Evolutionary Plant Defense Strategies: Life Histories and Contributions to Future Generations

Bruce A. Kimball
Graduate Degree Program in Ecology
Colorado State University, Ft. Collins, COа 80523 
Denver Wildlife Research Center
Building 16
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 
of plants.а 
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 
evolutionary concept.
Life Histories
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 
is minimized.
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.
Chemical Defense
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.
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(eds). Herbivores: Their Interactions with Secondary Plant Metabolites. 
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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 
Diego, CA.
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Boreal Plants in Relation to Vertebrate Herbivory. Oikos 40(3)357-368.
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Toit, J.T. 1991. Interactions Between Woody Plants and Browsing Mammals 
Mediated by Secondary Metabolites. Ann. Rev. Ecol. Syst. 22:431-446.
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Interactions Between Woody Plants and Browsing Mammals. J. Range Manage. 
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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 
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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. 
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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.
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Vol 10. Plenum Press, NY. 
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Crassulaceae. Biochem. Syst. Ecol. 23(2):157-165.
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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 
Tachigalia spp
Apiaceaeа Tauschia decipiensааааааааааа Gentianaceae ааFrasera speciosaааааааааааааааааааааааааааааааааааааааааааааа 
Frasera caroliniensis Apocynaceaeааа Cerberiopsis candelabrumааааааааааааааааааааааааааааааааааа 
Gesneriaceaeаа Boea spp Araliaceaeаааа Harmsiopanax ingensааааааааааааааа 
Streptocarpus spp
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 


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