Abstract
Gene flow may occur both through pollen movement and seed dispersal, although their relative contribution to overall species gene flow is not understood for most tropical trees, which compromises management recommendations. We investigated the implications of seed dispersal limitation, pollen dispersal capacity, and mating system to the spatial genetic structure of populations of the Neotropical legume tree, Centrolobium tomentosum, in Brazil’s Atlantic Forest. We estimated seed dispersal distribution by counting individuals around adult trees; pollen dispersal distribution and outcrossing rates from adult and offspring genotypes, using seven microsatellite loci. Spatial genetic structure was inferred through the correlation among kinship coefficients and geographical distances between pairs of individuals, using nuclear and chloroplast microsatellite markers. We observed restricted seed dispersal, with most seeds (78%) falling up to 10 m from the adult tree trunk. The best-fitted pollen dispersal distribution was the exponential power distribution, with a heavy tail and average pollen dispersal distance of 3191 m. The mating system was preferably allogamous, with an average of eight pollen donors. There was significant spatial genetic structure in all populations, with stronger structure obtained from chloroplast DNA, which suggests that the restricted gene flow by seed dispersal may be compensated by high outcrossing rates and long-distance pollen flow promoted by the large bees that pollinate the species. Our results emphasize the importance of pollination services in fragmented tropical landscapes, where most tree species are pollinated by animals and a large number of species experience seed dispersal limitation.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Aguilar R, Ashworth L, Galetto L, Aizen MA (2006) Plant reproductive susceptibility to habitat fragmentation: review and synthesis through a meta-analysis. Ecol Lett 9(8):968–980. https://doi.org/10.1111/j.1461-0248.2006.00927.x
Aidar MPM (1992) Ecologia do araribá (Centrolobium tomentosum Guill. ex Benth - Fabaceae) e o ecótono mata ciliar da bacia do rio Jacaré-Pepira, São Paulo. Dissertation. Universidade Estadual de Campinas, Campinas
Aidar MPM, Joly CA (2003) Dinâmica da produção e decomposição da serapilheira do araribá (Centrolobium tomentosum Guill. ex Benth.—Fabaceae) em uma mata ciliar, Rio Jacaré-Pepira, São Paulo. Braz J Bot Bot 26(2):193–202. https://doi.org/10.1590/S0100-84042003000200007
Aizen MA, Ashworth L, Galetto L (2002) Reproductive success in fragmented habitats: do compatibility systems and pollination specialization matter? J Veg Sci 13(6):885–892. https://doi.org/10.1111/j.1654-1103.2002.tb02118.x
Austerlitz F, Smouse PE (2001) Two-generation analysis of pollen flow across a landscape. II. Relation between Φft, pollen dispersal and interfemale distance. Genetics 157(2):851–857
Banks-Leite C, Pardini R, Tambosi LR, Pearse WD, Bueno AA, Bruscagin RT, Condez TH, Dixo M, Igari AT, Martensen AC, Metzger JP (2014) Using ecological thresholds to evaluate the costs and benefits of set-asides in a biodiversity hotspot. Science 345:1041–1045. https://doi.org/10.1126/science.1255768
Basey AC, Fant JB, Kramer AT (2015) Producing native plant materials for restoration: 10 rules to collect and maintain genetic diversity. NPJ 16(1):37–53. https://doi.org/10.3368/npj.16.1.37
Bawa KS (1974) Breeding systems of tree species of a lowland tropical community. Evol 28(1):85–92. https://doi.org/10.2307/2407241
Bawa KS (1990) Plant-pollinator interactions in tropical rain forests. Annu Rev Ecol Evol Syst 21:399–422. https://doi.org/10.1146/annurev.es.21.110190.002151
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 8(21):4398–408. https://doi.org/10.1111/j.1365-294X.2009.04365.x
Brancalion PH, Pinto SR, Pugliese L, Padovezi A, Rodrigues RR, Calmon M, Carrascosa H, Castro P, Mesquita B (2016) Governance innovations from a multi-stakeholder coalition to implement large-scale Forest Restoration in Brazil. World Dev Perspect 3:15–17. https://doi.org/10.1016/j.wdp.2016.11.003
Brancalion PHS, Bello C, Chazdon RL, Galetti M, Jordano P, RaF L, Medina A, Pizo MA, Reid JL (2018) Maximizing biodiversity conservation and carbon stocking in restored tropical forests. Conser Lett 11(4):e12454. https://doi.org/10.1111/conl.12454
Breed MF, Gardner MG, Ottewell KM, Navarro CM, Lowe AJ (2012) Changing trade-offs between inbreeding costs and reproductive assurance in Central American big-leaf mahogany (Swietenia macrophylla). Ecol Lett 15:444–452. https://doi.org/10.1111/j.1461-0248.2012.01752.x
Breed MF, Stead MG, Ottewell KM, Gardner MG, Lowe AJ (2013) Which provenance and where? Seed sourcing strategies for revegetation in a changing environment. Conserv Gen 14(1):1–10. https://doi.org/10.1007/s10592-012-0425-z
Carvalho PER (2005) Araruva. Embrapa Circular Técnica. Embrapa Forests, Colombo. https://www.infoteca.cnptia.embrapa.br/infoteca/bitstream/doc/281611/1/circtec103.pdf
Cavallari MM, Siqueira MV, Val TM et al (2014) A modified acidic approach for DNA extraction from plant species containing high levels of secondary metabolites. Gen Mol Res 13(3):6497–6502. https://doi.org/10.4238/2014.August.25.13
Chung MG, Epperson BK (2000) Clonal and spatial genetic structure in Eurya emarginata (Theaceae). Heredity 84(2):170–177. https://doi.org/10.1046/j.1365-2540.2000.00644.x
Cockerham CC (1969) Variance of gene frequencies. Evolution 23(1):72–84. https://doi.org/10.1111/j.1558-5646.1969.tb03496.x
Corriveau JL, Coleman AW (1988) Rapid screening method to detect potential biparental inheritance of plastid DNA and results for over 200 angiosperm species. Am J Bot 75(10):1443–1458. https://doi.org/10.1002/j.1537-2197.1988.tb11219.x
Dick CW, Hardy OJ, Jones FA, Petit RJ (2008) Spatial scales of pollen and seed-mediated gene flow in tropical rain forest trees. Trop Plant Biol 1(1):20–33. https://doi.org/10.1007/s12042-007-9006-6
Dixon KW (2009) Pollination and restoration. Science 325(5940):571–573. https://doi.org/10.1126/science.1176295
Durigan G, Franco GADC, Saito M et al (2000) Estrutura e diversidade do componente arbóreo da floresta na Estação Ecológica dos Caetetus, Gália, SP. Rev Bras Bot 23:371–383. https://doi.org/10.1590/S0100-84042000000400003
Dutech C, Seiter J, Petronelli P, Joly HI, Jarne P (2002) Evidence of low gene flow in a neotropical clustered tree species in two rainforest stands of French Guiana. Mol Ecol 11(4):725–738. https://doi.org/10.1046/j.1365-294X.2002.01475.x
Eckert CG, Kalisz S, Geber MA, Sargent R, Elle E, Cheptou PO, Goodwillie C, Johnston MO, Kelly JK, Moeller DA, Porcher E (2010) Plant mating systems in a changing world. TREE 25(1):35–43. https://doi.org/10.1016/j.tree.2009.06.013
Epperson BK (2007) Plant dispersal, neighbourhood size and isolation by distance. Mol Ecol 16(18):3854–3865. https://doi.org/10.1111/j.1365-294X.2007.03434.x
Farah FT, Rodrigues RR, Santos FAM et al (2014) Forest destructuring as revealed by the temporal dynamics of fundamental species—case study of Santa Genebra Forest in Brazil. Ecol Indic 37:40–44. https://doi.org/10.1016/j.ecolind.2013.09.011
Frankham R (1995) Effective population size/adult population size ratios in wildlife: a review. Gen Res 66(2):95–107. https://doi.org/10.1017/S0016672300034455
Frankham R, Bradshaw CJ, Brook BW (2014) Genetics in conservation management: revised recommendations for the 50/500 rules, Red List criteria and population viability analyses. Biol Conser 170:56–63. https://doi.org/10.1016/j.biocon.2013.12.036
Gallo L, Marchelli P (2014) Gene flow in the restoration of forest ecosystems. Genetic considerations in ecosystem restoration using native tree species. FAO and Biodiversity International, Rome
Garcia C, Arroy JM, Godoy JA, Jordano P (2005) Mating patterns, pollen dispersal, and the ecological maternal neighbourhood in a Prunusmahaleb L. population. Mol Ecol 14(6):1821–1830. https://doi.org/10.1111/j.1365-294X.2005.02542.x
Greene DF, Johnson EA (1998) Seed mass and early survivorship of tree species in upland clearings and shelterwoods. Can J Forest Res 28(9):1307–1316. https://doi.org/10.1139/x98-106
Griffin AR, Potts BM, Vaillancourt RE, Bell JC (2019) Life cycle expression of inbreeding depression in Eucalyptusregnans and inter-generational stability of its mixed mating system. Ann Bot 124(1):179–187. https://doi.org/10.1093/aob/mcz059
Hagen M, Wikelski M, Kissling WD (2011) Space use of bumblebees (Bombus spp.) revealed by radio-tracking. PLoS ONE 6(5):e19997. https://doi.org/10.1371/journal.pone.0019997
Hamrick JL (2004) Response of forest trees to global environmental changes. For Ecol Manag 197(1–3):323–335. https://doi.org/10.1016/j.foreco.2004.05.023
Hamrick JL, Godt MW (1996) Effects of life history traits on genetic diversity in plant species. Philos Trans R Soc B 351(1345):1291–1298. https://doi.org/10.1098/rstb.1996.0112
Hamrick JL, Murawski DA, Nason JD (1993) The influence of seed dispersal mechanisms on the genetic structure of tropical tree populations. Vegetation 107(1):281–297. https://doi.org/10.1007/BF00052230
Hardy OJ, Vekemans X (1999) Isolation by distance in a continuous population: reconciliation between spatial autocorrelation analysis and population genetics models. Heredity 83(2):145–154. https://doi.org/10.1046/j.1365-2540.1999.00558.x
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(4):618–620. https://doi.org/10.1046/j.1471-8286.2002.00305.x
Hardy OJ, Maggia L, Bandou E, Breyne P, Caron H, Chevallier MH, Doligez A, Dutech C, Kremer A, Latouch-Hallé CÉ, Troispoux V (2006) Fine-scale genetic structure and gene dispersal inferences in 10 Neotropical tree species. Mol Ecol 15(2):559–571. https://doi.org/10.1111/j.1365-294X.2005.02785.x
Harris LF, Johnson SD (2004) The consequences of habitat fragmentation for plant-pollinator mutualisms. Int J Trop Insect Sci 24(1):29–43. https://doi.org/10.1079/IJT20049
He T, Rao G, You R, Ge S, Hong D (2000) Spatial autocorrelation of genetic variation in three stands of Ophiopogon xylorrhizus (Liliaceae sl). Ann Bot 86(1):113–121. https://doi.org/10.1006/anbo.2000.1166
Jha S, Dick CW (2010) Native bees mediate long-distance pollen dispersal in a shade coffee landscape mosaic. PNAS 107(31):13760–13764. https://doi.org/10.1073/pnas.1002490107
Jump AS, Rico L, Coll M, Penuelas J (2012) Wide variation in spatial genetic structure between natural populations of the European beech (Fagus sylvatica) and its implications for SGS comparability. Heredity 108(6):633–639. https://doi.org/10.1038/hdy.2012.1
Keasar T, Shmida A, Motro U (1996) Innate movement rules in foraging bees: flight distances are affected by recent rewards and are correlated with choice of flower type. Behav Ecol Sociobiol 39(6):381–388. https://doi.org/10.1007/s002650050304
Keenan K, McGinnity P, Cross TF, Crozier WW, Prodöhl PA (2013) diveRsity: An R package for the estimation and exploration of population genetics parameters and their associated errors. Methods Ecol Evol 4(8):782–788. https://doi.org/10.1111/2041-210X.12067
Koeppen W (1948) Climatologia: con un estudio de los climas de la tierra. Fondo de Cultura Econômica, Mexico
Lacerda AEB, Kanashiro M, Sebbenn AM (2008) Long-pollen movement and deviation of random mating in a low-density continuous population of a tropical tree Hymenaea courbaril in the Brazilian Amazon. Biotropica 40(4):462–470. https://doi.org/10.1111/j.1744-7429.2008.00402.x
Lander TA, Boshier DH, Harris SA (2010) Fragmented but not isolated: contribution of single trees, small patches and long-distance pollen flow to genetic connectivity for Gomortega keule, an endangered Chilean tree. Biol Conserv 143(11):2583–2590. https://doi.org/10.1016/j.biocon.2010.06.028
Latouche-Hallé C, Ramboer A, Bandou E, Caron H, Kremer A (2004) Long-distance pollen flow and tolerance to selfing in a neotropical tree species. Mol Ecol 13(5):1055–1064. https://doi.org/10.1111/j.1365-294X.2004.02127.x
Loiselle BA, Sork VL, Nason J, Graham C (1995) Spatial genetic structure of a tropical understory shrub, Psychotria officinalis (Rubiaceae). Am J Bot 82(11):1420–1425. https://doi.org/10.2307/2445869
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. https://doi.org/10.1038/sj.hdy.6800725
Luna R, Epperson BK, Oyama K (2007) High levels of genetic variability and inbreeding in two Neotropical dioecious palms with contrasting life histories. Heredity 99(4):466–476. https://doi.org/10.1038/sj.hdy.6801027
Menz MH, Phillips RD, Winfree R, Kremen C, Aizen MA, Johnson SD, Dixon KW (2011) Reconnecting plants and pollinators: challenges in the restoration of pollination mutualisms. Trends Plant Sc 16(1):4–12. https://doi.org/10.1016/j.tplants.2010.09.006
Mijangos JL, Pacioni C, Spencer P, Craig MD (2015) Contribution of genetics to ecological restoration. Mol Ecol 24(1):22–37. https://doi.org/10.1111/mec.12995
Mills LS (2013) Conservation of wildlife populations: demography, genetics, and management. Wiley, West Sussex
Mitchell RJ, Flanagan RJ, Brown BJ, Waser NM, Karron JD (2009) New frontiers in competition for pollination. Ann Bot 103(9):1403–1413. https://doi.org/10.1093/aob/mcp062
Morellato LPC (1991) Estudo da fenologia de árvores, arbustos e lianas de uma floresta semi-decídua no Sudeste do Brasil. Universidade Estadual de Campinas, Campinas
Nielsen LR, Kjær ED (2010) Fine-scale gene flow and genetic structure in a relic Ulmus laevis population at its northern range. Tree Genet Genom 6(5):643–649. https://doi.org/10.1007/s11295-010-0280-3
Nogueira JCB (1977) Reflorestamento heterogêneo em essências indígenas. Instituto Florestal, São Paulo
Nunney L (1993) The influence of mating system and overlapping generations on effective population size. Evol 47(5):1329–1341. https://doi.org/10.1111/j.1558-5646.1993.tb02158.x
Pagano MC (2008) Rhizobia associated with neotropical tree Centrolobium tomentosum used in riparian restoration. Plant Soil Environ 54:498–508
Palstra FP, Fraser DJ (2012) Effective/census population size ratio estimation: a compendium and appraisal. Ecol Evol 2(9):2357–2365. https://doi.org/10.1002/ece3.329
Pasquet RS, Peltier A, Hufford MB, Oudin E, Saulnier J, Paul L, Knudsen JT, Herren HR, Gepts P (2008) Long-distance pollen flow assessment through evaluation of pollinator foraging range suggests transgene escape distances. PNAS 105(36):13456–13461. https://doi.org/10.1073/pnas.0806040105
Petit RJ, Hampe A (2006) Some evolutionary consequences of being a tree. Annu Rev Ecol Evol Syst 37:187–214. https://doi.org/10.1146/annurev.ecolsys.37.091305.110215
Portela RM, Tambarussi EV, de Aguiar AV et al (2020) Using a coalescent approach to assess gene flow and effective population size of Acrocomia aculeata (Jacq.) Lodd. Ex Mart. in the Brazilian Atlantic Forest. Tree Genet Genom 16:35. https://doi.org/10.1007/s11295-020-1426-6
Proft KM, Jones ME, Johnson CN, Burridge CP (2018) Making the connection: expanding the role of restoration genetics in restoring and evaluating connectivity. Rest Ecol 26(3):411–418. https://doi.org/10.1111/rec.12692
R Core Team (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
Reflora (2017) Herbário Virtual Reflora. Jardim Botânico do Rio de Janeiro. Available at http://www.herbariovirtualreflora.jbrj.gov.br. Accessed 27 July 2020
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. https://doi.org/10.1016/j.biocon.2009.02.021
Ritland K (1989) Correlated matings in the partial selfer Mimulus guttatus. Evol 43(4):848–859. https://doi.org/10.1111/j.1558-5646.1989.tb05182.x
Ritland K (2002b) Extensions of models for the estimation of mating systems using n independent loci. Heredity 88(4):221–228. https://doi.org/10.1038/sj.hdy.6800029
Ritland K (2002a). MLTR: a program to estimate multilocus out-crossing rate. http://genetics.forestry.ubc.ca/ritland/programs.html
Ritland K, Jain S (1981) A model for the estimation of outcrossing rate and gene frequencies using n independent loci. Heredity 47(1):35–52. https://doi.org/10.1038/hdy.1981.57
Robledo-Arnucio JJ, Austerlitz F, Smouse PE (2007) POLDISP: a software package for indirect estimation of contemporary pollen dispersal. Mol Ecol Notes 7(5):763–766. https://doi.org/10.1111/j.1471-8286.2007.01706.x
Rodrigues RR, Leitão Filho HDF, Crestana MSM (1992) Revegetação do entorno da represa de abastecimento de água do município de Iracemápolis, SP. Simpósio sobre recuperação de áreas degradadas. Anais, Curitiba
Rodrigues RR, Lima RA, Gandolfi S, Nave AG (2009) On the restoration of high diversity forests: 30 years of experience in the Brazilian Atlantic Forest. Biol Conserv 142(6):1242–1251. https://doi.org/10.1016/j.biocon.2008.12.008
Sant’Anna CS, Sebbenn AM, Klabunde GH, Bittencourt R, Nodari RO, Mantovani A, dos Reis MS (2013) Realized pollen and seed dispersal within a continuous population of the dioecious coniferous Brazilian pine [Araucaria angustifolia (Bertol.) Kuntze]. Conserv Gen 14(3):601–613. https://doi.org/10.1007/s10592-013-0451-5
Schoen DJ, Brown AH (1991) Intraspecific variation in population gene diversity and effective population size correlates with the mating system in plants. PNAS 88(10):4494–4497. https://doi.org/10.1073/pnas.88.10.4494
Sebbenn AM (2003) Tamanho amostral para conservação ex situ de espécies arbóreas com sistema misto de reprodução. Rev Inst Florest 15(2):147–162
Sebbenn AM (2006) Sistema de reprodução em espécies arbóreas tropicais e suas implicações para a seleção de árvores matrizes para reflorestamentos ambientais. Pomares de sementes de espécies florestais nativas. FUPEF, Curitiba
Sebbenn AM, CarvalhoACM FMLM 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. Heredity 106(1):134–145. https://doi.org/10.1038/hdy.2010.33
Seidler TG, Plotkin JB (2006) Seed dispersal and spatial pattern in tropical trees. PLoS Biol 4(11):e344. https://doi.org/10.1371/journal.pbio.0040344
Silva VS (2014) Sistema Reprodutivo e Diversidade Genética de Bertholletia excelsa em diferentes ambientes no Estado do Acre. Universidade Federal do Acre, Rio Branco
Smouse PE, Sork VL (2004) Measuring pollen flow in forest trees: an exposition of alternative approaches. Forest Ecol Manag 197(1–3):21–38. https://doi.org/10.1016/j.foreco.2004.05.049
Sujii PS, Schwarcz KD, Grando C et al (2015) Isolation and characterisation of microsatellite markers for Centrolobium tomentosum (Fabaceae), a neotropical tree species widely used for Atlantic Rainforest restoration. Conserv Gen Res 7(3):733–734. https://doi.org/10.1007/s12686-015-0448-0
Sujii PS, Schwarcz KD, Grando C, de Aguiar SE, Mori GM, Brancalion PH, Zucchi MI (2017) Recovery of genetic diversity levels of a Neotropical tree in Atlantic Forest restoration plantations. Biol Conserv 211:110–116. https://doi.org/10.1016/j.biocon.2017.05.006
Sujii PS, Nagai ME, Zucchi MI, Brancalion PH, James PM (2019) A genetic approach for simulating persistence of reintroduced tree species populations in restored forests. Ecol Model 403:35–43. https://doi.org/10.1016/j.ecolmodel.2019.04.014
Tambarussi EV, Boshier D, Vencovsky R, Freitas ML, Sebbenn AM (2015) Paternity analysis reveals significant isolation and near neighbor pollen dispersal in small Cariniana legalis Mart. Kuntze populations in the Brazilian Atlantic Forest. Ecol Evol 5(23):5588–5600. https://doi.org/10.1002/ece3.1816
Tambarussi EV, Boshier DH, Vencovsky R, Freitas ML, Di-Dio OJ, Sebbenn AM (2016) Several small: how inbreeding affects conservation of Cariniana legalis Mart. Kuntze (Lecythidaceae) the Brazilian Atlantic Forest’s largest tree. Int For Rev 18(4):502–510. https://doi.org/10.1505/146554816820127550
Tambarussi EV, Boshier D, Vencovsky R et al (2017) Inbreeding depression from selfing and mating between relatives in the Neotropical tree Cariniana legalis Mart. Kuntze Conserv Genet 18:225–234. https://doi.org/10.1007/s10592-016-0896-4
Tambarussi EV, Pereira FB, da Silva PH, Lee D, Bush D (2018) Are tree breeders properly predicting genetic gain? A case study involving Corymbia species. Euphytica 214(8):150. https://doi.org/10.1007/s10681-018-2229-9
Vekemans X, Hardy OJ (2004) New insights from fine-scale spatial genetic structure analyses in plant populations. Mol Ecol 13(4):921–935. https://doi.org/10.1046/j.1365-294X.2004.02076.x
Veron V, Caron H, Degen B (2005) Gene flow and mating system of the tropical tree Sextonia rubra. Silvae Genet 54(1–6):275–280. https://doi.org/10.1515/sg-2005-0040
Vogler DW, Kalisz S (2001) Sex among the flowers: the distribution of plant mating systems. Evol 55(1):202–204. https://doi.org/10.1111/j.0014-3820.2001.tb01285.x
Volis S, Ormanbekova D, Shulgina I (2016) Fine-scale spatial genetic structure in predominantly selfing plants with limited seed dispersal: a rule or exception? Plant Div 38(2):59–64. https://doi.org/10.1016/j.pld.2016.03.001
Waples RS (2005) Genetic estimates of contemporary effective population size: to what time periods do the estimates apply? Mol Ecol 14(11):3335–3352. https://doi.org/10.1111/j.1365-294X.2005.02673.x
Ward M, Dick CW, Gribel R, Lowe AJ (2005) To self, or not to self… A review of outcrossing and pollen-mediated gene flow in neotropical trees. Heredity 95(4):246–254. https://doi.org/10.1038/sj.hdy.6800712
Weising K, Gardner RC (1999) A set of conserved PCR primers for the analysis of simple sequence repeat polymorphisms in chloroplast genomes of dicotyledonous angiosperms. Genome 42:9–19. https://doi.org/10.1139/g98-104
Zucchi MI, Sujii PS, Mori GM, Viana JP, Grando C, Silvestre ED, Schwarcz KD et al (2017) Genetic diversity of reintroduced tree populations in restoration plantations of the Brazilian Atlantic Forest. Rest Ecot 26(4):694–701. https://doi.org/10.1111/rec.12620
Acknowledgements
For sampling and research permits, we thank Instituto Florestal (2518/2012; 493/2013), the Brazilian National Council for Scientific and Technological Development (CNPq-#304817/2015-5, #304899/2019-4 #310446/2015-5), and Chico Mendes Institute for Biodiversity Conservation (ICMBio- 29415-3). We are also thankful to Dr. José Baldin Pinheiro for laboratory infrastructure provided.
Funding
This research was supported by the São Paulo Research Foundation (BIOTA-FAPESP 2011/50296-8; FAPESP-2012/03246-8) and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES).
Author information
Authors and Affiliations
Contributions
All authors took part in discussing the results and composing and editing the manuscript. P.S.S, M.I.Z. and P.H.S.B. designed the experiment. P.S.S. carried out the research, analyzed the data and drafted the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflicts of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Sujii, P.S., Tambarussi, E.V., Grando, C. et al. High gene flow through pollen partially compensates spatial limited gene flow by seeds for a Neotropical tree in forest conservation and restoration areas. Conserv Genet 22, 383–396 (2021). https://doi.org/10.1007/s10592-021-01344-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10592-021-01344-3