Abstract
Maintaining habitat connectivity is crucial for maintaining genetic diversity and reducing the risk of inbreeding depression in numerous species. Human-modified habitats pose a threat to population persistence, particularly for amphibians that require both aquatic and terrestrial habitats and often exhibit low dispersal capacity. In this study, we investigated the genetic structure and variation of two sympatric newt species, Triturus cristatus and Lissotriton vulgaris, in an urbanized and agricultural landscape. Using a multiscale resistance modeling approach, we evaluated how landscape features affect gene flow in both species. Our results confirmed that the less abundant T. cristatus exhibited more genetically distinct demes than the more common L. vulgaris, which showed a more subtle structure. Additionally, levels of genetic variation were lower in T. cristatus than in L. vulgaris, but with a similar spatial distribution pattern across shared ponds. We found that the proportion of managed grassland in the study area played a major role in reducing the level of connectivity in both species. Furthermore, considering multiple spatial scales proved to be effective in improving the fit of the landscape resistance models, with the largest scale (900 m) providing the best fit. In T. cristatus, areas with low proportions of trees or high proportions of crop fields negatively affected genetic connectivity. Notably, resistance surfaces optimized for each species were highly correlated. The intensively managed grassland lacked the structural heterogeneity necessary for newts. Therefore, switching to a more traditional management approach in the landscape to increase spatial patchiness at the scale of dispersal would benefit both species.
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Data Availability
The genotypic data and non-smoothed rasters generated in this study are available in the Dryad Digital Repository https://doi.org/10.5061/dryad.bk3j9kdhz.
References
Allendorf FW, Luikart G, Aitken SN (2013) Genetics and the conservation of populations, 2nd edition edn. Wiley-Blackwell Publishing, Oxford, UK
Anderson CD, Epperson BK, Fortin M-J, Holderegger R, James PMA, Rosenberg MS, Scribner KT, Spear S (2010) Considering spatial and temporal scale in landscape-genetic studies of gene flow. Mol Ecol 19:3565–3575. https://doi.org/10.1111/j.1365-294X.2010.04757.x
Antunes B, Figueiredo-Vázquez C, Dudek K, Liana M, Pabijan M, Zieliński P, Babik W (2022) Landscape genetics reveals contrasting patterns of connectivity in two newt species (Lissotriton montandoni and L. vulgaris). Mol Ecol 00:1–16. https://doi.org/10.1111/mec.16543
Arntzen JW (2022) Coexistence of two newt species in a transition zone of range overlap. Contrib Zool 91:133–151. https://doi.org/10.1163/18759866-bja10028
Arntzen J, Teunis S (1993) A six year study on the population dynamics of the crested newt (Triturus cristatus) following the colonization of a newly created pond. Herpetol J 3:99–110
Arntzen JW, Abrahams C, Meilink WRM, Iosif R, Zuiderwijk A (2017) Amphibian decline, pond loss and reduced population connectivity under agricultural intensification over a 38 year period. Biodivers Conserv 26:1411–1430. https://doi.org/10.1007/s10531-017-1307-y
Baker JMR, Halliday TR (1999) Amphibian colonization of new ponds in an agricultural landscape. Herpetol J 9:55–63
Baker J, Beebee T, Buckley J, Gent T, Orchard D (2011) Amphibian habitat management handbook. Amphibian and reptile conservation, Bournemouth
Balkenhol N, Dudaniec RY, Krutovsky KV, Johnson JS, Cairns DM, Segelbacher G, Selkoe KA, von der Heyden S, Wang IJ, Selmoni O, Joost S (2019) Landscape genomics: understanding relationships between environmental heterogeneity and genomic characteristics of populations. In: Rajora OP (ed) Population genomics: concepts, approaches and applications. Springer International Publishing, Cham, pp 261–322. https://doi.org/10.1007/13836_2017_2
Bauder JM, Peterman WE, Spear SF, Jenkins CL, Whiteley AR, McGarigal K (2021) Multiscale assessment of functional connectivity: Landscape genetics of eastern indigo snakes in an anthropogenically fragmented landscape in central Florida. Mol Ecol 30:3422–3438. https://doi.org/10.1111/mec.15979
Brede EG, Beebee TJC (2004) Contrasting population structures in two sympatric anurans: implications for species conservation. Heredity 92:110–117. https://doi.org/10.1038/sj.hdy.6800391
Burkhart JJ, Peterman WE, Brocato ER, Romine KM, Willis MMS, Ousterhout BH, Anderson TL, Drake DL, Rowland FE, Semlitsch RD, Eggert LS (2017) The influence of breeding phenology on the genetic structure of four pond-breeding salamanders. Ecol Evol 7:4670–4681. https://doi.org/10.1002/ece3.3060
Cavalli-Sforza LL, Edwards AW (1967) Phylogenetic analysis. Models and estimation procedures. Am J Hum Genet 19:233–257
Cayuela H, Grolet O, Joly P (2018) Context-dependent dispersal, public information, and heterospecific attraction in newts. Oecologia 188:1069–1080. https://doi.org/10.1007/s00442-018-4267-3
Cayuela H, Schmidt BR, Weinbach A, Besnard A, Joly P (2019) Multiple density-dependent processes shape the dynamics of a spatially structured amphibian population. J Anim Ecol 88:164–177. https://doi.org/10.1111/1365-2656.12906
Clarke RT, Rothery P, Raybould AF (2002) Confidence limits for regression relationships between distance matrices: estimating gene flow with distance. J Agr Biol Envir St 7:361–372
Corander J, Marttinen P (2006) Bayesian identification of admixture events using multilocus molecular markers. Mol Ecol 15:2833–2843. https://doi.org/10.1111/j.1365-294X.2006.02994.x
Corander J, Marttinen P, Siren J, Tang J (2008a) Enhanced bayesian modelling in BAPS software for learning genetic structures of populations. BMC Bioinformatics 9:539. https://doi.org/10.1186/1471-2105-9-539
Corander J, Siren J, Arjas E (2008b) Bayesian spatial modeling of genetic population structure. Comput Stat 23:111–129. https://doi.org/10.1007/s00180-007-0072-x
Coster SS, Babbitt KJ, Cooper A, Kovach AI (2015) Limited influence of local and landscape factors on finescale gene flow in two pond-breeding amphibians. Mol Ecol 24:742–758. https://doi.org/10.1111/mec.13062
Cox K, Maes J, Van Calster H, Mergeay J (2017) Effect of the landscape matrix on gene flow in a coastal amphibian metapopulation. Conserv Genet. https://doi.org/10.1007/s10592-017-0985-z
Cox K, Denoël M, Van Calster H, Speybroeck J, Van de Poel S, Lewylle I, Verschaeve L, Van Breusegem A, Halfmaerten D, Adriaens D, Louette G (2021) Scale-dependent effects of terrestrial habitat on genetic variation in the great crested newt (Triturus cristatus). Landsc Ecol 36:3029–3048. https://doi.org/10.1007/s10980-021-01297-5
Cushman SA (2006) Effects of habitat loss and fragmentation on amphibians: a review and prospectus. Biol Conserv 128:231–240. https://doi.org/10.1016/j.biocon.2005.09.031
Cushman SA, McGarigal K (2004) Patterns in the species–environment relationship depend on both scale and choice of response variables. Oikos 105:117–124. https://doi.org/10.1111/j.0030-1299.2004.12524.x
De Troyer N, Eurie Forio MA, Roels K, De Meester L, Lemmens P, Declerck SAJ, Martens K, Goethals P (2020) Key management rules for agricultural alpine newt breeding ponds based on habitat suitability models. Global Ecol Conserv 23:e01086. https://doi.org/10.1016/j.gecco.2020.e01086
Denoël M (2012) Newt decline in Western Europe: highlights from relative distribution changes within guilds. Biodivers Conserv 21:2887–2898. https://doi.org/10.1007/s10531-012-0343-x
Denoël M, Ficetola GF (2008) Conservation of newt guilds in an agricultural landscape of Belgium: the importance of aquatic and terrestrial habitats. Aquat Conserv: Mar Freshwat Ecosyst 18:714–728. https://doi.org/10.1002/aqc.853
Denoël M, Perez A, Cornet Y, Ficetola GF (2013) Similar local and landscape processes affect both a common and a rare newt species. PLoS ONE 8:e62727. https://doi.org/10.1371/journal.pone.0062727
Denoël M, Dalleur S, Langrand E, Besnard A, Cayuela H (2018) Dispersal and alternative breeding site fidelity strategies in an amphibian. Ecography 41:1543–1555. https://doi.org/10.1111/ecog.03296
Dirzo R, Young HS, Galetti M, Ceballos G, Isaac NJB, Collen B (2014) Defaunation in the Anthropocene. Science 345:401–406. https://doi.org/10.1126/science.1251817
Dolmen D (1988) Coexistence and niche segregation in the newts. Amphibia-Reptilia 9:365–374. https://doi.org/10.1163/156853888X00044
Drechsler A, Geller D, Freund K, Schmeller DS, Künzel S, Rupp O, Loyau A, Denoël M, Valbuena-Ureña E, Steinfartz S (2013) What remains from a 454 run: estimation of success rates of microsatellite loci development in selected newt species (Calotriton asper, Lissotriton helveticus, and Triturus cristatus) and comparison with Illumina-based approaches. Ecol Evol 3:3947–3957. https://doi.org/10.1002/ece3.764
Dufresnes C, Perrin N (2015) Effect of biogeographic history on population vulnerability in European amphibians. Conserv Biol 29:1235–1241. https://doi.org/10.1111/cobi.12490
Edgar P, Bird DR (2006) Action plan for the conservation of the crested newt Triturus cristatus species complex in Europe. Council of the European Union, Strassbourg, Germany
Emel SL, Olson DH, Knowles LL, Storfer A (2019) Comparative landscape genetics of two endemic torrent salamander species, Rhyacotriton kezeri and R. variegatus: implications for forest management and species conservation. Conserv Genet 20:801–815. https://doi.org/10.1007/s10592-019-01172-6
Esri (2020) ArcGIS Desktop. Environmental Systems Research Institute, Redlands, CA
Frankham R, Briscoe DA, Ballou JD (2002) Introduction to conservation genetics. Cambridge University Press
Galpern P, Manseau M, Wilson P (2012) Grains of connectivity: analysis at multiple spatial scales in landscape genetics. Mol Ecol 21:3996–4009. https://doi.org/10.1111/j.1365-294X.2012.05677.x
Garcia-Gonzalez C, Campo D, Pola IG, Garcia-Vazquez E (2012) Rural road networks as barriers to gene flow for amphibians: species-dependent mitigation by traffic calming. Landsc Urban Plann 104:171–180. https://doi.org/10.1016/j.landurbplan.2011.10.012
Gauffre B, Boissinot A, Quiquempois V, Leblois R, Grillet P, Morin S, Picard D, Ribout C, Lourdais O (2022) Agricultural intensification alters marbled newt genetic diversity and gene flow through density and dispersal reduction. Mol Ecol 31:119–133. https://doi.org/10.1111/mec.16236
Goessens T, De Baere S, Deknock A, De Troyer N, Van Leeuwenberg R, Martel A, Pasmans F, Goethals P, Lens L, Spanoghe P, Vanhaecke L, Croubels S (2022) Agricultural contaminants in amphibian breeding ponds: occurrence, risk and correlation with agricultural land use. Sci Total Environ 806:150661. https://doi.org/10.1016/j.scitotenv.2021.150661
Goldberg C, Waits L (2010a) Comparative landscape genetics of two pond-breeding amphibian species in a highly modified agricultural landscape. Mol Ecol 19:3650–3663. https://doi.org/10.1111/j.1365-294X.2010.04673.x
Goldberg CS, Waits LP (2010b) Quantification and reduction of bias from sampling larvae to infer population and landscape genetic structure. Mol Ecol Resour 10:304–313. https://doi.org/10.1111/j.1755-0998.2009.02755.x
Goudet J, Jombart T (2021) hierfstat: Estimation and tests of hierarchical F-statistics. R package version 0.5–10, https://CRAN.R-project.org/package=hierfstat
Greenwald KR, Gibbs HL, Waite TA (2009a) Efficacy of land-cover models in predicting isolation of marbled salamander populations in a fragmented landscape. Conserv Biol 23:1232–1241. https://doi.org/10.1111/j.1523-1739.2009.01204.x
Greenwald KR, Purrenhage JL, Savage WK (2009b) Landcover predicts isolation in Ambystoma salamanders across region and species. Biol Conserv 142:2493–2500. https://doi.org/10.1016/j.biocon.2009.05.021
Gutiérrez-Rodríguez J, Gonçalves J, Civantos E, Martínez-Solano I (2017) Comparative landscape genetics of pond-breeding amphibians in Mediterranean temporal wetlands: the positive role of structural heterogeneity in promoting gene flow. Mol Ecol 26:5407–5420. https://doi.org/10.1111/mec.14272
Gutiérrez-Rodríguez J, Gonçalves J, Civantos E, Maia-Carvalho B, Caballero-Díaz C, Gonçalves H, Martínez-Solano Í (2022) The role of habitat features in patterns of population connectivity of two Mediterranean amphibians in arid landscapes of central Iberia. Landsc Ecol. https://doi.org/10.1007/s10980-022-01548-z
Hanski I (1998) Metapopulation dynamics. Nature 396:41–49. https://doi.org/10.1038/23876
Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620. https://doi.org/10.1046/j.1471-8286.2002.00305.x
Hartel T, Nemes S, Öllerer K, Cogălniceanu D, Moga C, Arntzen JW (2010) Using connectivity metrics and niche modelling to explore the occurrence of the northern crested newt Triturus cristatus (Amphibia, Caudata) in a traditionally managed landscape. Environ Conserv 37:195–200. https://doi.org/10.1017/S037689291000055X
Haugen H, Linløkken A, Østbye K, Heggenes J (2020) Landscape genetics of northern crested newt Triturus cristatus populations in a contrasting natural and human-impacted boreal forest. Conserv Genet 21:515–530. https://doi.org/10.1007/s10592-020-01266-6
Hijmans RJ (2022) terra: Spatial data analysis. R package version 1.5.21, https://CRAN.R-project.org/package=terra
Homola JJ, Loftin CS, Kinnison MT (2019) Landscape genetics reveals unique and shared effects of urbanization for two sympatric pool-breeding amphibians. Ecol Evol 9:11799–11823. https://doi.org/10.1002/ece3.5685
Ivanović A, Džukić G, Kalezić M (2012) A phenotypic point of view of the adaptive radiation of crested newts (Triturus cristatus superspecies, Caudata, Amphibia). Int J Evol Biol 2012:740605. https://doi.org/10.1155/2012/740605
Jackson ND, Fahrig L (2014) Landscape context affects genetic diversity at a much larger spatial extent than population abundance. Ecology 95:871–881. https://doi.org/10.1890/13-0388.1
Jackson HB, Fahrig L (2015) Are ecologists conducting research at the optimal scale? Global Ecol Biogeogr 24:52–63. https://doi.org/10.1111/geb.12233
Jehle R, Arntzen JW (2000) Post-breeding migrations of newts (Triturus cristatus and T. marmoratus) with contrasting ecological requirements. J Zool 251:297–306. https://doi.org/10.1111/j.1469-7998.2000.tb01080.x
Jehle R, Burke T, Arntzen JW (2005) Delineating fine-scale genetic units in amphibians: probing the primacy of ponds. Conserv Genet 6:227–234. https://doi.org/10.1007/s10592-004-7832-8
Jehle R, Thiesmeier B, Foster J (2011) The crested newt: a dwindling pond-dweller. Laurenti-Verlag, Bielefeld, Germany
Johanet A, Picard D, Garner TWJ, Dawson DA, Morales-Hojas R, Jehle R, Peltier D, Lemaire C (2009) Characterization of microsatellite loci in two closely related Lissotriton newt species. Conserv Genet 10:1903. https://doi.org/10.1007/s10592-009-9850-z
Johnson PTJ, Chase JM, Dosch KL, Hartson RB, Gross JA, Larson DJ, Sutherland DR, Carpenter SR (2007) Aquatic eutrophication promotes pathogenic infection in amphibians. P Natl Acad Sci USA 104:15781–15786. https://doi.org/10.1073/pnas.0707763104
Joly P, Miaud C, Lehmann A, Grolet O (2001) Habitat matrix effects on pond occupancy in newts. Conserv Biol 15:239–248. https://doi.org/10.1111/j.1523-1739.2001.99200.x
Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405. https://doi.org/10.1093/bioinformatics/btn129
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. https://doi.org/10.1038/hdy.2008.34
Karlsson T, Betzholtz PE, Malmgren JC (2007) Estimating viability and sensitivity of the great crested newt Triturus cristatus at a regional scale. Web Ecol 7:63–76. https://doi.org/10.5194/we-7-63-2007
Keenan K, McGinnity P, Cross TF, Crozier WW, Prodöhl PA (2013) diveRsity: an R package for the estimation and exploration of population genetics parameters and their associated errors. Methods Ecol Evol 4:782–788. https://doi.org/10.1111/2041-210X.12067
Kivimäki I, Shimbo M, Saerens M (2014) Developments in the theory of randomized shortest paths with a comparison of graph node distances. Phys A 393:600–616. https://doi.org/10.1016/j.physa.2013.09.016
Kovar R, Brabec M, Bocek R, Vita R (2009) Spring migration distances of some central european amphibian species. 30:367. https://doi.org/10.1163/156853809788795236
Krupa AP, Jehle R, Dawson DA, Gentle LK, Gibbs M, Arntzen J, Burke T (2002) Microsatellite loci in the crested newt (Triturus cristatus) and their utility in other newt taxa. Conserv Genet 3:87–89. https://doi.org/10.1023/A:1014239225553
Leyssen A, Scheers K, Smeekens V, Wils C, Packet J, De Knijf G, Denys L (2020) Watervlakken versie 1.1: polygonenkaart van stilstaand water in Vlaanderen. Uitgave 2020. Instituut voor Natuur- en Bosonderzoek, Brussels, Belgium. https://doi.org/10.21436/inbor.19088385
Libiger O, Nievergelt CM, Schork NJ (2009) Comparison of genetic distance measures using human SNP genotype data. Hum Biol 81:389–406. https://doi.org/10.3378/027.081.0401
Malmgren JC (2002) How does a newt find its way from a pond? Migration patterns after breeding and metamorphosis in great crested newts (Triturus cristatus) and smooth newts (T. vulgaris). Herpetol J 12:29–35
Manel S, Schwartz MK, Luikart G, Taberlet P (2003) Landscape genetics: combining landscape ecology and population genetics. Trends Ecol Evol 18:189–197. https://doi.org/10.1016/S0169-5347(03)00008-9
McCartney-Melstad E, Shaffer HB (2015) Amphibian molecular ecology and how it has informed conservation. Mol Ecol 24:5084–5109. https://doi.org/10.1111/mec.13391
McRae BH, Dickson BG, Keitt TH, Shah VB (2008) Using circuit theory to model connectivity in ecology, evolution, and conservation. Ecology 89:2712–2724. https://doi.org/10.1890/07-1861.1
Meehan ST (2013) IWT National smooth Newt Survey 2013 report. Dublin, Ireland
Miles LS, Rivkin LR, Johnson MTJ, Munshi-South J, Verrelli BC (2019) Gene flow and genetic drift in urban environments. Mol Ecol 28:4138–4151. https://doi.org/10.1111/mec.15221
Mims MC, Phillipsen IC, Lytle DA, Kirk EEH, Olden JD (2015) Ecological strategies predict associations between aquatic and genetic connectivity for dryland amphibians. Ecology 96:1371–1382. https://doi.org/10.1890/14-0490.1
Montano V, Jombart T (2017) An Eigenvalue test for spatial principal component analysis. BMC Bioinformatics 18:562. https://doi.org/10.1186/s12859-017-1988-y
Moor H, Bergamini A, Vorburger C, Holderegger R, Bühler C, Egger S, Schmidt BR (2022) Bending the curve: simple but massive conservation action leads to landscape-scale recovery of amphibians. P Natl Acad Sci USA 119:e2123070119. https://doi.org/10.1073/pnas.2123070119
Moran PAP (1948) The interpretation of statistical maps. J Roy Stat Soc Ser B (Stat Method) 10:243–251. https://doi.org/10.2307/2983777
Moran PAP (1950) Notes on continuous stochastic phenomena. Biometrika 37:17–23. https://doi.org/10.2307/2332142
Mulkeen CJ, Gibson-Brabazon S, Carlin C, Williams CD, Healy MG, Mackey P, Gormally MJ (2017) Habitat suitability assessment of constructed wetlands for the smooth newt (Lissotriton vulgaris [Linnaeus 1758]): A comparison with natural wetlands. Ecol Eng 106:532-540. https://doi.org/10.1016/j.ecoleng.2017.06.005
Müllner A (2001) Spatial patterns of migrating great crested newts and smooth newts: the importance of the terrestrial habitat surrounding the breeding pond. Rana 4:279–293
Nadachowska K, Flis I, Babik W, aw (2010) Characterization of microsatellite loci in the Carpathian newt (Lissotriton montandoni). Herpetol J 20:107–110
Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R² from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142. https://doi.org/10.1111/j.2041-210x.2012.00261.x
Newbold T, Hudson LN, Hill SLL, Contu S, Lysenko I, Senior RA, Börger L, Bennett DJ, Choimes A, Collen B, Day J, De Palma A, Díaz S, Echeverria-Londoño S, Edgar MJ, Feldman A, Garon M, Harrison MLK, Alhusseini T, Ingram DJ, Itescu Y, Kattge J, Kemp V, Kirkpatrick L, Kleyer M, Correia DLP, Martin CD, Meiri S, Novosolov M, Pan Y, Phillips HRP, Purves DW, Robinson A, Simpson J, Tuck SL, Weiher E, White HJ, Ewers RM, Mace GM, Scharlemann JPW, Purvis A (2015) Global effects of land use on local terrestrial biodiversity. Nature 520:45–50. https://doi.org/10.1038/nature14324
O’Brien D, Hall JE, Miró A, O’Brien K, Falaschi M, Jehle R (2021) Reversing a downward trend in threatened peripheral amphibian (Triturus cristatus) populations through interventions combining species, habitat and genetic information. J Nat Conserv 64:126077. https://doi.org/10.1016/j.jnc.2021.126077
O’Connell KA, Mulder KP, Maldonado J, Currie KL, Ferraro DM (2019) Sampling related individuals within ponds biases estimates of population structure in a pond-breeding amphibian. Ecol Evol 9:3620–3636. https://doi.org/10.1002/ece3.4994
Oldham RS, Keeble J, Swan MJS, Jeffcote M (2000) Evaluating the suitability of habitat for the great crested newt (Triturus cristatus). Herpetol J 10:143–155
Pebesma E (2018) Simple features for R: standardized support for spatial vector data. R J 10:439–446. https://doi.org/10.32614/RJ-2018-009
Peterman WE (2018) ResistanceGA: an R package for the optimization of resistance surfaces using genetic algorithms. Methods Ecol Evol 9:1638–1647. https://doi.org/10.1111/2041-210X.12984
Peterman WE, Locke JL, Semlitsch RD (2013) Spatial and temporal patterns of water loss in heterogeneous landscapes: using plaster models as amphibian analogues. Can J Zool 91:135–140. https://doi.org/10.1139/cjz-2012-0229
Peterman WE, Connette GM, Semlitsch RD, Eggert LS (2014) Ecological resistance surfaces predict fine-scale genetic differentiation in a terrestrial woodland salamander. Mol Ecol 23:2402–2413. https://doi.org/10.1111/mec.12747
Pimm SL, Jenkins CN, Abell R, Brooks TM, Gittleman JL, Joppa LN, Raven PH, Roberts CM, Sexton JO (2014) The biodiversity of species and their rates of extinction, distribution, and protection. Science 344:1246752. https://doi.org/10.1126/science.1246752
R Core Team (2021) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Radoux J, Bourdouxhe A, Coos W, Dufrêne M, Defourny P (2019) Improving ecotope segmentation by combining topographic and spectral data. Remote Sens 11:354. https://doi.org/10.3390/rs11030354
Rannap R, Briggs L (2006) The characteristics of great crested newt Triturus cristatus’ breeding ponds. Ministry of the Environment of the Republic of Estonia, Tallinn, Estonia
Rannap R, Lõhmus A, Briggs L (2009) Restoring ponds for amphibians: a success story. Hydrobiologia 634:87–95. https://doi.org/10.1007/s10750-009-9884-8
Rannap R, Lõhmus A, Linnamägi M (2012) Geographic variation in habitat requirements of two coexisting newt species in Europe. Acta Zool Acad Sci Hung 58:69–86
Revilla E, Wiegand T (2008) Individual movement behavior, matrix heterogeneity, and the dynamics of spatially structured populations. P Natl Acad Sci USA 105:19120–19125. https://doi.org/10.1073/pnas.0801725105
Richardson JL (2012) Divergent landscape effects on population connectivity in two co-occurring amphibian species. Mol Ecol 21:4437–4451. https://doi.org/10.1111/j.1365-294X.2012.05708.x
RStudio Team, RStudio (2021) RStudio: Integrated Development Environment for R. PBC, Boston, MA
Sánchez-Montes G, Wang J, Ariño AH, Martínez-Solano Í (2018) Mountains as barriers to gene flow in amphibians: quantifying the differential effect of a major mountain ridge on the genetic structure of four sympatric species with different life history traits. J Biogeogr 45:318–331. https://doi.org/10.1111/jbi.13132
Schmidt C, Garroway CJ (2021) The population genetics of urban and rural amphibians in North America. Mol Ecol 30:3918–3929. https://doi.org/10.1111/mec.16005
Schmidt P, Weddeling K, Thomas M, Rottscheidt R, Tarkhnishvili D, Hachtel M (2006) Dispersal of Triturus alpestris and T. vulgaris in agricultural landscapes–comparing estimates from allozyme markers and capture-mark-recapture analysis. Herpetologia Bonnensis 2:139–143
Scrucca L (2013) GA: A Package for genetic algorithms in R. J Stat Softw 53:1–37. https://doi.org/10.18637/jss.v053.i04
Segelbacher G, Cushman SA, Epperson BK, Fortin MJ, Francois O, Hardy OJ, Holderegger R, Taberlet P, Waits LP, Manel S (2010) Applications of landscape genetics in conservation biology: concepts and challenges. Conserv Genet 11:375–385. https://doi.org/10.1007/s10592-009-0044-5
Semlitsch RD (2008) Differentiating migration and dispersal processes for pond-breeding amphibians. J Wildl Manage 72:260–267. https://doi.org/10.2193/2007-082
Séré M, Thévenon S, Belem AMG, De Meeûs T (2017) Comparison of different genetic distances to test isolation by distance between populations. Heredity 119:55–63. https://doi.org/10.1038/hdy.2017.26
Sinsch U, Kirst C (2016) Homeward orientation of displaced newts (Triturus cristatus, Lissotriton vulgaris) is restricted to the range of routine movements. Ethol Ecol Evol 28:312–328. https://doi.org/10.1080/03949370.2015.1059893
Skei J, Ringsby T, Rønning L, Dolmen D (2006) Habitat use during the aquatic phase of the newts Triturus vulgaris (L.) and T. cristatus (Laurenti) in central Norway: proposition for a conservation and monitoring area. Amphibia-Reptilia 27:309–324. https://doi.org/10.1163/156853806778189972
Smith MA, Green DM (2005) Dispersal and the metapopulation paradigm in amphibian ecology and conservation: are all amphibian populations metapopulations? Ecography 28:110–128. https://doi.org/10.1111/j.0906-7590.2005.04042.x
Sotiropoulos K, Eleftherakos K, Tsaparis D, Kasapidis P, Magoulas A, Legakis A (2009) New polymorphic microsatellite loci for the greek smooth newt, Lissotriton vulgaris graecus, and their utility in the nominotypical subspecies. Mol Ecol Resour 9:292–295. https://doi.org/10.1111/j.1755-0998.2008.02245.x
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. https://doi.org/10.1007/s10592-013-0452-4
Speybroeck J, Beukema W, Bok B, Van Der Voort J, Velikov I (2016) Field guide to the amphibians and reptiles of Britain and Europe. Boomsbury Publishing, London
Storfer A, Murphy MA, Spear SF, Holderegger R, Waits LP (2010) Landscape genetics: where are we now? Mol Ecol 19:3496–3514. https://doi.org/10.1111/j.1365-294X.2010.04691.x
Thomas CD, Kunin WE (1999) The spatial structure of populations. J Anim Ecol 68:647–657. https://doi.org/10.1046/j.1365-2656.1999.00330.x
Unglaub B, Cayuela H, Schmidt BR, Preißler K, Glos J, Steinfartz S (2021) Context-dependent dispersal determines relatedness and genetic structure in a patchy amphibian population. Mol Ecol 30:5009–5028. https://doi.org/10.1111/mec.16114
Van Buskirk J (2005) Local and landscape influence on amphibian occurrence and abundance. Ecology 86:1936–1947. https://doi.org/10.1890/04-1237
Van Buskirk J (2012) Permeability of the landscape matrix between amphibian breeding sites. Ecol Evol 2:3160–3167. https://doi.org/10.1002/ece3.424
van Etten J (2017) R Package gdistance: distances and routes on geographical grids. J Stat Softw 76:1–21. https://doi.org/10.18637/jss.v076.i13
van Strien MJ, Keller D, Holderegger R, Ghazoul J, Kienast F, Bolliger J (2014) Landscape genetics as a tool for conservation planning: predicting the effects of landscape change on gene flow. Ecol Appl 24:327–339. https://doi.org/10.1890/13-0442.1
Vlaanderen AD (2014) Digitaal Hoogtemodel Vlaanderen II. Agentschap Digitaal Vlaanderen
Vlaanderen AD (2018) Orthofotomozaïek, middenschalig, zomeropnamen, 2018, Vlaanderen. Agentschap Digitaal Vlaanderen
Vuorio V, Tikkanen O-P, Mehtätalo L, Kouki J (2015) The effects of forest management on terrestrial habitats of a rare and a common newt species. Eur J Forest Res 134:377–388. https://doi.org/10.1007/s10342-014-0858-7
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370. https://doi.org/10.2307/2408641
Whiteley AR, McGarigal K, Schwartz MK (2014) Pronounced differences in genetic structure despite overall ecological similarity for two Ambystoma salamanders in the same landscape. Conserv Genet 15:573–591. https://doi.org/10.1007/s10592-014-0562-7
Wielstra B, Canestrelli D, Cvijanović M, Denoël M, Fijarczyk A, Jablonski D, Liana M, Naumov B, Olgun K, Pabijan M, Pezzarossa A, Popgeorgiev G, Salvi D, Si Y, Sillero N, Sotiropoulos K, Zieliński P, Babik W (2018) The distributions of the six species constituting the smooth newt species complex (Lissotriton vulgaris sensu lato and L. montandoni) – an addition to the New Atlas of Amphibians and Reptiles of Europe. Amphibia-Reptilia 39:252–259. https://doi.org/10.1163/15685381-17000128
Winiarski KJ, Peterman WE, McGarigal K (2020a) Evaluation of the R package ‘resistancega’: a promising approach towards the accurate optimization of landscape resistance surfaces. Mol Ecol Resour 20:1583–1596. https://doi.org/10.1111/1755-0998.13217
Winiarski KJ, Peterman WE, Whiteley AR, McGarigal K (2020b) Multiscale resistant kernel surfaces derived from inferred gene flow: an application with vernal pool breeding salamanders. Mol Ecol Resour 20:97–113. https://doi.org/10.1111/1755-0998.13089
Acknowledgements
We would like to thank R. Van Heghe, A. Martens, K. Van der Aa, K. Van Laer, N. Van Hoyweghen, L. Verschaeve, A. Vanden Broeck and S. Neyrinck for their assistance in sampling. We are grateful for the support of the municipal environmental services of Temse and Kruibeke and for their assistance in informing the owners of the ponds of the sampling campaign. Specifically, we want to thank J. Mortier and E. van Vlassenrode to grant us access to the Mercator high-voltage substation of Elia, J. De Laender for providing official permission to sample the ponds in the provincial park Roomacker, and De Vlaamse Waterweg and all the other owners that kindly allowed us to visit their grounds multiple times. Finally, we like to acknowledge Natuurpunt for sharing data on the occurrences of the species included in this study from waarnemingen.be and from the Hyla-database (INBODATAVR-173). The constructive comments of two anonymous reviewers greatly improved the manuscript.
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KC and RS conceived the study design. KC wrote the original draft. KC conducted the analyses. All authors conducted field work. AVB conducted laboratory work. All authors reviewed and edited the manuscript.
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The sampling permit ANB BL FF V19-00209-212 was provided by the Agency for Nature and Forest.
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Cox, K., Schepers, R., Van Breusegem, A. et al. The common ground in landscape effects on gene flow in two newt species in an agroecosystem. Conserv Genet 24, 807–826 (2023). https://doi.org/10.1007/s10592-023-01539-w
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DOI: https://doi.org/10.1007/s10592-023-01539-w