Metabolic traits are shaped by phylogenetic conservatism and environment, not just body size

Abstract

Metabolic rate dictates life’s tempo, yet how ecological and environmental factors integrate to shape metabolic traits remains contentious. Considering metabolic traits of 114 species of ants from seven subfamily clades along a 1,500 km climatic and soil phosphorus availability gradient in Australia, we tested four hypotheses relating to variation in metabolic rate due to niche conservatism, temperature, aridity, and ecological stoichiometry. We also tested the contested hygric hypothesis, which predicts that insect ventilation patterns can be modified to reduce water loss in arid environments. Mass-independent metabolic rate was phylogenetically conserved. The ant clade Myrmecia had metabolic rates 3 to 10× higher than other species, likely related to their large eye size, a correlate of cognitive complexity. Metabolic rate was higher in ants from warm, arid sites relative to those from wet, cool sites. A weak positive interaction between soil phosphorus and body mass indicated that, at sites with low soil phosphorus, smaller ants respired at higher rates than expected based on their mass—consistent with ecological stoichiometry theory. Larger ants, regardless of clade, were more likely to exhibit discontinuous gas exchange (DGC) with increasing aridity, likely reflecting a water conservation strategy. Phylogenetic conservatism of metabolic rate and a moderate influence of environment suggest that, in addition to biophysical geometric constraints, metabolic rate has evolved to match the energetic demands required of ecological strategies to address environmental stressors. For larger insect species confronting their metabolic limits, DGC may promote resilience in a world that is becoming hotter and more arid.