BIOS 5970: PLANT-HERBIVORE
INTERACTIONS
•  B. PLANT DEFENSES AND HERBIVORE FEEDING
•  Week 2.
•
1. The world is green:
•  Darwin “noted that sheep of different breeds have
different susceptibilities to plant poisons.”
•  “It is no surprise to an evolutionary ecologist that insects
quickly evolve resistance to insecticides. Long
evolutionary history has given insects the ability to
detoxify a myriad of natural plant poisons, and the
potential to evolve resistance to artificial toxins similar to
those with which they can naturally cope.”
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm --- Week 2: Plant defenses and herbivore feeding
Slide 1
2. Evolutionary trade-offs:
•  Trade-off between defense and growth
•
For example:
•  Allele differences at two loci determine whether
clover (Trifolium repens) is cyanogenic and produces
cyanide.
•  Cyanogenic plants grow more slowly than
acyanogenic plants
•  But this cost is more than compensated for by
effective defense against insect and snail herbivores.
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm --- Week 2: Plant defenses and herbivore feeding
Slide 2
3a. Testing hypotheses to explain
observations (patterns to processes):
•  Initial observation:
•
Woodland ants carry seeds of violets (Fig. 1.1)
and Dutchman's breeches (Fig. 2.1) - why?
•  a) Comparative method:
•
•
•
Ants take seeds to nests (some eaten, some
survive).
Dicentra has seeds with nutrient-rich
elaiosomes.
Inconclusive.
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm --- Week 2: Plant defenses and herbivore feeding
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3b. Testing hypotheses to explain
observations (patterns to processes):
•  b) Observation >> hypotheses:
•
Initial observations plus library research
suggested 3 alternative hypotheses:
•  (i) Ants are seed predators.
•  (ii) Ants remove seeds for nutrient-rich elaiosomes
but are not effective dispersal agents.
•  (iii) Ants disperse seeds.
•  Then see that ants keep Dicentra seeds in caches inside
their nests.
•  Seeds in ant nests are intact with elaiosomes chewed off.
•  However, ants abandon nests frequently.
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm --- Week 2: Plant defenses and herbivore feeding
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3c. Testing hypotheses to explain
observations (patterns to processes):
•  c) Experimental method:
•
Test whether seed survivorship (per capita) is
higher for seeds taken by ants than seeds left
alone.
•  Need replicated and controlled experiments.
•
Thus a combination of observational,
comparative, and experimental evidence is most
valuable to answer the original question.
•  see Table 2-1 for the results of an experiment in
which ants enhance seed survivorship during
germination.
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm --- Week 2: Plant defenses and herbivore feeding
Slide 5
4. Why is the Earth so green?
•  Bottom-up (plant defense) versus topdown control (natural enemies).
•  Adaptation and counteradaptation:
•
•
Plants use a variety of devices to protect roots,
stems, leaves, and seeds (flowers?).
For example:
•  Cellulose roughage slows digestion.
•  Exotic amino acids interfere with protein formation.
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm --- Week 2: Plant defenses and herbivore feeding
Slide 6
5. Herbivore counteradaptation to
plant defenses:
•  Herbivores counter-defend with ploys such
as:
•
Behavioral avoidance.
•
Digestive chemicals that dismantle lethal plant
molecules.
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm --- Week 2: Plant defenses and herbivore feeding
Slide 7
6. Tactics versus strategies:
•  Tactics can respond to particular
interactions within strategic, evolutionary,
phenotypic constraints.
•  Strategies determine the operation range of
various tactics.
•
Thus specialization is a feeding strategy, but
alkaloid detoxification is a tactic.
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm --- Week 2: Plant defenses and herbivore feeding
Slide 8
7. Herbivory:
•  Herbivory is not simply
the consumption of plants
by animals, it is a process
that describes the
interaction between plant
defense and herbivore
foraging (Fig.20.1 from
Malcolm, 1992).
•  450 million years of
evolution has produced
huge diversity in both
plants and herbivores.
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm --- Week 2: Plant defenses and herbivore feeding
Slide 9
8. Interactions among 3 trophic levels:
•  Tritrophic interactions:
•
Like herbivory,
predation is a process
that describes the
interaction between
defense and foraging
(Fig. 20.1: Malcolm,
1992)
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm --- Week 2: Plant defenses and herbivore feeding
Slide 10
9a. Plant defenses:
•  (1) Mechanical protection on the plant surface:
•  Includes spines, trichomes, glandular hairs (Fig. 3.2).
•  (2) Complex polymers or silica crystals to
reduce plant digestibility:
•  Digestibility Reducers (Table 3-1):
•  Dose-dependent or quantitative, because the more that are
present the less nutritional resource a herbivore receives.
•  Includes cellulose, hemicellulose, and pectin as complex
polysaccharides (Fig. 3-3) that can be 80-90% of plant dry
weight.
•  As well as lignins, tannins and silica.
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm --- Week 2: Plant defenses and herbivore feeding
Slide 11
9b. Plant defenses:
•  Omnivores & carnivores cannot digest nutrients in the
presence of digestibility reducers.
•  So many herbivores require symbiotic microbes
associated with digestive modifications.
•
•
Also lignins (complex phenolic polymers) bind to
polysaccharides; waxes or cutins and tannins (also
polyphenols but not bound to polysaccharides).
Condensed tannins bind to protein and reduce digestion by:
•  (i) Blocking the action of digestive enzymes, or,
•  (ii) Binding to proteins being digested, or
•  (iii) Interfering with protein activity in the gut wall.
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm --- Week 2: Plant defenses and herbivore feeding
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9c. Plant defenses:
•  (3) Toxins that kill or repel herbivores at low
concentrations:
•
Secondary compounds with a defensive rather than a
metabolic function
•  Secondary metabolites or allelochemicals (see Fig. 3-4 for
metabolic sources).
•  Qualitative toxins are poisonous and are very diverse (Table 3-1
and Fig. 3-5).
•  Include alkaloids, terpenoids and HCN
(Fig. 3-6 common in almonds and cherries etc.) which blocks
cytochrome oxidase and hence cellular respiration.
•  See Table 9-2 for evolution of toxic chemicals in plants.
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm --- Week 2: Plant defenses and herbivore feeding
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10. Constitutive versus Inducible defenses
•  Constitutive:
•
Permanent protection always present:
•  e.g. spines and trichomes as well as many chemicals that
reduce digestibility and also function as structural support.
•  They could also include some toxins.
•  Inducible:
•
Responses by individual plants to tissue damage:
•  e.g. very widespread proteinase inhibitors:
•  Polypeptides and proteins that block catalytic activity of proteolytic
enzymes by binding to the active site of the enzyme molecule.
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm --- Week 2: Plant defenses and herbivore feeding
Slide 14
11. Herbivore Foraging:
•  Scale: size range from aphids to elephants!
•  Dan Janzen: “the plant world is not colored green;
it is colored morphine, caffeine, tannin, phenol,
terpene, canavanine, latex, phytohemagglutinin,
oxalic acid, saponin, and L-dopa.”
•
•
•
Sensory modality for signal reception.
“Why do different herbivores eat different
plants?” (page 40).
Herbivores have mechanical, biochemical,
physiological, and behavioral countermeasures to plant
defenses (Table 3-2).
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm --- Week 2: Plant defenses and herbivore feeding
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12. Mechanical breakdown of plant food
•  To break open cells:
•
Mammals use teeth:
•  low-crowned and high-crowned (Figs. 3-8 & 9-8).
•
Birds use beaks (cardinal) or gravel-filled
gizzards (turkey, dodo).
•
Insects use chewing or sucking mouthparts
(Fig. 3-9).
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm --- Week 2: Plant defenses and herbivore feeding
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13. Microbial symbionts
•
•
Many herbivores have bacteria, flagellates and
protozoans that can synthesize necessary
vitamins, break down plant material, and
detoxify allelochemicals through anaerobic
fermentation.
Structural modifications to the gut:
•  Foregut (sheep) and hindgut (horse) fermentors
(Table 3-3).
•  Ruminants (Fig 3-10):
•  4-chambered stomach: rumen (+reticulum), omasum, and
abomasum.
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm --- Week 2: Plant defenses and herbivore feeding
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14. Herbivore gut ecosystems:
•
1 ml of sheep rumen fluid includes:
•  16,100 x 106 bacteria, 106 flagellates and 3.3 x 105
ciliated protozoans.
•
•
Whole sheep rumen holds 6L !
Digestion efficiency (Table 3-4):
•  Depends on volume, retention time and proportion of indigestible
material in plant food.
•  Larger herbivores (bison at 450-1,350 kg take 80 hours to
process fiber at about 70% efficiency) hold food longer than
smaller herbivores.
•  White-tailed deer at 48-100 kg take 45 hours to process food at
56% efficiency.
•  Humans at 60 kg digest only 9% of alfalfa fiber eaten.
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm --- Week 2: Plant defenses and herbivore feeding
Slide 18
15. Figure 3-12: Digestibilities of different
forages to mule deer.
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm --- Week 2: Plant defenses and herbivore feeding
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16. Insect herbivores:
•  Cannot use large gut volumes and high retention
times, so they specialize more and have a variety
of ways to use symbiotic microbes (Table 3-5).
•  Insects often have:
•
•
•
Long guts or elaborate cecae (Fig. 3-13), or,
Intracellular symbionts in mycetocytes together as
mycetomes (Fig. 3-14), or,
Fungal symbionts that are cultivated outside their bodies
(like leaf cutter ants and bark beetles).
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm --- Week 2: Plant defenses and herbivore feeding
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17. Digestive enzymes:
•  Both general and specific enzyme systems
are used.
•  The best known are:
•
Mixed-function oxidases (MFOs).
•  These are membrane-bound enzymes that detoxify a
wide range of poisons.
•  Vertebrates:
•  Highest activity in the microsomes of the endoplasmic
reticulum of liver cells.
•  Insects:
•  Mostly in fat bodies or midgut.
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm --- Week 2: Plant defenses and herbivore feeding
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18. Characteristics of MFO systems:
•  (1) Catalyze oxidative reactions.
•  (2) Nonspecific.
•  (3) Easily induced by exposure to novel toxins.
•
They detoxify (Fig. 3-15) by:
•  (1) Primary degradation to make water soluble
•  e.g. adding hydroxyl (-OH) groups)
•  (2) Conjugation with sugars, amino acids, sulfates, phosphates, or
other molecules headed for excretion.
•
•
This makes toxins soluble and excretable.
There is generally more MFO activity in insects with
broader diets than those with narrower diets and
generalists are better adapted for degrading novel toxins.
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm --- Week 2: Plant defenses and herbivore feeding
Slide 22
19. Choice and Avoidance:
•  Diet breadth spectrum:
•
•
•
Polyphagous - many food species
Oligophagous - few food species
Monophagous - single food species
•  Variable diet breadth poses different sets of
problems:
•
•
Most mammals have to be polyphagous, or at
least oligophagous, because they are large.
But most insects are small and less mobile and
need to be oligophagous or monophagous.
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm --- Week 2: Plant defenses and herbivore feeding
Slide 23
Figure 1.1: Formica podzolica ant
holding violet seed by its elaiosome
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm --- Week 2: Plant defenses and herbivore feeding
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Figure 2.1: Flowers of Dutchman’s breeches
(Dicentra cucullaria) and seed with elaiosome
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm --- Week 2: Plant defenses and herbivore feeding
Slide 25
Table 2.1: Seedling emergence of
violets in different treatments
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm --- Week 2: Plant defenses and herbivore feeding
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Figure 3.2:
External protection of
plants: (a) cactus
spines; (b) hooked bean
trichomes; (c) potato
glandular hairs
c
a
b
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm --- Week 2: Plant defenses and herbivore feeding
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Table 3.1:
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm --- Week 2: Plant defenses and herbivore feeding
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Figure 3.3:
Digestibility
reducers in
plants.
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm --- Week 2: Plant defenses and herbivore feeding
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Figure 3.4: Biosynthetic origins of
primary and secondary plant products
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm --- Week 2: Plant defenses and herbivore feeding
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Figure 3.5:
Some toxic secondary
compounds in plants:
caffeine from coffee beans
(Coffea),
strychnine from Strychnos fruits,
and the terpenes, pyrethrin from
Chrysanthemum and glaucolide A
from a sunflower.
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm --- Week 2: Plant defenses and herbivore feeding
Slide 31
Figure 3.6: Cyanide production by
damaged cherry leaves (Prunus).
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm --- Week 2: Plant defenses and herbivore feeding
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Table 9.2:
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm --- Week 2: Plant defenses and herbivore feeding
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Table 3.2:
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm --- Week 2: Plant defenses and herbivore feeding
Slide 34
Figure 3.8: Low crowned tooth of omnivorous browsing
mammal and high-crowned tooth of grazing mammal
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm --- Week 2: Plant defenses and herbivore feeding
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Figure 9.8: Diversity of grazing and browsing
Miocene horse genera of North America.
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm --- Week 2: Plant defenses and herbivore feeding
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Figure 3.9: Insect mouthparts (a) chewing
grasshopper, (b) seed-sucking milkweed bug.
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm --- Week 2: Plant defenses and herbivore feeding
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Table 3.3:
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm --- Week 2: Plant defenses and herbivore feeding
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Figure 3.10: Mammalian digestive tracts:
fore & hind-gut fermentors and a carnivore
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm --- Week 2: Plant defenses and herbivore feeding
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Table 3.4:
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm --- Week 2: Plant defenses and herbivore feeding
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Table 3.5:
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm --- Week 2: Plant defenses and herbivore feeding
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Figure 3.13: Grasshopper gut with expanded
volumes and ceca for microflora
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm --- Week 2: Plant defenses and herbivore feeding
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Figure 3.14: Mycetocytes in the
midgut of a chrysomelid beetle
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm --- Week 2: Plant defenses and herbivore feeding
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Figure 3.15: Mixed function oxidase (MFO) degradations of
toxins: (a) hydrolysis of DDT, (b) N-oxidation of nicotine.
BIOS 5970: Plant-Herbivore Interactions - Dr. S. Malcolm --- Week 2: Plant defenses and herbivore feeding
Slide 44