Root-feeding Insects

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 48521-547.
• 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 141574-1589.

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 feeders
Applications 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 beetle
  Diabrotica 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
Foliage Feeder
Root Feeder
Limits food available
Limits root growth
Root removal limits plants ability to foraging
for H20 and nutrients
Stress response increases soluble N and CH
Plant
Masters et al. Oikos 661 (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
Reed Canary Grass Cover
Purple Loosestrife 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
Generalists Ungulates
Specialists Insects
Herbivores
Other Plants
Ragwort
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 gt 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 lt 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
• LH stronger reduction than RH
• LH and RH did 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 Plants Effects 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
Campanulastrum americanum (L.) Small American
bellflower (Campanulaceae)
http//plants.usda.gov/java/profile?symbolCAAM18
photoIDcaam6_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
No effect days 31-100
Large effect in first 30 days
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 delta15N, 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
• With direct 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

35
(No Transcript)