HERBIVORY. Herbivory (a broad definition): the consumption of all or parts of living plants Seed...

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





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


Tim

Ro

ss

Resistance-related Plant Traits: Direct Defense

Morphological Characteristics

Leaf Toughness

Trichomes

Thorns

Chris Evans, River to River CWMA, Bugwood.org

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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

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http://aggie-horticulture.tamu.edu/gavelston

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Plant Defense

Resources

Defense Gro

wth &

Repro

duct

ion

How do plants

optimize types

& levels

of defense?


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-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


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


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


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?


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

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 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 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


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


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)

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, 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


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


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)

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