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Leaf-cutting ants alter seedling assemblages across second-growth stands of Brazilian Atlantic forest

Published online by Cambridge University Press:  01 June 2012

Paulo S. D. Silva ,
Inara R. Leal ,
Rainer Wirth ,
Felipe P. L. Melo  and
Marcelo Tabarelli
Paulo S. D. Silva
Affiliation:
Programa de Pós-Graduação em Biologia Vegetal, Universidade Federal de Pernambuco, Av. Prof. Moraes Rego, s/n, Cidade Universitária, CEP 50670-901, Recife, PE, Brazil
Inara R. Leal
Affiliation:
Departamento de Botânica, Universidade Federal de Pernambuco, Av. Prof. Moraes Rego, s/n, Cidade Universitária, CEP 50670-901, Recife, PE, Brazil
Rainer Wirth
Affiliation:
University of Kaiserslautern, Department of Plant Ecology and Systematics, Postfach 3049, 67653, Kaiserslautern, Germany
Felipe P. L. Melo
Affiliation:
Departamento de Botânica, Universidade Federal de Pernambuco, Av. Prof. Moraes Rego, s/n, Cidade Universitária, CEP 50670-901, Recife, PE, Brazil
Marcelo Tabarelli*
Affiliation:
Departamento de Botânica, Universidade Federal de Pernambuco, Av. Prof. Moraes Rego, s/n, Cidade Universitária, CEP 50670-901, Recife, PE, Brazil
*
2Corresponding author. Email: [email protected]
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Abstract:

Secondary forests promote an increased abundance of leaf-cutting ants (LCA) but the consequences on forest dynamics have been poorly addressed. Here we examine seedling assemblage attributes, seed germination and seedling survival across foraging zones of Atta cephalotes colonies inhabiting 15 second-growth patches (25–47 y old) of Atlantic forest. Seeds and seedlings were monitored within foraging zones and control sites over 1 y, including spots around ant nests. Overall, 1862 seedlings from 108 plant species were recorded. Seedling density decreased by 53% in foraging-zone plots (3.31 ± 0.23 seedlings m−2) when compared with control plots (7.02 ± 0.44 seedlings m−2) and a similar decrease was observed for species richness. Ant-induced alterations in the seedling assemblage were further indicated by segregation between foraging-zone and control plots (NMDS), habitat effects on species similarity (ANOSIM), and indicator tree species associated with control plots. While seed germination and seedling survivorship were uncorrelated to either nest distance or age of second-growth stands (with the exception of Tapirira guianensis), defoliation by LCAs was a significant cause of seedling mortality. Our results suggest that LCAs interfere with successional trajectories of Atlantic forest as foraging zones filter seedling establishment, supporting less-dense, impoverished and convergent seedling assemblages.

Keywords

Attaecological filterecosystem engineeringherbivoryforest regenerationplant recruitmentseed germination
Type
Research Article
Information
Journal of Tropical Ecology , Volume 28 , Issue 4 , July 2012 , pp. 361 - 368
Copyright
Copyright © Cambridge University Press 2012

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References

LITERATURE CITED

ALMEIDA, W. R., WIRTH, R. & LEAL, I. R. 2008. Edge-mediated reduction of phorid parasitism on leaf-cutting ants in a Brazilian Atlantic forest. Entomologia Experimentalis et Applicata 129:251–257.CrossRefGoogle Scholar
AUGSPURGER, C. K. 1984. Seedling survival of tropical tree species – interactions of dispersal distance, light-gaps, and pathogens. Ecology 65:1705–1712.CrossRefGoogle Scholar
BIEBER, A. G. D., OLIVEIRA, M. A., WIRTH, R., TABARELLI, M. & LEAL, I. R. 2011. Do abandoned nests of leaf-cutting ants enhance plant recruitment in the Atlantic Forest? Austral Ecology 36:220–232.CrossRefGoogle Scholar
CHAZDON, R. L., COLWELL, R. K., DENSLOW, J. S. & GUARIGUATA, M. R. 1998. Statistical methods for estimating species richness of woody regeneration in primary and secondary rain forests of Northeastern Costa Rica. Pp. 285–310 in Dallmeier, F. & Comiskey, J. A. (eds.). Forest biodiversity research, monitoring and modelling: conceptual background and old world case studies. Man and the Biosphere Series, vol 20. UNESCO, Paris and The Parthenon Publishing Group, Carnforth. 671 pp.Google Scholar
CHERRETT, J. M. 1989. Leaf-cutting ants. Pp. 473–486 in Lieth, H. & Werger, M. J. A. (eds.). Ecosystems of the world. Volume 14B. Elsevier, Amsterdam. 713 pp.Google Scholar
CORRÊA, M. M., SILVA, P. S. D., WIRTH, R., TABARELLI, M. & LEAL, I. R. 2010. How leaf-cutting ants impact forests: drastic nest effects on light environment and plant assemblages. Oecologia 162:103–115.CrossRefGoogle ScholarPubMed
DALLING, J. W. & WIRTH, R. 1998. Dispersal of Miconia argentea seeds by the leaf-cutting ant Atta colombica. Journal of Tropical Ecology 14:705–710.CrossRefGoogle Scholar
DOHM, C., LEAL, I. R., TABARELLI, M., MEYER, S. T. & WIRTH, R. 2011. Leaf-cutting ants proliferate in the Amazon: an expected response to forest edge? Journal of Tropical Ecology 27:645–649.CrossRefGoogle Scholar
DUFRÊNE, M. & LEGENDRE, P. 1997. Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecological Monographs 67:345–366.Google Scholar
FARJI-BRENER, A. G. 2001. Why are leaf-cutting ants more common in early secondary forests than in old-growth tropical forests? An evaluation of the palatable forage hypothesis. Oikos 92:169–177.CrossRefGoogle Scholar
FARJI-BRENER, A. G. & ILLES, A. E. 2000. Do leaf-cutting ant nests make “bottom-up” gaps in neotropical rain forests? A critical review of the evidence. Ecology Letters 3:219–227.CrossRefGoogle Scholar
FARJI-BRENER, A. G. & SILVA, J. F. 1995. Leaf-cutting ants and forest groves in a tropical parkland savanna of Venezuela – facilitated succession. Journal of Tropical Ecology 11:651–669.CrossRefGoogle Scholar
FOWLER, H. G., PAGANI, M. I., SILVA, O. A., FORTI, L. C. & SAES, N. B. 1989. A pest is a pest is a pest? The dilemma of neotropical leaf-cutting ants: keystone taxa of natural ecosystems. Environmental Management 13:671–675.CrossRefGoogle Scholar
GARRETTSON, M., STETZEL, J., HALPERN, B., HEARN, J., LUCEY, B. & MCKONE, M. 1998. Diversity and abundance of understory plants on active and abandoned nest of leaf-cutting ants (Atta cephalotes) in Costa Rica rain forest. Journal of Tropical Ecology 14:17–26.CrossRefGoogle Scholar
GRILLO, A., OLIVEIRA, M. A. & TABARELLI, M. 2006. Árvores. Pp. 191–216 in Porto, K. C., Almeida-Cortez, J. S. & Tabarelli, M. (eds.). Diversidade biológica e conservação da Floresta Atlântica ao Norte do Rio São Francisco. (First edition). Ministério do Meio Ambiente, Brasilia.Google Scholar
HULL-SANDERS, H. M. & HOWARD, J. J. 2003. Impact of Atta colombica colonies on understory vegetation and light availability in a neotropical forest. Biotropica 35:441–445.CrossRefGoogle Scholar
KOST, C., GAMA, DE, OLIVEIRA, E., KNOCH, T. & WIRTH, R. 2005. Spatio-temporal permanence and plasticity of foraging trails in young and mature leaf-cutting ant colonies (Atta spp.). Journal of Tropical Ecology 21:677–688.CrossRefGoogle Scholar
KREBS, C. 1999. Ecological methodology. (Second edition). Addison-Wesley Educational Publishers, Inc., Menlo Park. 620 pp.Google Scholar
MEYER, S. T., LEAL, I. R. & WIRTH, R. 2009. Persisting hyper-abundance of leaf-cutting ants (Atta spp.) at the edge of an old Atlantic forest fragment. Biotropica 41:711–716.CrossRefGoogle Scholar
MEYER, S. T., LEAL, I. R., TABARELLI, M. & WIRTH, R. 2011a. Ecosystem engineering by leaf-cutting ants: nests of Atta cephalotes drastically alter forest structure and microclimate. Ecological Entomology 36:14–24.CrossRefGoogle Scholar
MEYER, S. T., LEAL, I. R., TABARELLI, M. & WIRTH, R. 2011b. Performance and fate of tree seedlings on and around nests of the leaf-cutting ant Atta cephalotes: ecological filters in a fragmented forest. Austral Ecology 36:779–790.CrossRefGoogle Scholar
MOUTINHO, P., NEPSTAD, D. C. & DAVIDSON, E. A. 2003. Influence of leaf-cutting ant nests on secondary forest growth and soil properties in Amazonia. Ecology 84:1265–1276.CrossRefGoogle Scholar
NEPSTAD, D. C., UHL, C., PEREIRA, C. A. & SILVA, J. M. C. 1996. A comparative study of tree establishment in abandoned pasture and mature forest of eastern Amazonia. Oikos 76:25–39.CrossRefGoogle Scholar
NICOTRA, A. B., CHAZDON, R. L. & IRIARTE, S. V. B. 1999. Spatial heterogeneity of light and woody seedling regeneration in tropical wet forests. Ecology 80:1908–1926.CrossRefGoogle Scholar
PEÑALOZA, C. & FARJI-BRENER, A. G. 2003. The importance of treefall gaps as foraging sites for leaf-cutting ants depends on forest age. Journal of Tropical Ecology 19:603–605.CrossRefGoogle Scholar
RAO, M. 2000. Variation in leaf-cutter ant (Atta sp.) densities in forest isolates: the potential role of predation. Journal of Tropical Ecology 16:209–225.CrossRefGoogle Scholar
RAO, M., TERBORGH, J. & NUNEZ, P. 2001. Increased herbivory in forest isolates: implications for plant community structure and composition. Conservation Biology 15:624–633.CrossRefGoogle Scholar
ROCKWOOD, L. L. 1973. The effect of defoliation on seed production of six Costa Rican tree species. Ecology 54:1363–1369.CrossRefGoogle Scholar
SANTOS, B. A., PERES, C. A., GRILLO, A., ALVES-COSTA, C. P. & TABARELLI, M. 2008. Drastic erosion in functional attributes of tree assemblages in Atlantic forest fragments of northeastern Brazil. Biological Conservation 5:18–32.Google Scholar
SILVA, P. D., LEAL, I. R., WIRTH, R. & TABARELLI, M. 2007. Harvesting of Protium heptaphyllum (Aubl.) March. seeds (Burseraceae) by the leaf-cutting ant Atta sexdens L. promotes seed aggregation and seedling mortality. Revista Brasileira de Botânica 30:553–560.Google Scholar
SILVA, P. S. D., BIEBER, A. G. D., LEAL, I. R., WIRTH, R. & TABARELLI, M. 2009. Decreasing abundance of leaf-cutting ants across a chronosequence of advancing Atlantic forest regeneration. Journal of Tropical Ecology 25:223–227.CrossRefGoogle Scholar
SOKAL, R. R. & ROHLF, F. J. 1995. Biometry: the principles and practice of statistics in biological research. (Third edition). W.H. Freeman, New York. 887 pp.Google Scholar
STERNBERG, L. S. L., PINZON, M. C., MOREIRA, M. Z., MOUTINHO, P., ROJAS, E. L. & HERRE, E. A. 2007. Plants use macronutrients accumulated in leaf-cutting ant nests. Proceedings of the Royal Society of London B – Biological Science 274:315–321.CrossRefGoogle Scholar
SVENNING, J. C. 2000. Small canopy gaps influence plant distributions in the rain forest understory. Biotropica 32:252–261.CrossRefGoogle Scholar
URBAS, P., ARAÚJO, M. V., LEAL, I. R. & WIRTH, R. 2007. Cutting more from cut forests: edge effects on foraging and herbivory of leaf-cutting ants in Brazil. Biotropica 39:489–495.CrossRefGoogle Scholar
VASCONCELOS, H. L. & CHERRETT, J. M. 1995. Changes in leaf-cutting ant populations (Formicidae, Attini) after the clearing of mature forest in Brazilian Amazonia. Studies on Neotropical Fauna and Environment 30:107–113.CrossRefGoogle Scholar
VASCONCELOS, H. L. & CHERRETT, J. M. 1997. Leaf-cutting ants and early forest regeneration in central Amazonia: effects of herbivory on tree seedling establishment. Journal of Tropical Ecology 13:357–370.CrossRefGoogle Scholar
VASCONCELOS, H. L., VIEIRA-NETO, E. H. M., MUNDIM, F. M. & BRUNA, E. M. 2006. Roads alter the colonization dynamics of a keystone herbivore in neotropical savannas. Biotropica 38:661–665.CrossRefGoogle Scholar
VIEIRA-NETO, E. & VASCONCELOS, H. L. 2010. Developmental changes in factors limiting colony survival and growth of the leaf-cutter ant Atta laevigata. Oikos 33:538–544.Google Scholar
WEBER, N. A. 1972. Gardening ants, the attines. Memoirs of the American Philosophical Society 92:1–146.Google Scholar
WIRTH, R., BEYSCHLAG, W., RYEL, R., HERZ, H. & HÖLLDOBLER, B. 2003. The herbivory of leaf-cutting ants – a case study on Atta colombica in the tropical rainforest of Panama. Ecological Studies 164:1–230.CrossRefGoogle Scholar
WIRTH, R., MEYER, S. T., ALMEIDA, W. R., ARAUJO, M. V., BARBOSA, V. S. & LEAL, I. R. 2007. Increasing densities of leaf-cutting ants (Atta spp.) with proximity to the edge in a Brazilian Atlantic forest. Journal of Tropical Ecology 23:501–505.CrossRefGoogle Scholar