I Can See You: Temporal Variation in Ant Aggressiveness Towards Herbivores under Continuous Provision of High- or Low-quality Food Sources
DOI:
https://doi.org/10.13102/sociobiology.v67i1.4727Keywords:
ant-plant-herbivore interactions, artificial nectaries, semiarid environments, dummy caterpillars, multitrophic interactions, enemy free space.Abstract
To reduce herbivory, plants bearing extrafloral nectaries interact with ants and attract them by providing food. As plant bodyguards, ants respond to the resource provision and, using their antennae, detect chemical messages from the host plants that help them to locate herbivores. Ants can also use their vision to explore the environment; however, information is lacking on how interactions between visual signs and the availability of extrafloral nectar affect ant aggressiveness near resources. We addressed the following question in this study: does the ants’ ability to visualize potential herbivores enhance their aggression under a constant provision of a high-quality food source? Using an experimental approach within the semiarid intertropical region of Tehuacan-Cuicatlán (Mexico), we manipulated the availability of food sources by constantly offering artificial nectaries on the shrub Prosopis laevigata (Fabaceae). Over two time periods (day and night), we tested how the presence of a high-quality food source affected ant aggressiveness to herbivores. Therefore, we offered dummy caterpillars and counted the number of marks left by enemy attacks. Overall the attack rate was extremely high: 84.25% of the dummy caterpillars were injured. Ants were responsible for 86.22% of the marks left by enemies, and their aggression increased during the day, especially towards caterpillars in trees with high-quality food sources. During the night, ants probably rely mostly on their antennae to detect potential herbivores; therefore, their ability to detect dummy caterpillars was greater during the day. We show that, besides nectar quality and availability, visualizing herbivores may enhance ant aggressiveness.
Downloads
References
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: 317–328. doi: 10.1111/aec.12446
Buehlmann, C., Fernandes, A.S.D., Graham, P. (2018). The interaction of path integration and terrestrial visual cues in navigating desert ants: what can we learn from path characteristics? Journal of Experimental Biology 221: jeb167304. doi: 10.1242/jeb.167304
Calixto, E.S., Lange, D., Del-Claro, K. (2015). Foliar anti-herbivore defences in Qualea multiflora Mart. (Vochysiaceae): Changing strategy according to leaf development. Flora - Morphology, Distribution, Functional Ecology of Plants 212: 19–23. doi: 10.1016/j.flora.2015.02.001
Campos, R.I., Camacho, G.P. (2014). Ant–plant interactions: the importance of extrafloral nectaries versus hemipteran honeydew on plant defence against herbivores. Arthropod- Plant Interactions 8: 507–512. doi: 10.1007/s11829-014-9338-8
Dáttilo, W., Aguirre, A., Flores-Flores, R.V., Ahuatzin Flores, D., Corro Méndez, E.J. (2017) Plantas, hormigas y herbívoros interactúan en un ambiente semiárido en el centro de México, ¿cómo lo hacen? CONABIO. Biodiversitas 132: 12–16.
Dáttilo, W., Aguirre, A., Flores-Flores, R.V., Fagundes, R., Lange, D., García-Chávez, 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. doi: 10.1371/journal.pone.0099838
Del-Claro, K., Rico-Gray, V., Torezan-Silingardi, H.M., Alves-Silva, E., Fagundes, R., Lange, D., Dáttilo, W., Vilela, A.A., Aguirre, A., Rodriguez-Morales, D. (2016). Loss and gains in ant–plant interactions mediated by extrafloral nectar: fidelity, cheats, and lies. Insectes Sociaux 63: 207–221. doi: 10.1007/s00040-016-0466-2
Fagundes, R., Dáttilo, W., Ribeiro, S.P., Rico-Gray, V., Jordano, P., Del-Claro, K. (2017). Differences among ant species in plant protection are related to production of extrafloral nectar and 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: 137–142. doi: 10.1080/17429145.2013.782513
Fernandes, A.S.D., Buckley, C.L., Niven, J.E. (2018). Visual associative learning in wood ants. Journal of Experimental Biology 221: jeb173260. doi: 10.1242/jeb.173260
Fitzpatrick, G., Lanan, M.C., Bronstein, J.L. (2014). Thermal tolerance affects mutualist attendance in an ant-plant protection mutualism. Oecologia 176: 129–138. doi: 10.1007/s00442-014-3005-8
Flores-Flores, R.V., Aguirre, A., Anjos, D. V., Neves, F.S., Campos, R.I., Dáttilo, W. (2018). Food source quality and ant dominance hierarchy influence the outcomes of ant-plant interactions in an arid environment. Acta Oecologica 87: 13–19. doi: 10.1016/j.actao.2018.02.004
Freas, C.A., Wystrach, A., Narendra, A., Cheng, K. (2018). The view from the trees: Nocturnal bull ants, Myrmecia midas, use the surrounding panorama while descending from trees. Frontiers in Psychology 9: 1–15. doi: 10.3389/fpsyg.2018.00016
Frey, D., Vega, K., Zellweger, F., Ghazoul, J., Hansen, D., Moretti, M. (2018). Predation risk shaped by habitat and landscape complexity in urban environments. Journal of Applied Ecology 55: 2343–2353. doi: 10.1111/1365-2664.13189
Gottsberger, G., Schrauwen, J., Linskens, H.F. (1984). Aminoácidos y azúcares en el néctar, y su significado evolutivo putativo. Plant Systematics and Evolution 145: 55–77.
Graham, P., Cheng, K. (2009). Ants use the panoramic skyline as a visual cue during navigation. Current Biology 19: R935–R937. doi: 10.1016/j.cub.2009.08.015
Greiner, B., Narendra, A., Reid, S.F., Dacke, M., Ribi, W.A., Zeil, J. (2007). Eye structure correlates with distinct foraging - bout timing in primitive ants. Current Biology 17: 879–880. doi: 10.1016/j.cub.2007.08.015
Grover, C.D., Kay, A.D., Monson, J.A., Marsh, T.C., Holway, D.A. (2007). Linking nutrition and behavioural dominance: Carbohydrate scarcity limits aggression and activity in Argentine ants. Proceedings of the Royal Society B Biological Sciences 274: 2951–2957. doi: 0.1098/rspb.2007.1065
Heil, M. (2015). Extrafloral Nectar at the Plant-Insect Interface: A Spotlight on Chemical Ecology, Phenotypic Plasticity, and Food Webs. Annual Reviews Entomology 60: 213–232. doi: 10.1146/annurev-ento-010814-020753
Herrera, C.M. & Pellmyr, O. (2002). Plant-Animal Interactions: An evolutionary approach. Oxford: Wiley-Blackwell.
Hossie, T.J., Sherratt, T.N. (2012). Eyespots interact with body colour to protect caterpillar-like prey from avian predators. Animal Behaviour 84: 167–173. doi: 10.1016/j.anbehav.2012.04.027
Knaden, M., Graham, P. (2015). The Sensory Ecology of Ant Navigation: From Natural Environments to Neural Mechanisms. Annual Reviews Entomology 61: 63–76. doi: 10.1146/annurev-ento-010715-023703
Koptur, S. (1984). Experimental evidence for defence of Inga (Mimosoideae) saplings by ants. Ecology 65: 1787–1793.
Land, M.F. (1997). Visual acuity in insects. Annual Reviews Entomology 42: 147-77. doi: 10.1146/annurev.ento.42.1.147
Lange, D., Calixto, E.S., Del-Claro, K. (2017). Variation in extrafloral nectary productivity influences the ant foraging. PLoS One 12: 1–13. doi: 10.1371/journal.pone.0169492
Leles, B., Xiao, X., Pasion, B.O., Nakamura, A., Tomlinson, K.W. (2017). Does plant diversity increase top-down control of herbivorous insects in tropical forest? Oikos 126: 1142–1149. doi: 10.1111/oik.03562
Low, P.A., Sam, K., McArthur, C., Posa, M.R.C., Hochuli, D.F. (2014). Determining predator identity from attack marks left in model caterpillars: Guidelines for best practice. Entomologia Experimentalis et Applicata 152: 120–126. doi: 10.1111/eea.12207
Luna, P., Castro-Leal, L., Contreras-Cerón, R., Castillo-Meza, A.L. (2016). Formicids activity on Ferocactus latispinus (Cactaceae) in a semiarid environment of central México. Entomológica Mexicana 3: 530–536.
Moreno, C., Ferro, V.G. (2012). Intensity of attack on artificial caterpillars in different Cerrado vegetation types, Brazil. Bioikos 26: 71–75.
Nelson, A.S., Carvajal Acosta, N., Mooney, K.A. (2019). Plant chemical mediation of ant behavior. Current Opinions in Insect Science 32: 98–103. doi: 10.1016/j.cois.2018.12.003
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
Passos, F.C.S., Leal, L.C. (2019). Protein matters: ants remove herbivores more frequently from extrafloral nectary-bearing plants when habitats are protein poor. Biological Journal of the Linnean Society 127: 407–416. doi: 10.1093/biolinnean/blz033
Pringle, E.G., Akçay, E., Raab, T.K., Dirzo, R., Gordon, D.M. (2013). Water stress strengthens mutualism among ants, trees, and scale insects. PLoS Biol 11: e1001705. doi: 10.1371/journal.pbio.1001705
RCoreTeam, (2018). R: A language and environment for statistical computing. R A Lang. Environ. Stat. Comput.
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., Oliveira, P.S. (2007). The Ecology and Evolution of Ant-Plant Interactions. Chicago: University of Chicago Press.
Rico-Gray, V., Palacios-Rios, M., Garcia-Franco, J.G., Mackay, W.P. (2006). Richness and seasonal variation of ant-plant associations mediated by plant-derived food resources in the semiarid Zapotitlán valley, México. The American Midland Naturalist 140: 21–26. doi: 10.1674/0003-0031(1998)140[0021:rasvoa]2.0.co;2
Roslin, T., Hardwick, B., Novotny, V., Petry, W.K., Andrew, N.R., Asmus, A., Barrio, I.C., Basset, Y., Boesing, A.L., Bonebrake, T.C., Cameron, E.K., Dáttilo, W., Donoso, D.A., Drozd, P., Gray, C.L., Hik, D.S., Hill, S.J., Hopkins, T., Huang, S., Koane, B., Laird-Hopkins, B., Laukkanen, L., Lewis, O.T., Milne, S., Mwesige, I., Nakamura, A., Nell, C.S., Nichols, E., Prokurat, A., Sam, K., Schmidt, N.M., Slade, A., Slade, V., Suchanková, A., Teder, T., van Nouhuys, S., Vandvik, V., Weissflog, A., Zhukovich, V., Slade, E.M. (2017). Higher predation risk for insect prey at low latitudes and elevations. Science 356:742–744. doi: 10.1126/science.aaj1631
Strauss, S.Y. & Zangerl, A.R. (2002). Plant-insect interactions in terrestrial ecosystems. In: Herrera, C.M. & Pellmyr, O. (Eds.), Plant-animal interactions: an evolutionary approach (pp. 77–106). Hoboken: Blackwell Publishing.
Yamawo, A., Hada, Y., Suzuki, N. (2012). Variations in direct and indirect defences against herbivores on young plants of Mallotus japonicus in relation to soil moisture conditions. Journal of Plant Research 125: 71–76. doi: 10.1007/s10265-011-0407-0
Yilmaz, A., Aksoy, V., Camlitepe, Y., Giurfa, M. (2014). Eye structure, activity rhythms, and visually-driven behavior are tuned to visual niche in ants. Frontiers in Behavioral Neuroscience 8: 1–9. doi: 10.3389/fnbeh.2014.00205
Downloads
Published
How to Cite
Issue
Section
License
Sociobiology is a diamond open access journal which means that all content is freely available without charge to the user or his/her institution. Users are allowed to read, download, copy, distribute, print, search, or link to the full texts of the articles in this journal without asking prior permission from the publisher or the author. This is in accordance with the BOAI definition of open access.
Authors who publish with this journal agree to the following terms:
- Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
- Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
- Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work (See The Effect of Open Access).