Climate seasonality drives ant–plant–herbivore interactions via plant phenology in an extrafloral nectary‐bearing plant community

Abstract

Interactions between ants and plants bearing extrafloral nectaries (EFNs) are among the most common mutualisms in Neotropical regions. Plants secrete extrafloral nectar, a carbohydrate‐rich food that attracts ants, which in return protect plants against herbivores. This ant–plant mutualism is subjected to temporal variation, in which abiotic factors can drive the establishment and frequency of such mutualistic interaction. However, studies investigating how abiotic factors (e.g. climate) directly and indirectly influence ant–plant–herbivore interactions are incipient. In this study, we investigated direct and indirect (via plant phenology) effects of temperature and rainfall on ant–plant–herbivore interactions. To address these goals, each month we estimated six plant phenophases (newly flushed leaves, fully expanded leaves, deciduousness, floral buds, flowers and fruits), the activity of EFNs and abundance of ants and herbivores in 18 EFN‐bearing plant species growing in a markedly seasonal region (the Brazilian Cerrado) during a complete growing season. Our results showed that (a) there were marked seasonal patterns in all plant phenophases, EFN activity and the abundance of ants and herbivores; (b) the peak of EFN activity and ant and herbivore abundance simultaneously occurred at the beginning of the rainy season, when new leaves flushed and (c) rainfall directly and indirectly (via changes in the production of new leaves) influenced EFN activity and this in turn provoked changes in ant abundance (but not on herbivores). Synthesis. Overall, our results build towards a better understanding of how climate drives seasonal patterns in ant–plant–herbivore interactions, explicitly considering plant phenology over time.

Spatiotemporal niche‐based mechanisms support a stable coexistence of ants and spiders in an extrafloral nectary‐bearing plant community

“…These hypotheses are mainly based on the similarity of ants and spiders feeding behaviours, which can lead to competitive relationships and ultimately result in spatiotemporal niche segregation. Recently, we observed a significant peak of activity of ants in the rainy season at the same time as EFNs are active, considerably decreasing their activity (ants and EFNs) in the dry season (Calixto et al., 2020). Due to numerical representativeness and aggressive behaviour when on EFN‐bearing plants, ants can end up displacing spiders to other branches, and spiders can end up changing their phenological behaviours for periods of the year when there is less presence of ants in plants.…”

“…Furthermore, one may suggest that there is a temporal segregation during the day between ants and spiders, that is, ants occurring during the day and spiders at night. However, both groups are commonly present in EFN‐bearing plants in both periods of the day (Anjos et al., 2017; Calixto, Lange, Bronstein, et al., 2021; Calixto, Lange, & Del‐Claro, 2021; Calixto et al., 2020; Lange et al., 2017; Nahas et al., 2016).…”

“…Tropical savannas, such as the Brazilian Cerrado, is an advantageous environment to evaluate interspecific interactions and stabilizing mechanisms through the assessment of spatiotemporal co‐occurrence patterns. The Cerrado has two well‐defined seasons (rainy and dry season; Calixto et al., 2020; Novaes et al., 2020) and it is the most biodiverse savanna on Earth, considered a hotspot of biodiversity (Myers et al., 2000). These well‐marked climatic conditions can generate temporal partitions for the occurrence of different species.…”

“…These well‐marked climatic conditions can generate temporal partitions for the occurrence of different species. For instance, spiders and ants are among the most common predator arthropods inhabiting vegetation in this region (Calixto et al., 2018; Del‐Claro et al., 2017), which are frequently attracted by plant‐provided resources such as extrafloral nectar (Calixto et al., 2018; Calixto et al., 2020; Del‐Claro et al., 2017; Heil, 2015; Nahas et al., 2016; Taylor & Pfannenstiel, 2009). Extrafloral nectaries (EFNs) produce a sugar‐rich resource which is also composed of amino acids and other contents, works as a source of nutrient to balance the carbohydrate–protein ratio in the diet of ants and spiders (Byk & Del‐Claro, 2011; Calixto, Lange, Bronstein, et al., 2021; Lange et al., 2017; Nahas et al., 2016), and is mainly produced in the rainy season concomitantly to leaf flushing (Calixto et al., 2020; Lange et al., 2013).…”

“…To reach this goal, we assessed whether there are spatial‐ and temporal‐scale patterns of ants and spiders occurrence at both plant community and plant species level. We hypothesized that, although there is seasonal variation in resource availability (Belchior et al., 2016; Calixto et al., 2020; Lange et al., 2013), ants and spiders will coexist in plants through a spatiotemporal niche segregation. In particular, both groups could (a) occupy different branches if they are on the same plant at the same time (spatial non‐co‐occurrence patterns or spatial niche segregation); and (b) present greater abundance of individuals in different periods of the year (temporal non‐co‐occurrence patterns or temporal niche segregation).…”