Herbivory

1
Herbivory

• Impact of herbivores
• Plant responses
• Defense, including types and models
• Tolerance and overcompensation
• Plant signaling
• Third party defenses

2
What is the impact of herbivores on plants?
Impact

• Direct effects removal of leaves, sap, roots
  decreases photosynthetic capacity, changes growth
  form, reduces survival and reproduction.

3
Direct effects of herbivory
Impact

• Datura wrightii exposed to and protected from
  herbivores

Elle et al. 1999. Evolution 53 22-35
4
Direct effects of herbivory
Impact

• Effect of herbivory depends on
• Timing of feeding
• Age of tissue attacked
• Plant parts attacked
• Type of attack
• What plant parts/ages are most valuable?

5
What is the impact of herbivores on plants?
Impact

• Indirect effects increased disease
  transmission, reduced pollination success,
  increased expression of inbreeding depression

6
Sucking insect, flower size, inbreeding
Impact

• Flower size smaller in plants attacked by
  spittlebugs
• Selfing rate higher
• Mimulus guttatus has high inbreeding depression
  with selfing

IveyCarr 2005. AJB 92 1641-1649
7
Leaf herbivory and mating system
Impact

• More cleistogamous flowers (selfing) with more
  damage in Impatiens

Steets Ashman 2004. AJB 91 1046-1051
8
Plant Resistance Strategies
Escape
Avoidance Strategies
Defense
Resistance
Tolerance Strategies
Rosenthal and Kotanen 1994, TREE 9145-148
9
Plant Resistance

• Defense traits that reduce the amount of damage
  experienced
• Compensation/Tolerance the ability to maintain
  growth or fitness after experiencing damage
• Overcompensation higher fitness in damaged
  relative to undamaged plants

10
Defense
Defense

• Constitutive always present
• Induced turned on by damage

Induced
Constitutive
Proportion reliance on defenses
Probability of attack
Zangerl and Bazzaz 1992
11
Damage in Parsnips
Defense
Zangerl and Rutledge 1996. Am. Nat. 147599-608
12
and induction of xanthotoxin
Defense
13
Physical defenses
Defense

• silica, lignins, thorns, trichomes
• Latex and resins are physical and chemical

14
Chemical Defenses
Defense

• Usually secondary metabolites, e.g. not
  directly involved in primary metabolism
• Many compounds are used by humans
• Broadly, include toxins (qualitative defense) and
  quantitative defenses

15
Chemical defenses
Defense

• Nitrogen based defenses
• Often toxic in small quantities some are
  anti-feedants
• Alkaloids interfere with nervous system
  (nicotine, caffeine, atropine, morphine, cocaine,
  mescaline)
• Cyanogenic glycosides (cyanide!) also N-based

16
Chemical defenses
Defense

• Phenolics (Carbon based)
• Can be toxic, but also include digestibility
  reducers
• Tannins (in wine, oak leaves, used to tan
  leather) bind digestive enzymes (e.g. trypsin)
• Other Flavonoids are pigments, or used by us to
  fight cancer

17
Chemical defenses
Defense

• Terpenes (Carbon based)
• Lots of activities toxins, antifeedants, or
  just gummy
• Lots of smelly compounds eucalyptus oil,
  peppermint oil, camphor, turpentine
• Gummy compounds like latex
• Terpenes also components of pheromones, some act
  as defenses by interfering hormonally with
  growth, reproduction of insects

18
Are defenses costly?
Defense

• Models for their evolution assume so
• To demonstrate
• Must be quantified in absence of herbivores (e.g.
  no benefit of trait)
• Must control genetic background, environment,
  etc.

19
Examples of costs
Defense

• Berenbaum et al. 1986. Evolution 401215-1228
• Pastinaca sativa, wild parsnip
• Umbel production negatively correlated with
  furanocoumarins

20
Examples of costs
Defense

• Baldwin et al. 1990. Ecology 71252-262
• Nicotiana sylvestris, flowering tobacco
• Seed production negatively correlated with
  alkaloids

21
Examples of costs
Defense

• Elle et al. 1999. Evolution 5322-35
• Datura wrightii, sacred jimsonweed
• Glandular-trichome plants 45 fewer viable seeds
  than non-glandular

22
Costs of Resistance in Datura wrightii
Defense
Elle et al.1999. Evolution 53 22-35
23
Models of defense
Defense models

• Optimal defense theory
• Resource availability hypothesis
• Growth-differentiation balance hypothesis

24
Optimal defense model
Defense models

• Rhoades and Cates, Feeney, both 1976
• Tissues protected in proportion to value,
  probability of damage
• Unapparent species/individuals will have few
  defenses, and if present, toxins
• Apparent species/individuals will have
  generalized quantitative defenses

25
Optimal defense model
Defense models
Digestibility reducers quantitative
Effectiveness or cost of defense
No defense (escape)
Toxins qualitative
Tissue predictability ( apparency, or risk of
attack, or value of tissue)
26
Optimal defense example
Defense models

• Bracken fern (Pteridium aquilinum) change in
  defense strategy over time

27
Resource Availability Hypothesis
Defense models

• Also called the carbonnutrient balance
  hypothesis
• Bryant et al. 1983, Coley et al. 1985
• Species have inherent growth rates
• Nutrient availability/limiting factors determine
  type, quantity of defense

28
RAH the model for defense quantity
Defense models
29
RAH predictions of defense types
Defense models

• If soil nutrients more limiting than carbon
  (light), growth more limited than photosynthesis
  expect C-based defense
• In nutrient rich sites, or in shade,
  photosynthesis is limiting expect N-based
  defenses or plants outgrow damage

30
Evidence for RAH quantity(multiple tree species)
Defense models
Defense
Defense combination of fibre, tannin,
toughness, pubescence Herbivory leaf
damage/day
31
Evidence for RAH defense type
Defense models

• C-based defense decreases with N addition in
  Douglas fir
• Interpretation more N, photosynthetic rate
  becomes limiting less C available for defense

32
Growth-differentiation balance hypothesis
Defense models

• Herms and Mattson 1992
• Physiological trade-off between growth and
  differentiation at the cellular level
• Allocation to defense only when not growing
  maximally

33
GDBH
Defense models

• Low to moderate resource availability, rates of
  assimilation, growth, 2 metabolism positively
  correlated
• Moderate to high levels of resources, net
  assimilation constant, plant growth and 2
  metabolism negatively correlated

34
Growth-differentiation balance hypothesis
Defense models
Net assimilation
Relative growth rate
Metabolism
Secondary metabolism
Resource availability
Blue line red line black line
35
GDBH
Defense models

• In rich habitats expect high growth low defense
  allocation or outgrow damage
• In poor habitats expect small amount of
  constitutive defenses
• Intermediate habitats highest defense levels

36
GDBH evidence
Defense models

• Lower defense in rapidly growing apical meristems
  in brown alga

Oecologia 105361-368
37
Problem 8

• Do the results in the figure support or
  contradict the GDBH, and why?
• Bars plant mass
• Symbols trichomes

Oecologia 106181-191
38
Other potential plant responses
Tolerance/Overcompensation

• Compensation or tolerance
• Herbivory may release plants from apical
  dominance
• Plants may re-allocate resources after attack to
  most important structures fruits
• To demonstrate must examine plants after
  attack, compare fitness to plants with no attack

39
Tolerance in Radish
Tolerance/Overcompensation
Agrawal et al 1999 Evolution 531093-1104
40
Tolerance in invasive Senecio
Tolerance/Overcompensation
From Stastny, Schaffner, and Elle 2005. J.
Ecology 9327-37
41
Other potential plant responses
Tolerance/Overcompensation

• Overcompensation
• Can plants actually have higher fitness after
  attack?
• Mixed results!

42
Overcompensation
Tolerance/Overcompensation

• Ipomopsis aggregata browsed by elk occasionally
  have higher seed production than plants not
  browsed
• Evolution of response depends on predictability
  of damage at particular phenological stage

Paige and Whitham 1987 Am Nat 129407-416
43
Overcompensation
Tolerance/Overcompensation

• Herbivory increases male fitness in radish
  (damaged plants have more flowers)

Strauss et al 2001 Am Nat 158496-504
44
Tolerance and Overcompensation in field gentians
Tolerance/Overcompensation
Lennartson et al. 1998. Ecology 791061-1073
45
Chemical defenses can be unexpected
Signals

• Talking trees sometimes plants nearby damaged
  individuals will induce defenses, even when
  undamaged
• Damaged plants produce chemical signals that
  neighboring plants respond to

46
Talking Trees
Signals
47
Talking Trees
Signals
Coeff. of determin. r2 of leaf damage vs.
distance
Dolch and Tscharntke. 2000. Oecologia
125(4)504-511
48
Signals
Talking Trees
Dolch and Tscharntke. 2000. Oecologia
125(4)504-511
49
Other Talking Plants
Signals

• Flowering tobacco up-regulates defense chemical
  production when neighboring sagebrush is clipped

PPO polyphenol oxidase, a chemical
defense Baldwin et al. 2000. Oecologia 12566-71
50
Other Talking Plants
Signals

• Flowering tobacco damaged less when growing near
  clipped sagebrush

51
Other Talking Plants
Signals

• Signal released by sagebrush is Methyl jasmonate,
  a volatile cue that elicits a response in
  chemical defense pathways

52
Other things to talk to
Signals

• Some plant volatiles are recognized as signals by
  predators/parasitoids
• Wasps orient to volatiles emitted after damage

Thaler 1999. Nature 399686-688
53
Third-party defenses
Third-party defenses

• Ants commonly defend plants against herbivores
• Plant provides a home (acacias) or a snack (93
  of plant families have extrafloral nectaries,
  less common is production of food bodies)

54
Extrafloral nectaries importance
Third-party defenses

• Bush morning glory, Ipomoea leptophylla
• Plants with ants had fewer seeds destroyed by
  beetles, fewer stigmas eaten by grasshoppers
• Plants with ants had an order of magnitude
  greater seed production

55
Extrafloral nectaries importance
Third-party defenses

• Bean tree, Catalpa speciosa
• Plants with ants produced more mature fruits per
  branch

56
Extrafloral nectaries importance
Third-party defenses

• Little sunflower, Helianthella quinquenervis
• Plants with ants had fewer insect seed predators
• Seed predation 15 lower

57
Summary herbivory

• Effects of herbivores vary depending on plant
  traits and type/amount of damage
• Plants can utilize different strategies for
  resistance
• Several models predict how resources should be
  allocated to defense, but most have mixed support
• Range of resistance strategies impressive
  (tolerance, third party interactions,
  eavesdropping on signals, etc)