Abstract
Plants and ants engage in diverse mutualistic interactions that contribute to their adaptive fitness. However, the presence of ants in flowers can generate conflicts between plants and pollinators. These interactions are little studied in temperate grasslands, despite the ubiquitous interactions between ants and plants in this region. In this study, we investigated how the presence and mobility of Camponotus termitarius (Emery) ants on Eryngium chamissonis Urb. affect the frequency of insect visitation on the flowers of this plant. We constructed contrasts and tested using generalized linear mixed models (I) whether the presence of any organism in the inflorescences decreases insect visitation, (II) whether it is really the presence of ants that decreases visitor interaction, and (III) whether the ant behavior has a greater effect on potentially reducing visits. We showed that the interaction of ants with E. chamissonis affected the number of visits to flowers, mainly reducing the frequency of the two main groups, bees and flies. These effects were consistent regardless of the ants' behavior, indicating that the mere presence of these insects on flowers can alter the frequencies of floral visitors. Our work is one of the first to report the effects of the interaction between ants and flowers in temperate grasslands in southern South America. The observed effects may go beyond the simple risk of predation and competition for resources, involving broader ecological implications for this ant–plant interaction, including a negative impact on the reproduction of E. chamissonis.
Similar content being viewed by others
Data availability
Not applicable.
References
Agrawal S, Safarik S, Dickinson M (2014) The relative roles of vision and chemosensation in mate recognition of Drosophila melanogaster. J Exp Biol 217(15):2796–2805. https://doi.org/10.1242/jeb.105817
Andrade BO, Dröse W, Aguiar CAD et al (2023) 12,500+ and counting: biodiversity of the Brazilian Pampa. Front Biogeogr. https://doi.org/10.21425/F5FBG59288
Assunção MA, Torezan-Silingardi HM, Del-Claro K (2014) Do ant visitors to extrafloral nectaries of plants repel pollinators and cause an indirect cost of mutualism? Flora 209:244–249. https://doi.org/10.1016/j.flora.2014.03.003
Bates D, Mächler M, Bolker BM, Walker SC (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67(1):1–48. https://doi.org/10.18637/jss.v067.i01
Becker FG, Ramos RA, Moura LA (2007) Biodiversidade: Regiões da Lagoa do Casamento e dos Butiazais de Tapes, planície costeira do Rio Grande do Sul. Porto Alegre, Brazil, Brasília, DF
Belém SO, Guia BP, Campbell AJ et al (2020) Effects of ants (Hymenoptera: Formicidae) on flying insect visitor behaviour and fruit production in açaí palm (Euterpe oleracea Martius). Austral Entomol 59(3):612–618. https://doi.org/10.1111/aen.12458
Ben-Shachar MS, Lüdecke D, Makowski D (2020) “Effect size: estimation of effect size indices and standardized parameters. J Open Source Softw 5(56):2815. https://doi.org/10.21105/joss.02815
Benoit AD, Kalisz S (2020) Predator effects on plant-pollinator interactions, plant reproduction, mating systems, and evolution. Annu Rev Ecol Evol Syst 51:319–340. https://doi.org/10.1146/annurev-ecolsys-012120-094926
Bleil R, Blüthgen N, Junker RR (2011) Ant-plant mutualism in Hawai? Invasive ants reduce flower parasitism but also exploit floral nectar of the endemic shrub Vaccinium reticulatum (Ericaceae). Pac Sci 65(3):291–300. https://doi.org/10.2984/65.3.291
Calviño CI, Martínez SG, Downie SR (2008) The evolutionary history of Eryngium (Apiaceae, Saniculoideae): rapid radiations, long distance dispersals, and hybridizations. Mol Phylogenet Evol 46:1129–1150. https://doi.org/10.1016/j.ympev.2007.10.021
Campos RE (2010) Eryngium (Apiaceae) phytotelmata and their macroinvertebrate communities, including a review and bibliography. Hydrobiologia 652:311–328. https://doi.org/10.1007/s10750-010-0364-y
Campos RE, Fernández LA (2011) Coleopterans associated with plants that form phytotelmata in subtropical and temperate Argentina, South America. J Insect Sci 11:147. https://doi.org/10.1673/031.011.14701
Cardozo AL, Goldenberg R, Fiaschi P, Labiak P (2021) Eryngium (Apiaceae, Saniculoideae) in the state of Paraná, southern Brazil. Phytotaxa 507(1):1–50. https://doi.org/10.11646/phytotaxa.507.1.1
Cembrowski AR, Tan MG, Thomson JD, Frederickson ME (2014) Ants and ant scent reduce bumblebee pollination of artificial flowers. Am Nat 183:133–139. https://doi.org/10.1086/674101
Crawley MJ (2007) The R book. England, Chichester
Cuny MAC, Bourne ME, Dicke M, Poelman EH (2021) The enemy of my enemy is not always my friend: negative effects of carnivorous arthropods on plants. Funct Ecol 35(11):2365–2375
De Sousa-Lopes B, Calixto ES, Torezan-Silingardi HM et al (2020) Effects of ants on pollinator performance in a distylous pericarpial nectary-bearing Rubiaceae in Brazilian Cerrado. Sociobiology 67(2):173–185. https://doi.org/10.13102/sociobiology.v67i2.4846
Fernandez-Barrancos EP, Reid JL, Aronson J (2017) Tank bromeliad transplants as an enrichment strategy in southern Costa Rica. Restor Ecol 25(4):569–576. https://doi.org/10.1111/rec.12463
Fidelis A, Overbeck GE, Pillar VD, Pfadenhauer J (2009) The ecological value of Eryngium horridum in maintaining biodiversity in subtropical grasslands. Austral Ecol 34(5):558–566. https://doi.org/10.1111/j.1442-9993.2009.01959.x
Fox J, Weisberg S (2019) An R companion to applied regression, 3rd edn. Sage, Thousand Oaks CA
Gonçalves-Souza T, Brescovit AD, Rossa-Feres DDC, Romero GQ (2010) Bromeliads as biodiversity amplifiers and habitat segregation of spider communities in a Neotropical rainforest. J Arachnol 38(2):270–279. https://doi.org/10.1636/P09-58.1
Gonzálvez FG, Santamaría T, Corlett RT, Rodríguez-Gironés MA (2012) Flowers attract weaver ants that deter less effective pollinators. J Ecol 101(1):78–85. https://doi.org/10.1111/1365-2745.12006
Grether GF, Losin N, Anderson CN, Okamoto K (2009) The role of interspecific interference competition in character displacement and the evolution of competitor recognition. Biol Rev 84(4):617–635
Hansen DM, Müller CB (2009) Invasive ants disrupt gecko pollination and seed dispersal of the endangered plant Roussea simplex in Mauritius. Biotropica 41(2):202–208. https://doi.org/10.1111/j.1744-7429.2008.00473.x
Hartig F (2020) DHARma residual diagnostics for hierarchical (multi-level/mixed) regression models. 2020. R package version, v. 320.
Herrera CM (1987) Components of pollinator “quality”: comparative analysis of a diverse insect assemblage. Oikos 50(1):79–90. https://doi.org/10.2307/3565403
Higginson AD, Ruxton GD, Skelhorn J (2010) The impact of flower-dwelling predators on host plant reproductive success. Oecologia 164:411–421. https://doi.org/10.1007/s00442-010-1681-6
Hölldobler B, Wilson EO (2008) The superorganism: the beauty, elegance, and strangeness of insect societies. Cambridge
Ibarra-Isassi J, Oliveira PS (2018) Indirect effects of mutualism: ant–treehopper associations deter pollinators and reduce reproduction in a tropical shrub. Oecologia 186(3):691–701. https://doi.org/10.1007/s00442-017-4045-7
Ibarra-Isassi J, Sendoya SF (2016) Ants as floral visitors of Blutaparon portulacoides (A St-Hil) Mears (Amaranthaceae): an ant pollination system in the Atlantic Rainforest. Arthropod-Plant Interact 10(3):221–227. https://doi.org/10.1007/s11829-016-9429-9
Irwin RE, Bronstein JL, Manson JS, Richardson L (2010) Nectar robbing: ecological and evolutionary perspectives. Annu Rev Ecol Evol Syst 41:271–292
Joly AB (2005) Introdução À Taxonomia Vegetal. São Paulo
Juárez-Juárez B, Dáttilo W, Moreno CE (2023) Synthesis and perspectives on the study of ant-plant interaction networks: a global overview. Ecol Entomol 48:269–283. https://doi.org/10.1111/een.13227
Junker RR, Bleil R, Daehler CC, Blüthgen N (2010) Intra-floral resource partitioning between endemic and invasive flower visitors: consequences for pollinator effectiveness. Ecol Entomol 35(6):760–767. https://doi.org/10.1111/j.1365-2311.2010.01237.x
Lach L (2008) Argentine ants displace floral arthropods in a biodiversity hotspot. Divers Distrib 14(2):281–290. https://doi.org/10.1111/j.1472-4642.2007.00410.x
Laundré JW, Hernández L, Ripple WJ (2010) The landscape of fear: ecological implications of being afraid. Open Ecol J 3:1–7. https://doi.org/10.2174/1874213001003030001
Leonard AS, Dornhaus A, Papaj DR (2011) Flowers help bees cope with uncertainty: signal detection and the function of floral complexity. J Exp Biol 214(1):113–121. https://doi.org/10.1242/jeb.047407
Li J, Wang Z, Tan K et al (2014) Giant Asian honeybees use olfactory eavesdropping to detect and avoid ant predators. Anim Behav 97:69–76. https://doi.org/10.1016/j.anbehav.2014.08.015
Lindsey AH (1984) Reproductive biology of Apiaceae. I. Floral visitors to Thaspium and Zizia and their importance in pollination. Am J Bot 71(3):375–387. https://doi.org/10.1002/j.1537-2197.1984.tb12524.x
Miner MC, Wilson Rankin EE (2023) Bumble bee avoidance of Argentine ants and associated chemical cues. J. Insect Behav. 36:20–32. https://doi.org/10.1007/s10905-023-09815-w
Ness JH, Morris WF, Bronstein JL (2006) Integrating quality and quantity of mutualistic service to contrast ant species protecting Ferocactus wislizeni. Ecology 87(4):912–921. https://doi.org/10.1890/0012-9658(2006)87[912:IQAQOM]2.0.CO;2
Ohm JR, Miller TEX (2014) Balancing anti-herbivore benefits and anti-pollinator costs of defensive mutualists. Ecology 95(10):2924–2935. https://doi.org/10.1890/13-2309.1
Oleques SS, Souza-Chies TTD, Avila RS Jr (2021) Elucidating plant-pollinator interactions in South Brazilian grasslands: What do we know and where are we going? Acta Botanica Brasilica 35(3):323–338. https://doi.org/10.1590/0102-33062020abb0225
Oliveira PS (1997) The ecological function of extrafloral nectaries: herbivore deterrence by visiting ants and reproductive output in Caryocar brasiliense (Caryocaraceae). Funct Ecol 11:323–330. https://doi.org/10.1046/j.1365-2435.1997.00087.x
Palmer MS, Fieberg J, Swanson A et al (2017) A ‘dynamic’ landscape of fear: prey responses to spatiotemporal variations in predation risk across the lunar cycle. Ecol Lett 20(11):1364–1373. https://doi.org/10.1111/ele.12832
Pillar VP, Müller SC, Castilhos ZMS, Jacques AVÁ (2009) Campos Sulinos: Conservação e Uso Sustentável da Biodiversidade. Brazilia
Prugh LR, Sivy KJ, Mahoney PJ et al (2019) Designing studies of predation risk for improved inference in carnivore-ungulate systems. Biol Conserv 232:194–207. https://doi.org/10.1016/j.biocon.2019.02.011
R Development Core Team (2023) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Rico-Gray V, Oliveira PS (2007) The Ecology and evolution of ant-plant interactions. Chicago United States.
Rodríguez-Rodríguez MC, Jordano P, Valido A (2013) Quantity and quality components of effectiveness in insular pollinator assemblages. Oecologia 73(1):179–190. https://doi.org/10.1007/s00442-013-2606-y
Romero GQ, Antiqueira PA, Koricheva J (2011) A meta-analysis of predation risk effects on pollinator behaviour. PLoS ONE. https://doi.org/10.1371/journal.pone.0020689
Romero GQ, Koricheva J (2011) Contrasting cascade effects of carnivores on plant fitness: a meta-analysis. J Anim Ecol 80(3):696–704. https://doi.org/10.1111/j.1365-2656.2011.01808.x
Rosumek FB, Silveira FAO, Neves FS et al (2009) Ants on plants: a meta-analysis of the role of ants as plant biotic defenses. Oecologia 160(3):537–549. https://doi.org/10.1007/s00442-009-1309-x
Sendoya SF, Freitas AVL, Oliveira PS (2009) Egg-laying butterflies distinguish predaceous ants by sight. Am Nat 174(1):134–140. https://doi.org/10.1086/599302
Shantz HL (1954) The place of grasslands in the earth’s cover of vegetation. Ecology 35(2):142–145. https://doi.org/10.2307/1931110
Souza CS, Baronio GJ, Weirich CE et al (2020) Ants climb plants because they cannot swim: ant presence on flowers during the flood season reduces the frequency of floral visitors. Ecol Entomol 45(6):1337–1345. https://doi.org/10.1111/een.12917
Su W, Ma W, Zhang Q et al (2022) Honey bee foraging decisions influenced by pear volatiles. Agriculture 12(8):1074. https://doi.org/10.3390/agriculture12081074
Tsuji K, Hasyim A, Nakamura H, Nakamura K (2004) Asian weaver ants, Oecophylla smaragdina, and their repelling of pollinators. Ecol Res 19(6):669–673. https://doi.org/10.1111/j.1440-1703.2004.00682.x
Villamil N, Boege K, Stone GN (2019) Testing the Distraction Hypothesis: do extrafloral nectaries reduce ant-pollinator conflict? J Ecol 107(3):1377–1391. https://doi.org/10.1111/1365-2745.13135
Wanderley MGL, Shepherd GJ, Melhem TS, Giulietti AM, (2005) Flora fanerogâmica do Estado de São Paulo. Volume 4. São Paulo
Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer, New York
Acknowledgements
We thank Helena Romanowski and Viviane Ferro for laboratory support and other essential activities related to this research, the entire team of the Ant Ecology and Behavior Laboratory (LACEF/UFPel) for their assistance in the field expeditions, the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for promoting this research (process number 88887.667264/2022-00), and the Graduate Program in Animal Biology—UFRGS.
Author information
Authors and Affiliations
Contributions
AC, SFS, and DAC contributed to the conception and sampling design of the study. Material preparation and data collection were carried out by DAC, LMC, IMS, and NAA. The organization, data analysis, and preparation of the graphs were carried out by DAC, AC, and SFS. The first draft of the manuscript was written by DAC, and all authors commented on earlier versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
We declare that our work has no conflicts of interest. This study was supported by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) by a Brazilian government agency.
Additional information
Handling Editor: Abel Bernadou.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Carvalho, D.A., Costa, L.M., Silva, I.M. et al. Beyond nectar: exploring the effects of ant presence on the interaction of flower visitors of a rosette in grassland. Arthropod-Plant Interactions (2024). https://doi.org/10.1007/s11829-024-10049-6
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11829-024-10049-6