Nutrient subsidies to belowground microbes impact aboveground food web interactions

Historically, terrestrial food web theory has been compartmentalized into interactions among aboveground or belowground communities. In this study we took a more synthetic approach to understanding food web interactions by simultaneously examining four trophic levels and investigating how nutrient (nitrogen and carbon) and detrital subsidies impact the ability of the belowground microbial community to alter the abundance of aboveground arthropods (herbivores and predators) associated with the intertidal cord grass Spartina alterniflora. We manipulated carbon, nitrogen, and detrital resources in a field experiment and measured decomposition rate, soil nitrogen pools, plant biomass and quality, herbivore density, and arthropod predator abundance. Because carbon subsidies impact plant growth only indirectly (microbial pathways), whereas nitrogen additions both directly (plant uptake) and indirectly (microbial pathways) impact plant primary productivity, we were able to assess the effect of both belowground soil microbes and nutrient availability on aboveground herbivores and their predators. Herbivore density in the field was suppressed by carbon supplements. Carbon addition altered soil microbial dynamics (net potential ammonification, litter decomposition rate, DON [dissolved organic N] concentration), which limited inorganic soil nitrogen availability and reduced plant size as well as predator abundance. Nitrogen addition enhanced herbivore density by increasing plant size and quality directly by increasing inorganic soil nitrogen pools, and indirectly by enhancing microbial nitrification. Detritus adversely affected aboveground herbivores mainly by promoting predator aggregation. To date, the effects of carbon and nitrogen subsidies on salt marshes have been examined as isolated effects on either the aboveground or the belowground community. Our results emphasize the importance of directly addressing the soil microbial community as a factor that influences aboveground food web structure by affecting plant size and aboveground plant nitrogen.     

Constitutive and induced defenses to herbivory in above- and belowground plant tissues

A recent surge in attention devoted to the ecology of soil biota has prompted interest in quantifying similarities and differences between interactions occurring in above- and belowground communities. Furthermore, linkages that interconnect the dynamics of these two spatially distinct ecosystems are increasingly documented. We use a similar approach in the context of understanding plant defenses to herbivory, including how they are allocated between leaves and roots (constitutive defenses), and potential cross-system linkages (induced defenses). To explore these issues we utilized three different empirical approaches. First, we manipulated foliar and root herbivory on tobacco (Nicotiana tabacum) and measured changes in the secondary chemistry of above- and belowground tissues. Second, we reviewed published studies that compared levels of secondary chemistry between leaves and roots to determine how plants distribute putative defense chemicals across the above- and belowground systems. Last, we used meta-analysis to quantify the impact of induced responses across plant tissue types. In the tobacco system, leaf-chewing insects strongly induced higher levels of secondary metabolites in leaves but had no impact on root chemistry. Nematode root herbivores, however, elicited changes in both leaves and roots. Virtually all secondary chemicals measured were elevated in nematode-induced galls, whereas the impact of root herbivory on foliar chemistry was highly variable and depended on where chemicals were produced within the plant. Importantly, nematodes interfered with aboveground metabolites that have biosynthetic sites located in roots (e.g., nicotine) but had the opposite effect (i.e., nematodes elevated foliar expression) on chemicals produced in shoots (e.g., phenolics and terpenoids). Results from our literature review suggest that, overall, constitutive defense levels are extremely similar when comparing leaves with roots, although certain chemical classes (e.g., alkaloids, glucosinolates) are differentially allocated between above- and belowground parts. Based on a meta-analysis of induced defense studies we conclude that: (1) foliar induction generates strong responses in leaves, but much weaker responses in roots, and (2) root induction elicits responses of equal magnitude in both leaves and roots. We discuss the importance of this asymmetry and the paradox of cross-system induction in relation to optimal defense theory and interactions between above- and belowground herbivory.     

Latitudinal variation in top-down and bottom-up control of a salt marsh food web

The shrub Iva frutescens, which occupies the terrestrial border of U.S. Atlantic Coast salt marshes, supports a food web that varies strongly across latitude. We tested whether latitudinal variation in plant quality (higher at high latitudes), consumption by omnivores (a crab, present only at low latitudes), consumption by mesopredators (ladybugs, present at all latitudes), or the life history stage of an herbivorous beetle could explain continental-scale field patterns of herbivore density. In a mesocosm experiment, crabs exerted strong top-down control on herbivorous beetles, ladybugs exerted strong top-down control on aphids, and both predators benefited plants through trophic cascades. Latitude of plant origin had no effect on consumers. Herbivorous beetle density was greater if mesocosms were stocked with beetle adults rather than larvae, and aphid densities were reduced in the "adult beetle" treatment. Treatment combinations representing high and low latitudes produced patterns of herbivore density similar to those in the field. We conclude that latitudinal variation in plant quality is less important than latitudinal variation in top consumers and competition in mediating food web structure. Climate may also play a strong role in structuring high-latitude salt marshes by limiting the number of herbivore generations per growing season and causing high overwintering mortality.     

Host-plant-mediated competition via induced resistance: interactions between pest herbivores on potatoes.

Plant-mediated competition among insect herbivores occurs when one species induces changes in plant chemistry, nutrition, or morphology that render plants resistant to attack by others. We explored plant-mediated interspecific interactions between the potato leafhopper (Empoasca fabae) and the Colorado potato beetle (Leptinotarsa decemlineata), two important pests on potatoes. Leafhoppers colonize fields in advance of beetles, and thus the possibility exists that previous feeding by leafhoppers induces changes in potato plants that have adverse consequences for beetles. The consequences of leafhopper-induced resistance for beetle performance were studied in the greenhouse, field cages, and in large open-field plots. Potato plants were exposed to four densities of leafhoppers (none, low, moderate, and high), and visible feeding symptoms were measured as percentage leaf curling, chlorosis, and necrosis. The oviposition preference, performance, and survivorship of Colorado potato beetles were then measured on the four categories of induced plants in field-cage and greenhouse settings. In open field plots, survival on the four categories of induced plants was determined by placing cohorts of beetle adults onto plants and measuring the densities of resulting eggs, larvae, and emerging Fl adults. Leafhopper-induced symptoms on potato plants were density dependent, with the percentage of curled, chlorotic, and necrotic leaves increasing with leafhopper density. Previous feeding by leafhoppers adversely affected oviposition and larval performance of beetles. Fewer egg masses were deposited on plants that incurred high levels of leafhopper feeding. Similarly, larval development was delayed and emerging adult beetles weighed less when fed induced foliage from the high leafhopper-density treatment. Beetles survived less well in the field on plants experiencing moderate and high levels of leafhopper feeding as evidenced by lower densities of eggs, larvae, and emerging F1 adults. Overall, leafhoppers and beetles competed through feeding-induced changes in plant quality. Notably, the asymmetric interaction took place at a large spatial scale in open field plots and had negative consequences that persisted to the next beetle generation. Ultimately, to establish an effective management strategy for crop pests such as leafhoppers, it is essential to consider the positive indirect effects of induced resistance along with the negative direct effects on crop yield.     

Critical patch sizes for food-web modules

Because patch size and connectivity may strongly impact the assemblage of species that occur on a patch, the types of food-web interactions that occur among those species may also depend on spatial structure. Here, we identify whether food-web interactions among salt-marsh-inhabiting arthropods vary with patch size and connectivity, and how such changes in trophic structure might feed back to influence the spatial distribution of prey. In a multiyear survey, patch-restricted predators exhibited steeper occupancy-patch-size relationships than herbivores, and species' critical patch sizes were correlated with overall rarity. As a result, the presence of food-web modules depended strongly on patch size: large and well-connected patches supported complex food-web modules, but only the simplest modules involving the most abundant species were found on small patches. Habitat-generalist spiders dominated on small patches, and predation pressure from such species may contribute to the observed lower densities of mesopredators on small patches. Overall, patch size and connectivity influenced the types of modules present on a patch through differential loss of rare, patch-restricted predators, but predation by generalist predators may be a key mechanism influencing the spatial structure of certain prey species.     

Increased primary production shifts the structure and composition of a terrestrial arthropod community

Numerous studies have examined relationships between primary production and biodiversity at higher trophic levels. However, altered production in plant communities is often tightly linked with concomitant shifts in diversity and composition, and most studies have not disentangled the direct effects of production on consumers. Furthermore, when studies do examine the effects of plant production on animals in terrestrial systems, they are primarily confined to a subset of taxonomic or functional groups instead of investigating the responses of the entire community. Using natural monocultures of the salt marsh cordgrass Spartina alterniflora, we were able to examine the impacts of increased plant production, independent of changes in plant composition and/or diversity, on the trophic structure, composition, and diversity of the entire arthropod community. If arthropod species richness increased with greater plant production, we predicted that it would be driven by: (1) an increase in the number of rare species, and/or (2) an increase in arthropod abundance. Our results largely supported our predictions: species richness of herbivores, detritivores, predators, and parasitoids increased monotonically with increasing levels of plant production, and the diversity of rare species also increased with plant production. However, rare species that accounted for this difference were predators, parasitoids, and detritivores, not herbivores. Herbivore species richness could be simply explained by the relationship between abundance and diversity. Using nonmetric multidimensional scaling (NMDS) and analysis of similarity (ANOSIM), we also found significant changes in arthropod species composition with increasing levels of production. Our findings have important implications in the intertidal salt marsh, where human activities have increased nitrogen runoff into the marsh, and demonstrate that such nitrogen inputs cascade to affect community structure, diversity, and abundance in higher trophic levels.     

Arthropod food web restoration following removal of an invasive wetland plant.

Restoration of habitats impacted by invasive plants is becoming an increasingly important tool in the management of native biodiversity, though most studies do not go beyond monitoring the abundance of particular taxonomic groups, such as the return of native vegetation. Yet, the reestablishment of trophic interactions among organisms in restored habitats is equally important if we are to monitor and understand how ecosystems recover. This study examined whether food web interactions among arthropods (as inferred by abundance of naturally occurring stable isotopes of C [delta13C] and N [delta15N]) were reestablished in the restoration of a coastal Spartina alterniflora salt marsh that had been invaded by Phragmites australis. From patterns of C and N stable isotopes we infer that trophic interactions among arthropods in the native salt marsh habitats are characterized by reliance on the dominant marsh plant Spartina as a basal resource. Herbivores such as delphacid planthoppers and mirid bugs have isotope signatures characteristic of Spartina, and predatory arthropods such as dolicopodid flies and spiders likewise have delta13C and delta15N signatures typical of Spartina-derived resources (approximately -13 per thousand and 10 per thousand, respectively). Stable isotope patterns also suggest that the invasion of Phragmites into salt marshes and displacement of Spartina significantly alter arthropod food web interactions. Arthropods in Phragmites-dominated sites have delta13C isotope values between -18 per thousand and -20 per thousand, suggesting reliance on detritus and/or benthic microalgae as basal resources and not on Phragmites, which has a delta13C approximately -26 per thousand. Since most Phragmites herbivores are either feeding internally or are rare transients from nearby Spartina, these resources do not provide significant prey resources for other arthropod consumers. Rather, predator isotope signatures in the invaded habitats indicate dependence on detritus/algae as basal resources instead of the dominant vegetation. The reestablishment of Spartina after removal of Phragmites, however, not only returned species assemblages typical of reference (uninvaded) Spartina, but stable isotope signatures suggest that the trophic interactions among the arthropods were also similar in reestablished habitats. Specifically, both herbivores and predators showed characteristic Spartina signatures, suggesting the return of the original grazer-based food web structure in the restored habitats.