Canopy herbivory and succession in a Brazilian tropical seasonally dry forest
Keywords:
deciduous forest, folivory, forest layers, herbivore guilds, natural regenerationAbstract
The general pattern of herbivory throughout succession has been drawn chiefly from temperate forest studies and mainly at the understorey. This is one of the very few studies to document canopy herbivory in relation to successional stages of tropical seasonally dry forests. Diversity of free-feeding herbivores (chewing and sap-sucking) and leaf damage caused by insect guilds (folivores, leaf miners and galling insects) were quantified in the canopy of 117 trees distributed in three areas of intermediate stages and three of late stage of succession of a tropical seasonally dry forest, in Serra do Cipó, Minas Gerais, Brazil. The richness of the chewing and sap-sucking guilds of herbivores was higher in late succession stages. The abundance of sap-sucking herbivores was also higher in the late stage, whereas chewing insects were more abundant in the intermediate succession. Overall leaf damage was higher in the earlier stage of succession. Folivory was the most frequent type of leaf damage in both succession stages and was present in 92.33% of the leaves, followed by leaf mining in 14.58% of the leaves, and galls in 5.27% of the leaves. Folivory showed no difference between successional stages, while leaf miners and gallers showed higher frequencies in the intermediate stage. These results largely corroborate the pattern earlier documented for temperate forests, of increasing diversity of herbivores and decreasing leaf damage across succession. More specific studies in tropical forests, however, did not corroborate the pattern found in temperate regions. The present study emphasises the importance of sampling across canopy of multiple plant species and analysing herbivore guilds individually for better understanding herbivory in tropical dry forests.
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References
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Basset, Y.N.D. (2001). Communities of insect herbivores foraging on mature trees vs. seedlings of Pourouma bicolor (Cecropiaceae) in Panama. Oecologia, 129: 253-260.
Basset, Y.N.D., Hammond, P.M., Barrios, H., Holloway, J.D., Miller, S.E. (2003). Vertical stratification of arthropod assemblages. In: Basset, Y.; Novotny, V.; Miller, S.E.; Kitching, R.L. (Ed.) Arthropods of tropical forests – spatio-temporal dynamics and resource use in the canopy. Cambridge: Cambridge University Press, p. 17-27.
Boege, K. (2005). Herbivore attack in Casearia nitida influenced by plant ontogenetic variation in foliage quality and plant architecture. Oecologia, 143: 117-125.
Borror, D.J., Triplehorn, C.A., Johnson, N.F. (2002). An introduction to the study of insects. Philadelphia: Saunders College Publishing.
Brown, B.J., Ewel, J.J. (1987). Herbivory in Complex and Simple Tropical Successional Ecosystems. Ecology, 68: 108-116.
Campos, R.I., Vasconcelos, H.L., Ribeiro, S.P., Neves, F.S., Soares, J.P. (2006). Relationship between tree size and insect assemblages associated with Anadenanthera macrocarpa. Ecography, 29: 442-450.
Coelho, M.S., Almada, E.D., Quintino, A.V., Fernandes, G.W, Santos, R.M., Sanchez-Azofeifa, G.A., Espírito-Santo, M.M. (2012). Floristic composition and structure of a seasonally dry tropical forest at different successional stages in the Espinhaço mountains, southeastern Brazil. Interciencia, 37: 190-196.
Coley, P.D., Bryant, J., Chapin III, F. (1985). Resource availability and plant antiherbivore defense. Science, 230: 895-899.
Coley, P.D., Aide, T.M. (1991). Comparison of herbivory and plant defense in temperate and tropical broad-leaved forests. In: Price, P.W.; Lewinsohn, T.M.; Fernandes. G.W.; Benson, W.W. (Ed.) Plant animal interactions: evolutionary ecology in tropical and temperate regions. New York, John Wiley and Sons, pp. 25–49.
Corbet, S.A. (1995). Insects, plants and succession: advantages of long-term set aside. Agriculture, Ecosystems & Environment, 53: 201-217.
Costa, F.V., Neves, F.S., Silva J.O., Fagundes, M. (2011). Relationship between plant development, tannin concentration and insects associated with Copaifera langsdorffii (Fabaceae). Arthropod-Plant Interactions, 5: 9-18.
Crist, T.O., Pradhan-Devare, S.V., Summerville K.S. (2006). Spatial variation in insect community and species responses to habitat loss and plant community composition. Oecologia, 147: 510-521.
Cuevas-Reyes, P., Hanson, P., Dirzo, R., Oyama, K. (2004). Diversity of gall-inducing insects in a Mexican tropical dry forest: The importance of plant species richness, life forms, host plant age and plant density. Journal of Ecology, 92: 707-716.
Denno, R.F., Perfect, T.J. (1994). Plant hoppers: their ecology and management. New York: Chapman and Hall.
Dirzo R., Boege K. (2008). Patterns of herbivory and defense in tropical dry and rain forests. In: Carson, W.; Schnitzer, S.A. (Ed.) Tropical forest community ecology. West Sussex: Blackwell Science, p. 63-78.
Edwards-Jones, G., Brown, V.K. (1993). Successional trends in insect herbivore population densities: a field test of a hypothesis. Oikos, 66: 463-471.
Eiten, G. (1978). Delimitation of Cerrado concept. Vegetation, 36: 169-178.
Espírito-Santo, M.M., Neves, F.S., Andrade-Neto, F.R., Fernandes, G.W. (2007). Plant architecture and meristem dynamics as the mechanisms determining the diversity of gall-inducing insects. Oecologia, 153: 353-364.
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Feeny, P.D. (1976). Plant appearance and chemical defence. Recent Advances in Phytochemistry, 10: 1-40.
Filip, V., Dirzo, R.J., Maass, M., Sarukhán, J. (1995). Within- and among-year variation in the levels of herbivory on the foliage of trees from a Mexican tropical deciduous forest. Biotropica, 27: 78-86.
Fonseca, C.R., Fleck, T., Fernandes, G.W. (2006). Processes driving ontogenetic succession of galls in a canopy tree. Biotropica, 38: 514-521.
Giulietti, A.M., Menezes, N.L., Pirani, M.M., Wanderley, M.G.L. (1987). Flora da Serra do Cipó, Minas Gerais: caracterização e lista das espécies. Boletim de Botânica, 9: 1-151.
Godfray, H.C.J. (1985). The Absolute Abundance of Leaf Miners on Plants of Different Successional Stages. Oikos, 45: 17-25.
Godfray, H.C.J., Lawton, J.H. (2001). Scale and species numbers. Trends in Ecology and Evolution, 16: 400-404.
Golden, D.M., Crist, T.O. (1999). Experimental effects of habitat fragmentation on old-field canopy insects: species, guild, and community responses. Oecologia, 118: 371-380.
González, V. (2003). Bosques secos. In: Aguilera, M.; Azócar, A.; González-Jimánez, E. (Ed.) Biodiversidad en Venezuela, Tomo II. Caracas: Fundación Polar y Editorial ExLibris, p. 734-744.
Guariguata, M.R., Ostertag, R. (2001). Neotropical secondary forest succession: changes in structural and functional characteristics. Forest Ecology and Management, 148: 185-206.
Janzen, D.H., Waterman, P.G. (1984). A seasonal census of phenolics, fibre and alkaloids in foliage of forest trees in Costa Rica: some factors influencing their distribution and relation to host selection by Sphingidae and Saturniidae. Biological Journal of the Linnean Society, 21: 439-454.
Janzen, D.H. (1988). Tropical dry forests: the most endangered major tropical ecosystem. In: Wilson, E.O. (Ed.) Biodiversity. Washington, DC: National Academy Press, p. 130-137.
Kikuzawa, K. (1983). Leaf survival of woody plants in deciduous broadleaved forests. Tall trees. Canadian Journal of Botany, 62: 2551-2556.
Lawton, J.H., McNeil, S. (1979). Between the devil and the deep blue sea: on the problems of being a herbivore. In: Anderson, R.M.; Turner, B.D.; Taylor, L.R. (Ed.) Population dynamics. Oxford: Blackwell, p. 223-244.
Leps, J., Novotny, V., Basset, Y. (2001). Habitat and successional status of plants inrelation to the communities of their leaf-chewing herbivores in Papua New Guinea. Journal of Ecology, 89: 186-199.
Lewinsohn, T.M., Novotny, V., Basset, Y. (2005). Insects on plants: diversity of herbivore assemblages revisited. Annual Review of Ecology, Evolution, and Systematics, 36: 597-620.
Lowman, M.D. (1984). An assessment of techniques for measuring herbivory: Is rain forest defoliation more intense than we thought? Biotropica, 16(4): 264-68.
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Martinko, E.A., Hagen, R.H., Griffith, J.A. (2006). Successional change in the insect community of a fragmented landscape. Landscape Ecology, 21: 711-721.
Miles, L., Newton, A.C., Defries, R.S., Ravilious, C., May, I., Blyth, S., Kapos, V., Gordon, J.E. (2006). A global overview of the conservation status of tropical dry forests. Journal of Biogeography, 33: 491-505.
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Morellato, L.P.C., Talora, D.C., Takahasi, A., Bencke, C.C., Romera, E.C., Ziparro, V.B. (2000). Phenology of Atlantic rain forest trees: a comparative study. Biotropica, 32: 811-823.
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Neves, F.S., Silva, J.O., Fernandes, G.W. (2014). Insect Herbivores and Leaf Damage along Successional and Vertical Gradients in a Tropical Dry Forest. Biotropica 46: 14-24.
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Perry, D.R. (1978). A method of access into the crowns of emergent and canopy trees. Biotropica, 10: 155-157.
Poorter, L., Van de Plassche, M., Willems, S., Boo, R.G.A. (2004). Leaf traits and herbivory rates of tropical tree species differing in successional status. Plant Biology, 6: 746-754.
Quesada, M., Sanchez-Azofeifa, G.A., Alvarez-Añorve, M., Stoner, K.E., Avila-Cabadilla, L., Calvo-Alvarado, J., Castillo, A., Espírito-Santo, M.M., Fagundes, M., Fernandes, G.W., Gamon, J., Lopezaraiza-Mikel, M., Lawrence, D., Morellato, L.P.C., Powers, J.S., Neves, F.S., Rosas-Guerrero, V., Sayago, R., Sanchez-Montoya, G. (2009). Succession and management of tropical dry forests in the Americas: Review and new perspectives. Forest Ecology and Management, 258: 1014-1024.
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Siemann, E., Haarstad, J., Tilman, D. (1999). Dynamics of plant and arthropod diversity during old field succession. Ecography, 22: 406-414.
Silva, J.O., Espírito-Santo, M.M., Melo, G.A. (2011). Herbivory on Handroanthus ochraceus (Bignoniaceae) along a successional gradient in a tropical dry forest. Arthropod-Plant Interaction, 6: 45-57.
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Basset, Y.N.D. (2001). Communities of insect herbivores foraging on mature trees vs. seedlings of Pourouma bicolor (Cecropiaceae) in Panama. Oecologia, 129: 253-260.
Basset, Y.N.D., Hammond, P.M., Barrios, H., Holloway, J.D., Miller, S.E. (2003). Vertical stratification of arthropod assemblages. In: Basset, Y.; Novotny, V.; Miller, S.E.; Kitching, R.L. (Ed.) Arthropods of tropical forests – spatio-temporal dynamics and resource use in the canopy. Cambridge: Cambridge University Press, p. 17-27.
Boege, K. (2005). Herbivore attack in Casearia nitida influenced by plant ontogenetic variation in foliage quality and plant architecture. Oecologia, 143: 117-125.
Borror, D.J., Triplehorn, C.A., Johnson, N.F. (2002). An introduction to the study of insects. Philadelphia: Saunders College Publishing.
Brown, B.J., Ewel, J.J. (1987). Herbivory in Complex and Simple Tropical Successional Ecosystems. Ecology, 68: 108-116.
Campos, R.I., Vasconcelos, H.L., Ribeiro, S.P., Neves, F.S., Soares, J.P. (2006). Relationship between tree size and insect assemblages associated with Anadenanthera macrocarpa. Ecography, 29: 442-450.
Coelho, M.S., Almada, E.D., Quintino, A.V., Fernandes, G.W, Santos, R.M., Sanchez-Azofeifa, G.A., Espírito-Santo, M.M. (2012). Floristic composition and structure of a seasonally dry tropical forest at different successional stages in the Espinhaço mountains, southeastern Brazil. Interciencia, 37: 190-196.
Coley, P.D., Bryant, J., Chapin III, F. (1985). Resource availability and plant antiherbivore defense. Science, 230: 895-899.
Coley, P.D., Aide, T.M. (1991). Comparison of herbivory and plant defense in temperate and tropical broad-leaved forests. In: Price, P.W.; Lewinsohn, T.M.; Fernandes. G.W.; Benson, W.W. (Ed.) Plant animal interactions: evolutionary ecology in tropical and temperate regions. New York, John Wiley and Sons, pp. 25–49.
Corbet, S.A. (1995). Insects, plants and succession: advantages of long-term set aside. Agriculture, Ecosystems & Environment, 53: 201-217.
Costa, F.V., Neves, F.S., Silva J.O., Fagundes, M. (2011). Relationship between plant development, tannin concentration and insects associated with Copaifera langsdorffii (Fabaceae). Arthropod-Plant Interactions, 5: 9-18.
Crist, T.O., Pradhan-Devare, S.V., Summerville K.S. (2006). Spatial variation in insect community and species responses to habitat loss and plant community composition. Oecologia, 147: 510-521.
Cuevas-Reyes, P., Hanson, P., Dirzo, R., Oyama, K. (2004). Diversity of gall-inducing insects in a Mexican tropical dry forest: The importance of plant species richness, life forms, host plant age and plant density. Journal of Ecology, 92: 707-716.
Denno, R.F., Perfect, T.J. (1994). Plant hoppers: their ecology and management. New York: Chapman and Hall.
Dirzo R., Boege K. (2008). Patterns of herbivory and defense in tropical dry and rain forests. In: Carson, W.; Schnitzer, S.A. (Ed.) Tropical forest community ecology. West Sussex: Blackwell Science, p. 63-78.
Edwards-Jones, G., Brown, V.K. (1993). Successional trends in insect herbivore population densities: a field test of a hypothesis. Oikos, 66: 463-471.
Eiten, G. (1978). Delimitation of Cerrado concept. Vegetation, 36: 169-178.
Espírito-Santo, M.M., Neves, F.S., Andrade-Neto, F.R., Fernandes, G.W. (2007). Plant architecture and meristem dynamics as the mechanisms determining the diversity of gall-inducing insects. Oecologia, 153: 353-364.
Espírito-Santo, M.M., Sevilha, A.C., Anaya F.C., Barbosa, R., Fernandes, G.W., Sanchez-Azofeifa, G.A., Scariot, A., Noronha, S.E., Sampaio, C.A. (2009). Sustainability of tropical dry forests: Two case studies in southeastern and central Brazil. Forest Ecology and Management, 258: 922-930.
Feeny, P.D. (1976). Plant appearance and chemical defence. Recent Advances in Phytochemistry, 10: 1-40.
Filip, V., Dirzo, R.J., Maass, M., Sarukhán, J. (1995). Within- and among-year variation in the levels of herbivory on the foliage of trees from a Mexican tropical deciduous forest. Biotropica, 27: 78-86.
Fonseca, C.R., Fleck, T., Fernandes, G.W. (2006). Processes driving ontogenetic succession of galls in a canopy tree. Biotropica, 38: 514-521.
Giulietti, A.M., Menezes, N.L., Pirani, M.M., Wanderley, M.G.L. (1987). Flora da Serra do Cipó, Minas Gerais: caracterização e lista das espécies. Boletim de Botânica, 9: 1-151.
Godfray, H.C.J. (1985). The Absolute Abundance of Leaf Miners on Plants of Different Successional Stages. Oikos, 45: 17-25.
Godfray, H.C.J., Lawton, J.H. (2001). Scale and species numbers. Trends in Ecology and Evolution, 16: 400-404.
Golden, D.M., Crist, T.O. (1999). Experimental effects of habitat fragmentation on old-field canopy insects: species, guild, and community responses. Oecologia, 118: 371-380.
González, V. (2003). Bosques secos. In: Aguilera, M.; Azócar, A.; González-Jimánez, E. (Ed.) Biodiversidad en Venezuela, Tomo II. Caracas: Fundación Polar y Editorial ExLibris, p. 734-744.
Guariguata, M.R., Ostertag, R. (2001). Neotropical secondary forest succession: changes in structural and functional characteristics. Forest Ecology and Management, 148: 185-206.
Janzen, D.H., Waterman, P.G. (1984). A seasonal census of phenolics, fibre and alkaloids in foliage of forest trees in Costa Rica: some factors influencing their distribution and relation to host selection by Sphingidae and Saturniidae. Biological Journal of the Linnean Society, 21: 439-454.
Janzen, D.H. (1988). Tropical dry forests: the most endangered major tropical ecosystem. In: Wilson, E.O. (Ed.) Biodiversity. Washington, DC: National Academy Press, p. 130-137.
Kikuzawa, K. (1983). Leaf survival of woody plants in deciduous broadleaved forests. Tall trees. Canadian Journal of Botany, 62: 2551-2556.
Lawton, J.H., McNeil, S. (1979). Between the devil and the deep blue sea: on the problems of being a herbivore. In: Anderson, R.M.; Turner, B.D.; Taylor, L.R. (Ed.) Population dynamics. Oxford: Blackwell, p. 223-244.
Leps, J., Novotny, V., Basset, Y. (2001). Habitat and successional status of plants inrelation to the communities of their leaf-chewing herbivores in Papua New Guinea. Journal of Ecology, 89: 186-199.
Lewinsohn, T.M., Novotny, V., Basset, Y. (2005). Insects on plants: diversity of herbivore assemblages revisited. Annual Review of Ecology, Evolution, and Systematics, 36: 597-620.
Lowman, M.D. (1984). An assessment of techniques for measuring herbivory: Is rain forest defoliation more intense than we thought? Biotropica, 16(4): 264-68.
Lowman, M.D., Wittman, P.K. (1996). Forest canopies – methods, hypotheses and future directions. Annual Review of Ecology, Evolution, and Systematics, 27: 55-81.
Maass, J.M. (1995). Conversion of tropical dry forest to pasture and agriculture. In: Bullock, S.H.; Mooney, H.A.; Medina, E. (Eds.) Seasonally Dry Tropical Forests. New York: Cambridge University Press, p. 399-422.
Madeira, B.G., Espírito-Santo, M.M., D’ÂngeloNeto, S., Nunes, Y.R.F., Sánchez-Azofeifa, A.S., Fernandes, G.W., Quesada, M. (2009). Changes in tree and lianas communities along a successional gradient in a tropical dry forest in southeastern Brazil. Plant Ecology, 201: 291-304.
Martinko, E.A., Hagen, R.H., Griffith, J.A. (2006). Successional change in the insect community of a fragmented landscape. Landscape Ecology, 21: 711-721.
Miles, L., Newton, A.C., Defries, R.S., Ravilious, C., May, I., Blyth, S., Kapos, V., Gordon, J.E. (2006). A global overview of the conservation status of tropical dry forests. Journal of Biogeography, 33: 491-505.
Moran, C.V., Southwood, T.R.E. (1982). The guild composition of arthropod communities in trees. Journal of Animal Ecology, 51: 289-306.
Morellato, L.P.C., Talora, D.C., Takahasi, A., Bencke, C.C., Romera, E.C., Ziparro, V.B. (2000). Phenology of Atlantic rain forest trees: a comparative study. Biotropica, 32: 811-823.
Murphy, P.G., Lugo, A.E. (1986). Ecology of tropical dry forest. Annual Review of Ecology, Evolution, and Systematics, 17: 67-88.
Nassar, J.M., Rodríguez, J.P., Sánchez-Azofeifa, A., Garvin, T., Quesada, M. (2008). Manual of Methods: Human, Ecological and Biophysical Dimensions of Tropical Dry Forests. Caracas: Ediciones IVIC Instituto Venezolano de Investigaciones Científicas.
Neves, F.S., Braga, R.F., Espírito-Santo, M.M., Delabie, J.H.C., Fernandes, G.W., Sánchez-Azofeifa, G.A. (2010a). Diversity of arboreal ants in a Brazilian Tropical Dry Forest: Effects of seasonality and successional Stage. Sociobiology, 56: 177-194.
Neves, F.S., Araújo, L.S., Fagundes, M., Espírito-Santo, M.M., Fernandes, G.W., Sánchez-Azofeifa, G.A., Quesada, M. (2010b). Canopy herbivory and insect herbivore diversity in a dry forest-savanna transition in Brazil. Biotropica, 42: 112-118.
Neves, F.S., Silva, J.O., Fernandes, G.W. (2014). Insect Herbivores and Leaf Damage along Successional and Vertical Gradients in a Tropical Dry Forest. Biotropica 46: 14-24.
Novotny, V., Basset, Y., Kitching, R. (2003). Herbivore assemblages and their food resources. In: Basset, Y.; Novotny, V.; Miller, S.; Kitching, R. (Ed.) Arthropods of Tropical Forests: Spatio-Temporal Dynamics and Resource Use in the Canopy. Cambridge: Cambridge University Press, p. 40-53.
Parker, G.G. (1995). Structure and microclimate of forest canopies. In: Lowman, M.D.; Nadkarni, N.M. (Ed.) Forest canopies. San Diego: Academic Press, p. 431-455.
Perry, D.R. (1978). A method of access into the crowns of emergent and canopy trees. Biotropica, 10: 155-157.
Poorter, L., Van de Plassche, M., Willems, S., Boo, R.G.A. (2004). Leaf traits and herbivory rates of tropical tree species differing in successional status. Plant Biology, 6: 746-754.
Quesada, M., Sanchez-Azofeifa, G.A., Alvarez-Añorve, M., Stoner, K.E., Avila-Cabadilla, L., Calvo-Alvarado, J., Castillo, A., Espírito-Santo, M.M., Fagundes, M., Fernandes, G.W., Gamon, J., Lopezaraiza-Mikel, M., Lawrence, D., Morellato, L.P.C., Powers, J.S., Neves, F.S., Rosas-Guerrero, V., Sayago, R., Sanchez-Montoya, G. (2009). Succession and management of tropical dry forests in the Americas: Review and new perspectives. Forest Ecology and Management, 258: 1014-1024.
Sánchez-Azofeifa, G.A., Quesada, M., Rodríguez, J. P., Nassar, J.M., Stoner, K.E., Castillo, A., Garvin, T., Zent, E.L., Calvo-Alvarado, J.C., Kalacska, M.E.R. (2005). Research priorities for Neotropical dry forests. Biotropica, 37: 477-485.
SAS (2000). Categorical data analysis using the SAS system. Cary: SAS Institute.
Schulz, R., Machado, M. (2000). Uebelmannia and their environment. São Paulo: Schulz Publishing.
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