Tritrophic interactions in plant defense against herbivory describe the ecological impacts of three trophic levels on each other: the plant, the herbivore, and its natural enemies. They may also be called multitrophic interactions when further trophic levels, such as soil microbes, endophytes, or hyperparasitoids (higher-order predators) are considered. Tritrophic interactions join pollination and seed dispersal as vital biological functions which plants perform via cooperation with animals.
Natural enemies—predators, pathogens, and parasitoids that attack plant-feeding insects—can benefit plants by hindering the feeding behavior of the harmful insect. It is thought that many plant traits have evolved in response to this mutualism to make themselves more attractive to natural enemies. This recruitment of natural enemies functions to protect against excessive herbivory and is considered an indirect plant defense mechanism. Traits attractive to natural enemies can be physical, as in the cases of domatia and nectaries; or chemical, as in the case of induced plant volatile chemicals that help natural enemies pinpoint a food source.
Humans can take advantage of tritrophic interactions in the biological control of insect pests.
Chemical mechanisms of enemy attraction
Plants produce secondary metabolites known as allelochemicals. Rather than participating in basic metabolic processes, they mediate interactions between a plant and its environment, often attracting, repelling, or poisoning insects. They also help produce secondary cell wall components such as those that require amino acid modification.
In a tritrophic system, volatiles, which are released into the air, are superior to surface chemicals in drawing foraging natural enemies from afar. Plants also produce root volatiles which will drive tritrophic interactions between below-ground herbivores and their natural enemies. Some plant volatiles can be smelled by humans and give plants like basil, eucalyptus, and pine their distinctive odors. The mixture and ratios of individual volatiles emitted by a plant under given circumstances (also referred to as synomones in the context of natural enemy attraction) is referred to as a volatile profile. These are highly specific to certain plant species and are detectable meters from the source. Predators and parasitoids exploit the specificity of volatile profiles to navigate the complex infochemical signals presented by plants in their efforts to locate a particular prey species.
The production of volatiles is likely to be beneficial given two conditions: that they are effective in attracting natural enemies and that the natural enemies are effective in removing or impeding herbivores. However, volatile chemicals may not have evolved initially for this purpose; they act in within-plant signaling, attraction of pollinators, or repulsion of herbivores that dislike such odors.
Induced defenses
When an herbivore starts eating a plant, the plant may respond by increasing its production of volatiles or changing its volatile profile. This plasticity is controlled by either the jasmonic acid pathway or the salicylic acid pathway, depending largely on the herbivore; these substances are often called herbivore-induced plant volatiles (HIPVs). The plant hormone jasmonic acid increases in concentration when plants are damaged and is responsible for inducing the transcription of enzymes that synthesize secondary metabolites. This hormone also aids in the production of defensive proteins such as α-amylase inhibitors, as well as lectins. Since α-amylase breaks down starch, α-amylase inhibitors prevent insects from deriving nutrition from starch. Lectins likewise interfere with insect nutrient absorption as they bind to carbohydrates.
Though volatiles of any kind have an attractive effect on natural enemies, this effect is stronger for damaged plants than for undamaged plants, perhaps because induced volatiles signal definitive and recent herbivore activity. The inducibility gives rise to the idea that plants are sending out a "distress call" to the third trophic level in times of herbivore attack.
Natural enemies can distinguish between mechanical tissue damage, which might occur during events other than herbivory, and damage that is the direct result of insect feeding behavior. The presence of herbivore saliva or regurgitant mediates this differentiation, and the resulting chemical pathway leads to a stronger natural enemy response than mechanical damage could. The reliability of HIPVs in broadcasting the location of prey means that, for many foraging enemies, induced plant volatiles are more attractive than even the odors emitted by the prey insect itself.
Plants are able to determine what types of herbivore species are present, and will react differently given the herbivore's traits. If certain defense mechanisms are not effective, plants may turn to attracting natural enemies of herbivore populations. For example, wild tobacco plants use nicotine, a neurotoxin, to defend against herbivores. However, when faced with nicotine-tolerant herbivores, they will attract natural enemies.
Local and systemic signals
When herbivores trigger an inducible chemical defense pathway, the resulting HIPVs may be emitted either from the site of feeding damage (local induction) or from undamaged tissues belonging to a damaged plant (systemic induction). For example, when an herbivore feeds on a single corn seedling leaf, the plant will emit volatiles from all its leaves, whether or not they too have been damaged. Locally induced defenses aid parasitoids in targeting their foraging behaviors to the exact location of the herbivore on the plant. Systemic defenses are less spatially specific and may serve to confuse the enemy once the source plant is located. A plant might employ both local and systemic responses simultaneously.
Morphological mechanisms of enemy attraction
Domatia
Natural enemies must survive long enough and respond quickly enough to plant volatiles in order to benefit the plant through predatory behavior. Certain plant structures, called domatia, can selectively reinforce mutualisms with natural enemies and increase the fitness benefit they receive from that mutualism by ensuring the survival and proximity of natural enemies. Domatia provide a kind of housing or refuge for predators from both abiotic stressors, such as desiccation, and biotic stressors, such as predation from higher-order predators. Therefore, they not only ensure better survival, but eliminate the time required for natural enemies to locate and travel to the damaged plant. Natural enemies that make use of domatia are often said to serve as "bodyguards" for the plant on or in which they live. Domatia may be as well-developed as acacia tree thorns or as simple and incidental as a depression or crevice in a leaf stem, but they are distinguishable from galls and other similar structures in that they are not induced by the insect but formed constitutively by the plant.
Nutritional rewards
As long as natural enemies have some potential to be omnivorous, plants can provide food resources to encourage their retention and increase the impact they have on herbivore populations. This potential, however, can hinge on a number of the insect's traits. For example, hemipteran predators can use their sucking mouthparts to make use of leaves, stems, and fruits, but spiders with chelicerae cannot. Still, insects widely considered to be purely carnivorous have been observed to diverge from expected feeding behavior. Some plants simply tolerate a low level of herbivory by natural enemies for the service they provide in ridding the plant of more serious herbivores. Others, however, have structures thought to serve no purpose other than attracting and provisioning natural enemies. These structures derive from a long history of coevolution between the first and third trophic levels. A good example is the extrafloral nectaries that many myrmecophytes and other angiosperms sport on leaves, bracts, stems, and fruits. Nutritionally, extrafloral nectaries are similar to floral nectaries, but they do not lead the visiting insect to come into contact with pollen. Their existence is therefore not the product of a pollinator–plant mutualism, but rather a tritrophic, defensive interaction.
Herbivore sequestration of plant defensive compounds
The field of chemical ecology has elucidated additional types of plant multitrophic interactions that entail the transfer of defensive compounds across multiple trophic levels. For example, certain plant species in the Castilleja and Plantago genera have been found to produce defensive compounds called iridoid glycosides that are sequestered in the tissues of the Taylor's checkerspot butterfly larvae that have developed a tolerance for these compounds and are able to consume the foliage of these plants. These sequestered iridoid glycosides then confer chemical protection against bird predators to the butterfly larvae. Another example of this sort of multitrophic interaction in plants is the transfer of defensive alkaloids produced by endophytes living within a grass host to a hemiparasitic plant that is also using the grass as a host.
Human uses
Exploitation of tritrophic interactions can benefit agricultural systems. Biocontrol of crop pests can be exerted by the third trophic level, given an adequate population of natural enemies. However, the widespread use of pesticides or Bt crops can undermine natural enemies’ success. In some cases, populations of predators and parasitoids are decimated, necessitating even greater use of insecticide because the ecological service they provided in controlling herbivores has been lost.
Even when pesticides are not widely used, monocultures often have difficulty support natural enemies in great enough numbers for them to diminish pest populations. A lack of diversity in the first trophic level is linked to low abundance in the third because alternative resources that are necessary for stable, large natural enemy populations are missing from the system. Natural enemy diets can be subsidized by increasing landscape diversity through companion planting, border crops, cover crops, intercropping, or tolerance of some weed growth. When nectar or other sugar-rich resources are provided, the natural enemy population thrives.
Biological control
Morphological plant characteristics and natural enemy success
Beyond domatia and nutritional rewards, other plant characteristics influence the colonization of plants by natural enemies. These can include the physical size, shape, density, maturity, colour, and texture of a given plant species. Specific plant features such as the hairiness or glossiness of vegetation can have mixed effects on different natural enemies. For example, trichomes decrease hunting efficiency of many natural enemies, as trichomes tend to slow or prevent movement due to the physical obstacles they present or the adhesive secretions they produce. However, sometimes the prey species may be more impeded than the predator. For example, when the whitefly prey of the parasitoid Encarsia formosa is slowed by plant hairs, the parasitoid can detect and parasitize a higher number of juvenile whiteflies.
Many predatory coccinelid beetles have a preference for the type of leaf surface they frequent. Presented with the opportunity to land on glossy or hairy Brassica oleracea foliage, the beetles prefer the glossy foliage as they are better able to cling to these leaves. Studies are evaluating the effect of various plant genotypes on natural enemies.
Volatile organic compounds