Negative effects of ant-plant interaction on pollination: costs of a mutualism




mutualism, insect-plant interactions, pollination, foraging behavior


The mutualism of ants and extrafloral nectary (EFN)-bearing plants is known to reduce rates of herbivory. However, ants may have negative impacts on other mutualisms such as pollination, constituting an indirect cost of a facultative mutualism. For instance, when foraging on or close to reproductive plant parts ants might attack pollinators or inhibit their visits. We tested the hypothesis that ants on EFN-bearing plants may negatively influence pollinator behavior, ultimately reducing plant fitness (fruit set). The study was done in a reserve at Brazilian savannah using the EFN-bearing plant Banisteriopsis malifolia (Malpighiaceae). The experimental manipulation was carried out with four groups: control (free visitation of ants), without ants (ant-free branches), artificial ants (isolated branches with artificial ants on flowers) and plastic circles (isolated branches with plastic circles on flowers). We made observations on flower visitors and their interactions, and measured fruit formation as a proxy for plant fitness. Our results showed that pollinators hesitated to visit flowers with artificial ants, negatively affecting pollination, but did not hesitate to visit flowers with plastic circles, suggesting that they recognize the specific morphology of the ants. Pollinators spent more time per flower on the ant-free branches, and the fruiting rate was lower in the group with artificial ants. Our results confirm an indirect cost in this facultative mutualism, where the balance between these negative and positive effects of ants on EFN-bearing plants are not well known.


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Aguirre-Jaimes, A., Dáttilo, W., Rodríguez-Morales, D., Canchola-Orozco, S., Cocoletzi, E., Coates, R., Angeles, G. (2018). Foraging ants on the extrafloral nectaries repel nectar thieves but not the effective pollinator of Vigna luteola (Fabaceae) in a Mexican coastal sand dune. Sociobiology, 65: 621-629. doi: 10.13102/sociobiology.v65i4.3466

Almeida A.M., Figueiredo R.A. (2003). Ants visit nectaries of Epidendrum denticulatum (Orchidaceae) in Brazilian rainforest: effects on herbivory and pollination. Brazilian Journal of Biology, 63: 551-558. doi: 10.1590/S1519-69842 003000400002

Altshuler, D.L. (1999). Novel interactions of non-pollinating ants with pollinators and fruit consumers in a tropical forest. Oecologia, 119: 600-606. doi: 10.1007/s004420050825

Alvares, C.A., Stape, J.L., Sentelhas, P.C., De Moraes Gonçalves, J.L., Sparovek, G. (2013). Köppen’s climate classification map for Brazil. Meteorologische Zeitschrift, 22: 711-728. doi: 10.1127/0941-2948/2013/0507

Alves-Silva, E. (2011). Post Fire Resprouting of Banisteriopsis malifolia (Malpighiaceae) and the Role of Extrafloral Nectaries on the Associated Ant Fauna in a Brazilian Savanna. Sociobiology, 58: 327-339. doi: 10.6084/M9.FIGSHARE.155660

Amorim, F.W., Galetto, L., Sazima, M. (2013). Beyond the pollination syndrome: Nectar ecology and the role of diurnal and nocturnal pollinators in the reproductive success of Inga sessilis (Fabaceae). Plant Biology, 15: 317-327. doi: 10.11 11/j.1438-8677.2012.00643.x

Angeloni, F., Ouborg, N.J., Leimu, R. (2011). Meta-analysis on the association of population size and life history with inbreeding depression in plants. Biological Conservation, 144: 35-43. doi: 10.1016/j.biocon.2010.08.016

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: 244-249. doi: 10.1016/j.flora.2014.03.003

Ballantyne, G., Willmer, P. (2012). Floral visitors and ant scent marks: Noticed but not used? Ecological Entomology, 37: 402-409. doi: 10.1111/j.1365-2311.2012.01378.x

Barônio, G.J., Del-Claro, K. (2017). 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

Barroso, G.M., Morim, M.P., Peixoto, A.L., Ichaso, C.L.F., Barroso, D. (2004). Frutos e sementes: morfologia aplicada à sistemática de dicotiledôneas. Viçosa: UFV. 443 p

Blüthgen, N., Fiedler, K. (2004). Preferences for sugars and amino acids and their conditionality in a diverse nectarfeeding ant community. Journal of Animal Ecology, 73: 155-166. doi: 10.1111/j.1365-2656.2004.00789.x

Blüthgen, N., Gebauer, G., Fiedler, K. (2003). Disentangling a rainforest food web using stable isotopes: Dietary diversity in a species-rich ant community. Oecologia, 137: 426-435. doi: 10.1007/s00442-003-1347-8

Bronstein, J.L. (2021). The Gift That Keeps on Giving: Why Does Biological Diversity Accumulate Around Mutualisms? In K. Del-Claro & H.M. Torezan-Silingardi (Eds.), Plant-Animal Interactions (pp. 283-306) Springer International Publishing, Cham. doi: 10.1007/978-3-030-66877-8_11

Brooks, M.E.J.K.K., van Benthem, K., Magnusson, A., Berg, C.W., Nielsen, A., Skaug, H.J., Maechler, M., Bolker, B.M. (2017). glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. The R Journal, 9: 378-400. doi: 10.32614/RJ-2017-066

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: 33-38. doi: 10.1007/s10211-010-0071-8

Calixto, E.S., Lange, D., Moreira, X., Kleber, D. (2021a). Plant species-specificity of ant-plant mutualistic interactions: Differential predation of termites by Camponotus crassus on five species of extrafloral nectaried plants. Biotropica In press, 00, 1-9. doi: 10.1111/btp.12991

Calixto, E.S., Lange, D., Del-Claro, K. (2018). Protection mutualism: an overview of ant-plant interactions mediated by extrafloral nectaries. Oecologia Australis, 22: 410-425. doi: 10.4257/oeco.2018.2204.05

Calixto, E.S., Novaes, L.R., dos Santos, D.F.B., Lange, D., Moreira, X., Del-Claro, K. (2021b). Climate seasonality drives ant-plant-herbivore interactions via plant phenology in na extrafloral nectary-bearing plant community. Journal of Ecology, 109: 639-651. doi: 10.1111/1365-2745.13492

Cembrowski, Adam R., Tan, M.G., Thomson, J.D., Frederickson, M.E. (2014). Ants and ant scent reduce bumblebee pollination of artificial flowers. The American Naturalist, 183: 133-139. doi: 10.1086/674101

Dafni, A. (1992). Pollination ecology: A practical approach. Oxford: Oxford University Press, 250. doi: 10.1046/j.1420-9101.1993.6050776.x

Dáttilo, W., Aguirre, A., De La Torre, P.L., Kaminski, L.A., García-Chávez, J., Rico-Gray, V. (2016). Trait-mediated indirect interactions of ant shape on the attack of caterpillars and fruits. Biology Letters, 12: 12-15. doi: 10.1098/rsbl.2016.0401

Davidson, D.W., Cook, S.C., Snelling, R.R., Chua, T.H. (2003). Explaining the abundance of ants in lowland tropical rainforest canopies. Science, 300: 969-972. doi: 10.1126/science.1082074

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: 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., 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

Del-Claro, K., Rodriguez-Marales, D., Calixto, E.S., Martins, A.S., Torezan-Silingardi, H.M. (2019). Ant pollination of Paepalanthus lundii (Eriocaulaceae) in Brazilian savanna. Annals of Botany, 123: 1159-1165. doi: 10.1093/aob/mcz021

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

Fox, J. & Weisberg, S. (2011). An R companion to applied regression, California: Sage, 472 p.

Franzon, R.C., Gonçalves, R. da S., Antunes, L.E.C., Raseira, M. do C.B. (2010). Propagação vegetativa de genótipos de pitangueira (Eugenia uniflora L.) do sul do brasil por enxertia de garfagem. Revista Brasileira de Fruticultura, 32: 262-267. doi: 10.1590/S0100-29452010005000003

Fuster, F., Kaiser-Bunbury, C. N., Traveset, A. (2020). Pollination effectiveness of specialist and opportunistic nectar feeders influenced by invasive alien ants in the Seychelles. American Journal of Botany, 107: 957-969. doi: 10.1002/ajb2.1499

Galen, C. (1999). Flowers and enemies: predation by nectarthieving ants in relation to variation in floral form of an alpine wildflower, Polemonium viscosum. Oikos, 85: 426-434. doi: 10.2307/3546692

Gonzálvez, F.G., Santamaría, L., Corlett, R.T., Rodríguez-Gironés, M.A. (2013). Flowers attract weaver ants that deter less effective pollinators. Journal of Ecology, 101: 78-85. doi: 10.1111/1365-2745.12006

Gottsberger, G. & Silberbauer-Gottsberger, I. (2006). Life in the Cerrado: a South American Tropical Seasonal Ecosystem. Ulm: Reta Verlag, 277 p.

Hanna, C., Naughton, I., Boser, C., Alarcón, R., Hung, K.J., Holway, D. (2015). Floral visitation by the Argentine ant reduces bee visitation and plant seed set. Ecology, 96: 222-230. doi: 10.1890/14-0542.1

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

Holland J.N., Chamberlain S.A., Miller T.E.X. (2011). Consequences of ants and extrafloral nectar for a pollinating seed-consuming mutualism: ant satiation, floral distraction or plant defense? Oikos, 120: 381-388. doi: 10.1111/j.1600-0706.2010.18958.x

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: 691-701. doi: 10.1007/s00442-017-4045-7

Junker, R., Chung, A.Y.C., Blüthgen, N. (2007). Interaction between flowers, ants and pollinators: additional evidence for floral repellence against ants. Ecological Research, 22: 665-670. doi: 10.1007/s11284-006-0306-3

Koptur, S. (2005). Nectar as fuel for plant protectors. In F.L. Wackers, P.C.J. van Rijn, & J. Bruin (Eds.). Plant-Provided Food for Carnivore Insects (pp. 75-108). Cambridge University Press. doi: 10.1017/CBO9780511542220.004

Kwak, M.M., Jennersten, O. (1986). The significance of pollination time and frequency and of purity of pollen loads for seed set in Rhinanthus angustifolius (Scrophulariaceae) and Viscaria vulgaris (Caryophyllaceae). Oecologia, 70: 502-507.

Kuriakose, G., Sinu, P.A., Shivanna, K.R. (2018). Ant pollination of Syzygium occidentale, an endemic tree species of tropical rain forests of the Western Ghats, India. Arthropod-Plant Interactions, 12: 647-655. doi: 10.1007/s11829-018-9613-1

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

Lange, D., Calixto, E.S., Rosa, B.B., Sales, T.A., Del-Claro, K. (2019). Natural history and ecology of foraging of the Camponotus crassus Mayr, 1862 (Hymenoptera: Formicidae). Journal of Natural History, 53: 1737-1749. doi: 10.1080/00222933.2019.1660430

Lenth, R. (2020). emmeans: Estimated Marginal Means, aka Least-Squares Means [ Document]. R package version 1.3.0. (accessed date: 25 May, 2021)

Melati, B.G., Leal, L.C. (2018). Aggressive bodyguards are not always the best: Preferential interaction with more aggressive ant species reduces reproductive success of plant bearing extrafloral nectaries. PLoS ONE, 13: e0199764. doi: 10.1371/journal.pone.0199764

Nascimento, E.A., Del-Claro, K. (2010). Ant visitation to extrafloral nectaries decreases herbivory and increases fruit set in Chamaecrista debilis (Fabaceae) in a Neotropical savanna. Flora: Morphology, Distribution, Functional Ecology of Plants, 205: 754-756. doi: 10.1016/j.flora.2009.12.040

Ness, J.H. (2006). A mutualism’s indirect costs: The most aggressive plant bodyguards also deter pollinators. Oikos, 113: 506-514. doi: 10.1111/j.2006.0030-1299.14143.x

Ollerton, J., Winfree, R., Tarrant, S. (2011). How many flowering plants are pollinated by animals? Oikos, 120: 321-326. doi: 10.1111/j.1600-0706.2010.18644.x

R Core Team (2020). R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. 2630 p

Redmond, A.M., Robbins, L.E., Travis, J. (1989). The effects of pollination distance on seed production in three populations of Amianthium muscaetoxicum (Liliaceae). Oecologia, 79: 260-264. doi: 10.1007/BF00388486

Romero, G.Q., Koricheva, J. (2011). Contrasting cascade effects of carnivores on plant fitness: A meta-analysis. Journal of Animal Ecology, 80: 696-704. doi: 10.1111/j.1365-2656.2011.01808.x

Rosumek, F.B., Silveira, F.A.O.O., Neves, F.D.S., Newton, N.P., 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: 537-549. doi: 10.1007/s00442-009-1309-x

Santos A.T.F., Leal L.C. (2019). My plant, my rules: bodyguard ants of plants with extrafloral nectaries affect patterns of pollinator visits but not pollination success. Biological Journal of the Linnean Society, 126: 158-167. doi: 10.1093/biolinnean/bly165

Sinu, P.A., Sibisha, V.C., Reshmi, M.V.N., Reshmi, K.S., Jasna, T.V., Aswathi, K., Megha, P.P. (2017). Invasive ant (Anoplolepis gracilipes) disrupts pollination in pumpkin. Biological Invasions, 19: 2599-2607. doi: 10.1007/s10530-017-1470-9

Sousa-Lopes, B., Calixto, E.S., Torezan-Silingardi, H., Del-Claro, K. (2020). Effects of ants on pollinator performance in a distylous pericarpial nectary-bearing Rubiaceae in Brazilian Cerrado. Sociobiology, 67: 173-185. doi: 10.13102/sociobiology. v67i2.4846

Torezan-Silingardi, H.M. (2007). A influência dos herbívoros dos polinizadores e das características fenológicas sobre a frutificação de espécies da família Malpighiaceae em um cerrado de Minas Gerais. Ribeirão Preto: USP, 172 p

Torezan-Silingardi, H.M., Silberbauer-Gottsberger, I., Gottsberger, G. (2021). Pollination Ecology: Natural History, Perspectives and Future Directions. In: K. Del-Claro & H.M. Torezan-Silingardi (Eds.). Plant-Animal Interactions (pp. 119-174). Springer International Publishing, Cham. doi: 10.10 07/978-3-030-66877-8_6

Trager, M.D., Bhotika, S., Hostetler, J.A., Andrade, G. V., Rodriguez-Cabal, M.A., Mckeon, C.S., Osenberg, C.W., Bolker, B.M. (2010). Benefits for plants in ant-plant protective mutualisms: A meta-analysis. PLoS ONE, 5: e14308. doi: 10.1371/journal.pone.0014308

Tsuji, K., Hasyim, A., Nakamura, H., Nakamura, K. (2004). Assian weaver ants, Oecophylla smaradigma, and their repelling of pollinators. Ecological Research, 19: 669-673. doi: 10.1111/j.1440-1703.2004.00682.x

Unni, A.P., Mir, S.H., Rajesh, T.P., Ballullaya, U.P., Jose, T., Sinu, P.A. (2021). Native and invasive ants affect floral visits of pollinating honey bees in pumpkin flowers (Cucurbita maxima). Scientific Reports, 11: 4781. doi: 10.1038/s41598-021-83902-w

Venables, W.N., Ripley, B.D. (2003). Modern Applied Statistics with S., 4th ed. New York: Springer, 498 p

Vilela, A.A., Del Claro, 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, 12: 215-227. doi: 10.1007/s11829-017-9572-y

Vilela, A.A., Torezan-Silingardi, H.M., Del-Claro, K. (2014). Conditional outcomes in ant-plant-herbivore interactions influenced by sequential flowering. Flora: Morphology, Distribution, Functional Ecology of Plants, 209: 359-366. doi: 10.1016/j.flora.2014.04.004

Villamil, N., Boege, K., Stone, G. (2020). Ant guards influence the mating system of their plant hosts by altering pollinator behaviour. bioRxiv, preprint. doi: 10.1101/2020.02.11.943431

Villamil, N., Boege, K., Stone, G.N. (2019). Testing the Distraction Hypothesis: Do extrafloral nectaries reduce antpollinator conflict? Journal of Ecology, 107: 1377-1391. doi: 10.1111/1365-2745.13135

Villamil, N., Boege, K., Stone, G.N. (2018). Ant-pollinator conflict results in pollinator deterrence but no nectar tradeoffs. Frontiers in Plant Science, 9: 1-14. doi: 10.3389/fpls.2018.01093

Vogel, S. (1990). History of the Malpighiaceae in the light of pollination ecology. Memoirs of the New York Botanical Garden, 55: 130-142.

Wagner, D. (2000). Pollen viability reduction as a potential cost of ant association for Acacia constricta (Fabaceae). American Journal of Botany, 87: 711-715. doi: 10.2307/2656857

Willmer, P.G., Nuttman, C. V., Raine, N.E., Stone, G.N., Pattrick, J.G., Henson, K., Stillman, P., McIlroy, L., Potts, S.G., Knudsen, J.T. (2009). Floral volatiles controlling ant behaviour. Functional Ecology, 23: 888-900. doi: 10.1111/j.1365-2435.2009.01632.x




How to Cite

Nogueira, R. R., Santos, D. F. B., Calixto, E. S., Torezan-Silingardi, H. M. ., & Del-Claro, K. (2021). Negative effects of ant-plant interaction on pollination: costs of a mutualism. Sociobiology, 68(4), e7259.



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