Can metabolic traits explain animal community assembly and functioning?

Abstract

All animals on Earth compete for free energy, which is acquired, assimilated, and ultimately allocated to growth and reproduction. Competition is strongest within communities of sympatric, ecologically similar animals of roughly equal size (i.e. horizontal communities), which are often the focus of traditional community ecology. The replacement of taxonomic identities with functional traits has improved our ability to decipher the ecological dynamics that govern the assembly and functioning of animal communities. Yet, the use of low‐resolution and taxonomically idiosyncratic traits in animals may have hampered progress to date. An animal's metabolic rate (MR) determines the costs of basic organismal processes and activities, thus linking major aspects of the multifaceted constructs of ecological niches (where, when, and how energy is obtained) and ecological fitness (how much energy is accumulated and passed on to future generations). We review evidence from organismal physiology to large‐scale analyses across the tree of life to propose that MR gives rise to a group of meaningful functional traits – resting metabolic rate (RMR), maximum metabolic rate (MMR), and aerobic scope (AS) – that may permit an improved quantification of the energetic basis of species coexistence and, ultimately, the assembly and functioning of animal communities. Specifically, metabolic traits integrate across a variety of typical trait proxies for energy acquisition and allocation in animals (e.g. body size, diet, mobility, life history, habitat use), to yield a smaller suite of continuous quantities that: (1) can be precisely measured for individuals in a standardized fashion; and (2) apply to all animals regardless of their body plan, habitat, or taxonomic affiliation. While integrating metabolic traits into animal community ecology is neither a panacea to disentangling the nuanced effects of biological differences on animal community structure and functioning, nor without challenges, a small number of studies across different taxa suggest that MR may serve as a useful proxy for the energetic basis of competition in animals. Thus, the application of MR traits for animal communities can lead to a more general understanding of community assembly and functioning, enhance our ability to trace eco‐evolutionary dynamics from genotypes to phenotypes (and vice versa), and help predict the responses of animal communities to environmental change. While trait‐based ecology has improved our knowledge of animal communities to date, a more explicit energetic lens via the integration of metabolic traits may further strengthen the existing framework.

Metabolic rate and climate change across latitudes: evidence of mass-dependent responses in aquatic amphipods

“…The metabolic rate, i.e. rate of energy use, of organisms is considered a key parameter in ecology, linking individual organisms to populations and ecosystems through a unified currency of energy ( Brandl et al, 2022 ; Cozzoli et al, 2021 ; Glazier, 2015 ). Individual ectotherm metabolic rates tend to increase with increasing temperature, owing to its effect on the kinetic energy of cellular components ( Gillooly et al, 2001 ; but see Clarke and Fraser, 2004 ), although this trend has an upper thermal limit ( Schulte, 2015 ; Sinclair et al, 2016 ).…”

Going across taxa in functional ecology: Review and perspectives of an emerging field

“…Linking easily measured traits (e.g. biochemical universal properties of organisms) to scalable metrics could allow the inclusion of any organism in the Tree of Life along a continuum using integrative approaches, as already done in single trait approaches (Brown et al, 2004) and recently extended to multiple trait approaches (Brandl et al, 2023; Enquist et al, 2015; Schiettekatte et al, 2022). Significant advances in functional cross‐taxa research will come from working on the development of common metrics and traits to be applied across taxa.…”

“…While such common currency could be functionally analogous traits, other approaches could be complementary. For instance, energy and matter can be used as common universal currencies to unite all life forms, from Archaea to blue whale (Brandl et al, 2023;Brown et al, 2004Brown et al, , 2018Capdevila et al, 2020;Enquist et al, 2015;Healy et al, 2019;Junker et al, 2023;Margalef, 1963). Terrestrial organisms (98 taxa from Insecta to Mammalia) can be arranged along a common currency, the 'animal economics spectrum', that represents a trade-off in life history strategies of species (Junker et al, 2023; see Box 1).…”

“…Crossing such taxonomic barrier is crucial for uncovering the general principles that govern species interactions (Schleuning et al, 2023) and abundance distributions across space (Brown, 1984; Brown & Nicoletto, 1991; McGill et al, 2007; Preston, 1948), as well as determining the significance of individuals, species, and traits in ecosystem functioning (Weiss & Ray, 2019). Within this context, the study of multiple taxa in functional trait analysis can complement the traditional approaches that focus on individual taxa, enabling the identification of patterns and general processes that govern various ecosystems (Brandl et al, 2023; Brown et al, 2004; MacLean & Beissinger, 2017; Schmera et al, 2017). For instance, approaches using multiple taxa can enhance predictions of diversity patterns across environmental gradients, such as elevation (Mori et al, 2015), temperature (Brown et al, 2004), productivity (Hawkins et al, 2003) and urbanization (Nagy et al, 2018).…”

“…It has long been recognized that ecological communities and their interactions can be effectively characterized by species' universal traits, also known as ‘supertraits’ (Madin, Hoogenboom, et al, 2016), such as body size or trophic position (Bergmann, 1847; Brandl et al, 2023; Brown & Nicoletto, 1991; Brown et al, 2004; Elton, 1927; Margalef, 1963). Such organismal traits can be translated into common currencies of mass and energy, and have contributed substantially to the understanding of processes happening at higher organizational levels, such as population abundance, species interactions, community species richness and the energy flux within ecosystems (Allen et al, 2005; Brown et al, 2004; Elton, 1927; Enquist et al, 2015).…”