Chemical defenses

The plant kingdom is very rich in chemicals that apparently play no role in the normal pathways of plant biochemistry. These 'secondary' chemicals range from simple molecules like oxalic acid and cyanide to the more complex glu-cosinolates, alkaloids, terpenoids, saponins, flavonoids and tannins (Futuyma, 1983). Many of these have been shown to be toxic to a wide range of potential consumers. For example, populations of white clover, Trifolium repens, are commonly polymorphic for the ability to release hydrogen cyanide when the tissues are attacked. Plants that lack the ability to generate hydrogen cyanide are eaten by slugs and snails: the cyanogenic forms are nibbled but then rejected. Many researchers have assumed that coevolution seeds: dissipation or protection secondary chemicals: protectants?

protection against consumers has provided the selective pressure favoring the production of such chemicals. Many others, however, have questioned whether the selective force of herbivory is powerful enough for this (their production may be costly to the plants in terms of essential nutrients) and have pointed to other properties that they possess: for example as protectants against ultraviolet radiation (Shirley, 1996). None the less, in the few cases where selection experiments have been carried out, plants reared in the presence of consumers have evolved enhanced defenses against these enemies, relative to control plants reared in the absence of consumers (Rausher, 2001). Later, in Chapter 9 when we look in more detail at the interaction between predators and their prey, we will look at the costs and benefits of prey (especially plant) defense to both the prey itself and its consumers. Here, we focus more on the nature of those defenses.

If the attentions of herbivores select for plant defensive chemicals, then equally, those chemicals will select for adaptations in herbivores that can overcome them: a classic coevolutionary 'arms race'. This, though, suggests that plants should become ever more noxious and herbivores ever more specialized, leaving unanswered the question of why there are so many generalist herbivores, capable of feeding from many plants (Cornell & Hawkins, 2003). An answer has been suggested by 'apparency theory' (Feeny, 1976; Rhoades & Cates, 1976). This is based on the observation that noxious plant chemicals can be classified broadly into two types: (i) toxic (or qualitative) chemicals, which are poisonous even in small quantities; and (ii) digestion-reducing (or quantitative) chemicals, which act in proportion to their concentration. Tannins are an example of the second type. They bind proteins, rendering tissues such as mature oak leaves relatively indigestible. The theory further supposes that toxic chemicals, by virtue of their specificity, are likely to be the foundation of an arms race, requiring an equally simple and specific response from a herbivore; whereas chemicals that make plants generally indigestible are much more difficult to overcome.

Apparency theory then proposes that relatively short-lived, ephemeral plants (said to be 'unapparent') gain a measure of protection from consumers because of the unpredictability of their appearance in space and time. They therefore need to invest less in defense than predictable, long-lived ('apparent') species like forest trees. Moreover, the apparent species, precisely because they are apparent for long, predictable periods to a large number of herbivores, should invest in digestion-reducing chemicals that, while costly, will afford them broad protection; whereas unapparent plants should produce toxins since it is only likely to pay a few specialist species to coevolve against them.

Apparency theory, incorporating ideas on coevolution, therefore makes a number of predictions (Cornell & Hawkins, 2003). The most obvious is that more unapparent plants are more likely to be protected by simple, toxic compounds than by more complex, digestion-inhibiting compounds. This can even be seen in the changing balance of chemical defense in some plants as the season progresses. For example, in the bracken fern (Pteridium aquil-inum), the young leaves that push up through the soil in spring are less apparent to potential herbivores than the luxuriant foliage in late summer. The young leaves are rich in cyanogenic glucosinolates, whilst the tannin content steadily increases in concentration to its maximum in mature leaves (Rhoades & Cates, 1976).

A more subtle prediction of the theory is that specialist herbivores, having invested evolutionarily in overcoming particular chemicals, should perform best when faced with those chemicals (compared to chemicals they would not normally encounter); whereas generalists, having invested in performing well when faced with a wide range of chemicals, should perform least well when faced with chemicals that have provoked coevolutionary responses from specialists. This is supported by an analysis of a wide range of data sets for insect herbivores fed on artificial diets with added chemicals (892 insect/chemical combinations) shown in Figure 3.25.

Furthermore, plants are predicted to differ in their chemical defenses not only from species to species but also within an individual plant. 'Optimal defense theory' predicts that the more important an organ or tissue is for an organism's fitness, the better protected it will be; and in the present context, it predicts that more important plant parts should be protected by constitutive chemicals (produced all the time), whereas less important parts should rely on inducible chemicals, only produced in response to damage itself, and hence with far lower fixed costs to the plants (McKey, 1979; Strauss et al., 2004). This is confirmed, for example, by a study of wild radish, Raphanus sativus, in which plants were either subjected to herbivory by caterpillars of the butterfly, Pieris rapae, or left as unmanipulated controls (Strauss et al., 2004). Petals (and all parts of the flower) are known in this insect-pollinated plant to be highly important to fitness. Concentrations of protective glucosinolates were twice as high in petals as in undamaged leaves, and these levels were maintained constitutively, irrespective of whether the petals were damaged by the caterpillars (Figure 3.26). Leaves, on the other hand, have a much less direct influence on fitness: high levels of leaf damage can be sustained without any measurable effect on reproductive output. Constitutive levels of glucosinolates, as already noted, were low; but if the leaves were damaged the (induced) concentrations were even higher than in the petals.

Similar results were found for the brown seaweed, Sargassum filipendula, where the holdfast at its base was the most valuable tissue: without it the plant would be cast adrift in the water (Taylor et al., 2002). This was protected by costly constitutive, quantitative chemicals, whereas the much less valuable youngest stipes (effectively stems) near the tip of the plant were protected only by toxic chemicals induced by grazing.

apparency theory optimal defense theory: constitutive and inducible defenses

Figure 3.25 Combining data from a wide range of published studies, herbivores were split into three groups: 1, specialists (feeding from one or two plant families), 2, oligophages (3-9 families) and 3, generalists (more than nine families). Chemicals were split into two groups: (a) those that are, and ( b) those that are not, found in the normal hosts of specialists and oligophages. With increasing specialization, (a) herbivores suffered decreased mortality on chemicals that have not provoked a coevolutionary response from specialist herbivores, but (b) suffered higher mortality on chemicals that have not provoked such a response. Regressions: (a) y = 0.33x — 1.12; r2 = 0.032; t = 3.25; P = 0.0013; (b) y = 0.93 — 0.36x; r2 = 0.049; t = —4.35; P < 0.00001. (After Cornell & Hawkins, 2003.)

8 30

S3 20 jj

U Undamaged U Damaged i. I

Petal

Leaf

Figure 3.25 Combining data from a wide range of published studies, herbivores were split into three groups: 1, specialists (feeding from one or two plant families), 2, oligophages (3-9 families) and 3, generalists (more than nine families). Chemicals were split into two groups: (a) those that are, and ( b) those that are not, found in the normal hosts of specialists and oligophages. With increasing specialization, (a) herbivores suffered decreased mortality on chemicals that have not provoked a coevolutionary response from specialist herbivores, but (b) suffered higher mortality on chemicals that have not provoked such a response. Regressions: (a) y = 0.33x — 1.12; r2 = 0.032; t = 3.25; P = 0.0013; (b) y = 0.93 — 0.36x; r2 = 0.049; t = —4.35; P < 0.00001. (After Cornell & Hawkins, 2003.)

Animals have more options than plants when it comes to defending themselves, but some still make use of chemicals. For example, defensive secretions of sulfuric acid of pH 1 or 2 occur in some marine gastropod groups, including the cowries. Other animals that can tolerate the chemical defenses of their plant food, store and use them in their own defense. A classic example is the monarch butterfly (Danaus plexippus), whose caterpillars feed on milkweeds (Asclepias spp.). Milkweeds contain secondary chemicals, cardiac glycosides, which affect the vertebrate heartbeat and are poisonous to mammals and birds. Monarch caterpillars can store the poison, and it is still present in the adults, which in consequence are completely unacceptable to bird predators. A naive blue jay (Cyanocitta cristata) (i.e. one that has not tried a monarch

Figure 3.26 Concentrations of glucosinolates (|lg mg—1 dry mass) in the petals and leaves of wild radish, Raphanus sativus, either undamaged or damaged by caterpillars of Pieris rapae. Bars are standard errors. (After Strauss et al., 2004.)

butterfly before) will vomit violently after eating one, and once it recovers will reject all others on sight. In contrast, monarchs reared on cabbage are edible (Brower & Corvino, 1967).

Chemical defenses are not equally effective against all consumers. Indeed, what is unacceptable to most animals may be the chosen, even unique, diet of others. It is, after all, an inevitable consequence of having evolved resistance to a plant's defenses that a consumer will have gained access to a resource unavailable to most (or all) other species. For example, the tropical legume Dioclea metacarpa is toxic to almost all insect species because it contains a nonprotein amino acid, L-canavanine, which insects incorporate into their proteins in place of arginine. But a species of bruchid beetle, Caryedes brasil-iensis, has evolved a modified tRNA synthetase that distinguishes between L-canavanine and arginine, and the larvae of these beetles feed solely on D. metacarpa (Rosenthal et al., 1976).

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