PLANT DEFENSE AGAINST HERBIVORY

Plants have evolved an enormous array of mechanical and chemical defenses against the animals that eat them. These tools allow plants to survive and reproduce in the same area as herbivores and act to prevent herbivory or at least minimize damage incurred from feeding. Plant defenses include (1) mechanical protection on the surface of the plant, (2) complex polymers that reduce plant digestibility to animals, and (3) toxins that kill or repel herbivores. Plants also have features that enhance the probability of attracting natural enemies to herbivores. Specifically, they emit semiochemicals, odors that attract natural enemies, and provide food and housing to maintain the natural enemies’ presence. Defenses can either be constitutive, always present in the plant, or induced, produced or translocated following damage or stress. A given plant species often has many types of defensive mechanisms, mechanical or chemical, constitutive or induced, which additively allow the plant to escape from herbivores.

1 Types of Plant Defenses
2 History of Plant Defense
3 Plant Defense Hypotheses
4 See also
5 References
6 Further reading

Types of Plant Defenses

Chemical Defenses

Secondary Metabolic Products

Plants contain a wide variety of chemicals known as secondary metabolic products that are not essential in plant metabolism. These chemicals are often by-products in the synthesis of primary metabolic products, and if the plant is considered without reference to other organisms, there is no evident reason why the plant should produce them at all ^[1] . These secondary metabolic products, however, are often produced in large quantity and are metabolically expensive; they must be serving a valuable purpose. Observations of selective feeding by herbivorous insects suggest that the presence of these secondary metabolic products serves as repellents to herbivores ^[2] ^[3]. Secondary metabolic products produced by a plant that influences the behavior, growth, and survival of another species are known as allelochemicals ^[4].

There are several alternative explanations for the presence of allelochemicals in plants. Evidence ^[5] ^[6] suggest that flavonoids and cuticle waxes absorb between 90 – 99% of incoming ultraviolet (UV) radiation in cucumbers and maize, effectively acting as UV shields. Allelochemicals, particularly cuticle waxes, may also prevent undesired water loss and maintain sufficient amounts of water in plants during periods of plant stress and drought. Additionally, allelochemicals may act as storage compounds for essential plant nutrients such as nitrogen and phosphorus.

Qualitative vs. Quantitative Chemical Defenses

Allelochemicals can be characterized as either qualitative or quantitative. Qualitative allelochemicals are toxins that interfere with an herbivore’s metabolism, often by blocking specific biochemical reactions. For instance, alkaloids such as caffeine inhibit DNA and RNA synthesis, cyanogenic glycosides produce hydrogen cyanide (HCN) that blocks cellular respiration, and cardenolides and glucosinolates are emetics (agents that cause vomiting). Qualitative allelochemicals are not dosage dependent and are present in plants in relatively low concentrations (often less than 2% dry weight). These defenses have morphological properties (i.e. water soluble, small molecules, and inexpensive energetically) that facilitate rapid synthesis, transport, and storage. These chemicals are effective against non-adapted specialists and generalist herbivores.

Quantitative allelochemicals are digestibility reducers that make plant cell walls indigestible to animals. Condensed tannins inhibit herbivore digestion by both interfering with proteins and digestive enzymes, and binding to consumed plant proteins and making them more difficult to digest (Van Soest 1982). Silica and lignins, which are both completely indigestible to animals, grind down insect mandibles (appendages necessary for feeding). The effects of quantitative allelochemicals are dosage dependent and the higher these chemicals’ proportion in the herbivore’s diet, the less nutrition animals gain from ingesting plant tissues. Quantitative allelochemicals are present in high concentration in plants (5 – 40% dry weight) and are equally effective against specialist and generalist herbivores. Because they are typically large molecules, these defenses are energetically expensive to produce and maintain, and often take longer than smaller molecules to synthesize and transport.

Morphological Defenses

Plants have many external structural defenses that discourage herbivory. Depending on the herbivore’s physical characteristics (i.e. size and defensive armor), plant structural defenses on stems and leaves can deter, injure, or kill the grazer. Some defensive compounds are produced internally but are released onto the plant’s surface; for example, resins, lignins, silica, and wax cover the epidermis of terrestrial plants and alter the texture of the plant tissue to make its use difficult. A plant’s leaves and stem can be covered with sharp spines or trichomes. Cooper and Owen-Smith (1986) found that plant structural features like spines and thorns reduced feeding by large ungulate herbivores (e.g. kudu, impala, and goats) by restricting the herbivores’ feeding rate. Williams and Gilbert (1981) demonstrated that female butterflies are less likely to lay their eggs on plants that already have butterfly eggs. Several neotropical vines of the genus Passiflora contain physical structures resembling the yellow eggs of Heliconius butterflies on their leaves, thereby mimicking the presence of eggs on their leaves and preventing oviposition (the process of laying eggs; Williams and Gilbert 1981).

Constitutive vs. Induced Defenses

Defenses can further be classified as induced or constitutive. Constitutive defenses are those that are always present in the plant species. There is huge variation in the composition and concentration of constitutive defenses, ranging from mechanical defenses to digestibility reducers and toxins. Most external mechanical protections are built-in defenses (for an exception see Traw and Dawson 2002), and large quantitative defenses are almost all constitutive, in part because they are expensive to produce and difficult to mobilize.

Induced defenses are synthesized at and/or mobilized to the site of attack when a plant is injured. Induced defenses include secondary metabolic products, morphological, and physiological changes. Some defenses induced by damage result in greater resistance to herbivores (Karban et al. 1997). Why these defenses are inducible rather than constitutive is thought to be because increased defensive variability increases the effectiveness of defense (Karban et al. 1997). Karban et al. (1997) demonstrate theoretically that if herbivores can choose among different plants and plant tissues, they may avoid eating plants that have a variety of defenses (i.e. both constitutive and induced), thus possibly favoring defensive variability.

Indirect Defenses

Another category of plant defenses is those features that indirectly protect the plant by enhancing the probability of attracting natural enemies. One such feature is the plant’s ability to give off semiochemicals. Any chemical involved in the chemical interaction between organisms is called a semiochemical. One group of semiochemicals are allelochemics, consisting of allomones, which play a defensive role in interspecific communication, and kairomones, which are used by a higher trophic level for the discovery of food. When a plant is attacked it releases allelochemics that are different from its ratio of volatiles normally produced (Dicke and van Loon 2000). Predators use these volatiles as food cues, attracting them to the damaged plant and leading them to the feeding herbivores. The subsequent removal of herbivores by predators confers a fitness benefit to the plant; this demonstrates the indirect defensive capabilities of semiochemicals. Induced volatiles can also have costs, however, because studies have supported the idea that these volatiles also attract herbivores (Dicke and van Loon 2000).

Plants also provide housing and food items for natural enemies, known as “biotic” defense mechanisms, as a means to maintain the presence of natural enemies. For example, trees from the genus Macaranga are morphologically adapted with thin stem walls to create domatia (housing) for an ant species from the genus Crematogaster, who in turn protects its plant against herbivores (Heil et al. 1997). In addition to housing, this ant species obtains its food exclusively from the food bodies produced by the plant. Similarly, some Acacia tree species have thorns that are swollen at the base, forming a hollowing structure that acts as domatia to their protective ant species. Theses Acacia trees also produce nectar in extrafloral nectaries on their leaves as food for the ants (Young et al. 1997).

History of Plant Defense

It has been known since the late 17th century that plants contain noxious chemicals. These chemicals were used as early insecticides; in 1690, nicotine was extracted from tobacco and used as contact insecticide. In 1773, insect infested plants were treated with nicotine fumigation by heating tobacco and blowing the smoke over the plants (Ware and Whitaker 2004). The important role of secondary plant substances in plant defense was not introduced into the ecological literature until Dethier (1954) and Fraenkel (1959) who suggested that secondary metabolic products are used by plants as defenses against herbivores.

Understanding the variation in plant defense (i.e. phenotypic, genetic, and geographic) has dominated the plant-herbivore interactions literature beginning in the later half of the 20th century. Ehrlich and Raven (1964) investigated patterns of interaction between butterflies and their food plants to document coevolution between two organisms with a close ecological relationship. Patterns of food plant utilization within the plant families of Araliaceae and Umbelliferae led Ehrlich and Raven to conclude that secondary plant substances play a leading role in determining the plant’s palatability and use (Ehrlich and Raven 1964). The optimal defense hypothesis (OD) was developed by Feeny (1976) and Rhoades and Cates (1976, Rhoades 1979) and attempted to explain the pattern and variation in plant defenses in relation to the plant’s risk of attack, value, and cost of production. Mixed results of tests of OD, as well as advances in theory, resulted in the rise of new theories, including the Carbon:Nutrient Balance Hypothesis (Bryant et al. 1983, Tuomi et al. 1988), the Growth Rate Hypothesis (Coley et al. 1985), and the Growth-Differentiation Balance Hypothesis (originally Loomis 1953, reinterpreted by Hermes and Mattson 1992). These hypotheses act as “theoretically bases for recently published studies” (Stamp 2003). While the above-mentioned theories of plant defense are not perfect, they serve as a foundation for understanding patterns in plant defense and as a basis for evolving of new theories.

Plant Defense Hypotheses

One of the main objectives in the study of community ecology is to understand the pattern of plant defense. Several prominent theories developed within the past 30 years, including the Optimal Defense Hypothesis (OD; McKey 1974, Rhoades 1979), the Carbon:Nutrient Balance Hypothesis (CNB; Bryant et al. 1983, Tuomi et al. 1988), the Growth Rate Hypothesis (GR; Coley et al. 1985), and the Growth-Differentiation Balance Hypothesis (GDB; Loomis 1953, Hermes and Mattson 1992), proposed a variety of mechanisms to explain plant defense. Each of these theories will be discussed briefly below (reviewed in Stamp 2003).

Optimal Defense Hypothesis

OD addresses how the expression of defense in a particular plant reflects the defensive threat of that plant (reviewed by Stamp 2003). This hypothesis was originally outlined by McKey (1974) and later elaborated by Rhoades (1979). The pattern of OD can be explained by three main factors, namely risk of attack, value of plant part, and cost of defense.

The first factor is risk: how likely is it that a plant or certain plant parts will be attacked? This idea forms the basis for the Plant Apparency Hypothesis (Feeny 1976), which dictates that plants will invest heavily in broadly effective defenses when they are easily found by herbivores. Examples of these apparent plants include long-living trees, shrubs, and perennial grasses; these plants are protected with quantitative digestibility reducers that impart generalized protections (Feeny 1976). Short-lived plants of early successional stages and other unapparent plants, on the other hand, should invest in small amounts of qualitative toxins that are effective against all but specialist herbivores (Feeny 1976). Qualitative defenses are relatively small molecules and their toxicity is not dosage dependent, so they are expected to be less costly when compared to quantitative defenses (Feeny 1976).

The second factor is value: what is the fitness impact associated with the loss of a given quantity of tissue? Not all plant parts are equally valuable to the plant, and plant parts that more valuable are hypothesized to contain a larger proportion of a plant’s defenses. Similarly, a plant’s stage of development when a particular organ is lost affects the resulting change in fitness. The fitness value of a plant is commonly determined by removing a part of the plant and observing the subsequent fitness effect (McKey 1979, Krishik and Denno 1983). In general, reproductive parts are not as easily replaced as vegetative parts, terminal leaves have greater value than basal leaves, and loss of plant parts mid-season has a more negative effect on fitness as opposed to removal at the beginning or end of the season (Krischik and Denno 1983, Zangerl and Rutledge 1996).

The final tenet is cost: how much does a particular defense cost when considering energy spent and materials allocated? This tenet centers on the fact that defense has a cost and the materials and energy allocated to defense cannot be allocated simultaneously to another function (e.g. reproduction and growth). OD predicts that plants will allocate more energy towards defense when the benefits outweigh the costs, specifically where there is high herbivore pressure (for examples see Pennings et al. 2001).

Carbon:Nutrient Balance Hypothesis

CNB, also known as the Environmental Constraint Hypothesis, attempts to explain the expression of plant defense based on the availability of nutrients in the environment (Bryant et al. 1983, Tuomi et al. 1988). CNB predicts that plants growing on nitrogen-poor soils will use carbon-based defenses (mostly digestibility reducers), while those growing in low carbon environments (such as shady conditions) are more likely to use nitrogen-based toxins. The hypothesis further predicts that if plants are grown in low-nutrient conditions, then these plants will implement a defensive strategy composed of constitutive carbon-based defenses. If these plants are then exposed to nutrients (e.g. through the addition of fertilizers) the carbon-based defenses will be decreased.

Growth Rate Hypothesis

GR, also known as the Resource Availability Hypothesis, explains that the pattern of plant defense is determined by the inherent growth rate of the plant, which is in turn determined by the resources available to the plant. The major assumption made by GR is that resources are the limiting factor in determining the maximum growth rate of a plant species. GR predicts “…the optimal level of defense investment increases as the potential growth rate of the plant decreases” (Coley et al. 1985). Additionally, plants with inherently slow-growth rates that occur in resource-poor areas tend to have long-lived leaves and twigs. This may be because loss of plant appendages translates into a loss of necessary nutrients that are not easily replaced (Chapin III 1980).

Fine et al. (2004) provides a modern support for this hypothesis. In their study, Fine and colleagues conducted a reciprocal transplant study of seedlings of 20 species of trees between clay soils (nutrient rich) and white sand (nutrient poor). Seedlings originating from the nutrient poor white sand had higher levels of constitutive carbon-based defenses. When these seedlings were transplanted into nutrient rich clay soils they experienced higher mortality from herbivory, leading Fine et al. (2004) to conclude that there is a trade-off between growth rate and defense against herbivory that appears to restrict species to one habitat or the other.

Growth-Differentiation Balance Hypothesis

GDB explains the pattern of plant defense as a result of the differing allocation of energy between “growth-related processes” and “differentiation-related processes” in different environments (Loomis 1953, Herms and Mattson 1992). Stamp (2003) defines differentiation-related processes as “those processes that enhance the structure or function of existing cells (i.e. maturation and specialization).” GDB explains that a plant produces chemical defenses when the resources become available as a result of the net gain of energy from photosynthesis. The predictions of GDB include that plants have their highest concentrations of secondary metabolites at intermediate resource availability (Loomis 1953, Herms and Mattson 1992). Wilkens et al. (1996) provides support for this hypothesis through its examination of phenolic content in tomatoes at 4 nitrate levels, where the highest concentration of phenolics were measured at an intermediate nitrate level.

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