Keywords
Flujo del polen; dispersión de semillas; deforestación; polinización por colibríes; Análisis de parentesco; fragmentación
How to Cite
Abstract
In tropical trees, forest fragmentation has been shown to affect mating and gene flow patterns. Mobile dispersal vectors should be less sensitive to fragmented landscapes and may ameliorate the genetic effects of forest fragmentation on plant populations. To test this hypothesis, we analyzed gene flow patterns in Symphonia globulifera, a tropical tree species with highly mobile pollinators and seed dispersers in the Osa Peninsula in southern Costa Rica. We used microsatellites to study genetic diversity and realized gene flow patterns between a continuous forest and a forest fragment. We found high levels of genetic diversity in adults and seedlings at both sites. Parentage analyses suggest near-neighbor matings and frequent long-distance gene flow events. Half the progeny beneath an adult was not sired by that tree and the majority of established seedlings were the result of long-distance gene dispersal. Gene flow from the forest into the fragment was more common than from the fragment into the continuous forests. Despite long distance gene flow events, seedling spatial genetic structure was stronger and extended further in the forest fragment likely due to limited seed dispersal. We conclude that fragmentation affects gene flow in this tropical tree and may compromise its genetic diversity in forest fragments even for a species with mobile pollen and seed vectors.
References
Achard, F., Beuchle, R., Mayaux, P., Stibig, H.-J., Bodart, C., Brink, A., … Simonetti, D. (2014). Determination of tropical deforestation rates and related carbon losses from 1990 to 2010. Global Change Biology, 20(8), 2540-2554. DOI: 10.1111/gcb.12605
Aguilar, R., Ashworth, L., Galetto, L., & Aizen, M. A. (2006). Plant reproductive susceptibility to habitat fragmentation: review and synthesis through a meta-analysis. Ecology Letters, 9(8), 968-980. DOI: 10.1111/j.1461-0248.2006.00927.x
Aguilar, R., Quesada, M., Ashworth, L., Herrerias-Diego, Y., & Lobo, J. A. (2008). Genetic consequences of habitat fragmentation in plant populations: susceptible signals in plant traits and methodological approaches. Molecular Ecology, 17(24), 5177-5188. DOI: 10.1111/j.1365-294X.2008.03971.x
Aldrich, P. R., & Hamrick, J. L. (1998). Reproductive dominance of pasture trees in a fragmented tropical forest mosaic. Science, 281(5373), 103-105.
Aldrich, P. R., Hamrick, J. L., Chavarriaga, P., & Kochert, G. (1998). Microsatellite analysis of demographic genetic structure in fragmented populations of the tropical tree Symphonia globulifera. Molecular Ecology, 7, 933-944.
Allendorf, F. W., Luikart, G. H., & Aitken, S. N. (2012). Conservation and the Genetics of Populations (2nd ed.). Hoboken: Wiley-Blackwell.
Bacles, C. F. E., & Ennos, R. A. (2008). Paternity analysis of pollen-mediated gene flow for Fraxinus excelsior L. in a chronically fragmented landscape. Heredity, 101(4), 368-380. DOI: 10.1038/hdy.2008.66
Bacles, C. F. E., Lowe, A. J., & Ennos, R. A. (2006). Effective seed dispersal across a fragmented landscape. Science, 311(5761), 628. DOI: 10.1126/science.1121543
Barrantes, G., Jiménez, Q., Lobo, J., Maldonado, T., Quesada, M., & Quesada, R. (1999). Evaluacion de los planes de manejo forestal autorizados en el perıódo 1997-1999 en la Peninsula de Osa. Cumplimiento de normas tecnicas, ambientales e impacto sobre el bosque natural. Puerto Jimenez, Costa Rica: Fundacion Cecropia. Recuperado de http://www.apreflofas.or.cr/spa/documentos/informe_cecropia.pdf
Bayma, J. C., Arruda, M. S., & Neto, M. S. (1998). A prenylated xanthone from the bark of Symphonia globulifera. Phytochemistry, 49(4), 1159-1160.
Bezemer, N., Krauss, S. L., Phillips, R. D., Roberts, D. G., & Hopper, S. D. (2016). Paternity analysis reveals wide pollen dispersal and high multiple paternity in a small isolated population of the bird-pollinated Eucalyptus caesia (Myrtaceae). Heredity. DOI: 10.1038/hdy.2016.61
Bittrich, V., & Amaral, M. C. E. (1996). Pollination biology of Symphonia globulifera (Clusiaceae). Plant Systematics and Evolution, 200(1-2), 101-110. DOI: 10.1007/BF00984751
Breed, M. F., Ottewell, K. M., Gardner, M. G., Marklund, M. H. K., Dormontt, E. E., & Lowe, A. J. (2015). Mating patterns and pollinator mobility are critical traits in forest fragmentation genetics. Heredity, 115(2), 108-114. DOI: 10.1038/hdy.2013.48
Browne, L., Ottewell, K., & Karubian, J. (2015). Short-term genetic consequences of habitat loss and fragmentation for the neotropical palm Oenocarpus bataua. Heredity, 115(5), 389-395. DOI: 10.1038/hdy.2015.35
Burczyk, J., DiFazio, S. P., & Adams, W. T. (2004). Gene flow in forest trees: how far do genes really travel? Forest Genetics, 11(3/4), 179.
Carneiro, F. S., Degen, B., Kanashiro, M., de Lacerda, A. E. B., & Sebbenn, A. M. (2009). High levels of pollen dispersal detected through paternity analysis from a continuous Symphonia globulifera population in the Brazilian Amazon. Forest Ecology and Management, 258(7), 1260-1266. DOI: 10.1016/j.foreco.2009.06.019
Carneiro, F. S., Lacerda, A. E. B., Lemes, M. R., Gribel, R., Kanashiro, M., Wadt, L. H. O., & Sebbenn, A. M. (2011). Effects of selective logging on the mating system and pollen dispersal of Hymenaea courbaril L. (Leguminosae) in the Eastern Brazilian Amazon as revealed by microsatellite analysis. Forest Ecology and Management, 262(9), 1758-1765. DOI: 10.1016/j.foreco.2011.07.023
Cascante, A., Quesada, M., Lobo, J. A., & Fuchs, E. J. (2001). Effects of dry tropical forest fragmentation on the reproductive success and genetic structure of the tree Samanea saman. Conservation Biology, 16(1), 137-147.
Charlesworth, B., & Charlesworth, D. (1999). The genetic basis of inbreeding depression. Genetical Research, 74(3), 329-340.
Chung, M. Y., Epperson, B. K., & Chung, M. G. (2003). Genetic structure of age classes in Camellia japonica (Theaceae). Evolution, 57(1), 62-73.
Couvet, D. (2002). Deleterious effects of restricted gene flow in fragmented populations. Conservation Biology, 16(2), 369-376.
Degen, B., Bandou, E., & Caron, H. (2004). Limited pollen dispersal and biparental inbreeding in Symphonia globulifera in French Guiana. Heredity, 93(6), 585-591. DOI: 10.1038/sj.hdy.6800560
De-Lucas, A. I., González-Martínez, S. C., Vendramin, G. G., Hidalgo, E., & Heuertz, M. (2009). Spatial genetic structure in continuous and fragmented populations of Pinus pinaster Aiton. Molecular Ecology, 18(22), 4564-4576. DOI: 10.1111/j.1365-294X.2009.04372.x
Dick, C. W. (2001). Genetic rescue of remnant tropical trees by an alien pollinator. Proceedings of the Royal Society of London Series B-Biological Sciences, 268, 2391-2396.
Dick, C. W., & Heuertz, M. (2008). The complex biogeographic history of a widespread tropical tree species. Evolution, 62(11), 2760-2774. DOI: 10.1111/j.1558-5646.2008.00506.x
Earl, D. A., & von Holdt, B. M. (2011). STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources, 4(2), 359-361. DOI: 10.1007/s12686-011-9548-7
Ellstrand, N. C., & Elam, D. R. (1993). Population genetic consequences of small population size: Implications for plant conservation. Annual Review of Ecology and Systematics, 24, 217-242.
Epperson, B. (1992). Spatial structure of genetic variation within populations of forest trees. New Forests, 6(1), 257-278.
Evanno, G., Regnaut, S., & Goudet, J. (2005). Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology, 14(8), 2611-2620. DOI: 10.1111/j.1365-294X.2005.02553.x
Fenster, C. B., Vekemans, X., & Hardy, O. J. (2003). Quantifying gene flow from spatial genetic structure data in a metapopulation of Chamaecrista fasciculata (Leguminosae). Evolution. DOI: 10.1111/j.0014-3820.2003.tb00311.x
Fuchs, E. J., & Hamrick, J. L. (2010). Spatial genetic structure within size classes of the endangered tropical tree Guaiacum sanctum (Zygophyllaceae). American Journal of Botany, 97(7), 1200-1207. DOI: 10.3732/ajb.0900377
Fuchs, E. J., & Hamrick, J. L. (2011). Mating system and pollen flow between remnant populations of the endangered tropical tree, Guaiacum sanctum (Zygophyllaceae). Conservation Genetics, 12(1), 175-185. DOI: 10.1007/s10592-010-0130-8
Fuchs, E. J., Lobo, J. A., & Quesada, M. (2003). Effects of forest fragmentation and flowering phenology on the reproductive success and mating patterns of the tropical dry forest tree Pachira quinata. Conservation Biology, 17(1), 149-157. DOI: 10.1046/j.1523-1739.2003.01140.x
Gill, G. E., Fowler, R. T., & Mori, S. A. (1998). Pollination biology of Symphonia globulifera (Clusiaceae) in Central French Guiana. Biotropica, 30(1), 139-144.
Grivet, D., Robledo-Arnuncio, J. J., Smouse, P. E., & Sork, V. L. (2009). Relative contribution of contemporary pollen and seed dispersal to the effective parental size of seedling population of California valley oak (Quercus lobata Née). Molecular Ecology, 18(19), 3967-3979. DOI: 10.1111/j.1365-294X.2009.04326.x
Haddad, N. M., Brudvig, L. A., Clobert, J., Davies, K. F., Gonzalez, A., Holt, R. D., … Townshend, J. R. (2015). Habitat fragmentation and its lasting impact on Earth’s ecosystems. Science Advances, 1(2), e1500052. DOI: 10.1126/sciadv.1500052
Hadfield, J. D., Richardson, D. S., & Burke, T. (2006). Towards unbiased parentage assignment: combining genetic, behavioural and spatial data in a Bayesian framework. Molecular Ecology, 15(12), 3715-3730. DOI: 10.1111/j.1365-294X.2006.03050.x
Hamilton, M. B. (1999). Tropical tree gene flow and seed dispersal. Nature, 401(6749), 129-130. DOI: 10.1038/43597
Hamrick, J. L., & Loveless, M. D. (1987). Associations between the breeding system and the genetic-structure of tropical tree populations. American Journal Of Botany, 74(5), 642-642.
Hamrick, J. L., Murawski, D. A., & Nason, J. D. (1993). The influence of seed dispersal mechanisms on the genetic structure of tropical tree populations. Vegetatio, 107(108), 281-297.
Hamrick, J. L., & Trapnell, D. (2011). Using population genetic analyses to understand seed dispersal patterns. Acta Oecologica, 37(6), 641-649.
Hanson, T. R., Brunsfeld, S. J., Finegan, B., & Waits, L. P. (2008). Pollen dispersal and genetic structure of the tropical tree Dipteryx panamensis in a fragmented Costa Rican landscape. Molecular Ecology, 17(8), 2060-2073. DOI: 10.1111/j.1365-294X.2008.03726.x
Harder, L. D., & Barrett, S. C. H. (1996). Pollen Dispersal and Mating Patterns in Animal-Pollinated Plants. In D. G. Lloyd & S. C. H. Barrett (Eds.), Floral Biology (pp. 140-190). USA: Springer. DOI: 10.1007/978-1-4613-1165-2_6
Hardesty, B. D., Dick, C. W., Kremer, A., Hubbell, S., & Bermingham, E. (2005). Spatial genetic structure of Simarouba amara Aubl. (Simaroubaceae), a dioecious, animal-dispersed Neotropical tree, on Barro Colorado Island, Panama. Heredity, 95(4), 290-297.
Hardesty, B. D., Hubbell, S. P., & Bermingham, E. (2006). Genetic evidence of frequent long-distance recruitment in a vertebrate-dispersed tree. Ecology Letters, 9(5), 516-525. DOI: 10.1111/j.1461-0248.2006.00897.x
Hardy, O. J., & Vekemans, X. (2002). SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Molecular Ecology Notes, 2(4), 618-620. DOI: 10.1046/j.1471-8286.2002.00305.x
Helbig-Bonitz, M., Ferger, S. W., Böhning-Gaese, K., Tschapka, M., Howell, K., & Kalko, E. K. V. (2015). Bats are not birds - different responses to human land-use on a tropical mountain. Biotropica, 47(4), 497-508. DOI: 10.1111/btp.12221
Holdridge, L. R. (1967). Life zone ecology. San Jose, Costa Rica: Tropical Science Center.
Hufford, K. M., & Hamrick, J. L. (2003). Viability selection at three early life stages of the tropical tree, Platypodium elegans (Fabaceae, Papilionoideae). Evolution, 57(3), 518-526.
Ismail, S. A., Ghazoul, J., Ravikanth, G., Uma Shaanker, R., Kushalappa, C. G., & Kettle, C. J. (2012). Does long-distance pollen dispersal preclude inbreeding in tropical trees? Fragmentation genetics of Dysoxylum malabaricum in an agro-forest landscape. Molecular Ecology, 21(22), 5484-5496. DOI: 10.1111/mec.12054
Jakobsson, M., & Rosenberg, N. A. (2007). CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics, 23(14), 1801-1806. DOI: 10.1093/bioinformatics/btm233
Julio, N., Sobral, A., Dueñas, J. R., Di Rienzo, J., Renison, D., & Hensen, I. (2008). RAPD and ISSR markers indicate diminished gene flow due to recent fragmentation of Polylepis australis woodlands in central Argentina. Biochemical Systematics and Ecology, 36(5-6), 329-335. DOI: 10.1016/j.bse.2007.10.007
Kalinowski, S. T., Taper, M. L., & Marshall, T. C. (2007). Revising how the computer program Cervus accommodates genotyping error increases success in paternity assignment. Molecular Ecology, 16(5), 1099-1106. DOI: 10.1111/j.1365-294X.2007.03089.x
Konuma, A., Tsumura, Y., Lee, C. T., Lee, S. L., & Okuda, T. (2000). Estimation of gene flow in the tropical-rainforest tree Neobalanocarpus heimii (Dipterocarpaceae), inferred from paternity analysis. Molecular Ecology, 9(11), 1843-1852.
Lander, T. A., Boshier, D. H., & Harris, S. A. (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. Biological Conservation, 143(11), 2583-2590. DOI: 10.1016/j.biocon.2010.06.028
Leclerc, T., Vimal, R., Troispoux, V., Périgon, S., & Scotti, I. (2015). Life after disturbance (I): changes in the spatial genetic structure of Jacaranda copaia (Aubl.) D. Don (Bignonianceae) after logging in an intensively studied plot in French Guiana. Annals of Forest Science. DOI: 10.1007/s13595-015-0462-0
Loiselle, B. A., Sork, V. L., Nason, J., & Graham, C. (1995). Spatial genetic structure of a tropical understory shrub, Psychotria officinalis (Rubiaceae). American Journal of Botany, 82(11), 1420-1425.
Lowe, A. J., Boshier, D., Ward, M., Bacles, C. F. E., & Navarro, C. (2005). Genetic resource impacts of habitat loss and degradation; reconciling empirical evidence and predicted theory for neotropical trees. Heredity, 95(4), 255-273.
Marden, J. H., Mangan, S. A., Peterson, M. P., Wafula, E., Fescemyer, H. W., Der, J. P., … Comita, L. S. (2017). Ecological genomics of tropical trees: how local population size and allelic diversity of resistance genes relate to immune responses, cosusceptibility to pathogens, and negative density dependence. Molecular Ecology, 26(9), 2498-2513. DOI: 10.1111/mec.13999
Marshall, T. C., Slate, J., Kruuk, L. E., & Pemberton, J. M. (1998). Statistical confidence for likelihood-based paternity inference in natural populations. Molecular Ecology, 7(5), 639-655.
Meirmans, P. G., & Van Tienderen, P. H. (2004). Genotype and genodive: two programs for the analysis of genetic diversity of asexual organisms. Molecular Ecology Notes, 4(4), 792-794. DOI: 10.1111/j.1471-8286.2004.00770.x
Melo, A. T. de O., & Franceschinelli, E. V. (2016). Gene flow and fine-scale spatial genetic structure in Cabralea canjerana (Meliaceae), a common tree species from the Brazilian Atlantic forest. Journal of Tropical Ecology, 32(02), 135-145. DOI: 10.1017/S0266467416000067
Nason, J. D., & Hamrick, J. L. (1997). Reproductive and genetic consequences of forest fragmentation: Two case studies of neotropical canopy trees. Journal of Heredity, 88(4), 264-276.
Neuschulz, E. L., Mueller, T., Schleuning, M., & Böhning-Gaese, K. (2016). Pollination and seed dispersal are the most threatened processes of plant regeneration. Scientific Reports, 6, 29839. DOI: 10.1038/srep29839
Newman, D., & Pilson, D. (1997). Increased probability of extinction due to decreased genetic effective population size: experimental populations of Clarkia pulchella. Evolution, 51(2), 354. DOI: 10.2307/2411107
Pardini, E. A., & Hamrick, J. L. (2008). Inferring recruitment history from spatial genetic structure within populations of the colonizing tree Albizia julibrissin (Fabaceae). Molecular Ecology, 17(12), 2865-2879. DOI: 10.1111/j.1365-294X.2008.03807.x
Pascarella, J. (1992). Notes on flowering phenology, nectar robbing and pollination of Symphonia globulifera LF (Clusiaceae) in a lowland rain forest in Costa Rica. Brenesia, 38, 83-86.
Peakall, R. & Smouse, P. E. (2006). GenAlEx 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes, 6, 288-295.
Pritchard, J. K., Stephens, M., & Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics, 155(2), 945-959.
Pulliam, H. R. (1988). Sources, sinks, and population regulation. American naturalist, 652-661.
Pyke, G. H. (1984). Optimal Foraging Theory: A Critical Review. Annual Review of Ecology and Systematics, 15(1), 523-575. DOI: 10.1146/annurev.es.15.110184.002515
Quesada, M., Stoner, K. E., Lobo, J. A., Herrerias-Diego, Y., Palacios-Guevara, C., Munguia-Rosas, M. A., … Rosas-Guerrero, V. (2004). Effects of forest fragmentation on pollinator activity and consequences for plant reproductive success and mating patterns in bat-pollinated Bombacaceous trees. Biotropica, 36(2), 131-138. DOI: 10.1111/j.1744-7429.2004.tb00305.x
Quesada, M., Stoner, K. E., Rosas-Guerrero, V., Palacios-Guevara, C., & Lobo, J. A. (2003). Effects of habitat disruption on the activity of nectarivorous bats (Chiroptera: Phyllostomidae) in a dry tropical forest: implications for the reproductive success of the neotropical tree Ceiba grandiflora. Oecologia, 135(3), 400-406. DOI: 10.1007/s00442-003-1234-3
R Development Core Team. (2012). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Retrieved from http://www.R-project.org
Reed, D. H., & Frankham, R. (2003). Correlation between fitness and genetic diversity. Conservation biology, 17(1), 230-237.
Riba-Hernández, P., & Stoner, K. E. (2005). Massive destruction of Symphonia globulifera (Clusiaceae) flowers by Central American Spider monkeys (Ateles geoffroyi). Biotropica, 37(2), 274-278. DOI: 10.1111/j.1744-7429.2005.00037.x
Ripperger, S. P., Kalko, E. K. V., Rodríguez-Herrera, B., Mayer, F., & Tschapka, M. (2015). Frugivorous bats maintain functional habitat connectivity in agricultural landscapes but rely strongly on natural forest fragments. PLoS ONE, 10(4). DOI: 10.1371/journal.pone.0120535
Roberts, D. G., Ottewell, K. M., Whelan, R. J., & Ayre, D. J. (2014). Is the post-disturbance composition of a plant population determined by selection for outcrossed seedlings or by the composition of the seedbank? Heredity, 112(4), 409.
Rosas, F., Quesada, M., Lobo, J. A., & Sork, V. L. (2011). Effects of habitat fragmentation on pollen flow and genetic diversity of the endangered tropical tree Swietenia humilis (Meliaceae). Biological Conservation, 144(12), 3082-3088. DOI:10.1016/j.biocon.2011.10.003
Sanfiorenzo, A., Sanfiorenzo, M., Castro, R. V., Waits, L., & Finegan, B. (2018).Potential pollinators of understory populations of Symphonia globulifera in the Neotropics. Journal of Pollination Ecology, 22(1), 1-10. Retrieved from http://www.pollinationecology.org/index.php?journal=jpe&page=article&op=view&path %5B %5D=405
Schulke, B., & Waser, N. (2001). Long-distance pollinator flights and pollen dispersal between populations of Delphinium nuttallianum. Oecologia, 127(2), 239-245. DOI: 10.1007/s004420000586
Sebbenn, A. M., Carvalho, A. C. M., Freitas, M. L. M., Moraes, S. M. B., Gaino, A. P. S. C., da Silva, J. M., … Moraes, M. L. T. (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. DOI: 10.1038/hdy.2010.33
Segura, J. L., & Jimenez Vargas, D. (2014). Pollen dispersal patterns in a fragmented population of Carapa nicaraguensis (Meliaceae). International Journal of Plant Sciences, 175(2), 176-185. DOI: 10.1086/673304
Sezen, U. U., Chazdon, R. L., & Holsinger, K. E. (2009). Proximity is not a proxy for parentage in an animal-dispersed Neotropical canopy palm. Proceedings of the Royal Society B: Biological Sciences, 276(1664), 2037-2044. DOI: 10.1098/rspb.2008.1793
Sih, A., & Baltus, M.-S. (1987). Patch size, pollinator behavior, and pollinator limitation in catnip. Ecology, 1679-1690.
Slatkin, M. (1985). Gene Flow In Natural-Populations. Annual Review Of Ecology And Systematics, 16, 393-430.
Sork, V. L., & Smouse, P. E. (2006). Genetic analysis of landscape connectivity in tree populations. Landscape Ecology, 21(6), 821-836. DOI: 10.1007/s10980-005-5415-9
Stacy, E. A., Hamrick, J. L., Nason, J. D., Hubbell, S. P., Foster, R. B., & Condit, R. (1996). Pollen dispersal in low-density populations of three neotropical tree species. American Naturalist, 148(2), 275-298.
Torroba-Balmori, P., Budde, K. B., Heer, K., González-Martínez, S. C., Olsson, S., Scotti-Saintagne, C., … Heuertz, M. (2017). Altitudinal gradients, biogeographic history and microhabitat adaptation affect fine-scale spatial genetic structure in African and Neotropical populations of an ancient tropical tree species. PloS ONE, 12(8), e0182515.
Van Oosterhout, C., Hutchinson, W. F., Wills, D. P., & Shipley, P. (2004). MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes, 4(3), 535-538.
Vekemans, X., & Hardy, O. J. (2004). New insights from fine-scale spatial genetic structure analyses in plant populations. Molecular Ecology, 13(4), 921-935.
Vinson, C. C., Amaral, A. C., Sampaio, I., & Ciampi, A. Y. (2005). Characterization and isolation of DNA microsatellite primers for the tropical tree, Symphonia globulifera Linn. f. Molecular Ecology Notes, 5(2), 202-204. DOI: 10.1111/j.1471-8286.2005.00876.x
Vranckx, G., Jacquemyn, H., Muys, B., & Honnay, O. (2012). Meta-analysis of susceptibility of woody plants to loss of genetic diversity through habitat fragmentation. Conservation Biology, 26(2), 228-237. DOI: 10.1111/j.1523-1739.2011.01778.x
Wang, B. C., Sork, V. L., Leong, M. T., & Smith, T. B. (2007). Hunting of Mammals Reduces Seed Removal and Dispersal of the Afrotropical Tree Antrocaryon klaineanum (Anacardiaceae). Biotropica, 39(3), 340-347. DOI: 10.1111/j.1744-7429.2007.00275.x
Wang, J., Hill, W., Charlesworth, D., & Charlesworth, B. (1999). Dynamics of inbreeding depression due to deleterious mutations in small populations: mutation parameters and inbreeding rate. Genetical Research, 74(2), 165-178.
Wang, R., Compton, S. G., & Chen, X.-Y. (2011). Fragmentation can increase spatial genetic structure without decreasing pollen-mediated gene flow in a wind-pollinated tree. Molecular Ecology, 20(21), 4421-4432. DOI: 10.1111/j.1365-294X.2011.05293.x
White, G. M., Boshier, D. H., & Powell, W. (2002). Increased pollen flow counteracts fragmentation in a tropical dry forest: An example from Swietenia humilis Zuccarini. Proceedings of the National Academy of Sciences of the United States of America, 99(4), 2038-2042.
Young, A., Boyle, T., & Brown, T. (1996). The population genetic consequences of habitat fragmentation for plants. Trends in Ecology and Evolution, 11(10), 413-418.
Comments
This work is licensed under a Creative Commons Attribution 4.0 International License.
Copyright (c) 2019 Revista de Biología Tropical