Does plant biomass partitioning reflect energetic investments in carbon and nutrient foraging?

Studies of plant resource-use strategies along environmental gradients often assume that dry matter partitioning represents an individual's energy investment in foraging for above- versus below-ground resources. However, ecosystem-level studies of total below-ground carbon allocation (TBCA) in forests do not support the equivalency of energy (carbon) and dry matter partitioning, in part because allocation of carbon to below-ground pools and fluxes that are not accounted for by root biomass (e.g., mycorrhizal hyphae, rhizodeposition; root and soil respiration) can be substantial. Here, we apply this reasoning to individual plants in controlled environments and ask whether dry matter partitioning below-ground (root mass fraction, RMF) accurately reflects TBCA in studies of optimal partitioning theory. We quantified the relationship between RMF and TBCA in individual plants, using 311 observations from 51 studies that simultaneously measured both allocation variables. Our analysis included tests of whether the RMF-TBCA relationship depended on mutualist soil microbes, plant growth form, age and study methodology including isotopic pulse–chase duration. We found that RMF was a poor proxy for below-ground energy investment. This disconnect of RMF and TBCA was driven in part by plants of low RMF (<0.4) exhibiting significantly higher rates of root and soil respiration per unit root mass than plants of high RMF. Root colonization by mutualist microbes, including arbuscular mycorrhizal fungi and nitrogen-fixing bacteria, increased TBCA by 5%–7%, and TBCA was lower in grasses than other species by 9%–16%. These patterns were evident for relationships assessed both within and between species. We conclude that optimal partitioning studies of plants along environmental gradients are likely to underestimate plant energy allocation below-ground if the C costs of root and soil respiration are ignored, especially under conditions favouring low RMF. Because energy rather than biomass better reflects how assimilated C supports fitness, this omission of respired C suggests existing studies misrepresent the significance of below-ground processes to plant function. A free Plain Language Summary can be found within the Supporting Information of this article.