PROTECTION MUTUALISM: AN OVERVIEW OF ANT-PLANT INTERACTIONS MEDIATED BY EXTRAFLORAL NECTARIES
DOI:
https://doi.org/10.4257/oeco.2018.2204.05Keywords:
biotic defense, ecological interactions, herbivory, myrmecophilous plants, predatorsAbstract
Ants and plants bearing extrafloral nectaries (EFNs) are among the most abundant interacting organisms in the Neotropics, being considered excellent models for studies of ecological interactions. These mutualisms have been studied for more than 150 years. The first studies on this subject addressed the indirect benefit of the presence of ants on plants, reducing the foliar herbivory in most cases. Recently, the direct and indirect benefits of these interactions for ants and for EFNs-bearing plants survivorship, growth and reproduction, have shown conditionality to spatial and temporal variations. Here, we reviewed how the topic “protection mutualism in ant-plant interactions mediated by EFNs” has been approached more recently. A great number of papers dealing with this theme have been published in the last 30 years and new perspectives have emerged in the last decade. We showed how scientific and academic areas are working to improve the knowledge on protection mutualisms considering ant-plant ecological networks and how they can shape communities. Furthermore, we discuss some aspects related with the EFNs evolutionary hypotheses, the existence of conditionalities in ant-plant protection mutualism mediated by EFNs, and we provide some perspectives to inspire new studies that will help in the understanding of these fascinating ecological interactions.
References
Agosti, D., & Johnson, N. F. 2003. La nueva taxonomía de hormigas. In: F. Fernández (Ed.), Introducción a las hormigas de la región Neotropical. pp. 45–48. Bogotá D.C: Instituto Humboldt.
Agrawal, A. A. 1998. Induced responses to herbivory and increased plant performance. Science, 279(5354), 1201–1202. DOI: 10.1126/science.279.5354.1201
Agrawal, A. A., & Rutter, M. T. 1998. Dynamic anti-herbivore defense in ant-plants: the role of induced responses. Oikos, 83(2), 227–236. DOI: 10.2307/3546834
Aguirre, A., Coates, R., Cumplido-Barragán, G., Campos-Villanueva, A., & Díaz-Castelazo, C. 2013. Morphological characterization of extrafloral nectaries and associated ants in tropical vegetation of Los Tuxtlas, Mexico. Flora-Morphology, Distribution, Functional Ecology of Plants, 208(2), 147–156. DOI: 10.1016/j.flora.2013.02.008
Alves-Silva, E., Bächtold, A., Barônio, G. J., Torezan-Silingardi, H. M., & Del-Claro, K. 2015. Ant-herbivore interactions in an extrafloral nectaried plant: are ants good plant guards against curculionid beetles? Journal of Natural History, 49, 841–851.
Alves-Silva, E., & Del-Claro, K. 2014. Fire triggers the activity of extrafloral nectaries, but ants fail to protect the plant against herbivores in a Neotropical savanna. Arthropod-Plant Interactions, 8, 233–240. DOI: 10.1007/s11829-014-9301-8
Anjos, D. V., Caserio, B., Rezende, F. T., Ribeiro, S. P., Del-Claro, K., & Fagundes, R. 2017. Extrafloral-nectaries and interspecific aggressiveness regulate day/night turnover of ant species foraging for nectar on Bionia coriacea. Austral Ecology, 42(3), 317–328. DOI: 10.1111/aec.12446
Arimura, G. I., Kost, C., & Boland, W. 2005. Herbivore-induced, indirect plant defences. Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids, 1734(2), 91–111. DOI: 10.1016/j.bbalip.2005.03.001
Arimura, G., Ozawa, R., & Maffei, M. E. 2011. Recent advances in plant early signaling in response to herbivory. International Journal of Molecular Sciences, 12(6), 3723–3739. DOI: 10.3390/ijms12063723
Assunção, M. A., Torezan-Silingardi, H. M., & Del-Claro, K. 2014. Do ant visitors to extrafloral nectaries of plants repel pollinators and cause an indirect cost of mutualism? Flora-Morphology, Distribution, Functional Ecology of Plants, 209(5), 244–249. DOI: 10.1016/j.flora.2014.03.003
Baker, D. A., Hall, J. L., & Thorpe, J. R. 1978. A study of the extrafloral nectaries of Ricinus communis. New Phytology, 81, 129–137. DOI: 10.1111/j.1469-8137.1978.tb01612.x
Baker, H. G., & Baker, I. 1983. A brief historical review of the chemistry of floral nectar. In: B. Bentley & T. Elias (Eds.), The biology of nectaries. pp. 126–152. New York: Columbia University Press.
Baker-Meio, B., & Marquis, R. J. 2011. Context-dependent benefits from ant-plant mutualism in three sympatric varieties of Chamaecrista desvauxii. Journal of Ecology, 100, 242-252. DOI: 10.1111/j.1365-2745.2011.01892.x
Baldwin, I. T., & Preston, C. A. 1999. The eco-physiological complexity of plant responses to insect herbivores. Planta, 208(2), 137–145. DOI: 10.1007/s004250050543
Baldwin, I. T., & Schultz, J. C., 1983. Rapid changes in tree leaf chemistry induced by damage: evidence for communication between plants. Science, 221, 277–279.
Bascompte, J., & Jordano, P. 2007. Plant-animal mutualistic networks: the architecture of biodiversity. Annual Review of Ecology, Evolution, and Systematics, 38, 567–593. DOI: 10.1146/annurev.ecolsys.38.091206.095818
Bascompte, J., & Jordano, P. 2013. Mutualistic networks. Princeton University Press: p. 224.
Beattie, A. J. 1985. The evolutionary ecology of ant-plant mutualisms. Cambridge University Press: p. 182.
Becerra, J. X., & Venable, D. L. 1989. Extrafloral nectaries: a defense against ant-Homoptera mutualisms? Oikos, 55, 276–280.
Becerra, J. X., & Venable, D. L. 1991. The role of ant-homoptera mutualisms in the evolution of extrafloral nectaries. Oikos, 60, 105–106.
Belchior, C., Sendoya, S. F., & Del-Claro, K. 2016. Temporal variation in the abundance and richness of foliage-dwelling ants mediated by extrafloral nectar. PloS One, 11(7), e0158283. DOI: 10.1371/journal.pone.0158283
Belt, T. 1874. The Naturalist in Nicaragua. London: John Murray: p. 403.
Benson W. W. 1985. Amazon ant-plants. In: G. T. Prance & T. E. Lovejoy (Eds.), Amazonia. pp. 239–266. Oxford: Pergamon Press.
Bentley, B. L. 1977. Extrafloral nectaries and protection by pugnacious bodyguards. Annual Review of Ecology and Systematics, 8(1), 407–427. DOI: 10.1146/annurev.es.08.110177.002203
Berenbaum, M. 1983. Coumarins and caterpillars: a case for coevolution. Evolution, 37(1), 163–179. DOI: 10.1111/j.1558-5646.1983.tb05524.x
Bittleston, L. S., Pierce, N. E., Ellison, A. M., & Pringle, A. 2016. Convergence in multispecies interactions. Trends in Ecology & Evolution, 31(4), 269–280. DOI: 10.1016/j.tree.2016.01.006
Bixenmann, R. J., Coley, P. D., & Kursar, T. A. 2011. Is extrafloral nectar production induced by herbivores or ants in a tropical facultative ant-plant mutualism? Oecologia, 165(2), 417–425. DOI: 10.1007/s00442-010-1787-x
Blüthgen, N., & Feldhaar, H. 2010. Food and shelter: how resources influence ant ecology. In: L. P. C. Lach & K. Abbott (Eds.), Ant ecology. pp. 115–136. Oxford: Oxford University Press.
Blüthgen, N., Verhaagh, M., Goitía, W., Jaffe, K., Morawetz, W., & Barthlott, W. 2000. How plants shape the ant community in the Amazonian rainforest canopy: the role of extrafloral nectaries and homopteran honeydew. Oecologia, 125, 229–240. DOI: 10.1007/s004420000449
Bronstein, J. L. 1994. Conditional outcomes in mutualistic interactions. Trends in Ecology & Evolution, 9(6), 214–217. DOI: 10.1016/0169-5347(94)90246-1
Bronstein, J. L. 1998. The contribution of ant‐plant protection studies to our understanding of mutualism. Biotropica, 30(2), 150–161. DOI: 10.1111/j.1744-7429.1998.tb00050.x
Byk, J., & Del-Claro, K. 2010. Nectar-and pollen-gathering Cephalotes ants provide no protection against herbivory: a new manipulative experiment to test ant protective capabilities. Acta Ethologica, 13(1), 33–38. DOI: 10.1007/s10211-010-0071-8
Byk, J., & Del-Claro, K. 2011. Ant-plant interaction in the Neotropical savanna: direct beneficial effects of extrafloral nectar on ant colony fitness. Population Ecology, 53(2), 327–332. DOI: 10.1007/s10144-010-0240-7
Calixto, E. S., Lange, D., & Del-Claro, K. 2015. Foliar anti-herbivore defenses in Qualea multiflora Mart. (Vochysiaceae): changing strategy according to leaf development. Flora, 212, 19–23. DOI: 10.1016/j.flora.2015.02.001
Carrillo, J., Wang, Y., Ding, J., & Siemann, E. 2012. Induction of extrafloral nectar depends on herbivore type in invasive and native Chinese tallow seedlings. Basic and Applied Ecology, 13, 449–457. DOI: 10.1016/j.baae.2012.07.006
Cerdá, X., & Dejean, A. 2011. Predation by ants on arthropods and other animals. In: C. Polidori (Ed.), Predation in the Hymenoptera: an evolutionary perspective. pp. 39–78. Kerala: Transworld Research Network.
Chamberlain, S. A., & Holland, J. N. 2008. Density-mediated, context-dependent consumer-resource interactions between ants and extrafloral nectar plants. Ecology, 89(5), 1364–1374. DOI: 10.1890/07-1139.1
Chamberlain, S. A., & Holland, J. N. 2009. Quantitative synthesis of context dependency in ant-plant protection mutualisms. Ecology, 90(9), 2384–2392. DOI: 10.1890/08-1490.1
Coley, P. D., & Barone, J. A. 1996. Herbivory and plant defenses in tropical forests. Annual Review of Ecology and Systematics, 27, 305–335. DOI: 10.1146/annurev.ecolsys.27.1.305
Crawley, M. J. 1983. Herbivory, the dynamics of animal-plant interactions. Oxford: Blackwell Science Publications: p. 437.
Cuautle, M., & Rico-Gray, V. 2003. The effect of wasps and ants on the reproductive success of the extrafloral nectaried plant Turnera ulmifolia (Turneraceae). Functional Ecology, 17(3), 417–423. DOI: 10.1046/j.1365-2435.2003.00732.x
Dáttilo, W., Aguirre, A., Flores-Flores, R., Fagundes, R., Lange, D., García-Chavez, J., Del-Claro, K., & Rico-Gray, V. 2015. Secretory activity of extrafloral nectaries shaping multitrophic ant-plant-herbivore interactions in an arid environment. Journal of Arid Environments, 114, 104–109. DOI: 10.1016/j.jaridenv.2014.12.001
Dáttilo, W., Fagundes, R., Gurka, C. A. Q., Silva, M. S. A., Vieira, M. C. L., Izzo, T. J., Díaz-Castelazo, C., Del-Claro, K., & Rico-Gray, V. 2014. Individual-based ant-plant networks: diurnal-nocturnal structure and species-area relationship. PLoS One, 9(6), e99838. DOI: 10.1371/journal.pone.0099838
Dáttilo, W., Guimarães, P. R., & Izzo, T. J. 2013. Spatial structure of ant–plant mutualistic networks. Oikos, 122(11), 1643–1648. DOI: 10.1111/j.1600-0706.2013.00562.x
Dáttilo, W., Lara-Rodríguez, N., Jordano, P., Guimarães, P. R., Thompson, J. N., Marquis, R. J., Medeiros, L. M., Ortiz-Pulido, R., Marcos-García, M. A., & Rico-Gray, V. 2016. Unravelling Darwin's entangled bank: architecture and robustness of mutualistic networks with multiple interaction types. Proceedings of the Royal Society B, 283(1843), 20161564. DOI: 10.1098/rspb.2016.1564
Davidson, D. W. 1997. The role of resource imbalances in the evolutionary ecology of tropical arboreal ants. Biological Journal of the Linnean Society, 61(2), 153–181. DOI: 10.1111/j.1095-8312.1997.tb01785.x
Davidson, D. W., Snelling, R. R., & Longino, J. T. 1989. Competition among ants for myrmecophytes and the significance of plant trichomes. Biotropica, 64–73. DOI: 10.2307/2388444
Del-Claro, K. 2004. Multitrophic relationships, conditional mutualisms, and the study of interaction biodiversity in tropical savannas. Neotropical Entomology, 33(6), 665–672. DOI: 10.1590/S1519-566X2004000600002
Del-Claro, K. 2012. Origens e importância das relações plantas-animais para a ecologia e conservação. In: K. Del-Claro & H. M. Torezan-Silingardi (Eds.), Ecologia das interações plantas-animais: uma abordagem ecológico-evolutiva. pp. 37–50. Rio de Janeiro: Technical Books.
Del-Claro, K., & Marquis, R. J. 2015. Ant species identity has a greater effect than fire on the outcome of an ant protection system in Brazilian Cerrado. Biotropica, 47(4), 459–467. DOI: 10.1111/btp.12227
Del-Claro, K., Rico-Gray, V., Torezan-Silingardi, H. M., Alves-Silva, E., Fagundes, R., Lange, D., Dáttilo, W., Vilela, A. A., Aguirre, A., & Rodeiguez-Morales, D. 2016. Loss and gains in ant-plant interactions mediated by extrafloral nectar: Fidelity, cheats, and lies. Insectes Sociaux, 63(2), 207–221. DOI: 10.1007/s00040-016-0466-2
Del-Claro, K., Stefani, V., Lange, D., Vilela, A. A., Nahas, L., Velasques, M., & Torezan-Silingardi, H. M. 2013. The importance of natural history studies for a better comprehension of animal-plant interaction networks. Bioscience Journal, 29(2), 439–444.
Del-Claro, K., & Torezan-Silingardi, H. M. 2012. Ecologia das interações plantas-animais: uma abordagem ecológico-evolutiva. Rio de Janeiro: Technical Books: p. 336.
Díaz-Castelazo, C., Rico-Gray, V., Ortega, F., & Angeles, G. 2005. Morphological and secretory characterization of extrafloral nectaries in plants of coastal Veracruz, Mexico. Annals of Botany, 96(7), 1175–1189. DOI: 10.1093/aob/mci270
Duran-Flores, D., & Heil, M. 2016. Sources of specificity in plant damaged-self recognition. Current Opinion in Plant Biology, 32, 77–87. DOI: 10.1016/j.pbi.2016.06.019
Ehrlich, P. R., & Raven, P. H. 1964. Butterflies and plants: a study in coevolution. Evolution, 18(4), 586–608. DOI: 10.1111/j.1558-5646.1964.tb01674.x
Eubanks, M. D., & Styrsky, J. D. 2005. Effects of plant feeding on the performance of omnivorous “predators”. In: F. L. Wäckers, P. C. J. van Rijn & J. Bruin (Eds.), Plant-provided food for carnivorous insects: a protective mutualism and its applications. pp. 148–177. Cambridge: Cambridge University Press.
Fagundes, R. S., Anjos, D. V., Carvalho, R., & Del-Claro, K. 2015. Availability of food and nesting-sites as regulatory mechanisms for the recovery of ant diversity after fire disturbance. Sociobiology 62(1), 1–9. DOI: 10.13102/sociobiology.v62i1.1-9
Fagundes, R., Dáttilo, W., Ribeiro, S. P., Rico-Gray, V., Jordano, P., & Del-Claro, K. 2017. Differences between ant species in plant protection are influenced by the production of extrafloral nectar and related to the degree of leaf herbivory. Biological Journal of the Linnean Society, 122, 71–83. DOI: 10.1093/biolinnean/blx059 .
Falcão, J. C. F., Dáttilo, W., & Izzo, T. J. 2014. Temporal variation in extrafloral nectar secretion in different ontogenic stages of the fruits of Alibertia verrucosa S. Moore (Rubiaceae) in a Neotropical savanna. Journal of Plant Interactions, 9(1), 137–142. DOI: 10.1080/17429145.2013.782513
Floren, A., Biun, A., & Linsenmair, E. K. 2002. Arboreal ants as key predators in tropical lowland rainforest trees. Oecologia, 131(1), 137–144. DOI: 10.1007/s00442-002-0874-z
Fürstenberg-Hägg, J., Zagrobelny, M., & Bak, S. 2013. Plant Defense against Insect Herbivores. International Journal of Molecular Sciences, 14(5), 10242–10297. DOI: 10.3390/ijms140510242
González-Teuber, M., & Heil, M. 2009. Nectar chemistry is tailored for both attraction of mutualists and protection from exploiters. Plant Signaling & Behavior, 4(9), 809–813. DOI: 10.4161/psb.4.9.9393
Grimaldi, D., & Engel, M. S. 2005. Evolution of the Insects. New York: Cambridge University Press: p. 763.
Heil, M. 2008. Indirect defence via tritrophic interactions. New Phytologist, 178, 41–61. DOI: 10.1111/j.1469-8137.2007.02330.x
Heil, M. 2015. Extrafloral nectar at the plant-insect interface: a spotlight on chemical ecology, phenotypic plasticity, and food webs. Annual Review of Entomology, 60, 213–232. DOI: 10.1146/annurev-ento-010814-020753
Heil, M., Fiala, B., Baumann, B., & Linsenmair, K. E. 2000. Temporal, spatial and biotic variations in extrafloral nectar secretion by Macaranga tanarius. Functional Ecology, 14, 749–757. DOI: 10.1046/j.1365-2435.2000.00480.x
Heil, M., & Land, W. G. 2014. Danger signals-damaged-self recognition across the tree of life. Frontiers in Plant Science, 5(578), 1–16. DOI: 10.3389/fpls.2014.00578
Heil, M., & Silva-Bueno, J. C. 2007. Within-plant signaling by volatiles leads to induction and priming of an indirect plant defense in nature. Proceedings of the National Academy of Sciences, 104, 5467–5472. DOI: 10.1073/pnas.0610266104
Heinze, J., Hölldobler, B., & Peeters, C. 1994. Conflict and cooperation in ant societies. Naturwissenschaften, 81(11), 489–497. DOI: 10.1007/BF01132680
Holland, J. N., Chamberlain, S. A., & Horn, K. C., 2009. Optimal defence theory predicts investment in extrafloral nectar resources in an ant-plant mutualism. Journal of Ecology, 97, 89–96. DOI: 10.1111/j.1365-2745.2008.01446.x
Holland, J. N., Chamberlain, S. A., & Miller, T. E. 2011. Consequences of ants and extrafloral nectar for a pollinating seed-consuming mutualism: ant satiation, floral distraction or plant defense? Oikos, 120(3), 381–388. DOI: 10.1111/j.1600-0706.2010.18958.x
Hölldobler, B., & Wilson, E. O. 1990. The ants. Cambridge: Harvard University Press: p. 743.
Hunter Jr., M. L., Jacobson Jr., G. L., & Webb III, T. 1988. Paleoecology and the coarse-filter approach to maintaining biological diversity. Conservation Biology, 2(4), 375–385. DOI: 10.1111/j.1523-1739.1988.tb00202.x
Janzen, D. H. 1966. Coevolution of mutualism between ants and acacias in Central America. Evolution, 20(3), 249–275. DOI: 10.1111/j.1558-5646.1966.tb03364.x
Jones, I. M., & Koptur, S. 2015. Dynamic extrafloral nectar production: the timing of leaf damage affects the defensive response in Senna mexicana var. chapmanii (Fabaceae). American Journal of Botany, 102(1), 58–66. DOI: 10.3732/ajb.1400381
Karban, R. 1993. Costs and benefits of induced resistance and plant density for a native shrub, Gossypium thurberi. Ecology, 74, 9–19. DOI: 10.2307/1939496
Karban, R., & Baldwin, I. T. 1997. Induced Responses to Herbivory. Chicago: Chicago University Press: p. 317.
Karban, R., & Myers, J. H. 1989. Induced plant responses to herbivory. Annual Review of Ecology and Systematics, 20, 331–348. DOI: 10.1146/annurev.es.20.110189.001555
Kersch, M. F., & Fonseca, C. R. 2005. Abiotic factors and the conditional outcome of an ant-plant mutualism. Ecology, 86(8), 2117–2126. DOI: 10.1890/04-1916
Koptur, S. 1992. Extrafloral nectary-mediated interactions between insects and plants. In: E. Bernays (Ed.), Insect–plant interactions. pp 81–129. Florida: Boca Raton Press.
Koptur, S. 1994. Floral and extrafloral nectars of Costa Rican Inga trees: a comparison of their constituents and composition. Biotropica, 26(3), 276–284. DOI: 10.2307/2388848
Koptur, S. 2005. Nectar as fuel for plant protectors. In: F. L. Wäckers, P. C. J. van Rijn, & J. Bruin (Eds.), Plant-provided food for carnivorous insects: a protective mutualism and its applications. pp. 75–108. Cambridge: Cambridge University Press.
Koptur, S., Jones, I. M., & Peña, J. E. 2015. The influence of host plant extrafloral nectaries on multitrophic interactions: an experimental investigation. PloS One, 10(9), e0138157. DOI: 10.1371/journal.pone.0138157
Korndörfer, A. P., & Del-Claro, K. 2006. Ant defense versus induced defense in Lafoensia pacari (Lythraceae), a myrmecophilous tree of the Brazilian Cerrado. Biotropica, 38, 786–788. DOI: 10.1111/j.1744-7429.2006.00200.x
Kukalová-Peck, J. 1991. Fossil history and the evolution of hexapod structures. The Insects of Australia, 1, 141–179.
Labandeira, C. C. 1997. Insect mouthparts: ascertaining the paleobiology of insect feeding strategies. Annual Review of Ecology and Systematics, 28(1), 153–193. DOI: 10.1146/annurev.ecolsys.28.1.153
Labandeira, C. C. 1998. Early history of arthropod and vascular plant associations. Annual Review of Earth and Planetary Sciences, 26(1), 329–377. DOI: 10.1146/annurev.earth.26.1.329
Labandeira, C. C., & Sepkoski, J. J. 1993. Insect diversity in the fossil record. Science, 261(5119), 310–315.
Lange, D., Calixto, E. S., & Del-Claro, K. 2017. Variation in Extrafloral Nectary Productivity Influences the Ant Foraging. PloS One, 12(1), e0169492. DOI: 10.1371/journal.pone.0169492
Lange, D., Dattilo, W., & Del‐Claro, K. 2013. Influence of extrafloral nectary phenology on ant-plant mutualistic networks in a neotropical savanna. Ecological Entomology, 38(5), 463–469. DOI: 10.1111/een.12036
Lange, D., & Del-Claro, K. 2014. Ant-plant interaction in a tropical savanna: may the network structure vary over time and influence on the outcomes of associations?. PLoS One, 9(8), e105574. DOI: 10.1371/journal.pone.0105574
Leal, L. C., & Peixoto, P. E. 2016. Decreasing water availability across the globe improves the effectiveness of protective ant-plant mutualisms: a meta-analysis. Biological Reviews, 92(3), 1785–1794. DOI: 10.1111/brv.12307
Machado, S. R., Morellato, L. P. C., Sajo, M. G., & Oliveira, P. S. 2008. Morphological patterns of extrafloral nectaries in woody plant species of the Brazilian cerrado. Plant Biology, 10(5), 660–673. DOI: 10.1111/j.1438-8677.2008.00068.x
Marazzi, B., Bronstein, J. L., & Koptur, S. 2013. The diversity, ecology and evolution of extrafloral nectaries: current perspectives and future challenges. Annals of Botany, 111(6), 1243–1250. DOI: 10.1093/aob/mct109
Marquis, R. J. 2012. Uma abordagem geral das defesas das plantas contra ação dos herbívoros. In: K. Del-Claro & H. M. Torezan-Silingardi (Eds.), Ecologia das interações plantas-animais: uma abordagem ecológico-evolutiva. pp. 55–66. Rio de Janeiro: Technical Books.
Marquis, R. J., & Braker, H. E. 1994. Plant-herbivore interactions: diversity, specificity and impact. In: L. A. McDade (Ed.), La Selva: ecology and natural history of a neotropical rain forest. pp. 261–281. Chicago: University of Chicago Press.
May, R. M. 1988. How many species are there on earth? Science, 241(4872), 1441–1449.
McCann, K. S. 2000. The diversity-stability debate. Nature, 405(6783), 228–233. DOI: 10.1038/35012234
McKey, D. 1974. Adaptive patterns in alkaloid physiology. American Naturalist, 108(961), 305–320.
McKey, D. 1979. The distribution of plant secondary compounds within plants. In: G. A. Rosenthal & D. H. Janzen (Eds.), Herbivores: their interactions with secondary plant metabolites. pp. 55–133. New York: Academic press.
Michelangeli, F. A. 2005. Tococa (Melastomataceae). Flora Neotropica, 98, 1–114.
Misof, B., Liu, S., Meusemann, K., Peters, R. S., Donath, A., Mayer, C., Frandsen, P. B., Ware, J., Flouri, T., Beutel, R. G., Niehuis, O., Petersen, M., Izquierdo-Carrasco, F., Wappler, T., Rust, J., Aberer, A. J., Aspöck, U., Aspöck, H., Bartel, D., Blanke, A., Berger, S., Böhm, A., Buckley, T. R., Calcott, B., Chen J., Friedrich, F., Fukui, M., Fujita, M., Greve, C., Grobe, P., Gu, S., Huang, Y., Jermiin, L. S., Kawahara, A. Y., Krogmann, L., Kubiak, M., Lanfear, R., Letsch, H., Li, Y., Li, Z., Li, J., Lu, H., Machida, R., Mashimo, Y., Kapli, P., McKenna, D. D., Meng, G., Nakagaki, Y., Navarrete-Heredia, J. L., Ott, M., Ou, Y., Pass, G., Podsiadlowski, L., Pohl, H., Reumont von, B. M., Schütte, K., Sekiya, K., Shimizu, S., Slipinski, A., Stamatakis, A., Song, W., Su, X., Szucsich, N. U., Tan, M., Tan, X., Tang, M., Tang, J., Timelthaler, G., Tomizuka, S., Trautwein, M., Tong, X., Uchifune, T., Walzl, M. G., Wiegmann, B. M., Wilbrandt, J., Wipfler, B., Wong, T. K. F., Wu, Q., Wu, G., Xie, Y., Yang, S., Yang, Q., Yeates, D. K., Yoshizawa, K., Zhang, Q., Zhang, R., Zhang, W., Zhang, Y., Zhao, J., Zhou, C., Zhou, L., Ziesmann, T., Zou, S., Li, Y., Xu, X., Zhang, Y., Yang, H., Wang, J., Wang, J., Kjer, K. M., & Zhou, X.. 2014. Phylogenomics resolves the timing and pattern of insect evolution. Science, 346(6210), 763–767. DOI: 10.1126/science.1257570
Nahas, L., Gonzaga, M. O., & Del-Claro, K. 2012. Emergent impacts of ant and spider interactions: herbivory reduction in a tropical savanna tree. Biotropica, 44(4), 498–505. DOI: 10.1111/j.1744-7429.2011.00850.x
Ness, J. H. 2003. Catalpa bignonioides alters extrafloral nectar production after herbivory and attracts ant bodyguards. Oecologia, 134, 210–218. DOI: 10.1007/s00442-002-1110-6
Ness, J. H., Morris, W. F., & Bronstein, J. L. 2009. For ant‐protected plants, the best defense is a hungry offense. Ecology, 90(10), 2823–2831. DOI: 10.1890/08-1580.1
Noss, R. F. 1990. Indicators for monitoring biodiversity: a hierarchical approach. Conservation Biology, 4(4), 355–364. DOI: 10.1111/j.1523-1739.1990.tb00309.x
O'Dowd, D. J., & Catchpole, E. A. 1983. Ants and extrafloral nectaries: no evidence for plant protection in Helichrysum spp.-ant interactions. Oecologia, 59(2), 191–200. DOI: 10.1007/BF00378837
Ohgushi, T. 2016. Eco-evolutionary dynamics of plant-herbivore communities: incorporating plant phenotypic plasticity. Current Opinion in Insect Science, 14, 40–45. DOI: 10.1016/j.cois.2016.01.006
Oliveira, P. S., & Del-Claro, K. 2005. Multitrophic interactions in a neotropical savanna: Ant-hemipteran systems, associated insect herbivores, and a host plant. In: D. F. R. P. Burslem, M. A. Pinard & S. E. Hartley (Eds.), Biotic interactions in the tropics. pp. 414–438. Cambridge: Cambridge University Press.
Oliveira, P. S., & Freitas, A. V. 2004. Ant-plant-herbivore interactions in the neotropical cerrado savanna. Naturwissenschaften, 91(12), 557–570. DOI: 10.1007/s00114-004-0585-x
Oliveira, P. S., & Leitao-Filho, H. F. 1987. Extrafloral nectaries: their taxonomic distribution and abundance in the woody flora of cerrado vegetation in southeast Brazil. Biotropica, 19(2), 140–148. DOI: 10.2307/2388736
Oliveira, P. S., & Pie, M. R. 1998. Interaction between ants and plants bearing extrafloral nectaries in cerrado vegetation. Anais da Sociedade Entomológica do Brasil, 27(2), 161–176. DOI: 10.1590/S0301-80591998000200001
Oliveira, P. S., Sendoya S. F., & Del-Claro, K. 2012. Defesas bióticas contra herbívoros em plantas do Cerrado: Interações entre formigas, nectários extraflorais e insetos trofobiontes. In: K. Del-Claro & H. M. Torezan-Silingardi (Eds.), Ecologia das interações plantas-animais: Uma abordagem ecológico-evolutiva. pp. 155–168. Rio de Janeiro: Technical Books.
Oliveira, P. S., Silva, A. D., & Martins, A. B. 1987. Ant foraging on extrafloral nectaries of Qualea grandiflora (Vochysiaceae) in cerrado vegetation: ants as potential antiherbivore agents. Oecologia, 74(2), 228–230. DOI: 10.1007/BF00379363
Packard, A. S. 1890. Insects injurious to forest and shade trees. U.S.: Department of Agriculture, Entomological Commission Report: p. 957.
Paschold, A., Halitschke, R., & Baldwin, I. T. 2007. Co(i)-ordinating defenses: NaCOI1 mediates herbivore-induced resistance in Nicotiana attenuate and reveals the role of herbivore movement in avoiding defenses. Plant Journal, 51, 79–91. DOI: 10.1111/j.1365-313X.2007.03119.x
Pires, L. P., & Del-Claro, K. 2014. Variation in the outcomes of an ant-plant system: fire and leaf fungus infection reduce benefits to plants with extrafloral nectaries. Journal of Insect Science, 14, 1–10. DOI: 10.1093/jis/14.1.84
Pohl, S., Frederickson, M. E., Elgar, M. A., & Pierce, N. E. 2016. Colony Diet Influences Ant Worker Foraging and Attendance of Myrmecophilous Lycaenid Caterpillars. Frontiers in Ecology and Evolution, 4(114), 1–8. DOI: 10.3389/fevo.2016.00114.
Price, P. W., Denno, R. F., Eubanks, M. D., Finke, D. L., & Kaplan, I. 2011. Insect ecology: behavior, populations and communities. Cambridge: Cambridge University Press: p. 816.
Pulice, C. E., & Packer, A. A. 2008. Simulated herbivory induces extrafloral nectar production in Prunus avium. Functional Ecology, 22: 801–807. DOI: 10.1111/j.1365-2435.2008.01440.x
Rashbrook, V. K., Compton, S. G., & Lawton, J. H. 1992. Ant-herbivore interactions: reasons for the absence of benefits to a fern with foliar nectaries. Ecology, 73(6), 2167–2174. DOI: 10.2307/1941464
Rhoades, D. F. 1979. Evolution of plant defense against herbivores. In: G. A. Rosenthal & D. H. Janzen (Eds.), Herbivores: their interaction with secondary metabolites. pp. 1–55. New York: Academic Press.
Rico-Gray, V. 1989. The importance of floral and circum-floral nectar to ants inhabiting dry tropical lowlands. Biological Journal of the Linnean Society, 38: 173–181. DOI: 10.1111/j.1095-8312.1989.tb01572.x
Rico-Gray, V., Díaz-Castelazo, C., Ramírez-Hernández, A., Guimarães, P. R., & Holland, J. N. 2012. Abiotic factors shape temporal variation in the structure of an ant-plant network. Arthropod-Plant Interactions, 6, 289–295. DOI: 10.1007/s11829-011-9170-3
Rico-Gray, V., & Oliveira, P. S. 2007. The ecology and evolution of ant-plant interactions. Chicago: University of Chicago Press: p. 331.
Rico-Gray, V., & Thien, L. B., 1989. Effect of different ant species on the reproductive fitness of Schomburgkia tibicinis (Orchidaceae) in Mexico. Oecologia, 81, 487–489.
Riley, C. V. 1892. Some interrelations of plants and insects. Proceedings of the Biological Society of Washington, 7, 81–104.
Romero, G. Q., & Vasconcellos-Neto, J. 2004. Beneficial effects of flower‐dwelling predators on their host plant. Ecology, 85(2), 446–457. DOI: 10.1890/02-0327
Rosumek, F. B., Silveira, F. A., Neves, F. D. S., Barbosa, N. P. D. U., Diniz, L., Oki, Y., Pezzini, F., Fernandes, G. W. & Cornelissen, T. 2009. Ants on plants: a meta-analysis of the role of ants as plant biotic defenses. Oecologia, 160(3), 537–549. DOI: 10.1007/s00442-009-1309-x
Ruhren, S., & Handel, S. N. 1999. Jumping spiders (Salticidae) enhance the seed production of a plant with extrafloral nectaries. Oecologia, 119(2), 227–230. DOI: 10.1007/s004420050780
Schoonhoven, L. M., Van Loon, J. J., & Dicke, M. 2005. Insect-plant biology. Oxford University Press on Demand: p. 421.
Silvestre, R., Brandão, C. R. F., & Da Silva, R. R. 2003. Grupos funcionales de hormigas: el caso de los gremios del Cerrado. In: F. Fernández (Ed.), Introducción a las hormigas de la región Neotropical. pp. 113–148. Colombia: Alexander von Humboldt.
Stork, N. E. 1988. Insect diversity: facts, fiction and speculation. Biological Journal of the Linnean Society, 35(4), 321–337. DOI: 10.1111/j.1095-8312.1988.tb00474.x
Stork, N. E., McBroom, J., Gely, C., & Hamilton, A. J. 2015. New approaches narrow global species estimates for beetles, insects, and terrestrial arthropods. Proceedings of the National Academy of Sciences, 112(24), 7519–7523. DOI: 10.1073/pnas.1502408112
Stout, M. J., & Duffey, S. S. 1996. Characterization of induced resistance in tomato plants. Entomologia Experimentalis et Applicata, 79, 273-283. DOI: 10.1111/j.1570-7458.1996.tb00835.x
Thompson, J. N. 1994. The coevolutionary process. University of Chicago Press: p. 383.
Thompson, J. N. 1996. Evolutionary ecology and the conservation of biodiversity. Trends in Ecology and Evolution, 11, 300–303. DOI: http://dx.doi.org/10.1016/0169-5347(96)20048-5
Thompson, J. N. 2005. The geographic mosaic of coevolution. Chicago and London: The University of Chicago Press: p. 400.
Thompson, J. N. 2013. Relentless Evolution. Chicago: University of Chicago Press: p. 499.
Thompson, J. N. 2014. Interaction and coevolution. Chicago: University of Chicago Press: p. 178.
Torezan-Silingardi, H. M. 2012. Flores e animais: uma introdução à história natural da polinização. In: K. Del-Claro & H. M. Torezan-Silingardi (Eds.), Ecologia das Interações plantas-animais: uma abordagem ecológico-evolutiva. pp. 111–140. Rio de Janeiro: Technical Books Editora.
Vane-Wright, R. I., Humphries, C. J., & Williams, P. H. 1991. What to protect? Systematics and the agony of choice. Biological Conservation, 55(3), 235–254. DOI: 10.1016/0006-3207(91)90030-D
Vilela, A. A., Torezan-Silingardi, H. M., & Del-Claro, K., 2014. Conditional outcomes in ant–plant–herbivore interactions influenced by sequential flowering. Flora, 209, 359–366. DOI: 10.1016/j.flora.2014.04.004
Vilela, A. A., DelClaro, V. T. S., Torezan-Silingardi, H. M., & Del-Claro, K., 2017. Climate changes affecting biotic interactions, phenology, and reproductive success in a savanna community over a 10-year period. Arthropod-Plant Interactions. DOI: 10.1007/s11829-017-9572-y
Von Wettstein, R. 1889. Über die Compositen der österreichisch-ungarischen Flora mit zuckerabscheidenden Hüllschuppen. Sitzungsberichte der Kaiserlichen Akademie der Wissenschaften in Wien. Mathematisch-naturwissenschaftliche Classe, 97, 570–589.
Wäckers, F. L. 2001. A comparison of nectar-and honeydew sugars with respect to their utilization by the hymenopteran parasitoid Cotesia glomerata. Journal of Insect Physiology, 47(9), 1077–1084. DOI: 10.1016/S0022-1910(01)00088-9
Wäckers, F. L., & Bonifay, C. 2004. How to be sweet? Extrafloral nectar allocation by Gossypium hirsutum fits optimal defense theory predictions. Ecology, 85, 1512–1518. DOI: 10.1890/03-0422
Wäckers, F. L., van Rijn, P. C. J., & Bruin, J. 2005. Plant-provided food for carnivorous insects: a protective mutualism and its applications. Cambridge: Cambridge University Press: p. 359.
Wagner, D., & Nicklen, E. F. 2010. Ant nest location, soil nutrients and nutrient uptake by ant‐associated plants: does extrafloral nectar attract ant nests and thereby enhance plant nutrition? Journal of Ecology, 98(3), 614–624. DOI: 10.1111/j.1365-2745.2010.01640.x
Weber, M. G., & Keeler, K. H. 2013. The phylogenetic distribution of extrafloral nectaries in plants. Annals of Botany, 111(6), 1251–1261. DOI: 10.1093/aob/mcs225
Weber, M. G., Wagner, C. E., Best, R. J., Harmon, L. J., & Matthews, B. 2017. Evolution in a community context: on integrating ecological interactions and macroevolution. Trends in Ecology & Evolution, 32(4), 291–304. DOI: 10.1016/j.tree.2017.01.003
Whitney, K. D. 2004. Experimental evidence that both parties benefit in a facultative plant-spider mutualism. Ecology, 85(6), 1642–1650. DOI: 10.1890/03-0282
Wilder, S. M., & Eubanks, M. D. 2010. Extrafloral nectar content alters foraging preferences of a predatory ant. Biology Letters, 6(2), 177–179. DOI: 10.1098/rsbl.2009.0736.
Zangerl, A. R., & Rutledge, C. E. 1996. The probability of attack and patterns of constitutive and induced defense: a test of optimal defense theory. American Naturalist, 147, 599–608.
Zhang, S., Zhang, Y., & Ma, K. 2015. The equal effectiveness of different defensive strategies. Scientific Reports, 5, 13049. DOI: 1 0.1038/srep13049
