BIOS 5970: Plant-Herbivore Interactions • Week 4. Plant defense theory 1: history:

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BIOS 5970: Plant-Herbivore Interactions

Dr. Stephen Malcolm, Department of Biological Sciences

Week 4. Plant defense theory 1: history:

–   Lecture summary:

•   The world is green - why?

•   Explanatory theories:

–   Classical plant defense theory :

»   Dethier (1954); Fraenkel (1959); Ehrlich & Raven (1964).

–   Apparency theory :

»   Feeny (1976).

–   Optimal defense theory :

»   Rhoades & Cates (1976).

–   Feeding specialization hypothesis :

»   Futuyma (1976).

BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 4: Plant defense theory 1: history Slide - 1

2. Cost of herbivore feeding:

Herbivores have a negative impact on plant fitness

(Figure 4-2).

But the world is still green!

–   “ Somehow, millions of herbs, shrubs, and trees outgrow, outlast, or outdefend their herbivore enemies. One of the principal challenges of modern ecology is to understand how plants escape from herbivores in time and space.

–   “ Plant defense theories provide the organizing principles.

BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 4: Plant defense theory 1: history Slide - 2

3. Basic Plant Defense Theories:

•   “ The ease with which plants are located by herbivores provides one theoretical perspective ”

–   Apparency theory .

•   “ the ease with which plants mobilize resources to defend themselves provides another ”

–   Resource availability theory .

•   “ Both are grounded in the idea that plants evolve defensive capabilities, that are countered by adaptive evolution of animals that eat them ”

–   Classical theory .

BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 4: Plant defense theory 1: history Slide - 3

4. Classical Plant Defense Theory:

•   Dethier (1954) and Fraenkel (1959):

–   Different insect species react differently to different plants with different secondary chemistry.

•   Dethier and then Ehrlich & Raven (1964) first developed the “ classical theory of biochemical coevolution ” between plants and insects:

–   In adapting to evolved plant defenses, insect herbivores lose some ability to detoxify allelochemicals of unrelated plants and so their diet breadth is narrowed.

BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 4: Plant defense theory 1: history Slide - 4

5. Classical Plant Defense Theory:

•   “ The classical theory predicts that related taxa of insects become locked into a chemical arms race with related taxa of plants.

•   “ Why do animals eat some plants, and not others?

–   E.g.

Berenbaum's coumarins.

•   Tables 7.1

& 7.2, Figs. 7.1

& 7.2.

–   From Strong, Lawton & Southwood. 1984. Insects on Plants.

Community Patterns and Mechanisms.

Oxford: Blackwell.

Slide - 5 BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 4: Plant defense theory 1: history

6. Apparency & Optimal Defense Theory:

Feeny (1976), Rhoades & Cates (1976):

–   Plants that are easily found ( “ apparent ” ) by herbivores evolve different kinds of chemical defenses from those that are difficult for animals to locate ( “ unapparent ” ).

–   The distribution of qualitative ( toxic ) defenses and quantitative ( digestibility reducing ) defenses varies according to plant

“ apparency ” (Table 4-1, summary).

Slide - 6 BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 4: Plant defense theory 1: history

7. Apparency Theory and temporal variation:

•   Timing and synchrony are important (Fig. 4-3):

–   So life history timing could also be an effective defense:

•   E.g.

the November timing of oviposition by female winter moths and flight by males.

–   Because leaves of apparent plants change in digestibility with time, e.g.:

•   Increasing tannins and decreasing protein (Fig. 4-4).

•   Decrease in grass digestibility with age (Fig. 4-7).

•   Decrease in cherry and sorghum leaf nitrogen with age (Fig. 4.8) - grasses are apparent to grazers!

BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 4: Plant defense theory 1: history Slide - 7

8. Unapparent plants:

•   Specialists ( Pieris rapae ) on crucifers ( Brassica ) are much more affected by nutritional content

(nitrogen) than defensive chemical content

(glucosinolates such as sinigrin) - Fig. 4-5.

•   But these plants avoid specialists by being hard to find and avoid generalists by having toxic chemical defenses.

•   Is this logically inconsistent?

–   cabbage to oak?

–   aphid to elephant?

BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 4: Plant defense theory 1: history Slide - 8

9. Explanatory power of Apparency Theory:

Can apparency theory explain all observable patterns?

–   Patterns of chemical defense distribution (after

Futuyma, 1976) may be explained partially by variations in plant modularity (Table 4-2):

•   More ephemeral tissues may have defenses characteristic of unapparent plants and less ephemeral tissues may have defenses like those in apparent plants.

•   Alternatively, tissue age may be a better predictor of defense type.

BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 4: Plant defense theory 1: history Slide - 9

10. Field test of Apparency Theory:

•   Apparency theory partially held up for a test using persistent and pioneer tree species on Barro

Colorado Island in Panama:

–   Tables 4-3 and 4-4 after Coley (1983).

•   Mature leaves of persistents were grazed less

(0.04%/day) than those of pioneers (0.24%/day).

•   Exception:

–   Tannins were more prevalent in young trees for both pioneers and persistents.

Slide - 10 BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 4: Plant defense theory 1: history

11. Chemical response by plants to herbivory:

(1) Induction of chemical defenses:

–   Wound-induced defenses in birch trees ( Betula spp.) reduced fitness of the geometrid moth

Epirrita autumnata perhaps through increased phenolic content (Fig. 4-9).

(2) Reproductive compensation:

–   There is some evidence that plants can compensate for herbivory (see Fig. 8.3

of

Hendrix data from Begon et al.

1990)

Slide - 11 BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 4: Plant defense theory 1: history

12. Targets for plant defense:

•   It is important to bear in mind the relevant target or organism that a plant must aim at to defend itself.

–   For example, in the leaf cutter example the plant may have to target both the ant and its symbiotic fungus.

•   Thus plants can produce effective fungicides to kill the "microbial farm" of the ants.

•   But phenolics are useless against the ants because the fungus detoxifies them.

•   Thus receptor sites are almost certainly crucial to understanding plant herbivore interactions.

•   What do the plants target and why?

Slide - 12 BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 4: Plant defense theory 1: history

13. Feeding Specialization Hypothesis:

Futuyma (1976):

More specialist herbivore species on unapparent plants than on apparent plants:

–   More butterfly species on unapparent herbs, but more moth species on apparent plants:

•   Table 4-5 and Tables 1, 2 & 3 from Futuyma

(1976).

Slide - 13 BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 4: Plant defense theory 1: history

14. Test of the Feeding Specialization Hypothesis:

Mark Scriber tested to see whether specialists use their host plant leaves as food more effectively than generalists for swallowtail butterflies in the genus Papilio .

–   P. troilus :

•   spicebush swallowtail eats only spicebush ( Lindera ) and sassafras ( Sassafras ).

–   P. glaucus :

•   tiger swallowtail eats 20 food plant species.

Slide - 14 BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 4: Plant defense theory 1: history

15. Scriber ’ s results:

•   Spicebush vs tiger swallowtails:

–   Eat 163 vs 54 mg/day/g of Lindera leaves

–   At an efficiency of 21% vs 12%,

–   To produce a relative growth rate of 33 vs 6 mg/day/g.

•   Within a species, patterns of feeding specialization can be important and may lead to evolution of new species (Fig. 4-12).

•   P. glaucus canadensis is probably a different species.

•   Thus regional and local host specialization may be common.

Slide - 15 BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 4: Plant defense theory 1: history

Figure 4-2: Effects of leaf removal on seed production after

1 year (left) and 2 years (right) in Piper arieianum shrubs.

BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 4: Plant defense theory 1: history Slide - 16

Table 7.1:

From, Strong,

Lawton &

Southwood,

1984.

BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 4: Plant defense theory 1: history Slide - 17

Table 7.2: From, Strong, Lawton &

Southwood, 1984.

BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 4: Plant defense theory 1: history Slide - 18

Figure 7.1:

Number of plant species per genus in genera of Apiaceae with different chemistries.

More spp. in genera with angular and linear furanocoumarins

(Strong, Lawton &

Southwood, 1984: after Berenbaum,

1983).

BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 4: Plant defense theory 1: history Slide - 19

Figure 7.2:

Number of

Lepidopteran spp. associated with

Apiaceae that vary chemically

(Strong, Lawton &

Southwood, 1984: after

Berenbaum, 1983).

BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 4: Plant defense theory 1: history Slide - 20

BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 4: Plant defense theory 1: history Slide - 21

Figure 4-3:

Effects of oak bud burst timing (broken line) on synchrony with winter moth egg hatch and consequent larval mortality (stippling).

BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 4: Plant defense theory 1: history Slide - 22

Figure 4-4: Winter moth larval

size influenced by leaf age.

BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 4: Plant defense theory 1: history Slide - 23

Figure 4-7: Grass growth curve and changing

proportion digestible to herbivores.

BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 4: Plant defense theory 1: history Slide - 24

Figure 4-8: Seasonal changes in nutrient and cyanide content in black cherry and sorghum.

BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 4: Plant defense theory 1: history Slide - 25

Figure 4-5:

Increase in larval feeding efficiency of the butterfly Pieris rapae with increased dietary nitrogen.

BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 4: Plant defense theory 1: history Slide - 26

Table 4-2:

BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 4: Plant defense theory 1: history Slide - 27

Table 4-3:

BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 4: Plant defense theory 1: history Slide - 28

Table 4-4:

BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 4: Plant defense theory 1: history Slide - 29

Figure 4-9: Reduced growth survival and fecundity of larvae of the moth Epirrita autumnata fed leaves of birch trees that were damaged or had larval frass added.

BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 4: Plant defense theory 1: history Slide - 30

Figure 8.3: Compensation via reduced death rate in control and damaged flowers of wild parsnip, Pastinaca sativa (Begon, Harper & Townsend, 1990, 2nd ed.).

BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 4: Plant defense theory 1: history Slide - 31

Table 4-5:

BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 4: Plant defense theory 1: history Slide - 32

Table 1:

From, Futuyma (1976)

BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 4: Plant defense theory 1: history Slide - 33

Table 2: Futuyma (1976)

BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 4: Plant defense theory 1: history Slide - 34

Table 3: Futuyma (1976)

BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 4: Plant defense theory 1: history Slide - 35

Figure 4-12: Geographical ranges of two races of

the tiger swallowtail, Papilio glaucus.

BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm. Week 4: Plant defense theory 1: history Slide - 36

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