Herbivory prevention Studies of fungal infection consistently reveal that plants with endophytes are less likely to suffer substantial damage, and herbivores feeding on infected plants are less
productive. There are multiple modes through which endophytic fungi reduce insect herbivore damage, including avoidance (deterrence), reduced feeding, reduced
development rate, reduced growth and/or
population growth, reduced survival, and reduced oviposition.
Vertebrate herbivores such as birds, rabbits and deer show the same patterns of avoidance and reduced performance. Even below-ground herbivores such as
nematodes and root-feeding insects are reduced by endophyte infection. The strongest evidence for anti-herbivore benefits of fungal endophytes come from studies of herbivore populations being
extirpated when allowed to feed only on infected plants. Examples of local extinction have been documented in crickets, larval armyworms and
flour beetles. Yet chemical defenses produced by fungal endophytes are not universally effective, and numerous insect herbivores are unaffected by a given compound at one or more life history stages; larval stages are often more susceptible to toxins than adults. Even endophytes which purportedly provide some defense benefit to their hosts such as the Neotyphidium partner of many grass species in the
alpine tundra do not always lead to avoidance or ill-effects on herbivores due to spatial variation in levels of consumption.
Mutualism-pathogenicity continuum Not all endophytic symbioses confer protection from herbivores – only some species associations act as defense mutualisms. The difference between a
mutualistic endophyte and a
pathogenic one can be indistinct and dependent on interactions with other species or environmental conditions. Some endophytic fungi can counteract the negative impacts of pathogenic fungi in some plants such as Siberian ryegrass (
Elymus sibiricus) by increasing seed
germination, coleoptile and
radicle length, and seedling weight. Some fungi which are pathogens in the absence of herbivores may become beneficial under high levels of insect damage, such as species which kill plant cells in order to make nutrients available for their own growth, thereby altering nutritional content of leaves and making them a less desirable foodstuff. This is not unusual among fungi, as non-endophytic plant pathogens have similar conditionally beneficial effects on defense. Some species of endophyte may be beneficial for the plants in other ways (e.g. nutrient and water uptake) but will provide less benefit as a plant receives more damage and not produce defensive chemicals in response. The effect of one fungus on the plant can be altered when multiple strains of fungi are infecting a given individual in combination. Some endomycorrhizae may actually promote herbivore damage by making plants more susceptible to it. For example, some oak fungal endophytes are positively correlated with the levels of damage from
leaf miners (
Cameraria spp.), although negatively correlated with number of larvae present due to a reduction of oviposition on infected plants, which partially mitigates the higher damage rate. This continuum between mutualism and pathogenicity of endophytic fungi has major implications for plant fitness depending on the species of partners available in a given environment; mutualist status is conditional in a way similar to
pollination and can shift from one to the other just as frequently.
Fitness and competitive ability Fungal endophytes which provide defensive services to their host plants may exert
selective pressures favouring association through enhanced
fitness relative to uninfected hosts. The fungus Neotyphodium spp. infects grasses and increases fitness under conditions with high levels of
interspecific competition. It does this through a combination of benefits including anti-herbivore defenses and growth promoting factors. The customary assumption that plant growth promotion is the main way fungal mutualists improve fitness under attack from herbivores is changing; alteration of plant chemical composition and induced resistance are now recognized as factors of great importance in improving competitive ability and fecundity. Plants undefended by chemical or physical means at certain points in their life histories have higher survival rates when infected with beneficial endophytic fungi. The general trend of plants infected with mutualistic fungi outperforming uninfected plants under moderate to high herbivory exerts selection for higher levels of fungal association as herbivory levels increase. Unsurprisingly, low to moderate levels of herbivore damage also increases the levels of infection by beneficial endophytic fungi. In some cases the symbiosis between fungus and plant reaches a point of inseparability; fungal material is transmitted vertically from the maternal parent plant to seeds, forming a near-obligate mutualism. Having a mutualistic relationship with endophytic fungi can promote seed production and seed germination rates in some plant species, such as perennial ryegrass (
Lolium perenne) and tall fescue (
Festuca arundinacea). The fungi can also benefit the growth of the seedlings as it can enhance seedling growth rate, tiller number and height, and overall biomass. Mechanisms of microbial association defense, protecting the seeds rather than the already established plants, can have such drastic impacts on seed survival that they have been recognized to be an important aspect of the larger 'seed defence theory'.
Climate change The range of associated plants and fungi may be altered as
climate changes, and not necessarily in a synchronous fashion. Plants may lose or gain endophytes, with as yet unknown impacts on defense and fitness, although generalist species may provide indirect defense in new habitats more often than not. Above-ground and below-ground associations can be mutual drivers of diversity, so altering the interactions between plants and their fungi may also have drastic effects on the community at large, including herbivores. Changes in distribution may bring plants into
competition with previously established local species, making the fungal community – and particularly the pathogenic role of fungus – important in determining outcomes of competition with non-native
invasive species. As
carbon dioxide levels rise, the amplified photosynthesis will increase the pool of carbohydrates available to endophytic partners, potentially altering the strength of associations. Infected
C3 plants show greater relative growth rate under high conditions compared to uninfected plants, and it is possible that the fungi drive this pattern of increased carbohydrate production. Levels of herbivory may also increase as temperature and carbon dioxide concentrations rise. However, should plants remain associated with their current symbiotic fungi, evidence suggests that the degree of defense afforded them should not be altered. Although the amount of damage caused by herbivores frequently increases under elevated levels of atmospheric , the proportion of damage remains constant when host plants are infected by their fungal endophytes. The change in
carbon-nitrogen ratio will also have important consequences for herbivores. As carbohydrate levels increase within plants, relative nitrogen content will fall, having the dual effects of reducing nutritional benefit per unit
biomass and also lowering concentrations of nitrogen-based defenses such as alkaloids. == History of research ==