Herbivore attack is widely known to reduce
food quality and to increase chemical defenses and other
traits responsible for herbivore resistance. Researchers at
the Max Planck Institute for Chemical Ecology in Jena/Germany
demonstrated that inducible defenses allow plants to forgo
the costs of defense when not needed (PNAS, vol. 95, July 7,
1998).
All plants use chemical defenses to protect themselves from
attack by herbivores and pathogens and a majority of these
chemical defenses are inducibly deployed in some species,
that is their production is dramatically increased after
attack. Inducible defenses are inherently inferior to
constitutively deployed defenses due to the time lag between
the first attack and the activation of the defense, a delay
which could leave a plant vulnerable for hours or even days
as the defense is activated. Why then is this mode of defense
deployment so common, having been demonstrated in over 110
plant-herbivore interactions? The commonly-held explanation
is that chemical defenses are beneficial and increase a
plant's fitness when it is under attack, but they are
costly when not needed, utilizing resources that could be
used instead for growth or reproduction, or by other means
decrease the fitness of well-defended plants when grown in
competition with less-defended plants in environments lacking
herbivores. For example, plants that are chemically
well-defended may have a lower reproductive success than
undefended plants due to difficulties in attracting
pollinators. In short, inducible defenses are thought to have
evolved as a cost-savings measure, allowing plants to time
the production of a chemical defense with the prevailing
environmental conditions and forgo the costs of defense when
they are not needed.
Despite the general acceptance that inducible responses are
adaptive, two critical assumptions remain untested.
Surprisingly, it has yet to be demonstrated that an inducible
complexities of ecological interactions in nature frequently
wreak havoc with the best defense strategies. For example,
plant chemical defenses are frequently sequestered by
specialist herbivores for their own defense, thereby turning
a plant's defense against itself. Many inducible
chemical responses, such as protease inhibitors which slow
herbivore growth by reducing their digestive efficiency, may
only function as defenses in nature when expressed in concert
with other responses, such as the induced alarm calls of
plants that increase the vulnerability of the herbivore to
its own predators. Without the use of the third trophic
level, an plant may lose more leaf area and have a lower
fitness as a result of slowing the growth rates of their
herbivores. These considerations underscore the importance of
examining the benefits of induced defenses in natural
populations.
A second, untested assumption is that the induced,
well-defended phenotype has a lower fitness than the
uniduced, poorly-defended phenotype in environments without
herbivores. While genetical analysis of
constitutively-deployed chemical defenses support the view
that chemical defense can be costly, the phenotypic costs of
an induced defense, that is, the fitness difference between
the induced and uninduced members of the same genotype
remains to be critically evaluated, due in large part to the
experimental difficulties of activating defenses without
wounding or controlling for the fitness consequences of
tissue lost during induction. If induced defenses are costly
due either to the resource demands of their production or to
other ecological costs, then these costs can best be
evaluated in the environments in which these responses
presumably evolved.
Nicotiana attenuata synthesizes the toxic alkaloid, nicotine,
in its roots and dramatically increases its rate of nicotine
synthesis after leaf wounding and herbivory, which, in turn,
results in a systemic increase in nicotine concentrations in
both vegetative and reproductive tissues. In laboratory
feeding trials, induced levels of nicotine protect plants
against nicotine-tolerant herbivores, but these herbivores
may suffer lower rates of parasitisms when feeding on plants
with high nicotine concentrations, indicating that this
induced defense may have both ecological benefits and costs.
Moreover, 6% of an N. attenuata plant's total
nitrogen content is in this toxin alone in an induced plant,
and this nitrogen is not available for other activities such
as seed production, suggesting that inducing nicotine
production may incur large resource-based costs. Hence, it is
reasonable to suppose that the fitness consequences of
producing this toxin will vary greatly depending on the
plant's habitat.
The discovery of the endogenous wound signals which plants
use to activate induced responses, have provided researchers
with valuable tools to activate defenses independently of
herbivore attack in plants growing in their native habitats.
Jasmonic acid, a ubiquitous wound-hormone known to increase
the synthesis of diverse defense-related metabolites, is
strongly implicated as a long-distance endogenous
wound-signal activating nicotine synthesis in the roots after
leaf wounding and it is reasonable to propose that the
treatments of roots with jasmonate will stimulate responses
comparable to those elicited by leaf wounding.
N. attenuata has life history characteristics that make it
particularly useful for a test of the cost-benefit model for
induced defenses. It is an ephemeral member of the annual
community in burned sagebrush, blackbrush and pinyon-juniper
forests of the Great Basin desert and synchronizes its growth
with the post-fire environment by producing dormant seeds
that germinate in response to cellulose combustion product(s)
found in wood smoke. Such synchronization allows this species
to exploit the ephemeral but nutrient-rich, herbivore- and
competition-poor environments that are commonly found after
fires. This temporal window of growth opportunity is
frequently quite short, for as post-fire succession proceeds,
herbivores and competitors quickly recolonize the burned
habitats and plants found after each successive growing
season after a fire are smaller and attacked more frequently
by herbivores than those of the preceding season. It can be
the most abundant species during the first growing season
after a fire but it rarely persists for more than three years
after fires. Hence, by studying plants growing in
different-aged burns, one can study plants with different
attack probabilities.
To test the cost-benefit model, 745 matched pairs of
naturally occurring plants in 4 natural populations in SW
Utah were established: 2 in 1-year-old burns (IA and IB)
where herbivory is typically low (350 plant pairs) and 2 in
2-year-old burns (IIA and IIB) where herbivory is typically
much higher (345 pairs). A fifth population of 50 pairs was
created in a nearby field-plantation where plants were
protected from herbivores with fencing and pyrethrin
insecticide applications. The amount of jasmonate required to
add to the roots of plants in order to elicit an induced
nicotine response was determined and one member of each pair
was treated during early rosette-stage growth (May-June). The
effects of jasmonate induction on nicotine production,
herbivory and lifetime viable seed production was determined.
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The
root-produced toxin, nicotine, increases after herbivore
attack in the native, post-fire annual, Nicotiana attenuata,
and is internally activated by the wound-hormone, jasmonic
acid. The roots of plants were treated with the methyl ester
of this hormone (methyl jasmonate; 500µg suspended in 10 ml
water, while control members of the pair were treated with 10
ml water) to elicit a response in one member of each of 745
matched pairs of plants growing in native populations in
southwestern Utah (USA) with different probabilities of
attack from herbivores (primarily rabbits and the larvae of
the tobacco specialist, Manduca sexta).The lifetime
production of viable seed was measured from all plants to
determine the fitness consequences of jasmonate induction.
The results strongly support the cost-benefit model for
inducible defenses. Jasmonate treatment significantly
increased nicotine concentrations in the leaves of treated
plants 22-54% above those of their control,
water-treated counterparts. In populations where plants were
being heavily attacked (populations IIA, B), nicotine
concentrations of leaves from control plants were comparable
to those of unattacked jasmonate-induced plants from the
other populations, but the effect of jasmonate treatment was
retained; clearly, the jasmonate treatment had not saturated
the plants' nicotine response. How do these changes
affect plant fitness as estimated by their lifetime viable
seed production? The answer depends critically on the
plant's environment, particularly, the likelihood of
herbivore attack.
For plants in environments with high herbivory (the
2-year-old burns, populations IIA, B), the benefit of
jasmonate-treatments could be readily seen. For example, in
population IIA, 10 days after the treatment, 33% of the
control plants had lost more than 40% of their leaf area to
herbivores, as compared to 1% for Jasmonate-treated plants.
However, this protective effect of jasmonate treatment did
not translate into a fitness benefit for the plants in this
population in which 81% of plants did not survive to produce
any viable seed. No pairs survived to produce seed in the
second 2-year-old burn (IIB).
For plants growing completely protected from herbivores
(i.e., in the plantation) jasmonate-treatment significantly
reduced lifetime viable seed production by 26% (9.9 capsules
plant- 1 or 1552 viable seeds). A similar cost was
observed between induced and uninduced members of pairs
growing in population IB which had largely escaped herbivory
and lost less than 5% of their leaf area to herbivores by the
end of the growing season. In this population,
jasmonate-treatment reduced the lifetime capsule production
by 18% (26 capsules plant- 1). This reduction is similar to
the reduction associated with removing half of a plant's
leaf area at the rosette-stage of growth: 27% reduction
equivalent to 23 fewer capsules plant- 1 or 2021 viable
seeds. Hence when plants are protected or escape from
herbivore attack, plants treated with jasmonate produced
significantly fewer viable seeds at the time of senescence.
This cost, however, becomes a net fitness benefit for plants
growing in populations that have a higher probability of
herbivore attack.
For plants in environments with modest herbivory (population
IA), 241 pairs (80%) survived to produce seed, and of these
surviving pairs, 358 individual plants (74%) lost 20% or more
of their leaf area to herbivores by the first week of July.
The number of mature capsules produced at the end of the
growing season differed significantly within pairs, and the
magnitude and sign of these differences depended on whether
or not the plants had been attacked by herbivores. Overall,
jasmonate-treated plants matured on average 11% more viable
seed (6 capsules or a 349-viable-seed-plant- 1 benefit of
jasmonate-treatment). Of these 241 surviving pairs, both
members of 160 pairs lost 20% or more of their leaf area to
herbivores; in this subset of attacked plant pairs,
Jasmonate-treated plants matured 8 capsules and 537 viable
seeds more than their control counterparts. In 13 pairs, only
the jasmonate-treated member of the pair was similarly
attacked, and in these, viable seed production did not differ
significantly. In 25 pairs, only the control member of the
pair was attacked, and in these pairs, the jasmonate-treated
plants matured on average 35 more capsules and 2848 viable
seeds more than controls (a 58-60% benefit). To summarize, in
populations with an intermediate level of attack,
jasmonate-induced plants had a higher fitness than control
plants. Interestingly, the cost of jasmonate-induction was
also detectable in the 43 pairs in which both members escaped
herbivore attack; jasmonate-treated plants produced on
average 20% less viable seed than did controls (13 fewer
capsules and 1476-viable-seed-plant- 1 cost of
jasmonate-treatment).
This study provides strong support for the contention that
jasmonate-induced responses are examples of adaptive
phenotypic plasticity. By timing their germination and growth
with the post-fire environment, N. attenuata plants exploit a
small phenological window of low herbivore pressure and high
resource availability. However, within this window of
opportunity, the probability of herbivore attack is highly
variable and inducible defenses allow plants to cope with
this variability by altering their defensive phenotype
adaptively. The resistance traits elicted by jasmonates
are costly in terms of seed production, but these costs are
offset by their benefit when the probability of fitness
reductions due to herbivore attack is high. The advances in
understanding the signal transduction pathways that mediate
the defense responses of plants provide ecologists with the
opportunity to rigorously test the costs and benefits of
defenses under natural conditions and provide important
insights into the design of ecologically-benign agricultural
practices.
Journal
Proceedings of the National Academy of Sciences