3.2 The role of ant competitive hierarchy on network structure
Dominant ants realized, on average, 3.12 \(\pm\) 2.02 (mean \(\pm\) SD) interaction and subordinate ants realized 2.47 \(\pm\ \)1.79 interactions with plants along the networks. Dominant ants represented, on average, 71.62% \(\pm\) 18.1% of all the ant species in the networks, and this proportion was not affected by variation in the mean precipitation rate (GLMM; \(\chi^{2}\) = 1.743, df = 1, p = 0.186). However, the connectance of dominant (\(C_{d}\)) and subordinate (\(C_{s}\)) ant species varied along the precipitation gradient. Contrary to our expectations, both increased as the precipitation rate decreased (\(C_{d}\): 0.38 \(\pm\) 0.16; LMM; \(\chi^{2}\) = 16.209. df = 1, p < 0.001; Estimate = 1; Fig. 3a; \(C_{s}\): 0.32 \(\pm\)0.22; LMM; \(\chi^{2}\) = 10.441, df = 1, p < 0.001; Estimate = 0.99; Fig. 3b).
The mean RR for dominant ant species was 0.72\(\ \pm\ \)0.16, and it was not influenced by the variation in the mean precipitation rate (GLM;\(\chi^{2}\) = 0.093, df = 1, p = 0.173; Fig. 2c). In the same way, the mean RR of subordinate ants (0.79\(\ \pm\ \)0.21) was similar to the RR of dominant ants and it was also not affected by variation in the mean precipitation rate (GLM; \(\chi^{2}\) = 0.149, df = 1, p = 0.149; Fig. 2d). We also observed no variation in Jaccard index along the precipitation gradient (0.40 \(\pm\) 0.31; GLS; \(F_{1,34}\) = 0.244, p = 0624), indicating that the dominant-subordinate overlap in the plant usage is not influenced by water availability.
We observed a data gap at intermediary levels of precipitation rate (254.11 to 433.82 mm – see Fig.1). Because of this gap, data from the wettest networks in our dataset (representing one paper with 12 networks form the same location, all with mean precipitation rate of 433.82 mm) could behave as outliers, compromising the fit of our models. To evaluate this bias, we removed these networks from our dataset and performed again all analyses described in the Statistical analysis section. In all cases, there was no qualitative change in any results described above, indicating that our results were not biased by the asymmetric distribution of the networks along the precipitation gradient (see Support information).
DISCUSSION
Our results showed that as the habitats become drier, the number of ant and plant species interacting with each other decreases, resulting in smaller networks. However, the mean precipitation rate did not affect any other metric describing the structure of the ant-plant networks. Also different from our expectations, the connectance of dominant and subordinate ants increased as the mean precipitation rate declined. Considering that connectance is a metric that intuitively accounts for the probability that any pair of species interact in the network (Landi et al. 2018), it indicates that the decline in water availability at the broader scales increases the generalization of ant-plant interactions. In turn, it increases the chances of both dominant and subordinate ant’s species interact with species of EFN-bearing plants. Interestingly, the mean precipitation rate did not affect the RRd, RRs, or Jaccard similarity index. This lack of effect suggests that changes in the connectance of dominant and subordinate ant species are not due to changes in competitive ant behavior towards the plants but rather a consequence of processes related to the variation in species richness of the network along the precipitation gradient.
Several studies have shown that ant and EFN-plant communities’ richness declines along precipitation gradients (Dunn et al. 2009, Luo et al. 2022, Queiroz et al. 2022). For this reason, it is not surprising that the species richness of ant-plant networks declined with the decline of the mean precipitation rate. However, we observed no effect of the mean precipitation rate on any other descriptors of the ant-plant networks. This is an unexpected result since species richness of networks network is a crucial trait shaping the structure of ecological networks (Boccaletti et al. 2006, Minoarivelo and Hui 2016, Mariani et al. 2019) and, the influence of the mean precipitation rate on it would lead to modifications in other aspects of the network. However, we controlled, in our analysis, the effects of species richness on the metrics describing the network structure (connectance, nestedness, and modularity), either by using normalized metrics (as zQ and zNODF) or the species richness as a weighted factor in our models. For this reason, the lack of precipitation effect on the network structure indicates that variation in water availability had no additional effect on the network structure other than those deriving from the variation in the species richness. This finding directly contrasts with the results from studies evaluating the role of precipitation in ant-plant networks at the local scale (Rico-gray et al. 1998, Rico-Gray et al. 2012, Câmara et al. 2018). At local scale, variation in climatic conditions across the sampled habitats tends to be relatively smaller, resulting in the observation of ant-plant interactions along a relatively narrower precipitation gradient than ours. Therefore, it is possible that the role of water availability in shaping the patterns of ant-plant interactions at the community level is relatively stronger at the local scale, with effects at a broader scale being likely an indirect consequence of its effects on the diversity of ant and plant assemblages across communities.
Similar to the metrics describing the structure of the ant-plant networks, the progressive generalization of ant-plant interactions along our macroecological water gradient is likely a consequence of the negative effects of water scarcity on the number of ant and plant species interacting with each other along the precipitation gradient. Two mechanisms can drive this increased generalization. First, it is possible that the decline of the richness of plant species available in the drier environment increases the relative value of any plant partner to ants, regardless of its quality. In this scenario, interacting with the maximum of plant species available can be as or more advantageous to dominant ants than monopolizing the few high-quality plant species available in drier habitats. By reducing the monopolization strength of high-quality plants, dominant ants allow the visitation of the subordinate ones to more plant species explaining why both dominant and subordinate ants increased their connectance with the decline in the mean precipitation rate. Alternatively, it is possible that, although less rich, plant species with EFNs are more abundant in drier habitats. Since ants and plants are sessile organisms, their interaction depends on how close the ant nests and plants are (Dáttilo et al. 2013c), and this proximity should increase as more abundant ant and plant species populations are. In this case, any increase in the abundance of plants with EFNs in a community may increase the probability of all plant and ant species interacting, leading to a more generalized pattern of ant-plant interaction.
Our results related to the mean RRd, RRs, and the Jaccard index supports the mechanism stating the increase in probability of interaction due to abundance and spatial distribution of ants and plants. The resource range is a normalization of how many links a given species makes, being not influenced by the network connectance or species richness (Poisot et al. 2012). Then, if the generalization in the patterns of ant attendance to EFN plants in drier environments would be driven by changes in the competitive behavior of ants, we could expect an increase in the mean RR for both dominant and subordinate ants. Additionally, if both dominant and subordinate ants use more plant species available as drier the habitat, we may expect an increase in dominant-subordinate overlap as the mean precipitation rate decreases. However, we observe no effect of the mean precipitation rate on the RR values or the degree of dominant-subordinate overlapping along the gradient. It indicates that ants and plants interact similarly along the water gradient, and the generalization in the patterns of ant-plant interaction may be just a consequence of an increased probability of ant-plant species interaction in poorer drier communities.
The preponderant role of the species richness on the generalization of ant-plant interactions may have two significant ecological implications for the dynamic of these interactions across habitats. First, theoretical models have shown that connectance tends to beget stability and persistence of mutualistic networks in space and time (e.g. Thébault and Fontaine 2010, Sauve et al. 2014). Therefore, more connected ant-plant networks may be more stable (but see Allesina and Tang 2012) and persistent than the ones from wetter habitats. In this case, by increasing the overall connectance and the connectance of subordinate and dominant ant species in the networks, the decline in water availability may indirectly increase ant-plant interaction persistence, including its persistence in the face of environmental disturbances. In the face of the current biodiversity crisis, it suggests that, at broader scale, the decline in water availability may be associated with a decline in the susceptibility of ant-plant interactions to environmental disturbance. Like the ones driven by human activities and climate change.
Second, although water availability had no effect on the competitive behavior of dominant ant species, it is likely that they are the main ones driving the direct and indirect effects among ant and plant species with EFNs and the network structure along water gradients. Due to their numerical and behavioral dominance, dominant ant species are commonly the most connected species in ant-plant networks worldwide, holding a higher number of interactions with the plant species available (Dáttilo et al. 2014b, Costa et al. 2016). Although both dominant and subordinate ants became more connected to the plants as the precipitation declined, water availability did not affect the degree of the network nestedness, suggesting the maintenance of the role of dominant ant species in regulating this mutualism, regardless of water availability. Finally, it is important to highlight that the significant role of community richness in shaping mutualistic networks along environmental macroecological gradients has already been reported in other studies using other mutualistic systems as a model, like pollination (e.g. Devoto et al. 2005, Lance et al. 2017). It suggests that the role of community diversity in shaping mutualistic networks at a broader scale is not restricted to ant-plant interactions, being more general than previously expected.
REFERENCES
Albrecht, M. et al. 2010. Plant-pollinator network assembly along the chronosequence of a glacier foreland. - Oikos 119: 1610–1624.
Allesina, S. and Tang, S. 2012. Stability criteria for complex ecosystems. - Nature: 5–8.
Almeida-Neto, M. et al. 2008. A consistent metric for nestedness analysis in ecological systems: reconciling concept and measurement. - Oikos 117: 1227–1239.
Andersen, A. N. 1995. A Classification of Australian Ant Communities, Based on Functional Groups Which Parallel Plant Life-Forms in Relation to Stress and Disturbance. - J. Biogeogr. 22: 15–29.
Andersen, A. N. 1997. Functional groups and patterns of organization in North American ant communities: a comparison with Australia. - J. Biogeogr. 24: 433–460.
Andersen, A. N. and Patel, A. D. 1994. Meat ants as dominant members of Australian ant communities: an experimental test of their influence on the foraging success and forager abundance of other species. - Oecologia 98: 15–24.
Arnan, X. et al. 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: 783–94.
Baccaro, F. et al. 2011. Efeitos da distância entre iscas nas estimativas de abundância e riqueza de formigas em uma floresta de terra-firme na Amazônia Central. - Acta Amaz. 41: 115–122.
Bascompte, J. and Jordano, P. 2007a. Plant-Animal Mutualistic Networks: The Architecture of Biodiversity. - Annu. Rev. Ecol. Evol. Syst. 38: 567–593.
Bascompte, J. and Jordano, P. 2007b. Plant-Animal Mutualistic Networks: The Architecture of Biodiversity. - Annu. Rev. Ecol. Evol. Syst. 38: 567–593.
Bascompte, J. et al. 2003. The nested assembly of plant-animal mutualistic networks. - Proc. Natl. Acad. Sci. 100: 9383–9387.
Bates, D. and Pinheiro, J. 2000. Mixed-Effects Models in S and S-PLUS. - Springer.
Bates, D. et al. 2015. Fitting Linear Mixed-Effects Models Using lme4. - J. Stat. Softw. 67: 1–48.
Blüthgen, N. and Fiedler, K. 2004a. Competition for Composition: Lessons from Nectar-Feeding Ant Communities. - Ecology 85: 1479–1485.
Blüthgen, N. and Fiedler, K. 2004b. Preferences for sugars and amino acids and their conditionality in a diverse nectar-feeding ant community. - J. Anim. Ecol. 73: 155–166.
Blüthgen, N. and Fiedler, K. 2004c. Preferences for sugars and amino acids and their conditionality in a diverse nectar-feeding ant community. - J. Anim. Ecol. 73: 155–166.
Blüthgen, N. and Menzel, F. 2006. Measuring specialization in species interaction networks. - BMC Ecol. 6: 5–12.
Blüthgen, N. et al. 2008. What Do Interaction Network Metrics Tell Us About Specialization and Biological Traits? Nico. - Ecology 89: 3387–3399.
Boccaletti, S. et al. 2006. Complex networks: Structure and dynamics. - Phys. Rep. 424: 175–308.
Buckley, R. and Gullan, P. 1991. More Aggressive Ant Species (Hymenoptera: Formicidae) Provide Better Protection for Soft Scales and Mealybugs (Hommoptera: Coccidae, Pseudococcidae). - Biotroipca 23: 282–286.
Câmara, T. et al. 2018. Effects of chronic anthropogenic disturbance and rainfall on the specialization of ant – plant mutualistic networks in the Caatinga , a Brazilian dry forest. - J. Anim. Ecol. 87: 1022–1033.
Cerdá, X. et al. 2013. Is competition a significant hallmark of ant (Hymenoptera: Formicidae) ecology? - Myrmecological News 18: 131–147.
Contreras, H. L. et al. 2013. The effect of ambient humidity on the foraging behavior of the hawkmoth Manduca sexta. - J. Comp. Physiol. A Neuroethol. Sensory, Neural, Behav. Physiol. 199: 1053–1063.
Costa, F. V. et al. 2016. Few ant species play a central role linking different plant resources in a network in rupestrian grasslands. - PLoS One 11: 1–17.
da Silva, C. H. F. et al. 2019. Extrafloral nectar as a driver of ant community spatial structure along disturbance and rainfall gradients in Brazilian dry forest. - J. Trop. Ecol. 35: 280–287.
Dáttilo, W. et al. 2013a. Soil and vegetation features determine the nested pattern of ant-plant networks in a tropical rainforest. - Ecol. Entomol. 38: 374–380.
Dáttilo, W. et al. 2013b. Spatial structure of ant-plant mutualistic networks. - Oikos 122: 1643–1648.
Dáttilo, W. et al. 2013c. Spatial structure of ant – plant mutualistic networks. - Oikos 122: 1643–1648.
Dáttilo, W. et al. 2014a. The structure of ant-plant ecological networks: Is abundance enough? - Ecology 95: 475–485.
Dáttilo, W. et al. 2014b. Ant dominance hierarchy determines the nested pattern in ant-plant networks. - Biol. J. Linn. Soc. 113: 405–414.
Devoto, M. et al. 2005. Patterns of interaction between plants and pollinators along an environmental gradient. - Oikos 109: 461–472.
Díaz-Castelazo, C. et al. 2013. Long-term temporal variation in the organization of an ant-plant network. - Ann. Bot. 111: 1285–1293.
Dunn, R. R. et al. 2009. Climatic drivers of hemispheric asymmetry in global patterns of ant species richness. - Ecol. Lett. 12: 324–333.
Fagundes, R. et al. 2017. Differences among ant species in plant protection are related to production of extrafloral nectar and degree of leaf herbivory. - Biol. J. Linn. Soc. 122: 71–83.
Flores-Flores, R. V. et al. 2018. Food source quality and ant dominance hierarchy influence the outcomes of ant-plant interactions in an arid environment. - Acta Oecologica 87: 13–19.
Guimarães, P. R. 2020. The structure of ecological networks across levels of organization. - Annu. Rev. Ecol. Syst. 51: 433–460.
Guimarães, P. R. and Guimarães, P. 2006. Improving the analyses of nestedness for large sets of matrices. - Environ. Model. Softw. 21: 1512–1513.
Guimaraes Jr, P. R. et al. 2006. Asymmetries in specialization in ant-plant mutualistic networks. - Proc. R. Soc. B Biol. Sci. 273: 2041–2047.
Guimerà, R. and Amaral, L. A. N. 2005. Cartography of complex networks: modules and universal roles. - J. Stat. Mech. Theory Exp. 02: P02001.
Heil, M. 2008. Indirect defence via tritrophic interactions. - New Phytol. 178: 41–61.
Heil, M. 2011. Nectar: Generation, regulation and ecological functions. - Trends Plant Sci. 16: 191–200.
Heil, M. 2015. Extrafloral Nectar at the Plant-Insect Interface: A Spotlight on Chemical Ecology, Phenotypic Plasticity, and Food Webs. - Annu. Rev. Entomol. 60: 213–232.
Horvitz, C. C. and Schemske, D. W. 1984. Effects of ants and an ant-tended herbivore on seed production of a neotropical herb. - Ecology 65: 1369–1378.
Jordano, P. 1987. Patterns of Mutualistic Interactions in Pollination and Seed Dispersal: Connectance, Dependence Asymmetries, and Coevolution. - Am. Nat. 129: 657–677.
Jordano, P. et al. 2003. Invariant properties in coevolutionary networks of plant-animal interactions. - Ecol. Lett. 6: 69–81.
Kersch & Fonseca 2005. ABIOTIC FACTORS AND THE CONDITIONAL OUTCOME OF AN ANT – PLANT MUTUALISM. - Ecol. Soc. Am. 86: 2117–2126.
Konapala, G. et al. 2020. Climate change will affect global water availability through compounding changes in seasonal precipitation and evaporation. - Nat. Commun. 11: 1–10.
Lance, R. F. et al. 2017. Precipitation and the robustness of a plant and flower-visiting insect network in a xeric ecosystem. - J. Arid Environ. 144: 48–59.
Landi, P. et al. 2018. Complexity and stability of ecological networks: a review of the theory. - Popul. Ecol. 60: 319–345.
Lasmar, C. J. et al. 2021. Geographical variation in ant foraging activity and resource use is driven by climate and net primary productivity. - J. Biogeogr. 00: 1–12.
Leal, L. C. and Peixoto, P. E. C. 2017. Decreasing water availability across the globe improves the effectiveness of protective ant-plant mutualisms: A meta-analysis. - Biol. Rev. 92: 1785–1794.
Leal, L. C. et al. 2022. Which traits optimize plant benefits? Meta‐analysis on the effect of partner traits on the outcome of an ant‐plant protective mutualism.
Luna, P. et al. 2018. Beta diversity of ant-plant interactions over day-night periods and plant physiognomies in a semiarid environment. - J. Arid Environ. 156: 69–76.
Luo, Y. et al. 2022. Climate and ant richness explain the global distribution of ant-plant mutualisms. - bioRxiv in press.
Maia, K. P. et al. 2019. Does the sociality of pollinators shape the organisation of pollination networks? - Oikos: 1–12.
Mariani, M. S. et al. 2019. Nestedness in complex networks: Observation, emergence, and implications. - Phys. Rep. 813: 1–90.
Marquitti, F. M. D. et al. 2013. MODULAR: Software for the Autonomous Computation of Modularity in Large Network Sets.: arXiv:1304.2917.
Miller, T. E. X. 2007. Does having multiple partners weaken the benefits of facultative mutualism? A test with cacti and cactus-tending ants. - Oikos 116: 500–512.
Minoarivelo, H. O. and Hui, C. 2016. Trait-mediated interaction leads to structural emergence in mutualistic networks. - Evol. Ecol. 30: 105–121.
Newman, M. E. J. 2006. Modularity and community structure in networks. - Proc. Natl. Acad. Sci. U. S. A. 103: 8577–8582.
Olesen, J. M. et al. 2007. The modularity of pollination networks. - Proc. Natl. Acad. Sci. 104: 19891–19896.
Parr, C. and Gibb, H. 2010. Competition and the Role of Dominant ants. - In: Lach, L. et al. (eds), Ant Ecology. pp. 424.
Pellissier, L. et al. 2018. Comparing species interaction networks along environmental gradients. - Biol. Rev. 93: 785–800.
Plowman, N. S. et al. 2017. Network reorganization and breakdown of an ant – plant protection mutualism with elevation. - Proc. R. Soc. B Biol. Sci. in press.
Poisot, T. et al. 2012. A comparative study of ecological specialization estimators. - Methods Ecol. Evol. 3: 537–544.
Pringle, E. G. et al. 2013. Water Stress Strengthens Mutualism Among Ants, Trees, and Scale Insects. - PLoS Biol. 11: e1001705.
Queiroz, A. C. M. et al. 2022. Ant diversity decreases during the dry season: A meta‐analysis of the effects of seasonality on ant richness and abundance. - Biotropica 00: 1–11.
R Core Team 2022. R: A Language and Environment for Statistical Computing. in press.
Rico-gray, V. et al. 1998. Geographical and Seasonal Variation in the Richness of Ant-Plant Interactions in Mexico. - Biotropica 30: 190–200.
Rico-Gray, V. et al. 2012. Abiotic factors shape temporal variation in the structure of an ant – plant network. - Arthropod. Plant. Interact. 6: 289–295.
Ruffner, G. A. and Clark, W. D. 1986. Extrafloral Nectar of Ferocactus acanthodes (Cactaceae): Composition and Its Importance to Ants. - Am. J. Bot. 73: 185–189.
Sauve, A. M. C. et al. 2014. Structure-stability relationships in networks combining mutualistic and antagonistic interactions. - Oikos 123: 378–384.
Stuble, K. L. et al. 2017. Dominance hierarchies are a dominant paradigm in ant ecology (Hymenoptera: Formicidae), but should they be? and what is a dominance hierarchy anyways? - Myrmecological News 24: 71–81.
Thébault, E. and Fontaine, C. 2010. Stability of ecological communities and the architecture of mutualistic and trophic networks. - Science (80-. ). 329: 853–856.
Tylianakis, J. M. and Morris, R. J. 2017. Ecological Networks Across Environmental Gradients. - Annu. Rev. Ecol. Evol. Syst. 48: 25–48.
Vázquez, D. P. et al. 2005. Interaction frequency as a surrogate for the total effect of animal mutualists on plants. - Ecol. Lett. 8: 1088–1094.
Xu, F. F. and Chen, J. 2010. Competition hierarchy and plant defense in a guild of ants on tropical Passiflora. - Insectes Soc. 57: 343–349.
Yodzis, P. 1980. The connectance of real ecosystems. - Nature 284: 544–545.
Zuur, A. F. et al. 2009. Mixed Effects Models and Extensions in Ecology with R. - Springler-Verlag.