Foraging ants on the extrafloral nectaries repel nectar thieves but not the effective pollinator of Vigna luteola (Fabaceae) in a Mexican coastal sand dune
Keywords:ant-plant relationship, experimental manipulation, multitrophic interactions, mutualisms, Los Tuxtlas
While some studies have shown that ants that visit extrafloral nectaries may defend their host plants against potential herbivores, recent researches have shown that such ant-plant mutualism may be broken in some cases. For example, the presence of ants on plants could also drive away pollinators and seed dispersers. However, it is not yet known what mechanisms could favor that ant presence on plants does not affect other mutualistic interactions involving plants. In this work, we performed a series of field experiments to test the hypothesis that the presence of ants on EFNs located at the base of the inflorescences of Vigna luteola (Fabaceae) may have a negative effect on floral visitors but not on potential pollinators in a Mexican coastal sand dune. In general, we found that the presence of ants on the plants decreased the rate of flower visitation. However, we observed that the time of visitation of the effective pollinators the bee (Pseudocentron) sp. on the flowers was less compared to that of other floral visitors. This strategy may allow that ants cannot aggressively scare away the effective pollinators. In summary, we show that the effective pollinators of V. luteola present strategies that allow them to visit the flowers without being aggressively attacked by the ants that visit the extrafloral nectaries (EFNs). Therefore, the presence of ants on plants could have a dual function: protecting plants against potential herbivores as well as, filtering flowers against nectar thieves.
Aguirre, A., Coates, R., Cumplido-Barragán, G., Campos-Villanueva, A. & Díaz-Castelazo, C. (2013). Morphological characterization of extrafl oral nectaries and associated ants intropical vegetation of Los Tuxtlas, Mexico. Flora, 208: 147-156. doi: 10.1016/j.fl ora.2013.02.008.
Agulló , M. A., Brizuela, M. M., Hoc, P. S., Di Stilio, V. S., Palacios, R. A., Genise, J. & Hazeldine, P. (1993). Relación unidad de polinización - visitantes florales en Vigna luteola (Leguminosae, Phseoleae). Boletín de la Sociedad Argentina de Botá nica, 29: 131-138.
Altshuler, D. (1999). Novel interactions of non-pollinating ants with pollinators and fruit consumers in a tropical forest. Oecologia, 119: 600-606. doi:10.1007/s004420050825.
Apple, J.L. & Feener, D.H. (2001). Ant visitation of extrafloral nectaries of Passiflora: the effects of nectary attributes and ant behavior on patterns in facultative ant-plant mutualisms. Oecologia, 127 (3): 409-416. doi: 10.1007/s004420000605.
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, 209(5-6): 244-249. doi 10.1016/j.fl ora.2014.03.003.
Barônio, G.J. & Del-Claro, K.(2018). Increase in ant density promotes dual effects on bee behaviour and plant reproductive performance. Arthropod-Plant Interactions, 12: 201-213. doi: 10.1007/s11829-017-9573-x.
Byk, J. & Del-Claro, K. (2011). Ant–plant interaction in the Neotropical savanna: direct beneficial effects of extrafloral nectar on ant colony fi tness. Population Ecology, 53:327-332. doi: 10.1007/s10144-010-0240-7.
Dáttilo, W., Aguirre, A., Flores-Flores, R.V., Fagundes, R., Lange, D., Garcia-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., Aguirre, A., De La Torre, L.P., Kaminski, L.A., García-Chavez, J.& Rico-Gray, V. (2016). Trait-mediated indirect interactions of ant shape on the attack of caterpillars and fruits. Biology Letters, 12: 1-4. doi: 10.1098/rsbl.2016.0401
De Souza, J.M.T., Snak, C. & Varassin, I.G. (2017). Floral divergence and temporal pollinator partitioning in two synchronopatric species of Vigna (Leguminosae Papilionoideae). Arthropod-Plant Interactions, 11(3): 285-297. doi: 10.1007/s11829-017-9498-4.
de Vega, C., Arista, M., Ortiz, P.L., Herrera, C.M. & Talavera, S. (2009). The ant-pollination system of Cytinus hypocistis (Cytinaceae), a Mediterranean root holoparasite. Annals of Botany, 103(7): 1065-1075. doi: 10.1093/aob/mcp049.
Del-Claro, K., Rico-Gray, V., Torezan-Silingardi, H. M., Alves-Silva, E., Fagundes, R., Lange, D., Dáttilo, W., Vilela, A., Aguirre, A. & Rodríguez-Morales, D. (2016). Loss and gains in ant-plant interactions mediated by extrafl oral nectar: fidelity, cheats, and lies. Insectes Sociaux, 63:207-221. doi: 10.1007/s00040-016-0466-2.
Delgado-Salinas, A., Thulin, M., Pasquet, R., Weeden, N. & Lavin, M (2011). Vigna (Leguminosae) sensu lato: the names and identities of the American segregate genera. American Journal of Botany, 98: 1694-1715. doi:10.3732/ajb.1100069.
Elias, TS. (1983). Extrafloral nectaries: their structure and distribution. In B. Bentley, T. Elias (Eds.), The biology of nectaries (pp. 174–203). New York: Columbia University Press.
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.
Gonzalez, A. M., & Marazzi, B. (2018). Extrafloral nectaries in Fabaceae: filling gaps in structural and anatomical diversity in the family. Botanical Journal of the Linnean Society, 187:26-45. doi: 10.1093/botlinnean/boy004.
González-Soriano, E., Dirzo, R., & Vogt, R.C. (1997). Historia Natural de Los Tuxtlas: México, D.F. UNAM-CONABIO. Heil, M.(2011). Nectar: generation, regulation and ecological functions. Trends in Plant Science, 16: 191-200. doi: 10.1016/j.tplants.2011.01.003.
Hernández-Cumplido, J., Forter, B., Moreira, X., Heil, M. & Benrey, B.(2016). Induced floral and extrafloral néctar production affect ant-pollinator interactions and plant fitness. Biotropica, 48: 342-348. doi: 10.1111/btp.12283.
Ibarra-Isassi, J. & Oliveira, P.S. (2018). Indirect effects of mutualism: ant–treehopper associations deter pollinators and reduce reproduction in a tropical shrub. Oecologia, 186(3): 691-701. doi: 10.1007/s00442-017-4045-7.
Jones, I. M., Koptur, S., & Peña, J. E. (2017). Exploring whether and how ants (Hymenoptera: Formicidae) affect reproductive fitness in Senna mexicana var. chapmanii (Fabaceae). Florida Entomologist, 100: 539-545. doi 10.1653/024.100.0308.
Koptur, S. 1984. Experimental evidence for defense of Inga (Mimosoideae) saplings by ants.Ecology, 65: 1787-1793.
Koptur, S. (1992a). Extrafl oral nectary, mediated interactions between insects and plants. In E.A. Bernays (Ed.), Insect-Plant Interactions. CRC Press.
Koptur , S. (1992b). Plants with extrafloral nectaries and ants in Everglades habitats. The Florida Entomologist, 75: 38-50. doi: 10.2307/3495479.
Koptur, S., Pascale, W. & Zuriany, O. (2010). Ants and plants with extrafloral nectaries in fire successional habitats on Andros (Bahamas). Florida Entomologist, 93: 90-99. doi: 10.1653/024.093.0112.
Luna, P., García-Chávez, J.H. & Dáttilo, W.(2018). Complex foraging ecology of the red harvester ant and its effect on the soil seed bank. Acta Oecologica, 86: 57-65. doi: 10.1016/j.actao.2017.12.003.
Marazzi, B., Bronstein, J. L., & Koptur, S. (2013). The diversity, ecology and evolution of extrafl oral nectaries: Current perspectives and future challenges. Annals of Botany, 111:1243–1250. doi: 10.1093/aob/mct109.
McKey, D.(1989). Interactions between ants and leguminous plants. Stirton, C, H,, Zarucchi, J, L ed (s). Advances in legume biology. Monographs in Systematic Botany from the Missouri Botanical Garden, 29: 673-718.
Nascimento, E. & Del-Claro, K. (2010). Ant visitation to extrafloral nectaries decreases herbivory and increases fruit set in Chamaecrista debilis (Fabaceae) in a Neotropical savanna. Flora, 205: 754-756. doi: 10.1016/j.fl ora.2009.12.040.
Ojeda, F.S., Hoc, P.S., García, A. & Teresa, M. (2013). Morphology of seeds and seedlings of four species of Vigna savi (Leguminosae, Phaseolinae). Acta Botanica Brasilica, 27: 483-489.
Ojeda, F.S., Hoc, P.S., Galati, B.G. & García, M.T.A. (2014). Ontogeny of the extrafloral nectaries of Vigna adenantha (Leguminosae, Phaseolae) and its relation with floral development. Botanical Studies, 55:74.
Oliveira, P.S., 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). Functional Ecology, 13: 623-631. doi: 10.1046/j.1365-2435.1999.00360.x.
Pascal, L.M., Motte-Florac, E.F. & McKey, D.B. (2000) Secretory structures on the leaf rachis of Caesalpinieae and Mimosoideae (Leguminosae): implications for the evolution of nectary glands. American Journal of Botany, 87:327–338 doi: 10.2307/2656628.
Pasquet, R.S. (2004). New Synonyms of Vigna luteola (Jacq.) Benth. (Leguminosae - Papilionoideae - Phaseoleae). Kew Bulletin, 59: 637. doi: 10.2307/4119438.
Pringle, E.G., Dirzo, R. & Gordon, D.M.(2012). Plant defense, herbivory, and the growth of Cordia alliodora trees and their symbiotic Azteca ant colonies. Oecologia, 170: 677-685. doi: 10.1007/s00442-012-2340-x.
R Development Core Team. (2016). R: A language and environment for statistical computing, version 3.3.0. R Foundation for Statistical Computing, Vienna Austria. Retrieved from https://www.r-project.org/.
Rico-Gray, V. & Oliveira, P.S. (2007). The ecology and evolution of ant-plant interactions. Chicago: The University of Chicago Press, 331 p.
Standley, P.C. & Steyermark, J.A. (1946). Flora of Guatemala. Vol. 24, Part V. Chicago Natural History Museum.
How to Cite
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).