Bruce A. Kimball
Graduate Degree Program in Ecology
Colorado State University, Ft. Collins, COа 80523
Denver Wildlife Research Center
Denver Federal Center
Denver, COа 80225
No subject in the study of chemical ecology is as unique as the study of
plant defenses.а This uniqueness probably results from the fact that no other area
is so burdened with theory.а The majority of theories have employed growth as the
currency against which trade-offs are measured.а Future theories should be developed
where fitness is not viewed from a plant growth point of view, but rather from a
reproductive view.а Life history affords a foundation for which we can evaluate
plant contributions to future generations as the currency.а
Life history incorporates the pattern of plant development, reproduction, and
mortality.а Inclusion of growth form leads to four strategies: 1) Annuals, 2)
Iteroparous perennial herbs, 3) Iteroparous perennial woody plants, and 4)
Semelparous perennials.а These life history strategies incorporate longevity of
tissues, reproductive strategy, and mortality while not considering environmental
constraints such as resource stress or disturbance.а Thus, induced defenses
resulting from stress or disturbance are considered separate from the evolution of
plant defense strategies.
My hypotheses states that the kind of defenses employed by a plant can be predicted
by its life history traits.а Differences in the defenses employed by annuals versus
woody perennials are derived not from the nature of the environment, but rather by
the organisms' investment to future generations.а Current plant defense theories are
reviewed in the context of their reliance on growth as an indication of fitness.а
The defense strategies of plants as observed through their life histories are also
discussed with the emphasis on long-lived semelparous plants for which little is
The study of plant defense is unique in the field of chemical ecology
in that no other area is so burdened with theory (Berenbaum, 1995).а Ever since the
landmark paper of Fraenkel (1959), scientists have fought to generate theories which
adequately explain the strategies employed by plants to chemically defend
themselves.а The majority of theories have employed physiological models i.e. the
cost of defense is considered a trade-off with growth.а Consideration of optimal
defense (Rhoades, 1979) has added the evolutionary aspect to the generation of plant
defense theory.а However, it is interesting that even in these evolutionary models
the currency is still individual fitness rather than contributions to future
generations.а The question arises, "Is a plant optimizing growth or reproductive
capability with respect to the cost of chemical defense".а I think that we must look
closer at plant life histories to answer this question.
Life history is a term given to the pattern of development, reproduction, and
mortality exhibited by an organism (Crawley, 1986).а MacArthur and Wilson (1967)
offered a linear life history strategy which stated that organisms fall somewhere on
the continuum from growth rate maximizers (r-selected) to competitors (k-selected).а
Grime (1977) noted that environmental stress was not adequately accounted for and
offered a triangular model of plant life history.а Here, a 1:1:1 trade-off was
assumed among a plant's ability to cope with disturbance (ruderal), competition
(competitive), and stress (stress-tolerant).а Through the inclusion of growth form
to life history, Crawley (1986) classified plants by the following strategies: 1)
annuals, 2) iteroparous perennial herbs, 3) iteroparous perennial woody plants, and
4) semelparous perennials.а Note that these life history strategies incorporate
longevity of tissues, reproductive strategy, and mortality.а They do not consider
environmental constraints such as resource stress or disturbance.
Confounding defense theory are the ideas of constitutive versus induced defenses.а I
liken this dichotomy to the notion of importance versus intensity of competition.а
Intensity is clearly a proximate phenomenon.а This is the reductionist view.а On the
other hand, importance considers the evolutionary consequences.а This is a
phenomenological view.а Here, I take a phenomenological view of plant defense and
concur with Perrin (1993) that the optimal organism will seek to maximize
contributions to future generations rather than optimize individual growth.
Plant Defense Theories
While Grime's (1977) plant strategies were not developed with
plant defense strictly in mind, he did note that stress-tolerant plants would be
predicted to be under intense natural selection for developing anti-herbivore
defenses.а However, it is not clear what life history traits are associated with
stress-tolerant plants.а Grime included perennial herbs and woody plants in this
group, but also included these same growth forms in his competitive classification
The prediction that perennial woody plants would select for defense under stressful
environmental conditions is a paramount prediction of the resource availability
hypothesis (RAH).а Coley et al. (1985) noted that the production of defensive
compounds is only favored when the cost of their production is less than the benefit
of increased protection against herbivores.а The RAH predicts that the quantity and
type of defenses produced by plants will be dependent on the availability of the
resources.а Thus, a plant must consider the trade-off of investing in growth versus
investing in defense.а In tropical trees, Coley (1987) noted that this trade-off was
much less for slow growing species.а This observation leads to the prediction that
fast growing trees would invest in the cheapest type of defense while slow growing
trees would benefit from investments in more expensive defense strategies (de Jung,
The relative costs and types of defenses employed by plants were first assessed by
Feeny (1976).а His plant apparency theory has served as a primary paradigm for most
research in this field.а Feeny characterized plants as either "bound to be found"
(apparent) or not predictably distributed (unapparent).а Plants could be
(un)apparent in space and/or time.а Apparency theory predicts that apparent plants
will be defended differently than unapparent ones.а Apparent plants would be
predicted to employ "quantitative" defenses.а Quantitative defenses are dose
dependent compounds which are considered to be costly to produce.а Feeding
deterrents such as tannins, terpenes, and flavanoids are quantitative defenses.а
These defenses are termed "immobile" defenses in the RAH vernacular.а Conversely,
qualitative defenses are the toxins which are lethal in small concentrations and are
thus considered to be less costly to produce than quantitative defenses.а These
types of defenses are known as "mobile" defenses in the RAH.а In addition to plants
being considered (un)apparent, specific plant tissues can be considered (un)apparent
in space and/or time.
Plant apparency theory predicts that long-lived plants (i.e. long-lived tissues) are
temporally apparent and would be highly defended by quantitative defenses.а Feeny
noted the difference in defenses employed by long-lived oak trees which employed
tannins in defense of foliage and the annual mustard which employs toxic
glucosinolates for defense.а However, the vastly different life history strategies
of these plants may account for these differences.
Coley (1987) reconciled the differences between apparency and RAH by employing
Grime's (1977) plant strategies.а She demonstrated that plant apparency works well
when considering ruderal plants, but stress-tolerant and competitive plants seem to
follow the predictions of RAH more closely.а While incorporation of the
environmental constraints allowed Coley to defend RAH, it still does not consider
the contributions to future generations, merely plant response to environmental
Bryant et al. (1983) proposed the carbon-nutrient balance (CNB) theory prior to
Coley's RAH.а The connection is obvious in that the CNB is much more specific about
the roles of carbon allocation and nutrient availability.а This basis of the CNB is
that nutrient deficiencies limit growth more than the rate of photosynthesis.а In
nutrient poor environments, a plant would be expected to decrease its growth yet
photosynthesize at an undiminished rate.а Thus, excess carbon would be available for
the production of carbon-based defenses (e.g. terpenes).а Conversely, when the
carbon:nutrient ratio is reduced, because of diminished light for instance,
production of carbon based defenses would be expected to be reduced.а This theory
has been largely dismissed in favor of RAH because of the observation that increased
carbon supply in woody plants does not necessarily translate into an increase in
production of carbon-based defenses (Lincoln and Couvet, 1989).
The growth-differentiation hypothesis (GDH) was originally proposed by Loomis (1932)
as a strategy for plant growth.а Cell division and enlargement are growth processes
while processes such as maturation and secondary metabolite synthesis are termed
differentiation.а As opposed to the RAH, GDH expresses a genetic trade-off between a
plant's investment in growth and defense.а Again we see the tie-in with availability
of resources.а According to GDH, as resources are limited, cell growth processes are
limited more than differentiation processes.а In other words, the trade-off between
growth and defense is expressed at a plant physiological level as a trade-off
between growth and differentiation processes.а
An evolutionary view sprung from the work of Rhoades and Cates (1976) which was
similar to the idea of plant apparency.а This introduction of plant evolution
suggests that ephemeral (unapparent) plants would be driven to employ divergent
(qualitative) defenses because of pressures exerted by adapting herbivores.а
Similarly, predictable (apparent) plants would employ convergent (quantitative)
defenses.а Thus, Rhoades (1979) presented the optimal defense theory.а Two
hypotheses emerged from this theory, 1) organisms evolve defenses in a manner that
maximize individual fitness, and 2) defenses are costly.а It is from this point that
future models should be developed concerning plant defense theory.а Specifically,
fitness should not be viewed from an individual plant survival view, but rather from
a reproductive view.а Further, induced defenses resulting from environmental stress
or disturbances such as herbivory should be considered separate from the
Annual plants are semelparous with short-lived tissues.а They are
considered to be r-selected plants with the ability for massive reproduction.а
Annuals maximize fitness (contributions to future generations) by early reproduction
(Crawley, 1986).а Thus the important tradeoff is the ability to choose between
growth or early reproduction.а It seems probable that the tradeoff between growth
and defense is not an important driving force for annual plants.а Annuals tend to
allocate more energy to reproduction regardless of the level of available resources
(Mutkainen and Walls, 1995).а Because of the high fecundity of annuals and the
ability of annual seeds to lie dormant for several years, herbivory will have a
relatively low impact on contributions to future generations.а Therefore, it is
predicted that these plants would minimize investments into chemical defenses.
Iteroparous perennial herbs have several evolutionary advantages which maximize
fitness (Crawley, 1986).а First, these plants need not invest resources into
permanent structures which are vulnerable to attack.а Second, is their ability to
"move" in space by employing rhizomes, stolons, or rooting shoots.а Based on these
life history adaptations, iteroparous perennial herbs also will be minimally
impacted by herbivory.а Here too, it is predicted that chemical defense investment
Iteroparous woody plants do not have the advantages of their herbaceous
counterparts.а Woody structures are vulnerable year round and these plants are
unable to "move" in space.а Further, these plants delay investment in reproduction
for several years.а The impact of herbivory on future generations can be great.а
Therefore, iteroparous woody plants are predicted to heavily invest into chemical
defenses, particularly in juvenile stages.
The most unusual of the plant life history strategies is the semelparous perennials.а
This strategy includes the biennials and the extremely rare long-lived semelparous
perennials.а These plants typically are rosettes with large tap roots (Young and
Augspurger, 1991).а At the time of reproduction, massive amounts of resources are
translocated and death occurs following the reproductive event.а This has been
termed the "big bang" strategy (Crawley, 1986).а Semelparity is an evolutionary
strategy which leads to greater fecundity (Schaffer and Schaffer, 1979).а However,
herbivory could greatly impact the ability of these plants to contribute to future
generations.а Here, the prediction is that semelparous perennials, particularly the
long-lived variety, will also invest heavily into plant chemical defenses.
Current literature is rife with examples of the so-called
qualitative defenses employed by annual and perennial herbs.а Examples include the
cardenolides of perennial milkweeds (Brower et al, 1988), the glucosinolates of
annual mustards (Louda and Mole, 1991), furanocoumarins in annual apiaceae
(Berenbaum, 1991) cyanogenic glycosides of numerous herbaceous species (Seigler,
1991) and the alkaloids of many perennials (Robinson, 1979).а However, little work
has been reported on the comparison of defense strategies employed by annual and
perennial herbs.а Mutkainen and Walls (1995) hypothesized that perennials should
show stronger induced responses to herbivory than annual plants.а
The defense strategies of iteroparous woody plants have been frequently reviewed.а
As expected, woody plants invest in costly quantitative defenses (Bryant and
Kuropat, 1980; Bryant et al., 1991; Bryant et al., 1992).а This is particularly true
in juvenile stages when these plants must protect themselves until first
reproduction (Bryant et al., 1991).
Few researchers have investigated the chemical defenses of semelparous perennial
plants.а Bouwmeester, et al. (1995) did compare the defenses of annual vs. biennial
caraway and found greater terpenoid investment in the seeds of the biennial variety.а
Of the long-lived semelparous varieties, Young and Augspurger (1991) identified 40
genera of plants with this life history (Table 1).а Literature review has produced
little as far as investigation into the types of chemical defenses employed.а
Defense in general is not well studied for this life history (Smith and Young
(1987).а However, some interesting work has been conducted.
Stevens et al. (1995a) studied the alkaloid distribution in the family crassulaceae.а
In this study, two genera which have the long-lived semelparous life history,
Aeonium and Kalanchoe, did not contain any of the alkaloids distributed throughout
the iteroparous varieties.а In fact, costly tannins were found in the Kalanchoe
genus.а This is the most compelling evidence that the semelparous life forms may
invest more heavily into chemical plant defense versus their iteroparous
counterparts.а Wink et al. (1995) similarly looked at the distribution of
quinolizidine alkaloids in 56 species of lupine.а While they reported high levels of
alkaloids in lupine species, the lone semelparous species, alopecuroides, was not
Of the so-called quantitative defenses, the phenolics are the largest class of
compounds reported in long-lived semelparous plants.а Flavonoids have been reported
in three genera of the Asteraceae family (Bohm and Fong, 1990) and in the genera
Tillandsia (Cabrera et al., 1995), Agave (Parmar et al., 1992), and Aeonium (Stevens
et al., 1995b).а Finally, other quantitative defense compounds which have also been
identified include saponins from semelparous Agave (Uniyal, et al., 1990) and
monoterpenes in semelparous Hymenoxys (Gao, et al., 1991).
Based on contributions to future generations, it is predicted that
semelparous annual and iteroparous perennial herbs will not make relatively large
investments into constitutive chemical defense.а In fact, prior investigations have
shown that plants with these life histories tend to rely on qualitative defenses.а
These defenses are considered to be "cheap" because they are required in low doses
and can be mobilized throughout the plant.
Conversely, iteroparous woody plants and semelparous perennials are predicted to
invest heavily in constitutive defenses in order to maximize their contributions to
future generations.а Much research has focused on the quantitative defenses employed
by trees and shrubs.а Quantitative defenses are considered to be expensive because
large amounts are required to deter most herbivores.
The defenses of the semelparous perennials have not been well studied.а It seems
logical that plants that store energy (often for decades) for one reproductive event
would invest in quantitative defenses.а Of the work reviewed, it appears as though
plants with this life history do rely on feeding deterrents such as tannins,
flavanoids, and monoterpenes rather than qualitative toxins.
Berenbaum, M.R. 1991. Coumarins. Chapter 6 in G.A. Rosenthal and M.R. Berenbaum
(eds). Herbivores: Their Interactions with Secondary Plant Metabolites.
Academic Press, Sandiego, CA.
Berenbaum, M.R. 1995. The Chemistry of Defense: Theory and Practice. Proc. Nat.
Acad. Sci. USA. 92:2-8.
Bohm, B.A. and Fong, C. 1990. The Nonpolar Flavanoids of Wilkesia and
Argyroxiphium. Phytochemistry. 29(4):1175-1178.
Bouwmeester, H.J.; Davies, J.A.R.; and Toxopeus, H. 1995. Enantiomeric Composition
of Carvone, Limonene, and Carveols in Seeds of Dill and Biennial Caraway
Varieties. J. Agric. Food Chem. 43:3057-3064.
Brower, L.P.; Nelson, C.J.; Seiber, J.N.; Fink, L.S. and Bond, C. 1988. Exaptation
as an Alternative to Coevolution in the Cardenolide-based Chemical Defense of
Monarch Butterflies (Danus plexippus L.) Against Avian Predators. Chapter 15
in K.C. Spencer (ed). Chemical Mediation of Coevolution. Academic Press, San
Bryant, J.P. and Kuropat, P.J. 1980. Selection of Winter Forage by Subarctic
Browsing Vertebrates: The Role of Plant Chemistry. Ann. Rev. Ecol. Syst.
Bryant, J.P.; Chapin III, F.S.; and Klein, D.R. 1983. Carbon/Nutrient Balance of
Boreal Plants in Relation to Vertebrate Herbivory. Oikos 40(3)357-368.
Bryant, J.P., Provenza, F.D., Pastor, J., Reichardt, P.B., Clausen, T.P., and du
Toit, J.T. 1991. Interactions Between Woody Plants and Browsing Mammals
Mediated by Secondary Metabolites. Ann. Rev. Ecol. Syst. 22:431-446.
Bryant, J.P., Reichardt, P.B., and Clausen, T.P. 1992. Chemically Mediated
Interactions Between Woody Plants and Browsing Mammals. J. Range Manage.
Coley, P.D.; Bryant, J.P.; and Chapin III, F.S. 1985. Resource Availability and
Plant Antiherbivore Defense. Science 230(4728):895-899.
Coley. P.D. 1987. Interspecific Variation in Plant Anti-Herbivore Properties: The
Role of Habitat Quality and Rate of Disturbance. New Phytol. 106(Suppl):251-
de Jung, T.J. 1995. Why Fast-Growing Plants do not Bother about Defence. Oikos.
Cabrera, G.M.; Gallo, M.; and Seldes, A.M. 1995. A 3,4,-Seco-cycloartane Derivative
from Tillandsia useneoides. Phytochemistry. 38(1):139-153.
Crawley, M.J. 1986. Life History and Environment. Chapter 8 in M.J. Crawley (ed).
Plant Ecology. Blackwell Scientific Publication, Oxford.
Feeny, P. 1976. Plant Apparency and Chemical Defense, pp 1-40, in J.W. Wallace and
R.L. Nansel (eds). Biological Interactions Between Plants and Insects. Recent
Advances in Phytochemistry, Vol 10. Plenum Press, NY.
Fraenkel, G.S. 1959. The Raison d'Etre of Secondary Plant Substances. Science.
Gao, F.; Wang, H.; Mabry, T.J.; and Jakupovic, J. 1991. Monoterpene glycosides,
sesquiterpene lactone glycoside and sesquiterpene aglycones from Hymenoxys
ivesiana. Phytochemistry. 30(2):553-562.
Grime, J.P. 1977. Evidence for the Existence of Three Primary Strategies in Plants
and Its Relevance to Ecological and Evolutionary Theory. Am. Nat. 111:1169-
Lincoln, D.E. and Couvet, D. 1989. The Effect of Carbon Supply on Allocation to
Allelochemicals and Caterpillar Consumption of Peppermint. Oecologia 78:112-114.
Loomis, W.E. 1932. Growth-Differentiation Balance vs. Carbohydrate-Nitrogen Ratio.
Proc. Am. Soc. Hotic. Sci. 29:240-245.
Louda S. and Mole, S. 1991. Glucosinolates: Chemistry and Ecology. Chapter 4 in
G.A. Rosenthal and M.R. Berenbaum (eds). Herbivores: Their Interactions with
Secondary Plant Metabolites. Academic Press, Sandiego, CA.
MacArthur, R.H. and Wilson, O.E. 1967. The Theory of Island Biogeography.
Princeton University Press, Princeton, NJ.
Mutikainen, P. and Walls, M. 1955. Growth, Reproduction and Defence in Nettles:
Responses to Herbivory Modified by Competition and Fertilization. Oecologia.
Parmar, V.S.; Jha, H.N.; Gupta, A.K.; and Prasad, A.K. 1992. Agamanone, a Flavanone
from Agave americana. Phytochemistry. 31(7):2567-2568.
Perrin, N. 1993. On Future Discounts and Economic Analogy in Life-History Studies.
Funct. Ecol. 7:506-508.
Rhoades, D.F. and Cates, R.G. 1976. Toward a General Theory of Plant Antiherbivore
Chemistry, pp 168-213 in J.W. Wallace and R.L. Nansel (eds). Biological
Interactions Between Plants and Insects. Recent Advances in Phytochemistry,
Vol 10. Plenum Press, NY.
Rhoades, D.F. 1979. Evolution of Plant Chemical Defense Against Herbivores. Chapter
1 in Rosenthal, G.A. and Janzen, D.H. (eds). Herbivores: Their Interaction with
Secondary Plant Metabolites. Academic Press, NY.
Robinson, T. 1979. The Evolutionary Ecology of Alkaloids. Chapter 11 in in
Rosenthal, G.A. and Janzen, D.H. (eds). Herbivores: Their Interaction with
Secondary Plant Metabolites. Academic Press, NY.
Schaffer, W.M. and Schaffer, M.V. 1979. The Adaptive Significance of Variations in
Reproductive Habit in the Agavaceae II: Pollinator Foraging Behavior and Selection
for Increased Reproductive Expenditure. Ecology. 60(5):1051-1069
Seigler, D.S. 1991. Cyanide and Cyanogenic Glycosides. Chapter 2 in G.A. Rosenthal
and M.R. Berenbaum (eds). Herbivores: Their Interactions with Secondary Plant
Metabolites. Academic Press, Sandiego, CA.
Smith, A.P. and Young, T.P. 1987. Tropical Alpine Plant Ecology. Ann. Rev. Ecol.
Syst. 18:137- 158.
Stevens, J.F.; Hart, H.; Van-Ham, R.; Elema, E.T.; Van-Den-Ent, M.; Wildeboer, M.;
and Zwaving, J.H. 1995a. Distribution of Alkaloids and Tannins in the
Crassulaceae. Biochem. Syst. Ecol. 23(2):157-165.
Stevens, J.F.; Hart, T.; and Wollenweber, E. 1995b. The Systematic and Evolutionary
Significance of Exudate Flavanoids in Aeonium. Phytochemistry. 39(4):805-813.
Uniyal, G.C.; Agrawal, P.K.; Thakur, R.S.; and Sati, O.P. 1990. Steroidal
glycosides from Agave cantala. Phytochemistry. 29(3):937-940.
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Young, T.P. and Augspurger, C.K. 1991. Ecology and Evolution of Long-lived
Semelparous Plants. TREE. 6:285-289.
а Table 1.а Long-lived Semelparous plants (after Young and Augspurger, 1991)
а Familyааааааааааааааааааааааааааааааааа Familyа
Acanthaceaeааа Aechmanthera sppааааааааааааа Crassulaceaeаа Aeonium sppаааааааааа
Brillentarsia nitensаааааааааааааааааааааааа Greenovia sppаааааааааа Mimulopsis
solmsiiааааааааааааааааааааа Kalanchoe sppаааааааааа Strobilanthes sppааааааааааааааааааааааааааааааааааа
Epacridaceaeаа Drachophyllum verticallatum Agavaceae Agave sppаааааааааа Furcraea
sppааааааааааааааааа Fabeaceae Lupinus alopecuroidesаааааааааа Yucca whipplei sppааааааааааааааааааааа
Apiaceaeа Tauschia decipiensааааааааааа Gentianaceae ааFrasera speciosaааааааааааааааааааааааааааааааааааааааааааааа
Frasera caroliniensis Apocynaceaeааа Cerberiopsis candelabrumааааааааааааааааааааааааааааааааааа
Gesneriaceaeаа Boea spp Araliaceaeаааа Harmsiopanax ingensааааааааааааааа
Asteraceaeаааа Argyroxiphium sppаааааааааааа Lobeliaceaeааа Lobelia sppаааааааааа
Espeletia floccosaааааааааааааааааааааа Trematolobelia sppаааааааааа Phoenicoseris
sppаааааааааааааааааа Centaurodendron dracenoidesаа Musaceaeа Ensete sppааааааааааааааа
Wilkesia gymnoxiphiumаааааааааа Dendrosereris sppаааааааааааа Orchidaceaeааа Orchis
sppаааааааааа Hymenoxys sppаааааааааа Yunquea tenziiаааааааааа Palmaeааа Corypha sppааааааааааааааааааааааааааааааааааааааааааааа
Plectocomia spp Boraginaceaeаа Echium wildprettiаааааааааааааааааааааааааааааааааааааааааааааааа
Rutaceaeа Spathelia sppааааааа Bromeliaceaeаа Puya sppаааааааааааааааааааааааааа
Sohnreyia excelsiaаааааааааа Tillandsia sppаааааааааааааааааааааааааааааааааааааааааааааа