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Naturwissenschaften

, Volume 91, Issue 12, pp 557–570 | Cite as

Ant–plant–herbivore interactions in the neotropical cerrado savanna

  • Paulo S. Oliveira
  • André V. L. Freitas
Review

Abstract

The Brazilian cerrado savanna covers nearly 2 million km2 and has a high incidence on foliage of various liquid food sources such as extrafloral nectar and insect exudates. These liquid rewards generate intense ant activity on cerrado foliage, making ant–plant–herbivore interactions especially prevalent in this biome. We present data on the distribution and abundance of extrafloral nectaries in the woody flora of cerrado communities and in the flora of other habitats worldwide, and stress the relevance of liquid food sources (including hemipteran honeydew) for the ant fauna. Consumption by ants of plant and insect exudates significantly affects the activity of the associated herbivores of cerrado plant species, with varying impacts on the reproductive output of the plants. Experiments with an ant–plant–butterfly system unequivocally demonstrate that the behavior of both immature and adult lepidopterans is closely related to the use of a risky host plant, where intensive visitation by ants can have a severe impact on caterpillar survival. We discuss recent evidence suggesting that the occurrence of liquid rewards on leaves plays a key role in mediating the foraging ecology of foliage-dwelling ants, and that facultative ant–plant mutualisms are important in structuring the community of canopy arthropods. Ant-mediated effects on cerrado herbivore communities can be revealed by experiments performed on wide spatial scales, including many environmental factors such as soil fertility and vegetation structure. We also present some research questions that could be rewarding to investigate in this major neotropical savanna.

Keywords

Extrafloral Nectar Liquid Reward Herbivore Deterrence Cerrado Savanna Caryocar Brasiliense 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

We are grateful to Bert Hölldobler for the invitation to write this review. R. Cogni, H.P. Dutra, A. Moraes, and K.S. Brown provided valuable comments on the manuscript. The final version was considerably improved by comments from two anonymous referees. R. Raimundo and A. Midori helped with the illustrations. We thank the Instituto Florestal de São Paulo for allowing us to work in its cerrado reserves. Our studies in cerrado were supported by grants from the Brazilian Research Council (CNPq), the Universidade Estadual de Campinas (FAEP), and the Fundação de Amparo à Pesquisa do Estado de São Paulo (Biota #FAPESP).

References

  1. Andersen AN (1991a) Sampling communities of ground-foraging ants: pitfall catches compared with quadrat counts in an Australian tropical savanna. Aust J Ecol 16:273–279Google Scholar
  2. Andersen AN (1991b) Responses of ground-foraging ant communities to three experimental fire regimes in a savanna forest of tropical Australia. Biotropica 23:575–585Google Scholar
  3. Andersen AN, Patel AD (1994) Meat ants as dominant members of Australian ant communities: an experimental test of their influence on the foraging success and forager abundance of other species. Oecologia 98:15–24CrossRefGoogle Scholar
  4. Araújo LM, Lara ACF, Fernández GW (1995) Utilization of Apion sp. (Coleoptera: Apionidae) galls by an ant community in southeast Brazil. Trop Zool 8:319–324Google Scholar
  5. Atsatt PR (1981) Lycaenid butterflies and ants: selection for enemy-free space. Am Nat 118:638–654CrossRefGoogle Scholar
  6. Barbosa P, Benrey B (1998) The influence of plants on insect parasitoids: implications for conservation biological control. In: Barbosa P (ed) Conservation biological control. Academic Press, San Diego, Calif., pp 55–82Google Scholar
  7. Barbosa P, Wratten SD (1998) Influence of plants on invertebrate predators: implications to conservation biological control. In: Barbosa P (ed) Conservation biological control. Academic Press, San Diego, Calif., pp 83–100Google Scholar
  8. Barton AM (1986) Spatial variation in the effect of ants on an extrafloral nectary plant. Ecology 67:495–504Google Scholar
  9. Beattie AJ (1985) The evolutionary ecology of ant–plant mutualisms. Cambridge University Press, CambridgeGoogle Scholar
  10. Beattie AJ, Hughes L (2002) Ant–plant interactions. In: Herrera CM, Pellmyr O (eds) Plant–animal interactions: an evolutionary approach. Blackwell Science, Oxford, pp 211–235Google Scholar
  11. Becerra JX, Venable DL (1989) Extrafloral nectaries: a defense against ant–Homoptera mutualism? Oikos 55:276–280Google Scholar
  12. Benson WW, Brown KS, Gilbert, LE (1976) Coevolution of plants and herbivores: passion flower butterflies. Evolution 29:659–680Google Scholar
  13. Bentley BL (1976) Plants bearing extrafloral nectaries and the associated ant community: interhabitat differences in the reduction of herbivore damage. Ecology 57:815–820Google Scholar
  14. Bentley BL (1977) Extrafloral nectaries and protection by pugnacious bodyguards. Annu Rev Ecol Syst 8:407–427CrossRefGoogle Scholar
  15. Bizerril MXA, Vieira EM (2002) Azteca ants as antiherbivore agents of Tococa formicaria (Melastomataceae) in Brazilian cerrado. Stud Neotrop Fauna Environ 37:145–149CrossRefGoogle Scholar
  16. Blüthgen N, Reifenrath K (2003) Extrafloral nectaries in an Australian rainforest: structure and distribution. Aust J Bot 51:515–527CrossRefGoogle Scholar
  17. Blüthgen N, Verhaagh M, Goitía W, Jaffé K, Morawetz W, Barthlott W (2000) How plants shape the ant community in the Amazonian rainforest canopy: the key role of extrafloral nectaries and homopteran honeydew. Oecologia 125:229–240CrossRefGoogle Scholar
  18. Bronstein JL (1998) The contribution of ant–plant protection studies to our understanding of mutualism. Biotropica 30:150–161Google Scholar
  19. Bronstein JL, Barbosa P (2002) Multitrophic/multispecies mutualistic interactions: the role of non-mutualists in shaping and mediating mutualisms. In: Tscharntke T, Hawkins BA (eds) Multitrophic level interactions. Cambridge University Press, Cambridge, pp 44–66Google Scholar
  20. Brown KS Jr (1981) The biology of Heliconius and related genera. Annu Rev Entomol 26:427–456CrossRefGoogle Scholar
  21. Buckley R (1982) Ant–plant interactions in Australia. Junk, The HagueGoogle Scholar
  22. Buckley R. (1987) Interactions involving plants, Homoptera, and ants. Annu Rev Ecol Syst 18:111–138CrossRefGoogle Scholar
  23. Carroll CR (1979) A comparative study of two ant faunas: the stem-nesting ant communities of Liberia, West Africa, and Costa Rica, Central America. Am Nat 113:551–561CrossRefGoogle Scholar
  24. Carroll CR, Janzen DH (1973) Ecology of foraging by ants. Annu Rev Ecol Syst 4:231–257CrossRefGoogle Scholar
  25. Cogni R, Freitas AVL, Oliveira PS (2003) Interhabitat differences in ant activity on plant foliage: ants at extrafloral nectarines of Hibiscus pernambucensis in sandy and mangrove forests. Entomol Exp Appl 107:125–131Google Scholar
  26. Coley PD, Aide TM (1991) Comparison of herbivory and plant defenses in temperate and tropical broad-leaved forests. In: Price PW, Lewinsohn TM, Fernandes GW, Benson WW (eds) Plant–animal interactions: evolutionary ecology in tropical and temperate regions. Wiley, New York, pp 25–49Google Scholar
  27. Costa FMCB, Oliveira-Filho AT, Oliveira PS (1992) The role of extrafloral nectaries in Qualea grandiflora (Vochysiaceae) in limiting herbivory: an experiment of ant protection in cerrado vegetation. Ecol Entomol 17:362–365Google Scholar
  28. Cuautle M, Rico-Gray V (2003) The effect of wasps and ants on the reproductive success of the extrafloral nectaried plant Turnera ulmifolia (Turneraceae). Funct Ecol 17:417–423CrossRefGoogle Scholar
  29. Cushman JH (1991) Host–plant mediation of insect mutualisms: variable outcomes in herbivore-ant interactions. Oikos 61:138–144Google Scholar
  30. Dansa CVA, Rocha CFD (1992) An ant–membracid–plant interaction in a cerrado area of Brazil. J Trop Ecol 8:339–348Google Scholar
  31. Davidson DW (1997) The role of resource imbalances in the evolutionary ecology of tropical arboreal ants. Biol J Linn Soc 61:153–181CrossRefGoogle Scholar
  32. Davidson DW, McKey D (1993) The evolutionary ecology of symbiotic ant–plant relationships. J Hym Res 2:13–83Google Scholar
  33. Davidson DW, Cook SC, Snelling RR, Chua TH (2003) Explaining the abundance of ants in lowland tropical rainforest canopies. Science 300:969–972CrossRefPubMedGoogle Scholar
  34. Dejean A, McKey D, Gibernau M, Belin M (2000) The arboreal ant mosaic in a Cameroonian rainforest (Hymenoptera: Formicidae). Sociobiology 35:403–423Google Scholar
  35. De la Fuente MAS, Marquis RJ (1999) The role of ant-tended extrafloral nectaries in the protection and benefit of a neotropical rainforest tree. Oecologia 118:192–202CrossRefGoogle Scholar
  36. Del-Claro K, Mound LA (1996) Phenology and description of a new species of Liothrips (Thysanoptera: Phlaeothripidae) from Didymopanax (Araliaceae) in Brazilian cerrado. Rev Biol Trop 44:193–197Google Scholar
  37. Del-Claro K, Oliveira PS (1993) Ant–Homoptera interaction: do alternative sugar sources distract tending ants? Oikos 68:202–206Google Scholar
  38. Del-Claro K, Oliveira PS (1996) Honeydew flicking by treehoppers provides cues to potential tending ants. Anim Behav 51:1071–1075CrossRefGoogle Scholar
  39. Del-Claro K, Oliveira PS (1999) Ant–Homoptera interactions in neotropical savanna: the honeydew-producing treehopper Guayaquila xiphias (Membracidae) and its associated ant fauna on Didymopanax vinosum (Araliaceae). Biotropica 31:135–144Google Scholar
  40. Del-Claro K, Oliveira PS (2000) Conditional outcomes in a neotropical treehopper-ant association: temporal and species-specific effects. Oecologia 124:156–165CrossRefGoogle Scholar
  41. Del-Claro K, Berto V, Réu W (1996) Effect of herbivore deterrence by ants on the fruit set of an extrafloral nectary plant, Qualea multiflora (Vochysiaceae). J Trop Ecol 12:887–892Google Scholar
  42. DeVries PJ (1987) The butterflies of Costa Rica and their natural history. Princeton University Press, Princeton, N.J.Google Scholar
  43. DeVries PJ (1991) Mutualism between Thisbe irenea butterflies and ants, and the role of ant ecology in the evolution of larval–ant associations. Biol J Linn Soc 43:179–195Google Scholar
  44. Díaz-Castelazo C, Rico-Gray V, Oliveira PS, Cuautle M (2004) Extrafloral nectary-mediated ant–plant interactions in the coastal vegetation of Veracruz, Mexico: richness, occurrence, seasonality and ant foraging patterns. Ecoscience 11Google Scholar
  45. Diniz IR, Morais HC (1997) Lepidopteran caterpillar fauna of cerrado host plants. Biodivers Conserv 6:817–836CrossRefGoogle Scholar
  46. Dyer LA, Coley PD (2002) Tritrophic interactions in tropical versus temperate communities. In: Tscharntke T, Hawkins BA (eds) Multitrophic level interactions. Cambridge University Press, Cambridge, pp. 67–88Google Scholar
  47. Fernandes GW, Boecklen WJ, Martins RP, Castro AG (1988) Ants associated with a coleopterous leaf-bud gall on Xylopia aromatica (Annonaceae). Proc Entomol Soc Wash 91:81–87Google Scholar
  48. Ferreira SO (1994) Nectários extraflorais de Ouratea spectabilis (Ochnaceae) e a comunidade de formigas associadas: um estudo em vegetação de cerrado, no sudeste do Brasil. Master’s thesis, Universidade Estadual de Campinas, Campinas, BrasilGoogle Scholar
  49. Fiala B (1990) Extrafloral nectaries versus ant–Homoptera mutualism: a comment on Becerra and Venable. Oikos 59:281–282Google Scholar
  50. Fiala B, Linsenmaier KE (1995) Distribution and abundance of plants with extrafloral nectarines in the woody floral of a lowland primary forest in Malaysia. Biodivers Conserv 4:165–182CrossRefGoogle Scholar
  51. Fittkau EJ, Klinge H (1973) On biomass and trophic structure of the central Amazonian rain forest ecosystem. Biotropica 5:2–14Google Scholar
  52. Fonseca CR, Ganade G (1996) Asymmetries, compartments and null interactions in an Amazonian ant–plant community. J Anim Ecol 65:339–347Google Scholar
  53. Franco AC (2002) Ecophysiology of woody plants. In: Oliveira PS, Marquis RJ (eds) The cerrados of Brazil: ecology and natural history of a neotropical savanna. Columbia University Press, New York, pp 178–197Google Scholar
  54. Freitas AVL, Oliveira PS (1992) Biology and behavior of Eunica bechina (Lepidoptera: Nymphalidae) with special reference to larval defense against ant predation. J Res Lepid 31:1–11Google Scholar
  55. Freitas AVL, Oliveira PS (1996) Ants as selective agents on herbivore biology: effects on the behaviour of a non-myrmecophilous butterfly. J Anim Ecol 65:205–210Google Scholar
  56. Gilbert LE (1980) Food web organization and the conservation of neotropical diversity. In: Soulé ME, Wilcox BA (eds) Conservation biology: an evolutionary-ecological perspective. Sinauer, Sunderland, Mass., pp 11–33Google Scholar
  57. Goebel R, Fernandez E, Begue JM, Alauzet C (1999) Predation by Pheidole megacephala (Fabricius) (Hym: Formicidae) on eggs of the sugarcane stem borer Chilo sacchariphagus (Bojer) (Lep.: Pyralidae) in Reunion Island. Ann Soc Entomol Fr 35:440–442Google Scholar
  58. Gottsberger G, Silberbauer-Gottsberger I (1983) Dispersal and distribution in the cerrado vegetation of Brazil. Sonderbd Naturwiss Ver Hamburg 7:315–353Google Scholar
  59. Heads PA, Lawton JH (1985) Bracken, ants and extrafloral nectaries. III. How insect herbivores avoid predation. Ecol Entomol 10:29–42Google Scholar
  60. Heil M, McKey D (2003) Protective ant–plant interactions as model systems in ecological and evolutionary research. Annu Rev Ecol Evol Syst 34:425–453CrossRefGoogle Scholar
  61. Hölldobler B, Wilson EO (1990) The ants. Harvard University Press, Cambridge, Mass.Google Scholar
  62. Huxley CR, Cutler DF (eds) (1991) Ant–plant interactions. Oxford University Press, OxfordGoogle Scholar
  63. Inouye DW, Taylor OR (1979) A temperate region plant–ant–seed predator system: consequences of extrafloral nectar secretion by Helianthella quinquinervis. Ecology 60:1–7Google Scholar
  64. Janzen DH (1967) Interaction of the bull’s horn acacia ( Acacia cornigera L.) with an ant inhabitant ( Pseudomyrmex ferruginea F. Smith) in Eastern Mexico. Kans Univ Sci Bull 47:315–558Google Scholar
  65. Jeanne RL (1979) A latitudinal gradient in rates of ant predation. Ecology 60:1211–1224Google Scholar
  66. Kaspari M (2000) A primer on ant ecology. In: Agosti D, Majer JD, Alonso LE, Schultz TR (eds) Ants: standard methods for measuring and monitoring biodiversity. Smithsonian Institution Press, Washington, D.C., pp 9–24Google Scholar
  67. Keeler KH (1979a) Distribution of extrafloral nectaries and ants at two elevations in Jamaica. Biotropica 11:152–154Google Scholar
  68. Keeler KH (1979b) Distribution of plants with extrafloral nectaries in a temperate flora (Nebraska). Prairie Nat 11:33–37Google Scholar
  69. Keeler KH (1980) Distribution of plants with extrafloral nectaries in temperate communities. Am Midl Nat 104:274–280Google Scholar
  70. Keeler KH (1981a) Cover of plants with extrafloral nectaries at four northern California sites. Madroño 28:26–29Google Scholar
  71. Keeler KH (1981b) A model of selection for facultative nonsymbiotic mutualism. Am Nat 118:488–498CrossRefGoogle Scholar
  72. Keeler KH (1985) Extrafloral nectaries on plants in communities without ants: Hawaii. Oikos 44:407–414Google Scholar
  73. Kelly CA (1986) Extrafloral nectaries: ants, herbivores and fecundity in Cassia fasciculata. Oecologia 69:600–605CrossRefGoogle Scholar
  74. Kluge RL (1991) Biological control of triffid weed, Chromolaena odorata (Asteraceae), in South Africa. Agric Ecosyst Environ 37:193–197CrossRefGoogle Scholar
  75. Koptur S (1984) Experimental evidence for defense of Inga (Mimosoideae) saplings by ants. Ecology 65:1787–1793Google Scholar
  76. Koptur S (1992a) Extrafloral nectary-mediated interactions between insects and plants. In: Bernays E (ed) Insect–plant interactions, vol 4. CRC, Boca Raton, Fla., pp 81–129Google Scholar
  77. Koptur S (1992b) Plants with extrafloral nectaries and ants in Everglades habitats. Fla Entomol 75:38–50Google Scholar
  78. Lopes BC (1995) Treehoppers (Homoptera: Membracidae) in southeast Brazil: use of host plants. Rev Bras Zool 12:595–608Google Scholar
  79. Machado G, Freitas, AVL (2001) Larval defence against ant predation in the butterfly Smyrna blomfildia. Ecol Entomol 26:436–439Google Scholar
  80. Majer JD (1990) The abundance and diversity of arboreal ants in northern Australia. Biotropica 22:191–199Google Scholar
  81. Majer JD, Delabie JHC (1994) Comparison of the ant communities of annually inundated and terra firme forests at Trombetas in the Brazilian Amazon. Insectes Soc 41:343–359Google Scholar
  82. Malicky H (1971) New aspects of the association between lycaenid larvae (Lycaenidae) and ants (Formicidae, Hymenoptera). J Lep Soc 24:190–202Google Scholar
  83. Marquis RJ (1992) Selective impact of herbivores. In Fritz RS, Simms EL (eds) Plant resistance to herbivores and pathogens: ecology, evolution, and genetics. University of Chicago Press, Chicago, pp 301–325Google Scholar
  84. Messina FJ (1981) Plant protection as a consequence of an ant–membracid mutualism: interactions on goldenrod ( Solidago sp.). Ecology 62:1433–1440Google Scholar
  85. Morais HC (1980) Estrutura de uma comunidade de formigas arborícolas em vegetação de campo cerrado. Master’s thesis, Universidade Estadual de Campinas, Campinas, BrasilGoogle Scholar
  86. Morais HC, Benson WW (1988) Recolonização de vegetação de cerrado após queimada, por formigas arborícolas. Rev Bras Biol 48:459–466Google Scholar
  87. Morellato LPC, Oliveira PS (1991) Distribution of extrafloral nectaries in different vegetation types of Amazonian Brazil. Flora 185:33–38Google Scholar
  88. Motta PEF, Curi N, Franzmeier DP (2002) Relation of soils and geomorphic surfaces in the Brazilian cerrado. In: Oliveira PS, Marquis RJ (eds) The cerrados of Brazil: ecology and natural history of a neotropical savanna. Columbia University Press, New York, pp 13–32Google Scholar
  89. Oliveira PS (1997) The ecological function of extrafloral nectaries: herbivore deterrence by visiting ants and reproductive output in Caryocar brasiliense (Caryocaraceae). Funct Ecol 11:323–330CrossRefGoogle Scholar
  90. Oliveira PS, Brandão CRF (1991) The ant community associated with extrafloral nectaries in Brazilian cerrados. In: Cutler DF, Huxley CR (eds) Ant–plant interactions. Oxford University Press, Oxford, pp 198–212Google Scholar
  91. Oliveira PS, Del-Claro K (2004) Multitrophic interactions in a neotropical savanna: ant–hemipteran systems, associated insect herbivores, and a host plant. In: Burslem DFRP, Pinard MA, Hartley SE (eds) Biotic interactions in the tropics. Cambridge University Press, Cambridge (in press)Google Scholar
  92. Oliveira PS, Freitas AVL (1991) Hostplant record for Eunica bechina magnipunctata (Nymphalidae) and observations on oviposition sites and immature biology. J Res Lepid 30:140–141Google Scholar
  93. Oliveira PS, Leitão-Filho HF (1987) Extrafloral nectaries: their taxonomic distribution and abundance in the woody flora of cerrado vegetation in Southeast Brazil. Biotropica 19:140–148Google Scholar
  94. Oliveira PS, Marquis RJ (eds) (2002) The cerrados of Brazil: ecology and natural history of a neotropical savanna. Columbia University Press, New YorkGoogle Scholar
  95. Oliveira PS, Oliveira-Filho AT (1991) Distribution of extrafloral nectaries in the woody flora of tropical communities in Western Brazil. In: Price PW, Lewinsohn TM, Fernandes GW, Benson WW (eds) Plant–animal interactions: evolutionary ecology in tropical and temperate regions. Wiley, New York, pp 163–175Google Scholar
  96. Oliveira PS, Pie MR (1998) Interaction between ants and plants bearing extrafloral nectaries in cerrado vegetation. An Soc Entomol Bras 27:161–176Google Scholar
  97. Oliveira PS, Silva AF da, Martins AB (1987) Ant foraging on extrafloral nectaries of Qualea grandiflora (Vochysiaceae) in cerrado vegetation: ants as potential antiherbivore agents. Oecologia 74:228–230CrossRefGoogle Scholar
  98. Oliveira PS, Klitzke C, Vieira E (1995) The ant fauna associated with the extrafloral nectaries of Ouratea hexasperma (Ochnaceae) in an area of cerrado vegetation in Central Brazil. Entomol Mon Mag 131:77–82Google Scholar
  99. Oliveira PS, Rico-Gray V, Díaz-Castelazo C, Castillo-Guevara C (1999) Interaction between ants, extrafloral nectaries, and insect herbivores in neotropical coastal sand dunes: herbivore deterrence by visiting ants increases fruit set in Opuntia stricta (Cactaceae). Funct Ecol 13:623–631CrossRefGoogle Scholar
  100. Oliveira PS, Freitas AVL, Del-Claro K (2002) Ant foraging on plant foliage: contrasting effects on the behavioral ecology of insect herbivores. In: Oliveira PS, Marquis RJ (eds) The cerrados of Brazil: ecology and natural history of a neotropical savanna. Columbia University Press, New York, pp 287–305Google Scholar
  101. Oliveira-Filho AT, Ratter JA (2002) Vegetation physiognomies and woody flora of the cerrado biome. In: Oliveira PS, Marquis RJ (eds) The cerrados of Brazil: ecology and natural history of a neotropical savanna. Columbia University Press, New York, pp 91–120Google Scholar
  102. Pace ML, Cole JJ, Carpenter SR, Kitchell JF (1999) Trophic cascades revealed in diverse ecosystems. Trends Ecol Evol 14:483–488CrossRefPubMedGoogle Scholar
  103. Paiva EAS, Morais HC, Isaias RMS, Rocha DMS, Oliveira PE (2001) Occurrence and structure of extrafloral nectaries in Pterodon pubescens Benth. and Pterodon polygalaeflorus Benth. Pesq Agropec Bras 36:219–224Google Scholar
  104. Pemberton RW (1988) The abundance of plants bearing extrafloral nectaries in Colorado and Mojave desert communities of southern California. Madroño 35:238–246Google Scholar
  105. Pemberton RW (1990) The occurrence of extrafloral nectaries in Korean plants. Korean J Ecol 13:251–266Google Scholar
  106. Pemberton RW (1998) The occurrence and abundance of plants with extrafloral nectaries, the basis for antiherbivore mutualisms, along a latitudinal gradient in Asia. J Biogeogr 25:661–668CrossRefGoogle Scholar
  107. Pierce NE, Elgar MA (1985) The influence of ants on host plant selection by Jalmenus evagora, a myrmecophilous lycaenid butterfly. Behav Ecol Sociobiol 16:209–222CrossRefGoogle Scholar
  108. Pierce NE, Nash DR (1999) The imperial blue: Jalmenus evagoras (Lycaenidae). In: Kitching RL, Sheermeyer E, Jones RE, Pierce NE (eds) The biology of Australian butterflies. CSIRO, Sydney, pp 279–315Google Scholar
  109. Pierce NE, Braby MF, Heath A, Lohman DJ, Mathew J, Rand DB, Travassos MA (2002) The ecology and evolution of ant association in the Lycaenidae (Lepidoptera). Annu Rev Ecol Syst 47:733–771Google Scholar
  110. Price PW, Bouton CE, Gross P, McPheron BA, Thompson JN, Weis AE (1980) Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Annu Rev Ecol Syst 11:41–65CrossRefGoogle Scholar
  111. Rausher MD (1978) Search image for leaf shape in a butterfly. Science 200:1071–1073Google Scholar
  112. Rausher MD (1979) Egg recognition: its advantage to a butterfly. Anim Behav 27:1034–1040Google Scholar
  113. Ribas CR, Schoereder JH (2004) Determining factors of arboreal ant mosaics in cerrado vegetation (Hymenoptera: Formicidae). Sociobiology 44:49–68Google Scholar
  114. Ribas CR, Schoereder JH, Pic M, Soares SM (2003) Tree heterogeneity, resource availability, and larger scale processes regulating arboreal ant species richness. Aust Ecol 28:305–314CrossRefGoogle Scholar
  115. Rico-Gray V (1993) Use of plant-derived food resources by ants in the dry tropical lowlands of coastal Veracruz, Mexico. Biotropica 25:301–315Google Scholar
  116. Rico-Gray V, Thien LB (1983) Ant–mealybug interaction decreases reproductive fitness of Schomburgkia tibicinis (Orchidaceae) in Mexico. J Trop Ecol 5:109–112Google Scholar
  117. Rico-Gray V, Thien LB (1989) Effect of different ant species on the reproductive fitness of Schombrugkia tibicinis (Orchidaceae). Oecologia 81:487–489Google Scholar
  118. Rico-Gray V, Oliveira PS, Parra-Tabla V, Cuautle M, Díaz-Castelazo C (2004) Ant–plant interactions: their seasonal variation and effects on plant fitness. In: Martínez ML, Psuty NP (eds) Coastal dunes: ecology and conservation. Springer, Berlin Heidelberg New York, pp 221–239Google Scholar
  119. Ruhren S, Handel SN (1999) Jumping spiders (Salticidae) enhance the seed production of a plant with extrafloral nectaries. Oecologia 119:227–230CrossRefGoogle Scholar
  120. Salazar BA, Whitman DW (2001) Defensive tactics of caterpillars against predators and parasitoids. In: Ananthakrishnan TN (ed) Insect and plant defense dynamics. Science Publisher, Enfield, UK, pp 161–207Google Scholar
  121. Santos JC, Del-Claro K (2001) Interação entre formigas, herbívoros e nectários extraflorais em Tocoyena formosa (Cham. & Schlechdt.) K. Schum. (Rubiaceae) na vegetação do cerrado. Rev Bras Zoocien 3:77–92Google Scholar
  122. Schemske DW (1980) The evolutionary significance of extrafloral nectar production by Costus woodsonii (Zingiberaceae): an experimental analysis of ant protection. J Ecol 68:959–967Google Scholar
  123. Schupp EW, Feener DH (1991) Phylogeny, lifeform, and habitat dependence of ant-defended plants in a Panamanian forest. In: Cutler DF, Huxley CR (eds) Ant–plant interactions. Oxford University Press, Oxford, pp 175–197Google Scholar
  124. Shapiro AM (1981) The pierid red-egg syndrome. Am Nat 117:276–294CrossRefGoogle Scholar
  125. Smiley JT (1985) Heliconius caterpillar mortality during establishment on plants with and without attending ants. Ecology 66:845–849Google Scholar
  126. Soares SM, Schoereder, JH, DeSouza O (2001) Processes involved in species saturation of ground-dwelling ant communities (Hymenoptera: Formicidae). Aust Ecol 26:187–192CrossRefGoogle Scholar
  127. Sobrinho TG, Schoereder JH, Rodrigues LL, Collevatti RG (2002) Ant visitation (Hymenoptera: Formicidae) to extrafloral nectaries increases seed set and seed viability in the tropical weed Triumfetta semitriloba. Sociobiology 39:353–368Google Scholar
  128. Stephenson AG (1981) Flower and fruit abortion: proximate causes and ultimate functions. Annu Rev Ecol Syst 12:253–279CrossRefGoogle Scholar
  129. Tempel AS (1983) Bracken fern ( Pteridium aquilinum) and nectar-feeding ants: a nonmutualistic interaction. Ecology 64:1411–1422Google Scholar
  130. Thompson JN (1988) Variation in interspecific interactions. Annu Rev Ecol Syst 19:65–87CrossRefGoogle Scholar
  131. Thompson JN (1997) Conserving interaction biodiversity. In: Pickett STA, Ostfeld RS, Shachak M, Likens GE (eds) The ecological basis of conservation: heterogeneity, ecosystems, and biodiversity. Chapman and Hall, New York, pp 285–293Google Scholar
  132. Tilman D (1978) Cherries, ants and tent caterpillars: timing of nectar production in relation to susceptibility of caterpillars to ant predation. Ecology 59:686–692Google Scholar
  133. Tobin JE (1991) A neotropical rainforest canopy, ant community: some ecological considerations. In: Cutler DF, Huxley CR (eds) Ant–plant interactions. Oxford University Press, Oxford, pp 536–538Google Scholar
  134. Tobin JE (1995) Ecology and diversity of tropical forest canopy ants. In: Lowman MD, Nadkarni NM (eds) Forest canopies. Academic Press, San Diego, Calif., pp 129–147Google Scholar
  135. Way MJ (1963) Mutualism between ants and honeydew-producing homoptera. Annu Rev Entomol 8:307–344CrossRefGoogle Scholar
  136. Wilson EO (1987) The arboreal ant fauna of Peruvian Amazon forests: a first assessment. Biotropica 19:245–251Google Scholar
  137. Williams KS, Gilbert LE (1981) Insects as selective agents on plant vegetative morphology: egg mimicry reduces egg laying by butterflies. Science 212:467–469Google Scholar
  138. Willson MF, Price PW (1980) Resource limitation of fruit and seed production in some Asclepias species. Can J Bot 58:2229–2230Google Scholar
  139. Wirth R, Leal IR (2001) Does rainfall affect temporal variability of ant protection in Passiflora coccinea? EcoScience 8:450–453Google Scholar
  140. Wirth R, Herz H, Ryel RJ, Beyschlag W, Hölldobler B (eds) (2003) Herbivory of leaf-cutting ants: a case study of Atta colombica in the tropical rainforest of Panama. Springer, Berlin Heidelberg New YorkGoogle Scholar

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© Springer-Verlag 2004

Authors and Affiliations

  1. 1.Departamento de Zoologia, CP 6109Universidade Estadual de CampinasCampinas SPBrazil

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