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BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 7: Tritrophic Interactions Slide - 1

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.


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.


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.


4. The two paradoxes operate at different trophic levels:

From: Malcolm (1995)


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 Syst. 11: 41-65) described an unpublished experiment by Bouton, Price and Kogan (Table 1): –  It was not published in Am.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.


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.


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.


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).


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.


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.


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.


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.


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!


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.


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).


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.


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.


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.


19. The ecological dynamics and evolutionary potential of interactions among three trophic levels: From: Malcolm (1992)

Natural enemies of Aphis nerii: Included Peripheral Excluded

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