Download Defense against predation and herbivory

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.
Brooks and Dodson (1965) Predation, body size, and
composition of plankton
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
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 defense theory
Under what conditions do plants evolve different kinds of defenses?
What are the predictors for the level of defense exhibited?
Biochemical coevolution theory: Ehrlich and Raven (1964)
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
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
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 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?
Plant apparency theory (Feeny 1976)
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
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 Ecological correlates of plant defenses according to
apparency theory (from Howe and Westley 1988)
Examples
Properties
Distribution in plant
Distribution among
plants
Phylogeny
Qualitative defenses
Alkaloids, cyanogens,
terpenes
Small toxic molecules
New leaves, buds
Rare, short-lived herbs
Early successional
plants
Advanced angiosperms
Quantitative defenses
Cellulose, lignins,
silica, tannins
Complex polymers
Permanent woody
tissue
Common long-lived
late successional plants
Also in ancient ferns,
gymnosperms
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 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?
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!) 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.
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?
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.
Growth - mortality
for pioneer species in small gaps (10 %
Full sun)
Dalling & Hubbell
(2002)
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?
How do plants defend against generalist herbivores?
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
Leaf toughness explains why most damage occurs on young
leaves
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
Growth and defense characters of tropical trees (from Coley 1983 and subsequent work)
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
Delayed greening
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 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)