Herbivores are dependent onplants for food, and havecoevolved mechanisms to obtain this food despite the evolution of a diverse arsenal ofplant 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 reciprocalevolutionary change. When a herbivore eats a plant itselects 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 havecoevolved.[2] The escape and radiation mechanisms for coevolution, presents the idea that adaptations in herbivores and their host plants, has been the driving force behindspeciation.[3][4] The coevolution that occurs between plants and herbivores that ultimately results in the speciation of both can be further explained by theRed 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]
Herbivores have developed a diverse range of physical structures to facilitate the consumption of plant material. To break up intact plant tissues, mammals have developedteeth 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 andseeds.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 familySphingidae (sphinx moths), it has been observed that thecaterpillars of species which eat relatively soft leaves are equipped withincisors for tearing and chewing, while the species that feed on mature leaves and grasses cut them with toothless snippingmandibles (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 onrye grass (a relatively hard grass) when compared to individuals raised onred clover (a soft diet).[9] LarvalLepidoptera that feed on plants with high levels of condensedtannins (as intrees) have morealkaline midguts when compared to Lepidoptera that feed onherbs andforbs (pH of 8.67 vs. 8.29 respectively). Thismorphological difference can be explained by the fact that insoluble tannin-protein complexes can be broken down and absorbed as nutrients at alkalinepH levels.[10]
Herbivores generateenzymes that counter and reduce the effectiveness of numerous toxicsecondary metabolic products produced by plants. One such enzyme group, mixed functionoxidases (MFOs),detoxify harmful plant compounds by catalyzingoxidative 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 larvaltobacco hornworms.[12] The induction of P-450 after initialnicotine ingestion allowed the larval tobacco hornworms to increase feeding on the toxic plant tissues.[12]
An important enzyme produced by herbivorous insects isprotease. 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 produceprotease 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, includingS. exigua andL. 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 producesalivary enzymes that reduce the degree of defense generated by a host plant. The enzymeglucose oxidase, a component of saliva for thecaterpillarHelicoverpa zea, counteracts the production of induced defenses intobacco.[14] Similarly,aphid saliva reduces its host's induced response by forming a barrier between the aphid'sstylet and the plant cells.[15]
Herbivores can avoid plant defenses by eating plants selectively in space and time. For thewinter moth, feeding onoak leaves early in the season maximized the amount ofprotein 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 inHemiptera allow them to feed around areas of high toxin concentration. Several species of caterpillar feed onmaple leaves by "window feeding" on pieces of leaf and avoiding the tough areas, or those with a highlignin concentration.[17] Similarly, the cotton leaf perforator selectively avoids eating theepidermis andpigment glands of their hosts, which contain defensiveterpenoidaldehydes.[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 asgeophagy.
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 isinterspecific competition for food, wherespecialization 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]
Herbivores are unable to digest complexcellulose and rely onmutualistic, internalsymbioticbacteria,fungi, orprotozoa 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 plantsecondary metabolites. For example,fungal symbionts of cigarette beetles (Lasioderma serricorne) use certain plantallelochemicals 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 ahost plant's defenses. Some herbivores are more successful at feeding on damaged hosts.[1] As an example, several species ofbark beetle introduce blue stain fungi of the generaCeratocystis andOphiostoma 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]
Herbivores often manipulate their host plants to use them better as resources. Herbivorous insects favorably alter themicrohabitat in which the herbivore feeds to counter existing plant defenses. For example, caterpillars from the familiesPyralidae andCtenuchidae roll mature leaves of theneotropical shrubPsychotria 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 ofnitrogen.[26] Lepidoptera larvae also tie leaves together and feed on the inside of the leaves to decrease the effectiveness of thephototoxinhypericin inSt. John's-wort.[27]Herbivores also manipulate their microhabitat by forminggalls, 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 oflatex andresin 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 theleaf 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 afolivore 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]
Plant chemical defenses can be used by herbivores, by storing eaten plant chemicals, and using them in defense againstpredators. To be effective defensive agents, the sequestered chemicals cannot bemetabolized 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 ofinsects sequester and deploy plant chemicals for their own defense.[34] Caterpillar and adultmonarch butterflies storecardiac glycosides frommilkweed, making these organisms distasteful. After eating a monarch caterpillar or butterfly, thebird 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 familyHemiptera,Lygaeus kalmii andlarge milkweed bug (Oncopeltus fasciatus), are colored with bright orange and black, and are said to beaposematically 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 againstpathogens.[37] Additionally, secondary metabolic products can act as cues to identify a plant for feeding oroviposition (egg laying) by herbivores.
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