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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

Root-feeding Insects

Peter B. McEvoy

Oregon State University

outline
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
two articles for review
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.
the world is green hypothesis hairston smith and slobodkin 1960
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

motivation for studying root feeders applications in agriculture and biological control
Motivation for studying root feedersApplications in Agriculture and Biological Control

Blossey, B., and T. R. Hunt-Joshi. 2003

root feeders increasingly used for biological control of weeds
Root feeders increasingly used for Biological Control of Weeds

Number of Cases

Blossey, B., and T. R. Hunt-Joshi. 2003

root feeders as pests
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

root feeders as pests corn root worms
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

slide9
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)

biological control lower columbia river
Biological ControlLower Columbia River

Purple loosestrife

(Lythrum salicaria)

effects of invaders on the community
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?
invader abundance goes up diversity and ecosystem services go down
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

purple loosestrife and introduced biological control agents
Purple loosestrife and introduced biological control agents

Foliage-feeder

Capsule-feeder

Seed weevil Nanophyes marmoratus

Leaf beetles Galerucella spp.

Root weevil Hylobius transversovittatus

transient dynamics revealed by the purple loosestrife system
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

combinatorial ecology of biological weed control
Combinatorial Ecology of Biological Weed Control

Specialists: Insects

Generalists: Ungulates

Herbivores

Ragwort

Other Plants

Resources

herbivore effects on plant performance
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
important questions
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?
biological control hypothesis
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?
factorial experimental design
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
experimental layout
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

quick summary of results
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
slide22

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?

effects on plant performance 1997 2000
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

live biomass at final harvest
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

dead biomass at final harvest
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
slide26

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

insects and ecosystem function effects of resource pulses caused by cicadas
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

campanulastrum americanum l small american bellflower campanulaceae
Campanulastrumamericanum (L.) Small American bellflower (Campanulaceae)

http://plants.usda.gov/java/profile?symbol=CAAM18&photoID=caam6_005_ahp.tif

cicada life cycle
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

slide30
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

fig 2 cicada litterfall increases indices of soil nitrate and ammonium availability in forest soils
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

slide32

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

conclusions from cicadas
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
conclusions
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