Biochemical Genetics

, Volume 52, Issue 7–8, pp 321–337 | Cite as

Genetic Differentiation Among Populations of the Roseate Spoonbill (Platalea ajaja; Aves: Pelecaniformes) in Three Brazilian Wetlands



Effective population size, levels of genetic diversity, gene flow, and genetic structuring were assessed in 205 colonial Roseate spoonbills from 11 breeding colonies from north, central west, and south Brazil. Colonies and regions exhibited similar moderate levels of diversity at five microsatellite loci (mean expected heterozygosity range 0.50–0.62; allelic richness range 3.17–3.21). The central west region had the highest Ne (59). FST values revealed low but significant genetic structuring among colonies within the north and within the south regions. Significant global genetic structuring was found between the northern and central western populations as well as between the northern and southern populations. An individual-based Bayesian clustering method inferred three population clusters. Assignment tests correctly allocated up to 64% of individuals to their source regions. Collectively, results revealed complex demographic dynamics, with ongoing gene flow on a local scale, but genetic differentiation on a broader scale. Populations in the three regions may all be conserved, but special concern should be given to central western ones, which can significantly contribute to the species’ gene pool in Brazil.


Aquatic birds Breeding colonies Effective population size Nuclear markers Regional genetic structuring 

Supplementary material

10528_2014_9650_MOESM1_ESM.doc (254 kb)
Supplementary material 1 (DOC 254 kb)


  1. Alho CJR, Silva JSV (2012) Effects of severe floods and droughts on wildlife of the Pantanal wetland (Brazil): a review. Animals 2:590–610CrossRefGoogle Scholar
  2. Antas PTZ (1994) Migration and other movements among the lower Paraná River valley wetlands, Argentina, and the south Brazil/Pantanal weltlands. Bird Conserv Int 4:181–190CrossRefGoogle Scholar
  3. Arantes de Souza E, Nunes MFC, Roos AL, Araújo EFP (2008) Aves do Parque Nacional do Cabo Orange: guia de campo. Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis, AmapáGoogle Scholar
  4. Ayres M, Ayres Jr M, Lima Ayres D, Santos dos Santos AA (2007) Biostat 5.3: Aplicações estatísticas nas areas das ciências biomédicas. Sociedade Civil Mamirauá and Conservation International (eds). Instituto Mamirauá, BelémGoogle Scholar
  5. Bates EM, Deyoung RW, Ballard BM (2009) Genetic diversity and population structure of Reddish Egrets along the Texas coast. Waterbirds 32:430–436CrossRefGoogle Scholar
  6. Bicknell AWJ, Knight ME, Bilton D, Reid JB, Burke T, Votier SC (2012) Population genetic structure and long-distance dispersal among seabird populations: implications for colony persistence. Mol Ecol 21:2863–2876PubMedCrossRefGoogle Scholar
  7. BirdLife International (2013) Species factsheet: Platalea ajaja. Accessed 27 Jan 2014
  8. Bouzat JL, Walker BG, Boersma PD (2009) Regional genetic structure in the Magellanic Penguin (Spheniscus magellanicus) suggests metapopulation dynamics. Auk 126:326–334CrossRefGoogle Scholar
  9. Castello L, McGrath DG, Hess LL, Coe MT, Lefebvre PA, Petry P, Macedo MN, Reno VF, Arantes CC (2013) The vulnerability of Amazon freshwater ecosystems. Conserv Lett 6:217–229CrossRefGoogle Scholar
  10. Centrón S, Sánchez K (2011) Paraguay: informe annual. Censo Neotropical de aves acuáticas 2010 [em línea]. En: Unterkofler DA, Blanco DE (eds), El censo Neotropical de aves acuáticas 2009. Wetlands International, Buenos Aires. Accessed 27 Jan 2014
  11. Davis S, Acheson N (2007) Bolivia: informe anual. Censo Neotropical de Aves Acuáticas 2006 [en línea]. En Lesterhuis AJ, Blanco DE (eds), El censo Neotropical de aves acuáticas 2006: Una herramienta para la conservación. Wetlands International, Buenos Aires. Accessed 23 Jan 2014
  12. Del Lama SN, Lopes IF, Lama MAD (2002) Genetic variability and level of differentiation among Brazilian Pantanal Wood Stork populations. Biochem Genet 40:87–99PubMedCrossRefGoogle Scholar
  13. Develey PF, Goerck JM (2009) Brazil. Pp 99–112 in: C Devenish, DF Díaz Fernández, RP Clay, I Davidson, I Yépez Zabala (eds), Important bird areas Americas: priority sites for diversity conservation. BirdLife International (BirdLife Conservation Series 16). QuitoGoogle Scholar
  14. Dumas JV (2000) Roseate spoonbill (Ajaia ajaja). In: Poole A, Gill F (eds) The birds of North America, no. 490. The Birds of North America, Inc, PhiladelphiaGoogle Scholar
  15. Earl DA (2011) Structure Harvester version 0.6.1. Accessed 9 Jun 2013
  16. Encarnação CD, Diniz MG (1992) Relatório Técnico07/92: GETEC/fauna-IBAMA/MG. Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis, Belo HorizonteGoogle Scholar
  17. Eo SH, Doyle JM, DeWoody JA (2010) Genetic diversity in birds is associated with body mass and habitat type. J Zool 283:220–226CrossRefGoogle Scholar
  18. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:2611–2620PubMedCrossRefGoogle Scholar
  19. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distance among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491PubMedCentralPubMedGoogle Scholar
  20. Excoffier L, Laval G, Schneider S (2005) Arlequin version 3.0: an integrated software package for population genetics data analysis. Evol Bioinf Online 1:47–50Google Scholar
  21. Ferreira J, Pardini R, Metzger JP, Fonseca CR, Pompeu PS, Sparovek G, Louzada J (2012) Towards environmentally sustainable agriculture in Brazil: challenges and opportunities for applied ecological research. J Appl Ecol 49:535–541Google Scholar
  22. Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  23. Friesen V, Burg TM, McCoy KD (2007) Mechanisms of population differentiation in seabirds. Mol Ecol 16:1765–1785PubMedCrossRefGoogle Scholar
  24. Geraci J, Béchet A, Cézilly F, Ficheux S, Baccetti N, Samraoui B, Wattier R (2012) Greater flamingo colonies around the Mediterranean form a single interbreeding population and share a common history. J Avian Biol 43:341–354CrossRefGoogle Scholar
  25. Gianuca D, Vooren A, Gianuca AT (2009) Abundância e reprodução do colhereiro (Platalea ajaja) durante o pulso de 2008/2009 em uma colônia de Ciconiiformes no estuário da Lagoa dos Patos, RS. In: Simon JE, Raposo MA, Stopiglia R, Peres J (eds) Biogeografia de aves da Mata Atlantica: livro de resumos/XVII Congresso Brasileiro de Ornitologia. Tec Art, São PauloGoogle Scholar
  26. Gonçalves EC, Ferrari SF, Burlamaqui TCT, Miranda L, Santos MS, Silva A, Schneider MPC (2010) Genetic diversity and differentiation of three Brazilian populations of the Scarlet Ibis (Eudocimus ruber). J Ornithol 151:797–803CrossRefGoogle Scholar
  27. Goudet J (1995) Fstat version 1.2: a computer program to calculate F-statistics. J Hered 86:485–486Google Scholar
  28. Greenwood PJ, Harvey PH (1982) The natal and breeding dispersal of birds. Annu Rev Ecol Syst 13:1–21CrossRefGoogle Scholar
  29. Guadagnin DL, Peter AS, Perello LFC, Maltchik L (2005) Spatial and temporal patterns of waterbird assemblages in fragmented wetlands of southern Brazil. Waterbirds 28:261–272CrossRefGoogle Scholar
  30. Hare MP, Nunney L, Schwartz MK, Ruzzante DE, Burford M, Waples RS, Ruegg K, Palstra F (2011) Understanding and estimating effective population size for practical application in marine species management. Conserv Biol 25:438–449PubMedCrossRefGoogle Scholar
  31. Hill A, Green M, Palacios E (2012) Genetic diversity and population structure of North America’s rarest heron, the Reddish Egret (Egretta rufescens). Conserv Gen 13:535–543CrossRefGoogle Scholar
  32. Huang X, Zhou X, Chen M, Fang W, Chen X (2010) Isolation and characterization of microsatellite loci in the vulnerable Chinese egret (Egretta eulophotes, Aves). Conserv Gen 11:1211–1214CrossRefGoogle Scholar
  33. Jensen JL, Bohonak AJ, Kelley ST (2005) Isolation by distance, web service, version 3.16. BMC Genetics 6:13. Accessed 27 Jan 2014
  34. Jost L (2008) GST and its relatives do not measure differentiation. Mol Ecol 17:4015–4026PubMedCrossRefGoogle Scholar
  35. Köppen W, Geiger R (1928) Klimate der Erde, wall map. Verlag Justus Perthes, GothaGoogle Scholar
  36. Kushlan JA (1993) Colonial waterbirds as bioindicators of environmental change (review). Colon Waterbirds 16:223–251CrossRefGoogle Scholar
  37. Levin II, Parker PG (2012) Philopatry drives genetic differentiation in an island archipelago: comparative population genetics of Galapagos Nazca boobies (Sula granti) and great frigatebirds (Fregata minor). Ecol Evol 2:2775–2787PubMedCentralPubMedCrossRefGoogle Scholar
  38. Lopes IF, Miño CI, Del Lama SN (2007) Genetic diversity and evidence of recent demographic expansion in waterbird populations from the Brazilian Pantanal. Braz J Biol 67(S4):849–857PubMedCrossRefGoogle Scholar
  39. Lopes IF, Haig SM, Del Lama SN (2011) Genetic characterization of Neotropical Jabiru storks: insights for conservation. Waterbirds 33:425–437CrossRefGoogle Scholar
  40. Lorenz JJ, Langan-Mulrooney B, Frezza P, Harvey RG, Mazzotti FJ (2009) Roseate spoonbill reproduction as an indicator for restoration of the Everglades and the Everglades estuaries. Ecol Indic 9:S96–S107CrossRefGoogle Scholar
  41. Luikart G, Cornuet JM (1998) Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conserv Biol 12:228–237CrossRefGoogle Scholar
  42. Melvin SL, Gawlik DE, Scharff T (1999) Long-term movement patterns for seven species of wading birds. Waterbirds 22:411–416CrossRefGoogle Scholar
  43. Miño CI, Del Lama SN (2007) Genetic structure in Brazilian breeding colonies of the Roseate spoonbill (Platalea ajaja, Aves: Threskiornithidae). Genet Mol Res 6:238–247Google Scholar
  44. Miño CI, Sawyer GM, Benjamin RC, Del Lama SN (2009) Parentage and relatedness in captive and natural populations of the Roseate spoonbill (Aves: Ciconiiformes) based on microsatellite data. J Exp Zool Part A 311A(6):453–464CrossRefGoogle Scholar
  45. Morrison RIG, Serrano IL, Antas PTZ, Ross K (2008) Migratory birds in the Pantanal: distribution of nearctic shorebirds and water species in the Pantanal. WWF Brazil, BrasiliaGoogle Scholar
  46. Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590PubMedCentralPubMedGoogle Scholar
  47. Oomen RA, Reudink MW, Nocera JJ, Somers CM, Green MC, Kyle CJ (2011) Mitochondrial evidence for panmixia despite perceived barriers to gene flow in a widely distributed waterbird. J Hered 102:584–592PubMedCrossRefGoogle Scholar
  48. Paetkau D, Calvert W, Stirling I, Strobeck C (1995) Microsatellite analysis of population structure in Canadian polar bears. Mol Ecol 4:347–354PubMedCrossRefGoogle Scholar
  49. Paetkau D, Slade R, Burden M, Estoup A (2004) Genetic assignment methods for the direct, real-time estimation of migration rate: a simulation-based exploration of accuracy and power. Mol Ecol 13:55–65PubMedCrossRefGoogle Scholar
  50. 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
  51. Piry S, Luikart G, Cornuet JM (1999) Bottleneck: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503CrossRefGoogle Scholar
  52. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedCentralPubMedGoogle Scholar
  53. Raymond M, Rousset F (1995) An exact test for population differentiation. Evolution 49:1280CrossRefGoogle Scholar
  54. Reudink MW, Kyle CJ, Nocera JJ, Oomen RA, Green MC, Somers CM (2011) Panmixia on a continental scale in a widely distributed colonial waterbird. Biol J Linn Soc 102:583–592CrossRefGoogle Scholar
  55. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225CrossRefGoogle Scholar
  56. Rocha CD, Del Lama SN, Regitano LCD (2004) Lack of genetic structuring among tropical Brazilian wood stork populations and low genetic differentiation from North American populations. Biotropica 36:248–258Google Scholar
  57. Roesch LFW, Vieira FCB, Pereira VA, Schünemann AL, Teixeira IF, Senna AJT, Stefenon VM (2009) The Brazilian Pampa: a fragile biome. Diversity 1:182–198CrossRefGoogle Scholar
  58. Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation-by-distance. Genetics 146:1219–1228Google Scholar
  59. Sambrook J, Russell DW (2001) Molecular cloning, a laboratory manual, vol 1, 3rd edn. Cold Spring Harbor Laboratory Press, New YorkGoogle Scholar
  60. Santos MH, Lopes IF, Del Lama SN (2008) Population genetic study of mitochondrial DNA in Roseate spoonbill (Aves; Platalea ajaja) breeding colonies from the Pantanal wetlands, Brazil. Biochem Genet 46:492–505PubMedCrossRefGoogle Scholar
  61. Sawyer GM, Benjamin RC (2006) Isolation and characterization of microsatellite loci for parentage assessment in captive populations of Roseate spoonbill (Ajaia ajaja). Mol Ecol Notes 6:677–679CrossRefGoogle Scholar
  62. Sick H (1997) Ornitologia Brasileira. Segunda impressão, Rio de Janeiro, Brasil. Nova Fronteira, Edição revista e ampliada por José Fernando PachecoGoogle Scholar
  63. Silva F, Bello Fallavena MA (1995) Movimentos de dispersão de Platalea ajaja (Aves, Threskiornithidae) detectados através de anilhamento. Rev Ecol Lat Am 2:19–21Google Scholar
  64. Souza ASMC, Del Lama SN, Miño CI (2013) Conspecific brood parasitism in the White-faced Ibis Plegadis chihi (Aves: Pelecaniformes) revealed by microsatellites-based kinship-reconstruction. J Exp Zool Part A 319:277–284CrossRefGoogle Scholar
  65. Tomasulo-Seccomandi AM, Schable NA, Bryan AL Jr, Brisbin IL Jr, Del Lama SN, Glenn TC (2003) Development of microsatellite DNA loci from the wood stork (Aves, Ciconiidae, Mycteria americana). Mol Ecol Notes 3:563–566CrossRefGoogle Scholar
  66. Unterkofler DA, Blanco DE (2014) El Censo Neotropical de Aves Acuáticas 2013. Wetlands International, Buenos Aires.óndeAvesAcuáticas/Censoneotropicaldeavesaquáticas/ResultadosdelCNAA2013/tabid/3221/Default.aspx. Accessed 25 March 2014
  67. Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) Micro-Checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538CrossRefGoogle Scholar
  68. Wang J (2009) A new method for estimating effective population sizes from a single sample of multilocus genotypes. Mol Ecol 18:2148–2164PubMedCrossRefGoogle Scholar
  69. Waples RS (2006) A bias correction for estimates of effective population size based on linkage disequilibrium at unlinked gene loci. Conserv Gen 7:167–184CrossRefGoogle Scholar
  70. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370CrossRefGoogle Scholar
  71. Welch AJ, Fleischer RC, James HF, Wiley AE, Ostrom PH, Adams J, Duvall F, Holmes N, Hu D, Penniman J, Swindle KA (2012) Population divergence and gene flow in an endangered and highly mobile seabird. Heredity 109:19–28PubMedCentralPubMedCrossRefGoogle Scholar
  72. Wiley AE, Welch AJ, Ostrom PH, James HF, Stricker CA, Fleischer RC, Gandhi H, Adams J, Ainley DG, Duvall F, Holmes N, Hu D, Judge S, Penniman J, Swindle KA (2012) Foraging segregation and genetic divergence between geographically proximate colonies of a highly mobile seabird. Oecologia 168:119–130PubMedCrossRefGoogle Scholar
  73. Wright S (1951) The genetical structure of populations. Ann Eugen 15:323–354PubMedCrossRefGoogle Scholar
  74. Yeung CKL, Yu-Cheng H, Shou-Hsien L (2009) Isolation and characterization of 23 microsatellite loci in the black-faced spoonbill (Platalea minor) and amplification in other Ciconiiformes waterbirds. Conserv Gen 10:1081–1084CrossRefGoogle Scholar
  75. Zan S, Zhou L, Jiang H, Zhang B, Wu Z, Hou Y (2008) Genetic structure of the oriental white stork (Ciconia boyciana): implications for a breeding colony in a nonbreeding area. Integr Zool 3:235–244PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Carolina Isabel Miño
    • 1
    • 2
  • Silvia Nassif Del Lama
    • 1
  1. 1.Departamento de Genética e EvoluçãoUniversidade Federal de São CarlosSão CarlosBrazil
  2. 2.Departamento de Ecología, Genética y Evolución and IEGEBA-CONICET, Facultad de Ciencias Exactas y NaturalesUniversidad de Buenos Aires, Pabellón II Ciudad Universitaria (C1428EHA)Buenos AiresArgentina

Personalised recommendations