skip to main content

Attention:

The NSF Public Access Repository (NSF-PAR) system and access will be unavailable from 5:00 PM ET until 11:00 PM ET on Friday, June 21 due to maintenance. We apologize for the inconvenience.


Title: 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 CO2enrichment. 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.

 
more » « less
NSF-PAR ID:
10138837
Author(s) / Creator(s):
; ; ; ;
Publisher / Repository:
Proceedings of the National Academy of Sciences
Date Published:
Journal Name:
Proceedings of the National Academy of Sciences
Volume:
117
Issue:
13
ISSN:
0027-8424
Page Range / eLocation ID:
p. 7271-7275
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    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.

     
    more » « less
  2. Abstract

    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 inpCO2via nutrient dilution.

     
    more » « less
  3. BACKGROUND The availability of nitrogen (N) to plants and microbes has a major influence on the structure and function of ecosystems. Because N is an essential component of plant proteins, low N availability constrains the growth of plants and herbivores. To increase N availability, humans apply large amounts of fertilizer to agricultural systems. Losses from these systems, combined with atmospheric deposition of fossil fuel combustion products, introduce copious quantities of reactive N into ecosystems. The negative consequences of these anthropogenic N inputs—such as ecosystem eutrophication and reductions in terrestrial and aquatic biodiversity—are well documented. Yet although N availability is increasing in many locations, reactive N inputs are not evenly distributed globally. Furthermore, experiments and theory also suggest that global change factors such as elevated atmospheric CO 2 , rising temperatures, and altered precipitation and disturbance regimes can reduce the availability of N to plants and microbes in many terrestrial ecosystems. This can occur through increases in biotic demand for N or reductions in its supply to organisms. Reductions in N availability can be observed via several metrics, including lowered nitrogen concentrations ([N]) and isotope ratios (δ 15 N) in plant tissue, reduced rates of N mineralization, and reduced terrestrial N export to aquatic systems. However, a comprehensive synthesis of N availability metrics, outside of experimental settings and capable of revealing large-scale trends, has not yet been carried out. ADVANCES A growing body of observations confirms that N availability is declining in many nonagricultural ecosystems worldwide. Studies have demonstrated declining wood δ 15 N in forests across the continental US, declining foliar [N] in European forests, declining foliar [N] and δ 15 N in North American grasslands, and declining [N] in pollen from the US and southern Canada. This evidence is consistent with observed global-scale declines in foliar δ 15 N and [N] since 1980. Long-term monitoring of soil-based N availability indicators in unmanipulated systems is rare. However, forest studies in the northeast US have demonstrated decades-long decreases in soil N cycling and N exports to air and water, even in the face of elevated atmospheric N deposition. Collectively, these studies suggest a sustained decline in N availability across a range of terrestrial ecosystems, dating at least as far back as the early 20th century. Elevated atmospheric CO 2 levels are likely a main driver of declines in N availability. Terrestrial plants are now uniformly exposed to ~50% more of this essential resource than they were just 150 years ago, and experimentally exposing plants to elevated CO 2 often reduces foliar [N] as well as plant-available soil N. In addition, globally-rising temperatures may raise soil N supply in some systems but may also increase N losses and lead to lower foliar [N]. Changes in other ecosystem drivers—such as local climate patterns, N deposition rates, and disturbance regimes—individually affect smaller areas but may have important cumulative effects on global N availability. OUTLOOK Given the importance of N to ecosystem functioning, a decline in available N is likely to have far-reaching consequences. Reduced N availability likely constrains the response of plants to elevated CO 2 and the ability of ecosystems to sequester carbon. Because herbivore growth and reproduction scale with protein intake, declining foliar [N] may be contributing to widely reported declines in insect populations and may be negatively affecting the growth of grazing livestock and herbivorous wild mammals. Spatial and temporal patterns in N availability are not yet fully understood, particularly outside of Europe and North America. Developments in remote sensing, accompanied by additional historical reconstructions of N availability from tree rings, herbarium specimens, and sediments, will show how N availability trajectories vary among ecosystems. Such assessment and monitoring efforts need to be complemented by further experimental and theoretical investigations into the causes of declining N availability, its implications for global carbon sequestration, and how its effects propagate through food webs. Responses will need to involve reducing N demand via lowering atmospheric CO 2 concentrations, and/or increasing N supply. Successfully mitigating and adapting to declining N availability will require a broader understanding that this phenomenon is occurring alongside the more widely recognized issue of anthropogenic eutrophication. Intercalibration of isotopic records from leaves, tree rings, and lake sediments suggests that N availability in many terrestrial ecosystems has steadily declined since the beginning of the industrial era. Reductions in N availability may affect many aspects of ecosystem functioning, including carbon sequestration and herbivore nutrition. Shaded areas indicate 80% prediction intervals; marker size is proportional to the number of measurements in each annual mean. Isotope data: (tree ring) K. K. McLauchlan et al. , Sci. Rep. 7 , 7856 (2017); (lake sediment) G. W. Holtgrieve et al. , Science 334 , 1545–1548 (2011); (foliar) J. M. Craine et al. , Nat. Ecol. Evol. 2 , 1735–1744 (2018) 
    more » « less
  4. Abstract

    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.

     
    more » « less
  5. Abstract

    Vegetation greenness has increased across much of the global land surface over recent decades. This trend is projected to continue—particularly in northern latitudes—but future greening may be constrained by nutrient availability needed for plant carbon (C) assimilation in response to CO2enrichment (eCO2). eCO2impacts foliar chemistry and function, yet the relative strengths of these effects versus climate in driving patterns of vegetative greening remain uncertain. Here we combine satellite measurements of greening with a 135 year record of plant C and nitrogen (N) concentrations and stable isotope ratios (δ13C and δ15N) in the Northern Great Plains (NGP) of North America to examine N constraints on greening. We document significant greening over the past two decades with the highest proportional increases in net greening occurring in the dries and warmest areas. In contrast to the climate dependency of greening, we find spatially uniform increases in leaf‐level intercellular CO2and intrinsic water use efficiency that track rising atmospheric CO2. Despite large spatial variation in greening, we find sustained and climate‐independent declines in foliar N over the last century. Parallel declines in foliar δ15N and increases in C:N ratios point to diminished N availability as the likely cause. The simultaneous increase in greening and decline in foliar N across our study area points to increased N use efficiency (NUE) over the last two decades. However, our results suggest that plant NUE responses are likely insufficient to sustain observed greening trends in NGP grasslands in the future.

     
    more » « less