Publications by authors named "Eric W Seabloom"

96 Publications

Nitrogen and phosphorus fertilization consistently favor pathogenic over mutualistic fungi in grassland soils.

Nat Commun 2021 06 9;12(1):3484. Epub 2021 Jun 9.

Department of Ecology, Evolution, and Behavior, University of Minnesota, St Paul, MN, USA.

Ecosystems across the globe receive elevated inputs of nutrients, but the consequences of this for soil fungal guilds that mediate key ecosystem functions remain unclear. We find that nitrogen and phosphorus addition to 25 grasslands distributed across four continents promotes the relative abundance of fungal pathogens, suppresses mutualists, but does not affect saprotrophs. Structural equation models suggest that responses are often indirect and primarily mediated by nutrient-induced shifts in plant communities. Nutrient addition also reduces co-occurrences within and among fungal guilds, which could have important consequences for belowground interactions. Focusing only on plots that received no nutrient addition, soil properties influence pathogen abundance globally, whereas plant community characteristics influence mutualists, and climate influence saprotrophs. We show consistent, guild-level responses that enhance our ability to predict shifts in soil function related to anthropogenic eutrophication, which can have longer-term consequences for plant communities.
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http://dx.doi.org/10.1038/s41467-021-23605-yDOI Listing
June 2021

Community change can buffer chronic nitrogen impacts, but multiple nutrients tip the scale.

Ecology 2021 Jun 7;102(6):e03355. Epub 2021 May 7.

Department of Ecology, Evolution, and Behavior, University of Minnesota, 1987 Upper Buford Circle, St. Paul, Minnesota, 55108, USA.

Anthropogenic nitrogen (N) inputs are causing large changes in ecosystems worldwide. Many previous studies have examined the impact of N on terrestrial ecosystems; however, most have added N at rates that are much higher than predicted future deposition rates. Here, we present the results from a gradient of experimental N addition (0-10 g·N·m ) in a temperate grassland. After a decade of N addition, we found that all levels of N addition changed plant functional group composition, likely indicating altered function for plant communities exposed to 10 yr of N inputs. However, N addition only had weak impacts on species composition and this functional group shift was not driven by any particular species, suggesting high levels of functional redundancy among grasslands species. Adding other nutrients (P, K, and micronutrients) in combination with N caused substantially greater changes in the relative abundance of species and functional groups. Together, these results suggest that compositional change within functional groups may buffer grasslands from impacts of N deposition, but concurrent eutrophication with other elements will likely lead to substantial changes in plant composition and biomass.
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http://dx.doi.org/10.1002/ecy.3355DOI Listing
June 2021

Pliant pathogens: Estimating viral spread when confronted with new vector, host, and environmental conditions.

Ecol Evol 2021 Feb 26;11(4):1877-1887. Epub 2021 Jan 26.

Department of Ecology, Evolution, and Behavior University of Minnesota St. Paul MN USA.

Pathogen spread rates are determined, in part, by the performance of pathogens under altered environmental conditions and their ability to persist while switching among hosts and vectors.To determine the effects of new conditions (host, vector, and nutrient) on pathogen spread rate, we introduced a vector-borne viral plant pathogen, Barley Yellow Dwarf Virus PAV (BYDV-PAV) into hosts, vectors, and host nutrient supplies that it had not encountered for thousands of viral generations. We quantified pathogen prevalence over the course of two serial inoculations under the new conditions. Using individual-level transmission rates from this experiment, we parameterized a dynamical model of disease spread and projected spread across host populations through a growing season.A change in nutrient conditions (increased supply of phosphorus) reduced viral transmission whereas shifting to a new vector or host species had no effect on infection prevalence. However, the reduction in the new nutrient environment was only temporary; infection prevalence recovered after the second inoculation. . These results highlight how robust the pathogen, BYDV-PAV, is to changes in its biotic and abiotic environment. Our study also highlights the need to quantify longitudinal infection information beyond snapshot assessments to project disease risk for pathogens in new environments.
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http://dx.doi.org/10.1002/ece3.7178DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7882977PMC
February 2021

Lessons from movement ecology for the return to work: Modeling contacts and the spread of COVID-19.

PLoS One 2021 22;16(1):e0242955. Epub 2021 Jan 22.

Department of Ecology, Evolution, and Behavior, University of Minnesota, St. Paul, Minnesota, United States of America.

Human behavior (movement, social contacts) plays a central role in the spread of pathogens like SARS-CoV-2. The rapid spread of SARS-CoV-2 was driven by global human movement, and initial lockdown measures aimed to localize movement and contact in order to slow spread. Thus, movement and contact patterns need to be explicitly considered when making reopening decisions, especially regarding return to work. Here, as a case study, we consider the initial stages of resuming research at a large research university, using approaches from movement ecology and contact network epidemiology. First, we develop a dynamical pathogen model describing movement between home and work; we show that limiting social contact, via reduced people or reduced time in the workplace are fairly equivalent strategies to slow pathogen spread. Second, we develop a model based on spatial contact patterns within a specific office and lab building on campus; we show that restricting on-campus activities to labs (rather than labs and offices) could dramatically alter (modularize) contact network structure and thus, potentially reduce pathogen spread by providing a workplace mechanism to reduce contact. Here we argue that explicitly accounting for human movement and contact behavior in the workplace can provide additional strategies to slow pathogen spread that can be used in conjunction with ongoing public health efforts.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0242955PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7822505PMC
February 2021

Foliar fungi and plant diversity drive ecosystem carbon fluxes in experimental prairies.

Ecol Lett 2021 Mar 9;24(3):487-497. Epub 2020 Dec 9.

Department of Ecology, Evolution and Behavior, University of Minnesota, Twin Cities, Saint Paul, MI, USA.

Plant diversity and plant-consumer/pathogen interactions likely interact to influence ecosystem carbon fluxes but experimental evidence is scarce. We examined how experimental removal of foliar fungi, soil fungi and arthropods from experimental prairies planted with 1, 4 or 16 plant species affected instantaneous rates of carbon uptake (GPP), ecosystem respiration (R ) and net ecosystem exchange (NEE). Increasing plant diversity increased plant biomass, GPP and R , but NEE remained unchanged. Removing foliar fungi increased GPP and NEE, with the greatest effects at low plant diversity. After accounting for plant biomass, we found that removing foliar fungi increased mass-specific flux rates in the low-diversity plant communities by altering plant species composition and community-wide foliar nitrogen content. However, this effect disappeared when soil fungi and arthropods were also removed, demonstrating that both plant diversity and interactions among consumer groups determine the ecosystem-scale effects of plant-fungal interactions.
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http://dx.doi.org/10.1111/ele.13663DOI Listing
March 2021

General destabilizing effects of eutrophication on grassland productivity at multiple spatial scales.

Nat Commun 2020 10 23;11(1):5375. Epub 2020 Oct 23.

Department of Ecology, Evolution, and Behavior, University of MN, St. Paul, MN, 55108, USA.

Eutrophication is a widespread environmental change that usually reduces the stabilizing effect of plant diversity on productivity in local communities. Whether this effect is scale dependent remains to be elucidated. Here, we determine the relationship between plant diversity and temporal stability of productivity for 243 plant communities from 42 grasslands across the globe and quantify the effect of chronic fertilization on these relationships. Unfertilized local communities with more plant species exhibit greater asynchronous dynamics among species in response to natural environmental fluctuations, resulting in greater local stability (alpha stability). Moreover, neighborhood communities that have greater spatial variation in plant species composition within sites (higher beta diversity) have greater spatial asynchrony of productivity among communities, resulting in greater stability at the larger scale (gamma stability). Importantly, fertilization consistently weakens the contribution of plant diversity to both of these stabilizing mechanisms, thus diminishing the positive effect of biodiversity on stability at differing spatial scales. Our findings suggest that preserving grassland functional stability requires conservation of plant diversity within and among ecological communities.
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http://dx.doi.org/10.1038/s41467-020-19252-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7585434PMC
October 2020

Increasing effects of chronic nutrient enrichment on plant diversity loss and ecosystem productivity over time.

Ecology 2021 02 18;102(2):e03218. Epub 2021 Jan 18.

Department of Ecology, Evolution, and Behavior, University of Minnesota, St. Paul, Minnesota, 55108, USA.

Human activities are enriching many of Earth's ecosystems with biologically limiting mineral nutrients such as nitrogen (N) and phosphorus (P). In grasslands, this enrichment generally reduces plant diversity and increases productivity. The widely demonstrated positive effect of diversity on productivity suggests a potential negative feedback, whereby nutrient-induced declines in diversity reduce the initial gains in productivity arising from nutrient enrichment. In addition, plant productivity and diversity can be inhibited by accumulations of dead biomass, which may be altered by nutrient enrichment. Over longer time frames, nutrient addition may increase soil fertility by increasing soil organic matter and nutrient pools. We examined the effects of 5-11 yr of nutrient addition at 47 grasslands in 12 countries. Nutrient enrichment increased aboveground live biomass and reduced plant diversity at nearly all sites, and these effects became stronger over time. We did not find evidence that nutrient-induced losses of diversity reduced the positive effects of nutrients on biomass; however, nutrient effects on live biomass increased more slowly at sites where litter was also increasing, regardless of plant diversity. This work suggests that short-term experiments may underestimate the long-term nutrient enrichment effects on global grassland ecosystems.
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http://dx.doi.org/10.1002/ecy.3218DOI Listing
February 2021

Elements of disease in a changing world: modelling feedbacks between infectious disease and ecosystems.

Ecol Lett 2021 Jan 12;24(1):6-19. Epub 2020 Oct 12.

National Socio-Environmental Synthesis Center, Annapolis, MD, 21401, USA.

An overlooked effect of ecosystem eutrophication is the potential to alter disease dynamics in primary producers, inducing disease-mediated feedbacks that alter net primary productivity and elemental recycling. Models in disease ecology rarely track organisms past death, yet death from infection can alter important ecosystem processes including elemental recycling rates and nutrient supply to living hosts. In contrast, models in ecosystem ecology rarely track disease dynamics, yet elemental nutrient pools (e.g. nitrogen, phosphorus) can regulate important disease processes including pathogen reproduction and transmission. Thus, both disease and ecosystem ecology stand to grow as fields by exploring questions that arise at their intersection. However, we currently lack a framework explicitly linking these disciplines. We developed a stoichiometric model using elemental currencies to track primary producer biomass (carbon) in vegetation and soil pools, and to track prevalence and the basic reproduction number (R ) of a directly transmitted pathogen. This model, parameterised for a deciduous forest, demonstrates that anthropogenic nutrient supply can interact with disease to qualitatively alter both ecosystem and disease dynamics. Using this element-focused approach, we identify knowledge gaps and generate predictions about the impact of anthropogenic nutrient supply rates on infectious disease and feedbacks to ecosystem carbon and nutrient cycling.
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http://dx.doi.org/10.1111/ele.13617DOI Listing
January 2021

Plant diversity and litter accumulation mediate the loss of foliar endophyte fungal richness following nutrient addition.

Ecology 2021 01 1;102(1):e03210. Epub 2020 Dec 1.

Department of Ecology, Evolution, and Behavior, University of Minnesota, St Paul, Minnesota, 55108, USA.

Foliar fungal endophytes are ubiquitous plant symbionts that can affect plant growth and reproduction via their roles in pathogen and stress tolerance, as well as plant hormonal signaling. Despite their importance, we have a limited understanding of how foliar fungal endophytes respond to varying environmental conditions such as nutrient inputs. The responses of foliar fungal endophyte communities to increased nutrient deposition may be mediated by the simultaneous effects on within-host competition as well as the indirect impacts of altered host population size, plant productivity, and plant community diversity and composition. Here, we leveraged a 7-yr experiment manipulating nitrogen, phosphorus, potassium, and micronutrients to investigate how nutrient-induced changes to plant diversity, plant productivity, and plant community composition relate to changes in foliar fungal endophyte diversity and richness in a focal native grass host, Andropogon gerardii. We found limited evidence of direct effects of nutrients on endophyte diversity. Instead, the effects of nutrients on endophyte diversity appeared to be mediated by accumulation of plant litter and plant diversity loss. Specifically, nitrogen addition is associated with a 40% decrease in plant diversity and an 11% decrease in endophyte richness. Although nitrogen, phosphorus, and potassium addition increased aboveground live biomass and decreased relative Andropogon cover, endophyte diversity did not covary with live plant biomass or Andropogon cover. Our results suggest that fungal endophyte diversity within this focal host is determined in part by the diversity of the surrounding plant community and its potential impact on immigrant propagules and dispersal dynamics. Our results suggest that elemental nutrients reduce endophyte diversity indirectly via impacts on the local plant community, not direct response to nutrient addition. Thus, the effects of global change drivers, such as nutrient deposition, on characteristics of host populations and the diversity of their local communities are important for predicting the response of symbiont communities in a changing global environment.
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http://dx.doi.org/10.1002/ecy.3210DOI Listing
January 2021

Grassland ecosystem recovery after soil disturbance depends on nutrient supply rate.

Ecol Lett 2020 Dec 17;23(12):1756-1765. Epub 2020 Sep 17.

Department of Ecology, Evolution, and Behavior, University of MN, St. Paul, MN, 55108, USA.

Human disturbances alter the functioning and biodiversity of many ecosystems. These ecosystems may return to their pre-disturbance state after disturbance ceases; however, humans have altered the environment in ways that may change the rate or direction of this recovery. For example, human activities have increased supplies of biologically limiting nutrients, such as nitrogen (N) and phosphorus (P), which can reduce grassland diversity and increase productivity. We tracked the recovery of a grassland for two decades following an intensive agricultural disturbance under ambient and elevated nutrient conditions. Productivity returned to pre-disturbance levels quickly under ambient nutrient conditions, but nutrient addition slowed this recovery. In contrast, the effects of disturbance on diversity remained hidden for 15 years, at which point diversity began to increase in unfertilised plots. This work demonstrates that enrichment of terrestrial ecosystems by humans may alter the recovery of ecosystems and that disturbance effects may remain hidden for many years.
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http://dx.doi.org/10.1111/ele.13591DOI Listing
December 2020

Global impacts of fertilization and herbivore removal on soil net nitrogen mineralization are modulated by local climate and soil properties.

Glob Chang Biol 2020 Dec 22;26(12):7173-7185. Epub 2020 Sep 22.

Grupo de Investigaciones en Biología de la Conservación, INIBIOMA (CONICET-UNCOMA), Bariloche, Argentina.

Soil nitrogen (N) availability is critical for grassland functioning. However, human activities have increased the supply of biologically limiting nutrients, and changed the density and identity of mammalian herbivores. These anthropogenic changes may alter net soil N mineralization (soil net N ), that is, the net balance between N mineralization and immobilization, which could severely impact grassland structure and functioning. Yet, to date, little is known about how fertilization and herbivore removal individually, or jointly, affect soil net N across a wide range of grasslands that vary in soil and climatic properties. Here we collected data from 22 grasslands on five continents, all part of a globally replicated experiment, to assess how fertilization and herbivore removal affected potential (laboratory-based) and realized (field-based) soil net N . Herbivore removal in the absence of fertilization did not alter potential and realized soil net N . However, fertilization alone and in combination with herbivore removal consistently increased potential soil net N Realized soil net N , in contrast, significantly decreased in fertilized plots where herbivores were removed. Treatment effects on potential and realized soil net N were contingent on site-specific soil and climatic properties. Fertilization effects on potential soil net N were larger at sites with higher mean annual precipitation (MAP) and temperature of the wettest quarter (T.q.wet). Reciprocally, realized soil net N declined most strongly with fertilization and herbivore removal at sites with lower MAP and higher T.q.wet. In summary, our findings show that anthropogenic nutrient enrichment, herbivore exclusion and alterations in future climatic conditions can negatively impact soil net N across global grasslands under realistic field conditions. This is an important context-dependent knowledge for grassland management worldwide.
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http://dx.doi.org/10.1111/gcb.15308DOI Listing
December 2020

Nutritional constraints on brain evolution: Sodium and nitrogen limit brain size.

Evolution 2020 10 15;74(10):2304-2319. Epub 2020 Aug 15.

Department of Ecology, Evolution and Behavior, University of Minnesota, Minneapolis, Minnesota, 55455.

Nutrition has been hypothesized as an important constraint on brain evolution. However, it is unclear whether the availability of specific nutrients or the difficulty of locating high-quality diets limits brain evolution, especially over long periods of time. We found that dietary nutrient content predicted brain size across 42 species of butterflies. Brain size, relative to body size, was associated with the sodium and nitrogen content of a species' diet. There was no evidence that host plant apparency (measured by plant height) was related to brain evolution. The timing of diet shifts across species varied from 3.5 to 90 million years ago, but nutritional constraints did not lessen over time as species adapted to a diet. Although nutrition was linked to overall brain volume, there was no evidence that nutrition was related to the relative size of individual brain regions. Laboratory rearing experiments confirmed the underlying assumption of most comparative studies that the majority of interspecific trait variation stems from genetically based differences across species rather than developmental plasticity. This study highlights a novel role of sodium and nitrogen in brain evolution, which is additionally interesting given current anthropogenic change in the availability of these nutrients.
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http://dx.doi.org/10.1111/evo.14072DOI Listing
October 2020

Host nutrition mediates interactions between plant viruses, altering transmission and predicted disease spread.

Ecology 2020 11 2;101(11):e03155. Epub 2020 Sep 2.

Department of Ecology, Evolution, and Behavior, University of Minnesota, St. Paul, Minnesota, 55108, USA.

Interactions among co-infecting pathogens are common across host taxa and can affect infectious disease dynamics. Host nutrition can mediate these among-pathogen interactions, altering the establishment and growth of pathogens within hosts. It is unclear, however, how nutrition-mediated among-pathogen interactions affect transmission and the spread of disease through populations. We manipulated the nitrogen (N) and phosphorus (P) supplies to oat plants in growth chambers and evaluated interactions between two aphid-vectored Barley and Cereal Yellow Dwarf Viruses: PAV and RPV. We quantified the effect of each virus on the other's establishment, within-plant density, and transmission. Co-inoculation significantly increased PAV density when N and P supplies were low and tended to increase RPV density when N supply was high. Co-infection increased PAV transmission when N and P supplies were low and tended to increase RPV transmission when N supply was high. Despite the parallels between the effects of among-pathogen interactions on density and transmission, changes in virus density only partially explained changes in transmission, suggesting that virus density-independent processes contribute to transmission. A mathematical model describing the spread of two viruses through a plant population, parameterized with empirically derived transmission values, demonstrated that nutrition-mediated among-pathogen interactions could affect disease spread. Interactions that altered transmission through virus density-independent processes determined overall disease dynamics. Our work suggests that host nutrition alters disease spread through among-pathogen interactions that modify transmission.
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http://dx.doi.org/10.1002/ecy.3155DOI Listing
November 2020

Reducing dispersal limitation via seed addition increases species richness but not above-ground biomass.

Ecol Lett 2020 Oct 21;23(10):1442-1450. Epub 2020 Jun 21.

German Centre for Integrative Biodiversity Research (iDiv) Leipzig-Halle-Jena, Deutscher Platz 5e, Leipzig, 04103, Germany.

Seed dispersal limitation, which can be exacerbated by a number of anthropogenic causes, can result in local communities having fewer species than they might potentially support, representing a potential diversity deficit. The link between processes that shape natural variation in diversity, such as dispersal limitation, and the consequent effects on productivity is less well known. Here, we synthesised data from 12 seed addition experiments in grassland communities to examine the influence of reducing seed dispersal limitation (from 1 to 60 species added across experiments) on species richness and productivity. For every 10 species of seed added, we found that species richness increased by about two species. However, the increase in species richness by overcoming seed limitation did not lead to a concomitant increase in above-ground biomass production. This highlights the need to consider the relationship between biodiversity and ecosystem functioning in a pluralistic way that considers both the processes that shape diversity and productivity simultaneously in naturally assembled communities.
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http://dx.doi.org/10.1111/ele.13566DOI Listing
October 2020

Disease-mediated ecosystem services: Pathogens, plants, and people.

Trends Ecol Evol 2020 08 15;35(8):731-743. Epub 2020 Jun 15.

Department of Ecology, Evolution, and Behavior, University of Minnesota, St. Paul, MN, USA.

Despite the ubiquity of pathogens in ecological systems, their roles in influencing ecosystem services are often overlooked. Pathogens that infect primary producers (i.e., plants, algae, cyanobacteria) can have particularly strong effects because autotrophs are responsible for a wide range of provisioning, regulating, and cultural services. We review the roles of pathogens in mediating ecosystem services provided by autotrophs and outline scenarios in which infection may lead to unexpected outcomes in response to global change. Our synthesis highlights a deficit of information on this topic, and we outline a vision for future research that includes integrative theory and cross-system empirical studies. Ultimately, knowledge about the mediating roles of pathogens on ecosystem services should inform environmental policy and practice.
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http://dx.doi.org/10.1016/j.tree.2020.04.003DOI Listing
August 2020

Microbial processing of plant remains is co-limited by multiple nutrients in global grasslands.

Glob Chang Biol 2020 08 10;26(8):4572-4582. Epub 2020 Jun 10.

German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Leipzig, Germany.

Microbial processing of aggregate-unprotected organic matter inputs is key for soil fertility, long-term ecosystem carbon and nutrient sequestration and sustainable agriculture. We investigated the effects of adding multiple nutrients (nitrogen, phosphorus and potassium plus nine essential macro- and micro-nutrients) on decomposition and biochemical transformation of standard plant materials buried in 21 grasslands from four continents. Addition of multiple nutrients weakly but consistently increased decomposition and biochemical transformation of plant remains during the peak-season, concurrent with changes in microbial exoenzymatic activity. Higher mean annual precipitation and lower mean annual temperature were the main climatic drivers of higher decomposition rates, while biochemical transformation of plant remains was negatively related to temperature of the wettest quarter. Nutrients enhanced decomposition most at cool, high rainfall sites, indicating that in a warmer and drier future fertilized grassland soils will have an even more limited potential for microbial processing of plant remains.
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http://dx.doi.org/10.1111/gcb.15146DOI Listing
August 2020

Strong mineralogic control of soil organic matter composition in response to nutrient addition across diverse grassland sites.

Sci Total Environ 2020 Sep 6;736:137839. Epub 2020 Apr 6.

Earth and Biological Sciences Directorate, Pacific Northwest National Laboratory, 902 Battelle Blvd, Richland, WA 99354, USA; Department of Ecology, Evolution & Organismal Biology, Iowa State University, 251 Bessey Hall, Ames, IA 50011, USA. Electronic address:

Soil organic matter (SOM) dynamics are central to soil biogeochemistry and fertility. The retention of SOM is governed initially by interactions with minerals, which mediate the sorption of chemically diverse organic matter (OM) molecules via distinct surface areas and chemical functional group availabilities. Unifying principles of mineral-OM interactions remain elusive because of the multi-layered nature of biochemical-mineral interactions that contribute to soil aggregate formation and the heterogeneous nature of soils among ecosystems. This study sought to understand how soil mineralogy as well as nitrogen (N) enrichment regulate OM composition in grassland soils. Using a multi-site grassland experiment, we demonstrate that the composition of mineral-associated OM depended on the clay content and specific mineral composition in soils across the sites. With increasing abundance of ferrihydrite (Fh) across six different grassland locations, OM in the hydrophobic zone became more enriched in lipid- and protein-like compounds, whereas the kinetic zone OM became more enriched in lignin-like molecules. These relationships suggest that the persistence of various classes of OM in soils may depend on soil iron mineralogy and provide experimental evidence to support conceptual models of zonal mineral-OM associations. Experimental N addition disrupted the accumulation of protein-like molecules in the hydrophobic zone and the positive correlation of lignin-like molecules in the kinetic zone with Fh content, compared to unfertilized soils. These data suggest that mineralogy and clay content together influence the chemical composition not only of mineral-associated OM, but also of soluble compounds within the soil matrix. If these relationships are prevalent over larger spatial and temporal scales, they provide a foundation for understanding SOM cycling and persistence under a variety of environmental contexts.
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http://dx.doi.org/10.1016/j.scitotenv.2020.137839DOI Listing
September 2020

Nutrient availability controls the impact of mammalian herbivores on soil carbon and nitrogen pools in grasslands.

Glob Chang Biol 2020 Feb 3. Epub 2020 Feb 3.

Department of Terrestrial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, The Netherlands.

Grasslands are subject to considerable alteration due to human activities globally, including widespread changes in populations and composition of large mammalian herbivores and elevated supply of nutrients. Grassland soils remain important reservoirs of carbon (C) and nitrogen (N). Herbivores may affect both C and N pools and these changes likely interact with increases in soil nutrient availability. Given the scale of grassland soil fluxes, such changes can have striking consequences for atmospheric C concentrations and the climate. Here, we use the Nutrient Network experiment to examine the responses of soil C and N pools to mammalian herbivore exclusion across 22 grasslands, under ambient and elevated nutrient availabilities (fertilized with NPK + micronutrients). We show that the impact of herbivore exclusion on soil C and N pools depends on fertilization. Under ambient nutrient conditions, we observed no effect of herbivore exclusion, but under elevated nutrient supply, pools are smaller upon herbivore exclusion. The highest mean soil C and N pools were found in grazed and fertilized plots. The decrease in soil C and N upon herbivore exclusion in combination with fertilization correlated with a decrease in aboveground plant biomass and microbial activity, indicating a reduced storage of organic matter and microbial residues as soil C and N. The response of soil C and N pools to herbivore exclusion was contingent on temperature - herbivores likely cause losses of C and N in colder sites and increases in warmer sites. Additionally, grasslands that contain mammalian herbivores have the potential to sequester more N under increased temperature variability and nutrient enrichment than ungrazed grasslands. Our study highlights the importance of conserving mammalian herbivore populations in grasslands worldwide. We need to incorporate local-scale herbivory, and its interaction with nutrient enrichment and climate, within global-scale models to better predict land-atmosphere interactions under future climate change.
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http://dx.doi.org/10.1111/gcb.15023DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7155038PMC
February 2020

Nutrient addition increases grassland sensitivity to droughts.

Ecology 2020 05 18;101(5):e02981. Epub 2020 Feb 18.

Department of Ecology, Evolution, and Behavior, University of Minnesota, 140 Gortner Laboratory, 1479 Gortner Avenue, St. Paul, 55108, Minnesota, USA.

Grasslands worldwide are expected to experience an increase in extreme events such as drought, along with simultaneous increases in mineral nutrient inputs as a result of human industrial activities. These changes are likely to interact because elevated nutrient inputs may alter plant diversity and increase the sensitivity to droughts. Dividing a system's sensitivity to drought into resistance to change during the drought and rate of recovery after the drought generates insights into different dimensions of the system's resilience in the face of drought. Here, we examine the effects of experimental nutrient fertilization and the resulting diversity loss on the resistance to and recovery from severe regional droughts. We do this at 13 North American sites spanning gradients of aridity, five annual grasslands in California, and eight perennial grasslands in the Great Plains. We measured rate of resistance as the change in annual aboveground biomass (ANPP) per unit change in growing season precipitation as conditions declined from normal to drought. We measured recovery as the change in ANPP during the postdrought period and the return to normal precipitation. Resistance and recovery did not vary across the 400-mm range of mean growing season precipitation spanned by our sites in the Great Plains. However, chronic nutrient fertilization in the Great Plains reduced drought resistance and increased drought recovery. In the California annual grasslands, arid sites had a greater recovery postdrought than mesic sites, and nutrient addition had no consistent effects on resistance or recovery. Across all study sites, we found that predrought species richness in natural grasslands was not consistently associated with rates of resistance to or recovery from the drought, in contrast to earlier findings from experimentally assembled grassland communities. Taken together, these results suggest that human-induced eutrophication may destabilize grassland primary production, but the effects of this may vary across regions and flora, especially between perennial and annual-dominated grasslands.
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http://dx.doi.org/10.1002/ecy.2981DOI Listing
May 2020

Site-specific responses of foliar fungal microbiomes to nutrient addition and herbivory at different spatial scales.

Ecol Evol 2019 Nov 19;9(21):12231-12244. Epub 2019 Oct 19.

Department of Ecology, Evolution and Behavior University of Minnesota St. Paul Minnesota.

The plant microbiome can affect host function in many ways and characterizing the ecological factors that shape endophytic (microbes living inside host plant tissues) community diversity is a key step in understanding the impacts of environmental change on these communities. Phylogenetic relatedness among members of a community offers a way of quantifying phylogenetic diversity of a community and can provide insight into the ecological factors that shape endophyte microbiomes. We examined the effects of experimental nutrient addition and herbivory exclusion on the phylogenetic diversity of foliar fungal endophyte communities of the grass species at four sites in the Great Plains of the central USA. Using amplicon sequencing, we characterized the effects of fertilization and herbivory on fungal community phylogenetic diversity at spatial scales that spanned within-host to between sites across the Great Plains. Despite increasing fungal diversity and richness, at larger spatial scales, fungal microbiomes were composed of taxa showing random phylogenetic associations. Phylogenetic diversity did not differ systematically when summed across increasing spatial scales from a few meters within plots to hundreds of kilometers among sites. We observed substantial shifts in composition across sites, demonstrating distinct but similarly diverse fungal communities were maintained within sites across the region. In contrast, at the scale of within leaves, fungal communities tended to be comprised of closely related taxa regardless of the environment, but there were no shifts in phylogenetic composition among communities. We also found that nutrient addition (fertilization) and herbivory have varying effects at different sites. These results suggest that the direction and magnitude of the outcomes of environmental modifications likely depend on the spatial scale considered, and can also be constrained by regional site differences in microbial diversity and composition.
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http://dx.doi.org/10.1002/ece3.5711DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6854330PMC
November 2019

Global change effects on plant communities are magnified by time and the number of global change factors imposed.

Proc Natl Acad Sci U S A 2019 09 19;116(36):17867-17873. Epub 2019 Aug 19.

Systems Ecology, Department of Ecological Science, Vrije Universiteit, 1081 HV Amsterdam, The Netherlands.

Global change drivers (GCDs) are expected to alter community structure and consequently, the services that ecosystems provide. Yet, few experimental investigations have examined effects of GCDs on plant community structure across multiple ecosystem types, and those that do exist present conflicting patterns. In an unprecedented global synthesis of over 100 experiments that manipulated factors linked to GCDs, we show that herbaceous plant community responses depend on experimental manipulation length and number of factors manipulated. We found that plant communities are fairly resistant to experimentally manipulated GCDs in the short term (<10 y). In contrast, long-term (≥10 y) experiments show increasing community divergence of treatments from control conditions. Surprisingly, these community responses occurred with similar frequency across the GCD types manipulated in our database. However, community responses were more common when 3 or more GCDs were simultaneously manipulated, suggesting the emergence of additive or synergistic effects of multiple drivers, particularly over long time periods. In half of the cases, GCD manipulations caused a difference in community composition without a corresponding species richness difference, indicating that species reordering or replacement is an important mechanism of community responses to GCDs and should be given greater consideration when examining consequences of GCDs for the biodiversity-ecosystem function relationship. Human activities are currently driving unparalleled global changes worldwide. Our analyses provide the most comprehensive evidence to date that these human activities may have widespread impacts on plant community composition globally, which will increase in frequency over time and be greater in areas where communities face multiple GCDs simultaneously.
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http://dx.doi.org/10.1073/pnas.1819027116DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6731679PMC
September 2019

Testing for loss of Epichloë and non-epichloid symbionts under altered rainfall regimes.

Am J Bot 2019 08 6;106(8):1081-1089. Epub 2019 Aug 6.

Department of Biology, University of New Mexico, Albuquerque, NM, 87131, USA.

Premise: Microbial symbionts can buffer plant hosts from environmental change. Therefore, understanding how global change factors alter the associations between hosts and their microbial symbionts may improve predictions of future changes in host population dynamics and microbial diversity. Here, we investigated how one global change factor, precipitation, affected the maintenance or loss of symbiotic fungal endophytes in a C grass host. Specifically, we examined the distinct responses of Epichloë (vertically transmitted and systemic) and non-epichloid endophytes (typically horizontally transmitted and localized) by considering (1) how precipitation altered associations with Epichloë and non-epichloid endophytic taxa across host ontogeny, and (2) interactive effects of water availability and Epichloë on early seedling life history stages.

Methods: We manipulated the presence of Epichloë amarillans in American beachgrass (Ammophila breviligulata) in a multiyear field experiment that imposed three precipitation regimes (ambient or ±30% rainfall). In laboratory assays, we investigated the interactive effects of water availability and Epichloë on seed viability and germination.

Results: Reduced precipitation decreased the incidence of Epichloë in leaves in the final sampling period, but had no effect on associations with non-epichloid taxa. Epichloë reduced the incidence of non-epichloid endophytes, including systemic p-endophytes, in seeds. Laboratory assays suggested that association with Epichloë is likely maintained, in part, due to increased seed viability and germination regardless of water availability.

Conclusions: Our study empirically demonstrates several pathways for plant symbionts to be lost or maintained across host ontogeny and suggests that reductions in precipitation can drive the loss of a plant's microbial symbionts.
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http://dx.doi.org/10.1002/ajb2.1340DOI Listing
August 2019

Cross-scale dynamics in community and disease ecology: relative timescales shape the community ecology of pathogens.

Ecology 2019 11 30;100(11):e02836. Epub 2019 Aug 30.

Department of Ecology, Evolution, and Behavior, University of Minnesota, St. Paul, Minnesota, 55108, USA.

Communities of free-living organisms are shaped by processes operating within and among patches of habitat, whereas pathogen communities are shaped by analogous processes operating within and among hosts. Resource competition (R*) theory can describe dynamics within patches or hosts, and metacommunity dynamics describe competition-colonization trade-offs, extinction debts, and superinfection. However, models at this broader scale often assume instantaneous competitive exclusion in co-inhabited patches or co-infected hosts. Impacts of more gradual competitive exclusion on the abundance, distribution, and diversity of species are less clear. Here, we nest a general resource competition model within a metacommunity framework and manipulate the relative timescales for processes operating within and among patches/hosts. We focus on superinfection in pathogen communities. We compare cases where transmission depends on infection prevalence vs. the abundance of pathogens within hosts. Surprisingly, slowing the relative pace of competitive exclusion within hosts can decrease infection prevalence of the inferior competitor and increase prevalence of the superior competitor, depending on transmission and virulence. Slower within-host dynamics reduce the abundance of both pathogens within hosts and promote diversity at multiple scales: co-infections within individual hosts and co-occurrence in the host population. These results highlight surprising feedbacks that can emerge across scales and reinforce the rich cross-scale connections between community and disease ecology.
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http://dx.doi.org/10.1002/ecy.2836DOI Listing
November 2019

Effects of nutrient supply, herbivory, and host community on fungal endophyte diversity.

Ecology 2019 09 15;100(9):e02758. Epub 2019 Jul 15.

Department of Ecology, Evolution, and Behavior, University of Minnesota, St. Paul, Minnesota, 55108, USA.

The microbes contained within free-living organisms can alter host growth, reproduction, and interactions with the environment. In turn, processes occurring at larger scales determine the local biotic and abiotic environment of each host that may affect the diversity and composition of the microbiome community. Here, we examine variation in the diversity and composition of the foliar fungal microbiome in the grass host, Andropogon gerardii, across four mesic prairies in the central United States. Composition of fungal endophyte communities differed among sites and among individuals within a site, but was not consistently affected by experimental manipulation of nutrient supply to hosts (A. gerardii) or herbivore reduction via fencing. In contrast, mean fungal diversity was similar among sites but was limited by total plant biomass at the plot scale. Our work demonstrates that distributed experiments motivated by ecological theory are a powerful tool to unravel the multiscale processes governing microbial community composition and diversity.
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http://dx.doi.org/10.1002/ecy.2758DOI Listing
September 2019

Pathogens manipulate the preference of vectors, slowing disease spread in a multi-host system.

Ecol Lett 2019 Jul 15;22(7):1115-1125. Epub 2019 May 15.

Department of Ecology, Evolution, and Behavior, University of Minnesota, Saint Paul, MN, USA.

The spread of vector-borne pathogens depends on a complex set of interactions among pathogen, vector, and host. In single-host systems, pathogens can induce changes in vector preferences for infected vs. healthy hosts. Yet it is unclear if pathogens also induce changes in vector preference among host species, and how changes in vector behaviour alter the ecological dynamics of disease spread. Here, we couple multi-host preference experiments with a novel model of vector preference general to both single and multi-host communities. We show that viruliferous aphids exhibit strong preferences for healthy and long-lived hosts. Coupling experimental results with modelling to account for preference leads to a strong decrease in overall pathogen spread through multi-host communities due to non-random sorting of viruliferous vectors between preferred and non-preferred host species. Our results demonstrate the importance of the interplay between vector behaviour and host diversity as a key mechanism in the spread of vectored-diseases.
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http://dx.doi.org/10.1111/ele.13268DOI Listing
July 2019

Stability of grassland production is robust to changes in the consumer food web.

Ecol Lett 2019 Apr 12;22(4):707-716. Epub 2019 Feb 12.

Department of Ecology, Evolution and Behavior, University of Minnesota, Twin Cities, Minnesota, USA.

Theory predicts that consumers may stabilise or destabilise plant production depending on model assumptions, and tests in aquatic food webs suggest that trophic interactions are stabilising. We quantified the effects of trophic interactions on temporal variability (standard deviation) and temporal stability (mean/standard deviation) of grassland biomass production and the plant diversity-stability relationship by experimentally removing heterotrophs (large vertebrates, arthropods, foliar and soil fungi) from naturally and experimentally assembled grasslands of varying diversity. In both grassland types, trophic interactions proportionately decreased plant community biomass mean and variability over the course of 6 years, leading to no net change in temporal stability or the plant diversity-stability relationship. Heterotrophs also mediated plant coexistence; their removal reduced diversity in naturally assembled grasslands. Thus, herbivores and fungi reduce biomass production, concurrently reducing the temporal variability of energy and material fluxes. Because of this coupling, grassland stability is robust to large food web perturbations.
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http://dx.doi.org/10.1111/ele.13232DOI Listing
April 2019

Leaf nutrients, not specific leaf area, are consistent indicators of elevated nutrient inputs.

Nat Ecol Evol 2019 03 4;3(3):400-406. Epub 2019 Feb 4.

Forest Research Centre, School of Agriculture, University of Lisbon, Lisbon, Portugal.

Leaf traits are frequently measured in ecology to provide a 'common currency' for predicting how anthropogenic pressures impact ecosystem function. Here, we test whether leaf traits consistently respond to experimental treatments across 27 globally distributed grassland sites across 4 continents. We find that specific leaf area (leaf area per unit mass)-a commonly measured morphological trait inferring shifts between plant growth strategies-did not respond to up to four years of soil nutrient additions. Leaf nitrogen, phosphorus and potassium concentrations increased in response to the addition of each respective soil nutrient. We found few significant changes in leaf traits when vertebrate herbivores were excluded in the short-term. Leaf nitrogen and potassium concentrations were positively correlated with species turnover, suggesting that interspecific trait variation was a significant predictor of leaf nitrogen and potassium, but not of leaf phosphorus concentration. Climatic conditions and pretreatment soil nutrient levels also accounted for significant amounts of variation in the leaf traits measured. Overall, we find that leaf morphological traits, such as specific leaf area, are not appropriate indicators of plant response to anthropogenic perturbations in grasslands.
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http://dx.doi.org/10.1038/s41559-018-0790-1DOI Listing
March 2019

No evidence for trade-offs in plant responses to consumer food web manipulations.

Ecology 2018 09 1;99(9):1953-1963. Epub 2018 Aug 1.

Department of Plant Pathology, University of Minnesota, St. Paul, Minnesota, 55108, USA.

Plants face a range of trade-offs as they attempt to maximize their fitness within a complex web composed of competitors, mutualists, and herbivores. In addition to growth-defense and competition-defense trade-offs, plants must balance their response to a wide range of potential enemies including pathogens and vertebrate and invertebrate herbivores. We tested for trade-offs in plant species' responses to different types of consumers using a foodweb manipulation experiment in which we selectively excluded large vertebrate herbivores and removed foliar fungi, soil fungi, and insects from natural and experimentally planted grassland communities. We found no evidence for trade-offs in the ability of plants to defend themselves against different sets of consumers, although plants varied widely in their responses to removal of different consumer groups. In addition, the species-level responses to consumer removal in monoculture were uncorrelated with each species' response in more diverse communities, highlighting the important role of local context (e.g., competition and apparent competition) in determining the effects of consumers. Plants must balance their allocation of energy among a wide variety of tasks including growing, competing for limited resources, and defending themselves against an array of potential enemies. We found that while plant species differed greatly in their response to the removal of consumers, species that were susceptible to the effects of one consumer group (e.g., insect herbivores) also were susceptible to other consumer groups (e.g., fungal pathogens). This suggests that plants differ in their overall allocation to defense, but defense investment can proffer protection against a wide array of natural enemies. We also found that plant responses to consumers depended on the diversity of the surrounding plant community, suggesting that among-plant interactions can alter their susceptibility to the impacts of consumers.
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http://dx.doi.org/10.1002/ecy.2389DOI Listing
September 2018