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).背景 切叶蚁（Leaf-cutter ants，隶属于阿塔切叶蚁属Atta spp.与顶切叶蚁属Acromyrmex spp.）是新热带区（Neotropics）范围内的主要昆虫害虫与关键生态系统工程师（Leal等，2014；Wirth等，2003）。它们会在蚁巢周边采集植物组织，用以培育共生真菌作为作物，其植物切割活动近乎工业化规模：新热带区约15%的叶生物量，即每六片叶片中就有一片被切叶蚁蚁巢消耗（Costa等，2008；Fowler等，1989；Herz等，2007；Wirth等，2003），且超过半数的木本植物会受到它们的侵扰（Cherrett，1968；Rockwood，1976）。切叶蚁或许是最为贪食且多食性的植食昆虫（Lugo等，1973；Wirth等，2003），其觅食活动受多种环境条件影响，包括风力（Alma等，2016b）、降水（Steadman等，2020）与大气压力，而这些因素均会因气候变化产生波动。 尽管切叶蚁的觅食行为显然是复杂的多因子行为，但其核心仍是蚁类消费者与植物食物资源之间的生物力学相互作用：蚂蚁所能施加的力必须超过将上颚穿透植物组织所需的力（Püffel, Roces等，2023；Püffel, Walthaus等，2023）。可用咬合力的大小由工蚁体型决定，而最小所需切割力则由植物叶片的结构与力学特性决定，消费者与资源的特性相互作用。这种力学竞争使得切叶蚁的咬附结构在解剖学与生理学上均产生了极端特化：它们比例硕大的头部完全被最优排布的闭颚肌填满（Püffel等，2021）。其肌肉应力与单位体型咬合力均位列所有已测量动物的顶尖水平（Püffel, Johnston等，2023；Püffel, Roces等，2023），且其上颚近乎达到“理想锋利度”（Püffel, Walthaus等，2023）。因此，绝大多数体型的工蚁都能够切割绝大多数热带叶片；若缺乏这些特化结构，且咬合力无法匹配其体型，那么仅最大体型的工蚁才能完成这一关键力学任务（Püffel, Roces等，2023）。那么气候变暖将如何影响切叶蚁的资源可获得性？ 温度升高对蚂蚁的营养级相互作用存在多方面影响，包括改变其搜寻行为（Frizzi，2018）与觅食位点选择（Spicer等，2017；Traniello等，1984）。平均温度升高还会导致昆虫体型减小（Tseng等，2018），其中也包括蚂蚁（Molet等，2017），进而同步降低其可用咬合力（Püffel, Roces等，2023；Rühr等，2022）。由于切叶蚁的上颚已极为锋利，其切割力已接近切割力学所规定的最小值，因此切割叶片所需的力大概率不会受温度影响（Püffel, Walthaus等，2023），故而体型的任何变化都只会显著影响咬合力。鉴于切叶蚁的咬合力与体型之间的关系已被从机制上阐明（Püffel, Roces等，2023），我们可以预测这些变化将如何影响营养网络。一项针对网络结构变化的粗略估算可用于说明，网络科学如何整合生物力学与觅食生态学，以研究气候变化对营养级相互作用的影响。 为展示网络科学在气候变化背景下整合生物力学与觅食数据的潜力，我们构建并分析了六种假想温度下的假想植物-蚁二分网络。 数据集与方法 所有分析均在R 4.3.1版本（R Core Team，2023）中完成，数据通过‘tidyverse’包（Wickham等，2019）实现可复现处理。我们整合了两份数据集与部分额外的背景信息。切叶蚁生物量（作为体型的替代指标）与咬合力数据取自Püffel等（2023）的研究，涵盖3个蚁巢的248只个体蚂蚁。切叶蚁可利用的1197株植物（隶属于868个分类群）的所需切割力数据取自Onoda等（2011）。昆虫温度-体型关系取自Tseng等（2018）的研究：具体而言，温度每升高1℃，博物馆标本的体型会减小1.56%，以此代表长期的渐进式变化。基于这些数据，我们生成了蚂蚁与植物的边列表（即消费者与资源的成对列表），并为其赋予二元交互权重：当咬合力超过切割叶片所需的力时，权重设为1，反之则为0。随后，我们基于温度每升高1℃时体型减小1.56%的比例，调整咬合力，将该边列表复制到温度每升高1℃直至升高5℃的场景中，生成新的权重。为估算体型变化与咬合力的关系，我们使用了Püffel等（2023）的直接咬合力测量数据，结果显示沃氏阿塔切叶蚁（Atta vollenweideri）的最大咬合力T与体重m的关系为T ~ m^0.9。因此，若温度每升高1℃，体型减小1.56%（即体型系数变为0.9844），则最大咬合力的减小系数为0.9844^0.9。据此，我们计算了调整后的咬合力，并基于调整后的咬合力是否大于所需切割力，生成新的二元边列表权重。 我们构建了二分网络，其中消费者节点代表3个蚁巢，资源节点代表868个植物分类群。我们使用‘ggnetwork’（Briatte，2021）通过‘igraph’（Csardi & Nepusz，2006）将全部6个网络整合为一张可视化图，通过缩放的红色系色彩突出显示不同温度下交互链接的留存情况。我们通过‘bipartite’包（Dormann等，2008）计算了网络指标，具体包括消费者度（即蚂蚁被认为可与之交互的植物数量）与泛化度（即所有蚂蚁可访问的植物总范围），并通过‘ggplot2’（Wickham，2016）进行可视化对比。