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Forest fragmentation and edge effects on the genetic structure of Clusia sphaerocarpa and C. lechleri (Clusiaceae) in tropical montane forests

  • Amira Apaza Quevedo (a1) (a2), Matthias Schleuning (a1) (a3), Isabell Hensen (a1), Fransisco Saavedra (a1) (a3) (a2) and Walter Durka (a4)...

Fragmentation of tropical forests influences abiotic and biotic processes that affect the genetic structure of plant populations. In forest fragments, edge effects, i.e. changes of abiotic and biotic factors at forest edges, may be prevalent. In two forest fragments (c. 200 ha at c. 2450 m asl) of tropical montane forest in Bolivia, sympatric populations of the dioecious tree species Clusia sphaerocarpa and C. lechleri were used as case study species to compare genetic diversity and small-scale genetic structure (SGS) between edge and interior habitats. Eight microsatellite markers were employed to genotype 343 individuals including adults, juveniles and seedlings of C. sphaerocarpa and 196 of C. lechleri. Genetic differentiation was found between habitats in both species (ΦRT = 0.071 for C. sphaerocarpa and ΦRT = 0.028 for C. lechleri) and among ages in C. sphaerocarpaRT = 0.016). Overall, SGS was weak but significant with more pronounced SGS in C. lechleri (Sp = 0.0128) than in C. sphaerocarpa (Sp = 0.0073). However, positive spatial genetic autocorrelation extended only up to 10 m. For C. sphaerocarpa, SGS was stronger in seedling and juvenile stages than in adults and in the forest interior than at forest edges. Our results show that edge effects can extend to the genetic level by breaking-up local genetic structures, probably due to increased gene flow and enhanced pollination and seed-dispersal interactions at forest edges.

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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 7:933944.
BANKS, S. C. & PEAKALL, R. 2012. Genetic spatial autocorrelation can readily detect sex-biased dispersal. Molecular Ecology 21:20922105.
BAWA, K. S. 1992. Mating systems, genetic differentiation and speciation in tropical rain forest plants. Biotropica 24:250255.
BITTRICH, V. & AMARAL, M. C. E. 1996. Flower morphology and pollination biology of some Clusia species from the Gran Sabana (Venezuela). Kew Bulletin 51:681694.
CHOO, J., JUENGER, T. E. & SIMPSON, B. B. 2012. Consequences of frugivore-mediated seed dispersal for the spatial and genetic structures of a neotropical palm. Molecular Ecology 21:10191031.
DEBOUT, G. D. G., DOUCET, J. L. & HARDY, O. J. 2011. Population history and gene dispersal inferred from spatial genetic structure of a Central African timber tree, Distemonanthus benthamianus (Caesalpinioideae). Heredity 106:8899.
DE ROCA, S. 1993. Guttiferae. Pp. 337351 in Killeen, T. J., Beck, S. G. & Garcia, E. (eds.). Guía de arboles de Bolivia. Herbario Nacional de Bolivia & Missouri Botanical Garden, La Paz.
DEL CASTILLO, R. F., TRUJILLO-ARGUETA, S., SÁNCHEZ-VARGAS, N. & NEWTON, A. C. 2011. Genetic factors associated with population size may increase extinction risks and decrease colonization potential in a keystone tropical pine. Evolutionary Applications 4:574588.
DICK, C. W., HARDY, O. J., JONES, F. A. & PETIT, R. J. 2008. Spatial scales of pollen and seed-mediated gene flow in tropical rain forest trees. Tropical Plant Biology 1:2033.
DOLIGEZ, A., BARIL, C. & JOLY, H. I. 1998. Fine-scale spatial genetic structure with nonuniform distribution of individuals. Genetics 148:905919.
DOYLE, J. J. & DOYLE, J. L. 1987. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bulletin 19:1115.
DYER, R. J. 2007. Powers of discerning: challenges to understanding dispersal processes in natural populations. Molecular Ecology 16:48814882.
EZARD, T. H. G. & TRAVIS, J. M. J. 2006. The impact of habitat loss and fragmentation on genetic drift and fixation time. Oikos 114:367375.
FARWIG, N., BÖHNING-GAESE, K. & BLEHER, B. 2006. Enhanced seed dispersal of Prunus africana in fragmented and disturbed forests? Oecologia 147:238252.
FARWIG, N., BRAUN, C. & BÖHNING-GAESE, K. 2008. Human disturbance reduces genetic diversity of an endangered tropical tree, Prunus africana (Rosaceae). Conservation Genetics 9:317326.
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 57:9951007.
GARCÍA, C. & GRIVET, D. 2011. Molecular insights into seed dispersal mutualisms driving plant population recruitment. Acta Oecologica 37:632640.
GONZALES, E., HAMRICK, J. L., SMOUSE, P. E., TRAPNELL, D. W. & PEAKALL, R. 2010. The impact of landscape disturbance on spatial genetic structure in the guanacaste tree, Enterolobium cyclocarpum (Fabaceae). Journal of Heredity 101:133143.
GUSTAFSSON, M. H. G., WINTER, K. & BITTRICH, V. 2007. Diversity, phylogeny and classification of Clusia. Pp. 95116 in Lüttge, U. (ed.). Clusia: a woody neotropical genus of remarkable plasticity and diversity. Springer, Berlin.
HALE, M. L., SQUIRRELL, J., BORLAND, A. M. & WOLFF, K. 2002. Isolation of polymorphic microsatellite loci in the genus Clusia (Clusiaceae). Molecular Ecology Notes 2:506508.
HAMRICK, J. 2004. Response of forest trees to global environmental changes. Forest Ecology and Management 197:323335.
HAMRICK, J. L. 2010. Pollen and seed movement in disturbed tropical landscapes. Pp. 190211 in DeWoody, J. A., Bickham, J. W., Michler, C. H, Nichols, K. M., Rhodes, O. E. & Woeste, K. E. (eds.). Molecular approaches in natural resource conservation and management. Cambridge University Press, New York.
HAMRICK, J. L. & NASON, J. D. 1996. Consequences of dispersal in plants. Pp. 203236 in Rhodes, O. E., Chesser, R. K. & Smith, M. H. (eds.). Population dynamics in ecological space and time. University of Chicago Press, Chicago.
HAMRICK, J. L. & TRAPNELL, D. W. 2011. Using population genetic analyses to understand seed dispersal patterns. Acta Oecologica 37:641649.
HAMRICK, J. L., MURAWSKI, D. A. & NASON, J. D. 1993. The influence of seed dispersal mechanisms on the genetic structure of tropical tree populations. Plant Ecology 107/108:281297.
HANZAWA, F. M., BEATTIE, A. J. & CULVER, D. C. 1988. Directed dispersal: demographic analysis of an ant–seed mutualism. American Naturalist 131:113.
HENSEN, I., TEICH, I., HIRSCH, H., VON WEHRDEN, H. & RENINSON, D. 2011. Range-wide genetic structure and diversity of the endemic tree line species Polylepis australis (Rosaceae) in Argentina. American Journal of Botany 11:18251833.
HENSEN, I., CIERJACKS, A., HIRSCH, H., KESSLER, M., ROMOLEROUX, K., RENISON, D. & WESCHE, K. 2012. Historic and recent fragmentation coupled with altitude affect the genetic population structure of one of the world's highest tropical tree line species. Global Ecology and Biogeography 21:455464.
HURLBERT, S. H. 1971. The non concept of species diversity: a critique and alternative parameters. Ecology 52:577586.
KAMBACH, S., GUERRA, F., BECK, S., HENSEN, I. & SCHLEUNING, M. 2013. Human-induced disturbance alters pollinator communities in tropical montane forests. Diversity 5:114.
KESSLER, M. & BECK, S. G. 2001. Bolivia. Pp. 581622 in Kappelle, M. & Brown, A. D. (eds.). Bosques nublados del neotropico. INBio, Costa Rica.
KETTLE, C. J., HOLLINGSWORTH, P. M., JAFFRÉ, T., MORAN, B. & ENNOS, R. A. 2007. Identifying the early genetic consequences of habitat degradation in a highly threatened tropical conifer, Araucaria nemorosa Laubenfels. Molecular Ecology 16:35813591.
KETTLE, C. J., HOLLINGSWORTH, P. M., BURSLEM, D. F. R. P., MAYCOCK, C. R., KHOO, E. & GHAZOUL, J. 2011. Determinants of fine-scale spatial genetic structure in three co-occurring rain forest canopy trees in Borneo. Perspectives in Plant Ecology, Evolution and Systematics 13:4756.
KILLEEN, T. J., SILES, T., SORI, L. & BORREA, L. 2005. Estratificación de vegetación y cambio de uso de suelo en los Yungas y Alto Beni de La Paz. Ecología en Bolivia: Revista del Instituto de Ecología 40: 3269.
KIRIKA, J. M., BLEHER, B., BÖHNING-GAESE, K., CHIRA, R. & FARWIG, N. 2008. Fragmentation and local disturbance of forests reduce frugivore diversity and fruit removal in Ficus thonningii trees. Basic and Applied Ecology 9:663672.
KLOSS, L., FISCHER, M. & DURKA, W. 2011. Land-use effects on genetic structure of a common grassland herb: a matter of scale. Basic and Applied Ecology 12:440448.
KRAMER, A. T., ISON, J. L., ASHLEY, M. V. & HOWE, H. F. 2008. The paradox of forest fragmentation. Conservation Biology 22:878885.
LAURANCE, W. F., NASCIMENTO, H. E. M., LAURANCE, S. G., ANDRADE, A., EWERS, R. M., HARMS, K. E., LUIZÃO, R. C. C. & RIBEIRO, J. E. 2007. Habitat fragmentation, variable edge effects, and the landscape-divergence hypothesis. Plos ONE 2:e1017.
LEHOUCK, V., SPANHOVE, T., VANGESTEL, C., CORDEIRO, N. J. & LENS, L. 2009. Does landscape structure affect resource tracking by avian frugivores in a fragmented afrotropical forest? Ecography 32:789799.
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 82:14201425.
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 95:255273.
MENKE, S., BÖHNING-GAESE, K. & SCHLEUNING, M. 2012. Plant–frugivore networks are less specialized and more robust at forest–farmland edges than in the interior of a tropical forest. Oikos 121:15531566.
MICHALSKI, S. G. & DURKA, W. 2012. Assessment of provenance delineation by genetic differentiation patterns and estimates of gene flow in the common grassland plant Geranium pratense. Conservation Genetics 13:581592.
MURCIA, C. 1995. Edge effects in fragmented forests: implications for conservation. Trends in Ecology and Evolution 10:5862.
MYERS, N., MITTERMEIER, R. A., MITTERMEIER, C. G., FONSECA, G. A. B. & KENT, J. 2000. Biodiversity hotspots for conservation priorities. Nature 403:853858.
NASON, J. D., ALDRICH, P. R. & HAMRICK, J. L. 1997. Dispersal and the dynamics of genetic structure in fragmented tropical tree populations. Pp. 304320 in Laurance, W. F. & Bierregaard, R. O. (eds.). Tropical forest remnants: ecology, management and conservation of fragmented communities. The University of Chicago Press, Chicago.
NEI, M. 1987. Molecular evolutionary genetics. Columbia University Press, New York, 512 pp.
PASSOS, L. & OLIVEIRA, P. S. 2002. Ants affect the distribution and performance of seedlings of Clusia criuva, a primarily bird-dispersed rain forest tree. Journal of Ecology 90:517528.
RAMOS, F. N., DE LIMA, P. F., ZUCCHI, M. I., COLOMBO, C. A. & SOLFERINI, V. N. 2010. Genetic structure of tree and shrubby species among anthropogenic edges natural edges and interior of an Atlantic forest fragment. Biochemical Genetics 48:215228.
SAUNDERS, D. A., HOBBS, R. J. & MARGULES, C. R. 1991. Biological consequences of ecosystem fragmentation: a review. Conservation Biology 5:1832.
SHI, M., MICHALSKI, S. G., CHEN, X. Y. & DURKA, W. 2011. Isolation by elevation: genetic structure at neutral and putatively non-neutral loci in a dominant tree of subtropical forest, Castanopsis eyrei. Plos ONE 6:e21302.
SMOUSE, P. E., PEAKALL, R. & GONZALES, E. 2008. A heterogeneity test for fine-scale genetic structure. Molecular Ecology 17:33893400.
VAN GEERT, A., VAN ROSSUM, F. & TRIEST, L. 2008. Genetic diversity in adult and seedling populations of Primula vulgaris in a fragmented agricultural landscape. Conservation Genetics 9:845853.
VAN ROSSUM, F. & TRIEST, L. 2006. Fine-scale genetic structure of the common Primula elatior (Primulaceae) at an early stage of population fragmentation. American Journal of Botany 93:12811288.
VASCONCELOS, H. L. & LUIZÃO, F. J. 2004. Litter production and litter nutrient concentrations in a fragmented Amazonian landscape. Ecological Applications 14:884892.
VEKEMANS, X. & HARDY, O. J. 2004. New insights from fine-scale spatial genetic structure analyses in plant populations. Molecular Ecology 13:921935.
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 USA 99:20382042.
YOUNG, A., BOYLE, T. & BROWN, T. 1996. The population genetic consequences of habitat fragmentation for plants. Trends in Ecology and Evolution 11:413418.
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