Conservation Genetics

, Volume 9, Issue 6, pp 1403–1412 | Cite as

Weak genetic structuring indicates ongoing gene flow across White-ruffed Manakin (Corapipo altera) populations in a highly fragmented Costa Rica landscape

  • Jacob R. Barnett
  • Viviana Ruiz-Gutierrez
  • Aurélie Coulon
  • Irby J. LovetteEmail author
Research Article


We explored the effects of recent forest fragmentation on fine-scale patterns of population structuring and genetic diversity in populations of White-ruffed Manakins (Corapipo altera) inhabiting premontane forest fragments of varying size in southwestern Costa Rica. Habitat fragmentation is a major conservation concern for avian populations worldwide, but studies of the genetic effects of fragmentation on Neotropical birds are limited. We sampled 159 manakins from nine forest fragments of varying size within an 18 km radius, and genotyped these birds at 13 microsatellite loci. Bayesian clustering methods revealed that birds from all fragments comprised a single genetic population, and an MCMC approach showed that the fragments were likely to be at migration-drift equilibrium. F-statistics showed only modest levels of differentiation between forest fragments. We calculated allelic diversity indices for each fragment but found no correlation between genetic diversity and fragment size. These results suggest that manakins may retain substantial connectivity via inter-fragment dispersal despite habitat fragmentation.


Bayesian clustering Microsatellites Population connectivity Genetic diversity Habitat fragmentation Neotropical forests 



We thank Laura Stenzler, Chris Makarewich, Amanda Talaba, and Brynn McCleery for laboratory assistance, and Jeisson Figueroa, Brayner Serrano, Michael Atencio, and Mauricio Paniagua for assistance collecting samples in Costa Rica. Guillermo Durán prepared the maps and provided GIS expertise on the land use history of the region. We would also like to thank the staff at the Las Cruces Biological Station. We appreciated the suggestions of three anonymous reviewers. The work was supported by the Cornell University College of Agriculture and Life Sciences Charitable Trust, an Ann S. and Robert R. Morley Student Research Grant, the Fredric N. Gabler ‘93 Memorial Research Honors Endowment, the Guani Family Fund for Conservation Biology, The Latin American Studies Program at Cornell University’s Tinker Research Grant, and National Science Foundation grant DDEP: 51459 to VRG.


  1. American Ornithologists’ Union (1983) Check-list of North American birds, 7th edn (1998). Washington, DCGoogle Scholar
  2. Anciaes M, Marini MA (2000) The effects of fragmentation on fluctuating asymmetry in passerine birds of Brazilian tropical forests. J Appl Ecol 37:1013–1028CrossRefGoogle Scholar
  3. Anciaes M, Peterson AT (2006) Climate change effects on Neotropical manakin diversity based on ecological niche modeling. Condor 108:778–791CrossRefGoogle Scholar
  4. Barnett JR, Stenzler LM, Ruiz-Gutierrez V, Bogdanowicz SM, Lovette IJ (2007) Isolation and characterization of microsatellite markers from the White-ruffed Manakin, Corapipo altera (Aves, Pipridae). Mol Ecol Notes (in press)Google Scholar
  5. Bates JM (2000) Allozymic genetic structure and natural habitat fragmentation: data for five species of Amazonian forest birds. Condor 102:770–783CrossRefGoogle Scholar
  6. Bates JM (2002) The genetic effects of forest fragmentation on five species of Amazonian birds. J Avian Biol 33:276–294CrossRefGoogle Scholar
  7. Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (1996–2004) GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5000, Université de Montpellier II, Montpellier (France)Google Scholar
  8. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate—a practical and powerful approach to multiple testing. J R Statistical Soc B-Methodol 57:289–300Google Scholar
  9. Blake JG, Loiselle BA (2002) Manakins (Pipridae) in second-growth and old-growth forest: patterns of habitat use, movement, and survival. Auk 119:132–148CrossRefGoogle Scholar
  10. Borgella R, Gavin TA (2005) Avian community dynamics in a fragmented tropical landscape. Ecol Appl 15:1062–1073CrossRefGoogle Scholar
  11. Borgella R, Snow AA, Gavin TA (2001) Species richness and pollen loads of hummingbirds using forest fragments in southern Costa Rica. Biotropica 33:90–109Google Scholar
  12. Brown LM, Ramey RR II, Tamburini B, Gavin TA (2004) Population structure and mitochondrial DNA variation in sedentary Neotropical birds isolated by forest fragmentation. Conserv Genet 5:743–757CrossRefGoogle Scholar
  13. Brumfield RT, Capparella AP (1996) Historical diversification of birds in northwestern South America: a molecular perspective on the role of vicariant events. Evolution 50:1607–1624CrossRefGoogle Scholar
  14. Caizergues A, Ratti O, Helle P, Rotelli L, Ellison L, Rasplus J (2003) Population genetic structure of male black grouse (Tetrao tetrix L.) in fragmented vs. continuous landscapes. Mol Ecol 12:2297–2305PubMedCrossRefGoogle Scholar
  15. Canaday C (1996) Loss of insectivorous birds along a gradient of human impact in Amazonia. Biol Conserv 77:63–77CrossRefGoogle Scholar
  16. Capparella AP (1988) Genetic variation in neotropical birds: implications for the speciation process. Proc Int Ornitholog Congr 19:1658–1664Google Scholar
  17. Capparella AP (1992) Neotropical avian diversity and riverine barriers. Proc Int Ornitholog Congr 20:307–316Google Scholar
  18. Castellon TD, Sieving KE (2006) An experimental test of matrix permeability and corridor use by an endemic understory bird. Conserv Biol 20:135–145PubMedCrossRefGoogle Scholar
  19. Ciofi C, Beaumont MA, Swingland IR, Bruford MW (1999) Genetic divergence and units for conservation in the Komodo Dragon Varanus. Proc R Soc B-Biol Sci 266:2269–2274CrossRefGoogle Scholar
  20. Doherty PF, Grubb TC (2002) Survivorship of permanent-resident birds in a fragmented forested landscape. Ecology 83:844–857CrossRefGoogle Scholar
  21. Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587PubMedGoogle Scholar
  22. Ferraz G, Nichols JD, Hines JE, Stouffer PC, Bierregaard RO, Lovejoy TE (2007) A large-scale deforestation experiment: effects of patch area and isolation on Amazon birds. Science 315:238–241PubMedCrossRefGoogle Scholar
  23. Frankham R (1996) Relationship of genetic variation to population size in wildlife. Conserv Biol 10:1500–1508CrossRefGoogle Scholar
  24. Galbusera P, Githiru M, Lens L, Matthysen E (2004) Genetic equilibrium despite habitat fragmentation in an Afrotropical bird. Mol Ecol 13:1409–1421PubMedCrossRefGoogle Scholar
  25. Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices version Available from (accessed March 2007)
  26. Guillot G, Estoup A, Mortier F, Cosson JF (2005a) A spatial statistical model for landscape genetics. Genetics 170:1261–1280PubMedCrossRefGoogle Scholar
  27. Guillot G, Mortier F, Estoup A (2005b) Geneland: a program for landscape genetics. Mol Ecol Notes 5:712–715CrossRefGoogle Scholar
  28. Hartl DL, Clark AG (1989) Principles of population genetics, 2nd edn. Sinauer Associates, Sunderland, Massachusetts, 682 ppGoogle Scholar
  29. Hoglund J, Shorey L (2003) Local genetic structure in a white-bearded manakin population. Mol Ecol 12:2457–2463PubMedCrossRefGoogle Scholar
  30. Ihaka R, Gentleman R (1996) A language for data analysis and graphics. J Comput Graph Stat 5:299–314CrossRefGoogle Scholar
  31. Karr JR, Freemark KE (1983) Habitat selection and environmental gradients—dynamics in the stable tropics. Ecology 64:1481–1494CrossRefGoogle Scholar
  32. Kattan GH, Alvarez-Lopez H, Giraldo M (1994) Forest fragmentation and bird extinctions—San-Antonio 80 years later. Conserv Biol 8:138–146CrossRefGoogle Scholar
  33. Koenig WD, Van Vuren D, Hooge PN (1996) Detectability, philopatry, and the distribution of dispersal distances in vertebrates. Trends Ecol Evol 11:514–517CrossRefGoogle Scholar
  34. Laurance WF, Lovejoy TE et al (2002) Ecosystem decay of Amazonian forest fragments: a 22-year investigation. Conserv Biol 16:605–618CrossRefGoogle Scholar
  35. Laurance SGW, Stouffer PC, Laurance WF (2004) Effects of road clearings on movement patterns of understory rainforest birds in central Amazonia. Conserv Biol 18:1099–1109CrossRefGoogle Scholar
  36. Laurance SGW, Gomez MS (2005) Clearing width and movements of understory rainforest birds. Biotropica 37:149–152CrossRefGoogle Scholar
  37. Lowe A, Harris S, Ashton P (2004) Ecological genetics: design, analysis, and application. Blackwell, Oxford, UKGoogle Scholar
  38. McDonald DB (2003) Microsatellite DNA evidence for gene flow in neotropical lek-mating long-tailed manakins. Condor 105:580–586CrossRefGoogle Scholar
  39. Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295CrossRefGoogle Scholar
  40. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using mutilocus genotype data. Genetics 155:945–959PubMedGoogle Scholar
  41. Pritchard JK, Wen X, Falush D (2007) Documentation for structure software: version 2.2. (accessed March 2007)
  42. Raymond M, Rousset F (1995) GENEPOP version 1.2: population genetics sofware for exact tests and ecuminicism. J Hered 86:248–249Google Scholar
  43. Renjifo LM (1999) Composition changes in a subandean avifauna after long-term forest fragmentation. Conserv Biol 13:1124–1139CrossRefGoogle Scholar
  44. Ricklefs RE, Bermingham E (2001) Nonequilibrium diversity dynamics of the Lesser Antillean avifauna. Science 294:1522–1524PubMedCrossRefGoogle Scholar
  45. Robinson WD (1999) Long-term changes in the avifauna of Barro Colorado Island, Panama, a tropical forest isolate. Conserv Biol 13:85–97CrossRefGoogle Scholar
  46. Robinson SK, Thompson FR, Donovan TM, Whitehead DR, Faaborg J (1995) Regional forest fragmentation and the nesting success of migratory birds. Science 267:1987–1990PubMedCrossRefGoogle Scholar
  47. Robinson WD, Robinson TR, Robinson SK, Brawn JD (2000) Nesting success of understory forest birds in central Panama. J Avian Biol 31:151–164CrossRefGoogle Scholar
  48. Rosselli L (1994) The annual cycle of a tropical frugivorous altitudinal migrant Corapipo leucorrhoa (Pipridae) and its fruit resources. Bird Conserv Int 4:143–160CrossRefGoogle Scholar
  49. Rosselli L, Vasquez P, Ayub I (2002) The courtship displays and social system of the white-ruffed manakin in Costa Rica. Wilson Bull 114:165–178CrossRefGoogle Scholar
  50. Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228PubMedGoogle Scholar
  51. Ruiz-Gutierrez V, Gavin TA, Dhondt AA (in press) Effects of forest fragmentation on the survival of White-ruffed manakins in southwestern Costa Rica. Ecol ApplGoogle Scholar
  52. Sala O, Chapin F, Armesto J, Berlow E, Bloomfield J, Dirzo R, Huber-Sanwald E, Huenneke L, Jackson R, Kinzig A, Leemans R, Lodge D, Mooney H, Oesterheld M, Poff N, Sykes M, Walker B, Walker M, Wall D (2000) Biodiversity—global biodiversity scenarios for the year 2100. Science 287:1770–1774PubMedCrossRefGoogle Scholar
  53. Siegel S (1956) Nonparametric statistics for the behavioral sciences. McGraw-Hill, TokyoGoogle Scholar
  54. Sieving KE (1992) Nest predation and insular extinction of selected forest birds on Barro Colorado Island, Panama. Ecology 73:2310–2328CrossRefGoogle Scholar
  55. Skutch AF (1967) Life histories of Central American highland birds: White-ruffed Manakin (Corapipo leucorrhoa). Pub Nuttall Orn Club 7:68–75Google Scholar
  56. Slud P (1964) Birds of Costa Rica. B Am Mus Nat Hist 128:237–238Google Scholar
  57. Stouffer PC, Bierregaard RO (1995) Use of amazonian forest fragments by understory insectivorous birds. Ecology 76:2429–2445CrossRefGoogle Scholar
  58. Stouffer PC, Bierregaard RO, Strong C, Lovejoy TE (2006) Long-term landscape change and bird abundance in Amazonian rainforest fragments. Conserv Biol 20:1212–1223PubMedCrossRefGoogle Scholar
  59. Stratford JA, Stouffer PC (1999) Local extinctions of terrestrial insectivorous birds in a fragmented landscape near Manaus, Brazil. Conserv Biol 13:1416–1423CrossRefGoogle Scholar
  60. Thery M (1992) The evolution of leks through female choice: differential clustering and space utilization in six sympatric manakins. Behav Ecol Sociobiol 30:227–237CrossRefGoogle Scholar
  61. Uezu A, Metzger JP, Vielliard JME (2005) Effects of structural and functional connectivity and patch size on the abundance of seven Atlantic Forest bird species. Biol Conserv 123:507–519CrossRefGoogle Scholar
  62. Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol 4:535–538CrossRefGoogle Scholar
  63. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370CrossRefGoogle Scholar
  64. Woxvold IA, Adcock GJ, Mulder RA (2006) Fine-scale genetic structure and dispersal in cooperatively breeding apostlebirds. Mol Ecol 15:3139–3146PubMedCrossRefGoogle Scholar
  65. Zanette LP, Doyle P, Tremont SM (2000) Food shortage in small fragments: evidence from an area-sensitive passerine. Ecology 81:1654–1666CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  • Jacob R. Barnett
    • 1
  • Viviana Ruiz-Gutierrez
    • 1
  • Aurélie Coulon
    • 1
  • Irby J. Lovette
    • 1
    Email author
  1. 1.Fuller Evolutionary Biology Program, Laboratory of OrnithologyCornell UniversityIthacaUSA

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