Nutrient dilution and climate cycles underlie declines in a dominant insect herbivore.

Evidence for global insect declines mounts, increasing our need to understand underlying mechanisms. We test the nutrient dilution (ND) hypothesis-the decreasing concentration of essential dietary minerals with increasing plant productivity-that particularly targets insect herbivores. Nutrient dilution can result from increased plant biomass due to climate or CO2 enrichment. Additionally, when considering long-term trends driven by climate, one must account for large-scale oscillations including El Niño Southern Oscillation (ENSO), North Atlantic Oscillation (NAO), and Pacific Decadal Oscillation (PDO). We combine long-term datasets of grasshopper abundance, climate, plant biomass, and end-of-season foliar elemental content to examine potential drivers of abundance cycles and trends of this dominant herbivore. Annual grasshopper abundances in 16- and 22-y time series from a Kansas prairie revealed both 5-y cycles and declines of 2.1-2.7%/y. Climate cycle indices of spring ENSO, summer NAO, and winter or spring PDO accounted for 40-54% of the variation in grasshopper abundance, mediated by effects of weather and host plants. Consistent with ND, grass biomass doubled and foliar concentrations of N, P, K, and Na-nutrients which limit grasshopper abundance-declined over the same period. The decline in plant nutrients accounted for 25% of the variation in grasshopper abundance over two decades. Thus a warming, wetter, more CO2-enriched world will likely contribute to declines in insect herbivores by depleting nutrients from their already nutrient-poor diet. Unlike other potential drivers of insect declines-habitat loss, light and chemical pollution-ND may be widespread in remaining natural areas.

How and why grasshopper community maturation rates are slowing on a North American tall grass prairie.

Invertebrate growth rates have been changing in the Anthropocene. We examine rates of seasonal maturation in a grasshopper community that has been declining annually greater than 2% a year over 34 years. As this grassland has experienced a 1°C increase in temperature, higher plant biomass and lower nutrient densities, the community is maturing more slowly. Community maturation had a nutritional component: declining in years/watersheds with lower plant nitrogen. The effects of fire frequency were consistent with effects of plant nitrogen. Principal components analysis also suggests associated changes in species composition-declines in the densities of grass feeders were associated with declines in community maturation rates. We conclude that slowed maturation rates-a trend counteracted by frequent burning-likely contribute to long-term decline of this dominant herbivore.

Sodium-enriched floral nectar increases pollinator visitation rate and diversity.

Plants have evolved a variety of approaches to attract pollinators, including enriching their nectar with essential nutrients. Because sodium is an essential nutrient for pollinators, and sodium concentration in nectar can vary both within and among species, we explored whether experimentally enriching floral nectar with sodium in five plant species would influence pollinator visitation and diversity. We found that the number of visits by pollinators increased on plants with sodium-enriched nectar, regardless of plant species, relative to plants receiving control nectar. Similarly, the number of species visiting plants with sodium-enriched nectar was twice that of controls. Our findings suggest that sodium in floral nectar may play an important but unappreciated role in the ecology and evolution of plant-pollinator mutualisms.

The nutritional geography of ants: Gradients of sodium and sugar limitation across North American grasslands.

Sugar and sodium are essential nutrients to above- and below-ground consumers. Unlike other properties of ecological communities such as abundance and richness, we know relatively little about nutritional geography-the sources and supply rates of nutrients, and how and why they vary across communities and ecosystems. Towards a remedy, we present a suite of hypotheses for how sodium and sugary exudate availability should vary for a common omnivore-the ants-and test them using a survey of 53 North American grasslands. We do so by running transects of salt and sugar baits and inferring the magnitude of environmental supplies as the inverse of their use as exogenous baits. We then use estimates of potential drivers of the availability of salt and sugary exudates-plant and soil nutrients, and bioclimatic variables-to test the best predictors of sodium and salt use by ant communities. Beyond a baseline of ant activity, salt use increased as an inverse of the amount of sodium in an ecosystem's plant tissue, but not its soils. Plant sodium varied by two orders of magnitude in grasslands across 16° latitude. This suggests that plant exudates are an important source of sodium for grassland consumers. The three drivers that best predict exogenous sugar use by ants all point to factors constraining sugar production: net above-ground productivity, how far the community is into that year's growing season (both reflecting the rates of photosynthesis) and, intriguingly, the potassium content of plant tissue, which is likely linked to exudate production via plant turgor. These data suggest that ants and other consumers across a range of grasslands and climate vary significantly in the demand and supply of sugar and salt. This nutritional geography ultimately arises from gradients of climate and biogeochemistry with implications for the geography of plant-consumer interactions.

Bottom-up when it is not top-down: Predators and plants control biomass of grassland arthropods.

We investigate where bottom-up and top-down control regulates ecological communities as a mechanism linking ecological gradients to the geography of consumer abundance and biomass. We use standardized surveys of 54 North American grasslands to test alternate hypotheses predicting 100-fold shifts in the biomass of four common grassland arthropod taxa-Auchenorrhyncha, sucking herbivores, Acrididae, chewing herbivores, Tettigoniidae, omnivores, and Araneae, predators. Bottom-up models predict that consumer biomass tracks plant quantity (e.g. productivity and standing biomass) and quality (nutrient content) and that ectotherm access to food increases with temperature. Each of the focal trophic groups responded differently to these drivers: the biomass of sucking herbivores and omnivores increased with plant biomass; that of chewing herbivores tracked plant quality; and predator biomass did not depend on plant quality, plant quantity or temperature. The Exploitation Ecosystem Hypothesis is a top-down hypothesis that predicts a shift from resource limitation of herbivores when plant production is low, to predator limitation when plant production is high. In grasslands where spider biomass was low, herbivore biomass increased with plant biomass, whereas bottom-up structuring was not evident when spiders were abundant. Furthermore, neither predator biomass nor trophic position (via stable isotope analysis) increased with plant biomass, suggesting predators themselves are top-down limited. Stable isotope analysis revealed that trophic position of the chewing herbivore and omnivore increased significantly with plant biomass, suggesting these groups increased scavenging and meat consumption in grasslands with higher carbohydrate availability. Taken together, our snapshot sampling documents gradients of food web structure across 54 grasslands, consistent with multiple hypotheses of bottom-up and top-down regulation.

A distributed experiment demonstrates widespread sodium limitation in grassland food webs.

Sodium (Na) has a unique role in food webs as a nutrient primarily limiting for plant consumers, but not other trophic levels. Environmental Na levels vary with proximity to coasts, local geomorphology, climate, and with anthropogenic inputs (e.g., road salt). We tested two key predictions across 54 grasslands in North America: Na shortfall commonly limits herbivore abundance, and the magnitude of this limitation varies inversely with environmental Na supplies. We tested them with a distributed pulse experiment and evaluated the relative importance of Na limitation to other classic drivers of climate, macronutrient levels, and plant productivity. Herbivore abundance increased by 45% with Na addition. Moreover, the magnitude of increase on Na addition plots decreased with increasing levels of plant Na, indicating Na satiation at sites with high Na concentrations in plant tissue. Our results demonstrate that invertebrate primary consumers are often Na limited and track local Na availability, with implications for the geography of invertebrate abundance and herbivory.

Fire and grazing modulate the structure and resistance of plant-floral visitor networks in a tallgrass prairie.

Significant loss of pollinator taxa and their interactions with flowering plants has resulted in growing reductions to pollination services globally. Ecological network analysis is a useful tool for evaluating factors that alter the interaction structure and resistance of systems to species loss, but is rarely applied across multiple empirical networks sampled within the same study. The non-random arrangement of species interactions within a community, or "network structure" such as nested or modular organization, is predicted to prevent extinction cascades in ecological networks. How ecological gradients such as disturbance regimes shape network structural properties remains poorly understood despite significant efforts to quantify interaction structure in natural systems. Here, we examine changes in the structure of plant-floral visitor networks in a tallgrass prairie using a decadal and landscape-scale experiment that manipulates prescribed burn frequency and ungulate grazing, resulting in different grassland states. Plant and floral visitor communities and accompanying network structure were impacted by grassland fire and grazing regimes. The presence of grazers increased flowering plant species richness, network floral visitor species richness, and decreased network nestedness. Fire frequency affected flowering plant and floral visitor community composition; community composition impacted network specialization and modularity. Grassland state resulting from fire-grazing interactions has important implications for the resistance of flowering plant and floral visitor communities to species loss.

Nutrient dilution and the future of herbivore populations.

Nutrient dilution (ND) - the decrease in the concentration of nutritional elements in plant tissue - arises from an increase in the mass of carbohydrates and/or a decrease in the 20+ essential elements. Increasing CO2 levels and its promotion of biomass are linked to nutrient dilution. We build a case for nutrient dilution as a key driver in global declines in herbivore abundance. Herbivores must build element-rich animal tissue from nutrient-poor plant tissue, and their abundance commonly increases with fertilization of both macro- and micronutrients. We predict the global impacts of nutrient dilution will be magnified in some of Earth's most biodiverse, highly productive, and/or nutrient-poor ecosystems and should favor specific traits of herbivores, including sap-feeding and ruminant microbiomes.

Stream macroinvertebrate communities in restored and impacted catchments respond differently to climate, land-use, and runoff over a decade.

Identifying which environmental drivers underlie degradation and improvements of ecological communities is a fundamental goal of ecology. Achieving this goal is a challenge due to diverse trends in both environmental conditions and ecological communities across regions, and it is constrained by the lack of long-term parallel monitoring of environmental and community data needed to study causal relationships. Here, we identify key environmental drivers using a high-resolution environmental - ecological dataset, an ensemble of the Soil and Water Assessment Tool (SWAT+) model, and ecological models to investigate effects of climate, land-use, and runoff on the decadal trend (2012-2021) of stream macroinvertebrate communities in a restored urban catchment and an impacted catchment with mixed land-uses in Germany. The decadal trends showed decreased precipitation, increased temperature, and reduced anthropogenic land-uses, which led to opposing runoff trends - with decreased runoff in the restored catchment and increased runoff in the impacted catchment. The two catchments also varied in decadal trends of taxonomic and trait composition and metrics. The most significant improvements over time were recorded in communities of the restored catchment sites, which have become wastewater free since 2007 to 2009. Within the restored catchment sites, community metric trends were primarily explained by land-use and evaporation trends, while community composition trends were mostly associated with precipitation and runoff trends. Meanwhile, the communities in the impacted catchment did not undergo significant changes between 2012 and 2021, likely influenced by the effects of prolonged droughts following floods after 2018. The results of our study confirm the significance of restoration and land-use management in fostering long-term improvements in stream communities, while climate change remains a prodigious threat. The coupling of long-term biodiversity monitoring with concurrent sampling of relevant environmental drivers is critical for preventative and restorative management in ecology.

Inland navigation and land use interact to impact European freshwater biodiversity.

Inland navigation in Europe is proposed to increase in the coming years, being promoted as a low-carbon form of transport. However, we currently lack knowledge on how this would impact biodiversity at large scales and interact with existing stressors. Here we addressed this knowledge gap by analysing fish and macroinvertebrate community time series across large European rivers comprising 19,592 observations from 4,049 sampling sites spanning the past 32 years. We found ship traffic to be associated with biodiversity declines, that is, loss of fish and macroinvertebrate taxonomic richness, diversity and trait richness. Ship traffic was also associated with increases in taxonomic evenness, which, in concert with richness decreases, was attributed to losses in rare taxa. Ship traffic was especially harmful for benthic taxa and those preferring slow flows. These effects often depended on local land use and riparian degradation. In fish, negative impacts of shipping were highest in urban and agricultural landscapes. Regarding navigation infrastructure, the negative impact of channelization on macroinvertebrates was evident only when riparian degradation was also high. Our results demonstrate the risk of increasing inland navigation on freshwater biodiversity. Integrative waterway management accounting for riparian habitats and landscape characteristics could help to mitigate these impacts.

Time series of freshwater macroinvertebrate abundances and site characteristics of European streams and rivers.

Freshwater macroinvertebrates are a diverse group and play key ecological roles, including accelerating nutrient cycling, filtering water, controlling primary producers, and providing food for predators. Their differences in tolerances and short generation times manifest in rapid community responses to change. Macroinvertebrate community composition is an indicator of water quality. In Europe, efforts to improve water quality following environmental legislation, primarily starting in the 1980s, may have driven a recovery of macroinvertebrate communities. Towards understanding temporal and spatial variation of these organisms, we compiled the TREAM dataset (Time seRies of European freshwAter Macroinvertebrates), consisting of macroinvertebrate community time series from 1,816 river and stream sites (mean length of 19.2 years and 14.9 sampling years) of 22 European countries sampled between 1968 and 2020. In total, the data include >93 million sampled individuals of 2,648 taxa from 959 genera and 212 families. These data can be used to test questions ranging from identifying drivers of the population dynamics of specific taxa to assessing the success of legislative and management restoration efforts.

Multi-decadal improvements in the ecological quality of European rivers are not consistently reflected in biodiversity metrics.

Humans impact terrestrial, marine and freshwater ecosystems, yet many broad-scale studies have found no systematic, negative biodiversity changes (for example, decreasing abundance or taxon richness). Here we show that mixed biodiversity responses may arise because community metrics show variable responses to anthropogenic impacts across broad spatial scales. We first quantified temporal trends in anthropogenic impacts for 1,365 riverine invertebrate communities from 23 European countries, based on similarity to least-impacted reference communities. Reference comparisons provide necessary, but often missing, baselines for evaluating whether communities are negatively impacted or have improved (less or more similar, respectively). We then determined whether changing impacts were consistently reflected in metrics of community abundance, taxon richness, evenness and composition. Invertebrate communities improved, that is, became more similar to reference conditions, from 1992 until the 2010s, after which improvements plateaued. Improvements were generally reflected by higher taxon richness, providing evidence that certain community metrics can broadly indicate anthropogenic impacts. However, richness responses were highly variable among sites, and we found no consistent responses in community abundance, evenness or composition. These findings suggest that, without sufficient data and careful metric selection, many common community metrics cannot reliably reflect anthropogenic impacts, helping explain the prevalence of mixed biodiversity trends.

Electrolytes on the prairie: How urine-like additions of Na and K shape the dynamics of a grassland food web.

The electrolytes Na and K both function to maintain water balance and membrane potential. However, these elements work differently in plants-where K is the primary electrolyte-than in animals-where ATPases require a balanced supply of Na and K. Here, we use monthly factorial additions of Na and K to simulate bovine urine inputs and explore how these electrolytes ramify through a prairie food web. Against a seasonal trend of increasing grass biomass and decreasing water and elemental tissue concentrations, +K and +Na plots boosted water content and, when added together, plant biomass. Compared to control plots, +Na and +K plots increased element concentrations in above-ground plant tissue early in summer and decreased them in September. Simultaneously, invertebrate abundance on Na and K additions were sequentially higher and lower than control plots from June to September and were most suppressed when grass was most nutrient rich. K was the more effective plant electrolyte, but Na frequently promoted similar changes in grass ionomes. The soluble/leachable ions of Na and K showed significant ability to shape plant growth, water content, and the 15-element ionome, with consequences for higher trophic levels. Grasslands with high inputs of Na and K-via large mammal grazers or coastal aerosol deposition-likely enhance the ability of plants to adjust their above-ground ionomes, with dramatic consequences for the distribution of invertebrate consumers.

How and why plant ionomes vary across North American grasslands and its implications for herbivore abundance.

Plant elemental content can vary up to 1,000-fold across grasslands, with implications for the herbivores the plants feed. We contrast the regulation, in grasses and forbs, of 12 elements essential to plants and animals (henceforth plant-essential), 7 essential to animals but not plants (animal-essential) and 6 with no known metabolic function (nonessential). Four hypotheses accounted for up to two thirds of the variation in grass and forb ionomes across 54 North American grasslands. Consistent with the supply-side hypothesis, the plant-essential ionome of both forbs and grasses tracked soil availability. Grass ionomes were more likely to harvest even nonessential elements like Cd and Sr. Consistent with the grazing hypothesis, cattle-grazed grasslands also accumulated a handful of metals like Cu and Cr. Consistent with the NP-catalysis hypothesis, increases in the macronutrients N and P in grasses were associated with higher densities of cofactors like Zn and Cu. The plant-essential elements of forbs, in contrast, consistently varied as per the nutrient-dilution hypothesis-there was a decrease in elemental parts per million with increasing local carbohydrate production. Combined, these data fit a working hypothesis that grasses maintain lower elemental densities and survive on nutrient-poor patches by opportunistically harvesting soil nutrients. In contrast, nutrient-rich forbs use episodes of high precipitation and temperature to build new carbohydrate biomass, raising leaves higher to compete for light, but diluting the nutrient content in every bite of tissue. Herbivores of forbs may thus be particularly prone to increases in pCO2 via nutrient dilution.

Trophic differences regulate grassland food webs: herbivores track food quality and predators select for habitat volume.

The impacts of altered biogeochemical cycles on ecological systems are likely to vary with trophic level. Predicting how these changes will affect ecological food webs is further complicated by human activities, which are simultaneously altering the availability of macronutrients like nitrogen (N) and phosphorus (P), and micronutrients such as sodium (Na). Here we contrast three hypotheses that predict how increasing nutrient availability will shape grassland food webs. We conducted a distributed factorial fertilization experiment (N and P crossed with NaCl) across four North American grasslands, quantifying the responses of aboveground plant biomass and volume, plant tissue and soil elemental concentrations, as well as the abundance of five arthropod functional groups. Fertilization with N and P increased plant biomass and foliar N and P concentrations in grasses but not forbs. Fertilization with Na had no effect on plant biomass but increased foliar Na concentrations. Consistent with the nutrient limitation hypothesis, we found strong evidence of nutrient limitation for insect herbivores across the four sites with sucking (phloem and xylem feeding) herbivores increasing in abundance with NP fertilization and chewing herbivores increasing in response to both Na and NP fertilization, and a trend for increased response of arthropods to lower plant nutrient availability. We found no evidence for an interaction of NaCl and NP on arthropod abundance as predicted by the serial colimitation hypothesis. Finally, consistent with the ecosystem size hypothesis, predator and parasitoid abundances increased with plant volume, but not fertilization. Our results suggest these functional group-specific responses to changes in plant nutrients and structure are key to predicting the future of grassland food webs in an era with increasing use of N and P fertilizers, and increasing terrestrial inputs of Na from road salt, saline irrigation water, and aerosols due to rising sea levels.

Tracking nutrients in space and time: Interactions between grazing lawns and drought drive abundances of tallgrass prairie grasshoppers.

We contrast the response of arthropod abundance and composition to bison grazing lawns during a drought and non-drought year, with an emphasis on acridid grasshoppers, an important grassland herbivore.Grazing lawns are grassland areas where regular grazing by mammalian herbivores creates patches of short-statured, high nutrient vegetation. Grazing lawns are predictable microsites that modify microclimate, plant structure, community composition, and nutrient availability, with likely repercussions for arthropod communities.One year of our study occurred during an extreme drought. Drought mimics some of the effects of mammalian grazers: decreasing above-ground plant biomass while increasing plant foliar percentage nitrogen.We sampled arthropods and nutrient availability on and nearby ("off") 10 bison-grazed grazing lawns in a tallgrass prairie in NE Kansas. Total grasshopper abundance was higher on grazing lawns and the magnitude of this difference increased in the wetter year of 2019 compared to 2018, when drought led to high grass foliar nitrogen concentrations on and off grazing lawns. Mixed-feeding grasshopper abundances were consistently higher on grazing lawns while grass-feeder and forb-feeder abundances were higher on lawns only in 2019, the wetter year. In contrast, the abundance of other arthropods (e.g., Hemiptera, Hymenoptera, and Araneae) did not differ on and off lawns, but increased overall in 2019, relative to the drought of 2018.Understanding these local scale patterns of abundances and community composition improves predictability of arthropod responses to ongoing habitat change.

Long-term data reveal unimodal responses of ground beetle abundance to precipitation and land use but no changes in taxonomic and functional diversity.

While much of global biodiversity is undoubtedly under threat, the responses of ecological communities to changing climate, land use intensification, and long-term changes in both taxonomic and functional diversity over time, has still not been fully explored for many taxonomic groups, especially invertebrates. We compiled time series of ground beetles covering the past two decades from 40 sites located in five regions across Germany. We calculated site-based trends for 21 community metrics representing taxonomic and functional diversity of ground beetles, activity density (a proxy for abundance), and activity densities of functional groups. We assessed both overall and regional temporal trends and the influence of the global change drivers of temperature, precipitation, and land use on ground beetle communities. While we did not detect overall temporal changes in ground beetle taxonomic and functional diversity, taxonomic turnover changed within two regions, illustrating that community change at the local scale does not always correspond to patterns at broader spatial scales. Additionally, ground beetle activity density had a unimodal response to both annual precipitation and land use. Limited temporal change in ground beetle communities may indicate a shifting baseline, where community degradation was reached prior to the start of our observation in 1999. In addition, nonlinear responses of animal communities to environmental change present a challenge when quantifying temporal trends.

Abiotic factors and plant biomass, not plant diversity, strongly shape grassland arthropods under drought conditions.

Arthropod abundance and diversity often track plant biomass and diversity at the local scale. However, under altered precipitation regimes and anthropogenic disturbances, plant-arthropod relationships are expected to be increasingly controlled by abiotic, rather than biotic, factors. We used an experimental precipitation gradient combined with human management in a temperate mixed-grass prairie to examine (1) how two drivers, altered precipitation and biomass removal, can synergistically affect abiotic factors and plant communities and (2) how these effects can cascade upward, impacting the arthropod food web. Both drought and hay harvest increased soil surface temperature, and drought decreased soil moisture. Arthropod abundance decreased with low soil moisture and, contrary to our predictions, decreased with increased plant biomass. Arthropod diversity increased with soil moisture, decreased with high surface temperatures, and tracked arthropod abundance but was unaffected by plant diversity or quality. Our experiment demonstrates that arthropod abundance is directly constrained by abiotic factors and plant biomass, in turn constraining local arthropod diversity. If robust, this result suggests climate change in the southern Great Plains may directly reduce arthropod diversity.

Structure of trophic and mutualistic networks across broad environmental gradients.

This study aims to understand how inherent ecological network structures of nestedness and modularity vary over large geographic scales with implications for community stability. Bipartite networks from previous research from 68 locations globally were analyzed. Using a meta-analysis approach, we examine relationships between the structure of 22 trophic and 46 mutualistic bipartite networks in response to extensive gradients of temperature and precipitation. Network structures varied significantly across temperature gradients. Trophic networks showed decreasing modularity with increasing variation in temperature within years. Nestedness of mutualistic networks decreased with increasing temperature variability between years. Mean annual precipitation and variability of precipitation were not found to have significant influence on the structure of either trophic or mutualistic networks. By examining changes in ecological networks across large-scale abiotic gradients, this study identifies temperature variability as a potential environmental mediator of community stability. Understanding these relationships contributes to our ability to predict responses of biodiversity to climate change at the community level.