Introduction

Biological control of plant pests involves the use of natural enemies to control arthropods that in turn are enemies of the plant. Classic theory on biocontrol focused on density-dependent interactions between natural enemies and plant pests (Hassell 1978), but largely ignored a role for the plant other than directly affecting the growth rate of the plant pest (i.e., resulting from nutritional quality and direct anti-herbivore defence of the plant). That the plant’s role goes far beyond setting the growth rate of the herbivore was realized much later. Prompted by a seminal review by Price et al. (1980), an avalanche of research now shows the multifarious ways in which plants influence the effectiveness of natural enemies against plant pests and the vulnerability of these pest organisms to their enemies. Such effects on the herbivore’s predators may arise from constitutive investment by the plant, or from versatile investments induced by herbivory. Thus, herbivore-induced changes in the state of the plant may directly and indirectly, i.e., via predators, affect herbivores (Dicke and Sabelis 1988; Turlings et al. 1995; Karban and Baldwin 1997). To the best of our knowledge, predators do not change the state of plants, but they can induce changes in behaviour and life history of herbivores, thereby indirectly affecting the plant (Schmitz et al. 2004). Moreover, herbivorous arthropods may foresee predation risk and avoid predator-occupied plants in response to chemical alarm from herbivores under attack (Janssen et al. 1998; Pallini et al. 1999; Nomikou et al. 2003; Lee et al. 2011). Taken together, tritrophic systems of arthropods on plants are replete with trait changes induced by organisms at adjacent trophic levels and with effects cascading across all trophic levels. Such indirect effects become ever more complex in multispecies food webs because they arise whenever there are more than two species (Werner and Peacor 2003). One example is competition between plant pest species, which not only directly compete for food or by interference, but may also compete indirectly via the plant’s defence response and via responses of shared and non-shared predators.

Introduction

Herbivory by arthropods induces a wealth of changes in the primary and secondary chemistry of plants (Karban and Baldwin 1997, Constabel 1999, Agrawal et al. 1999, Kessler and Baldwin 2002). These chemical changes in turn do not only affect the inducer, but also other herbivore species attacking the induced plant (Denno et al. 1995, Denno and Kaplan Chapter 2 this volume). This effect of one herbivore species on other herbivores is called “indirect,” because it can only arise via the plant as an intermediate organism (Wootton 1994). Moreover, it is called trait-mediated, because the immediate effect of herbivory is an induced change in plant quality, not in plant quantity (Werner and Peacor 2003, Schmitz et al. 2004).

The herbivore-induced state of plants may influence the community of arthopods that live on them. When the induced plant allocates much of its energy in compensatory growth or defense specifically aimed at the inducer, other herbivore species may profit from the increased nutritional quality or weakened defense of the plant, thereby giving rise to interspecific aggregations of herbivores on individual plants (Denno et al. 1995). If, however, the induced plant mounts a sufficiently generalized defense, the plant becomes “vaccinated” against attack by other herbivores, leading to species-poor communities of herbivorous arthropods on the plant (Karban and Baldwin 1997). Much the same reasoning applies to herbivore genotypes within a single species.

Behind the idle and quiet appearance of plants, warfare is an everyday issue. Herbivorous arthropods, below- and aboveground, continue to threaten a plant's existence, whereas their attack is countered by the plant in many ways. Plants defend themselves directly by modifying plant structure (e.g., cuticle thickness, leaf hairiness), lowering nutritional quality, decreasing digestibility and increasing toxicity, but also indirectly by promoting the effectiveness of enemies of the herbivores (Price et al. 1980). This indirect plant defense implies that plants provide chemical lures, shelter and/or food, whereas they gain protection in exchange (Sabelis et al. 1999a, b, c, d, 2002). Central American Acacia trees stand out as a landmark example (Janzen 1966). They have stipular thorns that are expanded and hollow and provide nesting sites for certain ants. In addition, they secrete nectar from large foliar nectaries and produce nutritive organs called Beltian bodies on the leaf pinnules. These food bodies are eagerly harvested by foraging ants and fed to their larvae. The ants in turn kill insect herbivores, repel mammalian herbivores, and destroy plants interfering with the Acacia tree. In this chapter, we focus on food provisioning as a strategy of the plant to boost the third trophic level and we discuss the conditions under which this particular mode of defense is favored by natural selection.

The argument that plants benefit from consumers of the foods they provide dates back to Thomas Belt in his book published in 1874.

Introduction

Why do plants cover the earth and give the world a green appearance? This question is not as trivial as it might seem at first sight. Hairston et al. (1960) hypothesized that herbivores cannot ransack the earth of its green blanket because they are kept low in number by predators. They tacitly ignored the possibility that plants defend themselves directly against a suite of herbivores and together exhibit such great diversity in defense mechanisms that “super” herbivores able to master all plant defenses did not evolve and those that overcome the defenses of some plants are limited by the availability of these plants. Strong et al. (1984) recognized both possibilities in their review on the impact of herbivorous arthropods on plants, but they also favored the view that predators suppress the densities of herbivores, and thereby reduce the threat of plants being eaten.

The two explanatory mechanisms (plant defense versus predator impact), however, may well act in concert. Ever since the seminal review paper by Price et al. (1980) ecologists have become increasingly aware that plant defenses include more than just trickery to reduce the herbivore's capacity for (population) growth. For example, the plant may provide facilities to promote the foraging success of the herbivore's enemies. This form of defense is termed indirect as opposed to direct defense against herbivores.

Introduction

Populations of arthropod herbivores may show periodical outbreaks, large amplitude cycles, strongly bounded fluctuations or stable equilibria. At small spatial scales they may also show dynamics different from those at large spatial scales, and they may even go extinct. There is a need to experimentally test models predicting the dynamical consequences of the mechanisms underlying these patterns. In particular, what needs an explanation is the observation that plants retain a green appearance despite attacks by herbivores (Hairston et al., 1960; Strong et al., 1984). There are two possible explanations: (i) plants defend themselves effectively against herbivores, (ii) predators suppress herbivore populations to very low levels. Hairston et al. (1960) tacitly ignored the first and emphasized the latter in formulating their so-called ‘the world is green’ hypothesis. The two explanatory mechanisms, however, are not mutually exclusive; the plant may promote predator foraging success and the herbivore's enemies may use the facilities offered by the plant.

Price et al. (1980) stimulated a growing awareness that plants may defend themselves both directly against herbivorous arthropods and indirectly by promoting natural enemies, for example, by providing protection, food, and alarm signals to the enemies of the herbivore. Direct defenses include plant structures that hinder feeding by the herbivore, and secondary plant compounds that inhibit digestion, intoxicate the herbivore or deter feeding. Before Price et al. (1980) appeared, examples of indirect defenses were already well-known from ant–plant interactions (Janzen, 1966; Bentley, 1977; see also historical reviews by Beattie, 1985, and Jolivet, 1996).