Species- and sex-specific connectivity effects of habitat fragmentation in a suite of woodland birds.

Loss of functional connectivity following habitat loss and fragmentation could drive species declines. A comprehensive understanding of fragmentation effects on functional connectivity of an ecological assemblage requires investigation of multiple species with different mobilities, at different spatial scales, for each sex, and in different landscapes. Based on published data on mobility and ecological responses to fragmentation of 10 woodland-dependent birds, and using simulation studies, we predicted that (1) fragmentation would impede dispersal and gene flow of eight "decliners" (species that disappear from suitable patches when landscape-level tree cover falls below species-specific thresholds), but not of two "tolerant" species (whose occurrence in suitable habitat patches is independent of landscape tree cover); and that fragmentation effects would be stronger (2) in the least mobile species, (3) in the more philopatric sex, and (4) in the more fragmented region. We tested these predictions by evaluating spatially explicit isolation-by-landscape-resistance models of gene flow in fragmented landscapes across a 50 x 170 km study area in central Victoria, Australia, using individual and population genetic distances. To account for sex-biased dispersal and potential scale- and configuration-specific effects, we fitted models specific to sex and geographic zones. As predicted, four of the least mobile decliners showed evidence of reduced genetic connectivity. The responses were strongly sex specific, but in opposite directions in the two most sedentary species. Both tolerant species and (unexpectedly) four of the more mobile decliners showed no reduction in gene flow. This is unlikely to be due to time lags because more mobile species develop genetic signatures of fragmentation faster than do less mobile ones. Weaker genetic effects were observed in the geographic zone with more aggregated vegetation, consistent with gene flow being unimpeded by landscape structure. Our results indicate that for all but the most sedentary species in our system, the movement of the more dispersive sex (females in most cases) maintains overall genetic connectivity across fragmented landscapes in the study area, despite some small-scale effects on the more philopatric sex for some species. Nevertheless, to improve population viability for the less mobile bird species, structural landscape connectivity must be increased.

[1]  P. Sunnucks,et al.  Does reduced mobility through fragmented landscapes explain patch extinction patterns for three honeyeaters? , 2014, The Journal of animal ecology.

[2]  J Andrew Royle,et al.  Current approaches using genetic distances produce poor estimates of landscape resistance to interindividual dispersal , 2013, Molecular ecology.

[3]  S. Cushman,et al.  Landscape genetics and limiting factors , 2013, Conservation Genetics.

[4]  Bradley C Fedy,et al.  Sample design effects in landscape genetics , 2013, Conservation Genetics.

[5]  T. Brinkman,et al.  Fine-scale social and spatial genetic structure in Sitka black-tailed deer , 2013, Conservation Genetics.

[6]  P. Sunnucks,et al.  Disrupted fine-scale population processes in fragmented landscapes despite large-scale genetic connectivity for a widespread and common cooperative breeder: the superb fairy-wren (Malurus cyaneus). , 2013, The Journal of animal ecology.

[7]  S. Cushman,et al.  Re-Evaluating Causal Modeling with Mantel Tests in Landscape Genetics , 2013 .

[8]  Peter L. Ralph,et al.  DISENTANGLING THE EFFECTS OF GEOGRAPHIC AND ECOLOGICAL ISOLATION ON GENETIC DIFFERENTIATION , 2013, Evolution; international journal of organic evolution.

[9]  Graeme Newell,et al.  Species distribution modelling for conservation planning in Victoria, Australia , 2013 .

[10]  Mary E. Blair,et al.  Scale-Dependent Effects of a Heterogeneous Landscape on Genetic Differentiation in the Central American Squirrel Monkey (Saimiri oerstedii) , 2012, PloS one.

[11]  P. Sunnucks,et al.  Genes and song: genetic and social connections in fragmented habitat in a woodland bird with limited dispersal. , 2012, Ecology.

[12]  R. Peakall,et al.  Genetic spatial autocorrelation can readily detect sex‐biased dispersal , 2012, Molecular ecology.

[13]  P. Sunnucks,et al.  Fine-scale effects of habitat loss and fragmentation despite large-scale gene flow for some regionally declining woodland bird species , 2012, Landscape Ecology.

[14]  Marie-Josée Fortin,et al.  Effects of sample size, number of markers, and allelic richness on the detection of spatial genetic pattern , 2012 .

[15]  M. White,et al.  Predicting Landscape-Genetic Consequences of Habitat Loss, Fragmentation and Mobility for Multiple Species of Woodland Birds , 2012, PloS one.

[16]  S. A. Cushman,et al.  Limiting factors and landscape connectivity: the American marten in the Rocky Mountains , 2011, Landscape Ecology.

[17]  Luc Lens,et al.  Genetic signature of population fragmentation varies with mobility in seven bird species of a fragmented Kenyan cloud forest , 2011, Molecular ecology.

[18]  V. Doerr,et al.  Dispersal behaviour of Brown Treecreepers predicts functional connectivity for several other woodland birds , 2011 .

[19]  H. Ford The causes of decline of birds of eucalypt woodlands: advances in our knowledge over the last 10 years , 2011 .

[20]  G. Luikart,et al.  Why replication is important in landscape genetics: American black bear in the Rocky Mountains , 2011, Molecular ecology.

[21]  P. Sunnucks Towards modelling persistence of woodland birds: the role of genetics , 2011 .

[22]  G. Luikart,et al.  Genomics and the future of conservation genetics , 2010, Nature Reviews Genetics.

[23]  G. Luikart,et al.  Quantifying the lag time to detect barriers in landscape genetics , 2010, Molecular ecology.

[24]  S. Cushman,et al.  Spurious correlations and inference in landscape genetics , 2010, Molecular ecology.

[25]  M. Fortin,et al.  Comparison of the Mantel test and alternative approaches for detecting complex multivariate relationships in the spatial analysis of genetic data , 2010, Molecular ecology resources.

[26]  M. Fortin,et al.  Considering spatial and temporal scale in landscape‐genetic studies of gene flow , 2010, Molecular ecology.

[27]  L. Excoffier,et al.  Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows , 2010, Molecular ecology resources.

[28]  Marie-Josée Fortin,et al.  Applications of landscape genetics in conservation biology: concepts and challenges , 2010, Conservation Genetics.

[29]  A. Bennett,et al.  Collapse of an avifauna: climate change appears to exacerbate habitat loss and degradation , 2009 .

[30]  James Q. Radford,et al.  Gap‐crossing decisions of forest birds in a fragmented landscape , 2009 .

[31]  Aurélie Coulon,et al.  Identifying future research needs in landscape genetics: where to from here? , 2009, Landscape Ecology.

[32]  Viral B. Shah,et al.  Using circuit theory to model connectivity in ecology, evolution, and conservation. , 2008, Ecology.

[33]  Lenore Fahrig,et al.  Non‐optimal animal movement in human‐altered landscapes , 2007 .

[34]  S. Banks,et al.  Sex and sociality in a disconnected world: A review of the impacts of habitat fragmentation on animal social interactions , 2007 .

[35]  Sarah C. Goslee,et al.  The ecodist Package for Dissimilarity-based Analysis of Ecological Data , 2007 .

[36]  A. Bennett,et al.  The relative importance of landscape properties for woodland birds in agricultural environments , 2007 .

[37]  S. Pimm,et al.  Dispersal of Amazonian birds in continuous and fragmented forest. , 2007, Ecology letters.

[38]  S. Kalinowski,et al.  Revising how the computer program cervus accommodates genotyping error increases success in paternity assignment , 2007, Molecular ecology.

[39]  S. MacEachern,et al.  When log‐dwellers meet loggers: impacts of forest fragmentation on two endemic log‐dwelling beetles in southeastern Australia , 2006, Molecular ecology.

[40]  P. Smouse,et al.  genalex 6: genetic analysis in Excel. Population genetic software for teaching and research , 2006 .

[41]  Andrew F. Bennett,et al.  Landscape-level thresholds of habitat cover for woodland-dependent birds , 2005 .

[42]  S. Banks,et al.  The effects of habitat fragmentation on the social kin structure and mating system of the agile antechinus, Antechinus agilis , 2005, Molecular ecology.

[43]  P. Goedhart,et al.  Gap Crossing Decisions by Reed Warblers (Acrocephalus Scirpaceus) in Agricultural Landscapes , 2005, Landscape Ecology.

[44]  Peter Menkhorst,et al.  Songful Handbook. "Handbook of Australian, New Zealand and Antarctic Birds, Volume 6: Pardalotes to Shrike-Thrushes" by P.J. Higgins and J.M. Peter (eds). [review] , 2003 .

[45]  C. Cooper,et al.  Effects of remnant size and connectivity on the response of Brown Treecreepers to habitat fragmentation , 2002 .

[46]  Stephen P. Ellner,et al.  SCALING UP ANIMAL MOVEMENTS IN HETEROGENEOUS LANDSCAPES: THE IMPORTANCE OF BEHAVIOR , 2002 .

[47]  C. Cooper,et al.  Experimental Evidence of Disrupted Dispersal Causing Decline of an Australian Passerine in Fragmented Habitat , 2002 .

[48]  M. Gardner,et al.  The impact of habitat fragmentation on dispersal of Cunningham’s skink (Egernia cunninghami): evidence from allelic and genotypic analyses of microsatellites , 2001, Molecular ecology.

[49]  S. Dale Female‐biased dispersal, low female recruitment, unpaired males, and the extinction of small and isolated bird populations , 2001 .

[50]  P. Sunnucks,et al.  Efficient genetic markers for population biology. , 2000, Trends in ecology & evolution.

[51]  Rod Peakall,et al.  Spatial autocorrelation analysis of individual multiallele and multilocus genetic structure , 1999, Heredity.

[52]  I. Hanski,et al.  Inbreeding and extinction in a butterfly metapopulation , 1998, Nature.

[53]  Monica G. Turner,et al.  Landscape connectivity and population distributions in heterogeneous environments , 1997 .

[54]  R. Mulder Natal and breeding dispersal in a co-operative, extra-group-mating bird , 1995 .

[55]  R. Mulder,et al.  Helpers liberate female fairy-wrens from constraints on extra-pair mate choice , 1994, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[56]  R. Noske,et al.  A Demographic Comparison of Cooperatively Breeding and Non-Cooperative Treecreepers (Climacteridae) , 1991 .

[57]  P. Sunnucks,et al.  Little evidence that condition, stress indicators, sex ratio, or homozygosity are related to landscape or habitat attributes in declining woodland birds , 2013 .

[58]  H. Ford,et al.  Responses of eastern yellow robins 'eopsaltria Australis' to translocation into vegetation remnants in a fragmented landscape , 2012 .

[59]  H. Ford Twinkling lights or turning down the dimmer switch?: Are there two patterns of extinction debt in fragmented landscapes? , 2011 .

[60]  R. Peakall,et al.  The absence of sex-biased dispersal in the cooperatively breeding grey-crowned babbler. , 2011, The Journal of animal ecology.

[61]  H. Possingham,et al.  Models based on individual level movement predict spatial patterns of genetic relatedness for two Australian forest birds , 2010, Landscape Ecology.

[62]  P. Higgins,et al.  Handbook of Australian, New Zealand and Antarctic birds. Volume 7 Part A: boatbill to larks , 2006 .

[63]  P. J. Higgins,et al.  Handbook of Australian, New Zealand and Antarctic birds. Volume 5: trant-Flycatchers to chats , 2001 .