Download BIOS 5970: Plant-Herbivore Interactions

BIOS 5970: Plant-Herbivore Interactions
Dr. Stephen Malcolm, Department of Biological Sciences
•  Week 7. Tritrophic Interactions:
–  Lecture summary:
•  Third trophic level benefits plants:
•  Two paradoxes generated by:
– Sublethal (chronic) chemical defenses.
– Lethal (acute) chemical defenses.
•  Plant signals:
– Green leaf volatiles.
•  Community dynamics:
– Influence of natural enemies on plant
investment in chemical defenses.
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 7: Tritrophic Interactions
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2. Benefits of the third trophic level:
Price et al.
1980.
Ann. Rev.
Ecol. Syst.
11: 41-65:
Stressed
the
importance
to plants of
natural
enemies of
herbivores.
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 7: Tritrophic Interactions
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3. Two paradoxes posed by the third
trophic level:
•  (1) The “sublethal” plant defense paradox:
–  Sublethal plant defenses like digestibility reducers may
result in more plant tissue loss to herbivores because
they are forced to eat more to maintain nutrition.
–  Paradox is resolved by predators because herbivores
grow slower and are more vulnerable to natural
enemies.
•  (2) The “lethal” plant defense paradox:
–  Plant toxins sequestered by adapted specialist
herbivores may increase herbivore fitness through
enhanced defense against natural enemies.
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 7: Tritrophic Interactions
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4. The two paradoxes operate at
different trophic levels:
From: Malcolm (1995)
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 7: Tritrophic Interactions
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5. Evidence for the Sublethal Plant
Defense Paradox:
•  In their 1980 paper, Price et al. (Ann. Rev. Ecol.
Syst. 11: 41-65) described an unpublished
experiment by Bouton, Price and Kogan (Table 1):
–  It was not published in Am. Nat. as cited in the
bibliography.
–  As far as I know has not been published in full.
–  The paradox occurs between plant and herbivore trophic
levels because plant investment in chemical defense
leads to a counterintuitive decrease in fitness.
–  The paradox is resolved by natural enemies in the third
trophic level.
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 7: Tritrophic Interactions
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6. Sublethal digestibility reducers:
•  It is paradoxical for a plant to invest in more
chemical defense when this makes the plant less fit
because herbivores have to eat more of the less
digestible diet to assimilate sufficient food to grow.
•  I call this the “sublethal” plant defense paradox
because of the paper by Clancy and Price in 1987
that was titled:
–  “Rapid herbivore growth enhances enemy attack:
sublethal plant defenses remain a paradox.” Ecology
68(3): 733-737.
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 7: Tritrophic Interactions
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7. Clancy and Price (1987):
•  Clancy and Price tested
resolution of the paradox by
natural enemies in a willow
gall system in which
ectoparasitoids attack sawfly
larvae inside their galls.
•  They found that parasitoids
were more likely to attack
sawflies in faster developing
galls (Fig. 2) contrary to the
expected result of higher
parasitism in slower
developing galls.
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 7: Tritrophic Interactions
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8. Larger galls were selected by
ectoparasitoids:
•  Figure 3:
Frequency distributions
of gall diameters for
penultimate and
ultimate instar larvae
and percentage galls
attacked in each size
category
(Clancy & Price, 1987).
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 7: Tritrophic Interactions
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9. Interpretation of Clancy & Price:
•  I think they have
misinterpreted
their data because
they show in their
Fig 1. that sawfly
larvae develop
faster in faster
growing galls and
that larger galls
grow faster.
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 7: Tritrophic Interactions
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10. Clancy & Price not inconsistent with paradox
resolution by natural enemies?:
•  Therefore faster growing larvae more vulnerable to
parasitism because they are in faster growing galls:
–  These galls are also larger and more obvious signals for
parasitoids.
•  So their results remain consistent with natural enemy
resolution of the “sublethal” plant defense paradox
because larger galls are more apparent to natural
enemies.
–  Large galls also represent similar increase in tissue
investment (cost) that is balanced by natural enemy attack
(benefits) much like the soybean tannins, bean beetles, and
predatory bugs investigated by Bouton et al.
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 7: Tritrophic Interactions
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11. The “lethal” plant defense paradox
•  Sublethal paradox operates between plant and
herbivore trophic levels and is resolved by natural
enemies at the third trophic level.
•  Lethal plant defense paradox occurs between
herbivore and natural enemy trophic levels
(Figure).
•  It is not known whether this paradox can be
resolved.
–  We hypothesize that it is resolved by reduction of
investment in chemical defenses to make herbivores
more vulnerable to natural enemies.
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 7: Tritrophic Interactions
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12. Sequestration of plant defenses:
•  The lethal defense paradox occurs because
most insect species are specialists:
–  Bernays & Graham. 1988. Ecology 69(4): 886-892.
•  It is also common for many of these
specialists to use host plant chemical
defenses for their own defenses against
natural enemies.
•  Thus increased investment in plant defense
can lead to enhanced herbivore fitness.
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 7: Tritrophic Interactions
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13. Reason for calling it the lethal plant
defense paradox:
•  I call the paradox, the “lethal” plant defense
paradox because the sequestered chemical
defenses always appear to be “toxins” or
“qualitative defenses” in the sense of
Rhoades and Cates and Feeny and these
are thought to be lethal or acute rather than
sublethal or chronic defenses.
•  This ‘title’ also reflects the influence of
Clancy and Price!
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 7: Tritrophic Interactions
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14. Plant signals:
•  “Talking plants” and plant volatiles:
–  Dicke, Marcel, Jan Bruin & Maurice W. Sabelis. 1993.
Herbivore-induced plant volatiles mediate plant-carnivore,
plant herbivore, and plant-plant interactions: Talking
plants revisited. Pages 182-196, in, J. Schultz and I.
Raskin (eds.) Plant Signals in Interactions with Other
Organisms. American Society of Plant Physiologists.
•  Good experimental evidence for “green leaf
volatiles” that plants emit when damaged by
herbivores.
•  Volatiles then attract, or signal, natural enemies of the
herbivores and benefit the plant.
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 7: Tritrophic Interactions
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15. Plant signals that attract natural enemies of
herbivores: the case of beans and mites:
Lima bean two-spotted
spider mite predatory mite
system
(Phaseolus
lunatus Tetranychus
urticae Phytoseiulus
persimilis)
(Figure 1,
Dicke et al.
1993).
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 7: Tritrophic Interactions
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16. Induction of signals:
•  As indicated in Figure 1 the system is even
more complex in that released volatiles also
repel subsequent herbivore attack and even
induce greater attractiveness in adjacent
plants for predatory mites and reduced
attractiveness for herbivorous mites.
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 7: Tritrophic Interactions
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17. Green leaf volatiles: Experimental protocol:
Dicke, M., P. Van Baarlen, R. Wessels & H. Dijkman. 1993. Herbivory induces systemic production of plant
volatiles that attract predators of the herbivore: extraction of endogenous elicitor. J. Chem. Ecol. 19(3): 581-599.
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 7: Tritrophic Interactions
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18. Green leaf volatiles: Experimental results:
•  Number of predators that
choose among
treatments A, B, C or D.
•  Predators choose air
from either leaves
infested with mites (A) or
leaves kept in water (C)
from (A).
•  Thus water contains a
plant-derived elicitor.
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 7: Tritrophic Interactions
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19. The ecological dynamics and evolutionary potential of
interactions among three trophic levels: From: Malcolm (1992)
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 7: Tritrophic Interactions
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Natural enemies of Aphis nerii:
Included
Slide 20
Peripheral
Excluded