There are four basic strategies plants use to reduce damage by herbivores. One strategy is to escape or avoid herbivores in time or in place, for example by growing in a location where plants are not easily found or accessed by herbivores or by repelling herbivores chemically (also termed non-preference or antixenosis). Another approach is the plant tolerates herbivores, by diverting the herbivore to eat non-essential parts of the plant, or developing an enhanced ability to recover from the damage caused by herbivory. Some plants encourage the presence of natural enemies of herbivores, which in turn protect the plant from herbivores. Finally, plants protect themselves by confrontation; the use of chemical or mechanical defenses, such as toxins that kill herbivores or reduce plant digestibility (also called antibiosis). These defenses can either be constitutive, always present in the plant, or induced, produced in reaction to damage or stress caused by herbivores.
Historically, insects have been the most significant herbivores, and the evolution of land plants is closely associated with the evolution of insects. While most plant defenses are directed against insects, other defenses have evolved that are aimed at vertebrate herbivores, such as birds and mammals. The study of plant defenses against herbivory is important, not only from an evolutionary view point, but also in the direct impact that these defenses have on agriculture, including human and livestock food sources, as well as the in the search for plants of medical importance.
The earliest land plants evolved from aquatic plants around (Ma) in the Ordovician period. These early land plants had no vascular system and required free water for their reproduction. Vascular plants appeared later and their diversification began in the Devonian era (about 400 Ma). Their reduced dependence on water resulted from adaptations such as protective coatings to reduce evaporation from their tissues. Reproduction and dispersal of vascular plants in these dry conditions was achieved through the evolution of specialized seed structures. The diversification of flowering plants (angiosperms) during the Cretaceous period is associated with the sudden burst of speciation in insects. This diversification of insects represented a major selective force in plant evolution, and led to selection of plants that had defensive adaptations. Early insect herbivores were mandibulate and bit or chewed vegetation; but the evolution of vascular plants lead to the co-evolution of other forms of herbivory, such as sap-sucking, leaf mining, gall forming and nectar-feeding.
Our understanding of herbivory in geological time comes from three sources: fossilised plants, which may preserve evidence of defence (such as spines), or herbivory-related damage; the observation of plant debris in fossilised animal faeces; and the construction of herbivore mouthparts.
Long thought to be a Mesozoic phenomenon, evidence for herbivory is found almost as soon as fossils which could show it. Within under 20 million years of the first fossils of sporangia and stems towards the close of the Silurian, around , there is evidence that they were being consumed. Animals fed on the spores of early Devonian plants, and the Rhynie chert also provides evidence that organisms fed on plants using a "pierce and suck" technique. Many plants of this time are preserved with spine-like enations, which may have performed a defensive role before being co-opted to develop into leaves.
During the ensuing 75 million years, plants evolved a range of more complex organs - from roots to seeds. There was a gap of 50 to 100 million years between each organ evolving, and it being fed upon. Hole feeding and skeletonisation are recorded in the early Permian, with surface fluid feeding evolving by the end of that period.
Herbivores depend on plants for food, and have evolved mechanisms to obtain this food despite the evolution of a diverse arsenal of plant defenses. Herbivore adaptations to plant defense have been likened to offensive traits and consist of adaptations that allow increased feeding and use of a host plant. Relationships between herbivores and their host plants often results in reciprocal evolutionary change, called co-evolution. When an herbivore eats a plant it selects for plants that can mount a defensive response. In cases where this relationship demonstrates specificity (the evolution of each trait is due to the other), and reciprocity (both traits must evolve), the species are thought to have co-evolved. The "escape and radiation" mechanism for co-evolution presents the idea that adaptations in herbivores and their host plants have been the driving force behind speciation, and have played a role in the radiation of insect species during the age of angiosperms. Some herbivores have evolved ways to hijack plant defenses to their own benefit, by sequestering these chemicals and using them to protect themselves from predators.
Induced defenses include secondary metabolic products, as well as morphological and physiological changes. An advantage of inducible, rather than constitutive defenses, is that increased variability increases the effectiveness of the defenses. This advantage comes from the suggestion that if herbivores can choose among different plants and plant tissues, they may avoid eating plants that have both constitutive and induced defenses.
The evolution of chemical defenses in plants is linked to the emergence of chemical substances that are not involved in the essential photosynthetic and metabolic activities. These substances, secondary metabolites, are organic compounds that are not directly involved in the normal growth, development or reproduction of organisms, and often produced as by-products during the synthesis of primary metabolic products. These secondary metabolites play a major role in defenses against herbivores.
Secondary metabolites are often characterized as either qualitative or quantitative. Qualitative metabolites are defined as toxins that interfere with an herbivore’s metabolism, often by blocking specific biochemical reactions. Qualitative chemicals are present in plants in relatively low concentrations (often less than 2% dry weight), and are not dosage dependent. These defenses have morphological properties (i.e. water soluble, small molecules, and are energetically inexpensive) that facilitate rapid synthesis, transport, and storage. These chemicals are effective against non-adapted specialists and generalist herbivores.
Quantitative chemicals are those that are present in high concentration in plants (5 – 40% dry weight) and are equally effective against all specialists and generalist herbivores. Most quantitative metabolites are digestibility reducers that make plant cell walls indigestible to animals. The effects of quantitative metabolites are dosage dependent and the higher these chemicals’ proportion in the herbivore’s diet, the less nutrition the herbivore can gain from ingesting plant tissues. Because they are typically large molecules, these defenses are energetically expensive to produce and maintain, and often take longer than smaller, qualitative chemicals to synthesize and transport, therefore these chemicals are expected to serve an important purpose within the plant.
Alkaloids are derived from various amino acids. Over 3000 known alkaloids exist, examples include nicotine, caffeine, morphine, colchicine, ergolines, strychnine, and quinine. Alkaloids have pharmacological effects on humans and other animals. Some alkaloids can inhibit or activate enzymes, or alter carbohydrate and fat storage by inhibiting the formation phosphodiester bonds involved in their breakdown. Certain alkaloids bind to nucleic acids and can inhibit synthesis of proteins and affect DNA repair mechanisms. Alkaloids can also affect cell membrane and cytoskeletal structure causing the cells to weaken, collapse, or leak, and can affect nerve transmission. Cyanogenic glycosides become toxic when they are broken down by enzymes in the herbivore's digestive tract and release hydrogen cyanide or prussic acid, which blocks cellular respiration. Glucosinolates can cause gastroenteritis, salivation, diarrhea, and irritation of the mouth.
The terpenoids, sometimes referred to as isoprenoids, are organic chemicals similar to terpenes, derived from five-carbon isoprene units. There are over 10,000 known types of terpenoids. Most are multicyclic structures which differ from one another in both functional groups, and in basic carbon skeletons. Monoterpenoids, continuing 2 isoprene units, are volatile essential oils such as citronella, limonene, menthol, camphor, and pinene. Diterpenoids, 4 isoprene units, are widely distributed in latex and resins, and can be quite toxic. Diterpenes are responsible for making Rhododendron leaves poisonous. Plant steroids and sterols are also produced from terpenoid precursors, including vitamin D, glycosides (such as digitalis) and saponins (which lyse red blood cells of herbivores).
Phenolics, sometimes called phenols, consist of an aromatic 6-carbon ring bonded to a hydroxy group. Some phenols have antiseptic properties, while others disrupt endocrine activity. Phenolics range from simple tannins to the more complex flavonoids that give plants much of their red, blue, yellow, and white pigments. Complex phenolics called polyphenols are capable of producing many different types of effects on humans, including antioxidant properties. Some examples of phenolics used for defense in plants are: lignin, silymarin and cannabinoids. Condensed tannins, polymers composed of 2 to 50 (or more) flavonoid molecules, inhibit herbivore digestion by binding to consumed plant proteins and making them more difficult for animals to digest, and by interfering with protein absorption and digestive enzymes. Silica and lignins, which are completely indigestible to animals, grind down insect mandibles (appendages necessary for feeding).
In addition to the three larger groups of substances mentioned above, fatty acid derivates, amino acids and even peptides are used as defence. The cholinergic toxine, cicutoxin of water hemlock, is an polyyne derived from the fatty acid metabolism. β-N-Oxalyl-L-α,β-diaminopropionic acid as simple amino acid is used by the sweet pea which leads also to intoxication in humans. The synthesis of fluoroacetate in several plants is an example for the use of small molecules to disturb the metabolism of the herbivore, in this case the citric acid cycle.
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. The leaves of holly plants, for instance, are very smooth and slippery making feeding difficult. Some plants produce gummosis or sap that traps insects.
A plant's leaves and stem may be covered with sharp spines or trichomes- hairs on the leaf often with barbs, sometimes containing irritants or poisons. Plant structural features like spines and thorns reduce feeding by large ungulate herbivores (e.g. kudu, impala, and goats) by restricting the herbivores' feeding rate, or by wearing down the molars as in pears. The structure of a plant, its branching and leaf arrangement may also be evolved to reduce herbivore impact. The shrubs of New Zealand have evolved special wide branching adaptations believed to be a response to browsing birds such as the moas. Similarly, African Acacias have dense thorns on the outside, but none in the middle of the crown, which is comparatively safe from herbivores such as giraffes. Young Acacias, which would be vulnerable due to their proximity to the ground, display a profusion of thorns gradually decreasing with age.
Trees such as coconut and other palms, may protect their fruit by multiple layers of armour, needing efficient tools to break through to the seed contents, and special skills to climb the tall and relatively smooth trunk.
This response lowers the surface area available to herbivores, which are presented with the underside of each leaflet, and results in a wilted appearance. It may also physically dislodge small herbivores, such as insects. Thigmonasty is not only useful in discouraging herbivores, however. For instance the venus flytrap makes use of it to catch its own food.
Plants also provide housing and food items for natural enemies of herbivores, known as “biotic” defense mechanisms, as a means to maintain their presence. For example, trees from the genus Macaranga have adapted their thin stem walls to create ideal housing for an ant species (genus Crematogaster), which, in turn, protects the plant from herbivores. In addition to providing housing, the plant also provides the ant with its exclusive food source; from the food bodies produced by the plant. Similarly, some Acacia tree species have developed thorns that are swollen at the base, forming a hollowing structure that acts as housing. Theses Acacia trees also produce nectar in extrafloral nectaries on their leaves as food for the ants.
Most plants have endophytes, microbial organisms that live within them. While some cause disease, others protect plants from herbivores and pathogenic microbes. Endophytes can help the plant by producing toxins harmful to other organisms that would attack the plant, such as alkaloid producing fungi which are common in grasses such as tall fescue (Festuca arundinacea).
There have been suggestions that leaf shedding may be a response that provides protection against diseases and certain kinds of pests such as leaf miners and gall forming insects. Other responses such as the change of leaf colours prior to fall have also been suggested as adaptations that may help undermine the camouflage of herbivores. Autumn leaf color has also been suggested to act as an honest warning signal of defensive commitment towards insect pests that migrate to the trees in autumn.
The first factor determining optimal defense is risk: how likely is it that a plant or certain plant parts will be attacked? This is also related to the plant apparency hypothesis, which states that a plant will invest heavily in broadly effective defenses when the plant is easily found by herbivores. Examples of apparent plants that produce generalized protections include long-living trees, shrubs, and perennial grasses. Unapparent plants, such as short-lived plants of early successional stages, on the other hand, preferentially invest in small amounts of qualitative toxins that are effective against all but the most specialized herbivores.
The second factor is the value of protection: would the plant be less able to survive and reproduce after removal of part of its structure by a herbivore? Not all plant parts are of equal evolutionary value, thus valuable parts contain more defenses. A plant’s stage of development at the time of feeding also affects the resulting change in fitness. Experimentally, the fitness value a plant structure is determined by removing that part of the plant and observing the effect. In general, reproductive parts are not as easily replaced as vegetative parts, terminal leaves have greater value than basal leaves, and the loss of plant parts mid-season has a greater negative effect on fitness than removal at the beginning or end of the season. Seeds in particular tend to be very well protected. For example, the seeds of many edible fruits and nuts contain cyanogenic glycosides such as amygdalin. This results from the need to balance the effort needed to make the fruit attractive to animal dispersers while ensuring that the seeds are not destroyed by the animal.
The final consideration is cost: how much will a particular defensive strategy cost a plant in energy and materials? This is particularly important, as energy spent on defense cannot be used for other functions, such as reproduction and growth. The optimal defense hypothesis predicts that plants will allocate more energy towards defense when the benefits of protection outweigh the costs, specifically in situations where there is high herbivore pressure.
A recent test of this model involved a reciprocal transplants of seedlings of 20 species of trees between clay soils (nutrient rich) and white sand (nutrient poor) to determine whether trade-offs between growth rate and defenses restrict species to one habitat. Seedlings originating from the nutrient-poor sand had higher levels of constitutive carbon-based defenses, but when they were transplanted into nutrient-rich clay soils, they experienced higher mortality from herbivory. These finding suggest that defensive strategies limit the habitats of some plants.
Fresh growth of grass is sometimes high in prussic acid content and can cause poisoning of grazing livestock. The production of cyanogenic chemicals in grasses is primarily a defense against herbivores.
The human innovation of cooking may have been particularly helpful in overcoming many of the defensive chemicals of plants. Many enzyme inhibitors in cereal grains and pulses, such as trypsin inhibitors prevalent in pulse crops, are denatured by cooking, making them digestible.
It has been known since the late 17th century that plants contain noxious chemicals which are avoided by insects. These chemicals have been used by man as early insecticides; in 1690 nicotine was extracted from tobacco and used as a contact insecticide. In 1773, insect infested plants were treated with nicotine fumigation by heating tobacco and blowing the smoke over the plants. The flowers of Chrysanthemum species contain pyrethrin which is a potent insecticide. In later years, the applications of plant resistance became an important area of research in agriculture and plant breeding, particularly because they can serve as a safe and low-cost alternative to the use of pesticides. The important role of secondary plant substances in plant defense was described in the late 1950s by Vincent Dethier and G.S. Fraenkel. The use of botanical pesticides is widespread and notable examples include Azadirachtin from the neem (Azadirachta indica), d-Limonene from Citrus species, Rotenone from Derris, Capsaicin from Chili Pepper and Pyrethrum.
The selective breeding of crop plants often involves selection against the plant's intrinsic resistance strategies. This makes crop plant varieties particularly susceptible to pests unlike their wild relatives. In breeding for host-plant resistance, it is often the wild relatives that provide the source of resistance genes. These genes are incorporated using conventional approaches to plant breeding, but have also been augmented by recombinant techniques, which allow introduction of genes from completely unrelated organisms. The most famous transgenic approach is the introduction of genes from the bacterial species, Bacillus thuringiensis, into plants. The bacterium produces proteins that, when ingested, kill lepidopteran caterpillars. The gene encoding for these highly toxic proteins, when introduced into the host plant genome, confers resistance against caterpillars, when the same toxic proteins are produced within the plant. This approach is controversial, however, due to the possibility of ecological and toxicological side effects.
Many currently available pharmaceuticals are derived from the secondary metabolites plants use to protect themselves from herbivores, including opium, aspirin, cocaine, and atropine. These chemicals have evolved to affect the biochemistry of insects in very specific ways. However, many of these biochemical pathways are conserved in vertebrates, including humans, and the chemicals act on human biochemistry in ways similar to that of insects. It has therefore been suggested that the study of plant-insect interactions may help in bioprospecting.
There is evidence that humans began using plant alkaloids in medical preparations as early as 3000 B.C. Although the active components of most medicinal plants have been isolated only recently (beginning in the early 19th century) these substances have been used as drugs throughout the human history in potions, medicines, teas and as poisons. For example, to combat herbivory by the larvae of some Lepidoptera species, Cinchona trees produce a variety of alkaloids, the most familiar of which is quinine. Quinine is extremely bitter, making the bark of the tree quite unpalatable, it is also an anti-fever agent, known as Jesuit's bark, and is especially useful in treating malaria.
Throughout history mandrakes (Mandragora officinarum) have been highly sought after for their reputed aphrodisiac properties. However, the roots of the mandrake plant also contain large quantities of the alkaloid scopolamine, which, at high doses, acts as a central nervous system depressant, and makes the plant highly toxic to herbivores. Scopolamine was later found to be medicinal use in pain management before and during labor; in smaller doses it is used to prevent motion sickness. One of the most well-known medicinally valuable terpenes is an anticancer drug, taxol, isolated from the bark of the Pacific yew, Taxus brevifolia, in the early 1960s.