Entomology
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Item Evidence for divergent selection between the molecular forms of Anopheles gambiae: role of predation(Springer Nature, 2008-01-11) Diabaté, Abdoulaye; Dabiré, Roch K; Heidenberger, Kyle; Crawford, Jacob; Lamp, William O; Culler, Lauren E; Lehmann, ToviThe molecular forms of Anopheles gambiae are undergoing speciation. They are characterized by a strong assortative mating and they display partial habitat segregation. The M form is mostly found in flooded/irrigated areas whereas the S form dominates in the surrounding areas, but the ecological factors that shape this habitat segregation are not known. Resource competition has been demonstrated between species undergoing divergent selection, but resource competition is not the only factor that can lead to divergence. In a field experiment using transplantation of first instar larvae, we evaluated the role of larval predators in mediating habitat segregation between the forms. We found a significant difference in the ability of the molecular forms to exploit the different larval sites conditioned on the presence of predators. In absence of predation, the molecular forms outcompeted each other in their respective natural habitats however, the developmental success of the M form was significantly higher than that of the S form in both habitats under predator pressure. Our results provide the first empirical evidence for specific adaptive differences between the molecular forms and stress the role of larval predation as one of the mechanisms contributing to their divergence.Item Toward reconstructing the evolution of advanced moths and butterflies (Lepidoptera: Ditrysia): an initial molecular study(Springer Nature, 2009-12-02) Regier, Jerome C; Zwick, Andreas; Cummings, Michael P; Kawahara, Akito Y; Cho, Soowon; Weller, Susan; Roe, Amanda; Baixeras, Joaquin; Brown, John W; Parr, Cynthia; Davis, Donald R; Epstein, Marc; Hallwachs, Winifred; Hausmann, Axel; Janzen, Daniel H; Kitching, Ian J; Solis, M Alma; Yen, Shen-Horn; Bazinet, Adam L; Mitter, CharlesIn the mega-diverse insect order Lepidoptera (butterflies and moths; 165,000 described species), deeper relationships are little understood within the clade Ditrysia, to which 98% of the species belong. To begin addressing this problem, we tested the ability of five protein-coding nuclear genes (6.7 kb total), and character subsets therein, to resolve relationships among 123 species representing 27 (of 33) superfamilies and 55 (of 100) families of Ditrysia under maximum likelihood analysis. Our trees show broad concordance with previous morphological hypotheses of ditrysian phylogeny, although most relationships among superfamilies are weakly supported. There are also notable surprises, such as a consistently closer relationship of Pyraloidea than of butterflies to most Macrolepidoptera. Monophyly is significantly rejected by one or more character sets for the putative clades Macrolepidoptera as currently defined (P < 0.05) and Macrolepidoptera excluding Noctuoidea and Bombycoidea sensu lato (P ≤ 0.005), and nearly so for the superfamily Drepanoidea as currently defined (P < 0.08). Superfamilies are typically recovered or nearly so, but usually without strong support. Relationships within superfamilies and families, however, are often robustly resolved. We provide some of the first strong molecular evidence on deeper splits within Pyraloidea, Tortricoidea, Geometroidea, Noctuoidea and others. Separate analyses of mostly synonymous versus non-synonymous character sets revealed notable differences (though not strong conflict), including a marked influence of compositional heterogeneity on apparent signal in the third codon position (nt3). As available model partitioning methods cannot correct for this variation, we assessed overall phylogeny resolution through separate examination of trees from each character set. Exploration of "tree space" with GARLI, using grid computing, showed that hundreds of searches are typically needed to find the best-feasible phylogeny estimate for these data. Our results (a) corroborate the broad outlines of the current working phylogenetic hypothesis for Ditrysia, (b) demonstrate that some prominent features of that hypothesis, including the position of the butterflies, need revision, and (c) resolve the majority of family and subfamily relationships within superfamilies as thus far sampled. Much further gene and taxon sampling will be needed, however, to strongly resolve individual deeper nodes.Item Ground-dwelling beetles as bioindicators in transgenic corn(2009) Lepping, Miles; Shrewsbury, Paula M; Dively, Galen P; Entomology; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)Ecological risk assessment for transgenic crops requires identification of appropriate biological indicator organisms for use in laboratory and field biomonitoring studies. Ground-dwelling predatory beetles in the families Carabidae and Staphylinidae comprise a diverse and abundant group of nontarget organisms in field corn systems where rootworm-resistant transgenic varieties are deployed. First, the utility of two sampling methods (pitfall trapping and suction-based litter extraction) was assessed for estimating ground beetle (Coleoptera: Carabidae) population parameters in Maryland cornfields. Sampling bias was established for pitfall trapping, confirming the limitations of this semi-quantitative method for capturing a representative portion of the epigeal community. Litter extraction data conformed to predictions for abundance in relation to trophic identity, body size and biomass. Litter extraction identified smaller bodied carabid omnivores and carnivores as numerically dominant over larger bodied species that have received focus in risk assessment studies. A small-bodied carabid, Elaphropus xanthopus (Dejean), was identified as the dominant carnivore, and therefore selected for nontarget exposure and toxicity studies. Second, in choice and no-choice experiments, corn pollen was identified as a realistic, direct exposure pathway to transgenic proteins for E. xanthopus. Third, organism-level exposure to Cry34Ab1 rootworm-resistant protein was demonstrated for E. xanthopus in the laboratory and field during corn pollen shed. Field studies also revealed contamination across transgenic and non-transgenic test plots, indicating experimental design must account for the movement of study organisms and/or transgenic plant tissues. Finally, a toxicity study examined the effects of dietary exposure to rootworm-resistant Cry34/35Ab1 corn pollen for two beetle species, a carabid, E. xanthopus, and a staphylinid, Strigota ambigua (Erichson). Transgenic pollen exposure did not affect longevity or sub-lethal behaviors for either species. Small-bodied, predatory ground beetles are recommended as candidate bioindicator organisms in risk assessment studies designed to optimize field monitoring, exposure detection, and bioassay for transgenic pesticides.Item GENETIC DIVERSIFICATION, SAPROPHYTIC COMPETENCE AND GENETIC ENHANCEMENT OF THE ENTOMOPATHOGENIC FUNGUS METARHIZIUM(2009) Pava-Ripoll, Monica Patricia; St. Leger, Raymond J; Entomology; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)Entomopathogenic fungi are being investigated as alternatives to chemical insecticides. This study explored the versatility of the entomopathogenic fungus Metarhizium anisopliae by examining its diversification, saprophytic competence and potential for genetic enhancement. M. anisopliae is a radiating species containing both generalist and specialized lineages with broad and narrow host ranges and as such provides an excellent model system to study the evolution of pathogenesis. Using 18S RNA and protease sequences, I demonstrated that strains can be selected representing evolutionary distances ranging from <1 to 8 MY and their natural molecular variation allows analysis of processes of adaptive change. M. anisopliae is particularly abundant in the rhizosphere. Germination of M. anisopliae strain 2575 was >96% in 1 mg/ml root exudate (RE) and growth in RE resulted in 29 (58%) genes being up-regulated and 21 (42%) down-regulated. The identity of these genes is helping to define the physiological requirements for rhizosphere competence. Hypothetical and orphans proteins (41.4%) were also actively expressed indicating that many previously uncharacterized genes may have functions related to survival at the soil-root interphase. Using the fungus as a delivery vehicle for foreign toxins presents a powerful approach for increasing virulence. M. anisopliae was modified to express a scorpion toxin (AaIT) in insect haemolymph and bioassayed against the coffee berry borer Hypothenemus hampei. AaIT increased mortality up to 56.6%, and reduced the medial lethal concentration (LC 50 ) by 15.7-fold and the average survival time (AST) by 20.1%. The AaIT gene and the M. anisopliae esterase gene (Mest1) were inserted into three strains of Beauveria bassiana (ARSEF 252, 8998 and 9184) with high, medium and low mortality, respectively, against the Colorado potato beetle (CPB) Leptinotarsa decemlineata. Mortality rates were strain- and dose- dependant and increased from 16.1 to 36.7% in single transformants (AaIT or Mest1) and from 7.1 to 33.5% in double transformants (AaIT-Mest1). The AST was reduced up to 33% and the LC50 up to 5.9-fold. Although singly both AaIT and Mest1 increased the killing power of B. bassiana against second instar CPB, combining AaIT and Mest1 together did not produce synergistic effects.Item KINEMATICS OF THE MAYFLY NYMPH GILL ARRAY: AN INTERMEDIATE REYNOLDS NUMBER VENTILATION PUMP(2009) Sensenig, Andrew T.; Shultz, Jeffrey W.; Kiger, Ken T.; Entomology; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)Comparative studies encompassing a wide range of aquatic animals have shown that rowing is exclusively used at low Reynolds numbers (Re <1) while flapping is predominantly used at Re > 100, but few studies have been undertaken to document the transition in individual species that traverse the intermediate Re regime using a single set of appendages. Thus, it is not generally known whether a gradual increase in Re within a system results in a gradual or sudden shift between rowing and flapping. Here I document both the kinematics of the appendages and the surrounding fluid of a nymphal mayfly Centroptilum triangulifer that uses a serial array of seven pairs of abdominal gill plates and operates at Reynolds numbers ranging from 2-22 during ontogeny. I found that some kinematic variables (stroke frequency and metachronal phase lag) did not change during ontogeny but that others changed substantially. Specifically, gills in small instars used strokes with large pitch and stroke-plane deviations, while larger instars used strokes with minimal pitch and minimal stroke-plane deviation. Gills in larger instars also acquired an intrinsic hinge that allowed passive asymmetric movement between half strokes. Net flow in small animals was directed ventrally and essentially parallel to the stroke plane (i.e. rowing), but net flow in large animals was directed dorsally and essentially transverse to the stroke plane (i.e. flapping). The metachronal phasing of the gills produced a time-dependent array of vortices associated with a net ventilatory current, a fluid kinematic pattern here termed a "phased vortex pump". Significantly, absolute vortex size did not change with increasing animal size or Re, indicating that the vortex diameter (Lv) decreased relative to intergill spacing (Lis) during mayfly growth. Given that effective flapping requires organized flow between adjacent appendages, I proposed the hypothesis that rowing should be favored when Lis / Lv < 1 and flapping should be favored when Lis / Lv > 1. Significantly, the rowing-to-flapping transition in Centroptilum triangulifer occurs at Re ~5, when maximum dynamic intergill distance equals vortex diameter. This result suggests that the Re-based rowing-flapping demarcation observed in a wide array of aquatic organisms is determined by the relative size of the propulsive mechanism and its self-generated vortices.Item Nutrient regulation by an omnivore and the effects on performance and distribution(2009) Pearson, Rachel Estelle Goeriz; Gruner, Daniel S; Entomology; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)Omnivores have a unique interaction with their nutritional environment because they have adapted to consume food from different trophic levels. To successfully navigate their variable resources, omnivores must maintain some level of nutrient regulation. To explore the effects of nutrient regulation by an omnivore, I used a salt marsh katydid, Conocephalus spartinae. To first address the ability of Conocephalus to perform on a wide range of diets and to regulate their nutritional intake, I used artificial diets that differed in relative amounts of protein and carbohydrate (Chapter 1). I found that Conocephalus survival decreased on a high protein diet due in part to a decrease in lipid stores but growth was not affected by diet. In a second experiment Conocephalus showed a degree of nutrient regulation as evidenced by the difference in what they actually ate and the predicted consumption if they had been feeding equally on the diets presented in each treatment. However, I did not find evidence for tight macronutrient regulation. Next I explored capacity of Conocephalus to regulate their nutrient intake (nitrogen and lipid) when fed naturally co-occurring prey (Chapter 2). I first established that the prey differed in their protein and lipid content and that these differences were related to the size of the prey species. When Conocephalus were fed different prey species individuals showed no differences in either growth or survival. In the final experiment, I found that Conocephalus did show evidence of a degree of nitrogen and lipid regulation because they did not feed equally on all of the prey species offered. Lastly, I documented the relationship between the ability of Conocephalus to locate plant and prey resources and the effect that these resources have on omnivore performance (Chapter 3). I found that Conocephalus aggregates in areas of high plant quality but that their numbers do not correspond to areas of high prey density. However, I found that katydid growth and survival was enhanced by prey availability but not plant quality. Overall, I documented how an organism like an omnivore relates to its nutritional environment and how nutrient regulation might affect performance and distribution. Last, I documented the relationship between the ability of katydids to locate plant and prey resources and the effect that these resources have on omnivore performance (Chapter 3). I found that katydids aggregate in areas of high plant quality but that their numbers do not correspond to areas of high prey density.Item Soldier neotenics of Zootermopsis nevadensis (Hagen) and Archotermopsis sp. (Isoptera: Termopsidae): Morphology, Development, Behavior, and Evolution(2009) Johnson, Susan Elaine; Thorne, Barbara L; Entomology; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)I: The relictual reproductive soldier neotenics of primitive Termopsid termites may offer insights into the evolution of eusociality and sterile castes in termites. II: Soldiers and helpers in a new Thai species of Archotermopsis do not display unusually complete gonad development. The first neotenic pair ever reported for this genus is described. III: Morphological differences between soldiers and soldier neotenics in the head and gonads are quantified in Z. nevadensis. There is not necessarily a clear delineation in morphology between soldiers and soldier neotenics. IV: Colony age and size do not significantly influence the differentiation or survival of male replacement reproductives in colonies of Z. nevadensis. Soldier neotenics' development is not significantly influenced by the presence of normal soldiers. V: Soldier neotenics and related female neotenics tend to have greater initial survival after interactions with colonies with only normal neotenics. Mostly helpers are aggressors, never soldier neotenics or neotenics.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 Indirect Effects of Imidacloprid on Natural Enemies of Spider Mites in Two Systems(2009) Creary, Scott; Raupp, Michael J; Entomology; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)With a growing number of reports showing secondary outbreaks of spider mites following systemic applications of imidacloprid, a study was designed to test the indirect effects of this insecticide on natural enemies of spider mites. We exposed two predators, Chrysoperla rufilabris and Stethorus punctillum, to mites that were reared on boxwoods and elms treated with imidacloprid and examined prey consumption, predator mobility and mortality. Mites reared on treated foliage were extremely toxic to predators, eliciting sharp reductions in feeding, locomotion, and longevity. These findings document that non-target pests feeding on plants treated with imidacloprid cause lethal and sublethal responses in natural enemies. We discuss implications on the compatibility of imidacloprid with IPM practices and infer impacts on generalist and specialist natural enemies.