Defensive responses of plants

The evolutionary selection pressure exerted by herbivores has led to a variety of plant physical and chemical defenses that resist attack (see Sections

3.7.3 and 3.7.4). These may be present and effective continuously (constitutive defense) or increased production may be induced by attack (inducible defence) (Karban et al., 1999). Thus, production of the defensive hydroxamic acid is induced when aphids (Rhopalo-siphum padi) attack the wild wheat Triticum uniaristatum (Gianoli & Niemeyer, 1997), and the prickles of dewberries on cattle-grazed plants are longer and sharper than those on ungrazed plants nearby (Abrahamson, 1975). Particular attention has been paid to rapidly inducible defenses, often the production of chemicals within the plant that inhibit the protease enzymes of the herbivores. These changes can occur within individual leaves, within branches or throughout whole tree canopies, and they may be detectable within a few hours, days or weeks, and last a few days, weeks or years; such responses have now been reported in more than 100 plant-herbivore systems (Karban & Baldwin, 1997).

There are, however, a number of ... or do they? problems in interpreting these responses

(Schultz, 1988). First, are they 'responses' at all, or merely an incidental consequence of regrowth tissue having different properties from that removed by the herbivores? In fact, this issue is mainly one of semantics - if the metabolic responses of a plant to tissue removal happen to be defensive, then natural selection will favor them and reinforce their use. A further problem is much more substantial: are induced chemicals actually defensive in the sense of having an ecologically significant effect on the herbivores that seem to have induced them? Finally, and of most significance, are they truly defensive in the sense of having a measurable, positive impact on the plant making them, especially after the costs of mounting the response have been taken into account?

Fowler and Lawton (1985) addressed the second problem - 'are the responses harmful to the herbivores?' - by reviewing the effects of rapidly inducible plant defenses and found little clear-cut evidence that they are effective against insect herbivores, despite a widespread belief that they were. For example, they found that most laboratory studies revealed only small adverse effects (less than 11%) on such characters as larval development time and pupal weight, with many studies that claimed a larger effect being flawed statistically, and they argued that such effects may have negligible consequences for field populations. However, there are also a number of cases, many of which have been published since Fowler and Lawton's review, in which the plant's responses do seem to be genuinely harmful to the herbivores. When larch trees were defoliated by the larch budmoth, Zeiraphera diniana, the survival and adult fecundity of the moths were reduced throughout the succeeding 4-5 years as a combined result of delayed leaf production, tougher leaves, higher fiber and resin concentration and lower nitrogen levels (Baltensweiler et al., 1977). Another common response to leaf damage is early abscission ('dropping off') of mined leaves; in the case of the leaf-mining insect Phyllonorycter spp. on willow trees (Salix lasiolepis), early abscission of mined leaves was an important mortality factor for the moths - that is, the herbivores were harmed by the response (Preszler & Price, 1993). As a final example, a few weeks of grazing on the brown seaweed Ascophyllum nodosum by snails (Littorina obtusata) induces substantially increased concentrations of phlorotannins (Figure 9.1a), which reduce further snail grazing (Figure 9.1b). In this case, simple clipping of the plants did not have the same effect as the herbivore. Indeed, grazing by another herbivore, the isopod Idotea granulosa, also failed to induce the chemical defense. The snails can stay and feed on the same plant for long time periods (the isopods are much more mobile), so that induced responses that take time to develop can still be effective in reducing damage by snails.

The final question - 'do plants benefit from their induced defensive responses?' - has proved the most difficult to answer and only a few well designed field studies have been performed (Karban et al., 1999). Agrawal (1998) estimated lifetime fitness of wild radish plants (Raphanus sativus) (as number of seeds produced multiplied by seed mass) assigned to one of three treatments: grazed plants (subject to grazing by the caterpillar of Pieris rapae), leaf damage controls (equivalent amount of biomass removed using scissors) and overall controls (undamaged). Damage-induced responses, both chemical and physical, included increased concentrations of defensive glucosinolates and increased densities of trichomes (hair-like structures). Earwigs (Forficula spp.) and other chewing herbivores caused 100% more leaf damage on the control and artificially leaf-clipped plants than on grazed plants and there were 30% more sucking green peach aphids (Myzus persicae) on the control and leaf-clipped plants (Figure 9.2a, b). Induction of resistance, caused by grazing by the P. rapae caterpillars, significantly increased the lifetime index of fitness by more than 60% compared to the control. However, leaf damage control plants (scissors) had 38% lower fitness than the overall controls, indicating the negative effect of tissue loss without the benefits of induction (Figure 9.2c).

This fitness benefit to wild radish occurred only in environments containing herbivores; in their absence, an induced defensive response was inappropriate and the plants suffered reduced fitness (Karban et al., 1999). A similar fitness benefit has been shown in a field experiment involving wild tobacco (Nicotiana attenuata) (Baldwin, 1998). A specialist consumer of wild tobacco, the catter-pillar of Manduca sexta, is remarkable in that it not only induces an accumulation of secondary metabolites and proteinase inhibitors when it feeds on wild tobacco, but it also induces the plants to plants make defensive responses...

are herbivores really adversely affected?...

... and do plants really benefit?

Ascophyllum Nodosum Benefits Plants

Figure 9.1 (a) Phlorotannin content of Ascophyllum nodosum plants after exposure to simulated herbivory (removing tissue with a hole punch) or grazing by real herbivores of two species. Means and standard errors are shown. Only the snail Littorina obtusata had the effect of inducing increased concentrations of the defensive chemical in the seaweed. Different letters indicate that means are significantly different (P < 0.05). (b) In a subsequent experiment, the snails were presented with algal shoots from the control and snail-grazed treatments in (a); the snails ate significantly less of plants with a high phlorotannin content. (After Pavia & Toth 2000.)

Figure 9.1 (a) Phlorotannin content of Ascophyllum nodosum plants after exposure to simulated herbivory (removing tissue with a hole punch) or grazing by real herbivores of two species. Means and standard errors are shown. Only the snail Littorina obtusata had the effect of inducing increased concentrations of the defensive chemical in the seaweed. Different letters indicate that means are significantly different (P < 0.05). (b) In a subsequent experiment, the snails were presented with algal shoots from the control and snail-grazed treatments in (a); the snails ate significantly less of plants with a high phlorotannin content. (After Pavia & Toth 2000.)

release volatile organic compounds that attract the generalist predatory bug Geocoris pallens, which feeds on the slow moving caterpillars (Kessler & Baldwin, 2004). Using molecular techniques, Zavala et al. (2004) were able to show that in the absence of herbivory, plant genotypes that produced little or no proteinase inhibitor grew faster and taller and produced more seed capsules than inhibitor-producing genotypes. Moreover, naturally occurring genotypes from Arizona that lacked the ability to produce proteinase inhibitors were damaged more, and sustained greater Manduca growth, in a laboratory experiment, compared with Utah inhibitor-producing genotypes (Glawe et al., 2003).

Figure 9.2 (a) Percentage of leaf area consumed by chewing herbivores and (b) number of aphids per plant, measured on two dates (April 6 and April 20) in three field treatments: overall control, damage control (tissue removed by scissors) and induced (caused by grazing of caterpillars of Pieris rapae). (c) The fitness of plants in the three treatments calculated by multiplying the number of seeds produced by the mean seed mass (in mg). (After Agrawal, 1998.)

It is clear from the wild radish and wild tobacco examples that the evolution of inducible (plastic) responses involves significant costs to the plant. We may expect inducible responses to be favored by selection only when past herbivory is a reliable predictor of future risk of herbivory and if the likelihood of herbivory is not constant (constant herbivory should select for a fixed defensive phenotype that is best for that set of conditions) (Karban et al., 1999). Of course, it is not only the costs of inducible defenses that can be set against fitness benefits. Constitutive defenses, such as spines, trichomes or defensive chemicals (particularly in the families Solanaceae and Brassicaceae), also have costs that have been measured (in phenotypes or genotypes lacking the defense) in terms of reductions in growth or the production of flowers, fruits or seeds (see review by Strauss et al., 2002).

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