Kevin E. Mueller

Impacts of Biodiversity Loss Escalate Through Time as Redundancy Fades

Give It Time Experimental ecological studies in recent years have provided a great deal of insight into how species diversify and influence ecosystem properties, but in most cases the experiments have been relatively brief (up to ∼5 years). Reich et al. (p. 589; see the Perspective by Cardinale) performed two 13- and 15-year grassland experiments and found that the effects of plant species richness on community-level processes like biomass production tend to be saturating at early stages but that those impacts grow stronger and more linear as experiments run longer. Stronger influences through time were largely driven by increasing amounts of “complementarity” among species, and these trends were correlated with greater expression of functional diversity in multispecies assemblages. Thus, the effects of diversity grow stronger through time as species gain more and more opportunity to vary in their use of the limiting biological resources in their environment, which emphasizes the functional importance of maintaining diversity in ecosystems. Long-term grassland experiments show that high-diversity species combinations become more functionally diverse with time. Plant diversity generally promotes biomass production, but how the shape of the response curve changes with time remains unclear. This is a critical knowledge gap because the shape of this relationship indicates the extent to which loss of the first few species will influence biomass production. Using two long-term (≥13 years) biodiversity experiments, we show that the effects of diversity on biomass productivity increased and became less saturating over time. Our analyses suggest that effects of diversity-dependent ecosystem feedbacks and interspecific complementarity accumulate over time, causing high-diversity species combinations that appeared functionally redundant during early years to become more functionally unique through time. Consequently, simplification of diverse ecosystems will likely have greater negative impacts on ecosystem functioning than has been suggested by short-term experiments.

Root depth distribution and the diversity-productivity relationship in a long-term grassland experiment

The relationship between plant diversity and productivity in grasslands could depend, partly, on how diversity affects vertical distributions of root biomass in soil; yet, no prior study has evaluated the links among diversity, root depth distributions, and productivity in a long-term experiment. We use data from a 12-year experiment to ask how plant species richness and composition influenced both observed and expected root depth distributions of plant communities. Expected root depth distributions were based on the abundance of species in each community and two traits of species that were measured in monocultures: root depth distributions and root to shoot ratios. The observed proportion of deep root biomass increased more than expected with species richness and was positively correlated with aboveground productivity. Indeed, the proportion of deep root biomass explained variation in productivity even after accounting for legume presence/abundance, and greater nitrogen availability in diverse plots. Diverse plots had root depth distributions that were twice as deep as expected from their species composition and corresponding monoculture traits, partly due to interactions between C4 grasses and legumes. These results suggest the productivity of diverse plant communities was partly dependent on belowground plant interactions that caused roots to be distributed more deeply in soil.

Integrating plant litter quality, soil organic matter stabilization, and the carbon saturation concept

Labile, high-quality, plant litters are hypothesized to promote soil organic matter (SOM) stabilization in mineral soil fractions that are physicochemically protected from rapid mineralization. However, the effect of litter quality on SOM stabilization is inconsistent. High-quality litters, characterized by high N concentrations, low C/N ratios, and low phenol/lignin concentrations, are not consistently stabilized in SOM with greater efficiency than low-quality litters characterized by low N concentrations, high C/N ratios, and high phenol/lignin concentrations. Here, we attempt to resolve these inconsistent results by developing a new conceptual model that links litter quality to the soil C saturation concept. Our model builds on the Microbial Efficiency-Matrix Stabilization framework (Cotrufo etxa0al., 2013) by suggesting the effect of litter quality on SOM stabilization is modulated by the extent of soil C saturation such that high-quality litters are not always stabilized in SOM with greater efficiency than low-quality litters.

Impacts of warming and elevated CO2 on a semi‐arid grassland are non‐additive, shift with precipitation, and reverse over time

It is unclear how elevated CO2 (eCO2 ) and the corresponding shifts in temperature and precipitation will interact to impact ecosystems over time. During a 7-year experiment in a semi-arid grassland, the response of plant biomass to eCO2 and warming was largely regulated by interannual precipitation, while the response of plant community composition was more sensitive to experiment duration. The combined effects of eCO2 and warming on aboveground plant biomass were less positive in wet growing seasons, but total plant biomass was consistently stimulated by ~xa025% due to unique, supra-additive responses of roots. Independent of precipitation, the combined effects of eCO2 and warming on C3 graminoids became increasingly positive and supra-additive over time, reversing an initial shift toward C4 grasses. Soil resources also responded dynamically and non-additively to eCO2 and warming, shaping the plant responses. Our results suggest grasslands are poised for drastic changes in function and highlight the need for long-term, factorial experiments.

Effects of plant diversity, N fertilization, and elevated carbon dioxide on grassland soil N cycling in a long-term experiment

The effects of global environmental changes on soil nitrogen (N) pools and fluxes have consequences for ecosystem functions such as plant productivity and N retention. In a 13-year grassland experiment, we evaluated how elevated atmospheric carbon dioxide (CO2 ), N fertilization, and plant species richness alter soil N cycling. We focused on soil inorganic N pools, including ammonium and nitrate, and two N fluxes, net N mineralization and net nitrification. In contrast with existing hypotheses, such as progressive N limitation, and with observations from other, often shorter, studies, elevated CO2 had relatively static and small, or insignificant, effects on soil inorganic N pools and fluxes. Nitrogen fertilization had inconsistent effects on soil N transformations, but increased soil nitrate and ammonium concentrations. Plant species richness had increasingly positive effects on soil N transformations over time, likely because in diverse subplots the concentrations of N in roots increased over time. Species richness also had increasingly positive effects on concentrations of ammonium in soil, perhaps because more carbon accumulated in soils of diverse subplots, providing exchange sites for ammonium. By contrast, subplots planted with 16 species had lower soil nitrate concentrations than less diverse subplots, especially when fertilized, probably due to greater N uptake capacity of subplots with 16 species. Monocultures of different plant functional types had distinct effects on N transformations and nitrate concentrations, such that not all monocultures differed from diverse subplots in the same manner. The first few years of data would not have adequately forecast the effects of N fertilization and diversity on soil N cycling in later years; therefore, the dearth of long-term manipulations of plant species richness and N inputs is a hindrance to forecasting the state of the soil N cycle and ecosystem functions in extant plant communities.

Effects of litter traits, soil biota, and soil chemistry on soil carbon stocks at a common garden with 14 tree species

Tree species interact with soil biota to impact soil organic carbon (C) pools, but it is unclear how this interaction is shaped by various ecological factors. We used multiple regression to describe how ~100 variables were related to soil organic C pools in a common garden experiment with 14 temperate tree species. Potential predictor variables included: (i) the abundance, chemical composition, and decomposition rates of leaf litter and fine roots, (ii) species richness and abundance of bacteria, fungi, and invertebrate animals in soil, and (iii) measures of soil acidity and texture. The amount of organic C in the organic horizon and upper 20xa0cm of mineral soil (i.e. the combined C pool) was strongly negatively correlated with earthworm abundance and strongly positively correlated with the abundance of aluminum, iron, and protons in mineral soils. After accounting for these factors, we identified additional correlations with soil biota and with litter traits. Rates of leaf litter decomposition, measured as litter mass loss, were negatively correlated with size of the combined soil organic C pool. Somewhat paradoxically, the combined soil organic C pool was also negatively related to the ratio of recalcitrant compounds to nitrogen in leaf litter. These apparent effects of litter traits probably arose because two independent components of litter “quality” were controlling different aspects of decomposition. Leaf litter mass loss rates were positively related with leaf litter calcium concentrations, reflecting greater utilization and depolymerization of calcium-rich leaf litter by earthworms and other soil biota, which presumably led to greater proportional losses of litter C as CO2 or dissolved organic C. The fraction of depolymerized and metabolized litter that is ultimately lost as CO2 is an inverse function of microbial C use efficiency, which increases with litter nutrient concentrations but decreases with concentrations of recalcitrant compounds (e.g. lignin); thus, high ratios of recalcitrant compounds to nitrogen in leaf litter likely caused a greater fraction of depolymerized litter to be lost as CO2. Existing conceptual models of soil C stabilization need to reconcile the effects of litter quality on these two potentially counteracting factors: rates of litter depolymerization and microbial C use efficiency.

Grazing intensity differentially regulates ANPP response to precipitation in North American semiarid grasslands

Grazing intensity elicits changes in the composition of plant functional groups in both shortgrass steppe (SGS) and northern mixed-grass prairie (NMP) in North America. How these grazing intensity-induced changes control aboveground net primary production (ANPP) responses to precipitation remains a central open question, especially in light of predicted climate changes. Here, we evaluated effects of four levels (none, light, moderate, and heavy) of long-term (>30xa0yr) grazing intensity in SGS and NMP on: (1) ANPP; (2) precipitation-use efficiency (PUE, ANPP : precipitation); and (3) precipitation marginal response (PMR; slope of a linear regression model between ANPP and precipitation). We advance prior work by examining: (1) the consequences of a range of grazing intensities (more grazed vs. ungrazed); and (2) how grazing-induced changes in ANPP and PUE are related both to shifts in functional group composition and physiological responses within each functional group. Spring (April-June) precipitation, the primary determinant of ANPP, was only 12% higher in NMP than in SGS, yet ANPP and PUE were 25% higher. Doubling grazing intensity in SGS and nearly doubling it in NMP reduced ANPP and PUE by only 24% and 33%, respectively. Increased grazing intensity reduced C3 graminoid biomass and increased C4 grass biomass in both grasslands. Functional group shifts affected PUE through biomass reductions, as PUE was positively associated with the relative abundance of C3 species and negatively with C4 species across both grasslands. At the community level, PMR was similar between grasslands and unaffected by grazing intensity. However, PMR of C3 graminoids in SGS was eightfold higher in the ungrazed treatment than under any grazed level. In NMP, PMR of C3 graminoids was only reduced under heavy grazing intensity. Knowing the ecological consequences of grazing intensity provides valuable information for mitigation and adaptation strategies in response to predicted climate change. For example, moderate grazing (the recommended rate) in SGS would sequester the same amount of aboveground carbon as light grazing because ANPP was nearly the same. In contrast, reductions in grazing intensity in NMP from moderate to light intensity would increase the amount of aboveground carbon sequestrated by 25% because of increased ANPP.

Thresholds and gradients in a semi‐arid grassland: long‐term grazing treatments induce slow, continuous and reversible vegetation change

1. Temporal changes in semi-arid ecosystems can include transitions between alternative stable states, involving thresholds and multiple domains of attraction, but can also include relatively continuous, symmetric and reversible shifts within a single stable state. Conceptual state-and-transition models (STMs) describe both types of ecosystem dynamics by including state transitions (plant community changes difficult-to-reverse without substantial input or effort) and phase shifts (easily reversible community changes) as consequences of management practices and environmental variability. Grazing management is purported to be the primary driver of state transitions in current STMs for North American grasslands, but there is limited empirical evidence from these grasslands showing that grazing can cause difficult-toreverse transitions between alternate stable states. 2. In a northern mixed-grass prairie in Wyoming, USA, we examined plant community responses to (i) long-term (33-year) grazing intensity treatments (none, light, moderate and heavy stocking rates) and (ii) 8 years of light or no grazing in pastures that were grazed heavily for the previous 25 years. 3. Long-term grazing treatments were associated with distinct, but not stable, plant communities. From year 22 to 33, heavier stocking rates decreased cover of dominant C3 grasses and increased cover of the dominant C4 grass Bouteloua gracilis. 4. Reversing stocking rates from heavy to light or no grazing resulted in reversal of changes induced by prior heavy stocking for dominant C3 grasses, but not for B. gracilis. For both groups, rates of change following grazing treatment reversals were consistent with rates of change during the initial years of the experiment (1982–1990). 5. Synthesis and applications. In a semi-arid rangeland with a long evolutionary history of grazing, different long-term grazing intensity treatments caused slow, continuous and directional changes with important management implications, but did not appear to induce alternative stable states. For this and similar ecosystems, quantifying the time-scales and compositional gradients associated with key phase shifts may be more important than identifying thresholds between alternative stable states.

A tale of two studies: detection and attribution of the impacts of invasive plants in observational surveys

1.Short-term experiments cannot characterize how long-lived, invasive shrubs influence ecological properties that can be slow to change, including native diversity and soil fertility. Observational studies are thus necessary, but often suffer from methodological issues. n n2.To highlight ways of improving the design and interpretation of observational studies that assess the impacts of invasive plants, we compare two studies of nutrient cycling and earthworms along two separate gradients of invasive shrub abundance. By considering the divergent sampling strategies and statistical analyses of these two studies, and interpreting their contradictory results in the context of other studies, we also aim to better describe the impacts of the focal invader, Rhamnus cathartica. n n3.In a new study of a single site in Minnesota, we observed positive correlations between buckthorn abundance and soil pH, soil nutrient pools, nutrient fluxes through leaf litterfall, earthworm abundance, and root biomass. Multiple regression models showed these relationships persisted after accounting for variability in soil texture and tree species composition. For a separate, more expansive study in Illinois, other authors reported little to no correlation between buckthorn abundance and 10 soil properties, including earthworm abundance, pH, and nutrient concentrations. However, like many other studies, their regression models only assessed predictors related to invader abundance. R2 values for models of ecosystem properties ranged from 0-0.79 (adjusted-R2) for our study in Minnesota and from <0.05-0.16 (unadjusted) for the prior study in Illinois. n n4.Differences in sampling error and use of predictor variables between the two studies likely explain the contrasting results. n n5.Synthesis and applications. To reduce the uncertainty of conclusions from observational studies of invasive plants, future studies must ensure that heterogeneity of soils and vegetation is adequately accounted for in the sampling strategy and statistical analyses (e.g., analysis of covariance, multiple regression). Particular attention should be given to ecosystem properties with variability that likely predates the invader (e.g., geophysical features and tree community composition). In our study, effects of buckthorn on ecosystem properties were not only robust to the inclusion of potentially confounding predictors, but also consistent with expectations based on ecological stoichiometry and mass balance of element flow. n nThis article is protected by copyright. All rights reserved.

Increase grants, too.

The News Focus story “Reshuffling graduate training” (J. Mervis, 31 July, p. [528][1]) suggests that a change in graduate student funding from grants to fellowships and traineeships will increase the independence of young scientists and boost U.S. science. We agree, but caution that shifting resources to fellowship programs could fail to produce desired results without additional increases in direct support for graduate student research.nnOur graduate educations are funded by a U.S. Department of Agriculture National Needs Traineeship and a U.S. Department of Energy Graduate Research Environmental Fellowship. Similar to fellowship programs funded by NSF, NIH, or the EPA, these training programs are prestigious but provide little or no research funding. Accordingly, recipients often work on ideas that are closely affiliated with existing grants rather than developing independent research. Moreover, the effectiveness of NSF Graduate Research Fellowships may also be limited by eligibility requirements that exclude students with masters degrees.nnStudents with a masters degree may be more prepared for independent research compared to counterparts with a bachelors degree. Nonetheless, training and fellowship programs can spur independence. We used our fellowships as a platform to compete for research grants. Research grants that we received from NSF and NOAA provide independence to develop our own ideas and experiments. An increase in research fellowships together with a substantial increase in research grants would be a more effective way to encourage graduate student creativity, autonomy, and success.nn [1]: /lookup/doi/10.1126/science.325_528