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Root-feeding Insects

Root-feeding Insects. Peter B. McEvoy Oregon State University. Outline. The nature of the root resource Effects of plants on insects Nutritional ecology of root-feeders Effects of insects on plants Ecophysiology of photosynthesis, water and nutrient use

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Root-feeding Insects

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  1. Root-feeding Insects Peter B. McEvoy Oregon State University

  2. Outline • The nature of the root resource • Effects of plants on insects • Nutritional ecology of root-feeders • Effects of insects on plants • Ecophysiology of photosynthesis, water and nutrient use • Source-sink dynamics, resource allocation patterns • Life histories (e.g. annual, biennial, perennial) • Population and Community Dynamics • Well-studied cases • Ecological studies - Periodic cicadas on trees • Agricultural systems • corn rootworm (Diabrotica spp.) feeding on maize roots • root fly (Delia spp.) feeding on Brassica crops • Sitona weevils feeding on legumes • Biological control systems • Flea beetle Longitarsus on ragwort • Root weevil Hylobius on purple loosestrife

  3. Two Articles for Review • ONE GENERAL: Blossey, B., and T. R. Hunt-Joshi. 2003. Belowground Herbivory by Insects: Influence on Plants and Aboveground Herbivores. Annual Review Entomology 48:521-547. • ONE SPECIFIC: Hunt-Joshi, T. R., B. Blossey, and R. B. Root. 2004. Root and leaf herbivory on Lythrum salicaria: Implications for plant performance and communities. Ecological Applications 14:1574-1589.

  4. The World is Green HypothesisHairston, Smith, and Slobodkin 1960 • Herbivores are regulated by top-down influence of natural enemies • And not the availability of plants • Contrary to this hypothesis, not all that is green is suitable food – quality as well as quantity matters. Much of it is toxic or indigestible. Carnivore Herbivore Plant

  5. Motivation for studying root feedersApplications in Agriculture and Biological Control Blossey, B., and T. R. Hunt-Joshi. 2003

  6. Root feeders increasingly used for Biological Control of Weeds Number of Cases Blossey, B., and T. R. Hunt-Joshi. 2003

  7. Root feeders as Pests Notching on white clover caused by adults • Lucerne weevilSitona discoideus Damage to roots by larvae www.agresearch.co.nz/CRW/images/LucerneWeevil.jpg

  8. Root Feeders as PestsCorn Root Worms Southern corn rootworm (spotted cucumber beetleDiabrotica undecimpunctata howardi , Coleoptera: Chrysomelidae) Northern corn rootworm Diabrotica barberi Western corn rootworm Diabrotica virgifera virgifera Heavy feeding by larvae causes injury to roots http://www.ent.iastate.edu/imagegal/coleoptera/rw/southerncornrwjb.html

  9. A conceptual model dead on arrivalpredicting root feeders would be negatively affected by competitively superior aboveground herbivores Root Feeder Foliage Feeder Limits food available Limits root growth Root removal limits plant’s ability to foraging for H20 and nutrients Stress response increases soluble N and CH Plant Masters et al. Oikos 66:1 (1993)

  10. Biological ControlLower Columbia River Purple loosestrife (Lythrum salicaria)

  11. Effects of invaders on the community • How do plant invasions influence community structure? Plant invasions reduce plant and animal diversity • Does biological control of a plant invader restore plant and animal diversity? Is passive restoration sufficient, or is active restoration necessary?

  12. Invader abundance goes up…. Diversity (and ecosystem services) go down Reed canary grass (Phalaris arundinacea) Purple loosestrife (Lythrum salicaria) y = -0.4179x + 41.162 R2 = 0.8705 y = -0.3549x + 35.695 R2 = 0.6497 Number of Plant Species Purple Loosestrife % Cover Reed Canary Grass % Cover

  13. Purple loosestrife and introduced biological control agents Foliage-feeder Capsule-feeder Seed weevil Nanophyes marmoratus Leaf beetles Galerucella spp. Root weevil Hylobius transversovittatus

  14. Transient dynamics revealed by the purple loosestrife system • Biological control resembles an invasion process • Releasing and Establishing Control Organisms • Increasing and Redistributing Control Organisms • Damaging and Suppressing the Target Organism • Managing Plant Succession • Ecology can guide development of biological control step-by-step Purple Loosestrife Lythrum salicaria

  15. Combinatorial Ecology of Biological Weed Control Specialists: Insects Generalists: Ungulates Herbivores Ragwort Other Plants Resources

  16. Herbivore Effects on Plant Performance • Both direct and indirect (i.e. via intermediate variables) effects – What prior examples have we seen? • Manifest at multiple organizational, spatial, and temporal scales of observation – How have we previously linked individuals and populations? • Hunt-Joshi et al. (2004) measure independent and interacting effects of a root-feeder (Hylobius) and foliage-feeder (Galerucella) on plant performance (measured as growth, biomass allocation), litter dynamics, plant community composition, and changes in canopy temperature, humidity, and light penetration

  17. Important questions • Plant performance. How do plant-feeding insects influence plant performance? • Plant population dynamics. How do plant-feeding insects influence plant vital rates and population dynamics? • Are the effects of (1) multiple herbivore species (root and foliage feeders), (2) plant competition and herbivory – antagonistic, independent, synergistic?

  18. Biological control hypothesis • Caricature:Absence of effective natural enemies is the cause of invasions, addition of effective natural enemies is the cure. • Direct and Indirect Effects of Biological Control: What are the independent and interacting effects of multiple herbivore species – a leaf-feeding beetle (Galerucella calmariensis L.) and a root-feeding weevil (Hylobius transversovittatus Goeze) on L. salicaria performance (growth, biomass allocation), litter accumulation and decomposition, light penetration through the canopy, and plant community composition?

  19. Factorial Experimental Design • Five treatments - Each replicated 10 times; 50 experimental units. Use a single, arbitrary, fixed level of each herbivore. Four-year duration 1997-2000. (1) leaf herbivory, (2) root herbivory, (3) combined leaf and root herbivory, (4) caged control (5) uncaged controls • Many Responses Variables (caution advised) - plant performance (stem height, density, flowering; stem growth rate), stem density and height of Aster lanceolatus; species richness of plant community • Also litter and canopy measurements • Analyzed using repeated-measures ANOVA

  20. Experimental Layout • Fifty 3.3 m length x 3.3 m width x 1.8 m height plots • Five treatments, 10 reps • Nine 1 x 1 m quadrats within each plot, 30 cm buffer between quadrats • Unwanted side effects • Cage changes microclimate - wind, light (15% shade), moisture • Cage excludes pollinators, resulting in near elimination of seed set Experimental Unit - Cage entraps predators that eat focal herbivores

  21. Quick Summary of Results • Main effects on plant performance • Increased over time. • Leaf herbivory > Root herbivory • Interactions - Leaf herbivory and root herbivory seldom interact in their effects • Community response (fig 6, 7) • Slight increase in Species Richness • Leaf herbivory increases biomass of other plants; root herbivory had no effect • Leaf herbivory increases Aster lanceolatus; root herbivory had no effect • Cages had unwanted side effects

  22. Shoot Growth Rate in final year 2000Independent effects: Leaf Herbivory yields stronger suppression than Root HerbivoryJoint effects: LHRH does not yield stronger suppression than LH • Fig. 1 LH <RH LHRH ~ RH Effects consistent across season UCC?

  23. Effects on Plant Performance 1997-2000 Stem Length • LH reduced stem height and flowering with a time delay, but had no effect on stem density • RH had no effect on stem height or flowering, but reduced stem density • No interaction between LH and RH on any of response variables Stem Density Flower frequency

  24. Live Biomass at Final Harvest • LH and RH reduced inflorescence, leaf and live stem biomass • LHstronger reduction than RH • LHand RHdid not interact in their effects UCC CC LH RH LHRH

  25. Dead Biomass at Final Harvest • RH increased shoot mortality (Fig 3D) • LH but not RH reduced standing dead (Fig 3E) • No LH x RH interaction

  26. Biomass Allocation in Living PlantsEffects of LH (leaf herbivory) and RH (root herbivory) on(A) Inflorescences (B) Leaves(C) StemsRoots not evaluated UCC CC LH RH LHRH

  27. Insects and Ecosystem FunctionEffects of Resource PulsesCaused by Cicadas (B) Upon emerging they mate, lay eggs, die and drop to forest floor (A) Cicadas accumulate N as they feed in juvenile stages (C) Accumulated N is released after a burst of microbial activity (D) Spike of N leads to increased N content and seed size in understory plant, the American bellflower (Campanulastrum americanum), an understory plant

  28. Campanulastrumamericanum (L.) Small American bellflower (Campanulaceae) http://plants.usda.gov/java/profile?symbol=CAAM18&photoID=caam6_005_ahp.tif

  29. Cicada Life Cycle Females Males After 12-17 yr below ground, nymphs exit via tunnels http://hydrodictyon.eeb.uconn.edu/projects/cicada/NA/Magicicada/index.html

  30. Fig. 1. Cicada litterfall increases soil bacterial and fungal PLFAs relative to those of controls, indicating increased microbial biomass No difference PHOSPHOLIPID FATTY ACIDS (PLFAs) No detectable differences between PLFAs between control (0 cicadas m-2) and treatment (120 cicadas m-2) after 7 days, differences emerge after 28 days Difference Bacteria Fungi L. H. Yang Science 306, 1565 -1567 (2004) Time in Days Published by AAAS

  31. Fig. 2. Cicada litterfall increases indices of soil nitrate and ammonium availability in forest soils Ammonium Large effect in first 30 days No effect days 31-100 Nitrate Large effect in first 30 days Continued effect days 31-100 L. H. Yang Science 306, 1565 -1567 (2004) NPP believe to be N-limited in these forests Published by AAAS

  32. Fig. 3. Cicada litterfall increases (A) foliage nitrogen content, (B) foliage {delta}15N, and (C) seed size in cicada-supplemented American bellflowers relative to controls Higher foliage N stable isotope of N seed mass Infer animal origin of N +140 cicadas m-2 L. H. Yang Science 306, 1565 -1567 (2004) Published by AAAS

  33. Conclusions from Cicadas • Cicada litterfall during emergence years can cause substantial pulsed enrichment of forest soils • Withdirect effects on belowground systems and indirect effects aboveground • Negative effects of Cicada herbivory and oviposition plants may be partially offset by positive effects on primary productivity due to pulse fertilization • Rare perturbations can have lasting effects in diverse ecological systems

  34. Conclusions • Foliage-feeders have been well-studied • …but root-feeders have been neglected • RF better known as pests and biocontrol organisms than as components of natural systems • Direct and indirect effects of root-feeders on individual plants are better known than effects on plant populations and communities or ecosystems • We need more cross-scale studies – looking across organizational, spatial and temporal scales to see how qualitative description changes with scale, to link processes occurring at difference scales

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