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.

Tropical ant community responses to experimental soil warming.

Climate change is one of the primary agents of the global decline in insect abundance. Because of their narrow thermal ranges, tropical ectotherms are predicted to be most threatened by global warming, yet tests of this prediction are often confounded by other anthropogenic disturbances. We used a tropical forest soil warming experiment to directly test the effect of temperature increase on litter-dwelling ants. Two years of continuous warming led to a change in ant community between warming and control plots. Specifically, six ant genera were recorded only on warming plots, and one genus only on control plots. Wasmannia auropuctata, a species often invasive elsewhere but native to this forest, was more abundant in warmed plots. Ant recruitment at baits was best predicted by soil surface temperature and ant heat tolerance. These results suggest that heat tolerance is useful for predicting changes in daily foraging activity, which is directly tied to colony fitness. We show that a 2-year increase in temperature (of 2-4°C) can have a profound effect on the most abundant insects, potentially favouring species with invasive traits and moderate heat tolerances.

The seventh macronutrient: how sodium shortfall ramifies through populations, food webs and ecosystems.

Of the 25 elements required to build most organisms, sodium has a unique set of characteristics that ramify through terrestrial ecology. In plants, sodium is found in low concentrations and has little metabolic function; in plant consumers, particularly animals, sodium is essential to running costly Na-K ATPases. Here I synthesise a diverse literature from physiology, agronomy and ecology, towards identifying sodium's place as the '7th macronutrient', one whose shortfall targets two trophic levels - herbivores and detritivores. I propose that sodium also plays a central, though unheralded role in herbivore digestion, via its importance to maintaining microbiomes and denaturing tannins. I highlight how sodium availability is a key determinant of consumer abundance and the geography of herbivory and detritivory. And I propose a re-appraisal of the assumption that, because sodium is metabolically unimportant to most plants, it is of little use. Instead, I suggest that sodium's critical role in limiting herbivore performance makes it a commodity used by plants to manipulate their herbivores and mutualists, and by consumers like bison and elephants to generate grazing lawns: dependable sources of sodium.

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.

Antibiotics as chemical warfare across multiple taxonomic domains and trophic levels in brown food webs.

Bacteria and fungi secrete antibiotics to suppress and kill other microbes, but can these compounds be agents of competition against macroorganisms? We explore how one competitive tactic, antibiotic production, can structure the composition and function of brown food webs. This aspect of warfare between microbes and invertebrates is particularly important today as antibiotics are introduced into ecosystems via anthropogenic activities, but the ecological implications of these introductions are largely unknown. We hypothesized that antimicrobial compounds act as agents of competition against invertebrate and microbial competitors. Using field-like mesocosms, we tested how antifungal and antibacterial compounds influence microbes, invertebrates, and decomposition in the brown food web. Both antibiotics changed prokaryotic microbial community composition, but only the antibacterial changed invertebrate composition. Antibacterials reduced the abundance of invertebrate detritivores by 34%. However, the addition of antimicrobials did not ramify up the food web as predator abundances were unaffected. Decomposition rates did not change. To test the mechanisms of antibiotic effects, we provided antibiotic-laden water to individual invertebrate detritivores in separate microcosm experiments. We found that the antibiotic compounds can directly harm invertebrate taxa, probably through a disruption of endosymbionts. Combined, our results show that antibiotic compounds could be an effective weapon for microbes to compete against both microbial and invertebrate competitors. In the context of human introductions, the detrimental effects of antibiotics on invertebrate communities indicates that the scope of this anthropogenic disturbance is much greater than previously expected.

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.

Biogeochemistry and forest composition shape nesting patterns of a dominant canopy ant.

Humans are increasing nutrient deposition across the globe, and we know little about how these changes influence consumer populations in tropical rainforests. We used a long-term fertilization experiment conducted in a Panamanian forest to explore how nutrient availability and tree traits affect abundance of a higher-level consumer. We added nitrogen, phosphorus and potassium in a factorial design for 18 years. Given that phosphorus often limits ecosystem processes in lowland tropical forests, and added nitrogen reduces insect abundance in our experiment, we first hypothesized that phosphorus addition would increase nest density and nest size of Azteca chartifex ants while nitrogen addition would have the opposite effects. We found 48% lower nest density in the canopy of nitrogen addition plots relative to plots that did not receive nitrogen. Phosphorus addition did not affect nest density or size. These nutrient effects were not diminished by the selectivity of host trees. In general, larger trees held more nests, despite their low frequencies across the forest, while some abundant species (e.g., palms) were rarely used. We further predicted higher nest frequency on trees with extrafloral nectaries, because this ant fuels its large colonies with extrafloral nectar. Despite the non-random distribution of A. chartifex nests, across tree species and nutrient treatments, trees with extrafloral nectaries did not host more nests. Our study suggests that areas of a tropical lowland forest which are not oversaturated with nitrogen, and contain large trees, have higher nest density. This could enable A. chartifex in similar areas to outcompete other ants due to high abundance.

Fifty Years of Mountain Passes: A Perspective on Dan Janzen's Classic Article.

In 1967, Dan Janzen published "Why Mountain Passes Are Higher in the Tropics" in The American Naturalist. Janzen's seminal article has captured the attention of generations of biologists and continues to inspire theoretical and empirical work. The underlying assumptions and derived predictions are broadly synthetic and widely applicable. Consequently, Janzen's "seasonality hypothesis" has proven relevant to physiology, climate change, ecology, and evolution. To celebrate the fiftieth anniversary of this highly influential article, we highlight the past, present, and future of this work and include a unique historical perspective from Janzen himself.

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.

Plant responses to fertilization experiments in lowland, species-rich, tropical forests.

We present a meta-analysis of plant responses to fertilization experiments conducted in lowland, species-rich, tropical forests. We also update a key result and present the first species-level analyses of tree growth rates for a 15-yr factorial nitrogen (N), phosphorus (P), and potassium (K) experiment conducted in central Panama. The update concerns community-level tree growth rates, which responded significantly to the addition of N and K together after 10 yr of fertilization but not after 15 yr. Our experimental soils are infertile for the region, and species whose regional distributions are strongly associated with low soil P availability dominate the local tree flora. Under these circumstances, we expect muted responses to fertilization, and we predicted species associated with low-P soils would respond most slowly. The data did not support this prediction, species-level tree growth responses to P addition were unrelated to species-level soil P associations. The meta-analysis demonstrated that nutrient limitation is widespread in lowland tropical forests and evaluated two directional hypotheses concerning plant responses to N addition and to P addition. The meta-analysis supported the hypothesis that tree (or biomass) growth rate responses to fertilization are weaker in old growth forests and stronger in secondary forests, where rapid biomass accumulation provides a nutrient sink. The meta-analysis found no support for the long-standing hypothesis that plant responses are stronger for P addition and weaker for N addition. We do not advocate discarding the latter hypothesis. There are only 14 fertilization experiments from lowland, species-rich, tropical forests, 13 of the 14 experiments added nutrients for five or fewer years, and responses vary widely among experiments. Potential fertilization responses should be muted when the species present are well adapted to nutrient-poor soils, as is the case in our experiment, and when pest pressure increases with fertilization, as it does in our experiment. The statistical power and especially the duration of fertilization experiments conducted in old growth, tropical forests might be insufficient to detect the slow, modest growth responses that are to be expected.

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.

Biogeochemistry drives diversity in the prokaryotes, fungi, and invertebrates of a Panama forest.

Humans are both fertilizing the world and depleting its soils, decreasing the diversity of aquatic ecosystems and terrestrial plants in the process. We know less about how nutrients shape the abundance and diversity of the prokaryotes, fungi, and invertebrates of Earth's soils. Here we explore this question in the soils of a Panama forest subject to a 13-yr fertilization with factorial combinations of nitrogen (N), phosphorus (P), and potassium (K) and a separate micronutrient cocktail. We contrast three hypotheses linking biogeochemistry to abundance and diversity. Consistent with the Stress Hypothesis, adding N suppressed the abundance of invertebrates and the richness of all three groups of organisms by ca. 1 SD or more below controls. Nitrogen addition plots were 0.8 pH units more acidic with 18% more exchangeable aluminum, which is toxic to both prokaryotes and eukaryotes. These stress effects were frequently reversed, however, when N was added with P (for prokaryotes and invertebrates) and with added K (for fungi). Consistent with the Abundance Hypothesis, adding P generally increased prokaryote and invertebrate diversity, and adding K enhanced invertebrate diversity. Also consistent with the Abundance Hypothesis, increases in invertebrate abundance generated increases in richness. We found little evidence for the Competition Hypothesis: that single nutrients suppressed diversity by favoring a subset of high nutrient specialists, and that nutrient combinations suppressed diversity even more. Instead, combinations of nutrients, and especially the cation/micronutrient treatment, yielded the largest increases in richness in the two eukaryote groups. In sum, changes in soil biogeochemistry revealed a diversity of responses among the three dominant soil groups, positive synergies among nutrients, and-in contrast with terrestrial plants-the frequent enhancement of soil biodiversity.

A global database of ant species abundances.

What forces structure ecological assemblages? A key limitation to general insights about assemblage structure is the availability of data that are collected at a small spatial grain (local assemblages) and a large spatial extent (global coverage). Here, we present published and unpublished data from 51 ,388 ant abundance and occurrence records of more than 2,693 species and 7,953 morphospecies from local assemblages collected at 4,212 locations around the world. Ants were selected because they are diverse and abundant globally, comprise a large fraction of animal biomass in most terrestrial communities, and are key contributors to a range of ecosystem functions. Data were collected between 1949 and 2014, and include, for each geo-referenced sampling site, both the identity of the ants collected and details of sampling design, habitat type, and degree of disturbance. The aim of compiling this data set was to provide comprehensive species abundance data in order to test relationships between assemblage structure and environmental and biogeographic factors. Data were collected using a variety of standardized methods, such as pitfall and Winkler traps, and will be valuable for studies investigating large-scale forces structuring local assemblages. Understanding such relationships is particularly critical under current rates of global change. We encourage authors holding additional data on systematically collected ant assemblages, especially those in dry and cold, and remote areas, to contact us and contribute their data to this growing data set.

Towards a geography of omnivory: Omnivores increase carnivory when sodium is limiting.

Towards understanding the geography of omnivory, we tested three hypotheses that predict the proportion of animal tissue consumed: the sodium limitation hypothesis predicts that omnivores increase animal consumption in Na-poor environments because Na bioaccumulates from plants to predators; thus, heterotrophs are Na-rich sources. The nitrogen limitation and habitat productivity hypotheses use the same logic to predict more animal consumption in N-poor and productive environments respectively. Omnivory is a common trophic strategy, but what determines the balance of plant and animal tissue omnivores consume is relatively unexplored. Most of what we know comes from single populations at local scales. Here we quantitatively test these three hypotheses at a large geographic scale and across 20 species of omnivorous ants. We tested each hypothesis using N stable isotopes (δ15 N) to quantify the degree of carnivory in ant populations in 20 forests that span 12° latitude from Georgia to Maine, USA. We used the difference in δ15 N between 20 ant conspecifics in 10 genera between two paired forests (10 pairs of 20 forests) that consisted of a coastal and inland forests on the same latitude to determine if the proportion of animal tissue consumed could be predicted based on Na, N or net primary productivity. Sodium gradients accounted for 18% of the variation in δ15 N, 45% if one outlier ant species was omitted. In contrast, the nitrogen limitation and habitat productivity hypotheses, which predict more animal consumption in N-poor and more productive environments respectively, failed to vary with δ15 N. Our results reveal a geography of omnivory driven in part by access to Na.

Thermal constraints on foraging of tropical canopy ants.

Small cursorial ectotherms risk overheating when foraging in the tropical forest canopy, where the surfaces of unshaded tree branches commonly exceed 50 °C. We quantified the heating and subsequent cooling rates of 11 common canopy ant species from Panama and tested the hypothesis that ant workers stop foraging at temperatures consistent with the prevention of overheating. We created hot experimental "sunflecks" on existing foraging trails of four ant species from different clades and spanning a broad range of body size, heating rate, and critical thermal maxima (CTmax). Different ant species exhibited very different heating rates in the lab, and these differences did not follow trends predicted by body size alone. Experiments with ant models showed that heating rates are strongly affected by color in addition to body size. Foraging workers of all species showed strong responses to heating and consistently abandoned focal sites between 36 and 44 °C. Atta colombica and Azteca trigona workers resumed foraging shortly after heat was removed, but Cephalotes atratus and Dolichoderus bispinosus workers continued to avoid the heated patch even after >5 min of cooling. Large foraging ants (C. atratus) responded slowly to developing thermal extremes, whereas small ants (A. trigona) evacuated sunflecks relatively quickly, and at lower estimated body temperatures than when revisiting previously heated patches. The results of this study provide the first field-based insight into how foraging ants respond behaviorally to the heterogeneous thermal landscape of the tropical forest canopy.