Skip to main content

Advertisement

Log in

Associations between forest fragmentation patterns and genetic structure in Pfrimer’s Parakeet (Pyrrhura pfrimeri), an endangered endemic to central Brazil’s dry forests

  • Research Article
  • Published:
Conservation Genetics Aims and scope Submit manuscript

Abstract

When habitat becomes fragmented, populations of species may become increasingly isolated. In the absence of habitat corridors, genetic structure may develop and populations risk reductions in genetic diversity from increased genetic drift and inbreeding. Deforestation of the Cerrado biome of Brazil, particularly of the dry forests within the Paranã River Basin, has incrementally occurred since the 1970s and increased forest fragmentation within the region. We performed landscape genetic analyses of Pfrimer’s parakeet (Pyrrhura pfrimeri), a globally endangered endemic to the region, to determine if forest fragmentation patterns were associated with genetic structuring in this species. We used previously generated satellite imagery that identified the locations of Paranã River Basin forest fragments in 1977, 1993/94, and 2008. Behavioral data quantifying the affinity of Pfrimer’s parakeet for forest habitat was used to parameterize empirically derived landscape conductance surfaces. Though genetic structure was observed among Pfrimer’s parakeet populations, no association between genetic and geographic distance was detected. Likewise, least cost path lengths, circuit theory-based resistance distances, and a new measure of least cost path length complexity could not be conclusively associated with genetic structure patterns. Instead, a new quantity that encapsulated connection redundancy from the 1977 forest fragmentation data provided the clearest associations with pairwise genetic differentiation patterns (Jost’s D: r = 0.72, P = 0.006; FST: r = 0.741, P = 0.001). Our analyses suggest a 35-year or more lag between deforestation and its effect on genetic structure. Because 66 % of the Paranã River Basin has been deforested since 1977, we expect that genetic structure will increase substantially among Pfrimer’s Parakeet populations in the future, especially if fragmentation continues at its current pace.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Balkenhol N, Gugerli F, Cushman SA, Waits LP, Coulon A, Arntzen JW, Holderegger R, Wagner HH (2009) Identifying future research needs in landscape genetics: where to from here? Landsc Ecol 24:455–463

    Article  Google Scholar 

  • Bélisle M (2005) Measuring landscape connectivity: the challenge of behavioral landscape ecology. Ecology 86:1988–1995

    Article  Google Scholar 

  • Bianchi CA (2008) Tiriba de Pfrimer Pyrrhura pfrimeri. In: Silveira L, Straube F (eds) Livro Vermelho da Fauna Brasileira. Fundacao Biodiversitas, Belo Horizonte, pp 483–484

    Google Scholar 

  • Bianchi CA (2010) Rapid endangered species assessment: a novel approach to improve extinction risk assessments in poorly known species. Oregon State University, Dissertation

    Google Scholar 

  • Bianchi CA, Haig SM (2012) Deforestation trends of tropical dry forests in central Brazil. Biotropica. doi:10.1111/btp.12010

  • BirdLife International (2008) Species factsheet: Pyrrhura pfrimeri. http://www.birdlife.org/datazone/speciesfactsheet.php?id=32205. Accessed 31 Jan 2010

  • Bohonak AJ (1999) Dispersal, gene flow, and population structure. Q Rev Biol 74:21–45

    Article  PubMed  CAS  Google Scholar 

  • Bonnet E, Van de Peer Y (2002) zt: a software tool for simple and partial Mantel tests. J Stat Softw 7:10

    Google Scholar 

  • Bossart JL, Prowell DP (1998) Genetic estimates of population structure and gene flow: limitations, lessons, and new directions. Trends Ecol Evol 13:202–206

    Article  PubMed  CAS  Google Scholar 

  • Braunisch V, Segelbacher G, Hirzel AH (2010) Modeling functional landscape connectivity from genetic population structure: a new spatially explicit approach. Mol Ecol 19:3664–3678

    Article  PubMed  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 

  • Douglas DH (1994) Least-cost path in GIS using an accumulated cost surface and slopelines. Cartographica 31:37–51

    Article  Google Scholar 

  • Draheim HM, Miller MP, Baird P, Haig SM (2010) Subspecific status and population genetic structure of Least Terns (Sternula antillarum) inferred by mitochondrial DNA control-region sequences and microsatellite DNA. Auk 127:807–819

    Article  Google Scholar 

  • Driezen K, Adriaensen F, Rondinini C, Doncaster CP, Matthysen E (2007) Evaluating least-cost model predictions with empirical dispersal data: a case-study using radiotracking data of hedgehogs (Erinaceus europaeus). Ecol Model 209:314–322

    Article  Google Scholar 

  • Dunham JB, Vinyard GL, Rieman BE (1997) Habitat fragmentation and extinction risk of Lahontan cutthroat trout. N Am J Fish Manage 17:1126–1133

    Article  Google Scholar 

  • Espírito-Santo MRM, Fagundes M, Sevilha AC, Scariot A, Azofeifa G, Noronha SE, Fernandes GW (2008) Florestas estacionais deciduais brasileiras: distribuição e estado de conservação. MG Biota 1:5–13

    Google Scholar 

  • Espírito-Santo M, Sevilha AC, Anaya FC, Barbosa R, Fernandes GW, Sanchez-Azofeifa GA, Scariot A, de Noronha SE, Sampaio CA (2009) Sustainability of tropical dry forests: two case studies in southeastern and central Brazil. For Ecol Manag 258:922–930

    Article  Google Scholar 

  • Etherington TR (2011) Python based GIS tools for landscape genetics: visualizing genetic relatedness and measuring landscape connectivity. Methods Ecol Evol 2:52–55

    Article  Google Scholar 

  • Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567

    Article  PubMed  Google Scholar 

  • Haig SM, Rhymer JM, Heckel DG (1994) Population differentiation in randomly amplified polymorphic DNA of red-cockaded woodpeckers. Mol Ecol 3:581–595

    Article  PubMed  CAS  Google Scholar 

  • Haig SM, Bronaugh WM, Crowhurst RS, D’Elia J, Eagles-Smith CA, Epps CW, Knaus B, Miller MP, Moses ML, Oyler-McCance S, Robinson WD, Sidlauskas B (2011) Genetic applications in avian conservation. Auk 128:205–229

    Article  Google Scholar 

  • Hamrick JL, Godt MJW (1996) Effects of life history traits on genetic diversity in plant species. Philos Trans R Soc Lond B 351:1291–1298

    Article  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Hutchison DW, Templeton AR (1999) Correlation of pairwise genetic and geographic distance measures: inferring the relative influences of gene flow and drift on the distribution of pairwise genetic variability. Evolution 53:1898–1914

    Article  Google Scholar 

  • Janzen DH (1967) Why mountain passes are higher in the tropics. Am Nat 101:233–249

    Article  Google Scholar 

  • Janzen DH (1988) Tropical dry forest: the most endangered major tropical ecosystem. In: Wilson EO (ed) Biodiversity. National Academies Press, Washington, DC, pp 130–137

    Google Scholar 

  • Jennings TN, Knaus BJ, Mullins TD, Haig SM (2011) Multiplexed microsatellite recovery using massively parallel sequencing. Mol Ecol Resour 11:1060–1067

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Kalinowski ST (2005) HP-Rare. A computer program for performing rarefaction on measures of allelic diversity. Mol Ecol Notes 5:187–189

    Article  CAS  Google Scholar 

  • Keyghobadi N (2007) The genetic implications of habitat fragmentation for animals. Can J Zool 85:1049–1064

    Article  Google Scholar 

  • Klink CA, Machado RB (2005) Conservation of the Brazilian Cerrado. Conserv Biol 19:707–713

    Article  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 19:4179–4191

    Article  Google Scholar 

  • Lee-Yaw JA, Davidson A, McRae BH, Green DM (2009) Do landscape processes predict phylogeographic patterns in the wood frog? Mol Ecol 18:1863–1874

    Article  PubMed  Google Scholar 

  • Lewis P, Zaykin D (2002) GDA: genetic data analysis. http://hydrodictyon.eeb.uconn.edu/people/plewis/software.php. Accessed 7 April 2011

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

    Google Scholar 

  • Lindsay DL, Barr KR, Lance RF, Tweddale SA, Hayden TJ, Leberg PL (2008) Habitat fragmentation and genetic diversity of an endangered, migratory songbird, the Golden-cheeked Warbler (Dendroica chrysoparia). Mol Ecol 17:2122–2133

    Article  PubMed  Google Scholar 

  • Loveless MD, Hamrick JL (1984) Ecological determinants of genetic structure in plant populations. Annu Rev Ecol Syst 15:65–95

    Article  Google Scholar 

  • Lowe AJ, Boshier D, Ward M, Bacles CFE, Navarro C (2005) Genetic resource impacts of habitat loss and degradation; reconciling empirical evidence and predicted theory for neotropical trees. Heredity 95:255–273

    Article  PubMed  CAS  Google Scholar 

  • Machado RB, Ramos Neto MB, Pereira PGP, Caldas EF, Gonçalves DA, Santos NS, Tabor K, Steininger M (2004) Estimativas de perda da área do Cerrado brasileiro. Relatório técnico não publicado, Conservação Internacional, Brasília, DF

    Google Scholar 

  • Manel S, Schwartz MK, Luikart G, Taberlet P (2003) Landscape genetics: combining landscape ecology and population genetics. Trends Ecol Evol 18:189–197

    Article  Google Scholar 

  • Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220

    PubMed  CAS  Google Scholar 

  • McRae BH (2006) Isolation by resistance. Evolution 60:1551–1561

    PubMed  Google Scholar 

  • McRae BH, Beier P (2007) Circuit theory predicts gene flow in plant and animal populations. Proc Natl Acad Sci USA 104:19885–19890

    Article  PubMed  CAS  Google Scholar 

  • McRae BH, Dickson BG, Keitt T, Shah VB (2008) Using circuit theory to model connectivity in ecology, evolution, and conservation. Ecology 89:2712–2724

    Article  PubMed  Google Scholar 

  • Melnick DJ (1987) The genetic consequences of primate social organization: a review of macaques, baboons, and velvet monkeys. Genetica 73:117–135

    PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Ministerio do Meio Ambiente (2003) Lista das Espécies da Fauna Brasileira Ameaçadas de Extinção. Instrucao Normativa n.3 de 27 de maio de 2003

  • Moore RP, Robinson WD, Lovette IJ, Robinson TR (2008) Experimental evidence for extreme dispersal limitation in tropical forest birds. Ecol Lett 11:960–968

    Article  PubMed  CAS  Google Scholar 

  • Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858

    Article  PubMed  CAS  Google Scholar 

  • Newman D, Tallmon DA (2001) Experimental evidence for beneficial fitness effects of gene flow in recently isolated populations. Conserv Biol 15:1054–1063

    Article  Google Scholar 

  • Newton I (2003) Geographical patterns in bird migration. In: Berthold P, Gwinner E, Sonnenschein E (eds) Avian migration. Springer, Berlin, pp 211–224

    Chapter  Google Scholar 

  • Noss RF, Csuti B (1997) Habitat fragmentation. In: Meffe GK, Carrol CR (eds) Principles of conservation biology, 2nd edn. Sinauer Associates, Inc., Sunderland, MA, pp 269–304

    Google Scholar 

  • Olmos F, Martuscelli P, Silva RS (1997) Distribution and dry-season ecology of Pfrimer’s conure Pyrrhura pfrimeri, with a reappraisal of Brazilian “Pyrrhura leucotis”. Ornitol Neotrop 8:121–132

    Google Scholar 

  • Pavlacky DC Jr, Goldizen AW, Prentis PJ, Nichols JA, Lowe AJ (2009) A landscape genetics approach for quantifying the relative influence of historic and contemporary habitat heterogeneity on the genetic connectivity of a rainforest bird. Mol Ecol 18:2945–2960

    Article  PubMed  Google Scholar 

  • Pinto N, Keitt TH (2009) Beyond the least-cost path: evaluating corridor redundancy using a graph-theoretic approach. Landsc Ecol 24:253–266

    Article  Google Scholar 

  • Rayfield B, Fortin M-J, Fall A (2011) Connectivity for conservation: a framework mo classify network measures. Ecology 92:847–858

    Article  PubMed  Google Scholar 

  • Reed DH (2004) Extinction risk in fragmented populations. Anim Conserv 7:181–191

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Ribeiro JF, Walter BMT, Sano SM, Almeida SP (1998) Fitofisionomias do bioma Cerrado. In: Sano SM, de Alemida SP (eds) Cerrado: ambiente e flora. EMBRAPA-CPAC, Planaltina, pp 89–166

    Google Scholar 

  • Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228

    PubMed  CAS  Google Scholar 

  • Russello MA, Saranathan V, Buhrman-Deever S, Eberhard J, Caccone A (2007) Characterization of polymorphic microsatellite loci for the invasive monk parakeet (Myiopsitta monachus). Mol Ecol Notes 7:990–992

    Article  CAS  Google Scholar 

  • Safner T, Miller MP, McRae BH, Fortin M-J, Manel S (2011) Comparison of Bayesian clustering and edge detection methods for inferring boundaries in landscape genetics. Int J Mol Sci 12:865–889

    Article  PubMed  CAS  Google Scholar 

  • Sanchez-Azofeifa GA, Quesada M, Rodriguez JP, Nassar JM, Stoner KE, Castillo A, Garvin T, Zent EL, Calvo-Alvarado JC, Kalacska MER, Fajardo L, Gamon JA, Cuevas-Reyes P (2005) Research priorities for neotropical dry forests. Biotropica 37:477–485

    Google Scholar 

  • Scariot AO, Sevilha AC (2005) Biodiversidade, Estrutura e Conservacao da Florestas Estacionais Deciduais no Cerrado. In: Scariot AO, Souza-Silva JC, Felfili JM (eds) Cerrado: ecologia. Biodiversidade e Conservacao, MMA, Brasilia, DF, pp 121–139

    Google Scholar 

  • Shah V, McRae BH (2008) Circuitscape: a tool for landscape ecology. In: Varoquaux G, Vaught T, Millmanm J (eds) Proceedings of the 7th Python in Science Conference (SciPy). Pasadena, California, pp 62–66

  • Silva J (1997) Endemic bird species and conservation in the Cerrado region, South America. Biodivers Conserv 6:435–450

    Article  Google Scholar 

  • Spear SF, Balkenhol N, Fortin M-J, McCrae B-H, Scribner K (2010) Use of resistance surfaces for landscape genetic studies: considerations for parameterization and analysis. Mol Ecol 19:3576–3591

    Article  PubMed  Google Scholar 

  • Storfer A, Murphy MA, Evans JS, Goldberg CS, Robinson S, Spear SF, Dezzani R, Delmelle E, Vierling L, Waits LP (2007) Putting the ‘landscape’ in landscape genetics. Heredity 98:128–142

    Article  PubMed  CAS  Google Scholar 

  • Van Dongten S, Backeljau T, Matthysen E, Dhondt AA (1997) Genetic population structure of the winter moth (Operophtera brumata L.) (Lepidoptera, Geometridae) in a fragmented landscape. Heredity 80:92–100

    Article  Google Scholar 

  • Wallace AR (1889) A narrative of travels on the Amazon and Rio Negro: with an account of the native tribes, and observations of the climate, geology and natural history of the Amazon Valley, 2nd edn. Ward, Lock and Company, London, 363 pp

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  • Westemeier RL, Brawn JD, Simpson SA, Esker TL, Jansen RW, Walk JW, Kershner EL, Bouzat JL, Page KN (1998) Tracking the long-term decline and recovery of an isolated population. Science 282:1695–1698

    Article  PubMed  CAS  Google Scholar 

  • Whitlock MC (2005) Combining probability from independent tests: the weighted Z-method is superior to Fisher’s approach. J Evol Biol 18:1368–1373

    Article  PubMed  CAS  Google Scholar 

  • Young A, Boyle T, Brown T (1996) The population genetic consequences of habitat fragmentation for plants. Trends Ecol Evol 11:413–418

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Fieldwork financial support was provided by USGS Forest and Rangeland Ecosystem Science Center, Fundação O Boticário de Proteção à Natureza, Cleveland Metroparks Zoo (Scott Neotropical Fund), Parrots International, Canadian Parrot Symposium, Pesquisa e Conservação do Cerrado (PEQUI), and Pacific Islands Conservation Research Association. We thank A. Portella and F. Bianchi for field assistance. We further thank T. Jennings, B. Knaus, and R. Cronn for their laboratory and bioinformatic assistance with the identification of microsatellite loci used in this investigation. A. Vandergast, C. Epps, B. McRae, and two anonymous reviewers provided helpful comments on analysis results and prior manuscript drafts. CAB was supported by a CAPES/Fulbright doctoral scholarship (15053166/201604-4). Any use of trade, product, or firm names is for descriptive purposes only and does not imply endorsement by the U.S. Government.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to M. P. Miller.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Miller, M.P., Bianchi, C.A., Mullins, T.D. et al. Associations between forest fragmentation patterns and genetic structure in Pfrimer’s Parakeet (Pyrrhura pfrimeri), an endangered endemic to central Brazil’s dry forests. Conserv Genet 14, 333–343 (2013). https://doi.org/10.1007/s10592-012-0420-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-012-0420-4

Keywords

Navigation