Valérie Fournier

Identifying the predator complex of Homalodisca vitripennis (Hemiptera: Cicadellidae): a comparative study of the efficacy of an ELISA and PCR gut content assay

A growing number of ecologists are using molecular gut content assays to qualitatively measure predation. The two most popular gut content assays are immunoassays employing pest-specific monoclonal antibodies (mAb) and polymerase chain reaction (PCR) assays employing pest-specific DNA. Here, we present results from the first study to simultaneously use both methods to identify predators of the glassy winged sharpshooter (GWSS), Homalodisca vitripennis (Germar) (Hemiptera: Cicadellidae). A total of 1,229 arthropod predators, representing 30 taxa, were collected from urban landscapes in central California and assayed first by means of enzyme-linked immunosorbent assay (ELISA) using a GWSS egg-specific mAb and then by PCR using a GWSS-specific DNA marker that amplifies a 197-base pair fragment of its cytochrome oxidase gene (subunit I). The gut content analyses revealed that GWSS remains were present in 15.5% of the predators examined, with 18% of the spiders and 11% of the insect predators testing positive. Common spider predators included members of the Salticidae, Clubionidae, Anyphaenidae, Miturgidae, and Corinnidae families. Common insect predators included lacewings (Neuroptera: Chrysopidae), praying mantis (Mantodea: Mantidae), ants (Hymenoptera: Formicidae), assassin bugs (Hemiptera: Reduviidae), and damsel bugs (Hemiptera: Nabidae). Comparison of the two assays indicated that they were not equally effective at detecting GWSS remains in predator guts. The advantages of combining the attributes of both types of assays to more precisely assess field predation and the pros and cons of each assay for mass-screening predators are discussed.

Development of molecular diagnostic markers for sharpshooters Homalodisca coagulata and Homalodisca liturata for use in predator gut content examinations

To aid in identifying key predators of Proconiini sharpshooter species present in California, we developed and tested molecular diagnostic markers for the glassy‐winged sharpshooter, Homalodisca coagulata (Say), and smoke‐tree sharpshooter, Homalodisca liturata (Ball) (Homoptera: Cicadellidae). Two different types of markers were compared, those targeting single‐copy sequence characterized amplified regions (SCAR) and mitochondrial markers targeting the multicopy cytochrome oxidase subunit genes I (COI) and II (COII). A total of six markers were developed, two SCAR and four mitochondrial COI or COII markers. Specificity assays demonstrated that SCAR marker HcF5/HcR7 was H. coagulata specific and HcF6/HcR9 was H. coagulata/H. liturata specific. COI (HcCOI‐F/R) and COII (HcCOII‐F4/R4) markers were H. coagulata specific, COII (G/S‐COII‐F/R) marker was H. coagulata/H. liturata specific, and lastly, COII marker (Hl‐COII‐F/R) was H. liturata specific. Sensitivity assays using genomic DNA showed the COI marker to be the most sensitive marker with a detection limit of 6 pg of DNA. This marker was 66‐fold more sensitive than marker Hl‐COII‐F/R that showed a detection limit of 400 pg of DNA. In addition, the COI marker was 4.2‐fold more sensitive than the COII marker. In predator gut assays, the COI and COII markers demonstrated significantly higher detection efficiency than the SCAR markers. Furthermore, the COI marker demonstrated slightly higher detection efficiency over the COII marker. Lastly, we describe the inclusion of an internal control (28S amplification) for predation studies performing predator gut analyses utilizing the polymerase chain reaction (PCR). This control was critical in order to monitor reactions for PCR failures, PCR inhibitors, and for the presence of DNA.

Dose-Response Susceptibility of Pest Aphids (Homoptera: Aphididae) and their Control on Hydroponically Grown Lettuce with the Entomopathogenic Fungus Verticillium lecanii, Azadirachtin, and Insecticidal Soap

Abstract The objective of our research was to identify alternatives to synthetic pesticide treatments to prevent aphid outbreaks in greenhouse lettuce crops. In the laboratory, we determined the susceptibility of three lettuce-infesting aphid species, Macrosiphum euphorbiae (Thomas), Myzus persicae (Sulzer), and Nasonovia ribisnigri (Mosley), to the hyphomycete Verticillium lecanii (Viegas) (strain Vertalec), the plant triterpenoid molecule azadirachtin (BioNeem), and an insecticidal soap (Safer’s). Estimated LC50 and LT50 obtained in the laboratory indicated that the three aphid species were susceptible to the entomopathogenic fungus, the plant extract, and the soap. Under greenhouse conditions, we assessed the potential of the three pesticides to reduce aphid populations and compared it with that of a synthetic insecticide, the organophosphate Malathion. Greenhouse experiments demonstrated that all three pesticides significantly reduced the population of each aphid species compared with the untreated plants. This study also revealed differences in aphid susceptibility between aphid species and between laboratory bioassays and greenhouse trials. The high initial aphid densities, difficulties to reach the aphids on the undersurface of leaves, stains left by Vertalec on the harvested lettuce, and high cosmetic standards for lettuce mitigated the performance of the insecticides. The potential of using Vertalec, BioNeem, and Safer’s soap for the control of lettuce aphids is discussed in relation to aphid species and crop management.

MULTIPLE PLANT EXPLOITERS ON A SHARED HOST: TESTING FOR NONADDITIVE EFFECTS ON PLANT PERFORMANCE

The combined impact of multiple plant parasites on plant performance can either be additive (the total damage equals the sum of the individual effects) or nonadditive (synergistic or antagonistic damage). Two statistical models are available for testing the independent (=additive) effects of two factors. Here we suggest that the natural history of the plant-parasite system should motivate the choice of a statistical model to test for additivity. Using in-field, manipulative experiments, we examined the interactions between the herbivorous mite Calacarus flagelliseta Fletchmann, De Moraes and Barbosa (Acari: Eriophyidae), the fungal pathogen Oidium caricae F. Noack (a powdery mildew), and their host plant Carica papaya L. in Hawaii. First, we found that herbivorous mites had a moderate negative effect on powdery mildew: when mites were absent, powdery mildew colonies were larger and more numerous. Second, we showed that each plant parasite, when evaluated alone, significantly reduced several measures of plant performance. Third, we found that the combined impact of mites and mildew on plant performance is mostly additive and, for a few variables, less than additive. Finally, we explored compensatory responses and found no evidence for nonlinearities in the relationship between plant performance and cumulative parasite impact. Plants are almost universally subject to attack by multiple herbivores and pathogens; thus a deeper understanding of how multiple plant parasites shape each others population dynamics and plant performance is essential to understanding plant-parasite interactions.

Herbivorous mites as ecological engineers: indirect effects on arthropods inhabiting papaya foliage.

We examined the potential of a leaf roller to indirectly influence a community of arthropods. Two mite species are the key herbivores on papaya leaves in Hawaii: a spider mite, Tetranychus cinnabarinus Boisduval, and an eriophyid mite, Calacarus flagelliseta, which induces upward curling of the leaf margin at the end of the summer when populations reach high densities. A survey and three manipulative field experiments demonstrated that (1) leaf rolls induce a consistent shift in the spatial distribution of spider mites and their predators, the coccinellid Stethorus siphonulus Kapur, the predatory mites Phytoseiulus spp., and the tangle-web building spider Nesticodes rufipes Lucas; (2) the overall abundance of spiders increases on leaves with rolls; (3) the specialist predators Stethorus and Phytoseiulus inhabit the rolls in response to their spider mite prey; and (4) the spider inhabits the rolls in response to the architecture of the roll itself. This study shows the importance of indirect effects in structuring a terrestrial community of herbivores.

Herbivore population suppression by an intermediate predator, Phytoseiulus macropilis, is insensitive to the presence of an intraguild predator: an advantage of small body size?

Recent work in terrestrial communities has highlighted a new question: what makes a predator act as a consumer of herbivores versus acting as a consumer of other predators? Here we test three predictions from a model (Rosenheim and Corbett in Ecology 84:2538–2548) that links predator foraging behavior with predator ecology: (1) widely foraging predators have the potential to suppress populations of sedentary herbivores; (2) sit and wait predators are unlikely to suppress populations of sedentary herbivores; and (3) sit and wait predators may act as top predators, suppressing populations of widely foraging intermediate predators and thereby releasing sedentary herbivore populations from control. Manipulative field experiments conducted with the arthropod community found on papaya, Carica papaya, provided support for the first two predictions: (1) the widely foraging predatory mite Phytoseiulus macropilis strongly suppressed populations of a sedentary herbivore, the spider mite Tetranychus cinnabarinus, whereas (2) the tangle-web spider Nesticodes rufipes, a classic sit and wait predator, failed to suppress Tetranychus population growth rates. However, our experiments provided no support for the third hypothesis; the sit and wait predator Nesticodes did not disrupt the suppression of Tetranychus populations by Phytoseiulus. This contrasts with an earlier study that demonstrated that Nesticodes can disrupt control of Tetranychus generated by another widely foraging predator, Stethorus siphonulus. Behavioral observations suggested a simple explanation for the differing sensitivity of Phytoseiulus and Stethorus to Nesticodes predation. Phytoseiulus is a much smaller predator than Stethorus, has a lower rate of prey consumption, and thus has a much smaller requirement to forage across the leaf surface for prey, thereby reducing its probability of encountering Nesticodes webs. Small body size may be a general means by which widely foraging intermediate predators can ameliorate their risk of predation by sit and wait top predators. This effect may partially or fully offset the general expectation from size-structured trophic interactions that smaller predators are subject to more intense intraguild predation.

Pollen Loads and Specificity of Native Pollinators of Lowbush Blueberry

ABSTRACT The reproduction of lowbush blueberry (Vaccinium angustifolium Aiton) is closely tied to insect pollination, owing to self-incompatibility. Many species are known to have greater pollination efficiency than the introduced Apis mellifera L., commonly used for commercial purposes. In this study, we measured the pollen loads of several antophilous insect species, mostly Apoidea and Syrphidae, present in four lowbush blueberry fields in Lac-St-Jean, Québec. To measure pollen loads and species specificity toward V. angustifolium, we net-collected 627 specimens of pollinators, retrieved their pollen loads, identified pollen taxa, and counted pollen grains. We found that the sizes of pollen loads were highly variable among species, ranging from a few hundred to more than 118,000 pollen grains per individual. Bombus and Andrena species in particular carried large amounts of Vaccinium pollen and thus may have greater pollination efficiency. Also, two species (Andrena bradleyi Viereck and Andrena Carolina Viereck) showed nearly monolectic behavior toward lowbush blueberry. Finally, we identified alternative forage plants visited by native pollinators, notably species of Acer, Rubus, Ilex mucronata, Ledum groenlandicum, and Taraxacum. Protecting these flowering plants should be part of management practices to maintain healthy pollinator communities in a lowbush blueberry agroecosystem.

Increased Acetylcholinesterase Expression in Bumble Bees During Neonicotinoid-Coated Corn Sowing

While honey bee exposure to systemic insecticides has received much attention, impacts on wild pollinators have not been as widely studied. Neonicotinoids have been shown to increase acetylcholinesterase (AChE) activity in honey bees at sublethal doses. High AChE levels may therefore act as a biomarker of exposure to neonicotinoids. This two-year study focused on establishing whether bumble bees living and foraging in agricultural areas using neonicotinoid crop protection show early biochemical signs of intoxication. Bumble bee colonies (Bombus impatiens) were placed in two different agricultural cropping areas: 1) control (≥3 km from fields planted with neonicotinoid-treated seeds) or 2) exposed (within 500 m of fields planted with neonicotinoid-treated seeds), and maintained for the duration of corn sowing. As determined by Real Time qPCR, AChE mRNA expression was initially significantly higher in bumble bees from exposed sites, then decreased throughout the planting season to reach a similar endpoint to that of bumble bees from control sites. These findings suggest that exposure to neonicotinoid seed coating particles during the planting season can alter bumble bee neuronal activity. To our knowledge, this is the first study to report in situ that bumble bees living in agricultural areas exhibit signs of neonicotinoid intoxication.

Taxonomic and functional trait diversity of wild bees in different urban settings

Urbanization is one of the major anthropogenic processes contributing to local habitat loss and extirpation of numerous species, including wild bees, the most widespread pollinators. Little is known about the mechanisms through which urbanization impacts wild bee communities, or the types of urban green spaces that best promote their conservation in cities. The main objective of this study was to describe and compare wild bee community diversity, structure, and dynamics in two Canadian cities, Montreal and Quebec City. A second objective was to compare functional trait diversity among three habitat types (cemeteries, community gardens and urban parks) within each city. Bees were collected using pan traps and netting on the same 46 sites, multiple times, over the active season in 2012 and 2013. A total of 32,237 specimens were identified, representing 200 species and 6 families, including two new continental records, Hylaeus communis Nylander (1852) and Anthidium florentinum (Fabricius, 1775). Despite high community evenness, we found significant abundance of diverse species, including exotic ones. Spatio-temporal analysis showed higher stability in the most urbanized city (Montreal) but low nestedness of species assemblages among the three urban habitats in both cities. Our study demonstrates that cities are home to diverse communities of wild bees, but in turn affect bee community structure and dynamics. We also found that community gardens harbour high levels of functional trait diversity. Urban agriculture therefore contributes substantially to the provision of functionally diverse bee communities and possibly to urban pollination services.

Pupal Development of Aethina tumida (Coleoptera: Nitidulidae) in Thermo-Hygrometric Soil Conditions Encountered in Temperate Climates

ABSTRACT The pupal development of Aethina tumida Murray (Coleoptera: Nitidulidae) was studied at various combinations of thermo-hygrometric soil conditions (temperatures of 16, 18, and 20°C and soil water content levels of 0.37, 0.56, and 0.73 m3 water per cubic meter of dry soil) representative of southeastern Canada. Survivorship and development duration of A. tumida pupae, as well as sex ratio and life span of emerging adults, were assessed. Assays were conducted in growth chambers on an average of 50 third-instar larvae per thermo-hygrometric combination. Results show that survivorship of pupae decreased with lower temperature and higher soil water content. Pupal development time shortened as temperature increased (69–78 d at 16°C, 47–54 d at 18°C, and 36–39 d at 20°C), but was longer in dryer soil. Optimal soil water content for pupal development was 0.56 m3 water per cubic meter of soil. We estimated that the minimum development temperature for pupae is between 10.2 and 13.2°C, depending on soil water content. The sex ratio of emerging adults was influenced by soil water content. We measured one female to one male for dry and intermediately wet soils and three females to one male for wet soils. Higher soil water content reduced the life span of emerging adults by half. This study contributes to a better understanding of A. tumida population dynamics in eastern Canada.