The multiple impacts of leaf-cutting ants and their novel ecological role in human-modified neotropical forests

Biotropica

Volumn 46, Issue 5, 2014, Pages 516-528

  Leal, Inara R ^a   Wirth, Rainer ^b   Tabarelli, Marcelo ^a  

^a FEDERAL UNIVERSITY OF PERNAMBUCO   (Brazil)

^b Rheinland Pfälzische Technische Universität Kaiserslautern Landau   (Germany)

Author keywords

Atta; Ecological filtering; Ecosystem engineering; Herbivory; Human modified landscapes; Microclimatic changes; Nutrient cycling; Seed dispersal

Indexed keywords

ANT; DEFORESTATION; DISTURBANCE; ECOSYSTEM ENGINEERING; HERBIVORY; HETEROGENEITY; HOMOGENEITY; NEOTROPICAL REGION; NUTRIENT CYCLING; RESEARCH; SEED DISPERSAL; VEGETATION;

EID: 84902709290     PISSN: 00063606     EISSN: 17447429     Source Type: Journal    
DOI: 10.1111/btp.12126     Document Type: Review

References (144)

1. Agrawal, A. A. 2011. Current trends in the evolutionary ecology of plant defence. Funct. Ecol. 25: 420-432.
2. Allan, E., and M. J. Crawley 2011. Contrasting effects of insect and molluscan herbivores on plant diversity in a long-term field experiment. Ecol. Lett. 14: 1246-1253.
3. Almeida, W. R., R. Wirth, and I. R. Leal 2008. Edge-mediated reduction of phorid parasitism on leaf-cutting ants in a Brazilian Atlantic forest. Entomol. Exp. Appl. 129: 251-257.
4. Alvarado, A., C. W. Berish, and F. Peralta 1981. Leaf-cutter ant (Atta cephalotes) influence on the morphology of andepts in Costa-Rica. Soil Sci. Soc. Am. J. 45: 790-794.
5. Arnold, A. E., and N. M. Asquith 2002. Herbivory in a fragmented tropical forest: patterns from islands at Lago Gatún. Panamá. Biodivers. Conserv. 11: 1663-1680.
6. Ayres, M. P. 1993. Global change, plant defense, and herbivory. In P. M. Kareiva, J. G. Kingsolver, and R. B. Huey (Eds.). Biotic interactions and global change, pp. 75-94. SinauerAssociates, Sunderland, MA, U.S.A.
7. Bale, J. S., G. J. Masters, I. D. Hodkinson, C. Awmack, T. M. Bezemer, V. K. Brown, J. Butterfield, A. Buse, J. C. Coulson, J. Farrar, J. E. G. Good, R. Harrington, S. Hartley, T. H. Jones, R. L. Lindroth, M. C. Press, I. Symrnioudis, A. D. Watt, and J. B. Whittaker 2002. Herbivory in global climate change research: direct effects of rising temperature on insect herbivores. Global Change Biol. 8: 1-16.
8. Belovsky, G. E., and J. B. Slade 2000. Insect herbivory accelerates nutrient cycling and increases plant production. Proc. Natl Acad. Sci. USA 97: 14412-14417.
9. Belyea, L. R. 2004. Beyond ecological filters: feedback networks in the assembly and restoration of community structure. In V. M. Temperton, R. J. Hobbs, T. Nuttle, and S. Halle (Eds.). Assembly rules and restoration ecology - Bridging the gap between theory and practice, pp 115-131. Island Press, Washington, DC, U.S.A.
10. Bieber, A. G. D., M. A. Oliveira, R. Wirth, M. Tabarelli, and I. R. Leal 2011. Do abandoned nests of leaf-cutting ants enhance plant recruitment in the Atlantic Forest? Austral Ecol. 36: 220-232.
11. Bittleston, L. S., F. Brockmann, W. Wcislo, and S. A. Van Bael 2011. Endophytic fungi reduce leaf-cutting ant damage to seedlings. Biol. Letters 7: 30-32.
12. Blanton, C. M., and J. J. Ewel 1985. Leaf-cutting ant herbivory in successional and agricultural tropical ecosystems. Ecology 66: 861-869.
13. Byrne, M. M., and J. Levey 1993. Removal of seeds from frugivore defecations by ants in a Costa Rican forest. Vegetatio 107: 363-374.
14. Carvalho, K. S., A. Alencar, J. Balch, and P. Moutinho 2012. Leafcutter ant nests inhibit low-intensity fire spread in the understory of transitional forests at the Amazon's forest-savanna boundary. Psyche Article ID 780713, 7 pages, doi:10.1155/2012/780713.
15. Cherrett, J. M. 1968. The foraging behavior of Atta cephalotes L. (Hymenoptera, Formicidae) I. Foraging pattern and plant species attacked in tropical rain forest. J. Anim. Ecol. 37: 387-403.
16. Cherrett, J. M. 1989. Leaf-cutting ants. In H. Lieth and M. J. A. Werger (Eds.). Ecosystems of the world, pp. 473-486. Elsevier, Amsterdam, the Netherlands.
17. Coley, P. D. 1980. Effects of leaf age and plant life history patterns on herbivory. Nature 284: 545-546.
18. Coley, P. D. 1998. Possible effects of climate change on plant/herbivore interactions in moist tropical forests. Climatic Change 39: 455-472.
19. Coley, P. D., and J. A. Barone 1996. Herbivory and plant defenses in tropical forests. Annu. Rev. Ecol. Syst. 27: 305-335.
20. Coley, P. D., J. P. Bryant, and F. S. Chapin III. 1985. Resource availability and plant anti-herbivore defense. Science 230: 895-899.
21. Corrêa, M. M., P. S. D. Silva, R. Wirth, M. Tabarelli, and I. R. Leal 2010. How leaf-cutting ants impact forests: drastic nest effects on light environment and plant assemblages. Oecologia 162: 103-115.
22. Costa, U. A. S., S. R. R. Pinto, F. A. Silva, M. Oliveira, D. B. Agra, E. Marques, and I. R. Leal 2014. O papel das formigas como dispersores secundários de sementes na Floresta Atlântica Nordestina. In M. Tabarelli, A. V. Aguiar Neto, I. R. Leal, and A. V. Lopes (Eds.). Serra Grande: uma floresta de ideias, pp 415-438. Editora Universitária da UFPE, Recife, Brazil.
23. Costa, A. N., H. L. Vasconcelos, E. H. M. Vieira-Neto, and E. M. Bruna 2008. Do herbivores exert top-down effects in Neotropical savannas? J. Veg. Sci. 19: 849-854.
24. Dalling, J. W., and R. Wirth 1998. Dispersal of Miconia argentea seeds by leaf-cutting ant Atta colombica. J. Trop. Ecol. 14: 705-710.
25. De Fine Licht, H. H., and J. J. Boomsma 2010. Forage collection, substrate preparation, and diet composition in fungus-growing ants. Ecol. Entomol. 35: 259-269.
26. Didham, R. K., J. H. Lawton, P. M. Hammond, and P. Eggleton 1998. Trophic structure stability and extinction dynamics of beetles (Coleoptera) in tropical forest fragments. Philos. Trans. Royal Soc. B-Biol. Sci. 353: 437-451.
27. Dirzo, R. 1984. Insect-plant interactions: some ecophysiological consequences of herbivory. In E. Medina, H. A. Mooney, and C. Vasquez-Yanes (Eds.). Physiological ecology of plants of the wet tropics, pp. 209-224. Junk Publishers, The Hague, the Netherlands.
28. Dohm, C., I. R. Leal, M. Tabarelli, S. T. Meyer, and R. Wirth 2011. Leaf-cutting ants proliferate in the Amazon: an expected response to forest edge? J. Trop. Ecol. 27: 645-649.
29. Dukes, J. S., and H. A. Mooney 1999. Does global change increase the success of biological invaders?. Trends Ecol. Evol. 14: 135-139.
30. Estrada, C., W. T. Wcislo, and S. A. Van Bael 2013. Symbiotic fungi alter plant chemistry that discourages leaf-cutting ants. New Phytol. 198: 241-251.
31. Falcão, P. F., S. R. R. Pinto, R. Wirth, and I. R. Leal 2011. Edge-induced narrowing of dietary diversity in leaf-cutting ants. B. Entomol. Res. 101: 305-311.
32. Farji-Brener, A. G., and A. Ruggiero 1994. Leaf-cutting ants (Atta and Acromyrmex) inhabitating Argentina: patterns in species richness and geographical range sizes. J. Biogeogr. 21: 391-399.
33. 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.
34. Farji-Brener, A. G. 2005. The effect of abandoned leaf-cutting ant nests on plant assemblage composition in a tropical rainforest of Costa Rica. Écoscience 12: 554-560.
35. Farji-Brener, A. G. 2007. How plants may benefit from their consumers: leaf-cutting ants indirectly improve anti-herbivore defenses in Carduus nutans L. Plant Ecol. 193: 31-38.
36. Farji-Brener, A. G. 2010. Leaf-cutting ant nests and soil biota abundance in a semi-arid steppe of northwestern Patagonia. Sociobiology 56: 549-557.
37. Farji-Brener, A. G., and L. Ghermandi 2000. The influence of nests of leaf-cutting ants on plant species diversity in road verges of northern Patagonia. J. Veg. Sci. 11: 453-460.
38. Farji-Brener, A. G., and L. Ghermandi 2008. Leaf-cutting ant nests near roads increase fitness of exotic plant species in natural protected areas. Proc. Roy. Soc. B-Biol. Sci. 275: 1431-1440.
39. Farji-Brener, A. G., E. Gianoli, and M. A. Molina-Montenegro 2009. Small-scale disturbances spread along trophic chains: leaf-cutting ant nests, plants, aphids, and tending ants. Ecol. Res. 24: 139-145.
40. Farji-Brener, A. G., and A. E. Illes 2000. Do leaf-cutting ant nests make "bottom-up" gaps in Neotropical rain forests? A critical review of the evidence. Ecol. Lett. 3: 219-227.
41. Farji-Brener, A. G., N. Lescano, and L. Ghermandi 2010. Ecological engineering by a native leaf-cutting ant increases the performance of exotic plant species. Oecologia 163: 163-169.
42. Farji-Brener, A. G., and C. A. Medina 2000. The importance of where to dump the refuse: seed banks and fine roots in nests of the leaf-cutting ant Atta cephalotes and A. colombica. Biotropica 32: 120-126.
43. Farji-Brener, A. G., and J. Silva 1995a. Leaf-cutting ants and forest groves in a tropical parkland savanna of Venezuela: facilitated succession? J. Trop. Ecol. 11: 651-669.
44. Farji-Brener, A. G., and J. Silva 1995b. Leaf-cutting ants and soil fertility in a well-drained savanna in western Venezuela. Biotropica 27: 250-253.
45. Farji-Brener, A. G., and J. Silva 1996. Leaf-cutter ants' (Atta laevigata) aid to the establishment success of Tapirira velutinifolia (Anacardiaceae) seedlings in a parkland savanna? J. Trop. Ecol. 12: 163-168.
46. Ferreira, A. V., E. M. Bruna, and H. L. Vasconcelos 2011. Seed predators limit plant recruitment in neotropical savannas. Oikos 120: 1013-1022.
47. Fornoni, J. 2011. Ecological and evolutionary implications of plant tolerance to herbivory. Funct. Ecol. 25: 399-407.
48. Fowler, H. G. 1983. Distribution patterns of Paraguayan leaf-cutting ants (Atta and Acromyrmex) (Formicidae: Attini). Stud. Neotrop. Fauna E. 18: 121-138.
49. Fowler, H. G., M. I. Pagani, O. A. Silva, L. C. Forti, and N. B. Saes 1989. A pest is a pest is a pest? The dilemma of neotropical leaf-cutting ants: keystone taxa of natural ecosystems. Environ. Manage. 13: 671-675.
50. Fraver, S., N. V. L. Brokaw, and A. P. Smith 1996. Delimiting the gap phase in the growth cycle of a Panamanian forest. J. Trop. Ecol. 14: 673-681.
51. Garrettson, M., J. F. Stetzel, B. S. Halpern, D. J. Hearn, B. T. Lucey, and M. J. Mckone 1998. Diversity and abundance of understorey plants on active and abandoned nests of leaf-cutting ants (Atta cephalotes) in a costa rican rain forest. J. Trop. Ecol. 14: 17-26.
52. van Gils, H. A. J. 2012. Atta sexdens (Hymenoptera: Formicidae) nests are located under higher canopy cover in Colombian Amazon rainforests. Rev. Colomb. Entomol. 38: 114-117.
53. van Gils, H. A. J., L. E. Gómez, and A. Gaigl 2011. Atta sexdens (L.) (Hymenoptera: Formicidae) demography in the Colombian Amazon: an evaluation of the Palatable Forage Hypothesis. Environ. Entomol. 40: 770-776.
54. van Gils, H. A. J., and C. Vanderwoude 2012. Leafcutter ant (Atta sexdens) (Hymenoptera: Formicidae) nest distribution responds to canopy removal and changes in micro-climate in the Southern Colombian Amazon. Fla. Entomol. 95: 914-921.
55. Grillo, A. S., M. A. Oliveira, and M. Tabarelli 2006. Árvores. In K. Pôrto, J. S. Almeida-Cortez, and M. Tabarelli (Eds). Diversidade Biológica e Conservação da Floresta Atlântica ao Norte do Rio São Francisco, pp. 191-216. Série Biodiversidade n° 14. Brasília, Ministério do Meio Ambiente, Brasília, Brazil.
56. Haines, B. 1978. Element and energy flows through colonies of the leaf-cutting ant, Atta colombica in Panama. Biotropica 10: 270-277.
57. Haines, B., E. Kramer, and D. Clark 1990. Abundance of the leaf-cutting ant Atta cephalotes in relation to vegetation development and soils in eastern Costa Rica. Bull. Ecol. Soc. Am. 71: 178.
58. Harvey, C. A., O. Komar, R. Chazdon, B. G. Ferguson, B. Finegan, D. M. Griffith, M. Martinez-Ramos, H. Morales, R. Nigh, L. Soto-Pinto, M. Van Breugel, and M. Wishnie 2008. Integrating agricultural landscapes with biodiversity conservation in the Mesoamerican hotspot. Conserv. Biol. 22: 8-15.
59. Herz, H., W. Beyschlag, and B. Hölldobler 2007. Herbivory rate of leaf-cutting ants in a tropical moist forest in Panama at the population and ecosystem scales. Biotropica 39: 482-488.
60. Hölldobler, B., and E. O. Wilson 2011. The leafcutter ants: civilization by instinct. W.W. Norton and Company Inc., London, U.K.
61. Horvitz, C. C. 1981. Analysis of how ant behaviors affect germination in a tropical myrmecochore Calathea microcephala (P. and E.) Koernicke (Marantaceae): microsite selection and aril removal by neotropical ants, Odontomachus, Pachycondyla, and Solenopsis (Formicidae). Oecologia 51: 47-52.
62. Howard, J. J. 1988. Leaf-cutting ant diet selection: relative influence of leaf-chemistry and physical features. Ecology 69: 250-260.
63. Hudson, T. M., B. Turner, H. Herz, and J. S. Robinson 2009. Temporal patterns of nutrient availability around nests of leaf-cutting ants (Atta colombica) in secondary moist tropical forest. Soil Biol. Biochem. 41: 1088-1093.
64. Hull-Sanders, H. M., and J. J. Howard 2003. Impact of Atta colombica colonies on understory vegetation and light availability in a neotropical forest. Biotropica 35: 441-445.
65. Huntly, N. 1991. Herbivores and the dynamics of communities and ecosystems. Annu. Rev. Ecol. Syst. 22: 477-503.
66. Jones, C. G., J. H. Lawton, and M. Shachak 1994. Organisms as ecosystem engineers. Oikos 69: 373-386.
67. Jonkman, J. 1978. Nests of the leaf-cutting ant Atta vollenweideri as accelerators of succession in pastures. Zeitschr. Angew. Entomol. 86: 25-34.
68. Koptur, S., C. L. Smith, and J. H. Lawton 1996. Effects of artificial defoliation on reproductive allocation in the common vetch, Vicia sativa (Fabaceae: Papilionoidae). Am. J. Bot. 83: 886-889.
69. Kost, C., E. Gama de Oliveira, T. Knoch, and R. Wirth 2005. Temporal and spatial patterns, plasticity, and ontogeny of foraging trails in leaf-cutting ants. J. Trop. Ecol. 21: 677-688.
70. Kost, C., M. Tremmel, and R. Wirth 2011. Do leaf cutting ants cut undetected? Testing the effect of ant-induced plant defences on foraging decisions in Atta colombica. PLoS ONE 6: e22340.
71. Landsberg, J., and C. Ohmart 1989. Levels of insect defoliation in forests: patterns and concepts. Trends Ecol. Evol. 4: 96-100.
72. Laurance, W. F., H. E. M. Nascimento, S. G. Laurance, A. C. Andrade, P. M. Fearnside, J. E. L. Ribeiro, and R. L. Capretz 2006. Rain forest fragmentation and the proliferation of successional trees. Ecology 87: 469-482.
73. Leal, I. R., and P. S. Oliveira 1998. Interactions between fungus-growing ants (Attini), fruits and seeds in cerrado vegetation in Southeast Brazil. Biotropica 30: 170-178.
74. Leal, I. R., W. Rainer, and M. Tabarelli 2012. Formigas cortadeiras e a ambiguidade de suas relações com plantas. In K. Del-Claro, and H. M. Torezan-Silingardi (Eds.). Ecologia das interações plantas-animais: uma abordagem ecológico-evolutiva, pp. 215-239. Technical Books Editora, Rio de Janeiro, RJ, Brazil.
75. Loiselle, B. A. 1990. Seeds in droppings of tropical fruit-eating birds: importance of considering seed composition. Oecologia 82: 494-500.
76. Maron, J. L., and E. Crone 2006. Herbivory: effects on plant abundance, distribution and population growth. Proc. Roy. Soc. B-Biol. Sci. 273: 2575-2584.
77. Marquis, R. J. 1984. Leaf herbivory decreases fitness of a tropical plant. Science 226: 537-539.
78. Marquis, R. J., E. A. Newell, and A. C. Villegas 1997. Non-structural carbohydrate accumulation and use in an understorey rain-forest shrub and relevance for the impact of leaf herbivory. Funct. Ecol. 11: 636-643.
79. Melo, F. P. L., V. Arroyo-Rodríguez, L. Fahrig, M. Martínez-Ramos, and M. Tabarelli 2013. On the hope for biodiversity-friendly tropical landscapes. Trends Ecol. Evol. 28: 462-468.
80. Meyer, S. 2008. Ecosystem engineering in fragmented forests: Edge-mediated hyper-abundance of leaf-cutting ants and resulting impacts on forest structure, microclimate, and regeneration. PhD thesis University of Kaiserslautern, Germany.
81. Meyer, S. T., I. R. Leal, M. Tabarelli, and R. Wirth 2011a. Ecosystem engineering by leaf-cutting ants: nests of Atta cephalotes drastically alter forest structure and microclimate. Ecol. Entomol. 36: 14-24.
82. Meyer, S. T., I. R. Leal, M. Tabarelli, and R. Wirth 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 Ecol. 36: 779-790.
83. Meyer, S. T., I. R. Leal, and R. Wirth 2009. Persisting hyper-abundance of keystone herbivores (Atta spp.) at the edge of an old Brazilian Atlantic Forest fragment. Biotropica 41: 711-716.
84. Meyer, S. T., M. Neubauer, E. J. Sayer, I. R. Leal, M. Tabarelli, and R. Wirth 2013. Leaf-cutting ants as ecosystem engineers: topsoil and litter perturbations around Atta cephalotes nests reduce nutrient availability. Ecol. Entomol. 38: 497-504.
85. Meyer, S. T., F. Roces, and R. Wirth 2006. Selecting the drought stressed: effects of plant stress on intraspecific and within plant herbivory patterns of the leaf-cutting ant Atta colombica. Funct. Ecol. 20: 973-984.
86. Montoya-Lerma, J., C. Giraldo-Echeverri, I. Armbrecht, A. Farji-Brener, and Z. Calle 2012. Leaf-cutting ants revisited: Towards rational management and control. Int. J. Pest Manage. 58: 225-247.
87. Moreira, A., L. C. Forti, A. P. Andrade, M. A. Boaretto, and J. F. S. Lopes 2004b. Nest architecture of Atta laevigata (F. Smith 1858) (Hymenoptera: Formicidae). Stud. Neotrop. Fauna E. 39: 109-116.
88. Moreira, A. A., L. C. Forti, M. A. C. Boaretto, A. P. P. Andrade, J. F. S. Lopes, and V. M. Ramos 2004a. External and internal structure of Atta bisphaerica Forel (Hymenoptera: Formicidae) nests. J. Appl. Entomol. 128: 204-211.
89. Moser, J. C. 2006. Complete excavation and mapping of a Texas leafcutting ant nest. Ann. Entomol. Soc. Am. 99: 891-897.
90. Moutinho, P. R., D. C. Nepstad, K. Araújo, and C. Uhl 1993. Formigas e floresta: estudo para a recuperação de áreas de pastagem. Ciência Hoje 15: 59-60.
91. Moutinho, P. R., D. C. Nepstad, and E. A. Davdson 2003. Influence of leaf-cutting ant nests on secondary forest growth and soil properties in Amazonia. Ecology 84: 1265-1276.
92. Mueller, U. G., S. A. Rehner, and T. R. Schultz 1998. The evolution of agriculture in ants. Science 281: 2034-2038.
93. Mundim, F. M., E. Bruna, E. Vieira-Neto, and H. L. Vasconcelos 2012. Attack frequency and the tolerance to herbivory of neotropical savanna trees. Oecologia 168: 405-414.
94. Mundim, F. M., A. N. Costa, and H. L. Vasconcelos 2008. Leaf nutrient content and host plant selection by leaf-cutter ants, Atta laevigata, in a Neotropical savanna. Entomol. Exp. App. 130: 47-54.
95. Nichols-Orians, C. M., and J. C. Schultz 1989. Leaf-toughness affects leaf harvesting by the leaf-cutter ant, Atta cephalotes (L.) (Hymenoptera:Formicidae). Biotropica 21: 80-83.
96. Nichols-Orians, C. M., and J. C. Schultz 1990. Interactions among leaf toughness, chemistry, and harvesting by attine ants. Ecol. Entomol. 15: 311-320.
97. Oliveira, M. A., M. T. Della-Lucia, and N. Anjos 1998. Occurrence and nest density of leaf-cutting ants under eucalypt plantations in southern Bahia. Rev. Bras. Entomol. 42: 17-21.
98. Oliveira, P. S., M. Galetti, F. Pedroni, and L. P. C. Morellato 1995. Seed cleaning by Mycocepurus goeldi ants (Attini) facilitates germination in Hymenaea courbaril (Caesalpiniaceae). Biotropica 27: 518-522.
99. Passos, L., and P. S. Oliveira 2003. Interactions between ants, fruits, and seeds in a restinga forest in south-eastern Brazil. J. Trop. Ecol. 19: 261-270.
100. Pinto-Tomás, A. A., M. A. Anderson, G. Suen, D. M. Stevenson, F. S. T. Chu, W. W. Cleland, P. J. Weimer, and C. R. Currie 2009. Symbiotic nitrogen fixation in the fungus gardens of leaf-cutter ants. Science 326: 1120-1123.
101. Pizo, M. A., P. R. Guimarães, Jr, and P. S. Oliveira 2005. Seed removal by ants from faeces produced by different vertebrate species. Écoscience 12: 136-140.
102. Rao, M., J. Terborgh, and P. Nunez 2001. Increased herbivory in forest isolates: implications for plant community structure and composition. Conserv. Biol. 15: 624-633.
103. Ribeiro Neto, J. D., B. X. Pinho, S. T. Meyer, R. Wirth, and I. R. Leal 2012. Drought stress drives intraspecific choice of food plants by Atta leaf-cutting ants. Entomol. Exp. App. 144: 209-215.
104. Rockwood, L. L. 1976. Plant selection and foraging patterns in two species of leaf-cutting ants (Atta). Ecology 57: 48-61.
105. Rojas, P. 1989. Entomofauna associated with the detritus of Atta mexicana F. Smith (Hymenoptera: Formicidae) in an arid zone of central Mexico. Acta Zool. Mex. Nueva Serie 33: 1-52.
106. Santos, B. A., C. A. Peres, M. A. Oliveira, A. S. Grillo, C. P. Alves-Costa, and M. Tabarelli 2008. Drastic erosion in functional attributes of tree assemblages in Atlantic forest fragments of northeastern Brazil. Biol. Conserv. 141: 249-260.
107. Saverschek, N., H. Herz, M. Wagner, and F. Roces 2010. Avoiding plants unsuitable for the symbiotic fungus: learning and long-term memory in leaf-cutting ants. Anim. Behav. 79: 689-698.
108. Schoenian, I., M. Spiteller, M. Ghaste, R. Wirth, H. Herz, and D. Spiteller 2011. Chemical basis of the synergism and antagonism in microbial communities in the nests of leaf-cutting ants. Proc. Natl Acad. Sci. USA 108: 1955-1960.
109. Schowalter, T. D., W. W. Hargrove, and D. A. Crossley, Jr. 1986. Herbivory in forested ecosystems. Annu. Rev. Entomol. 31: 177-196.
110. Schultz, T. R., and S. G. Brady 2008. Major evolutionary transitions in ant agriculture. Proc. Natl Acad. Sci. USA 105: 5435-5440.
111. Silva, P. S. D., A. G. D. Bieber, T. A. Knoch, M. Tabarelli, I. R. Leal, and R. Wirth 2013. Foraging in highly dynamic environments: leaf-cutting ants adjust foraging trail networks to pioneer plant availability. Entomol. Exp. App. 147: 110-119.
112. Silva, P. S. D., A. G. D. Bieber, I. R. Leal, R. Wirth, and M. Tabarelli 2009. Decreasing abundance of leaf-cutting ants across a chronosequence of advancing Atlantic forest regeneration. J. Trop. Ecol. 25: 223-227.
113. Silva, P. S. D., I. R. Leal, R. Wirth, P. F. L. Melo, and M. Tabarelli 2012. Leaf-cutting ants alter seedling assemblages across second-growth stands of Brazilian Atlantic forest. J. Trop. Ecol. 28: 361-368.
114. Silva, P. S. D., I. R. Leal, R. Wirth, and M. Tabarelli 2007. Harvesting of Protium heptaphyllum (Aubl.) March. seeds (Burseraceae) by the leaf-cutting ant Atta sexdens L. promotes seed aggregation and seedling mortality. Rev. Bras. Bot. 30: 553-560.
115. Sosa, B., and A. Brazeiro 2010. Positive ecosystem engineering effects of the ant Atta vollenweideri on the shrub Grabowskia duplicate. J. Veg. Sci. 21: 597-605.
116. Sosa, B., and A. Brazeiro 2012. Local and landscape-scale effects of an ant nest construction in an open dry forest of Uruguay. Ecol. Entomol. 37: 252-255.
117. Sousa-Souto, L., J. H. Schoereder, C. E. G. R. Schaefer, and W. L. Silva 2007. Leaf-cutting ants, seasonal burning and nutrient distribution in Cerrado vegetation. Austral Ecol. 32: 758-765.
118. Sousa-Souto, L., J. H. Schoereder, C. E. G. R. Schaefer, and W. L. Silva 2008. Ant nests and soil nutrient availability: the negative impact of fire. J. Trop. Ecol. 24: 639-646.
119. Tabarelli, M., A. V. Aguiar, L. C. Girão, C. A. Peres, and A. V. Lopes 2010. Effects of pioneer tree species hyperabundance on forest fragments in Northeastern Brazil. Conserv. Biol. 24: 1654-1663.
120. Tabarelli, M., A. V. Lopes, and C. A. Peres 2008. Edge-effects drive tropical forest fragments towards an early-successional system. Biotropica 40: 657-661.
121. Tabarelli, M., F. P. L. Melo, and C. A. Peres 2012a. The 'few winners and many losers' paradigm revisited: emerging prospects for tropical forest biodiversity. Biol. Conserv. 155: 136-140.
122. Tabarelli, M., J. M. C. Silva, and C. Gascon 2004. Forest fragmentation, synergisms and the impoverishment of neotropical forests. Biodivers. Conserv. 13: 1419-1425.
123. Teixeira, M. C., J. H. Schroeder, and A. J. Mayhé-Nunes 2003. Geographic distribution of Atta robusta Borgmeier (Hymenoptera: Formicidae). Neotrop. Entomol. 32: 719-721.
124. Terborgh, J., L. Lopez, V. P. Nunez, M. Rao, G. Shahabuddin, G. Orihuela, M. Riveros, R. Ascanio, G. H. Adler, T. D. Lambert, and L. Balbas 2001. Ecological meltdown in predator-free forest fragments. Science 294: 1923-1926.
125. Trumble, J. T., D. M. Kolodny-Hirsch, and I. P. Ting 1993. Plant compensatory for arthropod herbivory. Ann. Rev. Entomol. 38: 93-119.
126. Tscharntke, T., I. Steffan-Dewenter, A. Kruess, and C. Thies 2002. Characteristics of insect populations on habitat fragments: A mini review. Ecol. Res. 17: 229-239.
127. Tylianakis, J. M., R. K. Didham, J. Bascompte, and D. A. Wardle 2008. Global change and species interactions in terrestrial ecosystems. Ecol. Lett. 11: 1351-1363.
128. Urbas, P., M. V. Araújo, Jr., I. R. Leal, and R. Wirth 2007. Cutting more from cut forests: Edge effects on foraging and herbivory of leaf-cutting ants in Brazil. Biotropica 39: 489-495.
129. Valladares, G., L. Cagnolo, and A. Salvo 2012. Forest fragmentation leads to food web contraction. Oikos 121: 299-305.
130. Vasconcelos, H. L. 1988. Distribution of Atta (Hymenoptera - Formicidae) in a terra-firme rain forest of central Amazonia: density, species composition, and preliminary results on effects of forest fragmentation. Acta Amaz. 18: 309-315.
131. Vasconcelos, H. L. 1990. Habitat selection by the queens of the leaf-cutting ant Atta sexdens L. in Brazil. J. Trop. Ecol. 6: 249-252.
132. Vasconcelos, H. L., and J. M. Cherrett 1995. Changes in leaf-cutting ant populations (Formicidae, Attini) after the clearing of mature forest in Brazilian Amazonia. Stud. Neotrop. Fauna E. 30: 107-113.
133. Vasconcelos, H. L., and J. M. Cherrett 1996. The effect of wilting on the selection of leaves by the leaf-cutting ant Atta laevigata. Entomol. Exp. App. 78: 215-220.
134. Vasconcelos, H. L., and H. G. Fowler 1990. Foraging and fungal substrate selection by leaf-cutting ants. In R. K. Vander Meer, K. Jaffe, and A. Cedeno (Eds.). Applied myrmecology - a world perspective, pp 411-419. Westview Press, Boulder, CO, U.S.A.
135. Vasconcelos, H. L., E. H. M. Vieira-Neto, F. M. Mundim, and E. M. Bruna 2006. Roads alter the colonization dynamics of a keystone herbivore in neotropical savannas. Biotropica 38: 661-666.
136. Verchot, L. V., P. R. Moutinho, and E. A. Davidson 2003. Leaf-cutting and (Atta sexdens) and nutrient cycling: Deep soil inorganic nitrogen stocks, mineralization and nitrification in Eastern Amazonia. Soil Biol. Biochem. 35: 1219-1222.
137. Vieira-Neto, E. H. M., and H. L. Vasconcelos 2010. Developmental changes in factors limiting colony survival and growth of the leaf-cutter ant Atta laevigata. Ecography 33: 538-544.
138. Weber, N. A. 1966. Fungus growing ants. Science 153: 587-604.
139. Weber, N. A. 1972. Gardening ants: the Attines. The American Philosophical Society, Philadelphia, U.S.A.
140. Weisser, W. W., and E. Siemann 2004. The various effects of insects on ecosystem functioning. Ecological Studies 173, Springer-Verlag, Berlin, Germany.
141. Wirth, R., W. Beyschlag, H. Herz, R. J. Ryel, and B. Hölldobler 2003. Herbivory of leaf-cutter ants: a case study of Atta colombica in the tropical rainforest of Panama. Ecological Studies 164, Springer-Verlag, Berlin, Germany.
142. Wirth, R., I. R. Leal, and M. Tabarelli 2008. Plant-herbivore interactions at the forest edge. Progr. Bot. 69: 423-448.
143. Wirth, R., S. T. Meyer, W. R. Almeida, M. V. Araujo, Jr., V. S. Barbosa, and I. R. Leal 2007. Increasing densities of leaf-cutting ants (Atta spp.) with proximity to the edge in a Brazilian Atlantic forest. J. Trop. Ecol. 23: 501-505.
144. Wright, S. J. 2005. Tropical forests in a changing environment. Trends Ecol. Evol. 20: 553-560.