Traffic volume and highway permeability for a mammalian community in the Canadian Rocky Mountains. Can Geogr 49:321–331
Allendorf FW, England PR, Luikart G, Ritchie PA, Ryman N (2008) Genetic effects of harvest on wild animal populations. TREE 23:327–337
Balkenhol N, Waits LP (2009) Molecular road ecology: exploring the potential of genetics for investigating transportation impacts on wildlife. Mol Ecol 18:4151–4164
Bangs EE, Duff SA, Bailey TN (1985) Habitat differences and moose use of two large burns on the Kenai Peninsula, Alaska. Alces 21:17–35
Bellis ED, Graves HB (1978) Highway fences as deterrents to vehicle-deer collisions. Transp Res Rec 674:53–58
Bennet A (1983) Management of forestland for moose browse production on Fort Richardson. U.S. Army, Fort Richardson, Anchorage
Beyer HL (2009) Geospatial modeling environment software. www.spatialecology.com/gme
Bishop MD, Kappes SM, Keele JW, Stone RT, Sunden SLF, Hawkins GA, Toldo SS, Fries R, Grosz MD, Yoo J, Beattie CW (1994) A genetic linkage map for cattle. Genetics 136:619–639
Bjørneraas K, Herfinal I, Solberg EJ, Sæther B, van Moorter B, Rolandsen CM (2012) Habitat quality influences population distribution, individual space use and functional responses in habitat selection by a large herbivore. Oecologia 168:231–243
Boucher TV, Mead BR (2006) Vegetation change and forest regeneration on the Kenai Peninsula, Alaska following a spruce beetle outbreak, 1987–2000. For Ecol Manag 227:233–246
Carnahan T (2010) Unit 14C moose management report. In: Harper P (ed) Moose management report of survey and inventory activities, 1 July 2007–30 June 2009. Alaska Dept of Fish and Game, Juneau, pp 190–207
Center for Environmental Excellence by the American Association of State Highway and Transportation Officials (2009) Decision guide. Step 2: identify solution and options. http://environment.transportation.org/environmental_issues/wildlife_roads/decision_guide/manual/2_1.aspx. Assessed 17 June 2014
Clark RW, Brown WS, Stechert R, Zamudio KR (2010) Roads, interrupted dispersal, and genetic diversity in timber rattlesnakes. Conserv Biol 24:1059–1069
Clevenger AP, Waltho N (2005) Performance indices to identify attributes of highway crossing structures facilitating movement of large mammals. Biol Conserv 121:453–464
Collins WB, Helm DJ (1997) Moose, Alces alces, habitat relative to riparian succession in the boreal forest, Susitna River, Alaska. Can Field Nat 111:567–574
Coster SS, Kovach AI (2012) Anthropogenic influences on the spatial genetic structure of black bears. Conserv Genet 13:1247–1257
Coulon A, Guillot G, Cosson J-F, Angibault JMA, Aulagnier S, Cargnelutti B, Galan M, Hewison AJM (2006) Genetic structure is influenced by landscape features: empirical evidence from a roe deer population. Mol Ecol 15:1669–1679
Crawford NG (2010) SMOGD: software for the measurement of genetic diversity. Mol Ecol Resour 10:556–557
Del Frate GG, Spraker TH (1991) Moose vehicle interactions and an associated public awareness program on the Kenai Peninsula, Alaska. Alces 27:1–7
Delany KS, Riley SPD, Fisher RN (2010) A rapid, strong, convergent genetic response to urban habitat fragmentation in four divergent and widespread vertebrates. PLoS One 5(9):e12767
Dray S, Dufour AB (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22:1–20
Epps CW, Palsbøll PJ, Wehausen JD, Roderick GK, Ramey RR II, McCullough DR (2005) Highways block gene flow and cause rapid decline in genetic diversity of desert bighorn sheep. Ecol Lett 8:1029–1038
Fahrig L, Rytwinski T (2009) Effects of roads on animal abundance: an empirical review and synthesis. Ecol Soc 14:21
Farley S, Barboza P, Griese H, Gardner C (2012) Characterization of moose movement patterns, movement of black bears in relation to anthropogenic food sources, and wolf distribution and movement on JBER lands, of Elmendorf AFB and Ft Richardson AP. Alaska Dept of Fish and Game Report, Juneau
Finnegan LA, Wilson PJ, Price GN, Lowe SJ, Patterson BR, Fortin M-J, Murray DL (2012) The complimentary role of genetic and ecological data in understanding population structure: a case study using moose (Alces alces). Eur J Wildl Res 58:415–423
Frantz AC, Hamann J, Klein F (2008) Fine-scale genetic structure of red deer (Cervus elaphus) in a French temperate forest. Eur J of Wildl Res 54:44–52
Gaillard J-M (2007) Are moose only a large deer?: some life history considerations. Alces 43:1–11
Garrett LC, Conway GA (1999) Characteristics of moose-vehicle collisions in Anchorage, Alaska, 1991–1995. J Saf Res 30:219–223
Gerlach G, Musolf K (2000) Fragmentation of landscape as a cause for genetic subdivision in bank voles. Conserv Biol 14:1066–1074
Girard I, Ouellet JP, Courtois R, Dussault C, Breton L (2002) Effects of sampling effort based on GPS telemetry on home-range size estimations. J Wildl Manag 66:1290–1300
Goudet J (1995) FSTAT (version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486
Guillot G (2008) Inference of structure in subdivided populations at low levels of genetic differentiation. The correlated allele frequencies model revisited. Bioinformatics 24:2222–2228
Guillot G, Santos F (2009) A computer program to simulate multilocus genotype data with spatially auto-correlated allele frequencies. Mol Ecol Resour 9:1112–1120
Guillot G, Mortier F, Estoup A (2005a) GENELAND: a computer package for landscape genetics. Mol Ecol Notes 5:708–711
Guillot G, Estoup A, Mortier F, Cosson JF (2005b) A spatial statistical model for landscape genetics. Genetics 170:1261–1280
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
Hale JM, Heard GW, Smith KL, Parris KM, Austin JJ, Kearney M, Melville J (2013) Structure and fragmentation of growling grass frog metapopulations. Conserv Genet 14:313–322
Hartmann SA, Steyer K, Kraus RHS, Segelbacher G, Nowak C (2013) Potential barriers to gene flow in the endangered European wildcat (Felis silvestris). Conserv Genet 14:413–426
Hedrick PW (1999) Perspective: highly variable loci and their interpretation in evolution and conservation. Evolution 53:313–318
Hedrick PW (2005) A standardized genetic measure. Evolution 59:1633–1638
Hepenstrick D, Thiel D, Holderegger R, Gugerli F (2012) Genetic discontinuities in roe deer (Capreolus capreolus) coincide with fenced transportation infrastructure. Basic Appl Ecol 13:631–638
Holderegger R, Di Giulio M (2010) The genetic effects of roads: a review of empirical evidence. Basic Appl Ecol 11:522–531
Holdo RM, Fryxell JM, Sinclair ARE, Dobson A, Holt RD (2011) Predicted impact of barriers to migration of the Serengeti wildebeest population. PLoS One 6:e16370
Jaarsma CF, Van Langevelde F, Botma H (2006) Flattened fauna and mitigation: traffic victims related to road, traffic, vehicle, and species characteristics. Transp Res Part D 11:264–276
Jaeger JAG, Bowman J, Brennan J, Fahrig L, Bert D, Bouchard J, Charbonneau N, Frank K, Gruber B, von Toschanowitz KT (2005) Predicting when animal populations are at risk from roads: an interactive model of road avoidance behavior. Ecol Model 185:329–348
Jensen JL, Bohonak AJ, Kelley ST (2005) Isolation by distance, web service. BMC Genetics 6:13. v.3.23 http://ibdws.sdsu.edu/
Jombart T (2008) Adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405
Jombart T (2013) A tutorial for the spatial analysis of principal components (sPCA) using adegenet 1.4-0. http://http://cran.r-project.org/web/packages/adegenet/vignettes/adegenet-spca.pdf
Jombart T, Ahmed I (2011) Adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. Bioinformatics 27:3070–3071
Jost L (2008) GST and its relatives do not measure differentiation. Mol Ecol 17:4015–4026
Keller I, Largiader CR (2003) Recent habitat fragmentation caused by major roads leads to reduction of gene flow and loss of genetic variability in ground beetles. Philos T Roy Soc B 270:417–423
Kuehn R, Hindenlang KE, Holzgang O, Senn J, Stoeckle B, Sperisen C (2007) Genetic effect of transportation infrastructure on Roe Deer populations (Capreolus capreolus). J Hered 98:13–22
Landguth EL, Cushman SA, Schwartz MK, McKelvey KS, Murphy M, Luikart G (2010) Quantifying the lag time to detect barriers in landscape genetics. Mol Ecol 19:4179–4191
Latch EK, Dharmarajan G, Glaubitz JC, Rhodes OE (2006) Relative performance of Bayesian clustering software for inferring population substructure and individual assignment at low levels of population differentiation. Conserv Genet 7:295–302
Latch EK, Boarman WI, Walde A, Fleischer RC (2011) Fine-scale analysis reveals cryptic landscape genetic structure in desert tortoises. PLoS One 6(11):e27794
Laurian C, Dussault C, Ouellet J-P, Courtois R, Poulin M (2012) Interactions between a large herbivore and a road network. EcoScience 19:69–79
Lee JS, Ruell EW, Boydston EE, Lyren LA, Alonso RS, Troyer JL, Crooks KR, VandeWoude S (2012) Gene flow and pathogen transmission among bobcat (Lynx rufus) in a fragmented urban landscape. Mol Ecol 21:1617–1631
Leveau LM (2013) Bird traits in urban-rural gradients: how many functional groups are there? J Ornithol 15:655–662
Long ES, Diefenbach DR, Wallingford BD, Rosenberry CS (2010) Influences of roads, rivers, and mountains on natal dispersal of white-tailed deer. J Wildl Manag 74:1242–1249
Loranger AJ, Bailey TN, Larned WW (1991) Effects of forest succession after fire in moose wintering habitats on the Kenai Peninsula, Alaska. Alces 27:100–109
McDonald M (1991) Moose movement and mortality associated with the Glenn Highway expansion, Anchorage, Alaska. Alces 27:208–219
Medrano JF, Aasen E, Sharrow L (1990) DNA extraction from nucleated red blood cells. Biotechniques 8:43
Meirmans PG (2006) Using the AMOVA framework to estimate a standardized genetic differentiation measure. Evolution 60:2399–2402
Miller JR, Hobbs RJ (2002) Conservation where people live and work. Conserv Biol 16:330–337
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
Mills KJ, Patterson BR, Murray DL (2006) Effects of variable sampling frequencies on GPS transmitter efficiency and estimated wolf home range size and movement distance. Wildl Soc B 34:1463–1469
Mohr CO (1947) Table of equivalent populations of North American small mammals. Am Mid Nat 37:223–249
Morton J (2012) Of moose and men. US Fish and Wildlife Service website. http://www.fws.gov/refuge/Kenai/community/2012_article/01272012.html. Accessed 25 July 2013
Mueller S, Berthoud G (1997) Fauna/traffic safety: manual for civil engineers. Ecole Polytechnique Federale de Lausanne, Department de genie civil. LAVOC, Lausanne
Noel S, Ouellet M, Galois P, Lapointe FJ (2007) Impact of urban fragmentation on the genetic structure of the eastern red-backed salamander. Conserv Genet 8:599–606
Noss RF, Quigley HB, Hornocker MG, Merrill T, Paquet PC (1996) Conservation biology and carnivore conservation in the Rocky Mountains. Conserv Biol 10:949–963
Nussey DH, Coltman DW, Coulson T, Kruuk LEB, Donald A, Morris SJ, Clutton-Brock TH, Pemberton J (2005) Rapidly declining fine-scale spatial structure in the female red deer. Mol Ecol 14:3395–3405
R Development Core Team, R (2011) R: a language and environment for statistical computing. Vienna, Austria. http://www.R-project.org
Reh W, Seitz A (1990) The influence of land use on the genetic structure of populations of the common frog Rana temporaria. Biol Conserv 54:239–249
Riley SPD, Pollinger JP, Sauvajot RW, York EC, Bromley C, Fuller TK, Wayne RK (2006) A southern California freeway is a physical and social barrier to gene flow in carnivores. Mol Ecol 15:1741–1773
Røed KH, Midthjell L (1998) Microsatellites in reindeer, Rangifer tarandus, and their use in other cervids. Mol Ecol 7:1773–1776
Roffler GH, Adams LG, Talbot SL, Sage GK, Dale BW (2012) Range overlap and individual movements during breeding season influence genetic relationships of caribou herds in southcentral Alaska. J Mamm 95:1318–1330
Rothe TC, Lanigan SH, Martin PA, Tande GF (1983) Natural resource inventory of Elmendorf Air Force Base, Alaska. Part II. Management recommendations. United States Department of the Interior, Fish and Wildlife Species Report, Anchorage
Row JR, Blouin-Demers G, Lougheed SC (2010) Habitat distribution influences dispersal and fine-scale genetic population structure of eastern foxsnakes (Mintonius gloydi) across a fragmented landscape. Mol Ecol 19:5157–5171
Rutledge LY, Garroway CJ, Loveless KM, Patterson BR (2010) Genetic differentiation of eastern wolves in Algonquin Park despite bridging gene flow between coyotes and grey wolves. Heredity 105:520–531
Schuster R, Römer H, Germain RR (2013) Using multi-scale distribution and movement effects along a montane highway to identify optimal crossing locations for a large-bodied mammal community. PeerJ 1:e189
Schwartz M, McKelvey K (2009) Why sampling scheme matters: the effect of sampling scheme on landscape genetic results. Conserv Genet 10:441–452
Seiler A, Cederlund G, Jernelid H, Grängstedt, Ringaby E (2003) The barrier effect of highway E4 on migratory moose (Alces alces) in the high coast area, Sweden. In Turcott E (ed) Proceedings of the IENE conference on ‘Habitat Fragmentation due to Transport Infrastructure’, 13–14 November 2003. Brussels, Belgium, pp 1–18
Selva N, Kreft S, Kati V, Schluck M, Jonsson B-G, Mihok B, Okarma H, Ibisch PL (2011) Roadless and low-traffic areas as conservation targets in Europe. Environ Manag 48:865–877
Sonsthagen SA, Talbot SL, White CM (2004) Gene flow and genetic characterization of Northern Goshawks breeding in Utah. Condor 106:826–836
Sotiropoulos K, Eleftherakos K, Tsaparis D, Kasapidis P, Giokas S, Legakis A, Kotoulas G (2013) Fine scale spatial genetic structure of two syntopic newts across a network of ponds: implications for conservation. Conserv Genet 14:385–400
Trombulak SC, Frissell CA (2000) Review of ecological effects of roads on terrestrial and aquatic communities. Conserv Biol 14:18–30
Unfried TM, Hauser L, Marzluff JM (2013) Effects of urbanization of Song Sparrow (Melospiza melodia) population connectivity. Conserv Genet 14:41–53
Upton GJG, Fingleton B (1985) Spatial data analysis by example. Wiley, New York
Wang M, Schreiber A (2001) The impact of habitat fragmentation and social structure on the population genetics of roe deer (Capreolus capreolus L.) in Central Europe. Heredity 86:703–715
Waples RS, Gaggiotti O (2006) What is a population? An empirical evaluation of some genetic methods for identifying the number of gene pools and their degree of connectivity. Mol Ecol 15:1419–1439
Wattles DW, DeStefano S (2013) Space use and movements of moose in Massachusetts: implications for conservation of large mammals in a fragmented environment. Alces 49:65–81
Welch J (2012) Movement of moose in a nutritional landscape. Thesis, University of Alaska Fairbanks
Wilson GA, Strobeck C, Wu L, Coffin JW (1997) Characterization of microsatellite loci in caribou Rangifer tarandus, and their use in other artiodactyls. Mol Ecol 6:697–699
Wright S (1955) Classification of the factors of evolution. Cold Spring Harb Symp Quant Biol 20:16–24
Yan E (2012) Annual traffic volume report: Central Region 2010–2011–2012. Alaska Dept of Transportation and Public Facilities Report
Acknowledgments
This work was funded by Joint Base Elmendorf-Richardson, under the guidance of Herman Griese, Christopher Garner, Dave Battle, and Richard Graham. The military conservation agent program on Elmendorf Air base, Joe Welch, and Anchorage area Alaska Fish and Game staff provided extensive field assistance in Anchorage. John Crouse, Jeff Selinger, and pilots Jose DeCreeft, Tommy Levanger, and Joe Fieldman provided field assistance on the Kenai Peninsula. Kevin Sage and Sarah Sonsthagen provided laboratory and manuscript advice, while Kris Hundertmark provided advice on marker selection and Tony Fischbach, Gretchen Roeffler, Matt Sexson, and Elizabeth Solomon provided help on analytical and mapping issues. Three anonymous reviewers also provided helpful comments. Use of trade or product names does not imply endorsement by the U.S. Government.
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Wilson, R.E., Farley, S.D., McDonough, T.J. et al. A genetic discontinuity in moose (Alces alces) in Alaska corresponds with fenced transportation infrastructure. Conserv Genet 16, 791–800 (2015). https://doi.org/10.1007/s10592-015-0700-x
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DOI: https://doi.org/10.1007/s10592-015-0700-x