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Fine-scale effects of habitat loss and fragmentation despite large-scale gene flow for some regionally declining woodland bird species

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Abstract

Habitat loss and associated fragmentation effects are well-recognised threats to biodiversity. Loss of functional connectivity (mobility, gene flow and demographic continuity) could result in population decline in altered habitat, because smaller, isolated populations are more vulnerable to extinction. We tested whether substantial habitat reduction plus fragmentation is associated with reduced gene flow in three ‘decliner’ woodland-dependent bird species (eastern yellow robin, weebill and spotted pardalote) identified in earlier work to have declined disproportionately in heavily fragmented landscapes in the Box-Ironbark forest region in north-central Victoria, Australia. For these three decliners, and one ‘tolerant’ species (striated pardalote), we compared patterns of genetic diversity, relatedness, effective population size, sex-ratios and genic (allele frequency) differentiation among landscapes of different total tree cover, identified population subdivision at the regional scale, and explored fine-scale genotypic (individual-based genetic signature) structure. Unexpectedly high genetic connectivity across the study region was detected for ‘decliner’ and ‘tolerant’ species. Power analysis simulations suggest that moderate reductions in gene flow should have been detectable. However, there was evidence of local negative effects of reduced habitat extent and structural connectivity: slightly lower effective population sizes, lower genetic diversity, higher within-site relatedness and altered sex-ratios (for weebill and eastern yellow robin) in 10 × 10 km ‘landscapes’ with low vegetation cover. We conclude that reduced structural connectivity in the Box-Ironbark ecosystem may still allow sufficient gene flow to avoid the harmful effects of inbreeding in our study species. Although there may still be negative consequences of fragmentation for demographic connectivity, the high genetic connectivity of mobile bird species in this system suggests that reconnecting isolated habitat patches may be less important than increasing habitat extent and/or quality if these need to be traded off.

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References

  • Amos JN, Bennett AF, Mac Nally R, Newell G, Pavlova A, Radford JQ, Thomson JR, White M, Sunnucks P (2012) Predicting landscape-genetic consequences of habitat loss, fragmentation and mobility for multiple species of woodland birds. PLoS ONE 7:e30888. doi:10.1371/journal.pone.0030888

  • Backström N, Fagerberg S, Ellegren H (2008) Genomics of natural bird populations: a gene-based set of reference markers evenly spread across the avian genome. Mol Ecol 17(4):964–980

    Article  PubMed  Google Scholar 

  • Balloux F (2001) EASYPOP (version 1.7): a computer program for population genetics simulations. J Hered 92(3):301–302

    Article  PubMed  CAS  Google Scholar 

  • Banks SC, Piggott MP, Stow AJ, Taylor AC (2007) Sex and sociality in a disconnected world: a review of the impacts of habitat fragmentation on animal social interactions. Can J Zool 85(10):1065–1079

    Article  Google Scholar 

  • Barnett JR, Ruiz-Gutierrez V, Coulon A, Lovette IJ (2008) Weak genetic structuring indicates ongoing gene flow across White-ruffed Manakin (Corapipo altera) populations in a highly fragmented Costa Rica landscape. Conserv Genet 9(6):1403–1412

    Article  Google Scholar 

  • Bennett AF, Radford JQ (2009) Thresholds, incidence functions, and species-specific cues : responses of woodland birds to landscape structure in south-eastern Australia. In: Villard M, Jonsson BG (eds) Setting conservation targets for managed forest landscapes. Cambridge University Press, New York, pp 161–184

    Google Scholar 

  • Bennett AF, Radford JQ, Haslem A (2006) Properties of land mosaics: implications for nature conservation in agricultural environments. Biol Conserv 133(2):250–264

    Article  Google Scholar 

  • Broquet T, Petit EJ (2009) Molecular estimation of dispersal for ecology and population genetics. Annu Rev Ecol Evol Syst 40:193–216

    Article  Google Scholar 

  • Brown JH, Kodric-Brown A (1977) Turnover rates in insular biogeography: effect of immigration on extinction. Ecology 48:445–449

    Article  Google Scholar 

  • Callens T, Galbusera P, Matthysen E, Durand EY, Githiru M, Huyghe JR, Lens L (2011) Genetic signature of population fragmentation varies with mobility in seven bird species of a fragmented Kenyan cloud forest. Mol Ecol 20(9):1829–1844

    Article  PubMed  Google Scholar 

  • Caughley G (1994) Directions in conservation biology. J Anim Ecol 63(2):215–244

    Article  Google Scholar 

  • Chen C, Durand E, Forbes F, Francois O (2007) Bayesian clustering algorithms ascertaining spatial population structure: a new computer program and a comparison study. Mol Ecol Notes 7(5):747–756

    Article  Google Scholar 

  • Cooper CB, Walters JR (2002) Experimental evidence of disrupted dispersal causing decline of an Australian passerine in fragmented habitat. Conserv Biol 16(2):471–478

    Article  Google Scholar 

  • Cooper CB, Walters JR, Priddy J (2002) Landscape patterns and dispersal success: simulated population dynamics in the brown treecreeper. Ecol Appl 12(6):1576–1587

    Article  Google Scholar 

  • Coulon A, Fitzpatrick JW, Bowman R, Lovette IJ (2010) Effects of habitat fragmentation on effective dispersal of florida scrub-jays. Conserv Biol 24(4):1080–1088

    Article  PubMed  Google Scholar 

  • Debus SJS (2006) Breeding and population parameters of robins in a woodland remnant in northern New South Wales, Australia. Emu 106(2):147–156

    Article  Google Scholar 

  • Delaney KS, Riley SPD, Fisher RN (2010) A rapid, strong, and convergent genetic response to urban habitat fragmentation in four divergent and widespread vertebrates. PLoS ONE 5(9):e12767

    Article  PubMed  Google Scholar 

  • Doerr VAJ, Doerr ED, Davies MJ (2011) Dispersal behaviour of Brown Treecreepers predicts functional connectivity for several other woodland birds. Emu 111(1):71–83

    Article  Google Scholar 

  • ECC (2001) Box-ironbark forests and woodlands investigation final report. East Melbourne, Environment Conservation Council

  • Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: Linked loci and correlated allele frequencies. Genetics 164(4):1567–1587

    PubMed  CAS  Google Scholar 

  • Foley JA (2005) Global consequences of land use. Science 309(5734):570

    Article  PubMed  CAS  Google Scholar 

  • Ford HA (2011) The causes of decline of birds of eucalypt woodlands: advances in our knowledge over the last 10 years. Emu 111(1):1–9

    Article  Google Scholar 

  • Ford HA, Walters JR, Cooper CB, Debus SJS, Doerr VAJ (2009) Extinction debt or habitat change?—Ongoing losses of woodland birds in north-eastern New South Wales, Australia. Biol Conserv 142(12):3182–3190

    Article  Google Scholar 

  • Gerlach G, Jueterbock A, Kraemer P, Deppermann J, Harmand P (2010) Calculations of population differentiation based on GST and D: forget GST but not all of statistics! Mol Ecol 19(18):3845–3852

    Article  PubMed  Google Scholar 

  • Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3)

  • Griffiths R, Double MC, Orr K, Dawson RJG (1998) A DNA test to sex most birds. Mol Ecol 7(8):1071–1075

    Article  PubMed  CAS  Google Scholar 

  • Hanski I, Gilpin ME (eds) (1997) Metapopulation biology: ecology, genetics and evolution. Academic Press, San Diego

    Google Scholar 

  • Hansson B, Bensch S, Hasselquist D (2004) Lifetime fitness of short- and long-distance dispersing great reed warblers. Evolution 58(11):2546–2557

    PubMed  Google Scholar 

  • Harrison S (1991) Local extinction in a metapopulation context: an empirical evaluation. Biol J Linnean Soc 42:73–88

    Article  Google Scholar 

  • Hedrick PW (2005) A standardized genetic differentiation measure. Evolution 59(8):1633–1638

    PubMed  CAS  Google Scholar 

  • Higgins PJ, Peter JM (eds) (2002) Handbook of Australian, New Zealand and Antarctic birds, vol 6: Pardalotes to Shrike-thrushes. Oxford University Press, Melbourne

  • Jost L (2008) G(ST) and its relatives do not measure differentiation. Mol Ecol 17(18):4015–4026

    Article  PubMed  Google Scholar 

  • Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16(5):1099–1106

    Article  PubMed  Google Scholar 

  • Lada H, Mac Nally R, Taylor AC (2008) Distinguishing past from present gene flow along and across a river: the case of the carnivorous marsupial (Antechinus flavipes) on southern Australian floodplains. Conserv Genet 9(3):569–580

    Article  Google Scholar 

  • Landguth EL, Cushman SA (2010) CDPOP: an individual-based, cost-distance spatial population genetics model. Mol Ecol Resour 10:156–161

    Article  PubMed  CAS  Google Scholar 

  • 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(19):4179–4191

    Article  Google Scholar 

  • Lowe WH, Allendorf FW (2010) What can genetics tell us about population connectivity? Mol Ecol 19(15):3038–3051

    Article  PubMed  Google Scholar 

  • Mac Nally R, Bennett AF, Thomson JR, Radford JQ, Unmack G, Horrocks G, Vesk PA (2009) Collapse of an avifauna: climate change appears to exacerbate habitat loss and degradation. Divers Distrib 15(4):720–730

    Article  Google Scholar 

  • Mills LS, Allendorf FW (1996) The one-migrant-per-generation rule in conservation and management. Conserv Biol 10(6):1509–1518

    Article  Google Scholar 

  • Mylecraine KA, Bulgin NL, Gibbs HL, Vickery PD, Perkins DW (2008) Limited genetic structure and evidence for dispersal among populations of the endangered Florida grasshopper sparrow, Ammodramus savannarum floridanus. Conserv Genet 9(6):1633–1638

    Article  Google Scholar 

  • Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6(1):288–295

    Article  Google Scholar 

  • Peakall R, Ruibal M, Lindenmayer DB (2003) Spatial autocorrelation analysis offers new insights into gene flow in the Australian bush rat, Rattus fuscipes. Evolution 57(5):1182–1195

    PubMed  Google Scholar 

  • Peery MZ, Hall LA, Sellas A, Beissinger SR, Moritz C, Berube M, Raphael MG, Nelson SK, Golightly RT, McFarlane-Tranquilla L, Newman S, Palsboll PJ (2010) Genetic analyses of historic and modern marbled murrelets suggest decoupling of migration and gene flow after habitat fragmentation. Proc R Soc B 277(1682):697–706

    Article  PubMed  CAS  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155(2):945–959

    PubMed  CAS  Google Scholar 

  • Pulliam HR (1988) Sources, sinks, and population regulation. Am Naturalist 132:652–661

    Article  Google Scholar 

  • Queller DC, Goodnight KF (1989) Estimating relatedness using genetic-markers. Evolution 43(2):258–275

    Article  Google Scholar 

  • R Development Core Team (2009) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Radford JQ, Bennett AF (2007) The relative importance of landscape properties for woodland birds in agricultural environments. J Appl Ecol 44(4):737–747

    Article  Google Scholar 

  • Radford JQ, Bennett AF, Cheers GJ (2005) Landscape-level thresholds of habitat cover for woodland-dependent birds. Biol Conserv 124(3):317–337

    Article  Google Scholar 

  • Robertson OJ, Radford JQ (2009) Gap-crossing decisions of forest birds in a fragmented landscape. Aust Ecol 34(4):435–446

    Google Scholar 

  • Rogers K, Rogers A, Rogers D (1986) Bander’s aid: a guide to ageing and sexing bush birds. St. Andrews, Victoria

  • Rousset F (2008) GENEPOP ‘ 007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Resour 8(1):103–106

    Article  PubMed  Google Scholar 

  • Saunders DA, Hobbs RJ, Margules CR (1991) Biological consequences of ecosystem fragmentation—a review. Conserv Biol 5(1):18–32

    Article  Google Scholar 

  • Segelbacher G, Cushman SA, Epperson BK, Fortin M-J, 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

    Article  Google Scholar 

  • Shanahan DF, Possingham HP, Riginos C (2011) Models based on individual level movement predict spatial patterns of genetic relatedness for two Australian forest birds. Landscape Ecol 26(1):137–148

    Article  Google Scholar 

  • Smouse PE, Peakall R, Gonzales E (2008) A heterogeneity test for fine-scale genetic structure. Mol Ecol 17(14):3389–3400

    Article  PubMed  Google Scholar 

  • Spielman D, Brook BW, Frankham R (2004) Most species are not driven to extinction before genetic factors impact them. Proc Natl Acad Sci USA 101(42):15261–15264

    Article  PubMed  CAS  Google Scholar 

  • Stow AJ, Sunnucks P (2004) Inbreeding avoidance in Cunningham’s skinks (Egernia cunninghami) in natural and fragmented habitat. Mol Ecol 13(2):443–447

    Article  PubMed  CAS  Google Scholar 

  • Sunnucks P (2000) Efficient genetic markers for population biology. Trends Ecol Evol 15(5):199–203

    Article  PubMed  Google Scholar 

  • Sunnucks P (2011) Towards modelling persistence of woodland birds: the role of genetics. Emu 111(1):19–39

    Article  Google Scholar 

  • Tallmon DA, Koyuk A, Luikart G, Beaumont MA (2008) ONeSAMP: a program to estimate effective population size using approximate Bayesian computation. Mol Ecol Resour 8(2):299–301

    Article  PubMed  Google Scholar 

  • Taylor PD, Fahrig L, Henein K, Merriam G (1993) Connectivity is a vital element of landscape structure. Oikos 69:571–573

    Article  Google Scholar 

  • Veit ML, Robertson RJ, Hamel PB, Friesen VL (2005) Population genetic structure and dispersal across a fragmented landscape in cerulean warblers (Dendroica cerulea). Conserv Genet 6(2):159–174

    Article  Google Scholar 

  • Villard M-A, Jonsson BG (eds) (2009) Setting conservation targets for managed forest landscapes. Cambridge University Press, New York

    Google Scholar 

  • Walker FM, Sunnucks P, Taylor AC (2008) Evidence for habitat fragmentation altering within-population processes in wombats. Mol Ecol 17(7):1674–1684

    Article  PubMed  Google Scholar 

  • Watson JEM, Whittaker RJ, Freudenberger D (2005) Bird community responses to habitat fragmentation: how consistent are they across landscapes? J Biogeogr 32(8):1353–1370

    Article  Google Scholar 

  • Wiens JA (2001) The landscape context of dispersal. In: Clobert J, Danchin E, Dhondt AA, Nichols JD (eds) Dispersal. Oxford University Press, Oxford, pp 96–109

    Google Scholar 

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Acknowledgments

Funding was provided by the Australian Research Council Linkage Grant (LP0776322), the Victorian Department of Sustainability and Environment (DSE), Museum of Victoria, Victorian Department of Primary Industries, Parks Victoria, North Central Catchment Management Authority, and Goulburn Broken Catchment Management Authority. Birds Australia contributed towards NA’s PhD stipend, and Monash University Science Faculty funded a Dean’s Scholarship. We thank Holsworth Wildlife Research Endowment for valuable support to NA. Samples were collected under DSE permit number 10004294 under the Wildlife Act 1975 and the National Parks Act 1975, DSE permit number NWF10455 under section 52 of the forest Act 1958 and the Australian Bird and Bat Banding Scheme permit under approval and monitoring of Monash University ethics processes (BSCI/2007/07). We thank all the volunteers for the Birds Linkage project for assistance with fieldwork, and other Birds Linkage team members for diverse inputs. Jian Yen and three anonymous referees provided very helpful comments on drafts. Computationally intensive analyses (Structure and TESS) were performed on Monash Sun Grid.

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  1. James Q. Radford

    Present address: Bush Heritage Australia, 329, Flinders Lane, Melbourne, VIC, 8009, Australia

Authors and Affiliations

  1. School of Biological Sciences and Australian Centre for Biodiversity, Monash University, Clayton Campus, Melbourne, VIC, 3800, Australia

    Katherine A. Harrisson, Alexandra Pavlova, J. Nevil Amos, Naoko Takeuchi, Alan Lill & Paul Sunnucks

  2. Landscape Ecology Research Group, School of Life and Environmental Sciences, Deakin University, 221 Burwood Hwy, Burwood, VIC, 3125, Australia

    James Q. Radford

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  1. Katherine A. Harrisson
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  2. Alexandra Pavlova
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  3. J. Nevil Amos
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Correspondence to Katherine A. Harrisson.

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Harrisson, K.A., Pavlova, A., Amos, J.N. et al. Fine-scale effects of habitat loss and fragmentation despite large-scale gene flow for some regionally declining woodland bird species. Landscape Ecol 27, 813–827 (2012). https://doi.org/10.1007/s10980-012-9743-2

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