Entomology
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Item Nutrient co-limitation of primary producer communities(Blackwell, 2011) Harpole, Stanley; Ngai, Jacqueline; Cleland, Elsa; Seabloom, Eric; Borer, Elizabeth; Bracken, Matthew; Elser, James; Gruner, Daniel; Hillebrand, Helmut; Shurin, Jonathan; Smith, JenniferSynergistic interactions between multiple limiting resources are common, highlighting the importance of co-limitation as a constraint on primary production. Our concept of resource limitation has shifted over the past two decades from an earlier paradigm of single-resource limitation towards concepts of co-limitation by multiple resources, which are predicted by various theories. Herein, we summarise multiple-resource limitation responses in plant communities using a dataset of 641 studies that applied factorial addition of nitrogen (N) and phosphorus (P) in freshwater, marine and terrestrial systems. We found that more than half of the studies displayed some type of synergistic response to N and P addition. We found support for strict definitions of co-limitation in 28% of the studies: i.e. community biomass responded to only combined N and P addition, or to both N and P when added separately. Our results highlight the importance of interactions between N and P in regulating primary producer community biomass and point to the need for future studies that address the multiple mechanisms that could lead to different types of co-limitation.Item Effects of diet quality on performance and nutrient regulation in an omnivorous katydid(Blackwell, 2011) Pearson, Rachel; Behmer, Spencer; Gruner, Daniel; Denno, Robert1. Omnivores by definition eat both plants and animals. However, little is known about how diet macronutrient content affects omnivore performance, or the extent to which they can regulate macronutrient intake. We assessed these questions using the salt marsh katydid, Conocephalus spartinae Fox (Tettigoniidae). 2. In our first experiment we used artificial diets with different protein–carbohydrate ratios to assess the effects of diet quality on survival, growth, and lipid accumulation. We found that diets with a high protein–carbohydrate ratio negatively affected Conocephalus survival. Among surviving individuals growth was not significantly different across the treatments, but lipid content decreased significantly as the protein–carbohydrate ratio of diets increased. 3. In a second experiment we explored the ability of Conocephalus to regulate their protein–carbohydrate intake. Results revealed that Conocephalus did not feed randomly when presented with two nutritionally complementary foods. A detailed analysis of their protein–carbohydrate intake revealed selection for a protein-biased diet, but a lack of tight regulate of protein–carbohydrate intake. 4. We discuss how key macronutrients can limit omnivores, and how nutritional flexibility may enable omnivores to persist in nutritionally heterogeneous environments.Item Herbivore metabolism and stoichiometry each constrain herbivory at different organizational scales across ecosystems(Ecology Letters, 2009) Hillebrand, Helmut; Borer, Elizabeth; Bracken, Matthew; Cardinale, Brad; Cebrian, Just; Cleland, Elsa; Elser, James; Gruner, Daniel; Harpole, Stanley; Ngai, Jackie; Sandin, Stuart; Seabloom, Eric; Shurin, Jonathan; Smith, Jennifer; Smith, MelindaPlant-herbivore interactions mediate the trophic structure of ecosystems. We use a comprehensive data set extracted from the literature to test the relative explanatory power of two contrasting bodies of ecological theory, the metabolic theory of ecology (MTE) and ecological stoichiometry (ES), for per-capita and population-level rates of herbivory across ecosystems. We found that ambient temperature and herbivore body size (MTE) as well as stoichiometric mismatch (ES) both constrained herbivory, but at different scales of biological organization. Herbivore body size, which varied over 11 orders of magnitude, was the primary factor explaining variation in per-capita rates of herbivory. Stoichiometric mismatch explained more variation in population-level herbivory rates and also in per-capita rates when we examined data from within functionally similar trophic groups (e.g. zooplankton). Thus, predictions from metabolic and stoichiometric theories offer complementary explanations for patterns of herbivory that operate at different scales of biological organization.Item Host resistance reverses the outcome of competition between microparasites(Ecological Society of America, 2009) Gruner, Daniel; Kolekar, Arunima; McLaughlin, John; Strong, DonaldPredators and parasites can control the abundance or biomass of herbivores with indirect effects on producer communities and ecosystems, but the interplay of multiple natural enemies may yield unexpected dynamics. We experimentally examined interactions between two microparasites (entomopathogenic nematodes) isolated from sandy grassland soils of coastal California: Heterorhabditis marelatus (Heterorhabditidae) and Steinernema feltiae (Steinernematidae). Heterorhabditis marelatus drives trophic cascades by attacking root- and stem-boring ghost moth caterpillars (Hepialus californicus, Hepialidae), thereby indirectly protecting bush lupine shrubs (Lupinus arboreus, Fabaceae). Extensive field surveys demonstrated sympatric overlap in microhabitat use under lupine canopies and similar mean prevalence of the two nematode species. Using a response-surface design in the laboratory, we varied relative and absolute microparasite densities to test for competitive outcomes within an evolutionary naı¨ve host, larvae of the greater wax moth Galleria mellonella (Pyralidae), and within the native host Hepialus californicus. Independent of conspecific or interspecific density, S. feltiae dominated as expected over H. marelatus within the naı¨ve Galleria, but S. feltiae infected hosts at low frequency and showed lower reproductive fitness than H. marelatus within native Hepialus hosts. Contrary to studies that demonstrate the pairwise dominance of steinernematid over heterorhabditid species in laboratory hosts, host resistance to S. feltiae may provide a mechanism for coexistence of multiple microparasite species. We hypothesize that the ubiquitous field prevalence and rapid life history of S. feltiae imply its use of widespread, abundant but small-bodied hosts and indicate the lack of direct competition with H. marelatus in the Hepialus–Lupinus trophic cascade.Item Metapopulation dynamics override local limits on long-term parasite persistence(2008-12) Ram, Karthik; Preisser, Evan; Gruner, Daniel; Strong, DonaldA simple null model, particularly germane to small and vulnerable organisms such as parasites, is that local conditions set a stage upon which larger-scale dynamics play out. Soil moisture strongly influences survival of entomopathogenic nematodes (EPN), which in turn drive trophic cascades by protecting vegetation from root-feeding herbivores. In this study, we examine the mechanisms responsible for patchy occurrence of an entomopathogenic nematode, Heterorhabditis marelatus, in a California coastal prairie. One hypothesis proposes that biotic factors such as competition and natural enemies could regulate occurrence of EPN populations. We found that fungi and other enemies of EPN, although locally potent, did not explain the patterns of incidence across sites. Abiotic factors also have strong effects on EPN persistence, especially for vulnerable free-living stages. Thus, we tested the hypothesis that patchy occurrence of EPN on a large landscape was driven by differences in soil moisture. Our research uses long-term data on nematode incidence in combination with a landscapelevel experiment to demonstrate the lack of a correlation between soil moisture and long-term persistence. A year-long experiment showed EPN mortality was weakly correlated with soil moisture among our study sites. Thirteen years of data, however, showed that colonization rates were highly correlated with long-term persistence. Sites with highest long-term persistence experienced the highest rates of rhizosphere colonization, extinction, and turnover. As a result, we concluded that metapopulation dynamics override limitations set by local and short-term abiotic conditions to determine long-term persistence in this parasite-driven trophic cascade.Item Potential for entomopathogenic nematodes in biological control: a meta-analytical synthesis and insights from trophic cascade theory(2008) Denno, Robert; Gruner, Daniel; Kaplan, IanEntomopathogenic nematodes (EPN) are ubiquitous and generalized consumers of insects in soil food webs, occurring widely in and agricultural ecosystems on all continents. Augmentative releases of EPN have been used to enhance biological control of pests in agroecosystems. Pest managers strive to achieve a trophic cascade whereby natural-enemy effects permeate down through the food web to suppress host herbivores and increase crop production. Although trophic cascades have been studied in diverse aboveground arthropod-based systems, they are infrequently investigated in soil systems. Moreover, no overall quantitative assessment of the effectiveness of EPN in suppressing hosts with cascading benefits to plants has been made. Toward synthesizing the available but limited information on EPN and their ability to suppress prey and affect plant yield, we surveyed the literature and performed a meta-analysis of 35 published studies. Our analysis found that effect sizes for arthropod hosts as a result of EPN addition were consistently negative and indirect effects on plants were consistently positive. Results held across several different host metrics (abundance, fecundity and survival) and across several measures of plant performance (biomass, growth, yield and survival). Moreover, the relationship between plant and host effect size was strikingly and significantly negative. That is, the positive impact on plant responses generally increased as the negative effect of EPN on hosts intensified, providing strong support for the mechanism of trophic cascades. We also review the ways in which EPN might interact antagonistically with each other and other predators and pathogens to adversely affect host suppression and dampen trophic cascades. We conclude that the food web implications of multiple-enemy interactions involving EPN are poorly studied, but, as management techniques that promote the long-term persistence of EPN are improved, antagonistic interactions are more likely to arise. We hope that the likely occurrence of antagonistic interactions in soil food webs should stimulate researchers to conduct field experiments explicitly designed to examine multiple-enemy interactions involving EPN and their cascading effects to hosts and plants.Item Dynamics of a subterranean trophic cascade in space and time(2008) Ram, Karthik; Gruner, Daniel; McLaughlin, John; Preisser, Evan; Strong, DonaldTrophic cascades, whereby predators indirectly benefit plant biomass by reducing herbivore pressure, form the mechanistic basis for classical biological control of pest insects. Entomopathogenic nematodes (EPN) are lethal to a variety of insect hosts with soil-dwelling stages, making them promising biocontrol agents. EPN biological control programs, however, typically fail because nematodes do not establish, persist and/or recycle over multiple host generations in the field. A variety of factors such as local abiotic conditions, host quantity and quality, and rates of movement affect the probability of persistence. Here, we review results from 13 years of study on the biology and ecology of an endemic population of Heterorhabditis marelatus (Rhabditida: Heterorhabditidae) in a California coastal prairie. In a highly seasonal abiotic environment with intrinsic variation in soils, vegetation structure, and host availability, natural populations of H. marelatus persisted at high incidence at some but not all sites within our study area. Through a set of field and lab experiments, we describe mechanisms and hypotheses to understand the persistence of H. marelatus. We suggest that further ecological study of naturally occurring EPN populations can yield significant insight to improve the practice and management of biological control of soil-dwelling insect pests.Item A cross-system synthesis of herbivore and nutrient resource control on producer biomass(2008-07) Gruner, Daniel; Smith, Jennifer; Seabloom, Eric; Sandin, Stuart; Ngai, Jacqueline; Hillebrand, Helmut; Harpole, Stanley; Elser, James; Cleland, Elsa; Bracken, Matthew; Borer, Elizabeth; Bolker, BenjaminNutrient availability and consumption by herbivores control the biomass of primary producer communities to varying degrees across ecosystems. Ecological theory, individual experiments in many different systems, and system-specific quantitative reviews have suggested that 1) bottom-up control is pervasive but top-down control is more influential in aquatic habitats relative to terrestrial systems, and 2) bottom-up and top-down forces often interact to synergize or dampen relative influences on producer biomass. We use a simple set of dynamic models to review mechanistic hypotheses for these questions, and compare model predictions to empirical data from a comprehensive meta-analysis of 191 factorial manipulations of herbivores and nutrients from freshwater, marine and terrestrial ecosystems. Parameterized model equilibria suggest that interactive outcomes should be weak and less common than strict additivity. Producer community biomass responded positively to fertilization across all systems, although effects were most pronounced in freshwater. Herbivores suppressed producer biomass in both freshwater and marine systems, but effects were inconsistent on land. Importantly, we observed a striking absence of either synergistic or dampening interactive effects of nutrients and herbivores across ecosystem types and within most habitats. Marine temperate rocky reef systems, which showed superadditive synergism of nutrient and herbivore controls, represented an exception to this pattern. Experimental studies showed limited support for emergent interactive effects on producer community-level biomass. We suggest that compensation by multiple herbivore guilds, top-down control of herbivores, spatial and temporal heterogeneity, and herbivore-mediated nutrient recycling tend to reduce the expectation for consistent interactive effects on producer biomass. Continuing studies should expand the temporal and spatial scales of experiments, particularly in understudied terrestrial systems; broaden factorial designs to manipulate independently both multiple producer resources (e.g. nitrogen, phosphorus, light) and multiple herbivore taxa or guilds (e.g. vertebrates and invertebrates); and simultaneously assess the effects on not only producer biomass but also species diversity, community composition and structure, and nutrient status.Item Birds as predators in tropical agroforestry systems(2008-04) Van Bael, Sunshine; Philpott, Stacy; Greenberg, Russell; Bichier, Peter; Barber, Nicholas; Mooney, Kailen; Gruner, DanielInsectivorous birds reduce arthropod abundances and their damage to plants in some, but not all, studies where predation by birds has been assessed. The variation in bird effects may be due to characteristics such as plant productivity or quality, habitat complexity, and/or species diversity of predator and prey assemblages. Since agroforestry systems vary in such characteristics, these systems provide a good starting point for understanding when and where we can expect predation by birds to be important. We analyze data from bird exclosure studies in forests and agroforestry systems to ask whether birds consistently reduce their arthropod prey base and whether bird predation differs between forests and agroforestry systems. Further, we focus on agroforestry systems to ask whether the magnitude of bird predation (1) differs between canopy trees and understory plants, (2) differs when migratory birds are present or absent, and (3) correlates with bird abundance and diversity. We found that, across all studies, birds reduce all arthropods, herbivores, carnivores, and plant damage. We observed no difference in the magnitude of bird effects between agroforestry systems and forests despite simplified habitat structure and plant diversity in agroforests. Within agroforestry systems, bird reduction of arthropods was greater in the canopy than the crop layer. Top-down effects of bird predation were especially strong during censuses when migratory birds were present in agroforestry systems. Importantly, the diversity of the predator assemblage correlated with the magnitude of predator effects; where the diversity of birds, especially migratory birds, was greater, birds reduced arthropod densities to a greater extent. We outline potential mechanisms for relationships between bird predator, insect prey, and habitat characteristics, and we suggest future studies using tropical agroforests as a model system to further test these areas of ecological theory.Item Does species richness drive speciation? A reassessment with the Hawaiian biota(Ecography, 2008) Gruner, Daniel; Gotelli, Nicholas; Price, Jonathan; Cowie, Robert
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