Skip to main content

Advertisement

SpringerLink
Log in

Genetic structure of Bertholletia excelsa populations from the Amazon at different spatial scales

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

Abstract

Population genetic structure and genetic diversity levels are important issues to understand population dynamics and to guide forest management plans. The Brazil nut tree (Bertholletia excelsa Bonpl.) is an endemic species, widely distributed through Amazonian upland forests and also an important species for the local extractive economy. Our aim was to analyze the genetic structure of Brazil nut trees at both fine and large scales throughout the Amazon Basin, contributing to the knowledge base on this species and to generate information to support plans for its conservation. We genotyped individuals from nine sites distributed in five regions of the Brazilian Amazon using 11 microsatellite loci. We found an excess of heterozygotes in most populations, with significant negative inbreeding coefficients (f) for five of them and the fine-scale structure, when present, was very small. These results, as a consequence of self-incompatibility, indicate that conservation plans for B. excelsa must include the maintenance of genetic diversity within populations to ensure viable amounts of seeds for both economic purposes and for the local persistence of the species.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Avise JC, Hamrick JL (1996) Conservation genetics: case histories from nature. Chapman & Hall, New York

    Book  Google Scholar 

  • Azevedo VCR, Kanashiro M, Ciampi AY, Grattapaglia D (2007) Genetic structure and mating system of Manilkara huberi (Ducke) A. Chev., a heavily logged Amazonian timber species. J Hered 98(7):646–654

    Article  CAS  PubMed  Google Scholar 

  • Balloux F (2004) Heterozygote excess in small populations and the heterozygote-excess effective population size. Evolution 58(9):1891–1900

    Article  PubMed  Google Scholar 

  • Bittencourt JVM, Sebbenn AM (2009) Genetic effects of forest fragmentation in high-density Araucaria angustifolia populations in southern Brazil. Tree Genet Genomes 5(4):573–582

    Article  Google Scholar 

  • Bizoux JP, Daïnou K, Bourland N, Hardy OJ, Heuertz M, Mahy G, Doucet JL (2009) Spatial genetic structure in Milicia excelsa (Moraceae) indicates extensive gene dispersal in a low-density wind-pollinated tropical tree. Mol Ecol 18(21):4398–4408

    Article  CAS  PubMed  Google Scholar 

  • Bohonak AJ (2002) IBD (Isolation By Distance): a program for analyses of isolation by distance. J Hered 93:153–154

    Article  CAS  PubMed  Google Scholar 

  • Braga PIS (1979) Subdivisão fitogeográfica, tipos de vegetação, conservação e inventário florístico da floresta Amazônica. Supllemento Acta Amazonica 9:53–80

    Google Scholar 

  • Cavalcante MC (2008) Visitantes florais e poliniação da castanha-do-brasil (Bertholletia excelsa H.&B.) em cultivo na Amazônia central. Dissertation, Universidade Federal do Ceará

  • Cavalcante MC, Oliveira FF, Maués MM, Freitas BM (2012) Pollination requirements and the foraging behavior of potential pollinators of cultivated Brazil nut (Bertholletia excelsa Bonpl.) trees in Central Amazon rainforest. Psyche 2012:1–9

    Article  Google Scholar 

  • Clement CR, Cristo-Araújo MD, d’Eeckenbrugge GC, Pereira AA, Picanço-Rodrigues D (2010) Origin and domestication of native Amazonian crops. Diversity 2:72–106

    Article  Google Scholar 

  • Collevatti RG, Grattapaglia D, Hay JD (2001) Population genetic structure of the endangered tropical tree species Caryocar brasiliensis, based on variability at microsatellite loci. Mol Ecol 10(2):349–356

    Article  CAS  PubMed  Google Scholar 

  • Cotta JN, Kainer KA, Wadt LHO, Staudhammer CL (2008) Shifting cultivation effects on Brazil nut (Bertholletia excelsa) regeneration. Forest Ecol Manag 256:28–35

    Article  Google Scholar 

  • Doyle JJ, Doyle JL (1987) Isolation of plant DNA from fresh tissue. Focus 12:13–15

    Google Scholar 

  • Erickson DL, Hamrick JL, Kochert GD (2004) Ecological determinants of genetic diversity in an expanding population of the shrub Myrica cerifera. Mol Ecol 13:1655–1664

    Article  CAS  PubMed  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14(8):2611–2620

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed Central  Google Scholar 

  • Goudet J (1995) FSTAT (vers. 1.2): a computer program to calculate F statistics. J Hered 86:485–486

    Google Scholar 

  • Haffer J (1969) Speciation in Amazonian forest birds. Science 165:131–137

    Article  CAS  PubMed  Google Scholar 

  • Hamrick J, Godt M (1996) Effects of life history traits on genetic diversity in plant species. Philos Trans 351:1291–1298

    Article  Google Scholar 

  • Hansson B, Westerberg L (2002) On the correlation between heterozigosity and fitness in natural populations. Mol Ecol 11:2467–2474

    Article  PubMed  Google Scholar 

  • Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620

    Article  Google Scholar 

  • Haugaasen JM, Haugaasen T, Peres CA, Gribel R, Wegge P (2010) Seed dispersal of the Brazil nut tree (Bertholletia excelsa) by scatter-hoarding rodents in a central Amazonian forest. J Trop Ecol 26(3):251–262

    Article  Google Scholar 

  • Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Stat 6:65–67

    Google Scholar 

  • Hufford KM, Hamrick JL (2003) Viability selection at three early stages of the tropical tree, Platypodium elegans (Fabaceae, Papilionoideae). Evolution 57(3):518–526

    Article  PubMed  Google Scholar 

  • IBGE/SIDRA. Extração vegetal. http://www.sidra.ibge.gov.br/. Accessed 03 Oct 2010

  • IUCN 2010. IUCN Red List of Threatened Species. Version 2010.3. www.iucnredlist.org. Accessed 03 Oct 2010

  • Janzen DH (1971) Euglossine bees as long-distance pollinators of tropical plants. Science 171(3967):203–205

    Article  CAS  PubMed  Google Scholar 

  • Kalinowski ST (2009) How well do evolutionary trees describe genetic relationships between populations? Heredity 102:506–513

    Article  CAS  PubMed  Google Scholar 

  • Lacerda AE, Kanashiro M, Sebbenn AM (2008) Effects of reduced impact logging on genetic diversity and spatial genetic structure of a Hymenaea courbaril population in the Brazilian Amazon forest. For Ecol Manag 255(3):1034–1043

    Article  Google Scholar 

  • Le Guen V, Doaré F, Weber C, Seguin M (2009) Genetic structure of amazonian populations of Hevea brasiliensis is shaped by hydrographical network and isolation by distance. Tree Genet Genomes 5(4):673–683

    Article  Google Scholar 

  • Leite FAB, Brandão RL, de Oliveira Buzatti RS, de Lemos-Filho JP, Lovato MB (2014) Fine-scale genetic structure of the threatened rosewood Dalbergia nigra from the Atlantic forest: comparing saplings versus adults and small fragment versus continuous forest. Tree Genet Genomes 10(2):307–316

    Article  Google Scholar 

  • Lemes M, Gribel R, Proctor J, Grattapaglia D (2003) Population genetic structure of mahogany (Swietenia macrophylla King, Meliaceae) across the Brazilian Amazon, based on variation at microsatellite loci: implications for conservation. Mol Ecol 12:2875–2883

    Article  PubMed  Google Scholar 

  • Lewis PO, Zaykin D (2001) Genetic data analysis: computer program for the analysis of allelic data, 2001. Available at: http://lewis.eeb.uconn.edu/lewishome/software.html

  • Loiselle BA, Sork VL, Nasson J, Graham C (1995) Spatial genetic structure of a tropical understory shrub, Psychotria officinalis (Rubiaceae). Am J Bot 82:1420–1425

    Article  Google Scholar 

  • Maués MM (2002) Reprodutive phenology and pollination of the Brazil nut tree (Bertholletia excelsa Humb. & Bonpl., Lecythidaceae) in Eastern Amazonia. In: Kevan P, Imperatriz Fonseca VL (eds) Pollinating bees the conservation link between agriculture and nature. Ministry of Environment, Brasilia, pp 245–254

  • Medina SPG (2005) Frutíferas e plantas úteis na vida amazônica. CIFOR, Imazon, Belém

    Google Scholar 

  • Mori SA, Prance GT (1990) Taxonomy, ecology, and economic botany of the Brazil nut (Bertholletia excelsa Humb and Bonpl.: Lecythidaceae). Adv Econ Bot 8:130–150

    Google Scholar 

  • Müller CH, Rodrigues IA, Müller AA, Müller NRM (1980) Castanha-do-brasil: resultados de pesquisa. EMBRAPA-CPATU, Belém

    Google Scholar 

  • Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590

    CAS  PubMed Central  PubMed  Google Scholar 

  • O’Malley DM, Buckley DP, Prance GT, Bawa KS (1988) Genetics of Brazil Nut (Bertholletia excelsa Humb. & Bonpl.: Lecythidaceae). Theor Appl Genet 76:929–932

    Article  PubMed  Google Scholar 

  • Oliveira RS (2011) Dinâmica da regeneração e estrutura genética de Castanheira (Bertholletia excelsa Bonpl.) em duas populações exploradas no Vale do Rio Acre. Dissertation, Universidade Federal do Acre

  • Paiva PM, Guedes MC (2008) Regeneração natural de Castanha-do-Brasil (Bertholletia excelsa) em área de capoeira no Amapá. In: Anais do 1º Seminário do Projeto Kamukaia, pp 25–33

  • Paiva PM, Guedes MC, Funi C (2011) Brazil nut conservation through shifting cultivation. For Ecol Manag 261:508–514

    Article  Google Scholar 

  • Peres CA, Baider C (1997) Seed dispersal, spatial distribution and population structure of Brazilnut trees (Bertholletia excelsa) in southeastern Amazonia. J Trop Ecol 13:595–616

    Article  Google Scholar 

  • Peres CA, Baider C, Zuidema PA, Wadt LHO, Kainer KA, Gomes-Silva DAP, Salomão RP, Simões Luciana L, Franciosi ERN, Valverde FC, Gribel R, Shepard GH, Kanashiro M, Coventry P, Yu DW, Watkinson AR, Freckleton RP (2003) Demographic threats to the sustainability of Brazil nut exploitation. Science 302(5653):2112–2114

    Article  CAS  PubMed  Google Scholar 

  • Petit RJ, El Mousadik A, Pons O (1998) Identifying populations for conservation on the basis of genetic markers. Conserv Biol 12:844–855

    Article  Google Scholar 

  • Piotti A, Leonardi S, Heuertz M, Buiteveld J, Geburek T, Gerber S, Kramer K, Vettori C, Vendramin GG (2013) Within-population genetic structure in beech (Fagus sylvatica L.) Stands characterized by different disturbance histories: does forest management simplify population substructure? PLoS One 8(9):e73391

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155(2):945–959

    CAS  PubMed Central  PubMed  Google Scholar 

  • Reis A, Braga A, Lemes M, Gribel R, Collevatti R (2009) Development and characterization of microsatellite markers for the Brazil nut tree Bertholletia excelsa Humb. & Bonpl. (Lecythidaceae). Mol Ecol Resour 9(3):920–923

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4(4):406–425

    CAS  PubMed  Google Scholar 

  • Sampaio AJ (1942) A flora amazônica. RBG 4(2):57–72

    Google Scholar 

  • Schifino-Wittmann MT, Dall’Agnol M (2002) Auto-incompatibilidade em plantas. Ciência Rural 32:1083–1090

    Article  Google Scholar 

  • Scoles R, Gribel R (2011) Population structure of Brazil nut (Bertholletia excelsa, Lecythidaceae) stands in two areas with different occupation histories in the Brazilian Amazon. Hum Ecol 39:455–464

    Article  Google Scholar 

  • Shepard GH Jr, Ramirez H (2011) “Made in Brazil”: human dispersal of the Brazil nut (Bertholletia excelsa, Lecythidaceae) in ancient Amazonia. Econ Bot 65(1):44–65

    Article  Google Scholar 

  • Silva VS (2014) Sistema reprodutivo e diversidade genética de Bertholletia excelsa em diferentes ambientes no Estado do Acre. Dissertation, Universidade Federal do Acre

  • Sneath PHA, Soakal RR (1973) Numeral taxonomy. Freeman, San Francisco

    Google Scholar 

  • Sombroek W (2001) Spatial and temporal patterns of Amazon rainfall. Ambio 30(7):388–396

    CAS  PubMed  Google Scholar 

  • Sujii PS, Ciampi AY, Solferini VN, Azevedo VCR (2013) Isolation and characterization of microsatellite markers for Bertholletia excelsa (Lecythidaceae) population genetics analysis. Genet Mol Res (in press)

  • Tadaiesky N, Rebelo A, Vitor G (2008) Análise dos impactos ambientais provocados pelo turismo nos municípios de Bragança, Maracanã (Vila de Algodoal) e Salinópolis. In: Anais do Seminário Internacional de Turismo Sustentável, 2, Fortaleza

  • Tonini H, Costa P de, Kaminski PE (2009) Estrutura e produção de duas populações nativas de castanheira-do-brasil (Bertholletia excelsa O. Berg) em Roraima. FLORESTA 38(3): 445–457

  • Trivedi MR, Cornejo RH, Watkinson AR (2004) Seed predation on Brazil nuts (Bertholletia excelsa) by Macaws (Psittacidae) in Madre de Dios, Peru. Biotropica 36(1):118–122

    Google Scholar 

  • Vanzolini PE, Williams EE (1970) South American anoles: the geographic differentiation and evolution of Anolis chrysolepis species group (Sáuria, Iguanidae). Arq Zoo (São Paulo) 19:1–298

    Google Scholar 

  • Vekemans X, Hardy OJ (2004) New insights from fine-scale spatial genetic structure analyses in plant populations. Mol Ecol 13:921–935

    Article  CAS  PubMed  Google Scholar 

  • Vieira S, Trumbore S, Camargo PB, Selhorst D, Chambers JQ, Higuchi N (2005) Slow growth rates of Amazonian trees: consequences for carbon cycling. Proc Natl Acad Sci 102:18502–18507

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Vieira AH, Bentes-Gama MM, de Oliveira AC, Rocha RB, Locatelli M (2008) Comportamento Fenológico da Castanha-do-brasil (Bertholletia excelsa Bonpl.) em Porto Velho, Rondônia. In: Anais do 1º Seminário do Projeto Kamukaia, pp 53–57

  • Wadt LHO, Kainer KA, Gomes-Silva DAP (2005) Population structure and nut yield of Bertholletia excelsa stand in southwestern Amazonia. For Ecol Manag 211:371–384

    Article  Google Scholar 

  • Wadt LHO, Kainer KA, Staudhammer C, Serrano R (2008) Sustainable forest use in Brazilian extractive reserves: Natural regeneration of Brazil nut in exploited populations. Biol Conserv 141:332–346

    Article  Google Scholar 

  • Weir BS (1990) Genetic data analysis: methods for discrete population analysis. Sinauer Associates, Sunderland

    Google Scholar 

  • Weir B, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38(6):1358–1370

    Article  Google Scholar 

Download references

Acknowledgments

The authors would like to thank Dr. Ana Yamaguishi Ciampi, Lílian Maria da Silva Lima, and Paulo Emilio Kaminski for support on sample collection. We also thank Brazilian Agricultural Research Corporation (EMBRAPA) (units Acre, Genetic Resources and Biotechnology and Roraima) and Instituto de Desenvolvimento Agropecuário e Florestal Sustentável do Estado do Amazonas (IDAM). This work was funded by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP—Grant 09/50739-7 to VNS, fellowship to PSS), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Conselho Nacional de Desenvolvimento Científico e Tecnológico—CNPq (Proc 479626/2004-9), Natura Inovação e Tecnologia de Produtos Ltda (NATURA) and Fundação Arthur Bernardes (FUNARBE).

Author information

Authors and Affiliations

  1. Department of Genetics, Evolution and Bioagents, Institute of Biology, University of Campinas - Unicamp, PO Box: 6109, Campinas, SP, 13083-970, Brazil

    Patricia Sanae Sujii & Vera Nisaka Solferini

  2. Departamento de Biologia, Centro de Ciências Humanas e Biológicas, Universidade Federal de São Carlos, Campus Sorocaba, Rodovia João Leme dos Santos Km 110, Sorocaba, SP, Brazil

    Karina Martins

  3. Embrapa Acre, BR 364 km 14, Caixa Postal 321, Rio Branco, AC, Brazil

    Lucia Helena de Oliveira Wadt

  4. Laboratório de Genética Vegetal, Embrapa Recursos Genéticos e Biotecnologia, PqEB W5, Brasilia, DF, Brazil

    Vânia Cristina Rennó Azevedo

Authors
  1. Patricia Sanae Sujii
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Karina Martins
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lucia Helena de Oliveira Wadt
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Vânia Cristina Rennó Azevedo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Vera Nisaka Solferini
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Vera Nisaka Solferini.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 82 kb)

Supplementary material 2 (PDF 299 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sujii, P.S., Martins, K., Wadt, L.H.d. et al. Genetic structure of Bertholletia excelsa populations from the Amazon at different spatial scales. Conserv Genet 16, 955–964 (2015). https://doi.org/10.1007/s10592-015-0714-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-015-0714-4

Keywords

Search

Navigation