Understanding trophic interactions in a warming world by bridging foraging ecology and biomechanics with network science

Background

Leaf-cutter ants (Atta spp. and Acromyrmex spp.) are the principal insect pest and a major ecosystem engineer throughout the Neotropics (Leal et al., 2014; Wirth et al., 2003). They harvest plant matter in the surroundings of their colonies to grow a fungus as crop, and in doing so they cut plant matter on an almost industrial scale: about 15 % of the foliar biomass in the Neotropics, or about every sixth leaf, is consumed by leaf-cutter ant colonies (Costa et al., 2008; Fowler et al., 1989; Herz et al., 2007; Wirth et al., 2003), and more than half of all woody species are attacked by them (Cherrett, 1968; Rockwood, 1976). Leaf-cutter ants are perhaps the most voracious and polyphagous herbivorous insects (Lugo et al., 1973; Wirth et al., 2003), and their foraging activity is affected by a variety of environmental conditions, including wind (Alma et al., 2016b), precipitation (Steadman et al., 2020) and barometric pressure (Sujimoto et al., 2020), all of which will be subject to variation due to climate change.

Although leaf-cutter foraging is clearly a complex, multi-factorial behaviour, it has at its core a biomechanical interaction between ant consumer and plant food resource: the force the ants can apply must exceed the force required to drag the mandible through the tissue (Püffel, Roces, et al., 2023; Püffel, Walthaus, et al., 2023). The magnitude of the available bite force is determined by worker size, and the magnitude of the minimum required cutting force is determined by structural and mechanical properties of the plant leaf; consumer and resource properties interact. This mechanical competition has resulted in extraordinary adaptations in both the anatomy and physiology of the leaf-cutter ant bite apparatus: their disproportionately large heads are filled to the rim with optimally packed mandible closer muscles (Püffel et al., 2021). Both their muscle stress and size-specific bite forces are among the highest measured for any animal (Püffel, Johnston, et al., 2023; Püffel, Roces, et al., 2023), and their mandibles are close to “ideally sharp” (Püffel, Walthaus, et al., 2023). As a result, the vast majority of worker sizes can cut the majority of tropical leafs; without these adaptations, and a bite performance commensurate with their body size, only the largest workers would be able to perform this crucial mechanical task (Püffel, Roces, et al., 2023). How will a warming climate affect resource accessibility for the leaf-cutters?

Temperature increases have various implications for the trophic interactions of ants, including altered search behaviour (Frizzi, 2018), and foraging site selection (Spicer et al., 2017; Traniello et al., 1984). An increase in average temperatures can also drive body size decreases in insects (Tseng et al., 2018), including ants (Molet et al., 2017), concomitantly reducing their available bite force (Püffel, Roces, et al., 2023; Rühr et al., 2022). Since leaf-cutter mandibles are so sharp that they already cut with a force close to the minimum dictated by cutting mechanics, the force required to cut leaves will likely be unaffected (Püffel, Walthaus, et al., 2023), and any change in body size will therefore only significantly impact bite forces. Because the relationship between bite forces and body size in the leaf-cutter is well understood mechanistically (Püffel, Roces, et al., 2023), it is possible to predict how these changes will impact trophic networks. A very rough estimate of the change in network structure serves to illustrate how network science can integrate biomechanics and foraging ecology to study the effect of climate change on trophic interactions.

To demonstrate the potential of network science to integrate biomechanical and foraging data within the context of climate change, we constructed and analysed hypothetical plant-ant networks across six hypothetical temperatures.

Datasets and methods

All analysis was performed in R version 4.3.1 (R Core Team, 2023), and data processed reproducibly via the ‘tidyverse’ package (Wickham et al., 2019). We compiled two datasets and some additional contextual information. Leaf-cutter ant biomass (a proxy for body size) and bite force data were taken from Püffel et al. (2023) for 248 individual ants across three colonies. Required cutting forces for 1197 individual plants representing 868 taxa available to leaf-cutter ants were taken from Onoda et al. (2011). Insect temperature-body size relationships were taken from Tseng et al. (2018); specifically, a body size decrease of 1.56 % per degree Celsius increase for museum specimens, to represent gradual long-term change. Based on these data, edgelists (i.e., pairwise lists of consumers and resources) were generated for ants and plants in which binary interaction weights were applied; where bite forces exceeded the force required to cut leaves, a weighting of 1 was given, and 0 otherwise. This edgelist was then replicated for incremental increases of 1 °C up to a 5 °C increase by adjusting bite forces based on incremental body size decreases of 1.56 %. In order to estimate the change of bite force with body mass, we used direct bite force measurements from Püffel et al. (2023), which suggest that maximum bite force in Atta vollenweideri varies with body mass m as T ~ m^0.9. Thus, if body size decreases by a factor of 0.9844 (i.e., 1.56 % decrease) with every degree Celsius temperature increase, then the maximum bite force decreases by a factor of 0.98440.9. Consequently, adjusted bite forces were calculated, and new binary edgelist weightings generated based on whether the adjusted bite force was greater than the required cutting force.

Bipartite networks were constructed with consumer nodes and resource nodes representing the three ant colonies and the 868 plant taxa, respectively. All six networks were visualised using ‘ggnetwork’ (Briatte, 2021) via ‘igraph’ (Csardi & Nepusz, 2006) in a single network diagram to highlight persistence of links across temperatures using scaled red colours. Network metrics, specifically consumer degree (the number of plants ants were deemed able to interact with) and generality (the total range of plants accessible across all ants), were generated via the ‘bipartite’ package (Dormann et al., 2008) and visually compared via ‘ggplot2’ (Wickham, 2016).