Fungivory ormycophagy is the process of organisms consumingfungi. Many different organisms have been recorded to gain their energy from consuming fungi, including birds, mammals, insects, plants, amoebas, gastropods, nematodes, bacteria and other fungi. Some of these, which only eat fungi, are calledfungivores whereas others eat fungi as only part of their diet, beingomnivores.
Many mammals eat fungi, but only a few feed exclusively on fungi; most are opportunistic feeders and fungi only make up part of their diet.[1] At least 22 species ofprimate, includinghumans,bonobos,colobines,gorillas,lemurs,macaques,mangabeys,marmosets andvervet monkeys are known to feed on fungi. Most of these species spend less than 5% of the time they spend feeding eating fungi, and fungi therefore form only a small part of their diet. Some species spend longer foraging for fungi, and fungi account for a greater part of their diet;buffy-tufted marmosets spend up to 12% of their time consuming sporocarps,Goeldi’s monkeys spend up to 63% of their time doing so and theYunnan snub-nosed monkey spends up to 95% of its feeding time eatinglichens. Fungi are comparatively very rare in tropical rainforests compared to other food sources such as fruit and leaves, and they are also distributed more sparsely and appear unpredictably, making them a challenging source of food for Goeldi’s monkeys.[2]
Fungi are renowned for theirpoisons to deter animals from feeding on them: even today humans die from eating poisonous fungi. A natural consequence of this is the virtual absence of obligatevertebrate fungivores, with thediprotodont familyPotoridae being the major exception. One of the few extant vertebrate fungivores is thenorthern flying squirrel,[3] but it is believed that in the past there were numerous vertebrate fungivores and that toxin development greatly lessened their number and forced these species to abandon fungi or diversify.[4]
Many terrestrialgastropodmollusks are known to feed on fungi. It is the case in severalspecies ofslugs from distinctfamilies. Among them are thePhilomycidae (e. g.Philomycus carolinianus andPhylomicus flexuolaris) andAriolimacidae (Ariolimax californianus), which respectively feed on slime molds (myxomycetes) and mushrooms (basidiomycetes).[5] Species of mushroom producing fungi used as food source by slugs include milk-caps,Lactarius spp., the oyster mushroom,Pleurotus ostreatus and the penny bun,Boletus edulis. Other species pertaining to different genera, such asAgaricus,Pleurocybella andRussula, are also eaten by slugs. Slime molds used as food source by slugs includeStemonitis axifera andSymphytocarpus flaccidus.[5] Some slugs are selective towards certain parts or developmental stages of the fungi they eat, though this behavior varies greatly. Depending on the species and other factors, slugs eat only fungi at specific stages of development. Moreover, in other cases, whole mushrooms can be eaten, without any trace of selectivity.[5]
In 2008,Euprenolepis procera a species of ant from the rainforests of South East Asia was found to harvest mushrooms from the rainforest. Witte & Maschwitz found that their diet consisted almost entirely of mushrooms, representing a previously undiscovered feeding strategy in ants.[6] Severalbeetle families, including theErotylidae,Endomychidae, and certainTenebrionidae[7] also are specialists on fungi, though they may eat other foods occasionally.Other insects, likefungus gnats andscuttle flies,[8] utilize fungi at their larval stage. Feeding on fungi is crucial for dead wood eaters as this is the only way to acquire nutrients not available in nutritionally scarce dead wood.[9][10]
Jays (Perisoreus) are believed to be the first birds in which mycophagy was recorded. Canada jays (P. canadensis), Siberian jays (P. infaustus) and Oregon jays (P. obscurus) have all been recorded to eat mushrooms, with the stomachs of Siberian jays containing mostly fungi in the early winter. The ascomycete,Phaeangium lefebvrei found in north Africa and the Middle East is eaten by migrating birds in winter and early spring, mainly by species of lark (Alaudidae).Bedouin hunters have been reported to useP. lefebvrei as bait in traps to attract birds.[11] The ground-foragingsuperb lyrebirdMenura novaehollandiae has also been found to opportunistically forage on fungi.[12]
Fungi are known to form an important part of the diet of the southern cassowary (Casuarius casuarius) of Australia.Bracket fungi have been found in their droppings throughout the year, and Simpson in theAustralasian Mycological Newsletter suggested it is likely they also eat species ofAgaricales andPezizales but these have not been found in their droppings since they disintegrate when they are eaten. Emus (Dromaius novaehollandiae) will eat immatureLycoperdon andBovista fungi if presented to them as will brush turkeys (Alectura lathami) if offeredMycena, suggesting that species ofMegapodiidae may feed opportunistically on mushrooms.[13]
Mycoparasitism occurs when any fungus feeds on other fungi, a form ofparasitism, our knowledge of it in natural environments is very limited.[14]Collybia grow on dead mushrooms.
The fungal genus,Trichoderma producesenzymes such aschitinases which degrade thecell walls of other fungi.[15] They are able to detect other fungi and grow towards them, they then bind to the hyphae of other fungi usinglectins on the host fungi as a receptor, forming anappressorium. Once this is formed,Trichoderma inject toxic enzymes into the host and probablypeptaibolantibiotics, which create holes in the cell wall, allowingTrichoderma to grow inside of the host and feed.[16]Trichoderma are able to digestsclerotia, durable structures which contain food reserves, which is important if they are to control pathogenic fungi in the long term.[15]Trichoderma species have been recorded as protecting crops fromBotrytis cinerea,Rhizoctonia solani,Alternaria solani,Glomerella graminicola,Phytophthora capsici,Magnaporthe grisea andColletotrichum lindemuthianum; although this protection may not be entirely due toTrichoderma digesting these fungi, but by them improvingplant disease resistance indirectly.[16]
Bacterial mycophagy was a term coined in 2005, to describe the ability of some bacteria to "grow at the expense of living fungal hyphae". In a 2007 review in theNew Phytologist this definition was adapted to only include bacteria which play an active role in gaining nutrition from fungi, excluding those that feed off passive secretions by fungi, or off dead or damaged hyphae.[17] The majority of our knowledge in this area relates to interactions between bacteria and fungi in the soil and in or around plants, little is known about interactions in marine and freshwater habitats, or those occurring on or inside animals. It is not known what effects bacterial mycophagy has on the fungalcommunities in nature.[17]
There are three mechanisms by which bacteria feed on fungi; they either kill fungal cells, cause them to secrete more material out of their cells or enter into the cells to feed internally and they are categorised according to these habits. Those that kill fungal cells are called necrotrophs, the molecular mechanisms of this feeding are thought to overlap considerably with bacteria that feed on fungi after they have died naturally. Necrotrophs may kill the fungi through digesting their cell wall or by producing toxins which kill fungi, such astolaasin produced byPseudomonas tolaasii. Both of these mechanisms may be required since fungal cell walls are highly complex, so require many different enzymes to degrade them, and because experiments demonstrate that bacteria that produce toxins cannot always infect fungi. It is likely that these two systems actsynergistically, with the toxins killing or inhibiting the fungi andexoenzymes degrading the cell wall and digesting the fungus. Examples of necrotrophs includeStaphylococcus aureus which feed onCryptococcus neoformans,Aeromonascaviae which feed onRhizoctonia solani,Sclerotium rolfsii andFusarium oxysporum, and somemyxobacteria which feed onCochliobolus miyabeanus andRhizoctonia solani.[17]
Bacteria which manipulate fungi to produce more secretions which they in turn feed off are calledextracellular biotrophs; many bacteria feed on fungal secretions, but do not interact directly with the fungi and these are calledsaprotrophs, rather than biotrophs. Extracellular biotrophs could alter fungalphysiology in three ways; they alter theirdevelopment, thepermeability of their membranes (including theefflux of nutrients) and theirmetabolism. The precise signalling molecules that are used to achieve these changes are unknown, but it has been suggested thatauxins (better known for their role as aplant hormone) andquorum sensing molecules may be involved. Bacteria have been identified that manipulate fungi in these ways, for examplemycorrhiza helper bacteria (MHBs) andPseudomonas putida, but it remains to be demonstrated whether the changes they cause are directly beneficial to the bacteria. In the case of MHBs, which increase infection of plant roots bymycorrhizal fungi, they may benefit, because the fungi gain nutrition from the plant and in turn the fungi will secrete more sugars.[17]
The third group, that enter into living fungal cells are calledendocellular biotrophs. Some of these aretransmitted vertically whereas others are able to actively invade and subvert fungal cells. The molecular interactions involved in these interactions are mostly unknown. Many endocellular biotrophs, for example someBurkholderia species, belong to theβ-proteobacteria which also contains species which live inside the cells ofmammals and amoeba. Some of them, for exampleCandidatusGlomeribacter gigasporarum, which colonises the spores ofGigaspora margarita, have reducedgenome sizes indicating that they have become entirely dependent on the metabolic functions of the fungal cells in which they live. When all the endocellular bacteria insideG. margarita were removed, the fungus grew differently and was lessfit, suggesting that some bacteria may also provide services to the fungi they live in.[17]
Theciliate familyGrossglockneridae, including the speciesGrossglockneria acuta, feed exclusively on fungi.G. acuta first attaches themselves to a hyphae or sporangium via a feeding tube and then a ring-shaped structure, around 2 μm in diameter is observed to appear on the fungus, possibly consisting of degraded cell wall material.G. acuta then feeds through the hole in the cell wall for, on average, 10 minutes, before detaching itself and moving away. The precise mechanism of feeding is not known, but it conceivably involvesenzymes includingacid phosphatases,cellulases andchitinases.Microtubules are visible in the feeding tube, as are possible reserves ofcell membrane, which may be used to form foodvacuoles filled with the cytoplasm of the fungus, viaendocytosis, which are then transported back intoG. acuta. The holes made byG. acuta bear some similarities to those made by amoeba, but unlike amoebaG. acuta never engulfs the fungus.[18]
Around 90% of land plants live insymbiosis withmycorrhizal fungi,[19] where fungi gain sugars from plants and plants gainnutrients from the soil via the fungi. Some species of plant have evolved to manipulate this symbiosis, so that they no longer give fungi sugars that they produce and instead gain sugars from the fungi, a process called myco-heterotrophy. Some plants are only dependent on fungi as a source of sugars during the early stages of theirdevelopment, these include most of theorchids as well as manyferns andlycopods. Others are dependent on this food source for their entire lifetime, including some orchids andGentianaceae, and all species ofMonotropaceae andTriuridaceae.[20] Those that are dependent on fungi, but stillphotosynthesise are calledmixotrophs since they gain nutrition in more than one way, by gaining a significant amount of sugars from fungi, they are able to grow in the deep shade of forests. Examples include the orchidsEpipactis,Cephalanthera andPlantanthera and the tribePyroleae of the familyEricaceae.[19] Others, such asMonotropastrum humile, no longer photosynthesise and are totally dependent on fungi for nutrients.[20] Around 230 such species exist, and this trait is thought to haveevolved independently on five occasions outside of the orchid family. Some individuals of the orchid speciesCephalanthera damasonium are mixotrophs, but others do not photosynthesise.[21] Because the fungi that myco-heterotrophic plants gain sugars from in turn gain them from plants that do photosynthesise, they are considered indirectparasites of other plants.[20] The relationship between orchids andorchid mycorrhizae has been suggested to be somewhere betweenpredation and parasitism.[21]
The precise mechanisms by which these plants gain sugars from fungi are not known and has not been demonstrated scientifically. Two pathways have been proposed; they may either degrade fungal biomass, particularly the fungal hyphae which penetrate plant cells in a similar manner to inarbuscular mycorrhizae, or absorb sugars from the fungi by disrupting theircell membranes, throughmass flow. To prevent the sugars returning to the fungi, they must compartmentalise the sugars or convert them into forms which the fungi cannot use.[20]
Three insect lineages, beetles, ants and termites, independently evolved the ability to farm fungi between 40 and 60 million years ago. In a similar way to the way that human societies became more complex after the development of plant-based agriculture, the same occurred in these insect lineages when they evolved this ability and these insects are now of major importance in ecosystems.[22] The methods that insects use to farm fungi share fundamental similarities with human agriculture. Firstly, insects inoculate a particular habitat or substrate with fungi, much in the same as humans plant seeds in fields. Secondly, they cultivate the fungi by regulating the growing environment to try to improve the growth of the fungus, as well as protecting it from pests and diseases. Thirdly they harvest the fungus when it is mature and feed on it. Lastly they are dependent on the fungi they grow, in the same way that humans are dependent on crops.[23]
Ambrosia beetles, for exampleAustroplatypus incompertus, farmambrosia fungi inside of trees and feed on them. Themycangia (organs which carry fungal spores) of ambrosia beetles contain various species of fungus, including species ofAmbrosiomyces,Ambrosiella,Ascoidea,Ceratocystis,Dipodascus,Diplodia,Endomycopsis,Monacrosporium andTuberculariella.[24] The ambrosia fungi are only found in the beetles and their galleries, suggesting that they and the beetles have anobligatesymbiosis.[22]
Around 330 species oftermites in twelve genera of the subfamilyMacrotermitinae cultivate a specialised fungus in the genusTermitomyces. The fungus is kept in a specialised part of the nest in fungus cones. Worker termites eat plant matter, producing faecal pellets which they continuously place on top of the cone.[25] The fungus grows into this material and soon produces immature mushrooms, a rich source of protein, sugars and enzymes, which the worker termites eat. The nodules also containindigestible asexual spores, meaning that the faecal pellets produced by the workers always contain spores of the fungus that colonise the plant material that they defaecate. TheTermitomyces also fruits, forming mushrooms above ground, which mature at the same time that the first workers emerge from newly formed nests. The mushrooms produce spores that are wind dispersed, and through this method, new colonies acquire a fungal strain.[23] In some species, the genetic variation of the fungus is very low, suggesting that spores of the fungus are transmitted vertically from nest to nest, rather than from wind dispersed spores.[26]
Around 220described species, and more undescribed species of ants in thetribeAttini cultivate fungi. They are only found in theNew World and are thought to have evolved in theAmazon Rainforest, where they are mostdiverse today. For these ants, farmed fungi are the only source of food on which theirlarvae are raised on and are also an important food for adults.Queen ants carry a small part of fungus in small pouches in their mouthparts when they leave the nest to mate, allowing them to establish a new fungus garden when they form a new nest. Different lineages cultivate fungi on different substrates, those that evolved earlier do so on a wide range of plant matter, whereasleaf cutter ants are more selective, mainly using only fresh leaves and flowers. The fungi are members of the familiesLepiotaceae andPterulaceae. Other fungi in the genusEscovopsisparasitise the gardens andantibiotic-producing bacteria also inhabit the gardens.[23][27]
The marinesnailLittoraria irrorata, which lives in thesalt marshes of the southeast of the United States feeds on fungi that it encourages to grow. It creates and maintains wounds on the grass,Spartina alterniflora which are then infected by fungi, probably of the generaPhaeosphaeria andMycosphaerella, which are the preferred diet of the snail. They also deposit faeces on the wounds that they create, which encourage the growth of the fungi because they are rich in nitrogen and fungalhyphae. Juvenile snails raised on uninfected leaves do not grow and are more likely to die, indicating the importance of the fungi in the diet ofL. irrorata.[28]
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