Herbivore adaptations to plant defense

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Herbivores are dependent on plants for food, and have coevolved mechanisms to obtain this food despite the evolution of a diverse arsenal of plant defenses against herbivory. Herbivore adaptations to plant defense have been likened to "offensive traits" and consist of those traits that allow for increased feeding and use of a host. [1] Plants, on the other hand, protect their resources for use in growth and reproduction, by limiting the ability of herbivores to eat them. Relationships between herbivores and their host plants often results in reciprocal evolutionary change. When a herbivore eats a plant it selects for plants that can mount a defensive response, whether the response is incorporated biochemically or physically, or induced as a counterattack. 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 coevolved. [2] The escape and radiation mechanisms for coevolution, presents the idea that adaptations in herbivores and their host plants, has been the driving force behind speciation. [3] [4] The coevolution that occurs between plants and herbivores that ultimately results in the speciation of both can be further explained by the Red Queen hypothesis. This hypothesis states that competitive success and failure evolve back and forth through organizational learning. The act of an organism facing competition with another organism ultimately leads to an increase in the organism's performance due to selection. This increase in competitive success then forces the competing organism to increase its performance through selection as well, thus creating an "arms race" between the two species. Herbivores evolve due to plant defenses because plants must increase their competitive performance first due to herbivore competitive success. [5]

Contents

Mechanical adaptations

The molars of three species of elephant illustrate their different feeding preferences (l-asian elephant, c-african elephant, r-Mastodon ginganteum) Elefantenzaehne-drawing.jpg
The molars of three species of elephant illustrate their different feeding preferences (l-asian elephant, c-african elephant, r- Mastodon ginganteum)

Herbivores have developed a diverse range of physical structures to facilitate the consumption of plant material. To break up intact plant tissues, mammals have developed teeth structures that reflect their feeding preferences. For instance, frugivores (animals that feed primarily on fruit) and herbivores that feed on soft foliage have low-crowned teeth specialized for grinding foliage and seeds. Grazing animals that tend to eat hard, silica-rich grasses, have high-crowned teeth, which are capable of grinding tough plant tissues and do not wear down as quickly as low-crowned teeth. [6] Birds grind plant material or crush seeds using their beaks and gizzards.

Insect herbivores have evolved a wide range of tools to facilitate feeding. Often these tools reflect an individual's feeding strategy and its preferred food type. [7] Within the family Sphingidae (sphinx moths), it has been observed that the caterpillars of species which eat relatively soft leaves are equipped with incisors for tearing and chewing, while the species that feed on mature leaves and grasses cut them with toothless snipping mandibles (the uppermost pair of jaws in insects, used for feeding). [8]

A herbivore's diet often shapes its feeding adaptations. Grasshopper head size, and thus chewing power, was demonstrated to be greater for individuals raised on rye grass (a relatively hard grass) when compared to individuals raised on red clover (a soft diet). [9] Larval Lepidoptera that feed on plants with high levels of condensed tannins (as in trees) have more alkaline midguts when compared to Lepidoptera that feed on herbs and forbs (pH of 8.67 vs. 8.29 respectively). This morphological difference can be explained by the fact that insoluble tannin-protein complexes can be broken down and absorbed as nutrients at alkaline pH levels. [10]

Biochemical adaptations

Herbivores generate enzymes that counter and reduce the effectiveness of numerous toxic secondary metabolic products produced by plants. One such enzyme group, mixed function oxidases (MFOs), detoxify harmful plant compounds by catalyzing oxidative reactions. [11] Cytochrome P450 oxidases (or P-450), a specific class of MFO, have been specifically connected to detoxification of plant secondary metabolic products. One group linked herbivore feeding on plant material protected by chemical defenses with P-450 detoxification in larval tobacco hornworms. [12] The induction of P-450 after initial nicotine ingestion allowed the larval tobacco hornworms to increase feeding on the toxic plant tissues. [12]

An important enzyme produced by herbivorous insects is protease. The protease enzyme is a protein in the gut that helps the insect digest its main source of food: plant tissue. Many types of plants produce protease inhibitors, which inactivate proteases. Protease inactivation can lead to many issues such as reduced feeding, prolonged larval development time, and weight gain. However, many insects, including S. exigua and L. decemlineatu have been selected for mechanisms to avoid the effects of protease inhibitors. Some of these mechanisms include developing protease enzymes that are unaffected by the plant protease inhibitors, gaining the ability to degrade protease inhibitors, and acquiring mutations that allow the digesting of plant tissue without its destructive effects. [13]

Herbivores may also produce salivary enzymes that reduce the degree of defense generated by a host plant. The enzyme glucose oxidase, a component of saliva for the caterpillar Helicoverpa zea , counteracts the production of induced defenses in tobacco. [14] Similarly, aphid saliva reduces its host's induced response by forming a barrier between the aphid's stylet and the plant cells. [15]

Behavioral adaptations

Herbivores can avoid plant defenses by eating plants selectively in space and time. For the winter moth, feeding on oak leaves early in the season maximized the amount of protein and nutrients available to the moth, while minimizing the amount of tannins produced by the tree. [16] Herbivores can also spatially avoid plant defenses. The piercing mouthparts of species in Hemiptera allow them to feed around areas of high toxin concentration. Several species of caterpillar feed on maple leaves by "window feeding" on pieces of leaf and avoiding the tough areas, or those with a high lignin concentration. [17] Similarly, the cotton leaf perforator selectively avoids eating the epidermis and pigment glands of their hosts, which contain defensive terpenoid aldehydes. [1] Some plants only produce toxins in small amounts, and rapidly deploy them to the area under attack. Some beetles counter this adaptation by attacking target plants in groups, thereby allowing each individual beetle to avoid ingesting too much toxin. [18] Some animals ingest large amounts of poisons in their food, but then eat clay or other minerals, which neutralize the poisons. This behavior is known as geophagy.

Plant defense may explain, in part, why herbivores employ different life history strategies. Monophagous species (animals that eat plants from a single genus) must produce specialized enzymes to detoxify their food, or develop specialized structures to deal with sequestered chemicals. Polyphagous species (animals that eat plants from many different families), on the other hand, produce more detoxifying enzymes (specifically MFO) to deal with a range of plant chemical defenses. [19] Polyphagy often develops when a herbivore's host plants are rare as a necessity to gain enough food. Monophagy is favored when there is interspecific competition for food, where specialization often increases an animals' competitive ability to use a resource. [20]

One major example of herbivorous behavioral adaptations deals with introduced insecticides and pesticides. The introduction of new herbicides and pesticides only selects for insects that can ultimately avoid or utilize these chemicals over time. Adding toxin free plants to a population of transgenic plants, or genetically modified plants that produce their own insecticides, has been shown to minimize the rate of evolution in insects feeding on crop plants. But even so, the rate of adaptation is only increasing in these insects. [21]

Microbial symbionts

Galls (upper left and right) A knopper gall formed on an acorn on the branch of an English oak tree by the parthenogenetic gall wasp Andricus quercuscalicis. Gallwespe bedient sich Eichel2.jpg
Galls (upper left and right) A knopper gall formed on an acorn on the branch of an English oak tree by the parthenogenetic gall wasp Andricus quercuscalicis.

Herbivores are unable to digest complex cellulose and rely on mutualistic, internal symbiotic bacteria, fungi, or protozoa to break down cellulose so it can be used by the herbivore. Microbial symbionts also allow herbivores to eat plants that would otherwise be inedible by detoxifying plant secondary metabolites. For example, fungal symbionts of cigarette beetles ( Lasioderma serricorne ) use certain plant allelochemicals as their source of carbon, in addition to producing detoxification enzymes (esterases) to get rid of other toxins. [22] Microbial symbionts also assist in the acquisition of plant material by weakening a host plant's defenses. Some herbivores are more successful at feeding on damaged hosts. [1] As an example, several species of bark beetle introduce blue stain fungi of the genera Ceratocystis and Ophiostoma into trees before feeding. [23] The blue stain fungi cause lesions that reduce the trees' defensive mechanisms and allow the bark beetles to feed. [24] [25]

Host manipulation

Herbivores often manipulate their host plants to use them better as resources. Herbivorous insects favorably alter the microhabitat in which the herbivore feeds to counter existing plant defenses. For example, caterpillars from the families Pyralidae and Ctenuchidae roll mature leaves of the neotropical shrub Psychotria horizontalis around an expanding bud that they consume. By rolling the leaves, the insects reduce the amount of light reaching the bud by 95%, and this shading prevents leaf toughness and leaf tannin concentrations in the expanding bud, while maintaining the amount of nutritional gain of nitrogen. [26] Lepidoptera larvae also tie leaves together and feed on the inside of the leaves to decrease the effectiveness of the phototoxin hypericin in St. John's-wort. [27] Herbivores also manipulate their microhabitat by forming galls, plant structures made of plant tissue but controlled by the herbivore. Galls act as both domatia (housing), and food sources for the gall maker. The interior of a gall is composed of edible nutritious tissue. Aphid galls in narrow leaf cottonwood ( Populus angustifolia ) act as “physiologic sinks,” concentrating resources in the gall from the surrounding plant parts. [28] Galls may also provide the herbivore protection from predators. [29]

Some herbivores use feeding behaviors that are capable of disarming the defenses of their host plants. One such plant defensive strategy is the use of latex and resin canals that contain sticky toxins and digestibility reducers. These canal systems store fluids under pressure, and when ruptured (i.e. from herbivory) secondary metabolic products flow to the release point. [30] Herbivores can evade this defense, however, by damaging the leaf veins. This technique minimizes the outflow of latex or resin beyond the cut and allows herbivores to freely feed above the damaged section. Several strategies are employed by herbivores to relieve canal pressure, including vein cutting and trenching. Vein cutting is when a herbivore creates small openings along the length of the leaf vein, while trenching refers to the creation of a cut across the width the leaf allowing the individual to safely consume the separated portion. [31] There is also a third technique known as girdling where a folivore will create an incision going around the stem disconnecting the leaf from the canals in the rest of the plant. [31] The technique used by the herbivore corresponds to the architecture of the canal system. [32] Dussourd and Denno examined the behavior of 33 species of insect herbivores on 10 families of plants with canals and found that herbivores on plants with branching canal systems used vein cutting, while herbivores found on plants with net-like canal systems employed trenching to evade plant defenses. [32]


Herbivore use of plant chemicals

Monarch butterflies obtain poison from the plants they feed on as larvae, their distinctive appearance serving to warn predators. Monarch Butterfly Danaus plexippus on Echinacea purpurea 2800px.jpg
Monarch butterflies obtain poison from the plants they feed on as larvae, their distinctive appearance serving to warn predators.

Plant chemical defenses can be used by herbivores, by storing eaten plant chemicals, and using them in defense against predators. To be effective defensive agents, the sequestered chemicals cannot be metabolized into inactive products. Using plant chemicals can be costly to herbivores because it often requires specialized handling, storage, and modification. [33] This cost can be seen when plants that use chemical defenses are compared to those plants that do not, in situations when herbivores are excluded. Several species of insects sequester and deploy plant chemicals for their own defense. [34] Caterpillar and adult monarch butterflies store cardiac glycosides from milkweed, making these organisms distasteful. After eating a monarch caterpillar or butterfly, the bird predator will usually vomit, leading the bird to avoid eating similar looking butterflies in the future. [35] Two different species of milkweed bug in the family Hemiptera, Lygaeus kalmii and large milkweed bug (Oncopeltus fasciatus), are colored with bright orange and black, and are said to be aposematically colored, in that they "advertise" their distastefulness by being brightly colored. [36]

Secondary metabolic products can also be useful to herbivores due to the antibiotic properties of the toxins, which can protect herbivores against pathogens. [37] Additionally, secondary metabolic products can act as cues to identify a plant for feeding or oviposition (egg laying) by herbivores.

Related Research Articles

Herbivore Animal adapted to eating plant material

A herbivore is an animal anatomically and physiologically adapted to eating plant material, for example foliage or marine algae, for the main component of its diet. As a result of their plant diet, herbivorous animals typically have mouthparts adapted to rasping or grinding. Horses and other herbivores have wide flat teeth that are adapted to grinding grass, tree bark, and other tough plant material.

Caterpillar Larva of a butterfly or moth

Caterpillars are the larval stage of members of the order Lepidoptera.

<i>Erysimum</i> Genus of flowering plants

Erysimum, or wallflower, is a genus of flowering plants in the cabbage family, Brassicaceae. It includes more than 150 species, both popular garden plants and many wild forms. The genus Cheiranthus is sometimes included here in whole or in part. Erysimum has since the early 21st century been ascribed to a monogeneric cruciferous tribe, Erysimeae, characterised by sessile, stellate (star-shaped) and/or malpighiaceous (two-sided) trichomes, yellow to orange flowers and multiseeded siliques.

Chemical ecology is the study of chemically-mediated interactions between living organisms, and the effects of those interactions on the demography, behavior and ultimately evolution of the organisms involved. It is thus a vast and highly interdisciplinary field. Chemical ecologists seek to identify the specific molecules that function as signals mediating community or ecosystem processes and to understand the evolution of these signals. The substances that serve in such roles are typically small, readily-diffusible organic molecules, but can also include larger molecules and small peptides.

Folivore

In zoology, a folivore is a herbivore that specializes in eating leaves. Mature leaves contain a high proportion of hard-to-digest cellulose, less energy than other types of foods, and often toxic compounds. For this reason, folivorous animals tend to have long digestive tracts and slow metabolisms. Many enlist the help of symbiotic bacteria to release the nutrients in their diet. Additionally, as has been observed in folivorous primates, they exhibit a strong preference for immature leaves, which tend to be easier to masticate, tend to be higher in energy and protein, and lower in fibre and poisons than more mature fibrous leaves.

Plant defense against herbivory Range of adaptations evolved by plants

Plant defense against herbivory or host-plant resistance (HPR) describes a range of adaptations evolved by plants which improve their survival and reproduction by reducing the impact of herbivores. Plants can sense being touched, and they can use several strategies to defend against damage caused by herbivores. Many plants produce secondary metabolites, known as allelochemicals, that influence the behavior, growth, or survival of herbivores. These chemical defenses can act as repellents or toxins to herbivores, or reduce plant digestibility.

Leaf miner Larva of an insect that lives in and eats the leaf tissue of plants

A leaf miner is any one of numerous species of insects in which the larval stage lives in, and eats, the leaf tissue of plants. The vast majority of leaf-mining insects are moths (Lepidoptera), sawflies, and flies (Diptera), though some beetles also exhibit this behavior.

<i>Tetraopes tetrophthalmus</i> Species of beetle

The red milkweed beetle is a beetle in the family Cerambycidae. The binomial genus and species names are both derived from the Ancient Greek for "four eyes." As in many longhorn beetles, the antennae are situated very near the eye–in the red milkweed beetle, this adaptation has been carried to an extreme: the antennal base actually bisects the eye. The milkweed beetle, a herbivore, is given this name because they are generally host specific to milkweed plants. It is thought the beetle, which as an adult feeds on the foliage of the plant, and its early instars, which eat the roots, derive a measure of protection from predators by incorporating toxins from the plant into their bodies, thereby becoming distasteful, much as the monarch butterfly and its larvae do. They feed by opening veins in the milkweed plant, decreasing the beetles' exposure to latex-like sap. When startled, the beetles make a shrill noise. When interacting with another beetle, they make a 'purring' noise. The red and black coloring are aposematic, advertising the beetles' inedibility. There are many milkweed-eating species of insect that use the toxins contained in the plant as a chemical defense. Red milkweed beetles lay egg-clutches in mid-summer near the roots of the milkweed.

<i>Euchaetes egle</i> Species of moth

Euchaetes egle, the milkweed tiger moth or milkweed tussock moth, is a moth in the family Erebidae and the tribe Arctiini, the tiger moths. The species was first described by Dru Drury in 1773. It is a common mid- through late-summer feeder on milkweeds and dogbane. Like most species in this family, it has chemical defenses it acquires from its host plants, in this case, cardiac glycosides. These are retained in adults and deter bats, and presumably other predators, from feeding on them. Only very high cardiac glycoside concentrations deterred bats, however. Adults indicate their unpalatability with clicks from their tymbal organs.

Myrmecophily

Myrmecophily is the term applied to positive interspecies associations between ants and a variety of other organisms, such as plants, other arthropods, and fungi. Myrmecophily refers to mutualistic associations with ants, though in its more general use, the term may also refer to commensal or even parasitic interactions.

A laticifer is a type of elongated secretory cell found in the leaves and/or stems of plants that produce latex and rubber as secondary metabolites. Laticifers may be divided into:

<i>Heliconius melpomene</i> Species of butterfly

Heliconius melpomene, the postman butterfly, common postman or simply postman, is a brightly colored butterfly found throughout Central and South America. It was first described by Carl Linnaeus in his 1758 10th edition of Systema Naturae. Its coloration coevolved with a sister species H. erato as a warning to predators of its inedibility; this is an example of Müllerian mimicry. H. melpomene was one of the first butterfly species observed to forage for pollen, a behavior that is common in other groups but rare in butterflies. Because of the recent rapid evolutionary radiation of the genus Heliconius and overlapping of its habitat with other related species, H. melpomene has been the subject of extensive study on speciation and hybridization. These hybrids tend to have low fitness as they look different from the original species and no longer exhibit Müllerian mimicry.

Cardenolide

Cardenolide is a type of steroid. Many plants contain derivatives, collectively known as cardenolides, including many in the form of cardenolide glycosides (cardenolides that contain structural groups derived from sugars). Cardenolide glycosides are often toxic; specifically, they are heart-arresting. Cardenolides are toxic to animals through inhibition of the enzyme Na+/K+‐ATPase, which is responsible for maintaining the sodium and potassium ion gradients across cell membranes.

Plants and herbivores have co-evolved together for 350 million years. Plants have evolved many defense mechanisms against insect herbivory. Such defenses can be broadly classified into two categories: (1) permanent, constitutive defenses, and (2) temporary, inducible defenses. Both types are achieved through similar means but differ in that constitutive defenses are present before an herbivore attacks, while induced defenses are activated only when attacks occur. In addition to constitutive defenses, initiation of specific defense responses to herbivory is an important strategy for plant persistence and survival.

Chemical defense

Chemical defense is a life history strategy employed by many organisms to avoid consumption by producing toxic or repellent metabolites. The production of defensive chemicals occurs in plants, fungi, and bacteria, as well as invertebrate and vertebrate animals. The class of chemicals produced by organisms that are considered defensive may be considered in a strict sense to only apply to those aiding an organism in escaping herbivory or predation. However, the distinction between types of chemical interaction is subjective and defensive chemicals may also be considered to protect against reduced fitness by pests, parasites, and competitors. Many chemicals used for defensive purposes are secondary metabolites derived from primary metabolites which serve a physiological purpose in the organism. Secondary metabolites produced by plants are consumed and sequestered by a variety of arthropods and, in turn, toxins found in some amphibians, snakes, and even birds can be traced back to arthropod prey. There are a variety of special cases for considering mammalian antipredatory adaptations as chemical defenses as well.

Insects have a wide variety of predators, including birds, reptiles, amphibians, mammals, carnivorous plants, and other arthropods. The great majority (80–99.99%) of individuals born do not survive to reproductive age, with perhaps 50% of this mortality rate attributed to predation. In order to deal with this ongoing escapist battle, insects have evolved a wide range of defense mechanisms. The only restraint on these adaptations is that their cost, in terms of time and energy, does not exceed the benefit that they provide to the organism. The further that a feature tips the balance towards beneficial, the more likely that selection will act upon the trait, passing it down to further generations. The opposite also holds true; defenses that are too costly will have a little chance of being passed down. Examples of defenses that have withstood the test of time include hiding, escape by flight or running, and firmly holding ground to fight as well as producing chemicals and social structures that help prevent predation.

Plant use of endophytic fungi in defense

Plant use of endophytic fungi in defense occurs when endophytic fungi, which live symbiotically with the majority of plants by entering their cells, are utilized as an indirect defense against herbivores. In exchange for carbohydrate energy resources, the fungus provides benefits to the plant which can include increased water or nutrient uptake and protection from phytophagous insects, birds or mammals. Once associated, the fungi alter nutrient content of the plant and enhance or begin production of secondary metabolites. The change in chemical composition acts to deter herbivory by insects, grazing by ungulates and/or oviposition by adult insects. Endophyte-mediated defense can also be effective against pathogens and non-herbivory damage.

Wilhelm Boland is a German chemist.

Escape and radiate coevolution

Escape and radiate coevolution is a hypothesis proposing that a coevolutionary 'arms-race' between primary producers and their consumers contributes to the diversification of species by accelerating speciation rates. The hypothesized process involves the evolution of novel defenses in the host, allowing it to "escape" and then "radiate" into differing species.

Tritrophic interactions in plant defense

Tritrophic interactions, as they relate to 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, or hyperparasitoids, are considered. Tritrophic interactions join pollination and seed dispersal as vital biological functions which plants perform via cooperation with animals.

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