Recently, Svejcar et al.¹ identified technical challenges to restoring native species in sagebrush steppe and suggested developing strategic frameworks combining seed coating/packaging technology with specific planting methods, seeding rates, and timing of planting to overcome seasonal stresses and phenological/demographic bottlenecks to improve establishment of native plant populations. However, Svejcar et al.¹ did not directly address developing similar frameworks to guide improvement and selection of plant materials. They did summarize findings showing how crested wheatgrass (Agropyron cristatum), a Eurasian exotic widely planted across US sagebrush steppe, historically gained popularity and posited some of the mechanisms by which it does so, but did not examine where or why these features originated. Our purpose is to show that even a cursory examination of the systems crested wheatgrass occurs in provides considerable insight into what is needed to select and develop native plant materials with comparable versatility in the Great Basin sagebrush steppe.

Across rangeland systems of the Central Plains, Inter-mountain West, and Pacific Coast regions, Native North Americans were skilled land managers, and practiced landscape-scale practices like burning to encourage forage production, with distinct effects on North American plant community structure and dynamics.^2-4 But, especially in comparison to Central Plains grasslands, there is evidence that Great Basin sagebrush steppe was not as intensively managed, principally because it did not regularly support large populations of grazing herbivores.⁵ This stands in marked contrast with Eurasian steppe systems where crested wheatgrass evolved. Although modern humans have been in North America and Eurasia for millennia, Eurasian grassland and steppes have a longer history of larger, more intensive and diverse pastoral grazing systems across a broad swath of rangeland plant communities that developed in dramatically different soils and climate regimes.^6-13 Starting in at least 8,500 to 8,000 BCE, grazing lands across Eurasia came under increasingly intensive human management under a wide range of socio/politico/economic systems, most of which were structured to support traditional year-long grazing regimes in grassland and rangeland that first reduced in area after expansion of other agrarian land-use practices, and then in secondary rangelands developing after abandonment of these converted agrarian areas.^13-18

Thus, in addition to adapting to a huge range of natural biotic and abiotic variation, crested wheatgrass successfully adapted to complex, extensive, and shifting mosaics of anthropogenic land use management practices that varied in intensity, duration, and extent. There is evidence the Eurasian crested wheatgrass complex, consisting of crested wheatgrass (which combines fairway crested wheatgrass [Agropyron cristatum] with standard or desert crested wheatgrass [A. desertorum] as crested wheatgrass) and Siberian wheatgrass (A. fragile) represent a single gene pool, comprised of diploid, tetraploid, and hexaploid forms of a common genome, with a high degree of hybrid fertility between ploidy levels.^19,20 As crested wheatgrass is largely reproductively self-incompatible and relies extensively on outcrossing,¹⁹ locally developed adaptive traits could have readily spread across Eurasia, with ploidy levels modulating trait expression and effectiveness.

We consider the influence of human activity as a likely key in the development of adaptive plant characteristics that make crested wheatgrass so successful as a sagebrush steppe restoration species.Although North American sagebrush steppe also encompasses a similarly broad range of climate and edaphic diversity as Eurasian steppes, large swaths of North American sagebrush steppe went from seasonal use from nomadic herbivores to intensively, and in many cases continuously, grazed in just a few decades after the introduction of domestic livestock.^1,5 No doubt this had a profound direct effect on native perennial grasses in these impacted areas, as did the subsequent introduction and spread of annual grasses which,with no native counterpart,instituted extremely strong competitive regimes, accelerated fire cycles, and altered soil processes and nutrient cycling.^5,21-23 In less than a generation for some native perennial bunchgrasses,^24,25 a significant proportion of sagebrush steppe abruptly went from the late Pleistocene/early Anthropocene to the middle Anthropocene. Compared with the millennia plant adaptations to these pressures unfolded in Eurasian steppes, it is no wonder developing native plant materials capable of readily establishing into degraded sagebrush steppe is so problematic. We need to look on crested wheatgrass's success as reflecting it as fully a grass of the middle Anthropocene. Recognizing the human element shaped the functional characteristics of this grass—beyond subsequent material selection and modification after its introduction to North America^26,27—could provide us with a meaningful plant functional framework to assess and select native grass plant material for deployment into human-modified sagebrush steppe rangelands.

Since the advent of European settlement and the spread of invasive annual grasses, native perennial bunchgrasses have shown evidence of rapid evolution of improved competitive ability with invasive annuals, at least at a localized population level.^28-31 In addition, there has been considerable effort to develop and release native plant materials with plant traits to better endure abiotic stress and/or compete against non-native grasses under stressful conditions.^32-35 Still, despite these ongoing natural processes and human efforts, getting native grasses to establish readily from seed remains one, if not the, major barrier to restoring sagebrush steppe ecosystem functionality and resilience.³⁶ Given the diverse Eurasian pastoral systems crested wheatgrass has adapted to, we posit multiple natural and anthropogenic pressures have resulted in traits and functional attributes that span the demographic cycle from seed germination, seedling emergence and establishment, juvenile and adult vegetative growth, and seed production beyond what has been required of native North American perennial grass species. Given the rapid pace of biotic change in Great Basin plant communities, and the great spatial and temporal range in abiotic environments in which they exist, these adaptations may provide a useful framework for improvement of native plant materials. By establishing the functional mechanisms at each demographic step in crested wheatgrass, we could gain insights into the mechanisms underlying localized variation in the competitive ability in native grasses, as well establishing at what point in their demographic life cycle native grass species fall short.

Here we present results from our recent research that show such an approach can be useful. A key attribute to crested wheatgrass's success is its ability to consistently produce viable seed cohorts, and, although germination rates are similar to native species, crested wheatgrass seedlings are better able to survive through seedling emergence, which poses a strong demographic bottleneck to native grasses.^25,37,38 Four potential mechanisms for how emergence success could be attained are 1) greater investment to reproductive effort, 2) greater energetic seed reserves, 3) seedling tissue quality and relative allocation to aboveground and belowground growth, and 4) higher seedling physiological stress tolerance. We have found crested wheatgrass has seed heads with four-fold higher specific mass (g mass/m² surface area) compared with native grasses, and concurrent with seed head photosynthetic capacity and carbon fixation efficiency that was not only greater than in the native grasses studied, but equaled or exceeded its own flag leaves.³⁹ This higher per unit allocation to reproductive effort and greater capacity for carbon fixation at the site of seed production are consistent with 1) and 2) above and could result in greater investment to both seed quantity and quality, a feature apparently lacking in native grasses.⁴⁰ We also found emergent crested wheatgrass and bluebunch wheatgrass (Psuedororegnaria spicata) seedlings increased photosynthetic rates in response to defoliation; in the native bluebunch wheatgrass this decreased intrinsic water use efficiency (iWUE = ratio of net photosynthesis to stomatal conductance to water vapor) but increased iWUE in crested wheatgrass,⁴¹ which could facilitate higher carbon fixation under drying soil conditions that typically affect seedling survival.⁴² Moreover, defoliation induced a shift to lower root:shoot ratios in crested wheatgrass concurrent with higher aboveground tissue specific mass, and root specific mass was unaffected and considerably lower than in bluebunch wheatgrass, which allocated more biomass to belowground growth.⁴¹ These photosynthetic and tissue allocational responses are consistent with 3) and 4). Moreover, these findings for bluebunch wheatgrass are consistent with a species adapted to persist within a variable environment. However, measures of evolutionary success in the Anthropocene may be more about establishment and reproduction in an environment of increased biotic competition from non-native species and increased abiotic stress from altered fire regimes and greater interannual climate variability.

Our findings also suggest compensatory photosynthetic responses to herbivory that do not seem to affect herbivory tolerance in adult plants^43,44 may carry over from the seedling stage, when they clearly do. Ultimately, the fact that crested wheatgrass has greater reproductive photosynthetic capacity likely underlies its seedling success, because this could ensure production of seeds with greater energetic reserves to support post-germination seedling growth and would impart a longer emergence and establishment window compared with native grasses. Given the grazing-intensive nature of the diverse pastoral steppe systems crested wheatgrass originated from, developing the ability to withstand loss of parental plant foliage and maintain seed production and supplying seeds with energetic reserves would be particularly advantageous, given that long-term persistence and population dynamics of bunchgrasses are driven primarily by sexual reproduction.^24,25 As factors that define both the ecological and evolutionary success of desired vegetation change, we, as a profession, should re-consider and refine the attributes used to assess fitness of plant materials. We believe this process can benefit significantly from examining key physiological traits at critical demographic stages of successful non-native species, such as crested wheatgrass, that have evolved under stressors comparable to modern-day sagebrush steppe. This is a paradigm shift from apparent indicators of success, such as plant biomass, to more mechanistic and basal indicators of a plant's ability to physiologically cope with specific, and in some cases novel stressors in a world increasingly dominated by the direct and indirect effects of human activity.

Declaration of Competing Interest

None.