CHAPTER 17
Food and Technology
AS WELL AS being directly used for food, fungi have traditionally been the agents of fermentation for beer, cider, wine, and bread in Britain and Europe, plus a remarkable range of fermented products in the Far East, Africa, and around the world. In the industrial age, fungi have been used commercially in the manufacture of many other food-related products, from citric and oxalic acids to glycerine, fats, and proteins. Marmite™ and Quorn™ are also examples of factory-processed fungal products, as are fungal pharmaceuticals and antibiotics (Chapter 15). In other areas of technology, fungi again have important roles to play as biocontrol agents for unwanted pathogens and as bioremediation agents for unwanted chemicals.
FUNGI FOR FOOD & DRINK
Wild fungi
Fungi, along with seafish and shellfish, are among the last commercial foodstuffs hunted and collected in the wild. The reason is quite straightforward. Although a number of saprotophic and parasitic macrofungi can successfully be cultivated, sought-after ectomycorrhizal species like boletes (porcini or ceps), chanterelles, and truffles are as yet extremely difficult or impossible to grow.
Apart from field mushrooms, collecting wild fungi has always been a minority interest in Britain, long notorious as one of Europe’s few mycophobic nations (in company with Ireland, Belgium, and Holland). Nonetheless, in recent years there has been a greater willingness to sample new foods (Fig. 150) and an equal interest in collecting ‘food for free’. A survey of the top twenty edible fungi collected in Britain for personal use by enthusiasts placed Boletus edulis (the cep) first, followed by Macrolepiota procera (parasol), Agaricus campestris (field mushroom), Cantharellus cibarius (chanterelle), Lepista nuda (wood blewit), Coprinus comatus (shaggy ink cap), Calvatia gigantea (giant puffball), Agaricus arvensis (horse mushroom), Boletus badius (bay bolete), and Lepista saeva (blewit). The next ten included morels, hedgehog fungi, and oyster caps.
In Scotland, apart from collecting for personal use, the wild fungus trade was worth around £400,000 per year in the 1990s and involved some 350 people. The main species collected were chanterelles (Cantharellus cibarius), ceps (Boletus edulis), and hedgehog fungi (Hydnum repandum), over half of which were exported from the UK. Less than 15% remained in Scotland, where they were sold to specialist greengrocers and restaurants. The total trade in UK-collected fungi is currently estimated at around £2,500,000 p.a.
FIG 150. A wide range of tinned, bottled, and dried fungi are now widely available in delicatessens, supermarkets and speciality shops (RBG Kew).
Elsewhere, the trade is substantially higher. In Europe, major exporters include the Scandinavian countries, Baltic states, Spain, Eastern Europe, and the Balkans. In both Finland and Lithuania, for example, the value of edible fungi collected in native forests was estimated (in 1995) at around £10,000,000 per year, and in the Czech Republic considerably more at over £30,000,000 per year. Outside Europe, in the Pacific Northwest of the USA and Canada, around 2,000,000 kg p.a. of wild fungi were commercially harvested in the 1990s, the main groups being morels, chanterelles, matsutake, and boletes. Over 10,000 people were involved in the trade, as pickers, processers, and retailers, with the industry having a gross value of around £30,000,000 p.a.
Chanterelles and their allies
Chanterelles (Cantharellus cibarius), and their allies (principally C. tubaeformis, C. aurora, and Craterellus cornucopioides), are widely collected and marketed in Europe where they are found as ectomycorrhizal associates of forest trees. Their retail price (‘fresh’) varies, but is currently around £15–£30 per kilo. Globally, the trade in wild chanterelles and related species is estimated to be worth just over £1,000,000,000 per year. In North America, substantial quantities are collected in the Pacific Northwest mostly involving the species C. formosus and C. subalbidus. Turkey exported over 150 tons of chanterelles in 1990, mainly to Italy and Germany whilst, perhaps surprisingly, species like C. rufopunctatus from the savannah-like ‘miombo’ woodlands of central Africa, are exported in large quantities to Europe.
It was not always thus. Badham (1847) noted that ‘the Canth. cibarius is very abundant about Rome, where it fetches, not being in great esteem, from twopence to twopence halfpenny a pound’. At that time the chanterelle was also eaten in Britain, though Badham suggested that ‘the very existence of such a fungus at home is confined to the Freemasons who keep the secret!’. It was certainly a secret known only to a few. Britten (1877) remembered ‘on one occasion encountering a woodman who was lost in wonderment at our having collected a basket of ‘toadstools’…and when we told him that we were going to eat them, clearly thought our claim to a select apartment in the nearest lunatic asylum was absolutely indisputable’.
Boletes – ceps and porcini
Boletes, known as ‘ceps’ in France and ‘porcini’ in Italy, are also widely collected and some species are as sought after as chanterelles. The premium species is Boletus edulis (Fig. 151), but many other taxa of Boletus (including Xerocomus), Leccinum, and Suillus are also picked on a commercial scale. The global trade in these fungi is substantial. Turkey exported over 700 tons of boletes in 1990, and Arora (2000) noted that, by selling boletes to Italy, impoverished farmers in Bulgaria were earning enough to buy new tractors. In Britain, dried sliced boletes have long been available but, increasingly, ‘fresh’ specimens (some from as far afield as South Africa) can be found in supermarkets and delicatessens retailing at around £20–£50 per kilo.
FIG 151. Sometimes called the ‘penny bun bolete’, the cep Boletus edulis is one of the most popular wild, edible fungi in Europe (P. Roberts).
Morels
Morels (Morchella species) are among the largest of the ascomycetes and have long been valued as food. Unusually for larger fungi, they produce fruitbodies in the spring and in Victorian times were occasionally sold fresh in Covent Garden, though more generally obtained dried from Germany. Some species, notably Morchella conica and M. elata, are often associated with burnt ground, so much so that (according to Britten) ‘the peasants of Branderburgh and some other parts of Germany…set fire to the forests in order to obtain these fungi’, an occurrence so prevalent that it was prohibited by law. A more recent example of the same practice has been reported from Oregon in the USA.
Morel hunting is a favourite and lucrative springtime occupation in the United States. Weber (1988) provided a first-hand account of the morel season in Michigan, which involves several thousand people, festivals and competitions, and is a major part of the local tourist economy. In the 1980s morel hunting was said to bring in over £1,000,000 p.a. to the Cadillac region alone. The species collected include Morchella conica, M. esculenta (Fig. 152), and M. semilibera.
FIG 152. The morel Morchella esculenta is a large, spring-fruiting species with a preference for chalky ground. It is a sought-after edible species (B. Spooner).
North America and Turkey are said to be the major exporters of morels into Europe. Turkey produced nearly 50 tons in 1989, whilst Pakistan exports around 50 tons each year. At one time morels were also exported from Afghanistan.
Since the 1980s, it has also been possible to cultivate morels on a commercial scale, and a patent has been taken out on the process in the USA.
Matsutake and the white gold rush
Tricholoma matsutake is a large, edible species, found as an ectomycorrhizal associate of pine in the Far East. It has long been harvested as a seasonal speciality in Japan, where it is particularly valued for the aroma of the young, fresh fruitbodies (there is no market for it dried). In 1950, over 6000 tons were harvested in Japan, but by 1984 this had fallen to just 180 tons, possibly because of pollution and changes in forest management. Part of this shortfall was taken up by substantial imports from Korea, China, and Tibet (where some villagers have been earning ten times the local salary by collecting the fungus, building ‘matsutake mansions’ on the proceeds). But part also was taken up by the importation of a related American species, Tricholoma magnivelare, the ‘pine mushroom’. Altogether, global trade in Tricholoma matsutake and T. magnivelare is now estimated to be worth up to £3,500,000,000 per year.
With prices up to £30 per kilo being paid to collectors of T. magnivelare, the Japanese demand for the fungus has led to a ‘white gold rush’ in America. Tricholoma magnivelare is found from Alaska and the Yukon down to California and Mexico, with further populations running down from Quebec to the Great Smoky Mountains in Tennessee. Japanese Americans were collecting the species as far back as the 1930s, but the real boom started in the 1970s, when prices enabled some pickers to earn well over £500 per week in season. When this income rose to over £1000 per day in the late 1980s, turf wars broke out provoking headlines like ‘Mushrooms, guns, and money’ or ‘Bloody war erupts in US wilds – over mushrooms’. Added to this is the problem that the pine-mushroom industry is now worth far more than the traditional timber industry, producing conflicts between itinerant pine-mushroom pickers and resident loggers. Arora (1999) has written an engaging, illustrated account of the itinerants’ fiercely independent way of life. There is an additional conservation problem, since in America the most valuable button fruitbodies are often located by raking instead of being carefully hand-picked. This destroys the forest litter layers together with the mycelia of T. magnivelare and other ectomycorrhizal and saprotrophic species. As a result, there is now some regulation of collecting in parts of North America, including licensing (though the Texas ban on harvesting mushrooms more than six feet tall or three feet in diameter would seem less than effective).
Truffles and truffle-hunting
Truffles are ectomycorrhizal ascomycetous fungi which produce tuber-like fruitbodies underground, often at the interface between leaf-litter or humus layers and the harder, mineral-soil surface. Most of the edible species belong to the ‘true truffles’ in the genus Tuber, a few to the genus Terfezia. Since their spores are typically spread by the ingestion and defecation of animals (including insects, rodents, wild pigs, and the like – see Chapter Five), many truffles have enticing aromas when mature, some of which are also attractive to human beings.
Several species are collected commercially. The Piedmont or white truffle, Tuber magnatum, is the most pungent, sought-after and highly priced. It grows almost exclusively in northern and central Italy, with some small production in Slovenia and Croatia. Typical sites are on low hills (around 400–500 m) in open woodland, where it occurs as an ectomycorrhizal associate of oak and poplar, often in woodlands with walnut, and is collected in the autumn, between October and December. It is hunted with dogs, often (for no apparent reason) with two dogs, one of which locates the truffles, sits on the spot and barks, and is then replaced by the second dog which does the digging. Small spaniels seem to be favoured (Fig. 153). The headquarters of the white truffle trade is Alba, which holds an annual fair for the ‘tartufo bianco’ or ‘tartufo di Alba’. Around 5–20 tons are produced each year and retail prices range from £1400–£1900 per kilo, making it one of the most expensive foodstuffs on earth. In 2000, Milanese shops were asking no less than £4000 per kilo, whilst the top auction price reached an astonishing £9800 per kilo (50% more than the price for gold).
The Périgord or black truffle, Tuber melanosporum, is perhaps the best-known, thanks to its connections with French haute cuisine. It grows on well-drained, rather dry, sunny, calcareous hillsides (around 200–1000 m) in southern France, Italy, Spain, Portugal, Slovenia, Croatia, and Serbia. Associated trees are typically species of oak, but also include hazel, hornbeam, limes, and even conifers. In Italy, it tends to occur in rather scrubby areas, often old, abandoned hill farms, and is hunted with dogs, since a considerable amount of ground needs to be covered. In France, trufflers tend to own their private, inherited patch of truffle woodland and Tuber melanosporum can therefore still be hunted for by pigs, which are not willing to travel fast or far. The pigs are specifically sows, since the truffle aroma is similar to boar pheromone, a remarkably effective attractant. As a consequence, sows hunt truffles naturally and the problem for the hunters is to prevent them from immediately eating their finds. Dogs have to be trained to collect truffles. Tuber melanosporum is collected between November and March, and hence is sometimes known as the winter truffle. Retail prices fluctuate, but are currently around £250–£320 per kilo. The main market for the Périgord truffle is France itself. At the beginning of the last century, some 1000 tons were produced in France each year, but this has now collapsed to just 20–40 tons, probably as a result of changes in upland management. Italy produces around 30–50 tons per year, some of which are eaten locally, some exported. Around 30 tons are produced annually in Spain, most of which are exported to France.
FIG 153. A professional truffle hunter and dog in search of the Piedmont or white truffle Tuber magnatum in Italy (P. Roberts).
The summer truffle, Tuber aestivum, is far less pungent, far more widespread, and much less favoured (Fig. 154). It occurs in Britain and was once commercially hunted in southern England. Gilbert White, the celebrated naturalist of Selbourne in Hampshire, mentioned regular visits by truffle-hunters in his journals, as did his brother Henry in his diaries. A note of Gilbert White’s for August 1767, for example, says ‘Trufles…large & in plenty were taken by the trufle-hunters dogs Aug: 19 at Fyfield in a field of my Bror Henry’s, among the roots of a Grove of beeches.’ Another, for 11–17th October 1789 says ‘A trufle-hunter called on us, having in his pocket several large trufles found in the neighbourhood…Half a crown a pound was the price, which he asked for this commodity’. Half a crown a pound (27.5p per kilo) was a substantial sum of money in the eighteenth century.
FIG 154. A drawing of the truffle Tuber aestivum, once commercially hunted in England (E.Wakefield, RBG Kew).
Britten (1877) gave an account of a meeting with a truffle-hunter and his dog in Buckinghamshire and reprinted a description of the breed of dog concerned. The English truffle-dog was said to be white, black and white, or black, and similar to a small poodle, though rather longer in the leg (Fig. 155). In 1860 the truffle-hunters of Winterslow in Wiltshire petitioned parliament for an exemption from dog licences, claiming that they were ‘poor labouring men’ dependent on truffling for which ‘we do therefore keep and use a small pudle sort of dog’. It was not recorded whether the petition was successful. By 1891, Cooke noted that the truffle-dog was ‘now almost a rarity’.
Cooke also claimed that truffle hunting was formerly practised in Sussex and Kent, whilst Rolfe & Rolfe (1925) reported that ‘a few of the old truffle hunters are still to be found in Sussex’. Pigs were apparently still used in Sussex until about 1910, but truffle-dogs were more usual. Once located, the Sussex trufflers used a ‘spud’ made of ash wood to dig up the truffles.
The English truffling trade had died out by the end of the 1930s. One of the last local truffle-hunting families were the Olivers of Seven Points, and Ramsbottom (1953) named Alfred Collins as the last of the professional trufflers. Alfred, son of Eli Collins (also a truffler and possibly one of the petitioners mentioned above), was based in Winterslow, Wiltshire, but hunted as far afield as Somerset, Dorset, Oxfordshire, Berkshire, Surrey, Sussex, and the Isle of Wight. He used truffle-dogs or terriers, often carried poacher-style in pockets of a large coat, and a ‘spike’ to dig up truffles. Two kinds of truffle were hunted, ‘garlic’ (Tuber aestivum) and the smaller, paler ‘bud’ (possibly T. brumale). His price was 4s 6d per pound (50p per kilo) and the truffles were despatched all over the country. He gave up truffling in 1940, but, according to his daughter (Moody, 1985), his spikes and other memorabilia are in Salisbury Museum.
Truffles, however, continue to occur in England and, indeed, north into Scotland. The main species, Tuber aestivum, is normally found between May and October, and is still collected commercially in Italy, where the annual production is around 3–10 tons, and in France which produces around 10–15 tons. It retails for around £50 per kilo.
In France and more recently in Italy, considerable effort has been expended on ways to cultivate truffles. Since the species concerned are ectomycorrhizal, this is not possible in the conventional manner. But, beginning in the nineteenth century, attempts were made to sow acorns or grow oaks and other saplings in appropriate truffle-producing sites (truffières), sometimes ‘seeding’ the ground with spores or impregnated soil. In more recent years, substantial forestry programmes have been initiated involving the inoculation of oak and hazel saplings with Tuber species and then planting them out in the hope of a harvest in future years. This has already produced results, not only in Europe, but in Australia and New Zealand, both of which have areas where the soil and climate are suitable for Tuber melanosporum. Tasmania now has six truffières in production, with over 20 more planted. New Zealand also has six productive truffières and harvested its first commercial crop in 1997. In the similar hope of success, an attempt has been made to establish the first British truffières, starting in Hertfordshire in 1999.
In North Africa and the Middle East through to Iran, a relative of the truffles, Terfezia arenaria or the desert truffle, is widely eaten and sold in local markets. It is an ectomycorrhizal species associated with members of the Cistaceae, and there are other species in the Kalahari and elsewhere. Terfezia arenaria was considered a particular delicacy by the ancient Romans and is one of the many contenders for the ‘manna’ of the bible. In Britain, the basidiomycetous false truffle Melanogaster variegatus was at one time sold in the markets of Bath, Somerset, and was known as the ‘Bath truffle’. Rolfe & Rolfe (1925) also noted that ‘gentlemen from Soho’ collected the earthball Scleroderma citrinum as a substitute for truffles, notwithstanding the fact that it is poisonous. Perhaps not surprisingly, due to the high prices they command, this is not the only fraud involving truffles. Blackening cheaper white truffles with walnut juice to pass them off as more expensive species, and treating other dark-coloured fungi with artificial truffle flavour to fool inexperienced buyers are just two of many examples. Pegler et al. (1993) have provided a thorough, illustrated, taxonomic handbook on native British truffles and truffle-like fungi. Dubarry & Bucquet-Grenet (2001) have produced a nicely illustrated pocket guide to the ecology, history, and gastronomy of French and other European truffles.
Hedgehogs, lobsters, and other commercial species
Many other wild fungi are sold commercially, either ‘fresh’ or processed (dried, tinned, bottled, or frozen), and are frequently exported around the world.
In Britain, the traditional trade was almost entirely confined to the field mushroom (Agaricus campestris) and the horse mushroom (A. arvensis), both of which supplemented the shortfall in supplies of cultivated mushrooms. In times of glut, mushrooms were also made into a preserved sauce or ketchup. Berkeley in 1860 noted that an English ‘ketchup-merchant’ of his acquaintance had no less than 800 gallons on hand from local collections in a single season, with prices for ketchup mushrooms ranging from a penny to fivepence a pound (1p–4.5p per kilo). Rolfe & Rolfe (1925) reported that there was formerly some trade at Covent Garden in blewits (Lepista saeva) and parasols (Macrolepiota procera) for the same reason, but that this had ‘fallen away or entirely disappeared’ with the increase in mushroom cultivation. Blewits, however, continued to be sold in markets in the Midlands (from Gloucestershire to Nottinghamshire) up until more recent times. Britten (1877) noted that the polypore Grifola frondosa was ‘sometimes sold in the market at Norwich under the name of ‘morel’ (to which it certainly has no claim), at prices varying from sixpence to eighteenpence according to size’. The same species was also said to be valued in Italy and is now commercially grown in Japan.
The trade in Britain today is quite different and owes nothing to tradition, but to a general interest in exotic and unusual foods. The species sold are a cosmopolitan mix of cultivated and (generally) imported wild fungi, typically given French, Japanese, Chinese, or American names. In continental Europe, however, the trade is more traditional and to a certain extent local, though many species are shipped throughout the continent or imported from America and elsewhere. Among the more popular are hedgehog fungi or ‘pieds de mouton’ (Hydnum repandum); the fairy-ring champignon or ‘mousseron’ (Marasmius oreades); the saffron milk cap (Lactarius deliciosus), a species particularly favoured in Catalonia where it is known as ‘rovellons’; Tricholoma portentosum, known as ‘fredolics’ in Catalonia; the charcoal-burner or ‘charbonnier’ (Russula cyanoxantha); the cauliflower fungus (Sparassis crispa); grisettes (certain Amanita species); and many more. Even the honey fungus (Armillaria mellea agg.), characterised by Badham (1847) as ‘a nauseous disagreeable fungus…so repugnant to our notions of the savory, that few would make a second attempt, or get dangerously far in a first dish’, is widely eaten, particularly in Poland, where it is available fresh or preserved in jars.
The same or equivalent species are marketed in North America, with the addition of the peculiar ‘lobster fungus’, actually fruitbodies of Russula and Lactarius species which are parasitised by an ascomycete, Hypomyces lactifluorum. This covers its host toadstools in conspicuous reddish-orange mycelium, completely replacing the gills (Fig. 156). The parasitised fruitbodies are widely collected and sold, a usage which appears to be traditional among native American peoples. It is even occasionally imported into Britain.
Elsewhere, there are some distinctly local specialities. In Chile and Argentina, species of the curious golfball-like ascomycete Cyttaria can be found growing on southern beech trees (Nothofagus species). Darwin noted that the inhabitants of Tierra del Fuego collected and ate them as part of their staple diet and they continue to be sold in markets in Chile today.
In Haiti, one or more Psathyrella species, toadstools related to ink caps, are collected and eaten as part of a national dish called ‘riz noir’ or ‘riz djon-djon’ (djon-djon being the creole word for mushroom). The fungi are sold fresh or dried and exported in the latter state to Haitian communities overseas. In Mexico and Central America the corn smut, Ustilago maydis, which forms large galls on sweet corn (Zea mays), is widely eaten as a delicacy under the name ‘cuitlacoche’ and is sold fresh or tinned. A related smut, Ustilago esculenta, which galls wild rice (Zizania aquatica), is also eaten in China and the Far East.
FIG 156. The so-called ‘lobster fungus’, fruitbodies of Lactarius infected with the ascomycete Hypomyces lactifluorum. They become bright reddish-orange and are a sought-after delicacy (S. Evans).
Traditional collecting of wild fungi
An autumn visit to local markets in many continental European countries will often reveal an extraordinarily wide range of fungi on sale, not only the commercially marketed species noted above, but other less common, less favoured, or locally appreciated species (Fig. 157). In some countries, these markets are carefully licensed and controlled, so that only a limited range of permitted species can be offered for sale. Badham (1847) noted the appointment of an official ‘Ispettore dei Funghi’ in Rome, tasked to examine specimens brought in to market, tax those suitable for sale (a halfpenny on every ten pounds weight), and dispose of those which were rotten or dangeous by throwing them into the Tiber. Similar inspectors are employed in Switzerland and elsewhere today.
In Finland, an historically mycophobic nation, the collection of edible wild fungi has been officially encouraged by the government, who instituted a programme to train 1650 advisers and 50,000 collectors between 1969 and 1983. Curiously, Lactarius species are amongst the most favoured by the Finns, including Lactarius torminosus (the epithet means ‘griping’ or ‘fretting of the guts’).
In Africa, the use of fungi varies from region to region and culture to culture. Over 60 species of fungi are said to be collected as edible in Malawi, but in parts of Nigeria and other areas fungi are often associated with dung and decay and are widely shunned. Rammeloo & Walleyn (1993) have published a survey of sub-Saharan edible fungi.
In various places, the large, ball-like sclerotia of certain bracket fungi have been used as a foodstuff, sliced and eaten as a ‘native bread’. In Australia, this was known as ‘blackfellow’s bread’, and a massive specimen (now in the Herbarium at Kew) was displayed at the Great Exhibition of 1851. A similar polypore sclerotium (of Wolfiporia cocos) was collected for food in Japan and also in North America, where it was given the name of ‘tuckahoe’ or Indian bread. This species, called ‘fu ling’, is still much used in China and the Far East as a traditional tonic for ‘invigorating the spleen and tranquilising the mind’.
In Europe, the ‘fungus stone’, ‘pietra fungeia’, or ‘lapis fungifer’ was noted as a mediaeval marvel, associated with ‘the mysteries of the Lynx’ and believed to be the urine of wolves coagulated on mountain summits. When watered, this magical stone produced mushrooms and was much sought after by collectors of curiosities. Samuel Pepys much desired a specimen, whilst the Earl of Stafford actually possessed one. It is in fact the sclerotium of another polypore, Polyporus tuberaster, partly mixed with stones and earth.
Lichens have seldom been used for food (most are tough and bitter), but Iceland moss, Cetraria islandica, was once boiled in alkaline ashes and ground into a flour to ‘constitute the basis of the food of the poor Icelander’ (Lindsay, 1856). It is said that this was a useful ingredient of Scandinavian ship’s biscuits, since even weevils would not eat it. Rock tripe (Umbilicaria species) was also used in extremis, as in Sir John Franklin’s ill-fated expedition of 1819-22 to find the northwest passage, when his starving men ate lichen scraped from the rocks, as well as the leather from their boots, and possibly each other.
In the Far East, under less desperate conditions, another Umbilicaria species (U. esculenta – the name suggesting edibility) is favoured as a food in Hunan (China), Japan, and Korea. This is known as ‘Iwa-take’ or ‘rock-mushroom’, and similarly grows in rocky places, though usually on inaccessible cliffs where collecting is fraught with danger, commanding high market prices as a result. In the Middle East, Sphaerothallia esculenta, a desert lichen which blows in the wind like tumbleweed, is one of many organisms which have been claimed as the ‘manna’ of the bible. It can apparently be mixed with meal and baked as a bread, called ‘schirsad’ in Iran, and (according to Lindsay, 1856) ‘has sometimes served as food for hordes of men and cattle in the arid steppes of various countries between Algiers and Tartary’. Also in the Middle East, it is said that the ancient Egyptians were fond of adding Pseudevernia furfuracea to flour for breadmaking. This is the species still used in perfumery today (Fig. 145A) and would have given an unusual flavour to the bread. The lichen had to be imported by ship from Greece, so was clearly not eaten out of desperation. It was also one of the many items used in mummy embalming, being used with myrrh and other ingredients to pack the body cavity.
Cultivated mushrooms
Worldwide, around 4,250,000 tons of mushrooms and other macrofungi are grown for food each year. Almost 40% of this production is devoted to Agaricus bisporus and A. bitorquis, the familiar cultivated mushrooms of the western world.
The deliberate growing of mushrooms (as opposed to the picking of field mushrooms, Agaricus campestris) is believed to have started in France some 350 years ago. Atkins (1979) quoted instructions given by De Bonnefons in 1650 for preparing ‘a bed of Mules’or Asses’ soyl’ four fingers thick, casting upon it ‘all the parings and offalls of such Mushrooms as have been dressed in your Kitchen, together with the water wherein they were washed’, to obtain a ‘very good’ crop. More reliable methods, leading eventually to large scale commercial production, were rapidly developed, and in 1707 Tournefort gave the first scientific account of growing mushrooms in ridged beds for the Paris market.
French commercial cultivation was subsequently undertaken in disused mines in the former Seine department around Paris, the mines providing stable, year-round temperature and humidity. Robinson (1883) gave an English visitor’s account of the ‘great mushroom caves’. By 1918, over 300 commercial growers were based in these excavations, often working in conditions as difficult and dangerous as those suffered by the original miners. The mushrooms were grown on ridged beds of stable manure which was thrown down shafts and wheeled into place, sometimes along adits less than a metre high. Mushroom spawn (mycelium) was spread over the beds which were then cased (covered) with fine soil and kept moist with water. Fresh mushrooms appeared after some six weeks and continued to crop for up to eight months, after which the spent material was carted back to the surface and new beds made. Around 25 tons of mushrooms were produced each day, far more than in any other European country. Even today, Agaricus bisporus is still known in France as the ‘champignon de Paris’.
This French system was copied on a limited scale in Britain, the most extensive underground workings being in the old bathstone quarries at Corsham, Wiltshire. Other subterranean farms were at Bradford-on-Avon, also in Wiltshire, Godstone in Surrey, and in a disused railway tunnel in Edinburgh. The Bradford-on-Avon caves are still in use for mushroom growing today. An alternative ‘English method’ was to grow mushrooms in sheds, glasshouses, or even in the open (when the beds were covered in protective litter).
The modern system of growing mushrooms in sheds on shelves or trays (also in bags or troughs) was first developed in the United States in the 1890s and mechanised by the Dutch in the 1970s. Van Griensven (1988) has provided a thorough account of modern, commercial mushroom production.
Some 65,000 tons of mushrooms were produced in the UK in 2000, worth around £120,000,000. Worldwide, the value of the industry has been estimated at around £2,800,000,000 per year. Agaricus bisporus (A. brunnescens in the USA) is the main commercial species, grown in several different strains. At the beginning of the last century, cultivated mushrooms were typically cream or brown and often scaly, but in 1927 a cluster of white, scaleless fruitbodies was found growing amidst brown specimens and all modern white mushrooms are said to originate from this strain. Today ‘white strains’, ‘offwhite strains’, hybrid ‘white-offwhite strains’, and the original ‘brown strains’ are grown for different purposes. The first and last are marketed fresh, the brown strains as ‘chestnut’ mushrooms in Britain and ‘portabella’ or ‘crimini’ mushrooms in the USA (all invented commercial names for strains previously considered unsaleable), whilst the offwhite and hybrid strains are typically grown for canning and for processing.
Oyster caps, shiitake, wood ears, and monkey heads
Many other species of fungi have long been cultivated in the Far East and have increasingly penetrated western markets since the 1980s. Of these, oyster caps (Pleurotus species) account for over 20% of the annual world market for cultivated macrofungi, with shiitake (Lentinula edodes) and wood-ears (Auricularia cornea) accounting for over 10% each. All of these are saprotrophic or parasitic species and can be grown on dead wood or waste products.
Oyster caps, Pleurotus species, are now widely cultivated and easily available in British supermarkets. Pleurotus cornucopiae, a whitish species, and P. ostreatus, a typically greyish or bluish-brown species, are both common on hardwood logs in the wild in Britain, but are also grown commercially. Pink varieties of the common tropical species Pleurotus djamor are also cultivated, as is the oriental, yellow species P. citrinopileatus. All oyster caps are fleshy, gilled fungi which normally occur on decaying wood and are said to be ‘by far the easiest and least expensive [edible fungi] to grow’ (Stamets, 1993). Like shiitake, they can be grown on logs, but are so tractable that they are easily cultivated on any of a wide range of compacted waste products containing cellulose, including sawdust, straw, sugar cane bagasse, cottonseed hulls, oil palm waste, banana leaves, and coffee waste. Unusually, growing Pleurotus species appears to have been a comparatively recent American innovation from the turn of the last century, rather than a long-established Asian tradition.
Growing shiitake (Lentinula edodes) is, however, a venerable occupation, having been practised in China and Japan for at least the last 1000 years. Shiitake is a gilled, fleshy fungus which grows wild in the cooler forests of China, Japan, and Korea on logs and fallen branches of oak and ‘shii’ (Castanopsis species). Traditional cultivation consists of little more than encouraging this growth by felling logs of suitable size, drilling holes in them, and inserting wedges of wood mixed with mycelium from logs already supporting the fungus. This semi-natural, seasonal form of cultivation is still valued today, since it is said to produce the best quality shiitake which in turn fetch the highest prices.
China produced over 90,000 tons of shiitake in 1997, one third of which was exported. Most of this was undertaken by small rural farmers in the central highlands and it has been estimated that production on this scale requires the felling of some 100,000 trees each year, leading to massive deforestation. Methods of growing shiitake on compacted blocks of enriched sawdust have been developed which may be less destructive. These methods have also led to widespread cultivation of the fungus outside its natural range, not only in Asia but in Europe and North America. Since it currently retails (fresh) for around £10–25 per kilo in the west, shiitake-growing has been taken up by many small businesses, including some in Britain where it is now widely available fresh or dried in supermarkets.
Auricularia species are believed to be the first macrofungi deliberately grown for food, having been mentioned in a seventh century Chinese text. The main cultivated species, Auricularia cornea (synonym A. polytricha), sometimes known as the wood-ear, is a relative of the common British jew’s ear fungus (A. auricula-judae) and is widely found throughout the tropics and subtropics on dead and decaying wood. Though Auricularia species are extensively grown in the Far East, Oei (1996) noted that ‘taste and appearance may hamper [their] popularity in Western countries’, a reference to their thin, rubbery texture and delicate or imperceptible taste. Curiously, they are sold into the non-oriental market in Britain by being finely ground to tealeaf size and added to ‘woodland mushroom’ instant soups. Formerly they had some medical reputation in Britain (Chapter 15) and still retain this reputation in the Far East. Auricularia species are commercially grown in China and Taiwan on logs or in plastic tubes filled with an enriched sawdust or cottonseed hull mix. Despite their long history of cultivation, wood ears were once commercially collected in the wild, particularly in New Zealand. Indeed in the late nineteenth and early twentieth century, Auricularia was New Zealand’s second largest cash export after sheep, with over 1800 tons shipped to China between 1872 and 1883.
Tremella fuciformis is another ‘jelly fungus’, though only distantly related to Auricularia species. It is sometimes marketed as silver ears or white jelly fungus and has a white, frondose, seaweed-like appearance (Fig. 158). Like all Tremella species, it is parasitic on other fungi, a fact overlooked in traditional cultivation methods on logs, where the species grew fitfully whenever its host (the ascomycete Hypoxylon archeri) happened to be present. Nowadays, it is grown in China as a mixed host-parasite culture on logs or in plastic tubes filled with an enriched sawdust or cottonseed hull mix.
The paddy straw mushroom, Volvariella volvacea, is a pink-spored agaric with a large basal volva, but no ring. Fruitbodies are occasionally found in Britain, presumably as casual introductions, since it does not tolerate cold. The species is popular in south-east Asia, largely because it can be straightforwardly grown outdoors as a low-tech, low-cost crop. Traditionally, straw from the rice harvest was piled up to form raised beds in paddy fields and the mushrooms grown on that, but a variety of other substrates can be used including cotton waste, banana leaves, and even weeded-out water hyacinth, Eichhornia crassipes.
FIG 158. Sometimes sold as ‘silver ears’, Tremella fuciformis is an edible pantropical fungus, commercially cultivated in China (P. Roberts).
The velvet shank, Flammulina velutipes, has been cultivated in Asia since the ninth century or earlier. It is a frost-resistant, winter-fruiting agaric called ‘enokitake’ (snow peak mushroom) in Japanese and found throughout the temperate north, including Britain where it fruits in clusters on dead wood, particularly elm. Unusually for fungi, the cultivated form bears little resemblance to wild collections. This is purely a matter of technique. Flammulina velutipes is typically grown in plastic bottles containing an enriched sawdust mix. When beginning to fruit, collars are attached to the bottles and lighting is lowered to obtain dense bundles of long-stemmed, small-capped fruitbodies (sometimes sold as ‘golden needles’).
Hericium erinaceus, the monkey head or lion’s mane fungus, is a wood-rotting saprotroph producing large epaulet-like fruitbodies with a hymenium consisting of long, hanging spines (Fig. 163). It is a comparative newcomer to cultivation, but is quite easily grown on cellulose waste in a similar manner to Pleurotus species. The fungus occurs in England, particularly on old beech trees, but is scarce and legally protected under Schedule 8 of the Wildlife and Countryside Act 1981 (Chapter 18).
Several other fungi are cultivated for food on a comparatively small or local scale. The phalloid Dictyophora indusiata is widely cultivated in Asia, but (as a close relative of the stinkhorn) is unlikely to gain much acceptance in the west. The toadstools Stropharia ruguso-annulata (on mulch and in gardens) and Agrocybe cylindracea (on wood) are occasionally grown, as is the polypore Grifola frondosa, known as maitake in Japan. Blewits (Lepista saeva and L. nuda) are also now grown in Europe and generally marketed under the French name ‘pied bleu’.
Stamets (1993) has provided an excellent, illustrated guide to the small-scale growing of edible fungi in the west. A further standard text was published by Chang & Miles (1989).
Yeasts and the brewing of beer
Brewing from fermented grains appears to be almost as old as human civilisation, having been known to the ancient Sumerians some 9000 years ago, when up to 40% of their grain harvest was set aside for the production of beer. The addition of hops, an essential part of beer as we know it today, followed much later, in mediaeval times.
Production starts with the ‘malting’ of barley (or, more rarely, wheat or other cereals) by germinating it in warm damp conditions, causing the release of amylolytic enzymes which enable pectolytic enzymes to convert the grain starch into sugars. The dried and finished malt (known as ‘grist’ when milled) is ‘mashed’ in water at temperatures up to 75°C and the sweet liquid or ‘wort’ extracted and boiled with hops. After cooling and filtering, the wort is inoculated (‘pitched’) with various strains of the yeast Saccharomyces cerevisiae (brewer’s or baker’s yeast) which ferment the sugars into alcohol and carbon dioxide. The resulting rough ‘green beer’ is then further conditioned in casks or bottles, sometimes with the addition of extra hops and sugars, where a slow, secondary fermentation takes place. This fermentation continues up to the point when the beer is ready for drinking, the slow release of carbon dioxide giving the beer its sparkle and head.
In Britain, traditional brewing uses strains of ‘top-fermenting’ yeasts which rise through the wort to produce a foamy surface crust. In continental Europe and North America, ‘bottom-fermenting’ strains are used, in which the yeast sinks. This style of brewing is typical of lager and the yeast strain used is sometimes treated as a separate species, Saccharomyces carlsbergensis.
In modern, mass-market ‘beers’, the secondary fermentation is arrested by pasteurisation, creating a sterile liquid which is easy to transport, long-lasting, and requires no skill to manage. This liquid is carbonated during bottling, canning, or (with draught beers) at the point of sale, to produce a fizzy, beer-flavoured drink. A textbook on modern, industrial brewing methods was published by Hardwick (1995) with a more recent review paper by Hartmeier & Reiss (2002).
Cider and perry making
Cider is intrinsically easier to make than beer, since it depends on fermenting the natural sugars present in apples using the natural yeasts on the fruit. Apples are ground in a cider mill to form a thick ‘cheese’ which is then pressed in layers between straw or cloth to extract the juice. The yeasts present in the juice, principally Saccharomyces species, convert sugars into alcohol to form an initial rough cider; secondary bacterial fermentation then converts the sharp malic acids of the rough cider into milder lactic acids. Good quality ciders are still made from distinctive varieties of cider apples in the traditional cider counties (Cornwall, Devon, Somerset, Gloucestershire, Hereford, and Worcester) and from ordinary apples in Norfolk and south-East England. Other traditional cider centres include the Pays d’Auge area of Normandy and the Asturias region of Spain. As with beer, modern, mass-market ‘cider’ is a quite different drink made from apple concentrate, sugar, and various additives. It is pasteurised and then carbonated to produce a liquid that is bland, fizzy, and depressingly consistent.
Perry is made in a similar way to cider, but using perry pears, traditional varieties of which are still grown in small quantities, mainly in Gloucestershire, Hereford, and Worcester.
Wine, sake, and other fermented drinks
Wine is also made in a similar way to cider, the grapes being crushed to release the juice (‘must’) which is then naturally fermented by the yeasts, principally strains of Saccharomyces cerevisiae, growing with the fruit. A secondary, bacterial fermentation also takes place to convert malic acid into lactic acids. As with beer and cider, the whole process has long been industrialised, though with considerably more care. Mass-market wines are not normally carbonated, for example.
A mycologically interesting feature of certain sweet wines, principally Sauternes, is that the grapes are allowed to rot on the vine before harvesting. The rot, Botrytis cinerea, is the ubiquitous grey mould prevalent on soft fruits and other plant parts (Chapter Five) and normally regarded as a destructive pathogen. On grapes, however, initial attack by the ‘noble rot’ tends to shrivel the fruit and concentrate the sugars, many of which remain after fermentation.
The Japanese rice wine, sake, is made using a substantially different process. Rice is first fermented with the mould Aspergillus oryzae, to form a ‘koji’ starter (similar to soy sauce production, below). Further steamed rice is then added to the koji, together with water, and a traditional yeast mix containing Saccharomyces cerevisiae, to form a seed yeast stage or ‘moto’. Further koji, water, and steamed rice are added in stages to form a complex ‘moromi’ or mash from which the sake is finally removed by filtration.
Toddy or palm wine is a sweet fermented drink made from the sap of various palms in West Africa, India, South-East Asia, and South America. It contains Saccharomyces cerevisiae and other yeasts which are naturally introduced as a by-product of the tapping procedure. Kanji is an Indian drink prepared from carrots and beetroots fermented by a mix of yeasts, said to include Candida species and Hansenula anomala. Pulque is a Mexican drink made from agave juice fermented with lactobacilli and Saccharomyces species. Closer to home, ginger beer is a mildly alcoholic beverage made from ginger, sugar, and water also fermented with lactobacilli and Saccharomyces species.
Yeasts and bread-baking
Different strains of brewer’s yeast, the ubiquitous Saccharomyces cerevisiae, are also used in both traditional and industrial bread-baking. The leavening of bread with yeast is believed to have arisen anciently in Egypt, probably involving spontaneous yeast contamination during the mixing and baking process. Yeast fermentation in the dough releases carbon dioxide, causing loaves to rise and become porous. The yeast also produces complex by-products, including organic esters, alcohols, and carbonyls, which are responsible for much of the flavour of leavened bread. In India, papadams are traditionally made from gram flour fermented for a few hours before cooking. The fermentation medium usually comes from a previous batch and typically contains Saccharomyces cerevisiae and Candida species. In southern India, pancake-like idli are made from gram and rice flours. Principal fermenting agents for idli appear to be the yeasts Torulopsis candida and Trichosporon pullulans.
Fermented cheese and dairy products
If the idea of mouldy food seems unappetising, think for a moment of Penicillium roquefortii and P. camembertii. The first is the mould used not only in Roquefort cheese, but all blue cheeses including Stilton and Gorgonzola. It not only produces a distinctive taste in the veins of blue mould, but is responsible for ripening the cheeses, releasing enzymes which soften the curd and helping produce ketones and acids which substantially contribute to flavour and texture. Penicillium camembertii is the white mould which covers the surface of Camembert and Brie cheeses. Like P. roquefortii, it releases enzymes into the cheese which are responsible for creating the distinctive creamy texture and taste. In addition to these moulds, various ascomycetous yeasts such as Debaryomyces hansenii and Yarrowia lipolytica may also be important in cheese starter cultures.
Saint Paulin, Bel Paese, and the pungent Limburger are examples of cheeses which are ripened using a combination of surface yeasts and bacteria. Similar combinations are found in fermented milk products, notably kefir which originated in the Caucasus and results from the dual action of various yeasts (Candida kefyr and Saccharomyces unisporus form part of a typical commercial recipe) and bacteria such as Lactococcus lactis and Lactobacillus kefyr. Koumiss, the fermented mare’s milk popular in Russia, is a similar product using lactobacteria and the yeast Kluyveromyces marxianus. Both are considered to have tonic properties. Other more familiar milk products, like yoghurt, are fermented entirely by bacteria. Villi, a Finnish ‘ropy milk’ product, is ripened by the mould Geotrichum candidum.
Fermented meat and fish
A number of meat products, particularly sausages and hams, are ripened by moulds. These meats include some forms of salami, such as pepperoni, and Swiss hams such as Bauernspeck. Most of the moulds used with sausages are Penicillium species, particularly P. nalgiovense. Not surprisingly, these moulds are said to have a distinct effect on the taste.
Equally distinctive are the fermented fish products of Indo-China, Japan, and the East Indies. One example is bagoong, a salted fish paste from the Philippines which is fermented for up to a year using a mix of bacteria and yeasts, and is part of the staple diet in some areas. Slightly better known is katsuobushi, a hard, dry, fermented bonito tuna from Japan, mould-ripened with Aspergillus glaucus. Katsuobushi is a standard component of many standard soup stocks (‘dashi’) in Japanese cooking.
Soy sauce, tempeh, and other Far Eastern foods
In the Far East an extraordinarily wide range of fermented foods is produced, often on a large commercial scale. Amongst the best known in the West are soy sauce, miso, sufu, and tempeh, but Wang & Hesseltine (1986) provided notes on well over 100 different fermented products from China, IndoChina, Korea, Japan, and the East Indies. Nout & Aidoo (2002) have provided an update on Asian fungally fermented foods.
Soy sauce is traditionally made from soya beans cooked and mixed with variable proportions of wheat. The mix is fermented with a ‘koji’ starter consisting of the green moulds Aspergillus oryzae and A. sojae and is then further fermented in a brine solution (the ‘moromi’ mash) using a mix of lactobacteria and yeasts, including Zygosaccharomyces rouxii, Candida versatilis, and C. etchellsii. The pressed liquid from the moromi mash is the soy sauce itself, the whole process having taken some six months to complete. Modern industrial processes follow a similar path, but use selected, fast-acting fungus strains and production techniques which deliver a uniform product within a fortnight or so. Estimated annual production of soy sauce in China is around 1,700,000 tons with a further 1,200,000 tons produced in Japan. Soy sauce is also made in several other countries, including Malaysia and Indonesia where it is known as ‘kecap’, the origin of the English word for a spicy, savoury sauce.
Miso is a Japanese fermented paste, not too dissimilar from a thick soy sauce, but typically made with soya beans and rice, rather than wheat. The fermentation process involves the same fungal species. Several distinct varieties are made, varying in colour, saltiness, and sweetness, and the paste is mainly used as a basis for miso soups. Estimated annual production of miso is around 600,000 tons.
Sufu is a Chinese fermented bean curd sometimes called soya bean cheese. The basis is tofu, the rather bland, coagulated cubes of soya bean milk, which are treated with Actinomucor elegans or other zygomycetous moulds and then fermented in a mix of brine and alcohol. The popular hon-fang or red sufu is made with the addition of ang-kak (rice fermented with the yeast Monascus purpureus, used mainly for food colouring). Also popular is tsui-fang or ‘drunken cheese’, made with more than the usual amount of alcohol. The preparation of sufu combining bacterial as well as fungal fermentation resulting in ‘a strong, offensive odour’ is said to be ‘a top secret in the industry’ and is now becoming ‘a lost art’ (Wang & Fang, 1986). Estimated annual production of less offensive sufu is around 300,000 tons.
Tempeh is an Indonesian staple made from parboiled, pressed soya beans inoculated with Rhizopus moulds, particularly R. oligosporus. Mycelium of the mould grows rapidly through and over the soya beans, binding them together to form a tempeh cake which is sliced and fried, roasted, or added to soups. It is a major source of protein in the Indonesian diet. Oncom is a similar fermented cake made from peanuts and is a staple dish in western Java. Peanuts are first pressed for oil extraction, steamed, and then inoculated with the ascomycetous mould Neurospora intermedia. This grows over the peanut cake, producing a foodstuff similar to tempeh but coloured orange from the mould. Neither tempeh nor oncom have any keeping properties and must be eaten the same day they are prepared.
Gari, foo-foo, and other traditional foods
In the rain forests of equatorial West Africa, roots of cassava are pulped and fermented with bacteria and the ascomycetous yeast Geotrichum candidum to form a local staple known as gari. From experience in Cameroon, this closely resembles vinegar-flavoured tapioca, which indeed is more or less what it is. Foo-foo is a similar product from Nigeria and the Congo, probably involving lactobacteria and yeasts (Candida species).
Other local, fermented foods include the Hawaiian poi, a porridge-like preparation of taro prepared with lactobacteria and yeasts (including Candida vini and Geotrichum candidum); pozol, a simple dough of fermented maize eaten in southern Mexico, prepared with a wide and spontaneous mix of bacteria, yeasts, and moulds; kaanga-kopuwai, a Maori preparation of maize which turns the kernels ‘slimy and distinctly aromatic’; and kanjika, a soured rice gruel eaten by the Dravidians of India.
In Mexico and elsewhere, beans from the tree Theobroma cacao are placed in pits or sweat boxes and naturally fermented for up to 12 days by a complex succession of yeasts including Candida, Kluyveromyces, Saccharomyces, and Trichosporon species which macerate the pulp and drain off the liquor. The fermented beans are the basis for xocalatl, a local speciality which, sweetened and marketed under the name ‘chocolate’, has become one of the world’s most widely known and distinctive food products.
Hundreds more foods are fermented worldwide. Details of many of them can be found in an A-Z guide by Campbell-Platt (1987), with further substantial compilations by Steinkraus (1983) and Hesseltine & Wang (1986).
Kombucha, the Tibetan, Manchurian, or tea ‘mushroom’
A peculiar Asian concoction which has long been made from cultures of sweetened tea has in recent years been touted as a universal New Age panacea, capable of curing cancer, AIDS, rheumatism and hair loss, whilst also prolonging life. Called kombucha (or kambucha), hongo, the Tibetan, Manchurian, or Japanese tea ‘mushroom’, it is not an individual organism, but a highly variable consortium of yeasts and bacteria which forms large, gelatinous, lobate growths in tea-based media. The constituents change from culture to culture, so it is unlikely that any two kombuchas are the same; but the consortia frequently include acetobacteria and yeasts like Saccharomyces ludwigii, Schizosaccharomyces pombe, and Pichia fermentans. The bacterial-fungal consortium is kept alive by continually subculturing in a mix of sugar, tea, and water, the excess fluid from which is drunk by the brave or demented. Ramsbottom (1936) mentioned it as ‘tea cider’, noted the presence of a bacterium and yeast (S. ludwigii), and commented that there had been a ‘good deal of propaganda’ regarding its ‘reputed medicinal qualities.’ More on kombucha, including a bibliography, can be found in Roussin (1996).
Marmite™ yeast extract
In the nineteenth century, a German chemist, Baron von Liebig, found that spent brewer’s yeast could be made into an edible paste and in 1902 the Marmite Food Company was established at Burton-on-Trent, the heart of the British brewing industry, to develop yeast extract into a commercial product. Raw spent yeast from breweries, mixed with hop residues, is bitter and unpalatable, though sometimes used as an animal feed supplement. But after some refinements, the edible yeast extract Marmite™, with its distinctive savoury-salty taste, became popular as a vitamin source and dietary supplement in the 1920s and achieved more universal popularity in Britain during the Second World War. It is seldom eaten elsewhere but Vegemite™, an Australian yeast extract first produced in 1922 by Fred Walker & Co., is a similar product with an equally loyal following in its country of origin.
Quorn™ mycoprotein
Non-fermented food products from microfungi are rare. But since the 1980s, fungal protein has been commercially produced for human consumption from the mycelium of a non-pathogenic strain of the ascomycete Fusarium venenatum (originally misdetermined as F. graminearum).
Development of the process was initiated in Britain during the early 1960s, but it took twenty years before mycoprotein reached the supermarket shelves. Textured and flavoured, it is marketed as a meat-free health food, and as such provides an alternative to similar soya-based products (Trinci, 1992). Mycoprotein was launched in 1985 under the trade name Quorn™ and is now readily available as a range of fifty or more products, including meat-free burgers, sausages, and ready meals. By 1992, its UK retail value was £12,000,000 p.a., rising to over £100,000,000 p.a. by 2001.
Fungi as food additives: acids, vitamins and enzymes
Fungal fermentation processes are employed on a commercial scale to produce an extensive range of substances such as preservatives, vitamins, enzymes and other metabolites for the food industry. An example is citric acid, which is extensively used as an antioxidant, preservative, and flavour enhancer in a wide range of food products. It was once extracted from citrus fruits, but since 1923 has been commercially produced by fermentation of the mould Aspergillus niger, mainly using molasses as a substrate. Around 300,000 tons are produced each year. The production of vitamins, mainly as supplements for animal foodstuffs, is largely undertaken by chemical synthesis. However, since the 1970s riboflavin (vitamin B2) has increasingly been manufactured from soybeans using a fermentation process involving the ascomycete Ashbya gossypii. Some commercial production of β-carotene (provitamin A), used as an anti-oxidant and orange food colouring, is also undertaken using the zygomycete Blakeslea trispora. A few polyunsaturated fatty acids (vitamin F group) are commercially produced using the zygomycete Mortierella isabellina, whilst other biosynthetic processes use a species of the marine Thraustochytriales.
Rennin, the milk-clotting enzyme used in cheesemaking, is now largely derived from zygomycetous Mucor species. Pectic enzymes from Aspergillus niger and other moulds are extensively used for clarifying fruit juices, whilst fungal amylases, typically derived from Aspergillus oryzae, are used in commercial baking. Bigelis & Lasure (1987) provided details of many other fungus-derived enzymes used in a variety of processes, from the manufacture of non-sugar sweeteners to the removal of ‘flatulence factors’ from soya bean products.
FUNGI AS BIOCONTROL AGENTS
Fungi are natural control agents for many pests and diseases, so the possibilities of exploiting them commercially have long been researched, to the point where a number of products are now on sale. In recent years, this research and development (though still minimal compared to R&D in the chemical industry) has increased as a result of the banning of dangerous chemicals (e.g. the pesticide, methyl bromide) and the growth of the ‘organic food’ sector. Fungal products may well provide replacement treatments.
Fungi to control weeds
Though plant pathogenic fungi can be economically devastating when they attack our crops, a few redeem themselves by attacking our weeds instead. These beneficial plant pathogens have been extensively researched and occasionally put into use as fungal biocontrol agents.
In many countries, the unintentional introduction of alien weeds has caused huge problems not only on arable farms, but also in pastures and grasslands. Freed from their natural checks and restraints, some of these invasive weeds have totally overgrown crops and native vegetation. In such cases, the careful introduction of the weeds’ own host-specific pathogens, including fungi, can help bring them under control. This technique is generally known as the inoculative or ‘classical’ approach, the idea being that a single release of a tested pathogen will spread naturally and effectively through the weed population without further human interference. Host-specific rusts have been the main source of such inocula and have scored some success. The first to be tested was the rust Puccinia chondrillina which was introduced into Australia in 1971 to combat rush skeltonweed (Chondrilla juncea), a serious weed of cultivation introduced from Europe. The same fungus was introduced into the United States in 1975 for the same purpose. In Australia, the rust spread an encouraging 320 km in the first year, but proved an ineffective control which had little impact on the host population, mainly because several strains of the weed turned out to be rust-resistant. In America, however, infestation reductions of up to 87% were achieved in some areas. A further example was the 1973 release of blackberry rust, Phragmidium violaceum, in Chile to combat the spread of European brambles (Rubus fruticosus agg.), an objective which was achieved with some considerable success.
A different approach is the ‘inundative’ strategy, where pathogenic fungi are applied to weeds in much the same way as a conventional chemical herbicide. Several such ‘mycoherbicides’ have been tested and a very few have even been marketed commercially. DeVine®, for example, is a preparation containing the fungus-like blight Phytophthora palmivora marketed to Florida citrus growers to combat strangler vine (Morrenia odorata). The product was so successful, proving to be around 90% efficacious over a two to ten year period, that it was initially withdrawn for lack of repeat sales, though is currently available once more (Kilian et al., 1997).
In Britain, concern about bracken (Pteridium aquilinum) as an invasive weed species, as well as its apparent status as a potential carcinogen, has led to research into bracken parasites as potential mycoherbicides. Among the most important of these are the ascomycetes Ascochyta pteridis and Phoma aquilina, two of the causal agents of a disease known as ‘curl-tip’. Both have been investigated in Britain for bracken control, and A. pteridis has been assessed for its potential as a specific mycoherbicide. A wide range of further possibilities for weed control are being investigated worldwide (TeBeest, 1993; Evans et al., 2001).
The whole subject of mycoherbicides achieved some notoriety in 2000 with the revelation that the British and American governments were quietly financing research into a fungus for use against opium poppies in Afghanistan. The species concerned, an ascomycete called Pleospora papaveracea, was being developed in a former soviet biological warfare plant in Uzbekistan (BBC, 1998). At the same time a form of the ascomycetous plant pathogen, Fusarium oxysporum, was being developed with UN funding for use against coca plants in Colombia (Kleiner, 2000). These revelations were generally presented in terms of a major scare story, with visions of lethally toxic fungi running out of control. One South American newspaper even dubbed F. oxysporum ‘el hongo Frankenstein’. At present, however, it seems unlikely that many mycoherbicides – for weeds or for drugs – will go into full-scale production in the near future. Problems in bulk-growing plant pathogens, in storing them in viable condition, and in applying them at the right place and time are just the beginning. Successful mycoherbicides also have to compete with conventional chemical treatments in terms of cost, ease of use, and effectiveness, and all that adds up to a very tall order indeed.
Fungi to control fungi
There are basically two ways to utilise fungi themselves as a control for fungal diseases of crops. The first and more obvious method is to develop and deploy parasitic fungi to attack the plant pathogens. A commercial example of such a biofungicide is AQ10®, a preparation of the ascomycete Ampelomyces quisqualis a common parasite of powdery mildews. Tests on courgettes and cucumbers have shown substantial yield increases, with the added benefit of non-toxicity (as opposed to the traditional use of chemicals such as sulphur). The biofungicide Trichodex®, containing Trichoderma harzianum, is another commercial product said to be effective against the ubiquitous grey mould, Botrytis cinerea.
As well as these leaf sprays, soil-borne biofungicides have been developed to combat pathogens which attack plants through their root systems. Introducing the mycoparasitic ascomycete Gliocladium virens into soils has, for example, been shown significantly to reduce the incidence of damping-off by Rhizoctonia solani and Pythium species and a commercial product based on the fungus, Soilgard 12G®, is currently marketed in the United States.
A second and less obvious method of biocontrol is to use the natural antagonism of harmless fungal species to keep pathogenic species at bay. Many saprotrophic fungi growing on living leaf surfaces, for example, are antagonistic to other potential leaf colonisers, including some plant pathogens. As a result, these phylloplane fungi have potential use as biocontrols. A common phylloplane fungus, Cladosporium herbarum, has been shown to reduce Botrytis rots when sprayed onto soft fruits whilst spraying wheat with suspensions of phylloplane yeasts reduces leaf diseases. Aspire®, a commercial product based on the yeast Candida oleophila, is available in the United States as a treatment against post-harvest decay of pome and citrus fruits. Even without spraying, these phylloplane fungi may be providing some natural protection to plants. As a result, killing off the natural mycota by applying non-selective fungicides to crops may perversely increase rather than reduce the incidence of fungal disease.
In forestry, the harmless basidiomycete Phlebiopsis gigantea has been used on a commercial scale against the parasitic, wood-rotting polypore Heterobasidion annosum. Heterobasidion can quickly colonise the stumps of felled conifers, using them as a resource from which to attack living trees. But when fresh stumps are inoculated with Phlebiopsis (an aggressively territorial fungus), the Heterobasidion can gain no foothold. This form of biocontrol, pioneered in Thetford Forest, Norfolk, by Rishbeth (1961), was once widely used by the Forestry Commission, but has now fallen out of favour. It has, however, been adopted on a large scale in Finland and other Scandinavian countries where a spray-on suspension of propagules is marketed under the name Rotstop®.
Considerable research has been undertaken on the possibility of using other antagonistic species to keep parasitic, wood-rotting fungi in check. Hypholoma fasciculare (sulphur tuft), for example, may provide a possible biocontrol for use against Armillaria species (honey fungus).
The commercial use of fungi to control plant pathogens was reviewed by Whipps & Lumsden (2001) and a list of available products published by Butt et al. (2001).
Fungi to control insects and mites
Not surprisingly, entomopathogenic fungi (parasites of insects, mites, and other invertebrates) have been the subject of extensive research into their potential use as biocontrol agents for invertebrate pests.
Metarhizium anisopliae, an ascomycete anamorph (Nectriaceae), is one of the more successful control agents, with different strains attacking a range of pests including cockroaches, weevils, termites, whiteflies, and thrips. In the USA, a cockroach trap containing M. anisopliae spores is currently marketed under the trade-name Bio-Path® and a termiticide under the name Bio-Blast®, whilst in Germany a granular soil treatment called Biologic® containing M. anisopliae mycelium has been developed for use against the larvae of black vine weevils. Another anamorphic ascomycete, Beauveria bassiana (Clavicipitaceae), has an equally wide host range. Since the 1970s it has been mass-produced in Russia under the name Boverin® to control Colorado beetles and codling moths and it is extensively used in China where up to one million hectares of farmland and forest are treated each year against a variety of pests. In Britain, strains of the ascomycetous mould Verticillium lecanii are commercially available under the names Mycotal® (introduced in 1982) and Vertalec® (introduced in 1981) for greenhouse control of aphids and whiteflies respectively.
To date, however, only a few fungal pesticides have been marketed commercially compared to the vast range of chemical pesticides. In 1996, the cost of registering a pest control agent was around £250,000 in the USA alone, and fungal biocontrol agents have to compete with established chemical agents not only in performance, but in production costs, long-term storage, ease of use, and safety features. At present, it seems, many fungi have the potential to control pests, but only a few meet the criteria for commercial success (Butt et al., 2001, provided a list of available products).
Fungi to control nematodes
Nematodes (eel-worms) cause considerable economic damage, either by attacking the roots of commercial crops, or by infesting cattle and other livestock. Worldwide crop losses due to nematodes are immense, estimated at around £50,000,000,000 per year. However, the nematodes have their own parasites and predators in the form of specialist fungi (Chapter Five). As with insect pathogens, these nematophagous fungi have been extensively researched as potential biocontrol agents, though with rather less success. Part of the problem is the difficulty of growing many of the fungal species, particularly the endoparasites, in vitro. Another difficulty is understanding the ecology of nematophagous fungi in soil and pasture and, as a consequence, tracking the precise effects of experimental applications. It may be that toxins extracted from nematophagous fungi will prove more successful than the fungi themselves, and a commercial product DiTera®, based on the anamorphic ascomycete Myrothecium verrucaria, is now available for nematode control.
FUNGI FOR BIOREMEDIATION
Rotting down poisonous wastes
As part of the natural process of decomposition, many fungi and bacteria break down complex chemicals into simpler compounds. When the initial chemicals are toxic, this breakdown can have a beneficial ‘clean-up’ effect and can be artificially enhanced by encouraging existing fungi to work harder or by introducing novel fungi to the chemical mix.
Crude oil spillages are obvious candidates for this bioremediation treatment. Some fungal species thrive on the hydrocarbons found in oils – including the kerosene used in aviation fuel (Chapter 14) – and under the right conditions are capable of degrading them into simpler and less polluting substances. The ascomycetous mould Aspergillus terreus, for example, has been found as a natural degrader of oil spills, occurring (together with Fusarium solani) in North American oil damaged sites and in the devastated oil fields of Kuwait following the Gulf War. On-site treatments such as tilling, fertilisation, and irrigation can help these natural degraders – bacteria as well as fungi – break down some or all of the pollutants (Morgan & Watkinson, 1993, provided a brief review of methods).
As well as helping the soil’s natural mycota do its remedial work, researchers have also experimented with introducing novel fungal degraders to pollutants. Perhaps surprisingly, these fungal degraders include polypores and other wood-rotting basidiomycetes. But wood contains a wide range of oils, resins, gums, tannins, and other ‘extractives’ some of which are widely toxic, yet tolerated and even utilised by the wood-rotting fungi (Chapter Three). Lignin-degrading, white-rot basidiomycetes are amongst those which have been widely researched as potential biodegrading agents. The oyster fungus Pleurotus ostreatus has, for example, been shown to break down the aliphatic and aromatic hydrocarbons in crude oil and also the polychlorinated biphenyls (PCBs) in pesticides and other agents. The corticioid fungus Phanerochaete chrysosporium has been shown to break down PCBs, polycyclic aromatic hydrocarbons (PAHs) in creosote and other oils, some of the phenolic dyes in pulp-mill and textile effluents, and DDT pesticide residues. Some research has also been undertaken on biodegradation by brown-rot basidiomycetes.
Moulds (Aspergillus species) have been reported growing on gunpowder, but more remarkably some fungi can even degrade TNT. Phanerochaete chrysosporium is one of the species successfully tested, and trials have been made with fungi to clean naval dockyards of waste explosives on the ground.
Taking out toxic metals
As well as breaking down complex chemicals, many fungi are able to absorb and accumulate metals from the environment, and hence have a potential role in the bioremediation of toxic metal-rich effluents and contaminated sites. The mechanism is termed ‘biosorption’ and the metals involved include arsenic, cadmium, cobalt, copper, mercury, selenium, uranium, and zinc. Once taken up from soil or effluent, the metals can be recovered from the fungi and disposed of or recycled. Potentially useful species which have been studied include brewer’s yeast, Saccharomyces cerevisiae, and the zygomycete Rhizopus arrhizus, both of which are capable of being cultured in bulk, an essential attribute for practical use. A list of these and other potential bioremediation fungi, mostly ascomycetes, was published by Singleton & Tobin (1996).
‘Heterotrophic leaching’ is another mechanism whereby fungi can remove metals from the environment. This can involve several different processes, the commonest of which utilises fungally produced organic acids (such as citric and gluconic acid from Aspergillus niger) to solubilise and leach out metals, which can then be recovered. The techniques could be used to recover metals from the ash left over from municipal incinerators or from various kinds of manufacturing and recycling scrap, such as old electronics and circuit boards. Fungi could also be used to leach out unwanted metals in contaminated sites and to recover valuable trace metals from waste or low-grade ores in the mining industry. Fungal bioconversion of low-grade coal could produce more versatile and valuable hydrocarbon fuels.
Reclaiming wasteland with mycorrhizas
Slag heaps, coal tips, and landfills were once left to their own devices, but are now routinely planted with birch, conifers, and other rapidly growing trees. Most of these trees are ectomycorrhizal, but their fungal associates are absent from reclaimed sites. To enable the trees to grow, seedlings are therefore deliberately inoculated with appropriate fungi before planting out. In Britain, favoured species are the earthball Scleroderma citrinum and the agaric Paxillus involutus, both common fungi capable of forming mycorrhizas with a wide range of hosts. Inoculation of tree seedlings can be achieved by the transfer of soil or roots from existing mycorrhizas, by sowing with spore-encapsulated seed, or by mixing soil with cultured mycelium. In America, the puffball-like Pisolithus arhizus has been widely used to form mycorrhizas with pines and other trees planted out in industrial waste sites and a commercial formulation called MycoRhiz® has been marketed for this purpose.
Radioactive fungi
Rather alarmingly, agaric fruitbodies are good bioindicators of radioactive contamination through deposition, including fallout from the atmospheric testing of nuclear bombs and plume deposits from the Chernobyl reactor disaster. Fungi are particularly receptive to the radioactive isotope caesium137 (radiocaesium: 137Cs) which is taken up by growing mycelium as a surrogate for potassium, which has similar physicochemical properties. Measuring radionuclides in agarics therefore provides an estimate of the contamination of the substrata (leaf litter, soil, wood, etc.) in which they grow, though take-up of 137Cs varies substantially according to species, soil pH, and other factors. The subject was succinctly reviewed by Oolbekkink & Kuyper (1989) and in more detail by Reisinger (1994).
Investigation of a range of British agarics and other macrofungi following the Chernobyl accident, fortunately showed only modest levels of 137Cs accumulation in fruitbodies (well below EU limits for food products). Even for people who habitually eat wild fungi in Britain, the extra intake of radioactivity resulting from Chernobyl was and is minimal (Barnett et al., 2001). Much higher figures were obtained in central Europe and, of course, in Ukraine itself where contamination of edible fruitbodies exceeded safety limits.