HERBIVORY

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HERBIVORY
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Herbivory
Herbivory (a broad definition) the consumption
of all or parts of living plants Seed
predators granivores Parasites live in
close association with their host plants, e.g.,
parasitic plants, aphids, nematodes, etc.
The overwhelming majority of all species
interactions occur between herbivorous insects
and plants, simply because these two groups
comprise half of the macroscopic species on
Earth
(Strong 1988 Perhaps a bit of an
overstatement, but nevertheless conveys the
importance of plant-herbivore interactions)
Photo of Don Strong from U. C. Davis
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Herbivory
Herbivory (a broad definition) the consumption
of all or parts of living plants
Grazers consume plant parts (mostly green) near
the substrate, e.g., snails graze algae, antelope
graze grass including roots (a relatively
unexplored frontier)
Browsers consume plant parts (mostly green)
well above the substrate, e.g., deer browse the
leaves of shrubs and saplings
Frugivores consume fruits, often without
damaging the seeds within, in which case the
relationship is likely to be mutualistic
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Herbivory
Can herbivory of green parts ever be
advantageous to the plant?
Compensation overcompensation increases in
growth or reproduction beyond what would occur in
the absence of herbivory no net difference in
fitness for consumed vs. unconsumed plants
(compensation), or an advantage to consumed
plants (overcompensation) See McNaughton (1983)
Belsky et al. (1993)
Results supposedly supporting compensation or
overcompensation usually depended on faulty logic
or false assumptions (e.g., aboveground plant
production is proportional to total plant
production)
Overall assessment herbivory entails net costs
(ardent defenders of compensation
overcompensation notwithstanding)
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Costs of Herbivory
Complete defoliation that precludes reproduction
(owing to death, etc.) obviously results in net
costs e.g., Gypsy moth (Lymantria dispar)
defoliation
Less conspicuous damage may have significant
costs that are difficult to assess without
experimentation (e.g., grazing of ovules partial
defoliation resulting in decreased carbon budget)
Photos from Wikipedia
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Costs of Herbivory
Water calyces dissuade floral herbivores
P lt 0.01
Chrysothemis friedrichsthaliana Osa Peninsula,
Costa Rica
Photos from Greg Dimijian (plant) Jane Carlson
(moth) Figure redrawn from Carlson Harms (2007)
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Costs of Herbivory
Piper (Piperaceae) tropical and sub-tropical
shrubs (1400 species) includes black pepper
Observations Marquis (1984) examined herbivory
on Piper arieianum in forest understory, La
Selva, Costa Rica. Highly variable among plants
mean damage 1 - 6 leaf-tissue loss over 2 - 3
mo. Leaves often live 2.5 yr total lifetime
losses can be substantial. Missing leaf area on
entire plants ranged 4 - 50.
Photo of a species of Piper (not P. arieianum)
from Wikipedia
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Costs of Herbivory
Methods Marquis (1984) experimentally removed
leaf area with a hole-punch Treatments 0, 10,
30 50 of the plants total leaf area removed,
plus 100 removal of leaf area (mimicking
leaf-cutter ant damage) he then assessed growth
and reproduction over 2 yr
Results Small- and medium-sized plants suffered
50 reduction in growth with ?30 defoliation
seed production dropped 50 for both years after
defoliation
Conclusion Herbivory is costly
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Confronted with damaging herbivory, why is the
(non-desert / non-polar terrestrial near-shore)
world green?
Hairston, Smith Slobodkin (1960 HSS)
speculated that since the world is green
herbivores must fail to limit the plants they
feed on, so herbivores must be limited by their
own predators
In addition, since herbivory is costly to plants
even when it isnt fatal plants are expected
to evolve defenses against herbivores in this
case, the abundance of food for herbivores would
be illusory
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Costs of herbivory favor the evolution of defenses
Methods Marquis (1984) grew clones of several
genotypes in understory experimental arrays
Results Variation in resistance to herbivory
hada genetic component
Conclusions Large effects of damage on growth
reproductive output coupled with genotypic
variation in susceptibility to damage suggests
that defensive characters are under continuous
selection
Photo of a species of Piper (not P. arieianum)
from Wikipedia
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Plant defense traits
Plants use a variety of mechanical (toughness,
spines, etc.), chemical (alkaloids, phenolics,
terpenoids, latex, etc. the realm of chemical
ecology), developmental, and phenological defenses
Defenses may also be classified with reference to
their production Constitutive produced by
present in the plant irrespective of
attack Induced produced by present in the
plant in response to attack
E.g., Acacia trees that are protected from
browsing giraffes produce fewer, shorter thorns
(Young 1987) thorns are constitutive, but
exhibit inducible characteristics
? Derek McDonald
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Plant defense traits
Tiffin (2000) Resistance traits those that
reduce herbivory
Avoidance (antixenosis) traits
those that affect herbivore behavior
i.e., deter or repel herbivores
Antibiosis traits those that reduce
herbivore performance
Tolerance traits those that reduce the impact
of herbivory on fitness
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Resistant
Tolerant
Susceptible
Slide courtesy of Alyssa Stocks Hakes modified
from the original
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Benefits of defense are obvious in the presence
of herbivores

Resistant
Tolerant
Susceptible
Slide courtesy of Alyssa Stocks Hakes modified
from the original
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Costs of defense are obvious in the absence of
herbivores
Resistant
Tolerant
Susceptible
Slide courtesy of Alyssa Stocks Hakes modified
from the original
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Resistance-related Plant Traits
DIRECT
INDIRECT
Slide courtesy of Amanda Accamando modified from
the original
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Resistance-related Plant Traits Direct Defense
Secondary Metabolites

• Toxic chemicals
• Anti-nutritive compounds

Tim Ross
E.g., Tannins
Slide courtesy of Amanda Accamando modified from
the original
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Resistance-related Plant Traits Direct Defense
Slide courtesy of Amanda Accamando modified from
the original
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Milkweeds(Asclepias spp.)
Secondary Chemistry
Morphological Characteristics

• Cardenolides
• Toxic to many herbivores
• Specialist counter-adaptations

• Physical Barriers
• Trichomes
• Latex

Agrawal and Fishbein 2008 EcoEd Digital Library
monarchwatch.org
Slide courtesy of Amanda Accamando modifid from
the original
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Resistance-related Plant Traits Indirect Defense
EcoEd Digital Library
Slide courtesy of Amanda Accamando modified from
the original
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Plant Defense
Growth Reproduction
Defense

• How do plants
• optimize types
• levels
• of defense?

Resources
Slide courtesy of Amanda Accamando modified from
the original
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Trade-offs constraints
constraints
High Costs High Benefits
constraint line
Trait Y
Low Costs Low Benefits
Trait X
High Costs High Benefits
Low Costs Low Benefits
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Trade-offs constraints
A jack-of-all-trades is master of none Adam
Smith (1776) applied the concept to
economics Robert MacArthur (1961) applied
the concept to evolutionary ecology
So most organisms become the master of one (or a
few), i.e., they specialize
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Trade-offs constraints(Allocation)
Size of eyes
Size of horns
From Emlen (2000)
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Trade-offs constraints(Design)
Performance on branches
Performance on ground
From Losos et al. (2004)
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The efficacy of defenses against herbivores
Observations Adler (2000) realized that
hemiparasitic plants that obtain secondary
chemicals from their hosts would serve as good
experimental subjects
Methods Adler (2000) grew Indian paintbrush
(Castilleja indivisa) with either sweet or
bitter lines of lupines (Lupinus albus) that
differ in alkaloid production and she followed
their fates
Results Hemiparasites grown with bitter hosts
suffered lower herbivory, and experienced
increased seed set
? Lynn Adler
Conclusions Secondary chemicals can indeed
serve as beneficial plant defenses
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Plant Defense Theory
Ehrlich Raven (1964) Proposed a biochemical
co-evolutionary hypothesis to explain why plants
differ in their chemical defenses why
herbivores differ in their ability to detoxify,
tolerate, or otherwise handle specific chemical
defenses
Plants evolve defense chemicals in response to
attacks by insects, while insects counter-evolve
detoxification systems
Adaptation to the host-plant chemicals of one
host trades-off against the ability to consume
other hosts
Chemical arms races result in related plants
having complexes of defenses that exclude all but
their own specialist herbivores (that are
generally themselves closely related)
Photo from Greg Dimijian
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Co-evolution
Co-evolution (microevolutionary focus) An
evolutionary change in a trait of the individuals
of one population in response to a trait of the
individuals of a second population followed by
an evolutionary response by the second
population to the change in the first Janzen
(1980)
Diffuse co-evolution occurs when either or
both populations in the above definition are
represented by an array of populations that
generate a selective pressure as a group
Janzen (1980)
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Co-cladogenesis
Co-cladogenesis (e.g., co-speciation
macroevolutionary focus)
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Plant Defense Theory
Ehrlich Raven (1964) is incomplete it does not
anwer Do contrasting ecological circumstances
favor different types of defenses? Do
contrasting ecological circumstances favor
different levels of defenses? Why do plants
differ in overall vulnerability to
herbivores? Etc
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Plant Defense Theory
Plant-apparency theory (Feeny 1976 Rhoades
Cates 1976)
Apparent plants Trees, shrubs, and grasses from
late successional communities with long
generation times
Unapparent plants Short-lived herbaceous plants
of early successional environments
Plants that are easily found by herbivores
(apparent plants) should invest heavily in
quantitative defenses that make them less
digestible to all herbivores. Quantitative
because their effect is proportional to their
concentration. These defenses are costly.
Plants that are difficult to locate (unapparent
plants) should invest smaller amounts in
qualitative defenses that are effective against
all but specialist herbivores. These defenses
are less costly.
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Plant Defense Theory
Plant-apparency theory arose especially out of
Feenys studies on oaks (apparent) and wild
mustards (unapparent) in central New York
Oaks Defensive chemicals are primarily tannins,
that stunt larval growth and reduce fecundity of
insects when they reach maturity oaks only
suffer major outbreaks during early spring
bud-breaks before tannin concentrations in
expanding leaves reach toxic concentrations
Apparent
Mustards Very low concentrations of a variety
of glucosinolates, toxic at extremely low doses
to all but a few specialist herbivores
Unapparent
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Plant Defense Theory
Ecological correlates of plant defenses according
to plant-apparency theory (from Howe and Westley
1988)
Favored in apparent plants
Favored in unapparent plants
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Plant Defense Theory
Limits to plant-apparency theory Futuymas
(1976) review found some support, but also many
exceptions
Apparency is difficult to measure objectively
Can plant traits be more directly linked to
mechanisms of defense?
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Plant Defense Theory
Resource-availability theory (Coley et al. 1985)
Optimum strategy of defense is mediated by a
plants capacity to replace lost parts with
resources at its disposal
Whereas plant-apparency theory stresses the
economics of herbivore foraging efficiency,
resource-availability theory stresses the
economics of plant growth differentiation
(especially allocation)
According to resource-availability theory,
inherent growth rate and resource availability
are determinants of the amounts and kinds of
defenses that plants employ
Photo of Coley from U. Utah
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Species with high intrinsic growth rates are
adapted to life in a high resource environment
Plants that grow rapidly in high-resource
environments can inexpensively quickly replace
tissues lost to herbivores (i.e., the costs of
herbivory are low)
Why invest in costly immobile defenses that will
be discarded after a few months anyway?
Coley et al. (1985)
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Species with high intrinsic growth rates are
adapted to life in a high resource
environment Species with low intrinsic growth
rates are adapted to life in a low resource
environment
For slow growing plants in low resource
environments it is costly to replace lost tissue
Coley et al. (1985)
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Species with high intrinsic growth rates are
adapted to life in a high resource
environment Species with low intrinsic growth
rates are adapted to life in a low resource
environment Species that differ in intrinsic
growth rate and habitat preference should differ
in the optimal levels (arrows) of defense
investment to maximize realized growth rates
Coley et al. (1985)
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Immobile defenses (lignins, tannins) have a
saturating cumulative cost curve owing to low
turnover
Immobile defenses
Cumulative defense cost
Leaf lifetime
Coley et al. (1985)
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Immobile defenses (lignins, tannins) have a
saturating cumulative cost curve owing to low
turnover Mobile defenses (toxic, small
molecules) have a monotonically increasing
cumulative cost curve because they continuously
turn over
Mobile defenses
Immobile defenses
Cumulative defense cost
Leaf lifetime
Coley et al. (1985)
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Immobile defenses (lignins, tannins) have a
saturating cumulative cost curve owing to low
turnover Mobile defenses (toxic, small
molecules) have a monotonically increasing
cumulative cost curve because they continuously
turn over Where growth is slow, costly
replacement means tissues should be built to
last, and plants should use immobile defenses
(lignin and tannins) that are permanently
employed and less expensive over the long term
Mobile defenses advantageous
Immobile defenses advantageous
Mobile defenses
Immobile defenses
Cumulative defense cost
Leaf lifetime
Some live to 14 yr
Coley et al. (1985)
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Mobile defenses advantageous
Immobile defenses advantageous
What subtle assumption is being made?
Mobile defenses
Benefits are equivalent for mobile vs. immobile
defenses
Immobile defenses
Cumulative defense cost
Leaf lifetime
Coley et al. (1985)
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Plant Defense Theory
Resource availability theory arose out of
community-wide studies of herbivory by Coley
(1983, etc.) colleagues (e.g., Bryant Chapin)
Coley (1983) measured herbivory rates and
characterized plant defenses of 46 tree species
in lowland forest, Panama
Multivariate analyses to determine which traits
correlated with damage leaf toughness gt fiber
content gt nutritive value
Pioneer species have least tough leaves, lowest
phenolics and lowest fiber concentration
Mature leaves of pioneer trees were grazed six
times more rapidly than leaves of shade-tolerant
trees
In 70 of species, young leaves suffered higher
damage levels than mature leaves young leaves
have not toughened but have 2-3 times phenolics
of mature leaves
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Growth and defense characters of tropical trees,
from Coley (1983) and subsequent work
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Plant Defense Theory
Grubbs (1992) positive distrust of simplicity
concerning plant defenses
Grubb suggested that a univariate approach to
understanding the distribution of plant defenses
among species (e.g., apparency or resource
availability) was probably too simplistic
Grubb suggested that a combination of variables
determines the level type of defense found in a
given species, population, or individual plant,
including habitat productivity (resource
availability), accessibility of the plant to
herbivores, relative abundance of the plant (as
in apparency), plant architecture, phenological
pattern (especially relative to other plants in
the vicinity), nutritious value of the plant
(especially relative to other plants in the
vicinity), and the type of herbivores present
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Plant Defense Theory
At any rate, allocation to defense is part of the
resource budget of the plant plants that
allocate a large proportion of resources to
defense have little left to invest in leaf
production and therefore have low intrinsic
growth rates
Growth-defense (or growth-mortality) trade-off
High investment in defense low growth rate and
low mortality rate. Plants can grow in shade.
Low investment in defense high growth rate and
high mortality rate (in shade). Plants
constrained to sunny sites.
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Kitajima (1994) highlighted this trade-off and
challenged the paradigm that favored
physiological rates as the principle determinants
of shade-tolerance allocation patterns must also
be considered
Plants that grow fastest in high light (24 full
sun) also grow fastest in shade (2 full sun)
N 13 species that vary in shade tolerance
Kitajima (1994)
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Growth rate in sun or shade is positively
correlated with mortality rate in the
shade Mortality was caused by fungal
pathogens Allocation to defense may impose an
allocation-based trade-off between growth and
survivorship
Kitajima (1994)
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Plant Defense Theory
Hypotheses Defense Environment
Resource Availability Ho Coley et al. (1985) Defense increases in low resource environment
Growth Differentiation Balance Herms Mattson (1992) Defense decreases in low and high resource environment
Compensatory Continuum Ho Maschinski Whitham (1989) Tolerance decreases in low resource environment
Defense-Stress Cost Ho Siemens et al. (2003) Defense decreases under competition
Defense-Stress Benefit Ho Siemens et al. (2003) Defense increases under competition
Associational Resistance Tahvanainen Root (1972) Location by resistant neighbors lowers susceptibility of focal plant
Associational Susceptibility Brown Ewel (1987) Location by susceptible neighbors lowers resistance of focal plant
Slide courtesy of Alyssa Stocks Hakes modified
from the original
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Plant Resistance Neighbor Effects
Herbivory on a plant may be influenced by the
diversity composition of its neighborhood
Slide courtesy of Amanda Accamando modified from
the original
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Associational Resistance Framework

• Resource Concentration Hypothesis

Enemies Hypothesis
Repellant Plant Hypothesis
Attractant-Decoy Hypothesis
Hypotheses are interrelated and not necessarily
mutually exclusive
Slide courtesy of Amanda Accamando modified from
the original
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Resource Concentration Hypothesis (Root 1973)

• Resource abundance and species richness in a
  patch influence herbivory

Generalist herbivore abundance
Specialist herbivore abundance
Increased plant species richness
Slide courtesy of Amanda Accamando modified from
the original
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Enemies Hypothesis (Root 1973)

• Tritrophic interactions influence herbivory

Generalist herbivore abundance
Specialist herbivore abundance
Herbivore natural enemies
Increased plant species richness
Slide courtesy of Amanda Accamando modified from
the original
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Repellent Plant Hypothesis (Atsatt ODowd 1976)

• Plant neighborhood composition influences
  herbivory

Highly-defended neighborhood
Slide courtesy of Amanda Accamando modified from
the original
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Repellent Plant Hypothesis (Atsatt ODowd 1976)
Susceptible ? Resistant
Attractant Patch High herbivore pressure
Repellant Patch Low herbivore pressure
Slide courtesy of Amanda Accamando modified from
the original
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Attractant-Decoy Hypothesis (Atsatt ODowd 1976)

• Nearest neighbor influences herbivory

Slide courtesy of Amanda Accamando modified from
the original
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Plants are interdependent with respect to the
herbivore pressure they face
Generalist Herbivore abundance
Highly-defended neighbor
Specialist herbivore abundance
Herbivore natural enemies
Increased plant species richness
Highly-defended neighborhood
Slide courtesy of Amanda Accamando modified from
the original
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Herbivory does not occur in isolation from other
species-interactions
Costs of herbivory differ depending on food-web
architecture
Observations by Steinberg et al. (1995)
Kelp from NW coast of the U.S. experience low
herbivory rates (because otters limit urchin
populations) U.S. kelp are consequently poorly
defended
No otters, but plenty of urchins in Australia
herbivory rates are much higher Australian kelp
have 6 times higher concentrations of phenolics
Australian urchins relish U.S. kelp U.S. urchins
cant eat Australian kelp
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Herbivory does not occur in isolation from other
species-interactions
Herbivory may increase the costs of other species
interactions
Herbivores often damage plants such that plant
pathogens may enter (Marquis and Alexander 1992)
Leaf-chewing insects Bark-browsing
mammals Phloem- and xylem-tapping
insects Stem-boring insects Root-boring
insects All may provide entry points for
fungi, bacteria, nematodes, other pests,
parasites, pathogens to bypass the plants
external physical defenses
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Herbivory does not occur in isolation from other
species-interactions
Herbivory, plant defense, and the third trophic
level
Plants often exploit the third trophic level to
defend themselves
Pioneers are commonly myrmecophytes (ant
plants) because abundant light allows them to
make sugar and lipid awards relatively cheaply
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Herbivory does not occur in isolation from other
species-interactions
Herbivory, plant defense, and the third trophic
level
Plants often exploit the third trophic level to
defend themselves
Mites are also commonly found on plants, but
relatively little studied (Walter and ODowd
1992). Mites may live in plant domatia feed on
fungal spores. In N. Queensland 15 of trees
have domatia (ODowd and Wilson 1989).
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Herbivory does not occur in isolation from other
species-interactions
Herbivory, plant defense, and the third trophic
level
Plants often exploit the third trophic level to
defend themselves.
Quantitative defenses (tannins, fiber and
toughness) are apparently effective
anti-herbivore defenses, yet they do not present
an absolute barrier against herbivores. Their
effectiveness may result in part from their
influence on the third trophic level
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Herbivory does not occur in isolation from other
species-interactions
Herbivory, plant defense, and the third trophic
level
Quantitative defenses slow down insect feeding or
digestion rates
Slowing rates is important because most damage
occurs in the last instars of insect development
Slowing rates lengthens the time that larvae are
exposed to predators and parasitoids
(slow-growth-high-mortality hypothesis)
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Herbivory does not occur in isolation from other
species-interactions
Herbivory, plant defense, and the third trophic
level
Quantitative defenses slow down insect feeding or
digestion rates
Slowing rates is important because most damage
occurs in the last instars of insect development
Slowing rates lengthens the time that larvae are
exposed to predators and parasitoids
(slow-growth-high-mortality hypothesis)
Review of evidence for SG-HM Benrey and Denno
(1997)
Support for SG-HM in free-living larvae
higher mortality from parasitoids in slowly
developing larvae
SG-HM was not supported in cases where larvae
are protected (building shelters out of plant
material or inside galls)
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Herbivory does not occur in isolation from other
species-interactions
Herbivory, plant defense, and the third trophic
level
van Bael et al. (2003) assessed the impact of the
third trophic level on herbivory in the canopy of
tropical forests
Methods Bird exclosures vs. controls on paired
branches, both in canopy and understory
Results Bird exclusion increased herbivory in
the canopy, but not in the understory
Conclusions The impact of the third trophic
level, and the nature of trophic cascades,
differs with productivity
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Ghosts of Herbivory Past
Is the divaricate architecture of several
species of shrub in New Zealand an adaptation to
browsing by extinct moas? (Greenwood Atkinson
1980)
Photo from http//haasep.homepage.t-online.de/rese
arch.htm