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HERBIVORY
Herbivory (a broad definition): the consumption ofall 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…”
Herbivory
Photo of Don Strong from U. C. Davis
(Strong 1988; Perhaps a bit of an overstatement, but nevertheless conveys the importance of plant-herbivore interactions)
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
Herbivory (a broad definition): the consumption ofall or parts of living plants
Herbivory
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)
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)
Costs of Herbivory
Complete defoliation that precludes reproduction (owing to death, etc.) obviously results in net costs;
e.g., Gypsy moth (Lymantria dispar) defoliation
Photos from Wikipedia
Water calyces dissuade floral herbivores
P < 0.01
Chrysothemis friedrichsthalianaOsa Peninsula, Costa Rica
Costs of Herbivory
Photos from Greg Dimijian (plant) & Jane Carlson (moth); Figure redrawn from Carlson & Harms (2007)
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%.
Costs of Herbivory
Photo of a species of Piper (not P. arieianum) from Wikipedia
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
Costs of Herbivory
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
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
Confronted with damaging herbivory, why is the (non-desert / non-polar terrestrial & near-shore) world green?
Costs of herbivory favor the evolution of defenses
Photo of a species of Piper (not P. arieianum) from Wikipedia
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
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
Plant defense traits
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”
Slide courtesy of Alyssa Stocks Hakes; modified from the original
Resistant Tolerant Susceptible
Benefits of defense are obvious in the
presence of herbivores
Slide courtesy of Alyssa Stocks Hakes; modified from the original
Resistant Tolerant Susceptible
Slide courtesy of Alyssa Stocks Hakes; modified from the original
Resistant Tolerant Susceptible
Costs of defense are obvious in the
absence of herbivores
Resistance-related Plant Traits
Slide courtesy of Amanda Accamando; modified from the original
Resistance-related Plant Traits: Direct Defense
Secondary Metabolites
E.g., Tannins
Toxic chemicals
Anti-nutritive compounds
Slide courtesy of Amanda Accamando; modified from the original
Tim
Ro
ss
Resistance-related Plant Traits: Direct Defense
Morphological Characteristics
Leaf Toughness
Trichomes
Thorns
Chris Evans, River to River CWMA, Bugwood.org
Jam
es H
. Mill
er, U
SD
A F
ores
t Ser
vice
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mf.d
artm
outh
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esin
dex.
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l
Slide courtesy of Amanda Accamando; modified from the original
Secondary Chemistry
Milkweeds(Asclepias spp.)
Cardenolides• Toxic to many
herbivores
• Specialist counter-adaptations
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:
Plant Volatile Emissions
Extrafloral Nectariesw
ww
.usd
a.go
v
http://aggie-horticulture.tamu.edu/gavelston
Eco
Ed
Dig
ital L
ibra
ry
Slide courtesy of Amanda Accamando; modified from the original
Plant Defense
Resources
Defense Gro
wth &
Repro
duct
ion
How do plants
optimize types
& levels
of defense?
Slide courtesy of Amanda Accamando; modified from the original
Trait X
Trait Y
High Costs + High Benefits
Low Costs + Low Benefits
High Costs + High Benefits
Low Costs + Low Benefits
constraint line
Trade-offs & constraints & 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
From Emlen (2000)
Trade-offs & constraints(Allocation)
Size ofhorns
Size ofeyes
From Losos et al. (2004)
Trade-offs & constraints(Design)
Performance onground
Performance on branches
Lynn Adler
The efficacy of defenses against herbivores
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
Conclusions:
“Secondary chemicals” can indeed serve as beneficial plant defenses
Observations:
Adler (2000) realized that hemiparasitic plants that obtain “secondary chemicals” from their hosts would serve as good experimental subjects
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
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)
Co-evolution
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)
Host
Herbivore
Co-cladogenesis (e.g., co-speciation; macroevolutionary focus)…
Co-cladogenesis
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
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.
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.
Unapparent plants: Short-lived herbaceous plants of early successional environments
Plant Defense Theory
Mustards: Very low concentrations of a variety of glucosinolates, toxic at extremely low doses to all but a few specialist herbivores
Plant-apparency theory arose especially out of Feeny’s studies on oaks (apparent) and wild mustards (unapparent) in central New York
“Apparent”
“Unapparent”
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
Plant Defense Theory
Qualitative defenses
Quantitative defenses
Examples Alkaloids, cyanogens, terpenes
Cellulose & lignins (fiber), silica,
phenolics, tannins Properties Small toxic molecules Complex polymers
Distribution in plant New leaves, buds Permanent woody
tissue Distribution among plants
Rare, short-lived herbs;
Early successional plants
Common long-lived; Late successional
plants
Phylogeny Advanced angiosperms
Also in ancient ferns, gymnosperms
Ecological correlates of plant defenses according to plant-apparency theory (from Howe and Westley 1988)
Favored in “apparent” plants
Favored in “unapparent” 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
Plant Defense Theory
Photo of Coley from U. Utah
Species with high intrinsic growth rates are adapted to life in a high resource environment
Coley et al. (1985)
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?
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
Coley et al. (1985)
For slow growing plants in low resource environments it is costly to replace lost tissue
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)
Leaf lifetime
Cum
ulat
ive
defe
nse
cost
Immobile defenses (lignins, tannins) have a saturating cumulative cost curve owing to low turnover
Imm
obile
def
ense
s
Coley et al. (1985)
Leaf lifetime
Cum
ulat
ive
defe
nse
cost
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
Imm
obile
def
ense
s
Mobile defen
ses
Coley et al. (1985)
Leaf lifetime
Cum
ulat
ive
defe
nse
cost
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
Imm
obile
def
ense
s
Mobile defen
ses
Some live to 14 yr
Coley et al. (1985)
Leaf lifetime
Cum
ulat
ive
defe
nse
cost
Mobile defenses
advantageous
Immobile defenses
advantageous
Imm
obile
def
ense
s
Mobile defen
sesWhat subtle
assumption is being made?
Benefits are equivalent for mobile vs. immobile
defenses
Coley et al. (1985)
Slide courtesy of Alyssa Stocks Hakes; modified from the original
Plant Defense Theory
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 isolationfrom 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 isolationfrom 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 isolationfrom other species-interactions
van Bael et al. (2003) assessed the impact of the third trophic level on herbivory in the canopy of tropical forests
Herbivory, plant defense, and the third trophic level…
Conclusions: The impact of the third trophic level, and the nature of trophic cascades, differs with productivity
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
Herbivory does not occur in isolationfrom other species-interactions
Ghosts of Herbivory Past
Photo from http://haasep.homepage.t-online.de/research.htm
Is the “divaricate” architecture of several species of shrub in New Zealand an adaptation to browsing by extinct moas?
(Greenwood & Atkinson 1980)