Chapter 1: Matsutake: An Ancient Tradition
History of Matsutake
|Matsutake have been used and revered by the Japanese people for more than
a millennium and have become more
than just a seasonal delicacy. They also symbolize fertility, and by extension, good fortune and happiness. A gift of
matsutake is considered special and is cherished by those who receive it. According to Ohara
(1994), one of the earliest records extolling its virtues is found in a 759 A.D. poem.
Later references to matsutake often were related to activities of nobles and priests.
Records from the 13th to 17th centuries indicate that nobility enjoyed mushrooming
events and often sent matsutake as gifts, a tradition that persists today, especially in
the corporate world. During the 11th century in the Imperial Court of Kyoto, women
were prohibited from saying "matsutake" openly but instead were required to speak
of it with the honorific marker "0," as O-Matsu. Until the 17th and 18th centuries,
matsutake consumption was strictly limited to the imperial court. As matsutake
consumption became more common among the public during these centuries, vulgar
(phallic symbolism) and graphic short stories came into vogue, portraying comical
characters attempting to conceal their matsutake picking areas and indulging in
risque talk about the mushroom. It was in this same period that the first stirrings
of scientific interest were recorded: A Buddhist priest in Kyoto recorded the annual
productivity of matsutake (that is, mushroom numbers) in a mountain forest
(Kinkakujiyama). Later, based on the priest's diary, Professor M. Hamada of Kyoto University
was able to approximate the seasonal precipitation, temperature conditions, age and
ecological status of the mountain forest from 1636 to 1667 (Ohara 1994).
The Decline of Japanese Matsutake
|Matsutake shiros were once widespread and common in mixed pine forests
of Japan from Hokkaido in the north to Kyushu in the south. After World War II, they
became increasingly scarce, in spite of efforts to enhance productivity in local
forests. By 1981, productivity had declined to one-tenth of the pre-War levels, and
imports of Japanese matsutake, especially from South Korea, increased greatly to
meet demand (Kawai and Ogawa 1981). The quantity imported today differs from
season to season but can exceed 60 percent of the total retail market (EAITC
1990). Imported matsutake, especially species other than T. matsutake, are
generally perceived as lacking freshness, proper color, taste, and fragrance
and therefore are considered lower in quality and value. Whether or not this
perception is true, improved grading, handling, and marketing strategies, coupled
with a continuing decline of Japan's matsutake production, will certainly improve
the image and market value of imported mushrooms.
Since 1905, the matsutake forests of Japan have been plagued by the pine
nematode or pine weevil.' The nematode is transmitted to living pines by the
Japanese pine sawyer, a longhorn beetle. Invasion of vascular tissue by the
nematode results in wilt and rapid death (Futai 1979, 1980a, 1980b, 1980c;
Futai and Furuno 1979). Most host pines of matsutake, including the Japanese
black and red pines, are very susceptible to this devastating pathogen. Since the
introduction of the nematode at the start of the 20th century on the southern island
of Kyushu, it has steadily spread north-eastward. The current blight is the fourth in a
series of epidemics since 1905. The third epidemic lasted a decade, peaked in 1979,
and caused an estimated loss of 2.4 million cubic meters of pine wood. The current
epidemic began in 1990, and killed enough trees in one year to build 50,000 houses.
Recent reports indicate that the disease has also spread to forests of Okinawa,
Taiwan, South Korea, North Korea, and China. A combination of climatic,
socio-economic, and biological factors in Japan tends to increase the magnitude of the
blight. Pine mortality from the nematode often increases after prolonged drought
and high temperatures, which weaken the resistance of the pines to the parasite.
A change in the way communities use local forests also has adversely affected the
health of pine forests and, indirectly, matsutake productivity. For at least a millennium,
routine harvesting of understory shrubs and oak trees for charcoal favored growth of
shade-intolerant pines and the matsutake associated with them. In post-World War II
years, traditional charcoal- and wood-burning stoves were replaced by natural gas
burners, and the removal of woody shrubs for charcoal diminished. Trees and shrubs
that do not form matsutake mycorrhizae have consequently formed dense, brushy
understories that block sunlight needed by pine seedlings. While mature pines die
from nematode attacks, new pine seedlings find themselves at a competitive
disadvantage and have difficulty becoming established; hence, matsutake shiros
disappear along with their pine hosts as other tree species become dominant.
Essentially, the red and black pines introduced from the Korean Peninsula
flourished in the past under conditions no
longer existing in Japan. Although the Japanese have developed many silvicultural strategies to manage matsutake forests
(discussed below), matsutake production has disappeared from the vast stretches of
mountain pine forests that die each year. Indeed, Japan's temples and public parks
may eventually become the last refuge for matsutake pine forests, as suggested by
a respected Kyoto gardener, Mr. Shiro Nakane (c. 1992):
To me, this already seems to be the case. When I was a kid, I'd walk on
the paths right up there and gather matsutake from the many, many red
pine trees. Now I sometimes go up to the mountain with my two boys and
my dog, but the forest there has changed. The trees I remember are gone.
Still, different trees are appearing, and maybe this is nature's way.
|Other Species of Matsutake
|Two species of matsutake are recognized in Japan: Tricholoma matsutake and
T. bakamatsutake. The first is the principle Asian species and grows widely in
Japanese red pine (known as "aka-matsu") forests throughout Japan, South Korea,
North Korea, northeastern China, and Primorsk Kray, Russia. In Japan, T. matsutake
also associates with Japanese black pine, Japanese stone pine, Japanese white
pine, southern Japanese hemlock, northern Japanese hemlock, and Sakhalin spruce.
On the Korean Peninsula and in Manchuria, it associates with Korean pine; in
Sakhalin with Maries fir; and in Taiwan and along the east coast of China, with
Taiwan red pine (Hamada 1966, Ogawa 1982, Ohara 1981). It occurs in at least
eight provinces of China under various pines (often mixed with oaks), but most
often under Japanese red pine in the northeastern province of Jilin (Wang c. 1982).
Tricholoma bakamatsutake or "foolish pine mushroom," is less common and differs
from T. matsutake by its association with broadleaf trees, particularly Mongolian oak,
serrated-leafed oak, edible Asian tanoak, and chinkapin species (Ogawa and Ohara
1978). It, too, ranges from Hokkaido to Kyushu in Japan, and is found in Taiwan,
South Korea, North Korea and China. It has the same general morphology and
strong matsutake odor and taste of T. matsutake, but it differs from the latter in
being slightly smaller and more fragile, and in having cheilocystidia on the gills
(Hongo 1974). Thus, the two can be easily confused morphologically and indeed
may represent only ecotypes or variants of one "plastic" species.
The principal North American counterpart of the Asian matsutake species is
Tricholoma magnivelare. It is similar in texture, taste, and odor to Asian species
and has long been a favorite of Japanese-Americans and certain tribes of Native
Americans. Mushroom guides often refer to the American matsutake as either
T. ponderosum (Peck) Singer or Armillaria ponderosa (Peck)
Sacc. The epithet
"ponderosa," meaning large and heavy, is descriptive of the species. The earliest
name applied to the American matsutake was Agaricus magnivelare. "Magnivelare"
also describes the species well; it refers to the large well-developed veil, which
breaks or tears, leaving a membranous ring on the stalk. In his 1984 review of the
literature, Redhead determined that the nomenclaturally correct name is T.
magnivelare (Peck) Redhead. The species is morphologically distinct from the Japanese
species and is described by Smith and Weber (1980:127) as follows: "This large
white mushroom gradually develops cinnamon stains as it ages, and in age is quite
discolored. The cap may be up to 35 centimeters broad and covered with cinnamon
colored patches of tissue. The gills are white and slowly stain vinaceous cinnamon."
Arora (1986:191) ventures the most intriguing description of its unique spicy odor
as a "cross between red-hot [spicy cinnamon candy] and dirty socks.
A rarer and consequently less well-known species of North American matsutake is
T.caligatum, or "booted"
matsutake. It occurs in North America, Europe, and northern Africa. The species is generally smaller and more slender than
T. magnivefare, has a broad cap with dark vinaceous to cinnamon-brown scales or fibrillose
(hair like) patches, and has the same colors on the underside of the ring and the stalk below
the ring or "boot." The stalk above the ring is white and the odor of the mushroom is
quite variable. As Smith and Weber (1980:127) write: "One variety has an odor like
that of A. ponderosa, another has an odor somewhat like that of bitter almonds,
and a third no odor at all. The Japanese matsutake is one of the varieties of this
collective species." Likely the variability in odor is geographic; specimens found in
western North American smell more like the Japanese matsutake than those from
eastern North American (Arora 1986, Smith 1979). Tricholoma caligatum may be
found in pure coniferous stands, mixed coniferous and hardwood stands, and pure
hardwood stands. In general, T. caligatum seems to be closely related in size, odor,
and habitat to T. matsutake, T. bakamatsutake, and T. fulvocastaneum of Japan.
Kytovuori (1989) discusses the T. caligatum group in Europe: T. caligatum and
T. nauseosum are species with overlapping ranges in Europe and northern Africa.
After examining many specimens, he asserts that T. nauseosum of Europe is
synonymous with T. matsutake of Asia, and because T. nauseosum was named first,
it is therefore the valid name. Specimens originally described as T. nauseosum and
T. matsutake came from opposite sides of the Eurasian continent; hence, this claim
likely will require further verification (perhaps genetic comparisons) before it is widely
accepted. It would, however, be ironic if one of the most highly prized mushrooms in
the world ends up with the specific epithet "nauseosum" due to the priority rule of the
International Code of Botanical Nomenclature (Greuter 1994), which states that the
first name validly published for a species is the correct name. Kytovuori (1989) also
discusses the affinities between T. nauseosum and T.
magnivelare. He further
asserts that the T. caligatum of Europe is distinct from both T. nauseosum and the
T. caligatum of North America.
The global taxonomy of wide-ranging species like matsutake can be confusing even
for experts. To further complicate matters, commercial collectors and retailers often
make odor, taste, and value distinctions among specimens of the same matsutake
species collected from different areas. Species distinctions often are based on
descriptions of physical characteristics, and many of these have a range of gradations.
With the advent of easy global communication and techniques for genetic analysis,
taxonomists have powerful tools for distinguishing between actual species and local
ecotypic variation within a species. Readers are referred to Wang and others
(in press) for further discussion of the
global distribution of closely related matsutake species.
Look - Alike
|Tricholoma zeileri is another North American species related to
T. magnivelare. It is not considered a matsutake and has no commercial value, but it is often abundant
and is commonly found near shiros of T. magnivelare', hence, it may be considered
an indicator species (Hosford and Ohara 1990). This species resembles T.
magnivelare in shape, texture, and occurrence but usually is smaller and different in color,
odor, and taste. The cap is viscid at first but soon dries and cracks into small scales.
The cap ranges from yellow to orange and often develops distinct olive tones in
spots. The stem below the well-developed ring has colors similar to the cap. The
odor and taste of T. zeileri is similar to freshly ground meal (farinaceous), with an
added pungent metallic taste. Tricholoma zeileri fruits prolifically at about the same
time as other matsutake in the coniferous forests of the Pacific Northwest and
the Great Lakes area. It is closely related or identical to T. focale of Europe and
T. robustum of Japan.
The "imperial mushroom" (Catathelasma imperiale) is a species sometimes
mistaken for the American matsutake by novice collectors. Although typically larger
and lacking the distinctive odor of the American matsutake, the imperial mushroom
otherwise has a similar appearance. It is edible and collected commercially.
Deadly Amanita mushrooms are distinctive from matsutake, but they can fruit within
meters of each other (Pilz, personal observation), and poisonings from mistaking
Amanita smithiana for matsutake have occurred (Benjamin 1995, Leatham and others 1997, Tullos and Lindgren 1992). Amanita mushrooms have a brittle texture,
whereas matsutake have a fibrous texture (they can be peeled like string cheese).
The matsutake odor is also distinctive, when one is familiar with it. The usual
caveats apply: always make sure of your identification before eating any
mushroom, and then start with small quantities.
|Ecology of the Japanese
|The roots of ecological knowledge stem from ancient tradition. During the Edo
Period (1603-1867), a number of books contained descriptions (including habitat)
and illustrations of matsutake (Fig.
1). The book Honcho Shokkan (1697) was the
first to recognize the symbiotic relationship between matsutake and pine and to
promote matsutake cultivation by transplanting soil from matsutake shiros. No data
on either the success or failure of transplanting is mentioned. Early
research by Inoue in 1930, Kaneyuki in Hiroshima in 1955, Senbara in Kyoto in 1937, and
Asada (1937) added greatly to our knowledge of matsutake biology and ecology
and promoted further study. Senbara focused ecological research on the shiro and
its management and developed techniques later refined by Professor M. Hamada at
Kyoto University. His principal graduate students, M. Ogawa, H. Ohara, N.
Sagara, and K. Kinugawa, contributed information on matsutake mycorrhizae, microbial
interactions in the shiro, chemical treatment of the shiro, and effects of temperature on
formation of the mushrooms. The research of Hamada (1950), his students and
others, such as Tominaga (1963, 1973, 1978), is embodied in the following
discussion of matsutake shiros and forest management.
|Ohara (1994:29) defines a matsutake shiro as "...a subterranean biotic
community where mycorrhizal development plays a leading part over the soil constituents,
especially soil microbes." Ohara's definition emphasizes the key importance of the
fungus-root association in a shiro. The annual growth of a matsutake shiro (initially
located by the emergence of mushrooms) is typically followed by inserting bamboo
or flag markers at the exact point of fruiting. A few seasons of such marking provide
an accurate record of mushroom production and a map of the shiro's growth. The
growth of the shiro is directly correlated to mycorrhizal development in the soil
beneath the organic layer. Several zones are recognized in a soil profile of a shiro
(Fig. 2). Zone III, the currently active mycorrhizal zone
(AMZ), contains the
mycorrhizae directly below the mushroom. When fruiting occurs, the soil in this zone
becomes strongly desiccated and the mycorrhizae begin to deteriorate. The AMZ
contains about 10 times the number of fine rootlets (of Japanese red pine in this
case) compared to the zones on either side of it. Zone II contains young,
physiologically active mycorrhizae that will produce mushrooms the following season. The
mycorrhizae of both zones II and III appear as broomlike clusters. Structurally, the
mycorrhizae are classified as ectomycorrhizae but, unlike most
ectomycorrhizae, have loose, soft mantles with poorly developed Hartig nets. Zone I contains mycelium
and structural roots but no mycorrhizae. In zones IV and V (representing the previous
two years of fruiting), the soil is still granular and desiccated and contains decayed
mycorrhizae. Finally, in zone 0, there is no mycelium, and zone VII shows complete
recovery from the earlier effects of active mycorrhizae. All zones (O-VII) can be
recognized in the field by variation in the color of the soil profile, as well as soil
texture, relative moisture, and odor (the unique matsutake aroma). Ogawa and
Hamada (1965), Ohara (1966), and Ohara and Hamada (1967) also report qualitative
and quantitative differences in microbial populations for each zone, especially the
AMZ. Fruiting bodies begin to develop in the AMZ when soil temperature falls below
19 °C. About 20 days after initiation, the cap of the fruiting bodies opens (Kinugawa
1963). Fruiting typically ceases when shiro temperatures fall below 10 °C. The
species of plants and fungi present, their densities, health, age and ecological effects
on shiro productivity have been carefully studied (Ogawa 1982, Ohara 1974). The
results have been applied to forest management techniques intended to enhance
Enhancing Japanese Matsutake
|The following sections summarize management techniques employed to enhance
the production of matsutake (numbers and size of the mushrooms) in Japanese red
pine forests. More complete discussions of the subject can be found in books (in
Japanese) by Ogawa (1982) and Ogawa and lto (1989) and papers by Ohara (1994)
and Sagara and Hamada (1965). Although this discussion pertains to research
with the Japanese matsutake, many of the techniques may prove applicable to
the American matsutake.
Site Selection and Vegetation
|Important criteria for site selection include age of the pine trees; composition, density,
and stratification of tree species; canopy coverage; slope; and soil characteristics,
including moisture and temperature. Pines 40 to 50 years old are best for matsutake
production, but those over 50 exhibit declining production. Forests consisting
predominantly of pines, with few other tree and shrub species, are most favorable for
matsutake production. Ideal conditions also include an open canopy that allows light
to penetrate to a sparsely vegetated forest floor, and warm, well-drained soils with
thin litter and organic layers. Pine forests positioned on southwestern slopes and
ridge tops tend to be most suitable. Unfortunately, few sites are naturally optimal for
Forest management treatments employed for enhancement of matsutake
production differ from those used to maximize timber production. The primary objective is to
alter tree species composition, stand density, and soil conditions to encourage shiro
development. Ogawa (1982) has designed a schedule of silvicultural treatments that
produces ideal conditions for the establishment, growth, and fruiting of matsutake
shiros in a 30-year-old Japanese red pine forest. A similar set of treatments also
may be applied to younger stands over a longer period. This management regime
produces an open canopy and forest floor that is warm, dry, and free of excessive
debris and organic material. Under these conditions, pine roots proliferate near the
soil surface while many non host roots, bacteria, and saprobic and other mycorrhizal
fungi decline. In an experimental forest near Kyoto, these management procedures
increased the number of shiros from 12 to73 over 15 years (Ogawa 1982).
The first year includes thinning of pines and other competing tree species, removal of
shrubs, herbs, dead branches, and damaged or diseased trees. The increased light
penetration and air circulation reduce soil moisture and increase soil temperature.
Vegetation management during the second year includes removal of new sprouts,
weeding, and tree trimming. Soils with excess accumulation of litter and organic
matter are raked to expose the mineral soil. In effect, this eliminates pine roots
and pests, which tend to accumulate in the litter layer, decreases soil moisture,
and increases soil temperature to levels conducive to mushroom production. On
the other hand, if needed, a bare forest soil may be mulched with rice straw, to
increase moisture and lower temperature to levels again more conducive to the
matsutake. The third year of treatment is much the same as the second, but may
include another thinning of pine and pruning of non dominant trees. New sprouts,
weeds, and excess litter are again removed. By autumn of the third year, matsutake
shiros usually appear and marking of mushrooms begins. After the third year, management consists of annual inspection and cleanup of the
forest floor, removal of dead trees, and biannual pruning of understory vegetation.
Vigorous growth and gradual increase in numbers of shiros usually occurs between
the fifth and tenth years of treatment. After the tenth year, production of mushrooms
drops as the growth rate of maturing red pines declines.
|Several techniques, other than those discussed above, have been used to stimulate
the formation of matsutake primordia (small "protomushrooms" with the potential to
develop), increase the number of mushrooms that actually develop from the
primordia, or increase the eventual size and weight of the mushroom. Most of these
techniques operate by controlling humidity and temperature.
The "Hiroshima tunnel" (Plate 8) is one such method, where a
tunnel like construction
is placed over the physiologically active mycorrhizal zone (AMZ 11-111). The tunnel
roof is formed with fine-mesh netting or screening (as used in greenhouses) stretched
over wire wickets arching to a height of 30 centimeters and spanning up to 1 meter
in width. The length of the tunnel differs with the length of the active shiro front.
The tunnel shades and cools the soil to 20 °C or less for 4 to 5 days to initiate the
development of primordia. The tunnel netting also maintains soil moisture levels
and may control some insects.
Tominaga (1975) and other Japanese have reported success with this
method. Tominaga (1975, 1978) compared
two shiros over 3 years by using variable treatments, including artificial sprinkling of water, air-conditioning, and ice, beneath the
tunnel to control moisture and temperature. Some treatment combinations resulted in
two to six times greater mushroom production and 12 to 20 days earlier production
than without a tunnel.
On a smaller scale, the size of individual mushrooms and their rate of maturation
may be increased by covering them with damp soil or a small cup as they begin to
emerge, thus maintaining higher humidity and preventing the stunting of their growth
through desiccation (Lee 1989a). Plastic cups also may reduce insect damage by
acting as a barrier.
In the previous section, we described how foresters open forest stands to allow
sunlight to warm the forest floor, and in this section we describe techniques for
cooling the mycelium and sustaining high humidity. Although these activities may
appear contradictory, the vegetation management is intended to promote the establishment and growth of shiros and the formation of matsutake mycorrhizae with
selected host trees, whereas the cooling and humidity control are more localized
treatments to enhance fruiting.
|In addition to fruiting enhancement, various inoculation or
"seeding" methods have been tried over the years in attempts to
establish and spread matsutake shiros to new areas. Methods include
inoculating seedling roots before transplanting, transferring soil from
the active mycorrhizal zone of established shiros, and spreading spores
into new forest sites.
Seedling roots have been successfully inoculated in both field and
laboratory. Field inoculation involves planting mycorrhiza-free seedlings
in active shiros to form matsutake mycorrhizae, and subsequently (usually
the next year) transplanting them into appropriate habitat lacking
matsutake shiros. Laboratory inoculation involves isolating a sterile
culture of matsutake from the aseptic interior of a mushroom, growing it
on Hamada's medium (Hamada 1964), and placing it in contact with
mycorrhiza-free seedling roots. New matsutake shiros, unfortunately, have
not yet been successfully produced by planting inoculated seedlings. Soil
transfers from active shiros to likely habitats also have been attempted
without success at establishing new shiros. For further information on
these techniques, refer to Ogawa 1982, Ogawa and lto 1989, and Lee 1989b.
The simplest inoculation method is to cut a fully opened mushroom cap from its
stem and bury it near host plant roots or place it on the soil surface within a young
pine stand. Litter and organic layers should be removed from the soil to improve
the chance that spores will come into contact with appropriate host roots. Spore
suspensions also may be created by mixing spore prints or macerated gills in water.
Spore suspensions are then poured into holes in the soil near pine roots or mixed
with soil placed around the roots. Japanese matsutake spores are short-lived and
few apparently germinate. Repeated application as close as possible to young,
non colonized host roots often is necessary. The use of spore dissemination to
establish new matsutake shiros has had a long history. Those who claim success
are those who cleaned the forest floor of excess organic material and sowed spores
frequently over 5 years or more (Ogawa 1982).
Although attempts to establish new matsutake shiros have not yet yielded
much success, plantation establishment and
management for matsutake production holds the greatest promise for artificial cultivation. The high value of matsutake suggests
this approach may be economically feasible. Many of the techniques for truffle
(Tuber species) cultivation in plantations established with inoculated seedlings may
be adapted eventually to create matsutake plantations. Progress with this approach
has been demonstrated recently with chanterelle mushrooms (Danell 1994, Danell
and Camacho 1997). Even if the technology to do this is developed, success will
depend on using appropriate host trees, selecting adaptable matsutake strains, and
establishing the plantations in appropriate habitat (especially proper soils).
Artificially established matsutake plantations are unlikely to be developed on Federal lands in
the United States because other species would be displaced, an effect that would
conflict with management goals for preserving biological diversity and multiple use.
Managing natural stands (through activities such as thinning or controlled burns)
that already have matsutake populations does hold promise, however, for enhancing
fruiting within the context of Federal ecosystem management goals. Plantations for
American matsutake production may eventually become economically attractive for
private land owners.
Pure Culture Production
|Growing matsutake in pure culture and inducing it to fruit (without its mycorrhizal
tree symbionts) has been a goal of researchers and commercial interests for many
years. Unlike saprobic fungi that decompose organic matter, symbiotic mycorrhizal
fungi have complex biochemical interactions with their plant hosts. Although most
mycorrhizal fungi can be grown in pure culture, only a few have been induced to fruit
without colonizing the roots of a host plant (Ohta 1994; Pantidou 1961, 1962, 1964).
Both Japanese and American matsutake grow very slowly on nutrient media alone,
and innovative biotechnology developments will likely be needed to induce matsutake
to fruit in the absence of its tree partners.