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.

Temperature influences lipid content in the red harvester ant, Pogonomyrmex barbatus.

Temperature is one of the most important environmental conditions affecting physiological processes in ectothermic organisms like ants. Yet, we often lack information on how certain physiological traits covary with temperature across time. Here, we test predictions on how one trait-lipid content-covaries with temperature using a conspicuous, ground-dwelling harvester ant. We focus on lipid content as fat bodies are metabolically active tissues that are important for storing and releasing energy in response to demand, which could be vital for survival under variable temperatures. From March to November, we extracted lipids from surface workers of 14 colonies while simultaneously recording ground temperature. We first assessed if lipid content was highest during cooler temperatures when ants were less active and less metabolically stressed. In doing so, we found that lipid content of ants declined almost 70% from cool months (November lipid content = 14.6%) to hot months (August lipid content = 4.6%). We next assessed if lipid levels from a group of ants collected at a single time point could change by placing individuals into environmental chambers set at 10, 20, and 30°C (i.e., the approximate span of average temperatures from March to November). Temperature again had a significant impact such that after 10 days, lipid content of ants in the hottest chamber (30°C) had decreased by more than 75%. While intraspecific variation in physiological traits often follows seasonal patterns, our results suggest fluctuations in temperature may account for a portion of the variance observed in traits like lipid content.

Thermal tolerance of western corn rootworm: Critical thermal limits, knock-down resistance, and chill coma recovery.

Western corn rootworm, Diabrotica virgifera virgifera, is one of the most economically important crop pests in the world with estimates of damage and control approximating over $1 billion USD annually. Despite an abundance of research devoted to studying rootworm biology in the central Corn Belt of the United States, key aspects on their thermal ecology are still lacking. Here we address this knowledge gap by measuring critical thermal limits, knock-down resistance, and chill coma recovery. In doing so, we also address methodological questions surrounding measurements of thermal tolerance using a variety of dynamic and static assays. The average critical thermal maxima across all trials was 43.0 °C, while the average critical thermal minima was 2.5 °C. Critical thermal limits were relatively invariant across all treatments except at faster ramping rates. Knock-down resistance decreased with increasing temperature as survival dropped from 100% at 39 °C to 0% within 10 min at 44 °C. Recovery from chill coma increased by 1.62 min for each hour of exposure at 0 °C, while survival decreased by 50% after only 24 h. Combined, our results present the first composite picture of different thermal traits for western corn rootworm, which will be vital for predicting their survival and potential spread under future climate change scenarios.

Bioenergy landscapes drive trophic shifts in generalist ants.

Changes in trophic niche-the pathways through which an organism obtains energy and nutrients-are a fundamental way in which organisms respond to environmental conditions. But the capacity for species to alter their trophic niches in response to global change, and the ways they do so when able, remain largely unknown. Here we examine food webs in three long-term and large-scale experiments to test how resource availability and nutritional requirements interact to determine an organism's trophic niche in the context of one of the largest global trends in land use-the rise in bioenergy production. We use carbon and nitrogen stable isotope analyses to characterize arthropod food webs across three biofuel crops representing a gradient in plant resource richness (corn monocultures, fields dominated by native switchgrass and restored prairie), and to quantify changes in the trophic niche of a widespread generalist ant species across habitats. In doing so, we measure the effects of basal resource richness on food chain length, niche breadth and trophic position. We frame our results in the context of two hypotheses that explain variation in trophic niche-the niche variation hypothesis which emphasizes the importance of resource diversity and ecological opportunity, and the optimal diet hypothesis which emphasizes dietary constraints and the availability of optimal resources. Increasing plant richness lengthened food chains by 10%-20% compared to monocultures. Niche breadths of generalist ants did not vary with resource richness, suggesting they were limited by optimal diet requirements and constraints rather than by ecological opportunity. The ants instead responded to changes in plant richness by shifting their estimated trophic position. In resource-poor monocultures, the ants were top predators, sharing a trophic position with predatory spiders. In resource-rich environments, in contrast, the ants were omnivores, relying on a mix of animal prey and plant-based resources. In addition to highlighting novel ecosystem impacts of alternate bioenergy landscapes, our results suggest that niche breadth and trophic diversification depend more on the presence of optimal resources than on ecological opportunity alone.

Using metabolic and thermal ecology to predict temperature dependent ecosystem activity: a test with prairie ants.

As ecosystems warm, ectotherm consumer activity should also change. Here we use principles from metabolic and thermal ecology to explore how seasonal and diel temperature change shapes a prairie ant community's foraging rate and its demand for two fundamental resources: salt and sugar. From April through October 2016 we ran transects of vials filled with solutions of 0.5% NaCl and 1% sucrose. We first confirm a basic prediction rarely tested: the discovery rate of both food resources accelerated with soil temperature, but this increase was typically capped at midday due to extreme surface temperatures. We then tested the novel prediction that sodium demand accelerates with temperature, premised on a key thermal difference between sugar and sodium: sugar is stored in cells, while salt is pumped out of cells proportional to metabolic rate, and hence temperature. We found strong support for the resulting prediction that recruitment to NaCl baits accelerates with temperature more steeply than recruitment to 1% sucrose baits. A follow up experiment in 2017 verified that temperature-dependent recruitment to sucrose concentrations of 20% (mimicking rich extrafloral nectaries), while noisy, was still only half as temperature dependent as recruitment recorded for 0.5% NaCl. These results demonstrate how ecosystem warming accelerates then curtails the work done by a community of ectotherms, and how the demand and use of fundamental nutrients can be differentially temperature dependent.

From cryptic herbivore to predator: stable isotopes reveal consistent variability in trophic levels in an ant population.

Populations may collectively exhibit a broad diet because individuals have large diet breadths and/or because subpopulations of specialists co-occur. In social insect populations, the diet of the genetic individual, the colony, may similarly arise because workers are diet generalists or castes of specialists. We used elemental and isotopic methods to explore how the invasive red imported fire ant, Solenopsis invicta, achieves its status as a trophic generalist. In one 0.5-ha old field, 31 S. invicta colonies ranged from 1°-consumer to 2°-predator (δ15 N's 0.35-7.38‰), a range comparable to that shown in sampled ant communities. Moreover, a colony's trophic rank was stable despite δ15 N fluctuating 2.98‰ over the year. Colonies that fed at higher trophic levels were not larger, but consumed more C3 -based resources. Individual worker mass, however, did increase with δ15 N (r2  = 0.29, P < 0.001). The ninefold variation in worker mass within a colony generated trophic variance approximately 15% of the population of colonies. Combined, we show how intraspecific trait variation contributes to the trophic breadth of S. invicta, and suggest mechanisms that further explain how their trophic signature varies across space, but remains stable over time.

Sodium co-limits and catalyzes macronutrients in a prairie food web.

Nitrogen and phosphorus frequently limit terrestrial plant production, but have a mixed record in regulating the abundance of terrestrial invertebrates. We contrasted four ways that Na could interact with an NP fertilizer to shape the plants and invertebrates of an inland prairie. We applied NP and Na to m2 plots in a factorial design. Aboveground invertebrate abundance was independently co-limited by NaCl and NP, but with +NP plots supporting more individuals. We suggest the disparity arises because NP enhanced plant height by 35% (1 SD) over controls, providing both food and habitat, whereas NaCl provides only food. Belowground invertebrates showed evidence of serial co-limitation, where NaCl additions alone were ineffectual, but catalyzed access to NP. This suggests the increased belowground food availability in NP plots increased Na demand. Na and NP supply rates vary with climate, land use, and with inputs like urine. The co-limitation and catalysis of N and P by Na thus has the potential for predicting patterns of abundance and diversity across spatial scales.

Temperature influences desiccation resistance of bumble bees.

Ongoing climate change has increased temperatures and the frequency of droughts in many parts of the world, potentially intensifying the desiccation risk for insects. Because resisting desiccation becomes more difficult at higher temperatures and lower humidity, avoiding water loss is a key challenge facing terrestrial insects. However, few studies have examined the interactive effects of temperature and environmental humidity on desiccation resistance in insects. Such studies on bees (Hymenoptera: Apoidea: Anthophila) are especially rare, despite their ecological and economic importance. Here, we crossed temperature (20, 25, and 30 °C) with humidity (<5, 50, >95 % RH) manipulations and measured time to mortality, water loss rates, and the water content at mortality of bumble bees (Bombus impatiens). We found that both higher temperature and lower humidity increased water loss rates, while warmer temperatures reduced survival time and lower humidity decreased water content at mortality. Additionally, we observed large intraspecific variation in water balance traits between colonies, and larger individuals survived longer and could tolerate more water loss before mortality. This study raises important questions about the mechanisms underpinning water loss in bumble bees and suggests that frequent access to nectar may be especially important for bumble bees' water balance and survival in a warming and drying climate.

Testing the role of body size and litter depth on invertebrate diversity across six forests in North America.

Ecologists search for rules by which traits dictate the abundance and distribution of species. Here we search for rules that apply across three common taxa of litter invertebrates in six North American forests from Panama to Oregon. We use image analysis to quantify the abundance and body size distributions of mites, springtails, and spiders in 21 1-m2 plots per forest. We contrast three hypotheses: two of which focus on trait-abundance relationships and a third linking abundance to species richness. Despite three orders of magnitude variation in size, the predicted negative relationship between mean body size and abundance per area occurred in only 18% of cases, never for large bodied taxa like spiders. We likewise found only 18% of tests supported our prediction that increasing litter depth allows for high abundance; two-thirds of which occurred at a single deciduous forest in Massachusetts. In contrast, invertebrate abundance constrained species richness 76% of the time. Our results suggest that body size and habitat volume in brown food webs are rarely good predictors of variation in abundance, but that variation in diversity is generally well predicted by abundance.

Evaluation of a microbial inhibitor in artificial diets of a generalist caterpillar, Heliothis virescens.

Controlling microbial growth in artificial diets is a key component in the rearing of laboratory insects. In this study an antimicrobial agent, Diet Antimicrobial Agent (DAA), was tested for its ability to suppress microbial growth on a range of different diets, and for its effect on larval and pupal performance of individuals from two different strains of Heliothis virescens Fabricus (Lepidoptera: Noctuidae). In the first experiment, it was found that the presence of DAA in a pinto bean-based diet was highly effective at suppressing microbial growth relative to other methods, and that survival of caterpillars on diets with DAA was superior to other treatments. Caterpillars also performed best on diets with DAA, although this may have been the result of laboratory selection pressure as these caterpillars had been reared on pinto bean-based diets with DAA for several hundred generations. A second experiment was conducted, using different diets and a different strain of H. virescens to more fully evaluate DAA. Here it was found that DAA significantly suppressed microbial growth and development, particularly in synthetic diets. There was no significant effect of DAA on pupal development time or mass gain. There was a statistically significant effect of DAA on eclosion time for two of the diets, although the effect did not seem to be biologically meaningful. The findings suggest that DAA is an effective suppressor of microbial growth on artificial diets, and that its net effect on developing diet-reared insects is neutral.

Seasonal plasticity of thermal tolerance in ants.

Analyses of heat tolerance in insects often suggest that this trait is relatively invariant, leading to the use of fixed thermal maxima in models predicting future distribution of species in a warming world. Seasonal environments expose populations to a wide annual temperature variation. To evaluate the simplifying assumption of invariant thermal maxima, we quantified heat tolerance of 26 ant species across three seasons that vary two-fold in mean temperature. Our ultimate goal was to test the hypothesis that heat tolerance tracks monthly temperature. Ant foragers tested at the end of the summer, in September, had higher average critical thermal maximum (CTmax ) compared to those in March and December. Four out of five seasonal generalists, species actively foraging in all three focal months, had, on average, 6°C higher CTmax in September. The invasive fire ant, Solenopsis invicta, was among the thermally plastic species, but the native thermal specialists still maintained higher CTmax than S. invicta. Our study shows that heat tolerance can be plastic, and this should be considered when examining species-level adaptations. Moreover, the plasticity of thermal traits, while potentially costly, may also generate a competitive advantage over species with fixed traits and promote resilience to climate change.

The Economics of Optimal Foraging by the Red Imported Fire Ant.

For social organisms, foraging is often a complicated behavior where tasks are divided among numerous individuals. Here, we ask how one species, the red imported fire ant (Solenopsis invicta Buren) (Hymenoptera: Formicidae), collectively manages this behavior. We tested the Diminishing Returns Hypothesis, which posits that for social insects 1) foraging investment levels increase until diminishing gains result in a decelerating slope of return and 2) the level of investment is a function of the size of the collective group. We compared how different metrics of foraging (e.g., number of foragers, mass of foragers, and body size of foragers) are correlated and how these metrics change over time. We then tested the prediction that as fire ant colonies increase in size, both discovery time and the inflection point (i.e., the time point where colonial investment toward resources slows) should decrease while a colony's maximum foraging mass should increase. In congruence with our predictions, we found that fire ants recruited en masse toward baits, allocating 486 workers and 148 mg of biomass, on average, after 60 min: amounts that were not different 30 min prior. There was incredible variation across colonies with discovery time, the inflection point, and the maximum biomass of foragers all being significantly correlated with colony size. We suggest that biomass is a solid indicator of how social taxa invest their workforce toward resources and hypothesize ways that invasive fire ants are able to leverage their enormous workforce to dominate novel ecosystems by comparing their foraging and colony mass with co-occurring native species.

Invasive Saltcedar and Drought Impact Ant Communities and Isopods in South-Central Nebraska.

The establishment and spread of non-native species often results in negative impacts on biodiversity and ecosystem function. Several species of saltcedar, Tamarix spp. L., have been recently naturalized in large portions of the United States where they have altered plant and animal communities. To test the prediction that saltcedar negatively affects invertebrates, we measured ant genera diversity and the activity density of the exotic isopod Armadillidium vulgare Latrielle (Isopoda: Oniscoidea) for 2 yr using pitfall traps located within 30 5-m2 plots with or without saltcedar at a south-central Nebraska reservoir. From 2005 to 2006, we collected 10,837 ants representing 17 genera and 4,953 A. vulgare. Per plot, the average number of ant genera was not different between saltcedar (x̅ = 3.9) and non-saltcedar areas ( x̅ = 3.9); however, saltcedar plots were compositionally different and more similar from plot to plot (i.e., they had lower beta diversity than control plots) in 2005, but not in 2006. Isopods were likewise temporally affected with higher activity density (+89%) in control plots in 2005, but higher activity density (+27%) in saltcedar plots in 2006. The observed temporal differences occurred as the drought that initially enabled the saltcedar invasion became less severe in 2006. Combined, our results suggest that invertebrate groups like ants, which are generally omnivorous, may be better equipped than more specialized taxa like detritivores to withstand habitat changes due to invasions by non-native species, especially during extreme weather events such as prolonged droughts.

Species energy and Thermal Performance Theory predict 20-yr changes in ant community abundance and richness.

In an era of rapid climate change, and with it concern over insect declines, we used two theories to predict 20-yr changes in 34 North American ant communities. The ecosystems, from deserts to hardwood forests, were first surveyed in the 1990s. When resurveyed in 2016-2017, they averaged 1°C warmer with 200 g C·m-2 ·yr-1 higher plant productivity. Ant colony abundance changed from -49% to +61%. Consistent with Thermal Performance Theory, colony abundance increased with temperature increases < 1°C, then decreased as a site's mean monthly temperature change increased up to +2.4°C. Consistent with Species Energy Theory, (1) ant abundance tracked changes in a measure of energy availability (net aboveground productivity, g C·m-2 ·yr-1 ) and (2) increases in colony abundance drove increases in local plot- and transect-level species richness but not that of Chao 2, an estimate of the size of the species pool. Even after accounting for these drivers, local species richness was still higher ~20 yr after the original surveys, likely due to the increased activity of ant workers. These results suggest community changes are predictable using theory from geographical ecology, and that warming can first enhance but may ultimately decrease the abundance of this important insect taxon.

Disturbance Mediates Homogenization of Above and Belowground Invertebrate Communities.

Natural disturbances can occur stochastically with profound impacts on fauna and flora. Here we quantified the impact of a one in 100-yr flood on terrestrial invertebrate communities in south central Oklahoma. Before the flood, we observed 4,082 individuals from 92 species weighing a total of 18.61 g that belonged to compositionally different above or belowground communities. One year after the initial sampling period and 9 mo post-flood, we measured a 93% decrease in abundance, a 60% decrease in species richness, and a 64% decrease in biomass as well as increased compositional similarity between the above and belowground communities. Of the eight insect orders that were present before the flood, only the Coleoptera and Orthoptera increased immediately after the flood. Of these, only the Orthoptera remained at an elevated level across all post-flood sampling periods, specifically due to an increase in crickets (Orthoptera: Gryllidae). As we enter an era of global change, using natural perturbation experiments will improve our knowledge about the ecological processes that shape patterns of community assembly and biodiversity.