Fungivory or mycophagy is the process of organisms consuming fungi. 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 called fungivores whereas others eat fungi as only part of their diet, being omnivores.
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 of primate, including humans, bonobos, colobines, gorillas, lemurs, macaques, mangabeys, marmosets and vervet 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 the Yunnan snub-nosed monkey spends up to 95% of its feeding time eating lichens. 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 their poisons 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 obligate vertebrate fungivores, with the diprotodont family Potoridae being the major exception. One of the few extant vertebrate fungivores is the northern 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 terrestrial gastropod mollusks are known to feed on fungi. It is the case in several species of slugs from distinct families. Among them are the Philomycidae (e. g. Philomycus carolinianus and Phylomicus flexuolaris ) and Ariolimacidae ( 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 as Agaricus , Pleurocybella and Russula , are also eaten by slugs. Slime molds used as food source by slugs include Stemonitis axifera and Symphytocarpus 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] Several beetle families, including the Erotylidae, Endomychidae, and certain Tenebrionidae [7] also are specialists on fungi, though they may eat other foods occasionally. Other insects, like fungus gnats and scuttle 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 use P. lefebvrei as bait in traps to attract birds. [11] The ground-foraging superb lyrebird Menura 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 the Australasian Mycological Newsletter suggested it is likely they also eat species of Agaricales and Pezizales but these have not been found in their droppings since they disintegrate when they are eaten. Emus ( Dromaius novaehollandiae ) will eat immature Lycoperdon and Bovista fungi if presented to them as will brush turkeys ( Alectura lathami ) if offered Mycena , suggesting that species of Megapodiidae may feed opportunistically on mushrooms. [13]
Mycoparasitism occurs when any fungus feeds on other fungi, a form of parasitism, our knowledge of it in natural environments is very limited. [14] Collybia grow on dead mushrooms.
The fungal genus, Trichoderma produces enzymes such as chitinases which degrade the cell 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 using lectins on the host fungi as a receptor, forming an appressorium. Once this is formed, Trichoderma inject toxic enzymes into the host and probably peptaibol antibiotics, which create holes in the cell wall, allowing Trichoderma to grow inside of the host and feed. [16] Trichoderma are able to digest sclerotia, 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 from Botrytis cinerea , Rhizoctonia solani , Alternaria solani , Glomerella graminicola , Phytophthora capsici , Magnaporthe grisea and Colletotrichum lindemuthianum ; although this protection may not be entirely due to Trichoderma digesting these fungi, but by them improving plant 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 the New 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 fungal communities 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 as tolaasin produced by Pseudomonas 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 act synergistically, with the toxins killing or inhibiting the fungi and exoenzymes degrading the cell wall and digesting the fungus. Examples of necrotrophs include Staphylococcus aureus which feed on Cryptococcus neoformans , Aeromonas caviae which feed on Rhizoctonia solani , Sclerotium rolfsii and Fusarium oxysporum , and some myxobacteria which feed on Cochliobolus miyabeanus and Rhizoctonia solani . [17]
Bacteria which manipulate fungi to produce more secretions which they in turn feed off are called extracellular biotrophs; many bacteria feed on fungal secretions, but do not interact directly with the fungi and these are called saprotrophs, rather than biotrophs. Extracellular biotrophs could alter fungal physiology in three ways; they alter their development, the permeability of their membranes (including the efflux of nutrients) and their metabolism. The precise signalling molecules that are used to achieve these changes are unknown, but it has been suggested that auxins (better known for their role as a plant hormone) and quorum sensing molecules may be involved. Bacteria have been identified that manipulate fungi in these ways, for example mycorrhiza helper bacteria (MHBs) and Pseudomonas 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 by mycorrhizal 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 called endocellular biotrophs. Some of these are transmitted 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 some Burkholderia species, belong to the β-proteobacteria which also contains species which live inside the cells of mammals and amoeba. Some of them, for example Candidatus Glomeribacter gigasporarum, which colonises the spores of Gigaspora margarita , have reduced genome 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 inside G. margarita were removed, the fungus grew differently and was less fit, suggesting that some bacteria may also provide services to the fungi they live in. [17]
The ciliate family Grossglockneridae, including the species Grossglockneria 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 involves enzymes including acid phosphatases, cellulases and chitinases. Microtubules are visible in the feeding tube, as are possible reserves of cell membrane, which may be used to form food vacuoles filled with the cytoplasm of the fungus, via endocytosis, which are then transported back into G. acuta. The holes made by G. acuta bear some similarities to those made by amoeba, but unlike amoeba G. acuta never engulfs the fungus. [18]
Around 90% of land plants live in symbiosis with mycorrhizal fungi, [19] where fungi gain sugars from plants and plants gain nutrients 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 their development, these include most of the orchids as well as many ferns and lycopods. Others are dependent on this food source for their entire lifetime, including some orchids and Gentianaceae, and all species of Monotropaceae and Triuridaceae. [20] Those that are dependent on fungi, but still photosynthesise are called mixotrophs 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 orchids Epipactis , Cephalanthera and Plantanthera and the tribe Pyroleae of the family Ericaceae. [19] Others, such as Monotropastrum humile , no longer photosynthesise and are totally dependent on fungi for nutrients. [20] Around 230 such species exist, and this trait is thought to have evolved independently on five occasions outside of the orchid family. Some individuals of the orchid species Cephalanthera 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 indirect parasites of other plants. [20] The relationship between orchids and orchid mycorrhizae has been suggested to be somewhere between predation 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 in arbuscular mycorrhizae, or absorb sugars from the fungi by disrupting their cell membranes, through mass 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 example Austroplatypus incompertus , farm ambrosia fungi inside of trees and feed on them. The mycangia (organs which carry fungal spores) of ambrosia beetles contain various species of fungus, including species of Ambrosiomyces , Ambrosiella , Ascoidea , Ceratocystis , Dipodascus , Diplodia , Endomycopsis , Monacrosporium and Tuberculariella . [24] The ambrosia fungi are only found in the beetles and their galleries, suggesting that they and the beetles have an obligate symbiosis. [22]
Around 330 species of termites in twelve genera of the subfamily Macrotermitinae cultivate a specialised fungus in the genus Termitomyces . 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 contain indigestible 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. The Termitomyces 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 220 described species, and more undescribed species of ants in the tribe Attini cultivate fungi. They are only found in the New World and are thought to have evolved in the Amazon Rainforest, where they are most diverse today. For these ants, farmed fungi are the only source of food on which their larvae 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, whereas leaf cutter ants are more selective, mainly using only fresh leaves and flowers. The fungi are members of the families Lepiotaceae and Pterulaceae. Other fungi in the genus Escovopsis parasitise the gardens and antibiotic-producing bacteria also inhabit the gardens. [23] [27]
The marine snail Littoraria irrorata , which lives in the salt 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 genera Phaeosphaeria and Mycosphaerella , 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 fungal hyphae. Juvenile snails raised on uninfected leaves do not grow and are more likely to die, indicating the importance of the fungi in the diet of L. irrorata. [28]
Mycology is the branch of biology concerned with the study of fungi, including their taxonomy, genetics, biochemical properties, and use by humans. Fungi can be a source of tinder, food, traditional medicine, as well as entheogens, poison, and infection. Mycology branches into the field of phytopathology, the study of plant diseases. The two disciplines are closely related, because the vast majority of plant pathogens are fungi. A biologist specializing in mycology is called a mycologist.
Ascomycota is a phylum of the kingdom Fungi that, together with the Basidiomycota, forms the subkingdom Dikarya. Its members are commonly known as the sac fungi or ascomycetes. It is the largest phylum of Fungi, with over 64,000 species. The defining feature of this fungal group is the "ascus", a microscopic sexual structure in which nonmotile spores, called ascospores, are formed. However, some species of Ascomycota are asexual and thus do not form asci or ascospores. Familiar examples of sac fungi include morels, truffles, brewers' and bakers' yeast, dead man's fingers, and cup fungi. The fungal symbionts in the majority of lichens such as Cladonia belong to the Ascomycota.
A mycorrhiza is a symbiotic association between a fungus and a plant. The term mycorrhiza refers to the role of the fungus in the plant's rhizosphere, the plant root system and its surroundings. Mycorrhizae play important roles in plant nutrition, soil biology, and soil chemistry.
Fungus-growing ants comprise all the known fungus-growing ant species participating in ant–fungus mutualism. They are known for cutting grasses and leaves, carrying them to their colonies' nests, and using them to grow fungus on which they later feed.
Ant–fungus mutualism is a symbiosis seen between certain ant and fungal species, in which ants actively cultivate fungus much like humans farm crops as a food source. There is only evidence of two instances in which this form of agriculture evolved in ants resulting in a dependence on fungi for food. These instances were the attine ants and some ants that are part of the Megalomyrmex genus. In some species, the ants and fungi are dependent on each other for survival. This type of codependency is prevalent among herbivores who rely on plant material for nutrition. The fungus’ ability to convert the plant material into a food source accessible to their host makes them the ideal partner. The leafcutter ant is a well-known example of this symbiosis. Leafcutter ants species can be found in southern South America up to the United States. However, ants are not the only ground-dwelling arthropods which have developed symbioses with fungi. A similar mutualism with fungi is also noted in termites within the subfamily Macrotermitinae which are widely distributed throughout the Old World tropics with the highest diversity in Africa.
A sclerotium, is a compact mass of hardened fungal mycelium containing food reserves. One role of sclerotia is to survive environmental extremes. In some higher fungi such as ergot, sclerotia become detached and remain dormant until favorable growth conditions return. Sclerotia initially were mistaken for individual organisms and described as separate species until Louis René Tulasne proved in 1853 that sclerotia are only a stage in the life cycle of some fungi. Further investigation showed that this stage appears in many fungi belonging to many diverse groups. Sclerotia are important in the understanding of the life cycle and reproduction of fungi, as a food source, as medicine, and in agricultural blight management.
The term mycangium is used in biology for special structures on the body of an animal that are adapted for the transport of symbiotic fungi. This is seen in many xylophagous insects, which apparently derive much of their nutrition from the digestion of various fungi that are growing amidst the wood fibers. In some cases, as in ambrosia beetles, the fungi are the sole food, and the excavations in the wood are simply to make a suitable microenvironment for the fungus to grow. In other cases, wood tissue is the main food, and fungi weaken the defense response from the host plant.
Ophiocordyceps unilateralis, commonly known as zombie-ant fungus, is an insect-pathogenic fungus, discovered by the British naturalist Alfred Russel Wallace in 1859, and currently found predominantly in tropical forest ecosystems. O. unilateralis infects ants of the tribe Camponotini, with the full pathogenesis being characterized by alteration of the behavioral patterns of the infected ant. Infected hosts leave their canopy nests and foraging trails for the forest floor, an area with a temperature and humidity suitable for fungal growth; they then use their mandibles to attach themselves to a major vein on the underside of a leaf, where the host remains after its eventual death. The process, leading up to mortality, takes 4–10 days, and includes a reproductive stage where fruiting bodies grow from the ant's head, rupturing to release the fungus's spores. O. unilateralis is, in turn, also susceptible to fungal infection itself, an occurrence that can limit its impact on ant populations, which has otherwise been known to devastate ant colonies.
The Macrotermitinae, the fungus-growing termites, constitute a subfamily of the family Termitidae that is only found within the Old World tropics.
A fungus is any member of the group of eukaryotic organisms that includes microorganisms such as yeasts and molds, as well as the more familiar mushrooms. These organisms are classified as one of the traditional eukaryotic kingdoms, along with Animalia, Plantae and either Protista or Protozoa and Chromista.
Euprenolepis procera is a species of ant found in the rainforests of South East Asia. It was first described by Carlo Emery, an Italian entomologist, in 1900. In 2008, Witte & Maschwitz discovered that E. procera specialises in harvesting mushrooms in the rainforest for food, representing a new, previously unreported feeding strategy in ants.
The mycorrhizosphere is the region around a mycorrhizal fungus in which nutrients released from the fungus increase the microbial population and its activities. The roots of most terrestrial plants, including most crop plants and almost all woody plants, are colonized by mycorrhiza-forming symbiotic fungi. In this relationship, the plant roots are infected by a fungus, but the rest of the fungal mycelium continues to grow through the soil, digesting and absorbing nutrients and water and sharing these with its plant host. The fungus in turn benefits by receiving photosynthetic sugars from its host. The mycorrhizosphere consists of roots, hyphae of the directly connected mycorrhizal fungi, associated microorganisms, and the soil in their direct influence.
An ectomycorrhiza is a form of symbiotic relationship that occurs between a fungal symbiont, or mycobiont, and the roots of various plant species. The mycobiont is often from the phyla Basidiomycota and Ascomycota, and more rarely from the Zygomycota. Ectomycorrhizas form on the roots of around 2% of plant species, usually woody plants, including species from the birch, dipterocarp, myrtle, beech, willow, pine and rose families. Research on ectomycorrhizas is increasingly important in areas such as ecosystem management and restoration, forestry and agriculture.
Fungal-bacterial endosymbiosis encompasses the mutualistic relationship between a fungus and intracellular bacteria species residing within the fungus. Many examples of endosymbiotic relationships between bacteria and plants, algae and insects exist and have been well characterized, however fungal-bacteria endosymbiosis has been less well described.
Orchid mycorrhizae are endomycorrhizal fungi which develop symbiotic relationships with the roots and seeds of plants of the family Orchidaceae. Nearly all orchids are myco-heterotrophic at some point in their life cycle. Orchid mycorrhizae are critically important during orchid germination, as an orchid seed has virtually no energy reserve and obtains its carbon from the fungal symbiont.
A mycoparasite is an organism with the ability to parasitize fungi.
Leucocoprinus gongylophorus is a fungus in the family Agaricaceae which is cultivated by certain leafcutter ants. Like other species of fungi cultivated by ants, L. gongylophorus produces gongylidia, nutrient-rich hyphal swellings upon which the ants feed. Production of mushrooms occurs only once ants abandon the nest. L. gongylophorus is farmed by leaf cutter ant species belonging to the genera Atta and Acromyrmex, amongst others.
Hemibiotrophs are the spectrum of plant pathogens, including bacteria, oomycete and a group of plant pathogenic fungi that keep its host alive while establishing itself within the host tissue, taking up the nutrients with brief biotrophic-like phase. It then, in later stages of infection switches to a necrotrophic life-style, where it rampantly kills the host cells, deriving its nutrients from the dead tissues.
Gigaspora margarita is an Arbuscular Mycorrhizal Fungi (AMF) which means it is an obligate symbiont that creates mutualistic relationships with many different plant species. Being an AMF, G. margarita does not produce a fruiting body. All of its mycelium will be found in the soil, associating with plant roots. Though hard to distinguish between different species of AMF, microscopic distinctions can be made. A prominent morphological distinction for species in the Gigasporaceae family is their large sized spores. Gigaspora margarita is characterized by its large, white, pearl-like spores found anywhere from 260 - 400 micrometers. This is where it gets its name as margarita in Latin means pearl.
Trichoderma atroviride is a filamentous fungal species commonly found in the soil. This fungal species is of particular interest to researchers due to the plethora of secondary metabolites it makes which are used in industry The genus Trichoderma is known for its ubiquity in almost all soils and being easy to culture. Many Trichoderma's are also avirulent plant symbionts.
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