HERBIVORY
Photo of leafcutter ant from: http://phenomena.nationalgeographic.com/2012/12/27/
how-leafcutter-ants-evolved-from-farmers-into-cows/
Photo of dugong from: http://mgsupply.co/2013/11/dugong-grazing-the-sea-floorwhile-pilot-fish-hover-closely-for-small/
Herbivory
Herbivory (a broad definition): the consumption of
all or parts of living plants
“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 Strong from U. C. Davis
Herbivory
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
Seed “predators” = granivores
Parasites – generally live in close association with their host plants,
e.g., parasitic plants, aphids, nematodes, etc.
Herbivory & Stable Isotopes
XX
XX
= radioisotope
= stable isotope
isotopes
7
13N
14N
15N
16N
6
12C
13C
14C
15C
6
7
8
9
#
Protons
#
Neutrons
Herbivory & Stable Isotopes
Nonradioactive; differ in number of neutrons;
lighter form much more abundant in nature;
heavier form generally discriminated against in chemical rxns
Herbivory & Stable Isotopes
Figure from: http://6e.plantphys.net/topic09.07.html; data from: Cerling et al. (1997)
An herbivorous jumping spider
(Bagheera kiplingi) that exploits
an ant-plant mutualism
(Vachellia [formerly Acacia] &
Pseudomyrmex)
Figure from Meehan et al. (2009)
Proxy for Trophic Level
Herbivory & Stable Isotopes
An Herbivore in a Carnivorous Clade
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)
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
Costs of Herbivory
Water calyces dissuade floral herbivores
P < 0.01
Chrysothemis friedrichsthaliana
Osa Peninsula, Costa Rica
Photos from Greg Dimijian (plant) & Jane Carlson (moth); Figure redrawn from Carlson & Harms (2007)
Costs of Herbivory
Classic study: Tropical Piper
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
Costs of Herbivory
Classic study: Tropical Piper
Methods:
Marquis (1984) experimentally removed leaf area with a hole-punch
Treatments: 0, 10, 30 & 50% of the plant’s 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
Confronted with damaging herbivory, why is the (nondesert / 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 isn’t fatal –
plants are expected to evolve defenses against herbivores; in this case,
the abundance of food for herbivores would be illusory
Costs of Herbivory Favor the Evolution of Defenses
Classic study: Tropical Piper
Methods:
Marquis (1984) grew clones of several
genotypes in understory experimental
arrays
Results:
Variation in resistance to herbivory had
a 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
Plant Defense Traits
Defenses: mechanical (toughness, spines, latex, etc.), chemical
(alkaloids, phenolics, terpenoids, latex, etc. – the realm of chemical
ecology), developmental, and phenological
E.g., Acacias protected from
browsing giraffes produce
fewer, shorter thorns (Young
1987); thorns are
constitutive, but have
inducible characteristics
Defenses: classified with reference to production
Constitutive – produced & present irrespective of attack
Induced – produced & present in response to attack
Photo of browsing giraffe from: http://www.wildlife-pictures-online.com/giraffe-information.html
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”
Resistant
Tolerant
Slide courtesy of Alyssa Stocks Hakes; modified from the original
Susceptible
Benefits of defense
are obvious in the
presence of
herbivores
Resistant
Tolerant
Slide courtesy of Alyssa Stocks Hakes; modified from the original
Susceptible
Costs of defense are
obvious in the
absence of
herbivores
Resistant
Tolerant
Slide courtesy of Alyssa Stocks Hakes; modified from the original
Susceptible
Resistance-related Plant Traits
Slide courtesy of Amanda Accamando; modified from the original
Resistance-related Plant Traits:
Direct Defense
Secondary
Metabolites
Toxic chemicals
E.g., Tannins
Slide courtesy of Amanda Accamando; modified from the original
Tim Ross
Anti-nutritive compounds
James H. Miller, USDA Forest Service
Resistance-related Plant Traits:
Direct Defense
Morphological
Characteristics
Leaf Toughness
http://remf.dartmouth.edu/imagesindex.html
Trichomes
Slide courtesy of Amanda Accamando; modified from the original
Thorns
Chris Evans, River to River CWMA, Bugwood.org
Secondary
Chemistry
Milkweeds
(Asclepias spp.)
Cardenolides
• Toxic to many
herbivores
• Specialist
counteradaptations
Morphological
Characteristics
Physical
Barriers
• Trichomes
• Latex
Agrawal and Fishbein 2008; EcoEd Digital Library; monarchwatch.org
Slide courtesy of Amanda Accamando; modifid from the original
Resistance-related Plant Traits:
Indirect Defense
Natural Enemies
recruited by:
EcoEd Digital Library
Plant Volatile Emissions
www.usda.gov
Extrafloral Nectaries
Slide courtesy of Amanda Accamando; modified from the original
http://aggie-horticulture.tamu.edu/gavelston
Plant Defense
How do plants
optimize types
& levels
of defense?
Resources
Slide courtesy of Amanda Accamando; modified from the original
Trade-offs & constraints
High Costs + High Benefits
constraint line
Trait Y
Low Costs + Low Benefits
Low Costs +
Low Benefits
Trait X
High Costs +
High Benefits
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
Trade-offs & constraints
(Allocation)
Size of
eyes
Size of horns
Nijhout & Emlen (1998) Proceedings of the National Academy of Sciences, Fig. 1 d & e
Trade-offs & constraints
(Design)
Performance
on branches
Performance on
ground
From Losos et al. (2004)
The efficacy of defenses against herbivores
Hemiparasitic exploitation of “secondary chemicals”
Observations:
Adler (2000) used hemiparasitic plants that obtain “secondary chemicals”
from their hosts
Methods:
Grew Indian paintbrush (Castilleja indivisa) with either
“sweet” or “bitter” lines of lupines (Lupinus albus) –
that differ in alkaloid production
Results:
 Lynn Adler
Hemiparasites grown with “bitter” hosts suffered lower herbivory, but had
increased seed set
Conclusions:
“Secondary chemicals” can indeed serve as beneficial plant defenses
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 counterevolve 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
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)
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…
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.
Plant Defense Theory
Plant-apparency theory arose especially out of Feeny’s 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
Mustards: Very low concentrations of a
variety of glucosinolates, toxic at extremely
low doses to all but a few specialist
herbivores
“Apparent”
“Unapparent”
Plant Defense Theory
Ecological correlates of plant defenses according to
plant-apparency theory (from Howe and Westley 1988)
Examples
Properties
Qualitative
defenses
Alkaloids, cyanogens,
terpenes
Small toxic molecules
Distribution in plant
New leaves, buds
Distribution among
plants
Rare, short-lived
herbs;
Early successional
plants
Advanced
angiosperms
Phylogeny
Favored in
“unapparent” plants
Quantitative
defenses
Cellulose & lignins
(fiber), silica,
phenolics, tannins
Complex polymers
Permanent woody
tissue
Common long-lived;
Late successional
plants
Also in ancient ferns,
gymnosperms
Favored in
“apparent” plants
Plant Defense Theory
Limits to plant-apparency theory:
Futuyma’s (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?
Plant Defense Theory
Resource-availability theory (Coley et al. 1985)
Optimum strategy of defense is mediated by a plant’s 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
Species with high
intrinsic growth rates are
adapted to life in a high
resource environment
Plants that grow
rapidly in highresource 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?
From Coley et al. (1985)
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
From Coley et al. (1985)
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
From Coley et al. (1985)
Cumulative defense cost
Immobile defenses (lignins,
tannins) have a saturating
cumulative cost curve owing to
low turnover
Leaf lifetime
Redrawn from Coley et al. (1985)
Mobile defenses (toxic, small
molecules) have a monotonically
increasing cumulative cost curve
because they continuously turn
over
Cumulative defense cost
Immobile defenses (lignins,
tannins) have a saturating
cumulative cost curve owing to
low turnover
Leaf lifetime
Redrawn from Coley et al. (1985)
Immobile defenses (lignins,
tannins) have a saturating
cumulative cost curve owing to
low turnover
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
Immobile
defenses
advantageous
Cumulative defense cost
Mobile defenses (toxic, small
molecules) have a monotonically
increasing cumulative cost curve
because they continuously turn
over
Mobile
defenses
advantageous
Leaf lifetime
Some live
to 14 yr
Redrawn from Coley et al. (1985)
What subtle
assumption is
being made?
Benefits are equivalent
for mobile vs. immobile
defenses
Immobile
defenses
advantageous
Cumulative defense cost
Mobile
defenses
advantageous
Leaf lifetime
Redrawn from Coley et al. (1985)
Growth and defense characters of tropical trees,
from Coley (1983) and subsequent work
Variable
Pioneers
Shadetolerators
Maximum growth rate
High
Low
Leaf toughness
Low
High
Leaf protein content
High
Low
Leaf lifetime
Short
Long
Successional status
Often Early
Late
Herbivory rate
High
Low
Ability to replace tissue
High
Low
Defense investment
Low
High
Turnover rate of defense
High
Low
Leaf expansion rate
Normal
Low or High
Leaf greening rate
Normal
Low or High
Plant Defense Theory
Grubb’s (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), the type of herbivores present, etc.
Photo of Grubb from Seed Science Research (2013) v. 13
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.
Plant Defense Theory
Kitajima (1994) highlighted this trade-off and challenged the paradigm
that favored physiological rates as the principle determinants of shadetolerance; 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)
Plant Defense Theory
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)
Plant Defense Theory
Hypotheses
Defense & Environment
Resource Availability:
Defense increases in low resource
environment
Coley et al. (1985)
Growth Differentiation Balance:
Herms & Mattson (1992)
Compensatory Continuum:
Defense decreases in low and high resource
environment
Maschinski & Whitham (1989)
Tolerance decreases in low resource
environment
Defense-Stress Cost:
Defense decreases under competition
Siemens et al. (2003)
Defense-Stress Benefit:
Defense increases under competition
Siemens et al. (2003)
Associational Resistance:
Tahvanainen & Root (1972)
Associational Susceptibility:
Brown & Ewel (1987)
Location by resistant neighbors lowers
susceptibility of focal plant
Location by susceptible neighbors lowers
resistance of focal plant
Slide courtesy of Alyssa Stocks Hakes; modified from the original
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 can’t eat Australian kelp
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 plant’s
external physical defenses
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
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
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://www.tfsnz.org.nz/exploring-native-plant-curiosities/