Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-19T03:52:18.716Z Has data issue: false hasContentIssue false
  • English
  • Français

Leaf-cutting ant populations profit from human disturbances in tropical dry forest in Brazil

Published online by Cambridge University Press:  11 October 2017

Felipe F. S. Siqueira ,
José Domingos Ribeiro-Neto ,
Marcelo Tabarelli ,
Alan N. Andersen ,
Rainer Wirth  and
Inara R. Leal
Felipe F. S. Siqueira
Affiliation:
Programa de Pós-Graduação em Biologia Vegetal, Universidade Federal de Pernambuco, Av. Prof. Moraes Rego s/n, Cidade Universitária, 50670–901, Recife, PE, Brazil
José Domingos Ribeiro-Neto
Affiliation:
Programa de Pós-Graduação em Biologia Vegetal, Universidade Federal de Pernambuco, Av. Prof. Moraes Rego s/n, Cidade Universitária, 50670–901, Recife, PE, Brazil Departamento de Fitotecnia e Ciências Ambientais, Centro de Ciências Agrárias, Universidade Federal da Paraíba, Rodovia PB-079, 58397-000, Areia, PB, Brazil
Marcelo Tabarelli
Affiliation:
Departamento de Botânica, Universidade Federal de Pernambuco, Av. Prof. Moraes Rego s/n°, Cidade Universitária, 50670–901, Recife, PE, Brazil
Alan N. Andersen
Affiliation:
Research Institute for the Environment and Livelihoods, Charles Darwin University, NT 0909, Australia
Rainer Wirth
Affiliation:
Plant Ecology and Systematics, University of Kaiserslautern, PO Box 3049, 67663, Kaiserslautern, Germany
Inara R. Leal*
Affiliation:
Departamento de Botânica, Universidade Federal de Pernambuco, Av. Prof. Moraes Rego s/n°, Cidade Universitária, 50670–901, Recife, PE, Brazil
*
*Corresponding author. Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract:

Anthropogenic disturbance often results in the proliferation of native species of particular groups that leads to biotic homogenization. Leaf-cutting ants are an example of such winner organisms in tropical rain forests, but their response to disturbance in dry forests is poorly known. We investigated Atta colony density in areas of tropical dry forest in Brazil with different distance to roads and vegetation cover. Atta colonies were surveyed in 59 belt transects of 300 × 20 m, covering a total area of 35.4 ha. We found 224 Atta colonies, 131 of which were active and belonged to Atta opaciceps (87 colonies, 2.45 ha−1), A. sexdens (35 colonies, 0.98 ha−1) and A. laevigata (9 colonies, 0.25 ha−1). The density of active colonies sharply decreased from 15 ± 2.92 ha−1 in the 50-m zone along roads to only 2.55 ± 1.65 ha−1 at distances up to 300 m. The reverse pattern was observed for inactive colonies. Active Atta colonies preferentially occur in areas with low vegetation cover, while inactive colonies prefer areas with high vegetation cover. We demonstrate for the first time that anthropogenic disturbances promote the proliferation of leaf-cutting ants in dry forest in Brazil, which may affect plant regeneration via herbivory and ecosystem engineering as demonstrated for rain forests.

Keywords

Atta laevigataAtta opacicepsAtta sexdenschronic anthropogenic disturbancecolony densityecological releaseedge effectroadsseasonally dry tropical forest
Type
Research Article
Information
Journal of Tropical Ecology , Volume 33 , Issue 5 , September 2017 , pp. 337 - 344
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

LITERATURE CITED

AHRENDS, A., BURGESS, A. N. D., MILLEDGE, S. A. H., BULLING, M. T., FISHER, B., SMART, J. C. R., CLARKE, G. P., MHORO, B. E. & LEWIS, S. L. 2010. Predictable waves of sequential forest degradation and biodiversity loss spreading from an African city. Proceedings of the National Academy of Sciences USA 107:14556–14561.CrossRefGoogle ScholarPubMed
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
BARRERA, C. A., BUFFA, L. M. & VALLADARES, G. 2015. Do leaf-cutting ants benefit from forest fragmentation? Insights from community and species-specific responses in a fragmented dry forest. Insect Conservation and Diversity 8:456–463.CrossRefGoogle Scholar
BARRERA, C. A., BECKER, E. L., ELIZALDE, L. & QUEIROZ, J. M. 2017. Parasitoid phorid flies of leaf-cutting ants are negatively affected by loss of forest cover. Entomologia Experimentalis et Applicata 164: 66–77.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
BRANDÃO, C. R. F. 1995. Formigas dos Cerrados e Caatingas. Habilitation thesis, Universidade de São Paulo, 147 pp.Google Scholar
COFFIN, A. W. 2007. From roadkill to road ecology: a review of the ecological effects of roads. Journal of Transport Geography 15:396–406.Google Scholar
COLEY, P. D. & BARONE, J. A. 1996. Herbivory and plant defenses in tropical forests. Annual Review of Ecology and Systematics 27:305–335.CrossRefGoogle Scholar
COLEY, P. D., BRYANT, J. P. & CHAPIN, F. S. 1985. Resource availability and plant anti-herbivore defense. Science 230:895–899.CrossRefGoogle Scholar
CORRÊA, M., SILVA, P., 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
CORRÊA, M., SILVA, P. S. D., WIRTH, R., TABARELLI, M. & LEAL, I. R. 2016. Foraging activity of leaf-cutting ants changes light availability and plant assemblage in Atlantic forest. Ecological Entomology 41:442–450.CrossRefGoogle Scholar
COSTA, A. N. & VIEIRA-NETO, E. H. M. 2015. Species turnover regulates leafcutter ant densities in environmental gradients across the Brazilian Cerrado. Journal of Applied Entomology 140:474–478.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
ESTES, J. A, TERBORGH, J., BRASHARES, J. S., POWER, M. E., BERGER, J., BOND, W. J., CARPENTER, S. R., ESSINGTON, T. E., HOLT, R. D., JACKSON, J. B. C., MARQUIS, R. J., OKSANEN, L., OKSANEN, T., PAINE, R. T., PIKITCH, E. K., RIPPLE, W. J., SANDIN, S. A, SCHEFFER, M., SCHOENER, T. W., SHURIN, J. B., SINCLAIR, A. R. E., SOULÉ, M. E., VIRTANEN, R. & WARDLE, D. A. 2011. Trophic downgrading of planet Earth. Science 333:301–306.CrossRefGoogle ScholarPubMed
FAHRIG, L. 2013. Rethinking patch size and isolation effects: the habitat amount hypothesis. Journal of Biogeography 40:1649–1663.CrossRefGoogle Scholar
FALCÃO, P. F., PINTO, S. R. R., WIRTH, R. & LEAL, I. R. 2011. Edge-induced narrowing of dietary diversity in leaf-cutting ants. Bulletin of Entomological Research 101:305–311.CrossRefGoogle ScholarPubMed
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. 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
FORYS, E. A., ALLEN, C. R. & WOJCIK, D. P. 2002. Influence of proximity and amount of human development and roads on the occurrence of the red imported fire ant in the lower Florida Keys. Biological Conservation 108:7–33.CrossRefGoogle Scholar
FOWLER, H. G. 1983. Distribution patterns of Paraguayan leaf-cutting ants (Atta and Acromyrmex) (Formicidae: Attini). Studies on Neotropical Fauna Environment 18:121–138.CrossRefGoogle Scholar
FOWLER, H. G., PEREIRA, V. S. & FORTI, L.C. 1986. Population dynamics of leaf-cutting ants: a brief review. Pp. 123–145 in Lofgren, C. S. & Vander Meer, R. K. (eds). Fire ants and leaf-cutting ants: biology and management. Westview Press, London.Google Scholar
GOULD, W. 2000. Remote sensing of vegetation, plant species richness, and regional biodiversity hotspots. Ecological Applications 10:1861–1870.CrossRefGoogle Scholar
HÖLLDOBLER, B., & WILSON, E. O. 1990. The ants. Harvard University Press, Cambridge. 732 pp.CrossRefGoogle Scholar
JAFARI, R., LEWIS, M. M. & OSTENDORF, B. 2007. Evaluation of vegetation indices for assessing vegetation cover in southern arid lands in South Australia. Rangeland Journal 29:39–49.CrossRefGoogle Scholar
JAIN, A. K., MURTY, M. N. & FLYNN, P. J. 1999. Data clustering: a review. ACM Computing Surveys 31:265–323.CrossRefGoogle Scholar
LEAL, I. R., SILVA, J. M. C., TABARELLI, M. & LACHER, T. E. 2005. Changing the course of biodiversity conservation in the Caatinga of Northeastern Brazil. Conservation Biology 19:701–706.CrossRefGoogle Scholar
LEAL, I. R., WIRTH, R. & TABARELLI, M. 2014. The multiple impacts of leaf‐cutting ants and their novel ecological role in human‐modified neotropical forests. Biotropica 46:516–528.CrossRefGoogle Scholar
LIMA, A. L. A. & RODAL, M. J. N. 2010. Phenology and wood density of plants growing in the semi-arid region of northeastern Brazil. Journal of Arid Environment 74:1363–1373.CrossRefGoogle Scholar
LÔBO, D., LEÃO, T., MELO, F. P. L., SANTOS, A. M. M. & TABARELLI, M. 2011. Forest fragmentation drives Atlantic forest of northeastern Brazil to biotic homogenization. Diversity and Distributions 17:287–296.CrossRefGoogle Scholar
MAGRIN, G. O., MARENGO, J. A., BOULANGER, J. P., BUCKERIDGE, M. S., CASTELLANOS, E., POVEDA, G., SCARANO, F. R. & VICUÑA, S. 2014. Central and South America. Pp. 1499–1566 in Barros, V. R., Field, C. B., Dokken, D. J., Mastrandrea, M. D., Maach, K. L. & Bilir, T. E. (eds). Climate change 2014: impacts, adaptation, and vulnerability. Part b: regional aspects. Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge and New York.Google Scholar
MARTINSON, H. M. & FAGAN, W. F. 2014. Trophic disruption: a meta-analysis of how habitat fragmentation affects resource consumption in terrestrial arthropod systems. Ecology Letters 17:1178–1189.CrossRefGoogle ScholarPubMed
MARTORELL, C. & PETERS, E. M. 2005. The measurement of chronic disturbance and its effects on the threatened cactus Mammillaria pectinifera . Biological Conservation 124:199–207.CrossRefGoogle Scholar
MCKINNEY, M. L. & LOCKWOOD, J. L. 1999. Biotic homogenization: a few winners replacing many losers in the next mass extinction. Trends in Ecology and Evolution 14:450–453.CrossRefGoogle ScholarPubMed
MELO, F. P., SIQUEIRA, J. A., SANTOS, B. A., ALVARES-DA-SILVA, O., CEBALLOS, G. & BERNARD, E. 2014. Football and biodiversity conservation: Fifa and Brazil can still hit a green goal. Biotropica 46:257–259.CrossRefGoogle 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. 2011. 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., NEUBAUER, M., SAYER, E. J., LEAL, I. R., TABARELLI, M. & WIRTH, R. 2013. Leaf-cutting ants as ecosystem engineers: topsoil and litter perturbations around Atta cephalotes nests reduce nutrient availability. Ecological Entomology 38:497–504.CrossRefGoogle Scholar
MMA & IBAMA. 2010. Monitoramento do desmatamento nos biomas brasileiros por satélite: Monitoramento do Bioma Caatinga 2002 a 2008. Ministério do Meio Ambiente, Instituto Brasileiro do Meio Ambiente e Recursos Naturais Renováveis, Brasília. 46 pp.Google Scholar
MORRISON, L. W., KAWAZOE, E. A., GUERRA, R. & GILBERT, L. E. 2000. Ecological interactions of Pseudacteon parasitoids and Solenopsis ant hosts: environmental correlates of activity and effects on competitive hierarchies. Ecological Entomology 25:433–444.CrossRefGoogle Scholar
OLIVEIRA, D. G., PRATA, A. P. D. N., SOUTO, L. S. & FERREIRA, R. R. A. 2013. Does the edge effect influence plant community structure in a tropical dry forest? Revista Arvore 37:311–320.CrossRefGoogle Scholar
OLIVEIRA, M. A. DE, DELLA-LUCIA, T. M. C., ANJOS, N. DOS, DE OLIVEIRA, M. A. & DOS ANJOS, N. 1998. Occurrence and nest density of leaf-cutting ants in eucalypt plantations in southern Bahia. Revista Brasileira de Entomologia 42:17–21.Google Scholar
PENNINGTON, R. T., LAVIN, M. & OLIVEIRA-FILHO, A. 2009. Woody plant diversity, evolution, and ecology in the tropics: perspectives from seasonally dry tropical forests. Annual Review of Ecology, Evolution, and Systematics 40:437–457.CrossRefGoogle Scholar
PUREVDORJ, T., TATEISHI, R., ISHIYAMA, T. & HONDA, Y. 1998. Relationships between percent vegetation cover and vegetation indices. International Journal of Remote Sensing 19:3519–3535.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
RIBEIRO, E. M. S., ARROYO-RODRÍGUEZ, V., SANTOS, B. A., TABARELLI, M. & LEAL, I. R. 2015. Chronic anthropogenic disturbance drives the biological impoverishment of the Brazilian Caatinga vegetation. Journal of Applied Ecology 52:611–620.CrossRefGoogle Scholar
RIBEIRO, E. M. S., SANTOS, B. A., ARROYO-RODRÍGUES, V., TABARELLI, M., SOUZA, G. & LEAL, I. R. 2016. Phylogenetic impoverishment of plant communities following chronic human disturbances in the Brazilian Caatinga. Ecology 97:1583–1592.CrossRefGoogle ScholarPubMed
RIBEIRO-NETO, J. D., ARNAN, X., TABARELLI, M. & LEAL, I. R. 2016. Chronic anthropogenic disturbance causes homogenization of plant and ant communities in the Brazilian Caatinga. Biodiversity and Conservation 25:943–956.CrossRefGoogle Scholar
RITO, K. F., ARROYO-RODRÍGUEZ, V., QUEIROZ, R. T., LEAL, I. R. & TABARELLI, M. 2017a. Precipitation mediates the effect of human disturbance on the Brazilian Caatinga vegetation. Journal of Ecology. doi: 10.1111/1365-2745.12712.CrossRefGoogle Scholar
RITO, K. F., TABARELLI, M., & LEAL, I. R. 2017b. Euphorbiaceae responses to chronic anthropogenic disturbances in Caatinga vegetation: from species proliferation to biotic homogenization. Plant Ecology 218: 749–759.CrossRefGoogle Scholar
SANTOS, B. A., PERES, C. A., OLIVEIRA, M. 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 141:249–260.CrossRefGoogle Scholar
SANTOS, J. C., LEAL, I. R., ALMEIDA-CORTEZ, J. S., FERNANDES, G. W. & TABARELLI, M. 2011. Caatinga: the scientific negligence experienced by a dry tropical forest. Tropical Conservation Science 4:276–286.CrossRefGoogle Scholar
SILVA, P. S. D., WIRTH, R., TABARELLI, M. & LEAL, I. R. 2009. Decreasing abundance of leaf-cutting ants across a chronosequence of advancing Atlantic forest regeneration. Journal of Tropical Ecology 25:223–227.CrossRefGoogle Scholar
SINGH, S. P. 1998. Chronic disturbance, a principal cause of environmental degradation in developing countries. Environmental Conservation 25:1–2.CrossRefGoogle Scholar
SOCIEDADE NORDESTINA DE, ECOLOGIA. 2002. Projeto Técnico para a Criação do Parque Nacional do Catimbau/PE. Secretaria de Ciência, Tecnologia e Meio Ambiente de Pernambuco – SECTMA, Recife. 151 pp.Google Scholar
SUPERINA, M., & ABBA, A. M. 2014. What do we know about armadillos? An analysis of four centuries of knowledge about a group of South American mammals, with emphasis on their conservation. Mammal Review 44:69–80.CrossRefGoogle Scholar
TABARELLI, M., PERES, C. A. & MELO, F. P. L. 2012. The ‘few winners and many losers’ paradigm revisited: emerging prospects for tropical forest biodiversity. Biological Conservation 155:136–140.CrossRefGoogle Scholar
TERBORGH, J., LOPEZ, L., NUÑEZ, P., RAO, M., SHAHABUDDIN, G., ORIHUELA, G., RIVEROS, M., ASCANIO, R., ADLER, G. H., LAMBERT, T. D. & BALBAS, L. 2001. Ecological meltdown in predator-free forest fragments. Science 294:1923–1926.CrossRefGoogle ScholarPubMed
ULYSSÉA, M. A. & BRANDÃO, C. R. F. 2013. Ant species (Hymenoptera, Formicidae) from the seasonally dry tropical forest of northeastern Brazil: a compilation from field surveys in Bahia and literature records. Revista Brasileira de Entomologia 57:217–224.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. 1990. Foraging activity of two species of leaf-cutting ants (Atta) in a primary forest of the Central Amazon. Insectes Sociaux 37:131–145.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., 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. H. M. & VASCONCELOS, H. L. 2010. Developmental changes in factors limiting colony survival and growth of the leaf-cutter ant Atta laevigata . Ecography 33:538–544.CrossRefGoogle Scholar
VIEIRA-NETO, E. H. M., VASCONCELOS, H. L. & BRUNA, E. M. 2016. Roads increase population growth rates of a native leaf-cutter ant in Neotropical savannahs. Journal of Applied Ecology 53:983–992.CrossRefGoogle Scholar
WEBER, N. A. 1972. Gardening ants, the attines. The American Philosophical Society, Philadelphia. 146 pp.Google Scholar
WIRTH, R., HERZ, H., RYEL, R. J., BEYSCHLAG, W. & HOLLDOBLER, B. 2003. Herbivory of leaf-cutting ants: a case study on Atta colombica in the tropical rainforest of Panama. Springer-Verlag, Berlin. 230 pp.CrossRefGoogle Scholar
WIRTH, R., MEYER, S. T., ALMEIDA, W. R., ARAÚJO, 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
WIRTH, R., MEYER, S., LEAL, I. R. & TABARELLI, M. 2008. Plant herbivore interactions at the forest edge. Progress in Botany 69:423–448.CrossRefGoogle Scholar
WUELLNER, C. T. & SAUNDRES, J. B. 2003. Circadian and circannual patterns of activity and territory shifts: comparing a native ant (Solenopsis geminata, Hymenoptera: Formicidae) with its exotic, invasive congener (S. invicta) and its parasitoids (Pseudacteon spp., Diptera: Phoridae) at a Central Texas site. Annals of the Entomological Society of America 96:54–60.CrossRefGoogle Scholar
ZAR, J. H. 2010. Biostatistical analysis. Prentice Hall, Upper Saddle River. 663 pp.Google Scholar