Keywords
fruit production
habitat fragmentation
plant-pollinator interaction
moth pollination
reproductive success
pre-dispersal seed predation
seed set
How to Cite
Abstract
In Brazil, the Atlantic forest remnants have high biological diversity and a high level of endemism, but very little is known about the reproductive success of native species. Cabralea canjerana is a common tree in the Montane Atlantic forest, and its reproduction is highly dependent on pollinators. In order to contribute with the particular knowledge on this species, we collected data in three fragmented and three continuous forest sites, where the effects of fragmentation on both mutualistic (pollination) and antagonistic (seed predation) interactions were analysed. We determined fruit production and weight of 25 trees per site. The number of seeds and the percentage of predated and aborted seeds were also accessed for seven fruits of 10 trees per site. Pollinator visitation frequencies to flowers were recorded in two forest fragments and in two sites of the continuous forest. Our data showed that plants of C. canjerana produced more fruits (z-value=-8.24; p<0.0001) and seeds per fruit (z-value=-6.58; p=0.002) in the continuous than in the fragmented sites. This was likely due to differences in pollination, because the number of pollinator visits was higher in the continuous forest than in the fragments. Seed abortion (z-value=4.08, p<0.001) and predation (z-value=3.72, p=0.0002), on the other hand, were higher in the fragmented than in the continuous sites. Then, mutualistic and antagonistic interactions were affected by fragmentation, decreasing the reproductive success of the study tree. This study was the first to show a decrease in the reproductive output in forest fragments in an Atlantic forest tree species. This decrease may threaten the population structure and viability of C. canjerana in forest fragments.References
Ågren, J. (1996). Population size, pollinator limitation, and seed set in the self-incompatible herb Lythrum salicaria. Ecology, 77, 1779-1790.
Aguilar, R., & Galetto, L. (2004). Effects of forest fragmentation on male and female reproductive success in Cestrum parqui (Solanaceae). Oecologia, 138, 513-520.
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, 968-980.
Aguirre, A., & Dirzo, R. (2008). Effects of fragmentation on pollinator abundance and fruit set of an abundant understory palm in a Mexican tropical forest. Biological Conservation, 141, 75-384.
Aizen, M. A., & Feinsinger, P. (1994b). Habitat fragmentation, natives insect pollinators and and feral honey bee in Argentine ‘Chaco Serrano’. Ecological Applications, 4, 378-392.
Aizen, M. A., & Feinsinger, P. (1994a). Forest fragmentation, pollination and plant reproduction in a Chaco dry forest, Argentina. Ecology, 75, 330-351.
Aldrich, P. R., & Hamrick, J. L. (1998). Reproductive dominance of pasture trees in a fragmented tropical forest mosaic. Science, 281, 103-105.
Bates, D., Maechler, M., Bolker, B., & Walker S. (2014). Lme4: Linear mixed-effects models using Eigen and S4. R package version 1.1-7, http://CRAN.R-project.org/package=lme4.
Bolker, B. M., Brooks, M. E. Clark, C. J., Geange, S. W., Poulsen, J. R., Stevens, M. H. H., & White, J. S. (2009). Generalized linear mixed models: a practical guide for ecology and evolution. Trends in Ecology & Evolution, 24, 127-135.
Byers, D. L. (1995). Pollen quantity and quality as explanations for low seed set in small populations exemplified by Eupatorium (Asteraceae). American Journal of Botany, 82, 1000-1006.
Carmo, R. M. (2005). Biologia reprodutiva de Cabralea canjerana subsp. canjerana em Fragmentos de Mata Atlântica do Sul do estado Minas Gerais. (Ph.D. thesis). Universidade Federal de Minas Gerais, Brasil.
Carvalho, P. E. R. (1994). Espécies florestais brasileiras. Recomendações silviculturais, potencialidades e uso da madeira. Brasília DF: Embrapa/CNPF-SPI.
Cascante, A., Quesada, M., Lobo, J., & Fuchs, E. A. (2002). Effects of Dry Tropical Forest Fragmentation on the reproductive success and genetic structure of the tree Samanea saman. Conservation Biology, 16, 1-11.
Colling, G., & Matthies, D. (2004). The effects of plant population size on the interactions between the endangered plant Scorzonera humilis, a specialised herbivore, and a phytopathogenic fungus. Oikos, 105, 71-78.
Costin, B. J., Morgan, J. W., & Young, A. G. (2001). Reproductive success foes not decline in fragmented populations of Leucochrysum albicans subsp. Albicans var. tricolor (Asteraceae). Biological Conservation, 98, 273-284.
Cunningham, S. A. (2000). Depressed pollination in habitat fragments causes low fruit set. Proceedings of the Royal Society of London, B, 267, 1149-1152.
De Jong, T. J., & Klinkhamer, P. G. L. (1989). Limiting factors for seed production in Cynoglossum officinale. Oecologia, 80, 167-171.
Dick, C. W. (2001). Genetic rescue of remnant tropical trees by an alien pollinator. Proceedings of the Royal Society of London B, 268, 2391-2396.
Didham, R. K., Ghazoul, J., Stork, N. E., & Davis, A. J. (1996). Insects in fragmented forests: a functional approach. Trends in Ecology & Evolution, 11, 255-260.
Donaldson, J., Nänni, I., Zachariades, C., & Kemper, J. (2002). Effects of Habitat Fragmentation on Pollinator Diversity and Plant Reproductive Success in Renosterveld Shrublands of South Africa. Conservation Biology, 16, 1267-1276.
Dunley, B., Freitas, L., & Galetto, L. (2009). Reproduction of Byrsonima sericea (Malpighiaceae) in resting fragmented habitats in Southeastern Brazil. Biotropica, 41, 692-699.
Ehlers, B. K., & Olesen, J. M. (2003). Flower and fruit herbivory in a population of Centaurea scabiosa (Asteraceae): importance of population size and isolation. Ecoscience, 10, 45-48.
Elias, M. A. S., Franceschinelli, E. V., Borges, F. J. A., Ferreira, G. M., Juen, L., Carvalho, F. M. V. (2012). Reproductive success of Cardiopetalum calophyllum (Annonaceae) in fragments of Brazilian savanna. Journal of Tropical Ecology, 28, 317-320.
Faegri, K., & van der Pijl, L. (1979). The principles of pollination ecology. New York: Pergamon Press.
Farwig, N., Bleher, B., von der Gönna, S., & Böhning-Gaese, K. (2008). Does forest fragmentation and selective logging affect seed predators and seed predation rates of Prunus africana (Rosaceae)? Biotropica, 40(2), 218-224.
Fleury, M., & Galetti, M. (2006). Forest fragment size and microhabitat effects on palm seed predation. Biological Conservation, 131, 1-13.
França, G. S., & Stehmann, J. R. (2004). Composição florística e estrutura do componente arbóreo de uma floresta altimontana no município de Camanducaia, Minas Gerais, Brasil. Revista Brasileira de Botânica, 27, 19-30.
Galetti, M., Donatti, C., & Pires, A. S. (2006) Seed survival and dispersal of an endemic Atlantic forest palm: the combined effects of defaunation and forest fragmentation. Botanical Journal of Linnean Society, 151, 141-149.
Ghazoul, J. (2005). Pollen and seed dispersal among dispersed plants. Biological Review, 80, 413-443.
Greig, N. (1993). Predispersal seed predation on five Piper species in tropical rainforest. Oecologia, 93, 412-420.
Groom, M. J. (2001). Consequences of subpopulation isolation for pollination, herbivory, and population growth in Clarkia concinna (Onagraceae). Biological Conservation, 100, 55-63.
Hämback, P. A., & Beckerman, A. P. (2003). Herbivory and plant resource competition: a review of two interacting interactions. Oikos, 101, 26-37.
Herrerías-Diego, Y, Quesada, M., Stoner, K. E., Lobo, J. A., Hernández-Flores, Y., & Montoya, G. S. (2008). Effect of forest fragmentation on fruit and seed predation of the tropical dry forest tree Ceiba aesculifolia. Biological Conservation, 141(1), 241-248.
Jennersten, O. (1988). Pollination in Dianthus deltoids (Caryophyllaceae): Effects of habitat fragmentation on visitation and seed set. Conservation Biology, 2, 359-367.
Jennersten, O., & Nilsson, S. G. (1993). Insect flower visitation frequency and seed production in relation to patch size of Viscaria vulgaris (Caryophyllaceae). Oikos, 68, 283-292.
Jules, E. S. (1998). Habitat fragmentation and demographic chances for a common plant: Trillium in old-growth forest. Ecology, 79, 1645-1656.
Kéry, M., Matthies, D., & Fischer, M. (2001). The effect of plant population size on the interactions between the rare plant Gentiana cruciata and its specialized herbivore Maculinea rebeli. Journal of Ecology, 89, 418-427.
Kolb, A. (2008). Habitat fragmentation reduces plant fitness by disturbing pollination and modifying response to herbivory. Biological Conservation, 141, 2540-2549.
Kruess, A., & Tscharntke, T. (1994) Habitat fragmentation, species loss, and biological control. Science, 264, 1581-1584.
Kwak, M. M., Velterop, O., & Andel, J. (1998). Pollen and gene flow in fragmented habitats. Applied Vegetation Science, 1, 37-54.
Lopes, L. E., & Buzato, S. (2007). Variation in pollinator assemblages in a fragmented landscape and its effects on reproductive stages of a self-incompatible treelet Psychotria suterella (Rubiaceae). Oecologia, 154, 305-314.
Louda, S. M. (1982). Distribution ecology: variation in plant recruitment over a gradient in relation to insect seed predation. Ecological Monograph, 52, 25-41.
Lovejoy, T. E. (1980). Discontinuous wilderness: minimum areas for conservation. Parks, 5, 5-13.
Matheson, A., Buchamann, S., O'Toole, C., Westrich, P., & Williams, I. H. (1996). The conservation of bees. London: Academy Press.
Melo, M. S., Oliveira, D. E., & Franceschinelli, E. V., 2014. Low density and fertility of Murici (Byrsonima pachyphylla, Malpighiaceae) in small Cerrado remnants. Acta Botanica Brasilica, 28, 59-64.
Murcia, C. (1990). Effect of floral morphology on pollen receipt and removal in Ipomoea trichocarpa. Ecology, 71, 1098-1109.
Murcia, C. (1996). Forest fragmentation and the pollination on of Neotropical plants. In J. Schelhas, & R. Greenberg (Eds.) Forest Patches in tropical landscapes (pp. 19-37). Washington, DC: Island Press.
Nóbrega, A. M. F., Valeri, S. V., Paula, R. C., & Silva, S. A. (2008). Regeneração natural em remanescentes florestais e áreas reflorestadas da várzea do rio Mogi-Guaçu, Luiz Antônio-SP. Revista Árvore, 32, 909-920.
Oostermeijer, J. G. B., Altenburg, R.G. M., & den Nijs, H. C. M. (1995). Effects of outcrossing distance and selfing on fitness components in the rare Gentiana pneumonanthe (Gentianaceae). Acta Botanica Neerlandica, 44, 257-268.
Orrock, J. L., Danielson, B. J., & Burns, M. J. (2003). Spatial ecology of predator-prey interactions: corridors and patch shape influence seed predation. Ecology, 84, 2589-2599.
Orrock, J. L., Levey, D. J., & Danielson, B. J. (2006). Seed predation, not seed dispersal, explains the landscape-level abundance of an early-successional plant. Journal of Ecology, 94, 838-845.
Pinto, L. P., Hirota, M., & Fonseca, M. (2002). Panorama da Mata Atlântica e dos Campos Sulinos. In: Maury, C. M. (Ed). Biodiversidade brasileira: avaliação e identificação de áreas e ações prioritárias par conservação, utilização sustentável e repartição de benefícios da biodiversidade brasileira (pp. 215-266). Brasília DF: Ministério do Meio Ambiente.
Pizo, M. A. (1997). Seed dispersal and predation in two populations of Cabralea canjerana (Meliaceae) in the Atlantic Forest of southeastern Brazil. Journal of Tropical Ecology, 13, 559-577.
Powell, A. H., & Powell, J. V. N. (1987). Population dynamics of male euglossine bees in Amazonian forest fragments. Biotropica, 19, 176-179.
Prach, K., Pysek, P., & Smilauer, P. (1997). Changes in species traits during succession: A search for pattern. Oikos, 79, 201-205.
Quesada, M., Stoner, K. E., Lobo, J. A., Herrerias-Diego, Y., Palacios-Guevara, C., Munguía-Rosas, M. A., Salazar, K. A. O., & 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, 131-138.
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, 400-406.
R Development Core Team (2008). An Introduction to R: Notes on R, A Programming Environment for Data Analysis and Graphics (electronic edition): http://cran.r-project.org/doc/manuals/R-intro.html.
Rathcke, B. J., & Jules, E. S. (1993). Habitat fragmentation and plant-pollinator interactions. Current Science, 65, 273-276.
Roubik, D. W. (1993). Ecology and natural history of tropical bees. Cambridge, UK: Cambridge University Press.
Santos, T., & Telleria, J. L. (1994). Influence of forest fragmentation on seed consumption and dispersal of Spanish juniper Juniperus thurifera. Biological Conservation, 70, 129-134.
Saunders, D. A., Hobbs, R. J., & Margules, C. R. (1991). Biological consequences of ecosystem fragmentation: A Review. Conservation Biology, 5, 18-32.
Simberloff, D. (1993). Effects of fragmentation on some Florida ecosystems, and how to redress them. In D. A. Saunders, R. J. Hobbs, & P. R. Ehrlich (Eds.) Nature Conservation 3: Reconstruction of fragmented ecosystems (pp. 174-187). Chipping Norton: Surrey Beatty & Sons.
Tabarelli, M., Montovani, W., & Peres, C. A. (1999). Effects of habitat fragmentation on plant guild structure in the montane Atlantic forest of Southeastern Brazil. Biological Conservation, 91, 119-127.
Wagenius, S., & Lyon, S. P. (2010). Reproduction of Echinacea angustifolia in fragmented prairie is pollen-limited but not pollinator-limited. Ecology, 91, 733-742.
Young, H. (2002). Diurnal and nocturnal pollination of Silene alba (Caryophyllaceae). American Journal of Botany, 89, 433-440.
Zabel, J., & Tscharntke, T. 1998. Does fragmentation of Urtica habitat affect phytophagous and predatory insect differentially? Oecologia, 116, 419-425.
Comments
This work is licensed under a Creative Commons Attribution 4.0 International License.
Copyright (c) 2015 Revista de Biología Tropical