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Structure and fragmentation of growling grass frog metapopulations

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Abstract

Metapopulations occur in fragmented landscapes, and consist of demographically-independent populations connected by dispersal. Nevertheless, anthropogenic habitat fragmentation may be fatal to metapopulations, as it disrupts dispersal and gene flow, and undermines the balance between population extinction and colonization. Understanding the extent to which particular land-use practices disrupt dispersal and gene flow is therefore crucial for conserving metapopulations. We examined the structure and fragmentation of metapopulations of the endangered growling grass frog (Litoria raniformis) in an urbanizing landscape in southern Australia. Population clustering analyses revealed three distinct genetic units, corresponding to the three wetland clusters sampled. Isolation-by-distance was apparent between populations, and genetic distance was significantly correlated with the presence of urban barriers between populations. Our study provides evidence that urbanization fragments metapopulations of L. raniformis. Managers of L. raniformis in urbanizing landscapes should seek to mitigate effects of urbanization on dispersal and gene flow.

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References

  • Arens P, Bugter R, Westende W, Zollinger R, Stronks J, Vos C, Smulders M (2006) Microsatellite variation and population structure of a recovering tree frog (Hyla arborea; L.) metapopulation. Conserv Genet 7:825–835

    Article  CAS  Google Scholar 

  • Baldwin RF, Calhoun AJK, DeMaynadier PG (2006) Conservation planning for amphibian species with complex habitat requirements: a case study using movements and habitat selection of the wood frog Rana sylvatica. J Herpetol 40:442–453

    Article  Google Scholar 

  • Beebee TJC, Griffiths RA (2005) The amphibian decline crisis: a watershed for conservation biology? Biol Conserv 125:271–285

    Article  Google Scholar 

  • Bouzat J, Johnson J, Toepfer J, Simpson S, Esker T, Westemeier R (2009) Beyond the beneficial effects of translocations as an effective tool for the genetic restoration of isolated populations. Conserv Genet 10:191–201

    Article  Google Scholar 

  • Brand AB, Snodgrass JW (2010) Value of artificial habitats for amphibian reproduction in altered landscapes. Conserv Biol 24:295–301

    Article  PubMed  Google Scholar 

  • Brown JH, Kodric-Brown A (1977) Turnover rates in insular biogeography: effect of immigration on extinction. Ecology 58:445–449

    Article  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multi-model inference: a practical information-theoretic approach, 2nd edn. Springer, New York

    Google Scholar 

  • Burns EL, Ferrari G (2004) Microsatellite loci for the green and golden bell frog (Litoria aurea). Conserv Genet 5:421–423

    Article  CAS  Google Scholar 

  • Chapuis M-P, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631

    Article  PubMed  CAS  Google Scholar 

  • Cushman SA (2006) Effects of habitat loss and fragmentation on amphibians: a review and prospectus. Biol Conserv 128:231–240

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • DPCD (2009) Delivering Melbourne’s newest sustainable communities. Victorian Department of Planning and Community Development, Melbourne

    Google Scholar 

  • Ebenhard T (1991) Colonization in metapopulations: a review of theory and observations. Biol J Linn Soc 42:105–121

    Article  Google Scholar 

  • Eigenbrod F, Hecnar SJ, Fahrig L (2009) Quantifying the road-effect zone: threshold effects of a motorway on anuran populations in Ontario, Canada. Ecol Soc 14:24

    Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin ver 3.0: an integrated software package for population genetic analysis. Evol Bioinform Online 1:47–50

    CAS  Google Scholar 

  • Ferner JW (2007) A review of marking and individual recognition techniques for amphibians and reptiles. Society for the Study of Amphibians and Reptiles, Salt Lake City

    Google Scholar 

  • Forman RTT, Alexander LE (1998) Roads and their major ecological effects. Annu Rev Ecol Syst 29:207–231

    Article  Google Scholar 

  • Frankham R, Ballou JD, Briscoe D (2009) Introduction to conservation genetics, 2nd edn. Cambridge University Press, New York

    Google Scholar 

  • Gaggiotti OE, Hanski I (2004) Mechanisms of population extinction. In: Hanski I, Gaggiotti OE (eds) Ecology, Genetics and Evolution of Metapopulations. Academic Press, San Diego, pp 337–366

    Chapter  Google Scholar 

  • Gemmell NJ, Akiyama S (1996) A simple and efficient method for the extraction of DNA. Trends Genet 12:338–339

    Article  PubMed  CAS  Google Scholar 

  • Glista DJ, DeVault TL, DeWoody JA (2009) A review of mitigation measures for reducing wildlife mortality on roadways. Landsc Urban Plan 91:1–7

    Article  Google Scholar 

  • Goslee SC, Urban DL (2007) The ecodist package for dissimilarity-based analysis of ecological data. J Stat Softw 22:1–19

    Google Scholar 

  • Goslee SC, Urban DL (2012) Ecodist: dissimilarity-based functions for ecological analysis. http://cran.r-project.org/web/packages/ecodist/index.html. Accessed 16 April 2012

  • Haddad NM (1999) Corridor and distance effects on interpatch movements: a landscape experiment with butterflies. Ecol Appl 9:612–622

    Article  Google Scholar 

  • Hale JM (2010) Human-induced changes in the population genetic structure of frogs in south-eastern Australia. University of Melbourne, Melbourne

    Google Scholar 

  • Hale JM, Heard G, Smith K, Blacket M, Austin J, Melville J (2011) Microsatellite loci for the endangered growling grass frog (Litoria raniformis), with cross amplification in other Australian frog species. Conserv Genet Resour 3:593–595

    Article  Google Scholar 

  • Hamer AJ, McDonnell MJ (2008) Amphibian ecology and conservation in the urbanizing world: a review. Biol Conserv 141:2432–2449

    Article  Google Scholar 

  • Hamer AJ, Organ A (2008) Aspects of the ecology and conservation of the growling grass frog Litoria raniformis in an urban-fringe environment, southern Victoria. Aust Zool 34:393–407

    Google Scholar 

  • Hamer AJ, Lane SJ, Mahony MJ (2008) Movement patterns of adult green and golden bell frog Litoria aurea and the implications for conservation management. J Herpetol 42:397–407

    Article  Google Scholar 

  • Hamer AJ, Lane SJ, Mahony MJ (2010) Using probabilistic models to investigate the disappearance of a widespread frog-species complex in high-altitude regions of south-eastern Australia. Anim Conserv 13:275–285

    Article  Google Scholar 

  • Hanski I (1998) Metapopulation dynamics. Nature 396:41–49

    Article  CAS  Google Scholar 

  • Hanski I (1999) Metapopulation Ecology. Oxford University Press, Oxford

    Google Scholar 

  • Hanski I, Simberloff D (1997) The metapopulation approach: its history, conceptual domain and application to conservation. In: Hanski I, Gilpin ME (eds) Metapopulation biology: ecology genetics and evolution. Academic Press, San Diego, pp 5–26

    Chapter  Google Scholar 

  • Hanski I, Kuussaari M, Neimeinen M (1994) Metapopulation structure and migration in the butterfly Melitaea cinxia. Ecology 75:747–762

    Article  Google Scholar 

  • Harrison S, Ray C (2002) Plant population viability and metapopulation-level processes. In: Beissinger SR, McCullough DR (eds) Population viability analysis. University of Chicago Press, Chicago, pp 109–122

    Google Scholar 

  • Harrison S, Taylor AD (1997) Empirical evidence for metapopulation dynamics. In: Hanski I, Gilpin ME (eds) Metapopulation biology. Ecology genetics and evolution. Academic Press, San Diego, pp 27–42

    Chapter  Google Scholar 

  • Harveson PM, Grant WE, Lopez RR, Silvy NJ, Frank PA (2006) The role of dispersal in Florida key deer metapopulation dynamics. Ecol Model 195:393–401

    Article  Google Scholar 

  • Heard GW, Scroggie MP, Clemann N (2010) Guidelines for managing the endangered Growling Grass Frog in urbanizing landscapes. Arthur Rylah Insitute for environmental research technical report series no. 208. Victorian Department of Sustainbility and Environment, Heidelberg

    Google Scholar 

  • Heard GW, Scroggie MP, Malone BS (2012) Classical metapopulation theory as a useful paradigm for the conservation of an endangered amphibian. Biol Conserv 148:156–166

    Article  Google Scholar 

  • Hedrick PW (2005) Genetic restoration: a more comprehensive perspective than genetic rescue. Trends Ecol Evol 20:109

    Article  PubMed  Google Scholar 

  • Hels T, Buchwald E (2001) The effects of road kills on amphibian populations. Biol Conserv 99:331–340

    Article  Google Scholar 

  • Hitchings SP, Beebee TJC (1997) Genetic substructuring as a result of barriers to gene flow in urban Rana temporaria (common frog) populations: implications for biodiversity conservation. Heredity 79:117–127

    Article  PubMed  Google Scholar 

  • Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 9:1322–1332

    Article  PubMed  Google Scholar 

  • Kindvall O (1996) Habitat heterogeneity and survival in a bush cricket metapopulation. Ecology 77:207–214

    Article  Google Scholar 

  • Kritzer JP, Sale PF (eds) (2006) Marine Metapopulations. Elsevier Academic Press, San Diego

    Google Scholar 

  • Lahaye WS, Gutiérrez RJ, Akcakaya HR (1994) Spotted owl metapopulation dynamics in southern California. J Anim Ecol 63:775–785

    Article  Google Scholar 

  • Lindenmayer DB, Fischer J (2006) Habitat fragmentation and landscape change: an ecological and conservation synthesis. Island Press, Washington

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Magrach A, Larrinaga AR, SantamarÍA L (2012) Effects of matrix characteristics and interpatch distance on functional connectivity in fragmented temperate rainforests. Conserv Biol 26:238–247

    Article  PubMed  Google Scholar 

  • Mahony M (1999) Review of the declines and disappearances within the bell frog species group (Litoria aurea species group) in Australia. In: Campbell A (ed) Declines and disappearances of Australian frogs. Environment Australia, Canberra, pp 81–93

    Google Scholar 

  • Marsh DM, Trenham PC (2001) Metapopulation dynamics and amphibian conservation. Conserv Biol 15:40–49

    Google Scholar 

  • Mata C, Hervás I, Herranz J, Suárez F, Malo JE (2008) Are motorway wildlife passages worth building? Vertebrate use of road-crossing structures on a Spanish motorway. J Environ Manag 88:407–415

    Article  CAS  Google Scholar 

  • McKinney ML (2002) Urbanization, biodiversity, and conservation. BioScience 52:883–890

    Article  Google Scholar 

  • Menges ES (1990) Population viability analysis for an endangered plant. Conserv Biol 4:52–62

    Article  Google Scholar 

  • Moilanen A, Smith AT, Hanski I (1998) Long-term dynamics in a metapopulation of the American pika. Am Nat 152:530–542

    Article  PubMed  CAS  Google Scholar 

  • Ng SJ, Dole JW, Sauvajot RM, Riley SPD, Valone TJ (2004) Use of highway undercrossings by wildlife in southern California. Biol Conserv 115:499–507

    Article  Google Scholar 

  • Noël S, Ouellet M, Galois P, Lapointe F-J (2007) Impact of urban fragmentation on the genetic structure of the eastern red-backed salamander. Conserv Genet 8:599–606

    Article  Google Scholar 

  • Ouborg NJ (1993) Isolation, population size and extinction: the classical and metapopulation approaches applied to vascular plants along the Dutch Rhine-system. Oikos 66:298–308

    Article  Google Scholar 

  • Petranka JW, Harp EM, Holbrook CT, Hamel JA (2007) Long-term persistence of amphibian populations in a restored wetland complex. Biol Conserv 138:371–380

    Article  Google Scholar 

  • Possingham HP, Lindenmayer DB, Norton TW, Davies I (1994) Metapopulation viability analysis of the greater glider Petauroides volans in a wood production area. Biol Conserv 70:227–236

    Article  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Pritchard JK, Wen X, Falush D (2010) Documentation for structure software: version 2.3. http://pritch.bsd.uchicago.edu/structure.html. Accessed 29 Jan 2012

  • Pyke GH (2002) A review of the biology of the southern bell frog Litoria raniformis (Anura: Hylidae). Aust Zool 32:32–48

    Google Scholar 

  • R Development Core Team (2012) R: a language and environment for statistical computing. R foundation for statistical computing, Vienna. http://www.r-project.org/. Accessed 16 April 2012

  • Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conserv Biol 17:230–237

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

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

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Sagvik J, Uller T, Olsson M (2005) Outbreeding depression in the common frog, Rana temporaria. Conserv Genet 6:205–211

    Article  Google Scholar 

  • Semlitsch RD (2002) Critical elements for biologically based recovery plans of aquatic-breeding amphibians. Conserv Biol 16:619–629

    Article  Google Scholar 

  • Semlitsch RD (2003) Conservation of pond-breeding amphibians. In: Semlitsch RD (ed) Amphibian conservation. Smithsonian Institution, Washington, pp 8–23

    Google Scholar 

  • Sherman CDH, Wapstra E, Uller T, Olsson M (2008) Males with high genetic similarity to females sire more offspring in sperm competition in Peron’s tree frog Litoria peronii. Proc R Soc B 275:971–978

    Article  PubMed  CAS  Google Scholar 

  • Sjögren-Gulve P (1994) Distribution and extinction patterns within a northern metapopulation of the pool frog, Rana lessonae. Ecology 75:1357–1367

    Article  Google Scholar 

  • Skerratt L, Berger L, Speare R, Cashins S, McDonald K, Phillott A, Hines H, Kenyon N (2007) Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. EcoHealth 4:125–134

    Article  Google Scholar 

  • Smith MA, Green DM (2005) Dispersal and the metapopulation paradigm in amphibian ecology and conservation: are all amphibians metapopulations? Ecography 28:110–128

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Smouse PE, Long JC, Sokal RR (1986) Multiple regression and correlation extensions of the Mantel test of matrix correspondence. Syst Zool 35:627–632

    Article  Google Scholar 

  • Stuart SN, Chanson JS, Cox NA, Young BE, Rodrigues ASL, Fischman DL, Waller RW (2004) Status and trends of amphibian declines and extinctions worldwide. Science 306:1783–1786

    Article  PubMed  CAS  Google Scholar 

  • Suter W, Bollmann K, Holderegger R (2007) Landscape permeability: from individual dispersal to population persistence. In: Kienast F, Wildi O, Ghosh S (eds) A changing world, vol 8. Landscape series. Springer, The Netherlands, pp 157–174

  • Tallmon DA, Luikart G, Waples RS (2004) The alluring simplicity and complex reality of genetic rescue. Trends Ecol Evol 19:489–496

    Article  PubMed  Google Scholar 

  • Trombulak SC, Frissell CA (2000) Review of ecological effects of roads on terrestrial and aquatic communities. Conserv Biol 14:18–30

    Article  Google Scholar 

  • UNFPA (2007) State of the world population 2007: unleashing the potential urban growth. United Nations Population Fund, New York

    Google Scholar 

  • Verboom J, Schotman A, Opdam PFM, Metz JAJ (1991) European nuthatch metapopulations in a fragmented agricultural landscape. Oikos 61:149–156

    Article  Google Scholar 

  • Vos CC, Antonisse-de Jong AG, Goedhart PW, Smulders MJM (2001) Genetic similarity as a measure for connectivity between fragmented populations of the moor frog (Rana arvalis). Heredity 86:598–608

    Article  PubMed  CAS  Google Scholar 

  • Wassens S (2008) Review of the past distribution and decline of the southern bell frog Litoria raniformis in New South Wales. Aust Zool 34:446–452

    Google Scholar 

  • Wassens S, Watts RJ, Jansen A, Roshier D (2008) Movement patterns of southern bell frogs (Litoria raniformis) in response to flooding. Wildl Res 35:50–58

    Article  Google Scholar 

  • Williams BK, Nichols JD, Conroy MJ (2002) The Analysis and Management of Animal Populations. Academic Press, San Diego

    Google Scholar 

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Acknowledgments

Funding for this project was provided by an Australian Research Council Linkage Grant (LP0667815). Additional funding was provided to JH from the Holsworth Wildlife Endowment, Museum Victoria and the Loftus-Hills Memorial Grant (University of Melbourne). Tissue collection was conducted by GH with support from a David Myers Postgraduate Scholarship (La Trobe University), and grants from the Growling Grass Frog Trust Fund and Victorian Department of Sustainability and Environment. Manuscript preparation was supported by Australian Research Council Linkage Grant (LP0990161). We thank M. Littlejohn, B. Malone, M. Scroggie and P. Robertson for expert advice. Technical support was provided by staff of the Sciences Department, Museum Victoria, and the Department of Zoology, La Trobe University. Private landholders in the Merri Creek catchment kindly allowed us access to their properties for sampling purposes.

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Authors and Affiliations

  1. Sciences Department, Museum Victoria, Melbourne, VIC, 3053, Australia

    Joshua M. Hale, Katie L. Smith, Jeremy J. Austin & Jane Melville

  2. Department of Zoology, University of Melbourne, Melbourne, VIC, 3010, Australia

    Joshua M. Hale, Katie L. Smith & Michael Kearney

  3. School of Botany, University of Melbourne, Melbourne, VIC, 3010, Australia

    Joshua M. Hale, Geoffrey W. Heard, Katie L. Smith & Kirsten M. Parris

  4. Department of Zoology, La Trobe University, Bundoora, Melbourne, VIC, 3086, Australia

    Geoffrey W. Heard

  5. Australian Centre for Ancient DNA, University of Adelaide, Adelaide, SA, 5005, Australia

    Jeremy J. Austin

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  1. Joshua M. Hale
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Hale, J.M., Heard, G.W., Smith, K.L. et al. Structure and fragmentation of growling grass frog metapopulations. Conserv Genet 14, 313–322 (2013). https://doi.org/10.1007/s10592-012-0428-9

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