Defense against predation and herbivory Prey may escape predators via refugia, through shifts in body size (too big to eat, or two small to be energetically feasible to predate), or through changes in morphology and behavior.

At the population level, synchronous phenology (e.g., leaf and seed production, insect emergence may satiate predators.

Most complete theory concerns how plants defend against herbivory. Numerous hypotheses have been posited to explain within and among species variation in chemical and physical defenses.

Hypothesis: Size-dependent predation by fish determines the size structure of freshwater zooplankton

Observations: - lakes seldom contained abundant large zooplankton (>0.5 mm) and small Zooplankton (<0.5 mm) together - large zooplankton did not coexist with plankton feeding fish

Brooks and Dodson (1965) Predation, body size, and composition of plankton

Assumptions: Large zooplankton assumed to be superior competitors for food (phytoplankton) because of greater filtering efficiency

Planktivorous fish thought to selectively consume large-bodied, competitively superior plankton (greater numeric response)

Crystal lake Connecticut. No planktivorous fish (Alosa) Large plankton

Crystal lake 22 years later after introduction of Alosa

Herbivory and Plant defense

Herbivores play a key role in determining the trophic structure of terrestrial communities.

For plants, what determines how well they are defended from herbivores?

Explore here: risk of herbivory opportunity costs of herbivory costs of synthesizing defenses trade-offs of defense with other life-history traits and significance for species coexistence

Cost of herbivory

Obvious costs when complete defoliation of plants precludes reproduction or results in death

Less conspicuous herbivores may have significant costs (e.g. grazing of ovules or undispersed seeds affecting reproductive output, or partial defoliation resulting in decreased carbon budget)

Marquis (1984) Looked at the effect of simulated leaf herbivory by a weevil Ambetes on an understorey tropical shrub Piper arieianum in Costa Rica

Piper (Piperaceae; black pepper) huge genus of tropical and sub-tropical shrubs (~1400 spp)

Opportunity cost of herbivory is determined in part by leaf-life time. Piper plants lose 1-3 % of leaf area per month, but leaves live 30 months.

One time measure of missing leaf area on entire plants ranged between 3 and 50 %

Experimentally removed leaf area with a hole-punch to mimic the pattern of natural damage - some leaves lots of damage others remove little tissue…

Treatments of 0, 10, 30, 50, 100 % leaf area removal

Tracked growth and reproduction over following 2 years

Results: Small and medium sized plants showed a 50 % reduction in growth with > 30 % defoliation measured over the two years Seed production dropped in half for both first and second years after 30 % defoliation)

Large effects of damage on growth and reproductive output in Piper coupled with genotypic variation in susceptibility to damage suggests that defensive characters of Piper are under continuous selection

Coley (1986) herbivory in Cecropia peltata

Measured growth and herbivory of seedlings grown from seeds from several parent trees

Measured tannin levels in foliage as major chemical defense

In Cecropia, tannin concentration is negatively correlated with plant growth rate

In the field herbivory for ‘high’ tannin plants was lower (0.5 %) than for ‘low’ tannin plants (0.6 %)

Herbivory is not always associated with lower fitness

Paige and Whitham (1987)

Overcompensation in response to mammalian herbivory: the advantage of being eaten Am. Nat. 129:407-416 (and other papers)

Scarlet gilia (Ipomopsis aggregata)

Herbivores remove 95 % of the above ground biomass, but plants respond by ‘over compensating’ resulting in 2.5x greater seedling establishment.

77% of plants browsed once

33% of plants browsed twice

Once browsed, new inflorescences may have greater induced defenses

Plant species evolve secondary compounds in response to attack; insects evolve new detoxification systems to over-come them.

Adaptation to one set of host plant chemicals results in losing the ability to consume other hosts

Chemical arms races eventually results in plant families acquiring a complex of defenses that exclude all but a fauna of related taxa of specialist herbivores

Under what conditions do plants evolve different kinds of defenses? What are the predictors for the level of defense exhibited?

Plant defense theory

Biochemical coevolution theory: Ehrlich and Raven (1964)

Coevolutionary theory accounts for specialist herbivores (e.g. Berenbaum 1983 and citations on website)

Wild parsnip - watch out! Produces fouranocoumarins - toxins that cause skin damage under UV light

Webworm: specialist herbivore

However most plants are subjected to herbivory from a wide range of vertebrates and invertebrates

Why do plants differ so much in vulnerability to herbivores?

Parsnip webworm and wild parsnip (introduced to the US)

Webworms capable of metabolizing furanocoumarins and are capable of selecting parsnip chemical traits

Furanocoumarin profiles of plants match metabolizing capacity of local populations of webworms

Plants that are easily found by herbivores (‘apparent’ plants) should invest heavily in quantitative defenses that are effective against all herbivores.

Plants that are difficult to locate (‘unapparent’ plants) should invest smaller amounts in qualitative defenses that are effective against all but specialist herbivores

Plant apparency theory (Feeny 1976)

Apparent plants: Trees and shrubs, and grasses from late successional communities with long generation times

Unapparent plants: Short-lived herbaceous plants of early successional environments

Qualitative defenses Quantitative defensesExamples Alkaloids, cyanogens,

terpenesCellulose, lignins,silica, tannins

Properties Small toxic molecules Complex polymersDistribution in plant New leaves, buds Permanent woody

tissueDistribution amongplants

Rare, short-lived herbsEarly successionalplants

Common long-livedlate successional plants

Phylogeny Advanced angiosperms Also in ancient ferns,gymnosperms

Ecological correlates of plant defenses according to apparency theory (from Howe and Westley 1988)

Oaks: defensive chemicals are primarily tannins.

Oaks only suffer major outbreaks during early spring bud-breaks before tannin concentrations in expanding leaves reach toxic concentrations

Limits to apparency theory?

Apparency theory arose out of Feeny’s studies on Oaks (apparent) and mustard plants (unapparent) in central New York

Mustard: very low concentrations of a variety of glucosinolates, toxic at extremely low doses to all but specialist feeders

Resource availability theory (Coley 1985)

Plant defensive capabilities are mediated by their capacity to replace lost tissue given resources at their disposal.

Resource availability stresses economics of growth: inherent growth rate, and nutrient availability as determinants of the amounts and kinds of defenses that plants use.

Fast-growing plants in well-lit environments with fertile soils can easily replace leaves or other tissues lost to herbivores (their ‘cost of herbivory’ is relatively low).

What do the arrows indicate?

What do the upper and lower curves represent?

Resource availability theory predicts that fast growers should invest relatively little in defense, and should use mobile resources that can be moved out of quickly senescing tissue

Why invest costly immobile defenses in tissues that will be discarded after a few months anyway?

Slow growing plants, characteristic of low resource environments (eg deserts, forest understory, <infertile soils>) should invest more in defense because tissue is costly to replace.

Long-lived leaves can use immobile defenses (lignin and tannins) that are less expensive in the long run.

Plant structures in low resource environments can be extremely long-lived (e.g., 14 year old leaves!)

Growth-defense trade-off

High investment in defense = low growth rate and low mortality rate. Plants survive in shade, and are uncompetitive in sunlit sites

Low investment in defense = high growth rate and susceptibility to herbivores. Plants constrained to sunny sites.

Not that different from a growth-predation risk trade-off in animals?

Coley’s theory shows that allocation to defense is one component of a trade-off that limits the range of microsites in which plants regenerate.

Recognition of the cost of herbivory shifted a paradigm which stressed physiological traits as determining shade-tolerance to one in which allocational traits are emphasized

Kitajima (1994)

Plants that grow fastest in high light (24 % full sun) also grow fastest in shade (2 % full sun)

Points are species (n=13) varying in ‘shade tolerance’

Growth rate in sun or shade is positively correlated with mortality rate in the shade

In Kitajima’s growing house experiment mortality was attributable to fungal pathogens, but other sources of mortality are important in the field.

Dalling & Hubbell (2002)

Growth - mortality for pioneer species in small gaps (10 % Full sun)

Mortality is attributable to browsing damage and insect herbivores

Growth-mortality trade-off driven by herbivores/pathogens has important implications for understanding species distribution patterns (Wednesday’s readings):

• Among site variation in the ‘cost of herbivory’ (resource availability)

• Among site variation in ‘intensity of herbivory’ (do habitat requirements of herbivores differ from that of their food plants?)

• Understanding species invasions (can escape from herbivores shift where plants are able to grow?) What would you predict?

Coley (1983) measured herbivory rates and characterized plant defenses of 46 tree species in lowland forest, Panama

Multivariate analysis to determine what plant traits can account for variation in leaf damage across species.

Found best predictor of damage = leaf toughness>fiber content>nutritive value

Fast growing species have least tough leaves, lowest phenolics and fiber concentration

How do plants defend against generalist herbivores?

In 70 % of species, young leaves suffered higher damage than mature leaves - young leaves have not toughened but have 2-3 times [phenolics] of mature leaves

Fast growing pioneer species have more nutritious and less well defended leaves than slow-growing shade-tolerant species.

Leaves of pioneers were grazed six times more rapidly than leaves of shade-tolerant trees

Leaf toughness explains why most damage occurs on young leaves

Variable Pioneers Shade-tolerants

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

Growth and defense characters of tropical trees (from Coley 1983 and subsequent work)

Young leaves are white or pink and do no net photosynthesis

Only observe delayed greening in tropical forest understories, but is a common trait across evolutionary lineages

Delayed greening

Rapid leaf expansion

Develop whole leaves (or branches in a few days)

Brownea claviceps

Herbivory and the third trophic level

“Inviting friends to feast on foe”

Many ways that plant harness the third trophic level to defend themselves:

- fast growing trees are commonly ant plants because abundant light allows them to make sugar and lipid awards relatively cheaply

- mites are also common, but little studied (Walter and O’Dowd 1992). Mites live in domatia and feed on fungal spores and so might be important in protecting plants against pathogens?? In N. Queensland 15 % of trees have domatia (O’Dowd and Wilson 1989)

O’Dowd and Pemberton (1998). Looked at mites on leaves with domatia (D) and without domatia (ND) in two forests in Korea (KW) and (CH)

Species with domatia supported more predatory and fungus eating mites

Quantitative defenses slow down insect feeding and/or digestion rates

‘Quantitative’ defenses (tannins, fiber and toughness) do not present an absolute barrier against herbivores.

Hypothesis: Defensive effectiveness is due to mediation by the ‘third trophic level’

Slowing grazing rates is important because most damage occurs in the last instars of insect development

Slowing rates also lengthens the time that larvae are exposed to predators and parasitoids (‘slow-growth-high-mortality’ SG-HM hypothesis)

Evidence for SG-HM: Benrey and Denno (1997)

- Several studies using ‘free-living’ larvae show higher incidence of mortality from parasitoids for slow vs fast developing larvae. - Not supported in cases where larvae are protected (building shelters out of plant material or inside galls)

Fast developing larvae are better able to defend themselves against parasitoids

instar

Some plants may also send out a distress signal… (see lots of neat work by Karban et al at UC Davis on jasmonate signalling)

Thaler (1999) looked at the effect of Jasmonate a volatile chemical that induces chemical defense in plants.

Compared parasitism of caterpillars in induced vs non-induced plants

Summary

Plants and animal show numerous adaptations to reduce the probability of predation or rate of herbivory. Some of these are fixed, some are inducible. Incorporating defense of predation is important in understanding predator-prey dynamics

Anti-herbivore defenses are costly to produce and can help explain why plants show habitat specificity. Anti-predator defenses may have a similar effect in animal communities

Quantitative defenses are the most important general defenses of plants, some of these probably operate by involving a third trophic level (e.g., ants and parasitoids)