Skip to main content

Advertisement

SpringerLink
Log in

The role of very small fragments in conserving genetic diversity of a common tree in a hyper fragmented Brazilian Atlantic forest landscape

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

Abstract

In hyper fragmented biomes, conservation of extant biota relies on preservation and proper management of remnants. The maintenance of genetic diversity and functional connectivity in a landscape context is probably key to long-term conservation of remnant populations. We measured the genetic diversity in seedlings and adults of tree Copaifera langsdorffii and evaluated whether edge and density-dependent effects drive natural regeneration in a set of very small and degraded Brazilian Atlantic forest fragments. We evaluated the role of small remnants in the conservation of genetic diversity in a hyper fragmented landscape and discuss the challenge of long-term population sustainability of such altered habitats. High genetic diversity in adults indicated these fragments are valuable targets for C. langsdorffii in situ conservation, but both genetic diversity and divergence among patches decreased in seedlings. In our landscape, regeneration increased as it neared edges and adults; suggesting this population is resilient to fragmentation. However, at a broader scale, current levels of gene flow have not been sufficient to prevent the loss of genetic diversity across generations. Restoration plans, even at a small scale, are necessary to promote fragment connectivity and spatially expand opportunities for the fairly restricted gene flow observed in this severely fragmented Brazilian Atlantic forest region.

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

  • Aguilar R, Quesada M, Ashworth L, Herrerias-Diego Y, Lobo J (2008) Genetic consequences of habitat fragmentation in plant populations: susceptible signals in plant traits and methodological approaches. Mol Ecol 17:5177–5188. doi:10.1111/j.1365-294X.2008.03971.x

    Article  PubMed  Google Scholar 

  • Andreazzi CS, Pimenta CS, Pires AS, Fernandez FAZ, Oliveira-Santos LG, Menezes JFS (2012) Increased productivity and reduced seed predation favor a large-seeded palm in small Atlantic Forest fragments. Biotropica 44:237–245

    Article  Google Scholar 

  • Bacles CF, Jump AS (2011) Taking a tree’s perspective on forest fragmentation genetics. Trends Plant Sci 16:13–18. doi:10.1016/j.tplants.2010.10.002

    Article  CAS  PubMed  Google Scholar 

  • Brookfield JFY (1996) A simple new method for estimating null allele frequency from heterozygote deficiency. Mol Ecol Notes 5:453–455

    Article  CAS  Google Scholar 

  • Christianini AV, Oliveira PS (2013) Edge effects decrease ant-derived benefits to seedlings in a neotropical savanna. Arthropod-Plant Interactions 7:191–199. doi:10.1007/s11829-012-9229-9

    Article  Google Scholar 

  • Ciampi AY, Brondani RVP, Grattapaglia D (2000) Desenvolvimento de marcadores microssatélites para Copaifera langsdorffii Desf. (copaíba) Leguminosae—Caesalpinoideae e otimização de sistemas fluorescentes de genotipagem multiloco. vol 16. Embrapa Recursos Genéticos e Biotecnologia, Brasília

  • Cordeiro NJ, Howe HF (2003) Forest fragmentation severs mutualism between seed dispersers and an endemic African tree. Proc Natl Acad Sci USA 100:14052–14056. doi:10.1073/pnas.2331023100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Corrêa LS, Cardoso-Leite E, Castello ACD, Coelho S, Kortz AR, Villela FNJ, Koch I (2014) Estrutura, composição florística e caracterização sucessional em remanescente de floresta estacional semidecidual no sudeste do. Brasil Revista Árvore 38:799–809

    Article  Google Scholar 

  • Costa JAS (2007) Estudos taxonômicos, biossistemáticos e filogenéticos em Copaifera L. (Leguminosae: Detarieae) com ênfase nas espécies do brasil extra-amazônico. Universidade Estadual de Feira de Santana

  • Dabrowski MJ, Pilot M, Kruczyk M, Zmihorski M, Umer HM, Gliwicz J (2014) Reliability assessment of null allele detection: inconsistencies between and within different methods. Mole Ecol Resour 14:361–373. doi:10.1111/1755-0998.12177

    Article  CAS  Google Scholar 

  • Dabrowski MJ, Bornelov S, Kruczyk M, Baltzer N, Komorowski J (2015) ‘True’ null allele detection in microsatellite loci: a comparison of methods, assessment of difficulties and survey of possible improvements. Mole Ecol Resour 15:477–488. doi:10.1111/1755-0998.12326

    Article  CAS  Google Scholar 

  • Dayanandan S, Dole J, Bawa K, Kesseli R (1999) Population structure delineated with microsatellite markers in fragmented populations of a tropical tree, Carapa guianensis (Meliaceae). Mol Ecol 8:1585–1592

    Article  PubMed  Google Scholar 

  • de Mello K, Petri L, Cardoso-Leite E, Toppa RH (2014) Cenários ambientais para o ordenamento territorial de áreas de preservação permanente no município de Sorocaba, SP. Revista Árvore 38:309–317

    Article  Google Scholar 

  • Demšar U, Harris P, Brunsdon C, Fotheringham AS, McLoone S (2013) Principal component analysis on spatial data: an overview. Ann Assoc Am Geogr 103:106–128. doi:10.1080/00045608.2012.689236

    Article  Google Scholar 

  • Dirzo R, Miranda A (1991) Altered patterns of herbivory and diversity in the forest understory: A case study of the possible consequences of contemporary defaunation. In: Price PW, Lewinsohn TM, Fernandes GW, Benson WW (eds) Plant-animal interactions: Evolutionary ecology in tropical and temperate regions. Wiley, New York, pp 273–287

    Google Scholar 

  • Dirzo R, Young HS, Galetti M, Ceballos G, Isaac NJB, Coll B (2014) Defaunation in the Anthropocene. Science 345:401–406

    Article  CAS  PubMed  Google Scholar 

  • Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15

    Google Scholar 

  • El Mousadik A, Petit RJ (1996) High level of genetic differentiation for allelic richness among populations of the argan tree [Argania spinosa (L.) Skeels] endemic to Morocco. Theor Appl Genet 92:832–839

    Article  PubMed  Google Scholar 

  • Ewers RM, Thorpe S, Didham RK (2007) Synergistic interactions between edge and area effects in a heavily fragmented landscape. Ecology 88:96–106

    Article  PubMed  Google Scholar 

  • Finger A, Kettle CJ, Kaiser-Bunbury CN, Valentin T, Mougal J, Ghazoul J (2012) Forest fragmentation genetics in a formerly widespread island endemic tree: vateriopsis seychellarum (Dipterocarpaceae). Mol Ecol 21:2369–2382. doi:10.1111/j.1365-294X.2012.05543.x

    Article  CAS  PubMed  Google Scholar 

  • Fletcher RJ Jr (2005) Multiple edge effects and their implications in fragmented landscapes. J Anim Ecol 74:342–352. doi:10.1111/j.1365-2656.2005.00930

    Article  Google Scholar 

  • Freitas CV, Oliveira PE (2002) Biologia reprodutiva de Copaifera langsdorffii Desf. (Leguminosae, Caesalpinioideae). Revista Brasileira de Botânica 25:311–321

    Google Scholar 

  • Ganzhorn SM, Perez-Sweeney B, Thomas WW, Gaiotto FA, Lewis JD (2015) Effects of fragmentation on density and population genetics of a threatened tree species in a biodiversity hotspot. Endanger Species Res 26:189–199. doi:10.3354/esr00645

    Article  Google Scholar 

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

    Google Scholar 

  • Guillot G, Estoup A, Mortier F, Cosson JF (2005a) A spatial statistical model for landscape genetics. Genetics 170:1261–1280. doi:10.1534/genetics.104.033803

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guillot G, Mortier F, Estoup A (2005b) Geneland: a computer package for landscape genetics. Mol Ecol Notes 5:712–715. doi:10.1111/j.1471-8286.2005.01031.x

    Article  CAS  Google Scholar 

  • Haddad NK, Brudvig LA, Clobert J, Davies KF, Gonzalez A et al (2015) Habitat fragmentation and its lasting impact on Earth’s ecosystems. Sci Adv. doi:10.1126/sciadv.1500052

    PubMed  PubMed Central  Google Scholar 

  • Hamrick JL (2004) Response of forest trees to global environmental changes. For Ecol Manage 197:323–335. doi:10.1016/j.foreco.2004.05.023

    Article  Google Scholar 

  • Harms KE, Wright SJ, Calderón O, Hernández A, Herre EA (2000) Pervasive density-dependent recruitment enhances seedling diversity in a tropical forest. Nature 404:493–495

    Article  CAS  PubMed  Google Scholar 

  • Isagi Y, Tateno R, Matsuki Y, Hirao A, Watanabe S, Shibata M (2007) Genetic and reproductive consequences of forest fragmentation for populations of Magnolia obovata. Ecol Res 22:382–389. doi:10.1007/s11284-007-0360-5

    Article  Google Scholar 

  • Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405. doi:10.1093/bioinformatics/btn129

    Article  CAS  PubMed  Google Scholar 

  • Jombart T, Devillard S, Dufour AB, Pontier D (2008) Revealing cryptic spatial patterns in genetic variability by a new multivariate method. Heredity (Edinb) 101:92–103. doi:10.1038/hdy.2008.34

    Article  CAS  Google Scholar 

  • Kortz AR, Coelho S, Castello ACD, Corrêa LS, Cardoso-Leite E, Koch I (2014) Wood vegetation in Atlantic rain forest remnants in Sorocaba (São Paulo, Brazil). Check List 10:344–354

    Article  Google Scholar 

  • Kramer AT, Ison JL, Ashley MV, Howe HF (2008) The paradox of forest fragmentation genetics. Conserv Biol 22:878–885. doi:10.1111/j.1523-1739.2008.00944.x

    Article  PubMed  Google Scholar 

  • Laurance WF (2002) Hyperdynamism in fragmented habitats. J Veg Sci 13:595–602

    Article  Google Scholar 

  • Laurance WF et al (2011) The fate of Amazonian forest fragments: a 32-year investigation. Biol Conserv 144:56–67. doi:10.1016/j.biocon.2010.09.021

    Article  Google Scholar 

  • Lowe AJ, Boshier D, Ward M, Bacles CF, Navarro C (2005) Genetic resource impacts of habitat loss and degradation; reconciling empirical evidence and predicted theory for neotropical trees. Heredity 95:255–273. doi:10.1038/sj.hdy.6800725

    Article  CAS  PubMed  Google Scholar 

  • Malcolm JR (1994) Edge effects in Central Amazonian forest fragments. Ecology 75:2438–2445

    Article  Google Scholar 

  • Manoel RO, Alves PF, Dourado CL, Gaino APSC, Freitas MLM, Moraes MLT, Sebbenn AM (2012) Contemporary pollen flow, mating patterns and effective population size inferred from paternity analysis in a small fragmented population of the Neotropical tree Copaifera langsdorffii Desf. (Leguminosae-Caesalpinioideae). Conserv Genet 13:613–623. doi:10.1007/s10592-011-0311-0

    Article  Google Scholar 

  • Markl JS et al (2012) Meta-analysis of the effects of human disturbance on seed dispersal by animals. Conserv Biol 26:1072–1081. doi:10.1111/j.1523-1739.2012.01927.x

    Article  PubMed  Google Scholar 

  • Martins K, Santos JD, Gaiotto FA, Moreno MA, Kageyama PY (2008) Estrutura genética populacional de Copaifera langsdorffii Desf. (Leguminosae - Caesalpinioideae) em fragmentos florestais no Pontal do Paranapanema, SP, Brasil. Revista Brasileira de Botânica 31:61–69. doi:10.1590/S0100-84042008000100007

    Google Scholar 

  • Motta Junior JC, Lombardi JA (1990) Aves como agentes dispersores de copaíba (Copaifera langsdorffii, Caesalpiniaceae) em São Carlos, estado de São Paulo. Ararajuba 1:105–106

    Google Scholar 

  • Murcia C (1995) Edge effects in fragmented forests: implications for conservation. Trends Ecol Evol 10:58–62. doi:10.1016/S0169-5347(00)88977-6

    Article  CAS  PubMed  Google Scholar 

  • Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858. doi:10.1038/35002501

    Article  CAS  PubMed  Google Scholar 

  • Oliveira-Filho A, Camisão-Neto AA, Volpato MML (1996) Structure and dispersion of four tree populations in an area of montane semidecidous forest in southeastern Brazil. Biotropica 28:762–769

    Article  Google Scholar 

  • Pedroni F, Sanchez M, Santos FAM (2002) Fenologia da copaíba (Copaifera langsdorffii Desf.—Leguminosae, Caesalpinioideae) em uma floresta semidecídua no sudeste do Brasil. Revista Brasileira de Botânica 25:183–194

    Google Scholar 

  • Peres CA, Palacios E (2007) Basin-wide effects of game harvest on vertebrate population densities in amazonian forests: implications for animal-mediated seed dispersal. Biotropica 39:304–315

    Article  Google Scholar 

  • Pütz S, Groeneveld J, Alves LF, Metzger JP, Huth A (2011) Fragmentation drives tropical forest fragments to early successional states: a modelling study for Brazilian Atlantic forests. Ecol Model 222:1986–1997. doi:10.1016/j.ecolmodel.2011.03.038

    Article  Google Scholar 

  • R CoreTeam (2015) R: A language and environment for statistical computing. Vienna, Austria

  • Ribeiro RA, Simoes Ramos AC, De Lemos Filho JP, Lovato MB (2005) Genetic variation in remnant populations of Dalbergia nigra (Papilionoideae), an endangered tree from the Brazilian Atlantic Forest. Ann Bot 95:1171–1177. doi:10.1093/aob/mci128

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ribeiro MC, Metzger JP, Martensen AC, Ponzoni FJ, Hirota MM (2009) The Brazilian Atlantic Forest: how much is left, and how is the remaining forest distributed? Implications for conservation. Biol Conserv 142:1141–1153. doi:10.1016/j.biocon.2009.02.021

    Article  Google Scholar 

  • Santos BA, Peres CA, Oliveira MA, Grillo A, Alves-Costa CP, Tabarelli M (2008) Drastic erosion in functional attributes of tree assemblages in Atlantic forest fragments of northeastern Brazil. Biol Conserv 141:249–260. doi:10.1016/j.biocon.2007.09.018

    Article  Google Scholar 

  • Saunders DA, Hobbs RJ, Margules CR (1991) Biological consequences of ecosystem fragmentation: a review. Conserv Biol 5:18–32

    Article  Google Scholar 

  • Scofield DG, Smouse PE, Karubian J, Sork VL (2012) Use of alpha, beta, and gamma diversity measures to characterize seed dispersal by animals. Am Nat 180:719–732. doi:10.1086/668202

    Article  PubMed  Google Scholar 

  • Sebbenn AM et al (2011) Low levels of realized seed and pollen gene flow and strong spatial genetic structure in a small, isolated and fragmented population of the tropical tree Copaifera langsdorffii. Desf Hered (Edinb) 106:134–145. doi:10.1038/hdy.2010.33

    Article  CAS  Google Scholar 

  • Sheil D, Burslem DFRP, Alder D (1995) The interpretation and misinterpretation of mortality rate measures. J Ecol 83:331–333

    Article  Google Scholar 

  • Sork VL, Smouse PE (2006) Genetic analysis of landscape connectivity in tree populations. Landsc Ecol 21:821–836. doi:10.1007/s10980-005-5415-9

    Article  Google Scholar 

  • Sork VL, Smouse PE, Grivet D, Scofield DG (2015) Impact of asymmetric male and female gamete dispersal on allelic diversity and spatial genetic structure in valley oak (Quercus lobata Née). Evol Ecol 29(6):927–945

    Article  Google Scholar 

  • Tabarelli M, Lopes AV (2008) Edge-effects drive tropical forest fragments towards an early-successional system. Biotropica 40:657–661

    Article  Google Scholar 

  • Tabarelli M, Aguiar AV, Ribeiro MC, Metzger JP, Peres CA (2010) Prospects for biodiversity conservation in the Atlantic Forest: lessons from aging human-modified landscapes. Biol Conserv 143:2328–2340. doi:10.1016/j.biocon.2010.02.005

    Article  Google Scholar 

  • Tarazi R, Sebbenn AM, Kageyama PY, Vencovsky R (2013a) Edge effects enhance selfing and seed harvesting efforts in the insect-pollinated Neotropical tree Copaifera langsdorffii (Fabaceae). Heredity 110:578–585. doi:10.1038/hdy.2013.8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tarazi R, Sebbenn AM, Kageyama PY, Vencovsky R (2013b) Long-distance dispersal in a fire- and livestock-protected savanna. Ecol Evol 3:1003–1015. doi:10.1002/ece3.515

    Article  PubMed  PubMed Central  Google Scholar 

  • Templeton AR, Shaw K, Routman R, Davis SK (1990) The genetic consequences of habitat fragmentation. Ann Mo Bot Gard 77:13–27

    Article  Google Scholar 

  • Terborgh J (2013) Using Janzen-Connell to predict the consequences of defaunation and other disturbances of tropical forests. Biol Conserv 163:7–12. doi:10.1016/j.biocon.2013.01.015

    Article  Google Scholar 

  • Turner IM (1996) Species loss in fragments of tropical rain forest: a review of the evidence. J Appl Ecol 33:200–209

    Article  Google Scholar 

  • 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 4:535–538. doi:10.1111/j.1471-8286.2004.00684.x

    Article  Google Scholar 

  • Villard M-A, Metzger JP, Saura S (2014) REVIEW: beyond the fragmentation debate: a conceptual model to predict when habitat configuration really matters. J Appl Ecol 51:309–318. doi:10.1111/1365-2664.12190

    Article  Google Scholar 

  • White GM, Boshier DH, Powell W (2002) Increased pollen flow counteracts fragmentation in a tropical dry forest: an example from Swietenia humilis Zuccarini. Proc Natl Acad Sci USA 99:2038–2042. doi:10.1073/pnas.042649999

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Whittaker RH (1972) Evolution and measurement of species diversity. Taxon 21:213–251

    Article  Google Scholar 

  • Young A, Boyle T, Brown T (1996) The population genetic consequences of habitat fragmentation for plants. Trends Ecol Evol 11:6

    Article  Google Scholar 

Download references

Acknowledgments

We thank Ivonir Piotrowski, João Paulo de S. Curti and Thiago P. Telatin for helping in field work, and the owners of Fazenda São Roque, Fazenda Flores, and Ecoresidencial Fazenda Jequitibá for authorizing field work in their farms. We also thank Victoria Sork for her insightful comments on the first versions of this manuscript and Carla Américo for drawing the map. Two anonymous reviewers helped improve the manuscript. We finally thank São Paulo Research Foundation (FAPESP) grant 2012/01274-4 and FAPESP-University of Florida grant 2013/50119-4 for financial support. AFF received scientific initiation scholarships from National Council for Scientific and Technological Development (CNPq) in 2012 and from FAPESP in 2013 (Grant 2012/20363-8).

Author information

Authors and Affiliations

  1. Departamento de Biologia, Universidade Federal de São Carlos, Rodovia João Leme dos Santos, Km 110, Sorocaba, SP, 18052-780, Brazil

    Karina Martins, Renato Kenji Kimura & Ana Flávia Francisconi

  2. School of Forest Resources and Conservation, University of Florida, PO Box 110410, Gainesville, FL, 32611-0410, USA

    Salvador Gezan & Karen Kainer

  3. Center for Latin American Studies, Tropical Conservation and Development Program, University of Florida, Gainesville, FL, USA

    Karen Kainer

  4. Departamento de Ciências Ambientais, Universidade Federal de São Carlos, Rodovia João Leme dos Santos, Km 110, Sorocaba, SP, 18052-780, Brazil

    Alexander V. Christianini

Authors
  1. Karina Martins
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Renato Kenji Kimura
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ana Flávia Francisconi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Salvador Gezan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Karen Kainer
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Alexander V. Christianini
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Karina Martins.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 2247 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Martins, K., Kimura, R.K., Francisconi, A.F. et al. The role of very small fragments in conserving genetic diversity of a common tree in a hyper fragmented Brazilian Atlantic forest landscape. Conserv Genet 17, 509–520 (2016). https://doi.org/10.1007/s10592-015-0800-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-015-0800-7

Keywords

Search

Navigation