Intraspecific patterns in root trait variation: insights towards predicting plant community responses to environmental change
Fewer studies in this Special Issue examine how root traits varywithin species (Table 1). Based on interspecific plant resource economics frameworks, it is widely expected that root traits shift along a conservation axis: in more adverse environments (e.g ., with low resource availability or high biotic stress), species would produce roots with resource-conservative traits that prolong root lifespan and retain plant resources. Evidence is mounting, however, that this prediction does not hold at the intraspecific level (Weemstra and Valverde-Barrantes 2022). Along a biotic gradient, Gagliardi et al. (2022) test whether coffee (Coffea arabica ) plants altered their roots traits and associated endophytes along a biotic (coffee leaf rust) environmental gradient, but find that the root traits measured were not involved in foliar defenses. Such above-belowground decoupling may result from the different environmental factors that determine leaf disease development and belowground trait expressions (Gagliardi et al. 2022). Along an abiotic (elevational) environmental gradient, the study by Spitzer et al. (2022) on intraspecific variation in root traits across 16 tundra species highlights the variable ways through which different species alter a variety of root traits, or adjust the same root trait in different manners (both linearly and nonlinearly). This intraspecific trait variation (rather than species turnover) was also the main driver of root trait variation at the community level, in this study, emphasizing its importance for plant communities to cope with environmental change (Spitzer et al. 2022).
These species- and trait-specific changes in root attributes may result from the different root systems that plants can construe to handle environmental change. For example, when water availability decreases, plants can display multiple responses such as enhance their root mass fraction (i.e., root biomass per unit plant biomass), SRL, rooting depth, or investments in mycorrhizal symbiosis, to improve plant water uptake (Freschet et al. 2021a). This multitude of adaptive responses to a particular environmental cue would lead to highly idiosyncratic root trait patterns across species in response to the same stressor (Weemstra et al. 2021). This is further demonstrated by Slette and collaborators (2022) who show that the root morphological traits commonly measured and assumed to be involved in water uptake (e.g., SRL) did not change during or after droughts in their prairie grassland communities. In contrast, root productivity did significantly change (albeit in an opposite direction than generally assumed, i.e., it decreased in response to drought), but this trait is rarely measured, especially within species and in natural systems. Wang et al. (2021) arrive at similar conclusions when studying intraspecific variation in root traits in response to P limitations across different wheat genotypes. Their experimental work elucidates how different (above- and) belowground trait combinations allow plants from a single species to be equally productive under different levels of soil P, as also speculated by Dallstream et al. (2022).
The intraspecific insights that these studies raise have important implications for the interspecific RES framework. Not only can root traits be under strong plastic controls, thus changing the positions of species within the RES, but the direction in which species change is also contingent on the context, i.e., depending on species identity, environmental constraints, and temporal patterns (seasonality, ontogeny). For instance, species sampled in different seasons may display different root traits: under adverse conditions, acquisitive, lower-order roots may be shed, and only higher order roots (with distinct traits, such as higher root diameter; McCormack et al. 2015) may be sampled, and root traits themselves (like nitrogen concentration) may change over the seasons (Zadworny et al. 2015). Depending on root phenology, Species 1 (Figure 1) may appear to shift along the collaboration axis but this may not reflect a shift in the species’ dependency on mycorrhizal fungi. Similarly, root traits may change with plant ontogeny, changing from thin to thick roots as plants grow bigger (Leroy et al. 2022) (Species 2; Figure 1). Guo et al. (2022) further showed that allometric relationships (and thus covariations) among root traits also changed as a function of tree size in a tropical forest community. The position of species within the RES may thus change with time (at least, along the collaboration axis), but whether these shifts indeed reflect changes in the degree of mycorrhizal dependency is still controversial (see e.g., Leroy et al. (2022)). Temporal variation in root traits in including mycorrhizal colonization rates, both at the intra-, interspecific and community level, will warrant future research.
Several studies here further demonstrate the various traits involved in belowground resource uptake strategies, which are thus relevant in the context of a RES and of species’ responses to environmental change. These include, but are not restricted to, root foraging precision (Yang et al. 2021, Stiblíková et al. 2022), productivity (Yang et al. 2021, Slette et al. 2022), mechanical traits (Mao et al. 2022), exudation profiles (Dallstream et al. 2022) and enzymatic capacities (Wang et al. 2021), root biomass fractions and vertical distributions (Yang et al. 2021, Wang et al. 2021, Gagliardi et al. 2022), mycorrhizal fungal traits (Weemstra et al. 2022) or interactions with plant pathogens (Dai et al. 2022). If e.g., Species 3 in Figure 1 would adjust (combinations of) these traits whilst keeping the four key RES traits (root N, specific root length, root tissue density, and root diameter) constant, it may remain at the same position at the RES, but still display considerable belowground adjustments in their belowground strategies. At the same time, which traits are being adjusted could be species-specific (Spitzer et al. 2022), so that to conserve plant resources under environmental stress, Species 4 may enhance root diameter which in turn may enhance root lifespan (McCormack et al. 2012) whereas Species 5 increases root tissue density, as assumed by the RES framework. Together, the studies in this Species Issue provide highly important clues for the further development of the RES by identifying relevant additional traits that characterize species, their resource strategies, and coping mechanisms for environmental variation. They also show, however, that more work is needed at the intraspecific level, where root trait patterns are diverse but of great importance for predicting how plant communities cope with environmental change, and call for novel conceptual frameworks that capture this belowground plasticity (Weemstra and Valverde-Barrantes 2022).