Evolutionary Plant Defense
Strategies: Life Histories and Contributions to Future Generations
Bruce A. KimballGraduate Degree Program in EcologyColorado State University, Ft. Collins, COа 80523 USDA/APHIS/ADCDenver Wildlife Research CenterBuilding 16Denver Federal CenterDenver, COа 80225 ABSTRACTNo 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 known. Introduction 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, 1995). 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 stochasticity. 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 investigated.а 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). Summary 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. REFERENCES 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. 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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