Ant sharing by plant species bearing extrafloral nectaries has a low impact on plant herbivory in a tropical system
Corresponding Author
Caroline Souza
Centro de Ciências Naturais e Humanas, Universidade Federal do ABC, São Bernardo do Campo, São Paulo, Brazil
Correspondence
Anselmo Nogueira
Email: [email protected]; [email protected]
Search for more papers by this authorLaura C. Leal
Departamento de Ecologia e Biologia Evolutiva, Universidade Federal de São Paulo, Diadema, São Paulo, Brazil
Search for more papers by this authorFabrício B. Baccaro
Departamento de Biologia, Instituto de Biologia, Universidade Federal do Amazonas, Manaus, Amazonas, Brazil
Search for more papers by this authorPedro J. Bergamo
Instituto de Biociências, Universidade Estadual Paulista, Rio Claro, São Paulo, Brazil
Search for more papers by this authorJudith L. Bronstein
Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona, USA
Search for more papers by this authorPedro J. Rey
Departamento de Biología Animal, Biología Vegetal y Ecología, Universidad de Jaén, Jaén, Spain
Search for more papers by this authorCorresponding Author
Anselmo Nogueira
Centro de Ciências Naturais e Humanas, Universidade Federal do ABC, São Bernardo do Campo, São Paulo, Brazil
Correspondence
Anselmo Nogueira
Email: [email protected]; [email protected]
Search for more papers by this authorCorresponding Author
Caroline Souza
Centro de Ciências Naturais e Humanas, Universidade Federal do ABC, São Bernardo do Campo, São Paulo, Brazil
Correspondence
Anselmo Nogueira
Email: [email protected]; [email protected]
Search for more papers by this authorLaura C. Leal
Departamento de Ecologia e Biologia Evolutiva, Universidade Federal de São Paulo, Diadema, São Paulo, Brazil
Search for more papers by this authorFabrício B. Baccaro
Departamento de Biologia, Instituto de Biologia, Universidade Federal do Amazonas, Manaus, Amazonas, Brazil
Search for more papers by this authorPedro J. Bergamo
Instituto de Biociências, Universidade Estadual Paulista, Rio Claro, São Paulo, Brazil
Search for more papers by this authorJudith L. Bronstein
Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona, USA
Search for more papers by this authorPedro J. Rey
Departamento de Biología Animal, Biología Vegetal y Ecología, Universidad de Jaén, Jaén, Spain
Search for more papers by this authorCorresponding Author
Anselmo Nogueira
Centro de Ciências Naturais e Humanas, Universidade Federal do ABC, São Bernardo do Campo, São Paulo, Brazil
Correspondence
Anselmo Nogueira
Email: [email protected]; [email protected]
Search for more papers by this authorAbstract
- Plant species bearing extrafloral nectaries (EFNs) may indirectly influence other plant species by sharing protective ants, potentially altering herbivory levels. However, the propagation of indirect effects in this type of mutualism has seldom been investigated.
- We investigated indirect effects via ant sharing among 21 EFN-bearing plant species of the tribe Bignonieae distributed on 28 plots in the central Brazilian Amazon. We used an ecological network index to quantify potential indirect effects among plant species through shared dominant and subordinate ant species.
- Plant species that were more attractive to ants (promoter species) had the highest potential to indirectly influence ant visitation to less attractive plant species (receptor species) in the community, primarily through changes in the attraction of dominant ant species. However, these potential indirect effects did not result in significant differences in herbivory patterns among the studied plants. Ant attendance and herbivory levels were similar among promoter species, neighbouring plants, and non-neighbouring plants. Unlike other mutualisms involving plants (e.g., pollination), the indirect effects among plant species that share protective ants had limited consequences. The low levels of herbivory and the small foraging areas of shared ant defenders could be responsible for the observed limited impact of indirect interactions among plant species in this system.
- Synthesis: This study demonstrates that plant species with EFNs can indirectly influence other plant species through ant sharing. The attractiveness of certain plants to ants enables them to affect the ant visitation patterns of less attractive plants in the community. However, these indirect effects did not significantly alter herbivory levels among plants. Overall, this study advances ecological understanding by showing that the sharing of protective ants among plant species can in some cases confer limited costs and benefits, leading indirect interactions to have minimal impact on herbivory patterns.
CONFLICT OF INTEREST STATEMENT
The authors declare that there is no conflict of interest.
Open Research
DATA AVAILABILITY STATEMENT
The data are available on FigShare: https://doi.org/10.6084/m9.figshare.26496472.v2 (Souza et al., 2024).
Supporting Information
Filename | Description |
---|---|
jec14394-sup-0001-DataS1.docxWord 2007 document , 1.6 MB |
Table S1. Model comparison describing the variation of promoter and receptor degree of plant species considering the entire ant assemblage related to the average number of active nodes (NAN) and the secretory area of extrafloral nectaries (SA). Table S2. Model comparison describing the variation of promoter and receptor degree of plant species partitioned by the dominant ant species related to the average number of active nodes (NAN) and the secretory area of extrafloral nectaries (SA). Table S3. Model comparison describing the variation of promoter and receptor degree of plant species partitioned by the subordinate ant species related to the average number of active nodes (NAN) and secretory area of extrafloral nectaries (SA). Figure S1. Ant recruitment on plants (median) shows that dominant ant species have significantly higher average recruitment per active EFN than subordinate ants. Figure S2. Absence of a relationship between the number of active nodes and the receptor degree of plant species relative to (a) the entire ant assemblage, (b) dominant ant species partition, and (c) the subordinate ant species partition. Figure S3. Partial plots showing the proportion of leaflets consumed and the promoter degree concerning (a) all shared ants and (b) the shared dominant ant species; likewise, partial plots showing the average percentage of herbivory and (c) receptor degree for all visiting ant species and (d) the promoter degree for subordinate ant species. Figure S4. (a) The probability of interaction and (b) the number of dominant and subordinate ant species feeding on EFN of Bignonieae plants did not differ among the promoter plant species, neighbour plants, and non-neighbour plants in the plot scale evaluation. Figure S5. Plot showing that the mean percentage of damaged leaf area per plant did not differ between promoter, neighbour, and non-neighbour plants. Figure S6. The feeding strategies and ability to evade ant predation vary among herbivores. |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
REFERENCES
- Addicott, J. F. (1978). Competition for mutualists: Aphids and ants. Canadian Journal of Zoology, 56(10), 2093–2096.
10.1139/z78-283 Google Scholar
- Apple, J., & Feener, D. (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, 409–416.
- Armbruster, W. S., & McGuire, A. D. (1991). Experimental assessment of reproductive interactions between sympatric Aster and Erigeron (Asteraceae) in interior Alaska. American Journal of Botany, 78, 1449–1457.
- Arnan, X., Gaucherel, C., & Andersen, A. N. (2011). Dominance and species co-occurrence in highly diverse ant communities: A test of the interstitial hypothesis and discovery of a three-tiered competition cascade. Oecologia, 166, 783–794.
- Baccaro, F. B., & Ferraz, G. (2013). Estimating density of ant nests using distance sampling. Insectes Sociaux, 60, 103–110.
- Baccaro, F. B., Ketelhut, S. M., & de Morais, J. W. (2010). Resource distribution and soil moisture content can regulate bait control in an ant assemblage in central Amazonian forest. Austral Ecology, 35(3), 274–281.
10.1111/j.1442-9993.2009.02033.x Google Scholar
- Barton, B. T., & Ives, A. R. (2014). Species interactions and a chain of indirect effects driven by reduced precipitation. Ecology, 95, 486–494.
- Bates, D., Mächler, M., Bolker, B., & Walker, S. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software, 67(1), 1–48.
- Bentley, B. L. (1977). Extrafloral nectaries and protection by pugnacious bodyguards. Annual Review of Ecology and Systematics, 8, 407–427.
- Bergamo, P. J., Traveset, A., & Lázaro, A. (2021). Pollinator-mediated indirect effects on plant fecundity revealed by network indices. The American Naturalist, 198, 734–749.
- Bergamo, P. J., Wolowski, M., Maruyama, P. K., Vizentin-Bugoni, J., Carvalheiro, L. G., & Sazima, M. (2017). The potential indirect effects among plants via shared hummingbird pollinators are structured by phenotypic similarity. Ecology, 98, 1849–1858.
- Boege, K., & Marquis, R. J. (2005). Facing herbivory as you grow up: The ontogeny of resistance in plants. Trends in Ecology & Evolution, 20, 441–448.
- Brooks, M. E., Kristensen, K., van Benthem, K. J., 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(2), 378–400.
- Buckley, R. C. (1987). Interactions involving plants, Homoptera, and ants. Annual Review of Ecology and Systematics, 18, 111–135.
- Carlo, T. A. (2005). Interspecific neighbors change seed dispersal pattern of an avian-dispersed plant. Ecology, 86, 2440–2449.
- Carlo, T. A., Collazo, J. A., & Groom, M. J. (2003). Avian fruit preferences across a Puerto Rican forested landscape: Pattern consistency and implications for seed removal. Oecologia, 134, 119–131.
- Caruso, C. M. (1999). Pollination of Ipomopsis aggregata (Polemoniaceae): Effects of intra vs. interspecific competition. American Journal of Botany, 86, 663–668.
- Carvalheiro, L. G., Biesmeijer, J. C., Benadi, G., Fründ, J., Stang, M., Bartomeus, I., Kaiser-Bunbury, C. N., Baude, M., Gomes, S. I. F., Merckx, V., Baldock, K. C. R., Bennett, A. T. D., Boada, R., Bommarco, R., Cartar, R., Chacoff, N., Dänhardt, J., Dicks, L. V., Dormann, C. F., … Kunin, W. E. (2014). The potential for indirect effects between co-flowering plants via shared pollinators depends on resource abundance, accessibility and relatedness. Ecology Letters, 17, 1389–1399.
- Cerdá, X., Arnan, X., & Retana, J. (2013). Is competition a significant hallmark of ant (Hymenoptera: Formicidae) ecology? Myrmecological News, 18, 131–147.
- Chauvel, A., Lucas, Y., & Boulet, R. (1987). On the genesis of the soil mantle of the region of Manaus, Central Amazonia, Brazil. Experientia, 43(3), 234–241.
10.1007/BF01945546 Google Scholar
- Cohen, J. (1988). Statistical power analysis for the behavioral sciences ( 2nd ed.). Lawrence Erlbaum Associates Publishers.
10.1046/j.1526-4610.2001.111006343.x Google Scholar
- Coley, P. D., & Barone, J. A. (1996). Herbivory and plant defences in tropical forests. Annual Review of Ecology and Systematics, 27, 305–335.
10.1146/annurev.ecolsys.27.1.305 Google Scholar
- Crawley, M. J. (1993). Herbivory, the dynamics of animal–plant interactions (p. 437). Blackwell Science Publications.
- Delabie, J. H. C. (2001). Trophobiosis between Formicidae and Hemiptera (Sternorrhyncha and Auchenorrhyncha): An overview. Neotropical Entomology, 30(4), 501–516.
10.1590/S1519-566X2001000400001 Google Scholar
- Engel, V., Fischer, M. K., Wäckers, F. L., & Völkl, W. (2001). Interactions between extrafloral nectaries, aphids and ants: Are there competition effects between plant and homopteran sugar sources? Oecologia, 129(4), 577–584.
- Erickson, J., Pereira, F. R., & Baccaro, F. (2021). Competitive interaction between two ant species facilitates egg hatching in yellow-spotted Amazon River turtles (Podocnemis unifilis). South American Journal of Herpetology, 20(1), 84–91.
10.2994/SAJH-D-19-00114.1 Google Scholar
- Fine, P. V. A., Metz, M. R., Lokvam, J., Mesones, I., Zuñiga, J. M. A., Lamarre, G. P. A., & Baraloto, C. (2013). Insect herbivores, chemical innovation, and the evolution of habitat specialization in Amazonian trees. Ecology, 94(8), 1764–1775.
- Flores-Flores, R. V., Aguirre, A., Anjos, D. V., Neves, F. S., Campo, R. I., & Dattilo, 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.
- Ghazoul, J. (2006). Floral diversity and the facilitation of pollination. Journal of Ecology, 94, 295–304.
- Guimarães, P., Pires, M. M., Jordano, P., Bascompte, J., & Thompson, J. N. (2017). Indirect effects drive coevolution in mutualistic networks. Nature, 550, 511–514.
- Itioka, T., Nomura, M., Inui, Y., & Inoue, T. (2000). Difference in intensity of ant defence among three species of Macaranga myrmecophytes in a Southeast Asian dipterocarp forest. Biotropica, 32, 318–326.
- Johnson, C. A., & Bronstein, J. L. (2019). Coexistence and competitive exclusion in mutualism. Ecology, 100, e02708.
- Johnson, S. D., Peter, C. I., Nilsson, L. A., & Agren, J. (2003). Pollination success in a deceptive orchid is enhanced by co-occurring rewarding magnet plants. Ecology, 84, 2919–2927.
- Katayama, N., Hembry, D. H., Hojo, M. K., & Suzuki, N. (2013). Why do ants shift their foraging from extrafloral nectar to aphid honeydew? Ecological Research, 28, 919–926.
- Kendall, L. K., Mola, J. M., Portman, Z. M., Cariveau, D. P., Smith, H. G., & Bartomeus, I. (2022). The potential and realized foraging movements of bees are differentially determined by body size and sociality. Ecology, 103(11), e3809.
- Lanan, M. (2014). Spatiotemporal resource distribution and foraging strategies of ants (Hymenoptera: Formicidae). Myrmecol News, 20, 53–70.
- Leal, I. R., Fischer, E., Kost, C., Tabarelli, M., & Wirth, R. (2006). Ant protection against herbivores and nectar thieves in Passiflora coccinea flowers. Ecoscience, 13(4), 431–438.
10.2980/1195-6860(2006)13[431:APAHAN]2.0.CO;2 Google Scholar
- Leal, L. C., Nogueira, A., & Peixoto, P. E. C. (2023). Which traits optimize plant benefits? Meta-analysis on the effect of partner traits on the outcome of an ant–plant protective mutualism. Journal of Ecology, 111(1), 263–275.
10.1111/1365-2745.14031 Google Scholar
- Lohmann, L. G. (2006). Untangling the phylogeny of neotropical lianas (Bignonieae, Bignoniaceae). American Journal of Botany, 93, 304–318.
- MacArthur, R., & Pianka, E. (1966). On optimal use of a patchy environment. American Naturalist, 100, 603–609.
- Martínez, D., García, D., & Herrera, J. M. (2014). Consistency and reciprocity of indirect interactions between tree species mediated by frugivorous birds. Oikos, 123, 414–422.
- Menge, B. A. (1995). Indirect effects in marine rocky intertidal interaction webs: Patterns and importance. Ecological Monographs, 65, 21–74.
- Menge, B. A. (1996). Detection of direct versus indirect effects: Were experiments long enough? The American Naturalist, 149(5), 801–823.
10.1086/286025 Google Scholar
- Muchhala, N., Johnsen, S., & Smith, S. D. (2014). Competition for hummingbird pollination shapes flower color variation among in Andean Solanaceae. Evolution, 68, 2275–2286.
- Müller, C. B., Adriaanse, I. C. T., Belshaw, R., & Godfray, H. C. J. (1999). The structure of an aphid-parasitoid community. Journal of Animal Ecology, 68, 346–370.
- Ness, J. H., Morris, W. F., & Bronstein, J. L. (2006). Integrating quality and quantity of mutualistic service to contrast ant species protecting Ferocactus wislizeni. Ecology, 87, 912–921.
- Nogueira, A., Baccaro, F. B., Leal, L. C., Rey, P. J., Lohmann, L. G., & Bronstein, J. L. (2020). Variation in the production of plant tissues bearing extrafloral nectaries explains temporal patterns of ant attendance in Amazonian understory plants. Journal of Ecology, 108, 1578–1591.
- Nogueira, A., El Ottra, J. H. L., Guimarães, E., Machado, S. R., & Lohmann, L. G. (2013). Trichome structure and evolution in Neotropical lianas. Annals of Botany, 7, 1331–1350.
- Nogueira, A., Guimarães, E., Machado, S. R., & Lohmann, L. G. (2012). Do extrafloral nectaries present a defensive role against herbivores in two species of the family Bignoniaceae in a Neotropical savanna? Plant Ecology, 213, 289–301.
- Nogueira, A., Rey, P. J., Alcantara, J., Feitosa, R. M., & Lohmann, L. G. (2015). Geographic mosaic of plant evolution: Extrafloral nectary variation mediated by ant and herbivore assemblages. PLoS One, 10, e0123806.
- Nogueira, A., Rey, P. J., Alcantara, J., & Lohmann, L. G. (2016). Evidence of between-population differences in natural selection on extra-floral nectaries of the shrub (Bignoniaceae). Botany, 94(3), 201–213.
10.1139/cjb-2015-0201 Google Scholar
- Parr, C., & Gibb, H. (2010). Competition and the role of dominant ants. In L. Lach, C. L. Parr, & K. L. Abbott (Eds.), Ant ecology (pp. 77–96). Oxford University Press.
- Parr, C. L. (2008). Dominant ants can control assemblage species richness in a south African savanna. Journal of Animal Ecology, 77, 1191–1198.
- Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D., & R Core Team. (2022). nlme: Linear and nonlinear mixed effects models. R package version 3.1-155.
- Pires, M. M., O'Donnell, J. L., Burkle, L. A., Díaz-Castelazo, C., Hembry, D. H., Yeakel, J. D., Newman, E. A., Medeiros, L. P., de Aguiar, M. A. M., & Guimarães, P. R. (2020). The indirect paths to cascading effects of extinctions in mutualistic networks. Ecology, 101, e03080.
- Pyke, G. H. (1984). Optimal foraging theory: A critical review. Annual Review of Ecology and Systematics, 15, 523–575.
- R Development Core Team. (2021). R: A language and environment for statistical computing. R Foundation for Statistical Computing.
- Rathcke, B. (1983). Competition and facilitation among plants for pollination. In L. Real (Ed.), Pollination biology (pp. 305–329). Academic Press.
10.1016/B978-0-12-583980-8.50019-3 Google Scholar
- Rico-Gray, V., & Oliveira, P. S. (2007). The ecology and evolution of ant–plant interactions. The University of Chicago Press.
10.7208/chicago/9780226713540.001.0001 Google Scholar
- Rosumek, F. B., Silveira, F. A., Neves, F., Barbosa, 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 defences. Oecologia, 160, 537–549.
- Savolainen, R., & Vepsäläinen, K. (1998). A competition hierarchy among boreal ants: Impact on resource partitioning and community structure. Oikos, 51, 135–155.
- Schleuning, M., Fründ, J., Klein, A. M., Abrahamczyk, S., Alarcón, R., Albrecht, M., & Blüthgen, N. (2012). Specialization of mutualistic interaction networks decreases toward tropical latitudes. Current Biology, 22(20), 1925–1931.
- Schneider, S. S. (1989). Spatial foraging patterns of the African honeybee, Apis mellifera scutellata. Journal of Insect Behaviour, 2, 505–521.
- Seifan, M., Hoch, E. M., Hanoteaux, S., & Tielborger, K. (2014). The outcome of shared pollination services is affected by the density and spatial pattern of an attractive neighbour. Journal of Ecology, 102(4), 953–962.
- Souza, C., Leal, L. C., Baccaro, F. B., Bergamo, P. J., Bronstein, J. L., Rey, P. J., & Nogueira, A. (2024). Ant sharing by plant species bearing extrafloral nectaries has a low impact on plant herbivory in a tropical system. Figshare [Data set]. https://doi.org/10.6084/m9.figshare.26496472.v2
10.6084/m9.figshare.26496472.v2 Google Scholar
- Souza, C., Oliveira, F. M. P., Ribeiro, E. M. S., Silva, C. H. F., Durval, J. I. F., & Leal, I. R. (2022). Extrafloral nectar secretion does not mediate ant predatory activity on Pityrocarpa moniliformis plants in a seasonally dry forest. Acta Oecologica, 114, 103806.
10.1016/j.actao.2021.103806 Google Scholar
- Staab, M., Pietsch, S., Yan, H., Blüthgen, N., Cheng, A., Li, Y., Zhang, N., Ma, K., & Liu, X. (2023). Dear neighbor: Trees with extrafloral nectaries facilitate defense and growth of adjacent undefended trees. Ecology, 104, e4057.
- Tack, A. J. M., Gripenberg, S., & Roslin, T. (2011). Can we predict indirect interactions from quantitative food webs? An experimental approach. Journal of Animal Ecology, 80, 108–118.
- 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.
- Trumble, J. T., Kolodny-Hirsch, D. M., & Ting, I. P. (1993). Plant compensation for arthropod herbivory. Annual Review of Entomology, 38(1), 93–119.
- Tur, C., Saéz, A., Traveset, A., & Aizen, M. A. (2016). Evaluating the effects of pollinator-mediated interactions using pollen transfer networks: Evidence of widespread facilitation in south Andean plant communities. Ecology Letters, 19, 576–586.
- Vilà, M., Bartomeus, I., Dietzsch, A. C., Petanidou, T., Steffan-Dewenter, I., Stout, J., Stout, J. C., & Tscheulin, T. (2009). Invasive plant integration into native plant–pollinator networks across Europe. Proceedings of the Royal Society, 276, 3887–3893.
- Waddington, K. D., Visscher, P. K., Herbert, T. J., & Raveret Richter, M. (1994). Comparisons of forager distributions from matched honeybee colonies in suburban environments. Behavioral Ecology and Sociobiology, 35, 423–429.
- War, A. R., Paulraj, M. G., Ahmad, T., Buhroo, A. A., Hussain, B., Ignacimuthu, S., & Sharma, H. C. (2012). Mechanisms of plant defence against insect herbivores. Plant Signaling & Behavior, 7(10), 1306–1320.
- Wootton, J. T. (1994). The nature and consequences of indirect effects in ecological communities. Annual Review of Ecology and Systematics, 25, 443–466.
- Xu, F. F., & Chen, J. (2010). Competition hierarchy and plant defence in a guild of ants on tropical Passiflora. Insectes Sociaux, 57, 343–349.
- Yang, S. A., Ferrari, M. J., & Shea, K. (2011). Pollinator behavior mediates negative interactions between two congeneric invasive plant species. American Naturalist, 177, 110–118.
- Zakardjian, M., Geslin, B., Mitran, V., Franquet, E., & Jourdan, H. (2020). Effects of urbanization on plant–pollinator interactions in the tropics: An experimental approach using exotic plants. Insects, 11(11), 773.
- Zuur, A. F., Ieno, E. N., Walker, N., Saveliev, A. A., & Smith, G. M. (2009). Mixed effects models and extensions in ecology with R. Statistics for biology and health. Springer Science & Business Media.
10.1007/978-0-387-87458-6 Google Scholar