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.

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.

Life history traits associated with body size covary along a latitudinal gradient in a generalist grasshopper.

Animal body size often varies systematically along latitudinal gradients, where individuals are either larger or smaller with varying season length. This study examines ecotypic responses by the generalist grasshopper Melanoplus femurrubrum (Orthoptera: Acrididae) in body size and covarying, physiologically based life history traits along a latitudinal gradient with respect to seasonality and energetics. The latitudinal compensation hypothesis predicts that smaller body size occurs in colder sites when populations must compensate for time constraints due to short seasons. Shorter season length requires faster developmental and growth rates to complete life cycles in one season. Using a common garden experimental design under laboratory conditions, we examined how grasshopper body size, consumption, developmental time, growth rate and metabolism varied among populations collected along an extended latitudinal gradient. When reared at the same temperature in the lab, individuals from northern populations were smaller, developed more rapidly, and showed higher growth rates, as expected for adaptations to shorter and generally cooler growing seasons. Temperature-dependent, whole organism metabolic rate scaled positively with body size and was lower at northern sites, but mass-specific standard metabolic rate did not differ among sites. Total food consumption varied positively with body size, but northern populations exhibited a higher mass-specific consumption rate. Overall, compensatory life history responses corresponded with key predictions of the latitudinal compensation hypothesis in response to season length.

Ecological mechanisms underlying arthropod species diversity in grasslands.

Arthropods are an important component of grassland systems, contributing significantly to biodiversity and ecosystem structure and function. Climate, fire, and grazing by large herbivores are important drivers in grasslands worldwide. Arthropod responses to these drivers are highly variable and clear patterns are difficult to find, but responses are largely indirect with respect to changes in resources, species interactions, habitat structure, and habitat heterogeneity resulting from interactions among fire, grazing, and climate. Here, we review these ecological mechanisms influencing grassland arthropod diversity. We summarize hypotheses describing species diversity at local and regional scales and then discuss specific factors that may affect arthropod diversity in grassland systems. These factors include direct and indirect effects of grazing, fire, and climate, species interactions, above- and belowground interactions, and landscape-level effects.

Genetic variation and mating success in managed american plains bison.

The American plains bison (Bison bison) was pushed to the brink of extinction in the late 1800s but has since rebounded. Less than 5% of animals currently exist in conservation herds that are critical for maintaining genetic variability. Here, we use 25 microsatellite loci to assess genetic diversity and patterns of mating success over a 3-year period in a managed conservation herd at Konza Prairie Biological Station, Kansas (total number of individuals genotyped = 587). Heterozygosity was comparable to and allelic diversity higher than that in 11 other wild and managed herds for which similar estimates are available. Parentage analyses revealed that males within the oldest age classes (5-7 years) sired >90% of calves over the study period, consistent with a polygynous breeding system. Asymmetries in siring success also were observed within age classes, with the same males enjoying high siring success over multiple seasons. Empirical results of paternity will facilitate future modeling and empirical efforts to determine how demographic factors, population size, and variation in siring success interact to determine the retention (or loss) of genetic diversity in natural and managed herds, thus allowing informed recommendations for management practices and conservation efforts of this symbolic North American species.

Not just the usual suspects: insect herbivore populations and communities are associated with multiple plant nutrients.

The relationship between plant nutrient content and insect herbivore populations and community structure has long interested ecologists. Insect herbivores require multiple nutrients, but ecologists have focused mostly on nitrogen (an estimate of plant protein content), and more recently phosphorus (P); other nutrients have received little attention. Here we document nutrient variation in grass and forb samples from grassland habitats in central Nebraska using an elemental approach; in total we measured foliar concentrations of 12 elements (N and P, plus S, B, Ca, Mg, Na, K, Zn, Fe, Mn, and Cu). We detected significant variability among sites for N, P, Mg, Na, K, and Cu. We next used a model selection approach to explore how this nutritional variation and plant biomass correlate with grasshopper densities (collectively and at the feeding-guild level), and principal component analysis to explore nutrient correlations with grasshopper community species composition. When all grasshoppers were pooled, densities varied among sites, but only P was associated with abundance of the elements shown to vary between sites. Different responses occurred at the feeding-guild level. For grass specialists, densities were associated with N, plus P, Mg, and Na. For forb specialists, N and P were often associated with density, but associations with Na and K were also observed. Finally, mixed-feeder abundance was strongly associated with biomass, and to a lesser extent P, Mg, Na, and Cu. At the community level, B, Ca, Zn, and Cu, plus biomass, explained > 30% of species composition variation. Our results confirm the positive association of N and P with insect herbivore populations, while suggesting a potential role for Mg, Na, and K. They also demonstrate the importance of exploring effects at the feeding-guild level. We hope our data motivate ecologists to think beyond N and P when considering plant nutrient effects on insect herbivores, and make a call for studies to examine functional responses of insect herbivores to dietary manipulation of Mg, Na, and K. Finally, our results demonstrate correlations between variation in nutrients and species assemblages, but factors not linked to plant nutrient quality or biomass likely explain most of the observed variation.

Coexisting generalist herbivores occupy unique nutritional feeding niches.

A mainstay of ecological theory and practice is that coexisting species use different resources, leading to the local development of biodiversity. However, a problem arises for understanding coexistence of multiple species if they share critical resources too generally. Here, we employ an experimental framework grounded in nutritional physiology to show that closely related, cooccurring and generalist-feeding herbivores (seven grasshopper species in the genus Melanoplus; Orthoptera: Acrididae) eat protein and carbohydrate in different absolute amounts and ratios even if they eat the same plant taxa. The existence of species-specific nutritional niches provides a cryptic mechanism that helps explain how generalist herbivores with broadly overlapping diets might coexist. We also show that performance by grasshoppers allowed to mix their diets and thus regulate their protein-carbohydrate intake matched optimal performance peaks generated from no-choice treatments. These results indicate the active nature of diet selection to achieve balanced diets and provide buffering capacity in the face of variable food quality. Our empirical findings and experimental approach can be extended to generate and test predictions concerning the intensity of biotic interactions between species, the relative abundance of species, yearly fluctuations in population size, and the nature of interactions with natural enemies in tritrophic niche space.

Comparative genome scan detects host-related divergent selection in the grasshopper Hesperotettix viridis.

In this study, we used a comparative genome scan to examine patterns of population differentiation with respect to host plant use in Hesperotettix viridis, a Nearctic oligophagous grasshopper locally specialized on various Asteraceae including Solidago, Gutierrezia, and Ericameria. We identified amplified fragment length polymorphism (AFLP) loci with significantly elevated F(ST) (outlier loci) in multiple different-host and same-host comparisons of populations while controlling for geographic distance. By comparing the number and identities of outlier loci in different-host vs. same-host comparisons, we found evidence of host plant-related divergent selection for some population comparisons (Solidago- vs. Gutierrezia-feeders), while other comparisons (Ericameria- vs. Gutierrezia-feeders) failed to demonstrate a strong role for host association in population differentiation. In comparisons of Solidago- vs. Gutierrezia-feeding populations, a relatively high number of outlier loci observed repeatedly in different-host comparisons (35% of all outliers and 2.7% of all 625 AFLP loci) indicated a significant role for host-related selection in contributing to overall genomic differentiation in this grasshopper. Mitochondrial DNA sequence data revealed a star-shaped phylogeny with no host- or geography-related structure, low nucleotide diversity, and high haplotype diversity, suggesting a recent population expansion. mtDNA data do not suggest a long period of isolation in separate glacial refugia but are instead more compatible with a single glacial refugium and more recent divergence in host use. Our study adds to research documenting heterogeneity in differentiation across the genome as a consequence of divergent natural selection, a phenomenon that may occur as part of the process of ecological speciation.

Harmony on the prairie? Grassland plant and animal community responses to variation in climate across land-use gradients.

Human induced climate and land-use change are severely impacting global biodiversity, but how community composition and richness of multiple taxonomic groups change in response to local drivers and whether these responses are synchronous remains unclear. We used long-term community-level data from an experimentally manipulated grassland to assess the relative influence of climate and land use as drivers of community structure of four taxonomic groups: birds, mammals, grasshoppers, and plants. We also quantified the synchrony of responses among taxonomic groups across land-use gradients and compared climatic drivers of community structure across groups. All four taxonomic groups responded strongly to land use (fire frequency and grazing), while responses to climate variability were more pronounced in grasshoppers and small mammals. Animal groups exhibited asynchronous responses across all land-use treatments, but plant and animal groups, especially birds, exhibited synchronous responses in composition. Asynchrony was attributed to taxonomic groups responding to different components of climate variability, including both current climate conditions and lagged effects from the previous year. Data-driven land management strategies are crucial for sustaining native biodiversity in grassland systems, but asynchronous responses of taxonomic groups to climate variability across land-use gradients highlight a need to incorporate response heterogeneity into management planning.

Hyperspectral Analysis of Leaf Pigments and Nutritional Elements in Tallgrass Prairie Vegetation.

Understanding the spatial distribution of forage quality is important to address critical research questions in grassland science. Due to its efficiency and accuracy, there has been a widespread interest in mapping the canopy vegetation characteristics using remote sensing methods. In this study, foliar chlorophylls, carotenoids, and nutritional elements across multiple tallgrass prairie functional groups were quantified at the leaf level using hyperspectral analysis in the region of 470-800 nm, which was expected to be a precursor to further remote sensing of canopy vegetation quality. A method of spectral standardization was developed using a form of the normalized difference, which proved feasible to reduce the interference from background effects in the leaf reflectance measurements. Chlorophylls and carotenoids were retrieved through inverting the physical model PROSPECT 5. The foliar nutritional elements were modeled empirically. Partial least squares regression was used to build the linkages between the high-dimensional spectral predictor variables and the foliar biochemical contents. Results showed that the retrieval of leaf biochemistry through hyperspectral analysis can be accurate and robust across different tallgrass prairie functional groups. In addition, correlations were found between the leaf pigments and nutritional elements. Results provided insight into the use of pigment-related vegetation indices as the proxy of plant nutrition quality.

Does dietary P affect feeding and performance in the mixed-feeding grasshopper (Acrididae) Melanoplus bivitattus?

Although consequences of limited dietary protein and carbohydrate to performance are well studied for terrestrial insect herbivores, the importance of phosphorus (P) remains poorly understood. We examined the significance of dietary P to performance in fifth-instar nymphs of the grasshopper Melanoplus bivittatus fed artificial diets. Consumption, digestion, developmental rate, and growth in response to different levels of P nested within standard-Protein and carbohydrate diets were determined. Developmental rate was slowest on high-P diets; protein:carbohydrate concentration and P in diets affected frass production and consumption. Approximate digestibility and conversion of digested food were primarily influenced by the protein:carbohydrate quality of the diet but not P. Mass gain was marginally lower in the low-Protein:high carbohydrate diet used in this study. At the individual level, other than small effects to developmental rate at high concentrations for M. bivittatus, dietary P otherwise seems to have little effect on nymphal performance. To the degree that it is important, effects of dietary P depend on the concentrations of protein and carbohydrate in the diet.

Complex variation in habitat selection strategies among individuals driven by extrinsic factors.

Understanding behavioral strategies employed by animals to maximize fitness in the face of environmental heterogeneity, variability, and uncertainty is a central aim of animal ecology. Flexibility in behavior may be key to how animals respond to climate and environmental change. Using a mechanistic modeling framework for simultaneously quantifying the effects of habitat preference and intrinsic movement on space use at the landscape scale, we investigate how movement and habitat selection vary among individuals and years in response to forage quality-quantity tradeoffs, environmental conditions, and variable annual climate. We evaluated the association of dynamic, biotic forage resources and static, abiotic landscape features with large grazer movement decisions in an experimental landscape, where forage resources vary in response to prescribed burning, grazing by a native herbivore, the plains bison (Bison bison bison), and a continental climate. Our goal was to determine how biotic and abiotic factors mediate bison movement decisions in a nutritionally heterogeneous grassland. We integrated spatially explicit relocations of GPS-collared bison and extensive vegetation surveys to relate movement paths to grassland attributes over a time period spanning a regionwide drought and average weather conditions. Movement decisions were affected by foliar crude content and low stature forage biomass across years with substantial interannual variation in the magnitude of selection for forage quality and quantity. These differences were associated with interannual differences in climate and growing conditions from the previous year. Our results provide experimental evidence for understanding how the forage quality-quantity tradeoff and fine-scale topography drives fine-scale movement decisions under varying environmental conditions.

Foraging decisions underlying restricted space use: effects of fire and forage maturation on large herbivore nutrient uptake.

Recent models suggest that herbivores optimize nutrient intake by selecting patches of low to intermediate vegetation biomass. We assessed the application of this hypothesis to plains bison (Bison bison) in an experimental grassland managed with fire by estimating daily rates of nutrient intake in relation to grass biomass and by measuring patch selection in experimental watersheds in which grass biomass was manipulated by prescribed burning. Digestible crude protein content of grass declined linearly with increasing biomass, and the mean digestible protein content relative to grass biomass was greater in burned watersheds than watersheds not burned that spring (intercept; F 1,251 = 50.57, P < 0.0001). Linking these values to published functional response parameters, ad libitum protein intake, and protein expenditure parameters, Fryxell's (Am. Nat., 1991, 138, 478) model predicted that the daily rate of protein intake should be highest when bison feed in grasslands with 400-600 kg/ha. In burned grassland sites, where bison spend most of their time, availability of grass biomass ranged between 40 and 3650 kg/ha, bison selected foraging areas of roughly 690 kg/ha, close to the value for protein intake maximization predicted by the model. The seasonal net protein intake predicted for large grazers in this study suggest feeding in burned grassland can be more beneficial for nutrient uptake relative to unburned grassland as long as grass regrowth is possible. Foraging site selection for grass patches of low to intermediate biomass help explain patterns of uniform space use reported previously for large grazers in fire-prone systems.

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.

Predator-Prey Interactions are Context Dependent in a Grassland Plant-Grasshopper-Wolf Spider Food Chain.

Species interactions are often context dependent, where outcomes vary in response to one or more environmental factors. It remains unclear how abiotic conditions like temperature combine with biotic factors such as consumer density or food quality to affect resource availability or influence species interactions. Using the large grasshopper Melanoplus bivittatus (Say) and a common wolf spider [Rabidosa rabida (Walkenaer)], we conducted manipulative field experiments in tallgrass prairie to examine how spider-grasshopper interactions respond to manipulations of temperature, grasshopper density, and food quality. Grasshopper survival was density dependent, as were the effects of spider presence and food quality in context-dependent ways. In high grasshopper density treatments, predation resulted in increased grasshopper survival, likely as a result of reduced intraspecific competition in the presence of spiders. Spiders had no effect on grasshopper survival when grasshoppers were stocked at low densities. Effects of the experimental treatments were often interdependent so that effects were only observed when examined together with other treatments. The occurrence of trophic cascades was context dependent, where the effects of food quality and spider presence varied with temperature under high-density treatments. Temperature weakly affected the impact of spider presence on M. bivittatus survivorship when all treatments were considered simultaneously, but different context-dependent responses to spider presence and food quality were observed among the three temperature treatments under high-density conditions. Our results indicate that context-dependent species interactions are common and highlight the importance of understanding how key biotic and abiotic factors combine to influence species interactions.

Feeding patterns in grasshoppers (Orthoptera: Acrididae): Factors influencing diet specialization.

Diets of grasshopper species from two arid grassland communities in Trans-Pecos, Texas, were determined by gut analysis. Species-specific food plant choice and niche breadths are presented for each of these species. As a group, grasshoppers range from monophagous to polyphagous feeders although most species fall in the oligophagous to polyphagous group. Phylogenetic constraints are evident such that gomphocerinae are primarily grass feeders while melanoplinae feed predominantly on forbs; the oedipodinae show less clearcut tendencies.Feeding patterns are remarkably constant from site to site and overall, community niche breadth distributions between sites do not differ greatly. Individual species tend to eat the same plant species at various sites and maintain similar niche breadths. Species with relatively specialized diets tend to feed on predictable plant species such as grasses and long-lived perrenial forbs.Grasshopper feeding patterns present some problems to the current theory of herbivore diet specialization since forb feeding melanoplines tend to be polyphagous (contrary to predictions). Life history patterns unrelated to tracking host plants may explain some aspects of diet breadth since diet selectivities are presumably adjusted according to the probability of finding suitable food plants.

Differential herbivory on C3 versus C4 grasses by the grasshopper Ageneotettix deorum (Orthoptera: acrididae).

The hypothesis that graminivorous grasshoppers select C3 grasses over C4 grasses was tested with experiments in the field. It was found that the generalist, graminivorous grasshopper Ageneotettix deorum typically chooses C3 as opposed to C4 grasses when both types are equally available. This preference is attributed to the differences in leaf anatomies of C3 and C4 plants since crude protein, water, lignin, fiber, and silicon content or the size of the individual leaves tested do not explain the observed feeding pattern. However, examination of the actual food plant selection of actual field inhabiting grasshoppers indicates that food plant prefernce may only be a minor component of food selection in natural settings.

Plasticity and overcompensation in grass responses to herbivory.

Several hypotheses predict defoliation-induced increases in individual plant fitness. In this paper we examine three such hypotheses: the Herbivore Optimization Hypothesis (HOH); the Continuum of Responses Hypothesis (CRH); and the Growth Rate Model (GRM). All three have in common predictions based on responses of defoliated individuals with the objective of explaining community and higher level phenomena. The latter two extend theory by specifying conditions for overcompensatory responses. They differ in whether overcompensation is sensitive to conditions external (CRH) or internal (GRM) to the plant. We tested these hypotheses with field experiments in a grassland system in which two native, perennial grass species replace each other along a short topographic/resource gradient. We detected positive, neutral, and negative changes in plant mass in response to partial defoliation. Patterns of responses to the edaphic and competitive environment combinations were unique to each species and neither the CRH nor the GRM were able to consistently predict responses in these grasses. Predictions of the HOH were fully supported only by the species naturally limited to lower-resource environments: overcompensation occurred in natural environments and it occurred at herbivory levels these plants experience naturally. Thus, the overcompensatory response can be important for the maintenance of local plant population distributions. However, new mechanistic theory is needed to account for the trend common to both species: overcompensatory responses to herbivory were greater in the edaphic environment in which each species was naturally most abundant.