Feast or famine: How is global change affecting forage supply for Yellowstone's ungulate herds?

The ecological integrity of US national parks and other protected areas are under threat in the Anthropocene. For Yellowstone National Park (YNP), the impacts that global change has already had on the park's capacity to sustain its large migratory herds of wild ungulates is incompletely understood. Here we examine how two understudied components of global change, the historical increase in atmospheric CO2 and the spread of nonnative, invasive plant species, may have altered the capacity of YNP to provide forage for ungulates over the last 200-plus years. We performed two experiments: (1) a growth chamber study that determined the growth rates of important invasive and native YNP grasses that are forages for ungulates under preindustrial (280 ppm) versus modern (410 ppm) CO2 levels and (2) a field study that compared the effect of defoliation (clipping) on the shoot growth of invasive and native mesic grassland plants under ambient CO2 conditions in 2019. The growth chamber experiment revealed that modern CO2 increased the growth rates of both invasive and native grasses, and invasive grasses grew faster regardless of CO2 conditions. The field results showed a continuum of positive to negative responses of shoot growth to defoliation, with a subgroup of invasive species responding most positively. Altogether the results indicated that the historical increase in CO2 and the spread of invasive species, some of which were planted to provide forage for ungulates in the early and mid-1900s, have likely increased the capacity of forage production in YNP. However, rising CO2 has also resulted in regional warming and increased aridity in YNP, which will likely reduce grassland productivity. The challenge for global change biologists and park managers is to determine how competing components of global change have already affected and will increasingly affect forage dynamics and the sustainability of Yellowstone's iconic ungulate herds in the Anthropocene.

Fast but steady: An integrated leaf-stem-root trait syndrome for woody forest invaders.

Successful control and prevention of biological invasions depend on identifying traits of non-native species that promote fitness advantages in competition with native species. Here, we show that, among 76 native and non-native woody plants of deciduous forests of North America, invaders express a unique functional syndrome that combines high metabolic rate with robust leaves of longer lifespan and a greater duration of annual carbon gain, behaviours enabled by seasonally plastic xylem structure and rapid production of thin roots. This trait combination was absent in all native species examined and suggests the success of forest invaders is driven by a novel resource-use strategy. Furthermore, two traits alone-annual leaf duration and nuclear DNA content-separated native and invasive species with 93% accuracy, supporting the use of functional traits in invader risk assessments. A trait syndrome reflecting both fast growth capacity and understorey persistence may be a key driver of forest invasions.

Density-dependent plant growth drives grazer stimulation of aboveground net primary production in Yellowstone grasslands.

The mechanisms by which grazing animals influence aboveground net primary production (ANPP) in grasslands have long been an area of active research. The prevailing wisdom is that grazing can increase ANPP by increasing the availability of growth-limiting resources such as nitrogen and water, but recent theory suggests that the density-dependent growth of grassland vegetation can lead to grazer-stimulation of ANPP simply by removing shoot biomass and increasing relative growth rate (RGR). We compared the relative roles of resource availability and density-dependent growth in driving positive responses of ANPP to grazing in Yellowstone National Park. We measured the effects of clipping (50% simulated grazing intensity) and natural grazing on soil nitrogen availability, soil moisture, and shoot growth over 2 months in two grassland plant communities (mesic and dry) grazed primarily by bison. Clipping increased RGR by over 100% in both grassland types but had no effect on N availability or soil moisture during the same growth periods. Clipping stimulated ANPP only at mesic grassland, and the magnitude of this effect was strongly related to the initial plant biomass at the time of clipping relative to estimated peak biomass, supporting the density-dependent framework. Bison grazing had qualitatively similar effects on ANPP and RGR to clipping with no accompanying effects on N availability or soil moisture. Our results show how grazing can stimulate ANPP independent of a direct influence on resource availability simply by exploiting the dynamics of density-dependent plant growth.

More of the same? In situ leaf and root decomposition rates do not vary between 80 native and nonnative deciduous forest species.

Invaders often have greater rates of production and produce more labile litter than natives. The increased litter quantity and quality of invaders should increase nutrient cycling through faster litter decomposition. However, the limited number of invasive species that have been included in decomposition studies has hindered the ability to generalize their impacts on decomposition rates. Further, previous decomposition studies have neglected roots. We measured litter traits and decomposition rates of leaves for 42 native and 36 nonnative woody species, and those of fine roots for 23 native and 25 nonnative species that occur in temperate deciduous forests throughout the Eastern USA. Among the leaf and root traits that differed between native and invasive species, only leaf nitrogen was significantly associated with decomposition rate. However, native and nonnative species did not differ systematically in leaf and root decomposition rates. We found that among the parameters measured, litter decomposer activity was driven by litter chemical quality rather than tissue density and structure. Our results indicate that litter decomposition rate per se is not a pathway by which forest woody invasive species affect North American temperate forest soil carbon and nutrient processes.

Fine-scale belowground species associations in temperate grassland.

Evaluating how belowground processes contribute to plant community dynamics is hampered by limited information on the spatial structure of root communities at the scale that plants interact belowground. In this study, roots were mapped to the nearest one mm and molecularly identified by species on vertical (0-15 cm deep) surfaces of soil blocks excavated from dry and mesic grasslands in Yellowstone National Park (YNP) to examine the spatial relationships among species at the scale that roots interact. Our results indicated that average interspecific root - root distances for the majority of species were within a distance (3 mm) that roots have been shown to compete for resources. Most species placed their roots at random, although low root numbers for many species probably led to overestimating the occurrence of random patterns. According to theory, we expected that most of the remaining species would segregate their root systems to avoid competition. Instead we found that more species aggregated than segregated from others. Based on previous investigations, we hypothesize that species aggregate to increase uptake of water, nitrogen and/or phosphorus made available by neighbouring roots, or as a consequence of a reduction in the pathogenicity of soil biota growing in multispecies mixtures. Our results indicate that YNP grassland root communities are organized as closely interdigitating networks of species that potentially can support strong interactions among many species combinations. Future root research should address the prevalence and functional consequences of species aggregation across plant communities.

Grassland root communities: species distributions and how they are linked to aboveground abundance.

There is little comprehensive information on the distribution of root systems among coexisting species, despite the expected importance of those distributions in determining the composition and diversity of plant communities. This gap in knowledge is particularly acute for grasslands, which possess large numbers of species with morphologically indistinguishable roots. In this study we adapted a molecular method, fluorescent fragment length polymorphism, to identify root fragments and determine species root distributions in two grasslands in Yellowstone National Park (YNP). Aboveground biomass was measured, and soil cores (2 cm in diameter) were collected to depths of 40 cm and 90 cm in an upland, dry grassland and a mesic, slope-bottom grassland, respectively, at peak foliar expansion. Cores were subdivided, and species that occurred in each 10-cm interval were identified. The results indicated that the average number of species in 10-cm intervals (31 cm3) throughout the sampled soil profile was 3.9 and 2.8 species at a dry grassland and a mesic grassland, respectively. By contrast, there was an average of 6.7 and 14.1 species per 0.5 m2, determined by the presence of shoot material, at dry and mesic sites, respectively. There was no relationship between soil depth and number of species per 10-cm interval in either grassland, despite the exponential decline of root biomass with soil depth at both sites. There also was no relationship between root frequency (i.e., the percentage of samples in which a species occurred) and soil depth for the vast majority of species at both sites. The preponderance of species were distributed throughout the soil profile at both sites. Assembly analyses indicated that species root occurrences were randomly assorted in all soil intervals at both sites, with the exception that Festuca idahoensis segregated from Artemisia tridentata and Pseudoroegnaria spicata in 10-20 cm soil at the dry grassland. Root frequency throughout the entire sampled soil profile was positively associated with shoot biomass among species. Together these results indicated the importance of large, well-proliferated root systems in establishing aboveground dominance. The findings suggest that spatial belowground segregation of species probably plays a minor role in fostering resource partitioning and species coexistence in these YNP grasslands.

Ungulate and topographic control of arbuscular mycorrhizal fungal spore community composition in a temperate grassland.

Large herbivores and topo-edaphic gradients are well-documented, major determinants of grassland plant production and species composition. In contrast, there is limited information about how these factors together may influence the composition of the arbuscular mycorrhizal fungus (AMF) communities associated with plants. AMF are a common component of grassland ecosystems where they can influence plant productivity, diversity, and soil stability. In this study, AMF community composition was analyzed in paired plots located inside and outside 40-44-year-old ungulate exclosures at six grassland sites in Yellowstone National Park (YNP), USA, that varied in soil moisture and the availability of soil nitrogen (N) and phosphorus (P). AMF spore abundance, species richness, and the relative abundance of AMF species were determined from soil samples collected (1) randomly (n = 5 samples) within each of the 12 plots and (2) from beneath the dominant grass (n = 5 samples per plot) at each site. Randomly collected soil samples explored the effects of ungulates and topographic position on AMF composition at the plant community level, subsuming potential effects of ungulates on plant species composition. Dominant plant samples examined how grazers, in particular, influenced AMF communities, while controlling for host-plant identity. Grazing decreased AMF spore abundance across the landscape (examined by random sampling) but increased the AMF species richness associated with dominant plants. Grazing influenced the AMF species composition at the plant community level and at the host-plant level by shifting the relative abundances of individual AMF species. Individual AMF species responded differently to grazing and N and P availability. Our results demonstrate how soil moisture and N and P availability across the landscape interact with grazing to influence AMF species composition.

Plant rhizospheric N processes: what we don't know and why we should care.

An improved understanding of the rapid nitrogen fluxes that occur in plant rhizospheres has not been adequately incorporated into the study of how soil N availability and plant N uptake control a number of important ecological processes. One reason for this is that current methods that measure N availability do not account for the rapid exchange of resources between roots and their closely associated microbial communities. In this paper, we review the tight interactions between roots and microbes and discuss why ignoring the significance of these interactions has led to unrepresentative estimates of N availability in intact plant communities and an incomplete understanding of the environmental factors that control plant-available N. We also explain why current standard methods to measure soil N availability do not account for important rhizospheric processes. Finally, we issue a challenge to develop new methods that will estimate soil N transformations in intact plant communities and offer some potential approaches that may help catalyze this effort.

Short sampling intervals reveal very rapid root turnover in a temperate grassland.

Although root growth and mortality play critical regulatory roles in terrestrial ecosystems, little is known about the temporal scale of these dynamics. In temperate grasslands, root dynamics may be particularly rapid because of the high proportion of production allocated to very fine root biomass. In this study, we used minirhizotron tubes to estimate root growth and mortality in an upland grassland in Yellowstone National Park that was grazed by migratory herds of ungulates. Monthly rates of root growth and mortality were estimated from May to September 2005, by measuring the elongation (growth) and disappearance (mortality) of roots at 3-day intervals. Average daily growth (millimeters of root length) was approximately 5 times greater in May and June than in July, August, and September. Average daily mortality (millimeters of root length) did not differ among months. A comparison of the June-September rates of root growth and mortality derived from sampling at short (3-day) and long (1-month) time intervals indicated that the long sampling intervals underestimated both growth and mortality by approximately 60% relative to the short intervals. These results suggest that estimates of grassland root dynamics from minirhizotrons are influenced significantly by sampling interval length, and that rapid root turnover may play a more critical role in regulating energy and nutrient fluxes in temperate grasslands than has previously been recognized.

Drought effects on above- and belowground production of a grazed temperate grassland ecosystem.

The effect of climatic variation on terrestrial aboveground productivity (ANPP) has been well studied. However, little is known about how variable climate, including drought, may influence belowground productivity (BNPP), which constitutes most of the annual primary production of grasslands. The objectives of this study were to (1) examine how a 3-year period of declining moisture, which began as climatically wet to average across Yellowstone National Park (YNP) and ended in drought, affected ANPP and BNPP in grasslands of YNP and (2) how herds of grazing ungulates, which were shown previously to stimulate grassland shoot and root growth in YNP, may have interacted with climatic conditions to influence grassland production. ANPP and 0-20 cm BNPP, representing the bulk of the root dynamics, were measured in grazed and ungrazed (fenced) grassland at nine sites ranging widely in elevation, soil conditions and plant production during the 3-year study. Results revealed that 0-20 cm BNPP was strongly influenced by drought (P = 0.0005) and declined from 1999 to 2001 among ungrazed and grazed grasslands by 39 and 49%, respectively. The greater reduction in 0-20 cm BNPP among grazed grasslands was due, in part, to a decline (P = 0.07) in the stimulatory effect of grazing, i.e., the ratio g BNPP stimulated: g shoot consumed. In contrast, ANPP was unaffected by drought in either type of grassland. Thus, the effect of this drought in YNP was a large reduction in BNPP, which was a function of (1) a direct negative influence of increased moisture stress on root growth and (2) a weak interaction between drought and herbivory that led to a decline in the positive feedback from grazers to BNPP. These findings highlight the need to better understand factors that control root growth and to study the effects of climatic variation on grasslands within an ecosystem framework to include potentially important climate-consumer interactions.

Carbon dioxide fluxes in a spatially and temporally heterogeneous temperate grassland.

Landscape position, grazing, and seasonal variation in precipitation and temperature create spatial and temporal variability in soil processes, and plant biomass and composition in grasslands. However, it is unclear how this variation in plant and soil properties affects carbon dioxide (CO2) fluxes. The aim of this study is to explore the effect of grazing, topographic position, and seasonal variation in soil moisture and temperature on plant assimilation, shoot and soil respiration, and net ecosystem CO2 exchange (NEE). Carbon dioxide fluxes, vegetation, and environmental variables were measured once a month inside and outside long-term ungulate exclosures in hilltop (dry) to slope bottom (mesic) grassland throughout the 2004 growing season in Yellowstone National Park. There was no difference in vegetation properties and CO2 fluxes between the grazed and the ungrazed sites. The spatial and temporal variability in CO2 fluxes were related to differences in aboveground biomass and total shoot nitrogen content, which were both related to variability in soil moisture. All sites were CO2 sinks (NEE>0) for all our measurements taken throughout the growing season; but CO2 fluxes were four- to fivefold higher at sites supporting the most aboveground biomass located at slope bottoms, compared to the sites with low biomass located at hilltops or slopes. The dry sites assimilated more CO2 per gram aboveground biomass and stored proportionally more of the gross-assimilated CO2 in the soil, compared to wet sites. These results indicate large spatio-temporal variability of CO2 fluxes and suggest factors that control the variability in Yellowstone National Park.

The interactive effects of grazing ungulates and aboveground production on grassland diversity.

The variable and nonlinear relationships between plant species richness (SR) and aboveground production (NAP) among terrestrial ecosystems indicate that the energetic capacity of ecosystems interacts with other environmental factors to control diversity. One contributing factor determining plant diversity is herbivory; but few studies have effectively examined the interaction of herbivores and NAP on SR. The objective of this study was to investigate how NAP and herds of native migrating ungulates determine plant SR in grasslands of Yellowstone National Park. Plant SR at peak aboveground biomass was compared inside and outside ungulate exclosures at two spatial scales, 1.0 m2 ("local") and 100 m2 ("community"), in ten variable grasslands. NAP also was determined inside and outside exclosures. The relationship between SR and NAP was unimodal for grazed and ungrazed grassland at both spatial scales. Grazers increased local SR, independent of NAP. In contrast, herbivore effects on community SR ranged from no effect among low-productive grassland to an increasingly positive influence as NAP increased. In addition, ungulates reduced beta diversity (the contribution to community SR attributed to variability among local patches) at dry, low-productive and wet, high-productive sites. These results suggest that the size of the pool of species available to colonize grassland is an important factor controlling the response of grassland SR to herbivory, particularly from low- to intermediate-productive grassland.

Soil community composition and the regulation of grazed temperate grassland.

The effect of the community composition of soil microbes on ecosystem processes has received relatively little attention. Here we examined the variation in soil microbial composition in a Yellowstone National Park grassland and the effect of that variation on the growth, in a greenhouse, of the dominant grass in the community. Plants and their rhizospheric soil were collected from paired, Poa pratensis-dominated grassland plots located inside and outside a 40-year-old exclosure. P. pratensis aboveground, belowground, and whole plant growth were greater in pots with soil communities from grazed grassland compared to fenced grassland, indicating (1) soil microbial communities differed, and (2) this difference influenced the growth of the plant that dominated both grasslands. Treating pots with fungicide (benomyl) suppressed the soil community influence, indicating that different fungal communities caused the soil microbe effect. In addition, two lines of evidence are consistent with the hypothesis that arbuscular mycorrhizal fungal (AMF) species composition affected P. pratensis: (1) a divergence in AMF spore communities in the two field soils, and (2) little evidence of pathogenic fungi. These findings emphasize the need to examine the role that the composition of the soil microbial community plays in controlling terrestrial ecosystems.

Denitrification in a semi-arid grazing ecosystem.

The effect of large herbivores on gaseous N loss from grasslands, particularly via denitrification, is poorly understood. In this study, we examined the influence of native migratory ungulates on denitrification in grasslands of Yellowstone National Park in two ways, by (1) examining the effect of artificial urine application on denitrification, and (2) comparing rates inside and outside long-term exclosures at topographically diverse locations. Artificial urine did not influence denitrification 3 and 12 days after application at hilltop, mid-slope, and slope-bottom sites. Likewise, grazers had no effect on community-level denitrification at dry exclosure sites, where rates were low. At mesic sites, however, ungulates enhanced denitrification by as much as 4 kg N ha-1 year-1, which was double atmospheric N inputs to this ecosystem. Denitrification enzyme activity (DEA, a measure of denitrification potential) was positively associated with soil moisture at exclosure sites, and herbivores stimulated DEA when accounting for the soil moisture effect. Glucose additons to soils increased denitrification and nitrate additions had no influence, suggesting that denitrification was limited by the amount of labile soil carbon, which previously has been shown to be enhanced by ungulates in Yellowstone. These results indicate that denitrification can be an ecologically important flux in portions of semi-arid landscapes, and that there is a previously unsuspected regulation of this process by herbivores.

Herbivore influence on soil microbial biomass and nitrogen mineralization in a northern grassland ecosystem: Yellowstone National Park.

Microorganisms are largely responsible for soil nutrient cycling and energy flow in terrestrial ecosystems. Although soil microorganisms are affected by topography and grazing, little is known about how these two variables may interact to influence microbial processes. Even less is known about how these variables influence microorganisms in systems that contain large populations of free-roaming ungulates. In this study, we compared microbial biomass size and activity, as measured by in situ net N mineralization, inside and outside 35- to 40-year exclosures across a topographic gradient in northern Yellowstone National Park. The objective was to determine the relative effect of topography and large grazers on microbial biomass and nitrogen mineralization. Microbial C and N varied by almost an order of magnitude across sites. Topographic depressions that contained high plant biomass and fine-textured soils supported the greatest microbial biomass. We found that plant biomass accurately predicted microbial biomass across our sites suggesting that carbon inputs from plants constrained microbial biomass. Chronic grazing neither depleted soil C nor reduced microbial biomass. We hypothesize that microbial populations in grazed grasslands are sustained mainly by inputs of labile C from dung deposition and increased root turnover or root exudation beneath grazed plants. Mineral N fluxes were affected more by grazing than topography. Net N mineralization rates were highest in grazed grassland and increased from dry, unproductive to mesic, highly productive communities. Overall, our results indicate that topography mainly influences microbial biomass size, while mineral N fluxes (microbial activity) are affected more by grazing in this grassland ecosystem.

Evidence for the promotion of aboveground grassland production by native large herbivores in Yellowstone National Park.

We examined the effect of native large herbivores on aboveground primary production of nonforested habitat in Yellowstone National Park, Wyoming. Productivity of vegetation grazed by elk (Cervus elaphus) and bison (Bison bison) was compared with that of ungrazed (permanently fenced) vegetation at four sites. Two methods were used that, we believed, would provide the most accurate measurements under the different grazing regimes encountered in the study. Production of ungrazed vegetation in permanent exclosures (10×10 m or 15×15 m, 3 per site) and that of vegetation that was grazed only in the winter was taken as peak standing crop. Production of vegetation grazed during the growing season was the sum of significant increments (P<0.05) in standing crop inside temporary exclosures (1.5×1.5 m, 6 per site) moved every four weeks to account for herbivory.Aboveground productivity of grazed vegetation was .47% higher than that of ungrazed vegetation across sites (P<0.0003). This result could be explained by either a methodological or grazer effect. We believe it was the latter. Results from a computer simulation showed that sequential sampling with temporary exclosures resulted in a slight underestimation of production, suggesting that the reported differences between treatments were conservative. We suggest that stimulation of aboveground production by ungulates may be, in part, due to the migratory behavior of native ungulates that track young, high quality forage as it shifts spatially across the Yellowstone ecosystem.