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FUNGAL AND BACTERIAL SYMBIOSES AS POTENTIAL BIOLOGICAL MARKERS
OF EFFECTS OF ATMOSPHERIC DEPOSITION ON FOREST HEALTH
Donald H. Marx
USDA Forest Service
Southeastern Forest Experiment Station
Athens, GA 30602
ABSTRACT
Steven R. Shafer
USDA Agricultural Research Service
NC State University
Raleigh, NC 27695-7616
The ecological role and physiological functions of the different
microbial symbiotic associations, specifically ectomycorrhizae,
endomycorrhizae, and actinorhizae, which occur naturally on roots
of forest trees will be discussed.
The effects of man-made and natural stress on tree
physiological and soil processes which may cause change in (i)
microbial symbiont species composition in the root zone; (ii)
microbial symbiont species succession in developing stands of
trees; and (iii) morphological and physiological attributes of the
symbiotic associations will be presented. Essential methodologies
needed to study these interacting chemical and biological factors
on tree seedlings and on more mature trees will be proposed.
Microorganisms are present in great numbers on and near the
feeder roots of trees, and they play vital roles in numerous
physiological processes. These dynamic processes are mediated by
associations of microorganisms participating in saprophytic,
pathogenic and symbiotic root activities. The major symbiotic
associations on tree roots are mycorrhizae and actinorhizae.
MYCORRHIZAE
The term mycorrhiza (fungus-root) is used to described a structure that results from
a mutually beneficial association between the fine feeder roots of plants and species of
highly specialized, root-inhabiting fungi. Mycorrhizae are active, living components of the
soil and have some properties like those of roots and some like those of microorganisms.
The mycorrhizal fungi derive most if not all of their needed organic nutrition
(carbohydrates, vitamins, amino acids) from their symbiotic niche in the primary tissues
of roots. Evidence suggests that the mycorrhizal habit evolved as a survival mechanism
for both partners of the association, allowing each to survive in the existing
environments of low soil fertility, drought, disease, and temperature extremes. Because
of this coevolutionary process, mycorrhizae are as common on the root systems of trees
and other plants as are chloroplasts in their leaves. In examining plants in a natural
environment, the question is not "are the plants mycorrhizal" because they all are, but
rather "what type of mycorrhiza is present and what is the degree of mycorrhizal
development on the roots?" There are over 4000 publications on mycorrhizae in the
plant science literature.
217
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Endomycorrhizee
This type of mycorrhiza is the most widespread and comprises three groups,
Ericaceous mycorrhizae occur on four or five families in the Ericales. Orchidaceous
mycorrhizae are a distinct type that occur only in the plant family Orchidaceae. These
two groups of endomycorrhizae are not widespread and will not be discussed.
Vesicular-arbuscular mycorrhizae (YAM) form the third group of endomycorrhizae.
They occur on more plant species than do all other types of mycorrhizae combined and
have been observed in roots of over 1000 genera of plants representing some 200
families. It has been estimated (Kendrick and Berch 1985) that over 90% of the 300,000
species of vascular plants in the world form VAM. VAM fungi are ubiquitous in all
natural soils throughout the world except where they have been eliminated by man's
activities. Inoculum density and fungal species, however, differ in different soils
supporting different plants.
The fungi forming VAM belong to the class Zygomycetes and the family
Endogonaceae, which includes the genera Glomus, Gigaspora, Acaulospora, Sclerocystis,
Entrophospora, and Endogone. These fungi have very little host specificity. One VAM
fungus may have a plant host range including trees, vines, grasses, legumes, and desert
plants. The main characteristic of VAM is the presence of vesicles and/or arbuscules in
the primary root cortex. The endodermis, stele, and root meristems are not colonized.
Inter- and intracellular hyphae present in the cortex are connected to the external
mycelium that spreads and ramifies in soil. Some VAM produce large sporocarps (5-10
mm in diameter) containing many spores, and others form large ( 100-600 um in diameter),
single, thick-walled spores on the root surface, in the rhizosphere, or in the root tissues.
VAM fungi cannot grow saprophytically in soil and, therefore, can only grow while in
symbiotic association with their plant hosts. They may, however, survive for decades in
soil as dormant spores without plant associations.
VAM increase a plant's uptake of certain nutrients, particularly P. Cu. and Zn.
These elements are relatively immobile in soil, and zones of depletion develop near feeder
roots. The extramatrical growth of hyphae from VAM fungi can extend beyond the
feeder roots and increase the volume of soil from which these elements are absorbed.
The additional nutrient absorption due to VAM fungi can result in several-fold growth
increases in plants. The degree of plant benefit appears to be related to the plant's P
requirement, its ability to absorb nutrients from soil, the amount of available P in soil,
and the species of VAM fungus involved. Additions of available P to soil may eliminate
the plant's dependence on VAM (Baylis 1970, 1972~. However, it takes from 50 to 100
times the normal P levels found in forest soils to eliminate the VAM dependency of
hardwood trees (Kormanik et al., 1982~.
There are other significant benefits of VAM to plants. VAM are capable of
reducing the effects of various fungal pathogens and suppressing the effects of parasitic
nematodes (Schenck 1981~. VAM have also been shown to enhance water uptake,
increase tolerance to heavy metals, saline soils and drought, decrease transplant shock,
and bind soil into semistable aggregates.
Ectomycorrhizee
This type of association occurs on about 10% of the world flora. Trees belonging
to the Pinaceae (pine, fir, larch, spruce, hemlock), Fagaceae (oak, chestnut, beech),
Betulaceae (alder, birch), Salicaceae (poplar, willow), Juglandaceae (hickory, pecan),
Myrtaceae (eucalyptus), Ericaceae (Arbutus), and a few others form ectomycorrhizae.
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Some tree genera such as Alnus, Eucalyptus, Casuarina, Cupressus, Juniperus, Tilia,
Ulmus, and Arbutus will form both ectomycorrhizae and VAM, depending on soil
conditions and tree age.
Numerous fungi have been identified as forming ectomycorrhizae. In North
America alone it has been estimated that more than 2100 species of fungi form
ectomycorrhizae with forest trees. Worldwide, there are over 5000 species of fungi that
can form ectomycorrhizae on some 2000 species of woody plants. Among the
basidiomycetous fungi, species of Hymenomycetes (mushrooms) in the genera Boletus,
Cortinarius, Suill?vs, Russula, Gomphidius, Hebeloma, Tricholoma, Laccaria, and Lactarius
and species of the Gasteromycetes (puffballs) in the genera Rhizopogon, Sclerod~erma, and
Pisolithus form ectomycorrhizae. Certain orders in the Ascomycetes such as Eurotiales
(Cenococcum geophitum), Tuberales (truffles), and Pezizales have species that form
ectomycorrhizae on trees.
In ectomycorrhizae, intercellular hyphae surround cortical cells forming the Hartig
net, and several hyphal layers cover the outside of the feeder root forming the fungus
mantle. Ectomycorrhizal colonization normally changes the feeder root morphology and
color. They may be unforked, bifurcate, nodular, multi-forked (coralloid), or in other
shapes. Their color, which is usually determined by the color of the mycelium of the
fungal symbiont, may be jet-black, red, yellow, brown, white, or blends of these colors.
Unfortunately, with the exception of the above mentioned fungi, few of the hundreds
that exist in any given forest stand can be identified based on characteristics of the
ectomycorrhizae. The only sure way of identifying ectomycorrhizal fungi is with their
fruit bodies. As with VAM, ectomycorrhizal colonization is limited to the primary cortex
and does not spread beyond the endodermis or into meristem tissues of the feeder root.
Unlike VAM, however, many ectomycorrhizal fungi can be grown routinely in pure
culture. An important aspect of both VAM and ectomycorrhizal fungi is that neither
group of fungi can exist saprophytically in nature without a plant-host association.
Spores or resistant hyphae may survive long periods in soil without a plant host, but
the fungi from these propagules will not grow independent of their plant host as
saprophytes.
Ectomycorrhizal fungi aid the growth and development of trees. For some trees,
such as Pinus, they are indispensable for growth under natural conditions. The obligate
requirement of pine for ectomycorrhizae in a natural environment has been clearly shown
by numerous workers in tree regeneration trials in former treeless areas and in countries
without native ectomycorrhizal trees (Marx 1980, Mikola 1973~. Pine or other obligate
tree species can be grown from seed in aseptic culture, hydroponics, or elsewhere
without ectomycorrhizae. In these nonmycorrhizal conditions however, the seedlings must
be furnished with the factors (high nutrients, water) that are normally supplied by the
fungal symbiont and must be kept in a stress-free environment or they will die or not
grow normally. Mycorrhizae, especially ectomycorrhizae, appear to be the first line of
biological defense against stress for trees.
Trees with abundant ectomycorrhizae have a much larger, physiologically active,
root-fungus area for nutrient and water absorption than trees with few or no
ectomycorrhizae. This increase in surface area comes both from the multi-branching
habit of most ectomycorrhizae and from the extensive vegetative growth of hyphae of
the fungal symbionts from the ectomycorrhizae into the soil. These extramatrical hyphae
function as additional nutrient and water-absorbing entities and assure maximum nutrient
capture from the soil by the host. Ectomycorrhizae are able to absorb and accumulate
nitrogen, phosphorus, potassium, and calcium in the fungus mantles more rapidly, and for
longer periods of time, than nonmycorrhizal feeder roots. Ectomycorrhizae also appear
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to increase the tolerance of trees to drought, high soil temperatures, soil toxins (organic
and inorganic), and extremes of soil - acidity caused by high levels of sulfur or aluminum.
Ectomycorrhizae deter infection of feeder roots by root pathogens, such as species of
Pythium or PhytopAthora (Marx and Krupa 1978~. Hormone relationships induced by
fungal symbionts cause ectomycorrhizal roots to have greater longevity (length of
physiological activity) than nonmycorrhizal roots (Slankis 1973, Ng et al. 1982, Ek et al.
1983~. Not all species of fungi form ectomycorrhizae that have equal benefit to their
hosts. Some are more effective than others.
Many species of fungi are normally involved in the ectomycorrhizal associations of a
forest stand, a single tree species, an individual tree, or even a small segment of lateral
root. As many as three species of fungi have been isolated from an individual
ectomycorrhiza (Zak and Marx 1964~. Even as a single tree species can have numerous
species of fungi capable of forming ectomycorrhizae on its roots at any given time, a
single fungus can enter into ectomycorrhizal association with numerous tree species on
the same site. A single species of ectomycorrhizal fungus can develop numerous
biotypes or clones in a very limited area of a pure stand (Fries 1987~. Some fungi are
apparently host-specific; others have broad host ranges and form ectomycorrhizae with
members of numerous tree genera in diverse families.
Ectendomycorrhizae are intermediate types with features of both ecto- and
endomycorrhizae. In comparison to other mycorrhizal types, little research has been
done on them. They appear to have limited distribution in forest soils and tree nurseries
and are found on roots of normally ectomycorrhizal trees. Little is known of their
importance to trees.
Factors Affecting Mycorrhizal Development
Many factors affect mycorrhizal development. It is necessary, however, to separate
those that affect the tree from those that affect the fungal symbionts. Generally, any
soil or above-ground condition that influences root growth (i.e., carbon allocation) also
influences mycorrhizal development. The first prerequisite to mycorrhizal development is
that a susceptible feeder root be preformed by the plant host. Second, there must be
viable inoculum of a mycorrhizal fungus present in the rhizoplane to colonize the root.
Third, soil chemical, physical, and biological conditions must be favorable for successful
symbiotic colonization. The main factors influencing susceptibility of tree roots to
mycorrhizal infection appear to be photosynthetic potential and soil fertility. High light
intensity and low-to-mocterate soil fertility enhance mycorrhizal development; the other
extremes of these conditions (light intensity below 20% of full sunlight and excessively
high soil fertility) reduce, or may even prevent, ' mycorrhizal development. However, it
normally takes 10 to 50 times the nitrogen and phosphorus normally found in most forest
soils to significantly suppress mycorrhizal development of forest trees (Cline et al. in
press). Mechanical defoliation that reduces photosynthetic surfaces reduces mycorrhizal
development (Last et al. 1979~. Increased photosynthesis due to CO2 enrichment of the
atmosphere increases mycorrhizal development (O'Neill et al. 1987~. Light intensity and
fertility appear to influence either the biochemical status of feeder roots, such as
controlling levels of simple sugars, or the synthesis of new feeder roots, both of which
are products of carbon allocation (Ekwebelam and Reid 1983~. Roots growing rapidly
because of high soil fertility contain few simple sugars and they are not highly
susceptible to symbiotic colonization (Marx et al. 1977~. The supply of photosynthates
from the tree host to the fungal symbiont is of paramount importance to the
development, function, and maintenance of mycorrhizae.' This supply not only furnishes
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the energy and carbon for fungal growth but is intimately connected with nutrient uptake
of mycorrhizal roots (France and Reid 1983~.
The factors that affect the fungal symbionts directly are those which regulate
survival of the fungi in the soil or their growth on roots. Extremes of soil
temperatures, pH, moisture, etc., and presence of antagonistic soil microorganisms can
affect the survival of symbionts and thereby influence the mycorrhizal fungus inoculum
potential of the soil (Marx et al. 1984~. Unfortunately, with the exception of recent
work on fungicides (Marx et al. 1986, Marx and Cordell 1987), factors affecting survival
of inoculum of specific mycorrhizal fungi in soil have not been studied.
Actinorhizae
The term actinorhizae refers to the nodules that Frankia spp. form with roots of
their host plant. The nodules are lobed, coralloid, infection-induced lateral roots
exhibiting restricted apical growth but profuse branching.
Actinorhizal plants are fast-growing pioneer plants, mostly trees and shrubs, and are
important in the nitrogen economy of temperate forests. Typically, they colonize barren,
nutrient-poor soils. Roots of these plants are nodulated by filamentous bacteria in the
genus Frankia of the Actinomycetales. Taxonomically, actinorhizal plants are distributed
through at least 170 species among 22 genera in ~ plant families (Betulaceae,
Casuarinaceae, Coriaraceae, Datiscaceae, Elaeagnaceae, Myricaceae, Rhamnaceae, and
Rosaceae). However, not all species in all genera are affected. Like leguminous plants
with Rhizobium spp. or Bradyrhizobium spp., actinorhizal plants fix atmospheric N2 into
plant-available forms. Actinorhizal plants can fix up to 362 kg N/ha/yr, an amount
similar to that fixed by leguminous plant-rhizobial systems. The actinorhizal relationship
is beneficial to both organisms. Actinorhizal plants normally form mycorrhizae and
actinorhizae at the same time in natural environments. Some species lil~e AInus and
Casuarina can form tripartate symbioses, i.e., actinorhizae, VAM, and ectomycorrhizae, on
the same tree at the same time.
The characteristics of the actinorhizal infection reflect the great degree of
interaction between the symbionts. Frankia spp. are identified as thin, usually
nonseptate hyphae 0.8 to 1.2 um in diameter, forming intercalary or terminal sporangia
bearing spores and vesicles. Some strains have not been observed to sporulate. Some
isolates exhibit degrees of host-specificity while others do not. Hyphae of a strain of
Frankia that are compatible with the host penetrate a root hair and grow within the
root hair cell. Cortical cells in the vicinity begin to divide, even though they are not
yet infected. Hyphae then invade these cortical cells and begin to form vesicles. A
localized thickening, called the primary nodule, develops. A lateral root forms adjacent
to the primary nodule, and hyphae grow into the cortical cells from the primary nodule.
Thus, while prospective cells for infection in the primary nodule arise from
de-differentiation of cortical cells, cells for infection in the "true nodule" that develops
from the lateral roots arise from continued production of cells by the apical meristem of
the lateral root. The meristem itself is not infected. Once a cortical cell has
differentiated behind the meristem and starts to grow, hyphae infect the cell, coil around
the nucleus, and fill the cell. As an increasing number of cells in the true nodule
become infected and other apical meristems become active, the true nodule takes on a
lobed, coralloid appearance. Branched hyphae borne in intracellular clusters near the
host cell wall form swollen vesicles at the tips. These vesicles are probably the site of
N2 fixation. In alder nodules, each infected host cell contains one cluster of several
hundred vesicles in the upper tips of the nodule lobes. Lower parts of the lobes contain
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cells with degenerating endophyte, which seems to be digested eventually by the host
cells. Spores form in the late stages of the infection cycle, and decaying nodules release
spores into the soil. The pattern of cortical cells infected around the stele is
host-dependent. The same isolate in roots of different hosts may exhibit a different
infection pattern. Nodules last an average of 3 to 4 years but may persist for as long as
years. They may be over 3 cm in diameter and each can contain billions of spores.
Actinorhizae have great ecological and commercial significance. Many actinorhizal
plants (e.g., AInus spp. in the northern hemisphere) are important colonizers of N-poor
soils. Leguminous plants and other N-fixation symbioses are absent from large areas in
cool climates, such as in Canada and Scandinavia, so a large proportion of soil N in
those areas is derived through actinorhizae. Some alder spp. produce 15 to 25 tons of
biomass/ha/yr and are among the highest-yielding tree species in the temperate zone.
The N2-fixation activities of actinorhizae give rise to the ecological and commercial
importance of the relationship. Almost all Frankia spp. can use NH4+, NOB-, and
selected amino acids as sources of N and many exhibit growth on N-free cultural media.
In nodules, Frankia fixes N2 from the air into NH4+. However, more N2 is fixed than is
required by the endophyte, so some NH4+ is exported to the host cell cytoplasm,
converted to the amino acid citrulline, and translocated from the nodule to other parts
of the plant. Thus, a net accretion of N to the plant and to the site occurs.
Most factors affecting mycorrhizal development also affect actinorhizal
development. The nodule-forming process seems to be more sensitive than plant growth
to soil acidity. Most isolates of Frankia grow best in culture in pH 6.5-7.0 as do most
of their tree hosts. Vesicle formation and N2-fixation in culture can be suppressed with
increases in the availability of N. and nodulation is also suppressed by increased
concentrations of NH4+-N. This latter effect may be attributable to lowered C availablity
to the nodules under high-N conditions. As with mycorrhizae, actinorhizae represent a C
sink to the host. Nodulation and N2-fixation, therefore, are affected by host
photosynthetic rate. The activity of nodules is linked to the supply of photosynthate and
is altered by changes in light intensity, foliar area, girdling, mycorrhizal status (P
absorption), and C partitioning by the host. Any factor that supresses photosynthesis,
stimulates respiration, decreases photosynthetic area, and suppresses C transport to
roots affects actinorhizal development and function. For further information on
actinorhizae see Akkermans and Roelofsen (1980), Akkermans and Van Dijk (1981),
Akkermans et al. (1984) and Stowers (1987~.
ECOLOGICAL ASPECTS OF TREE SYMBIOSES
Other than the limited information presented above, there is a paucity of research
or observational data available on the ecology of endomycorrhizal and actinorhizal
associations of trees. The following discussion is, therefore, restricted to
ectomycorrhizal associations.
Fungal Succession and Forest Development
Terrestrial plant communities tend to be dominated by either endomycorrhizal or
ectomycorrhizal plants (Moser 1967~. During ecosystem succession to climax forest in
most temperate regions, the fungal associates of higher plants change from
endomycorrhizal or VAM dominance in herbaceous and scrub communities to
ectomycorrhizal dominance associated with trees (Rose 1980~. Tropical plant succession
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may progress from the nonmycorrhizal state of pioneer plants to an endomycorrhizal
status of climax hardwoods, such as those found in rain forest (Ianos 1980~.
In ectomycorrhizal fungus succession in forests, it is now recognized that there are
distinct early- and late-stage fungi. The pioneering work on this concept was done in
Scotland. Dighton and Mason (1985) suggested that early- stage fungi are similar to "r"
plant species (Harper 1977), since they spend most of their time in acts of colonization
then give way to other species in natural succession. They view late-stage fungi as
similar to "K" plant species since the latter are specialists in a resource-limited
environment with intense interference from their associates. In aseptic culture (i.e.,
without competition and other stresses) early- and late-stage fungi form ecto-
mycorrhizae on seedlings equally well. However, only the early-stage fungi are able to
rapidly colonize seedlings in natural, nonsterile soil that harbors competitors and other
stresses. Early-stage fungi may not totally disappear from mature stands, but they are
supplanted by more dominant species (Dighton et al. 1986a) or suppressed in
reproduction due to canopy characteristics. Last and Fleming (1985) suggest that the
differences in root physiology and rhizosphere populations between seedlings and mature
trees might be beneficial to volunteer seedlings. Late-stage ectomycorrhizae on the
mature trees may transfer carbon to these seedlings through the mycorrhizal bridge (Reid
and Woods 1969) and benefit seedling growth in the suboptimal light conditions in closed
canopy stands. This carbon transfer to seedlings may also function in clearcuts where
ectomycorrhizae are still viably attached to cut stumps and sprouts.
As trees become larger internal recycling of nutrients within the tree increases, and
demand for nutrients from soil generally decreases (Miller 1979~. The amount of carbon
available to support a mycorrhizal fungal symbiont may differ with tree size, with small
trees having limited supplies and supporting fungi with limited carbon demands, and
larger trees supporting more carbon demanding fungi (Mason et al. 1985, Last et al.
1985~. They concluded that the stage of development of the ecosystem would strongly
influence the resources available to mycorrhizal fungi, and that successional stages of
fungi occur due to their variable requirements for host carbon.
Associated with ectomycorrhizal fungus succession is increased fungal species
diversity with increasing stand age and increasing number of host species in the stand
(Mason et al. 1982, Last et al. 1984~. There is also evidence that the succession of
ectomycorrhizal fungi is influenced by a tree x soil interaction (Last et al. 1984~; seed
source, tree vigor and leaf retention (Mason et al. 1982~; and forest fertilization (Hora
1959, Shubin et al. 1977~. Fruit body production by these fungi, which is the main
parameter used to observe succession, is also strongly influenced by season of year,
rainfall amount and frequency, organic content of soil, root density, and degree of
ectomycorrhizal development (Wilkins and Harris 1946~. It is assumed that as
ectomycorrhizal development increases so does fruit body production as long as all other
factors are equal. The amount of fruit body production is an accurate surrogate for
degree of ectomycorrhizal development in bare-root tree nurseries (Marx et al. 1984~.
Whether this relationship holds true in complex ecosystems is unknown at this time.
Ectomycorrhiz~e and Net Primary Production
Ectomycorrhizae are important organs for the accumulation and storage of
soil-derived and host carbon-based nutrients. The first are essential for the tree host
and the latter for growth of hyphae and production of fruit bodies by the fungi. There
are no actual measurements of the quantities and types of plant carbon compounds used
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by ectomycorrhizal fungi as a proportion of total photosynthesis. Some estimates,
however, have been made in field situations.
The amount of photosynthate required to support a healthy and vigorous population
of ectomycorrhizal fungi on roots has been estimated in only a few cases. These
estimates, based on measured carbon content of fruit bodies and estimated carbon content
of the fungal mantle and extramatrical mycelia (turn-over rate), vary from a high of over
50°h in Douglas-fir forests in Oregon (Fogel and Hunt 1979) to a more likely 15% for the
same tree species (Vogt et al. 1982~. The first report did not verify that all fungal
components measured were ectomycorrhizal in origin; the latter report did.
Odum and Biever (1984) considered the ectomycorrhizal association a major
cybernetic control subsystem in terrestrial plant communities and concluded that it has
not been adequately considered in energy flow models. They based this conclusion on
measurements of the partitioning of net primary production between 4-year-old loblolly
pine and fruit bodies, ectomycorrhizae, and mycelia of specific fungi on severely eroded
soils in the Copper Basin of Tennessee. They estimated that from 15 to 25% of net
primary production flowed along the ectomycorrhizal pathway of trees on this site.
Production of fruit bodies by ectomycorrhizal fungi can be quite large in forest
stands. In Sweden, several thousand fruit bodies of over 70 species of ectomycorrhizal
fungi were collected during a 3-year period in a 5-ha stand of pure beech (Tyler 1984~.
In Scotland, a 5-year average of between 240,000 and 490,000 fruit bodies of
ectomycorrhizal fungi/ha were produced yearly under Scots pine (Richardson 1970~. In
Georgia, Thacker (1971) collected fruit bodies of ectomycorrhizal fungi for 1 year from
areas of about 3 ha in three different forest types. Collected fresh weights were 4812 g
of 31 fungal species in a 25-year-old pine plantation, 6560 g of 56 species in a
70-year-old pine stand, and 9991 g of 74 species in a 70-year-old pine-oak stand. This
report is the only one in the literature suggesting that fungal succession and increased
species diversity may occur in aging stands in the southern U.S.
ECTOMYCORRHIZAE AND ATMOSPHERIC DEPOSITION
Several controlled-exposure studies in recent years have shown that ambient or
above-ambient levels of atmospheric deposition can affect ectomycorrhizal development on
seedlings. Direct exposure of specific ectomycorrhizae of loblolly pine to Of and SO:
caused a significant reduction in their respiration, but respiration in nonmycorrhizal roots
was reduced more. Certain ectomycorrhizae were tolerant of On, while others were more
tolerant of SO2 (Carney et al. 1 97S, Garrett et al. 1982~. Shafer et al., ( 1985) found
that simulated rain treatments of pH 4.0 and 3.2 inhibited ectomycorrhizal development
of loblolly pine seedlings, but that rain treatment of pH 2.4 stimulated development.
Mahoney et al., (1985) found that root growth of loblolly pine was more heavily impacted
by O3 and SO2 in nonmycorrhizal than in mycorrhizal seedlings. Their results suggested
that ectomycorrhizae altered the pollution effects on root and shoot growth resulting in
more root growth and elimination of the effect of pollutants. Reich et al. (1985, 1986)
found that seedlings of white pine and northern red oak produced more short roots and
higher percentages of ectomycorrhizae after exposure to O~, and that SO2 and acid rain
treatments decreased both root parameters.
One could predict that any significant change in carbon allocation patterns to roots
caused by air pollution woulcl affect root growth and, subsequently, mycorrhizal
development (Reich et al. 1987, Winner et al. 1987~. Also, any significant change in soil
chemistry causing increased levels of available metals (A1, Zn, Pb, etc.) in solutions could
cause dysfunction in one or both partners in the symbiotic association (McCreight and
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Schroeder 1982, Jones et al. 1986, Wasserman et al. 1987~. Recently, Dixon and
Buschena (1988) showed that growth of nonmycorrhizal pine seedlings was reduced and
that ectomycorrhize protected the pine seedlings from toxicity caused by Cd, Cu. Ni, Pb,
and Zn. In Poland, Kowalski ( 1987) found distinct qualitative and quantitative changes in
ectomycorrhizae of various tree species planted on a prepared and fertilized site damaged
by industrial emission (SO2, Zn, and Pb). The percentage of living ectomycorrhizae
decreased with increasing pollution levels, but ectomycorrhizae were prevalent on even
the most pollution-damaged living trees. He concluded that reduced photosynthetic
activity, strongly altered soil chemistry, and high concentrations of heavy metals were
responsible for ectomycorrhizal depression. In the Netherlands, Termorshuizen and
Schaffers (1987) found three times more ectomycorrhizae, 20 times more fruit bodies,
and much greater fungus diversity in 5 to 1 0-year-old Pinus sylvestris than in 50- to
80-year-old trees. This observation appears to conflict with the succession and diversity
concept discussed earlier. However, in the older stand, these fungus parameters were
negatively correlated with concentrations of SO2, O3, and NH3. They were positively
correlated with the mean number of needleyears of these older trees. There were no
differences in soil chemistry between the two stands of trees. They concluded that the
lack of fungal species diversity on the old trees could cause a decreased resistance to
both man-made and natural stress. In Scotland, Dighton et al., ( 1 986b) applied 1500
mm/yr of pH 3.0 rain for 5 years to P. sylvestris trees and found a reduced abundance of
ectomycorrhizae and short roots. No abnormality in morphology was found in any
ectomycorrhizae. They concluded that increased levels of Al and Mn in the acid treated
soils reduced root growth, which caused a reduction in ectomycorrhizae. Numerous other
researchers in other parts of Europe have reported similar depressions in ectomycorrhizae
on trees with various degrees of foliar symptoms of air pollution damage (Blaschke 1981,
1982, Schlechte 1986~.
BETTER METHODS ARE NEEDED TO STUDY SYMBIOSES
Basically, we know only that unhealthy trees seem to have depressed root symbiotic
development compared to healthy trees. Biologically, this suppression is predictable. The
major problem is separating cause from effect -- the old chicken-and-egg dilemma. At
this time, we do not know what normal or abnormal populations of mycorrhizae or
actinorhizae are for any tree species, of any age, on any site, anywhere in the world.
How many species of symbionts are normal? What proportion of the short roots should
be symbiotically colonized? Is microbial succession from young to older trees a
worldwide phenomenon? Does it occur in actinorhizal and VAM tree systems? Is
succession caused directly by changing root physiology, soil characteristics, or
rhizosphere populations? If so, could atmospheric deposition alter succession? Or is
succession happening simply because it has had time to happen? Can normal succession
be interrupted by any form of plant stress? For ectomycorrhizae, is the presence of
late-stage fungi the result of physiological change in aging trees? Or is it simply due to
the fact that late-stage fungi do not proliferate or reproduce as rapidly, do not produce
spores in a manner that ensures rapid dissemination, do not produce as many spores as
do early-stage fungi and, therefore, take longer to appear in the system? Are the
late-stage fungi more or less susceptible to dysfunctions in physiology of roots or
foliage? Do exposure experiments on tree seedlings with early-stage ectomycorrhizae
contribute meaningfully to our understanding of the reaction of late-stage/mature trees
to the same exposure. Since we cannot recognize "normal", how are we to recognize
"abnormal" populations of symbiotic associations? The answer is very simple -- we can't!
Answers to these simple questions exist only for a few very isolated situations that may
not apply elsewhere. The biggest problem is that reliable and standardized methods to
study symbiotic relationships in the field do not exist (Schenck 1982~. Only in recent
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226
years have we been able to develop reasonably standardized methods for mycorrhizal
research on small tree seedlings with specific ectomycorrhizal fungi in a rather
controlled environment, the tree nursery.
Cline et al. (in press) discussed briefly the inherent problems in mycorrhizal
assessments and concluded that these assessments must be coupled to the root growth
rate, or to existing root biomass. Percent short root colonization is a widely used and
reasonably reliable assessment parameter for seedlings of comparabl sizes, but it has
serious limitations elsewhere. It is important to know the total number of short roots
that are available for potential colonization. A percent of short roots colonized tells us
little because one seedling may have 4000 short roots, and another 400. A visual
estimation of 50% infection tells little unless the 1 0-fold difference in total number of
short roots is also known. Number of mycorrhizae/cm of lateral root has little value
unless total number and length of lateral roots are also known. The diverse morphology
of ectomycorrhizae also creates assessment problems. One mature ectomycorrhiza of
Pisolithus tinctorius may have more surface area and more fungus tissue (more carbon
demand) than 20 ectomycorrhizae formed by Cenococcum geophilum on the same seedling.
How do we accurately measure the amount of fungal biomass? Gravimetric (France et
al. 1985) and catalytic potential (Iyer 1978) methods have been developed but neither
method measures lateral root length or short roots.
Growth rate of lateral roots may have profound effects on mycorrhizal assessments.
For example, mycorrhizal status may appear to decrease in a situation that stimulates
lateral root growth. In the presence of a lateral root growth stimulator, mycorrhizal
infection may lag behind lateral root extension and short root proliferation, thereby,
suggesting a depression in mycorrhizae. Examples of conditions or agents that stimulate
lateral root growth include fertilization (especially with phosphorus), warming of soils in
spring, and water becoming available after prolonged deficit.
Conversely, mycorrhizal status may appear to increase in the presence of a lateral
root growth inhibitor. If root growth slows or stops, the growth rate of the fungi and
roots may be more closely matched or the mycorrhizae may develop faster than new
short roots can be produced. The result is a net increase in numbers of mycorrhizae
over time and a higher percentage of short roots colonized without a significant increase
in total numbers of short roots. A few inhibitors of lateral root growth are rapid
defoliation (storm damage), moderate soil water deficits, soils getting colder in fall, soil
compaction, and depleted available soil phosphorus. Thus, the time of root sampling for
mycorrhizal assessments can influence greatly the perception of mycorrhizal status.
Very few methods have been developed to study survival of inoculum of microbial
symbionts in soil. Depression of symbiotic associations could be caused by depressed
survival of their inocula in soil. None of these symbionts can be isolated directly from
soil but, in the case of ectomycorrhizal and actinorhizal symbionts, they can be
reisolated from roots with considerable effort. Reisolation results, which vary from 1 to
10% success, however, do not relate directly to survival potential of the specific
microorganisms. Techniques have been developed to study the effects of various soil
treatments on survival of vegetative inoculum of Pisolithus tinctorius in nursery soil
(Marx et al. 1986, Marx and Cordell 1987~. This procedure uses nonmycorrhizal roots of
pine seedlings as a fast "trap" of viable inoculum and is reasonably quantitative. This
technique could be modified to test survival of other propagules of these microorganisms,
such as spores and sclerotia. A problem remains, however, because of the apparent
physiological differences between early-stage (like P. tinctorius) and late-stage fungi.
With this technique, can seedling roots be used as a "trap" for inocula of late-stage
fungi? Can nonmycorrhizal seedlings be transplanted into variously treated soil collected
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227
from mature stands and form mycorrhizae with late-stage fungi? Another ecological
aspect of symbiotic associations, especially ectomycorrhizae, which has been completely
ignored is what can happen to the airborne spores of these fungi while in flight. During
fruit body production by these fungi, thousands of spores/m3 of air/day (LeTacon et al.,
1987) are airborne for various periods of time. What effects do gaseous pollutants, such
as Of and S02, have on their viability during this spore-flight period? What effect does
acidic rain have during spore washout from the air?
There is no easy way to assess accurately root symbiotic associations on tree
seedlings, on small trees, or in natural soil. Reliable and reproducible methods to
qualitatively and quantitatively assess root symbioses must be developed if we are ever to
understand their reaction to man-made and natural stresses in either experimental or
real-world situations. When we realize that the "abnormal" environment of today may be
the "normal" environment of tomorrow, we must not delay in developing these methods.
CONCLUSION
Common biological sense indicates that root symbiotic associations are responsive to
effects of atmospheric deposition on forests. Unfortunately, at this time, base-line data
does not exist as to the symbiotic status of healthy forests. Techniques to assess
quantitatively and qualitatively symbiotic associations on forests containing trees of
different age and species, do not currently exist and must be developed before this
information can be produced. Because of these limitations, it is doubtful that symbiotic
associations can be used today as potential biological markers of the effects of
atmospheric deposition on forest health.
SUMMARY
1. Root symbioses (mycorrhizae or actinorhizae) are as common on roots of plants in
forest ecosystems as are chloroplasts in leaves of plants in the ecosystems.
2. A forest ecosystem, a stand of mixed tree species, a plantation of trees, a single
tree, or a small segment of lateral root on a tree can have many types of symbioses with
multiple microbial species.
3. Susceptible short roots on lateral roots must be formed by the tree host before root
colonization by microbial symbionts can occur.
4. Viable inoculum of the symbiotic microorganisms must be present near susceptible
roots before symbiotic colonization can occur.
5. Edaphic factors can strongly influence root colonization by affecting root growth and,
probably, inoculum survival and viability of the microbial symbionts.
6. Vitality of root symbiotic associations is strongly dependent on tree host physiology,
mainly photosynthesis. Reduced photosynthesis equals reduced root symbioses.
7. Ectomycorrhizal fungal succession apparently occurs during the development of forest
stands. Increasing age of stands and increasing number of tree species in the stand
increase ectomycorrhizal fungus species diversity.
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228
S. Current methods to measure root symbionts or their function have severe limitations,
especially for ecological studies, and better methods must be developed.
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Representative terms from entire chapter:
root growth
