Bioenergetic approaches to terrestrial food webs – new traits for new habitats

Food webs tend to be strongly size-structured, with larger, slower-growing consumers eating broader ranges of smaller, faster-growing resources (Williams & Martinez 2000, Brose et al. 2006). Bioenergetic network models use species’ body size as a key trait to constrain the feeding and vital rates of species (via “allometric scaling laws”), creating plausible simulations of food web dynamics that have successfully reproduced the strengths of feeding interactions (Berlow et al. 2009, Schneider et al. 2012), effects of species removals (Berlow et al. 2009, Schneider et al. 2012), and seasonal dynamics (Boit et al. 2012, Jonsson et al.2018) in both simple and complex systems. However, these predictions systematically break down when trophic interactions are primarily structured by traits other than body size, in the presence of behavioral strategies such as group hunting, and in the presence of non-feeding effects such as habitat facilitation (Berlow et al. 2009, Kalinoski & DeLong 2016, Jonsson et al. 2018). In particular, terrestrial plants are eaten by herbivores both far larger and far smaller than themselves, and some types of herbivory, such as on fruits and flower nectar, provide plants with mutualistic reproductive effects like seed dispersal and pollination. Perhaps because these ‘exceptions’ to the general understanding of trophic interactions are so numerous in aboveground terrestrial systems, food web research has largely focused on aquatic systems (Brose et al. 2019), such that there is little understanding of the structure and dynamics of terrestrial food webs.

In a previous work, I incorporated mutualistic interactions into bioenergetic food web models by allowing animals’ feeding rate on mutualistic rewards (and therefore the benefits they provide to plants) to be a function of their body size. A major limitation of this work is that the production of plants’ vegetative biomass follows the traditional bioenergetic approach of food web theory, which assumes that plants (like phytoplankton) are the smallest and most productive organisms in the system. Plants in terrestrial systems vary in size, growth, and turnover of their biomass, and unlike in aquatic systems where body size determines feeding interactions, terrestrial herbivory is determined more by traits such as phytochemistry and the shape of consumer’s mouthparts (Eklöf et al. 2013; Schneider et al. 2016). As a result, theoretical development and empirical tests of bioenergetic food web theory have largely excluded terrestrial plant-herbivore interactions from their scope (Brose et al. 2019).

Here, we proposed an extension to bioenergetic network theory to account for variation among terrestrial plants. Recent research suggests that vascular plants in terrestrial ecosystems exist along a ‘fast-slow’ axis of growth and life history (Salguero-Gómez et al. 2016, 2017). Fast-growing plants tend to be smaller, leafier, more nutritious for consumers (lower C:N,P ratio), and less resistant (high ingestibility) but more tolerant to herbivory. Slow-growing plants tend to be larger, woodier, less nutritious for consumers, and more resistant but less tolerant of herbivory (Valdovinos, Hale, et al. 2023). We propose to use the matching of this ‘fast-slow axis’ of plant growth (determined by a suite of plant traits) with animal traits (body size and digestive capacity for different chemicals) to broadly determine whether animals can feed on plant tissues and the bioenergetics of the interaction, including trophic efficiencies and foraging effort. We discuss how this variation may propagate through food webs to create differences between aquatic and terrestrial ecosystems, and highlight new, open questions.

Citation: Valdovinos, F. S., Hale, K. R. S., Dritz, S., Glaum, P. R., McCann, K. S., Simon, S. M., Thébault, E., Wetzel, W. C., Wootton, K. L., & Yeakel, J. D. (2023) A bioenergetic framework for aboveground terrestrial food webs. Trends in Ecology and Evolution 38:301– 312. https://doi.org/10.1016/j.tree.2022.11.004

Abstract: Bioenergetic approaches have been greatly influential for understanding community functioning and stability and predicting effects of environmental changes on biodiversity. These approaches use allometric relationships to establish species’ trophic interactions and consumption rates and have been successfully applied to aquatic ecosystems. Terrestrial ecosystems, where body mass is less predictive of plant–consumer interactions, present inherent challenges that these models have yet to meet. Here, we discuss the processes governing terrestrial plant–consumer interactions and develop a bioenergetic framework integrating those processes. Our framework integrates bioenergetics specific to terrestrial plants and their consumers within a food web approach while also considering mutualistic interactions. Such a framework is poised to advance our understanding of terrestrial food webs and to predict their responses to environmental changes.