Annals of Botany 77: 365–374, 1996
The Structure and Function of the Ericoid Mycorrhizal Root
D. J. READ
Department of Animal & Plant Sciences, Uni ersity of Sheﬃeld, PO Box 601, Sheﬃeld, S10 2UQ, UK
Received: 3 February 1995 Accepted: 9 December 1995
The uniformity of structure of the anatomically simple ericoid mycorrhizal hair root across many plant families,
including Epacridaceae, that are diagnostic of heathland, and the characteristic restriction of its occurrence to
nutrient impoverished soils, are both emphasized. The extent to which the predominantly ascomycetous fungal
endophytes of these roots are taxonomically related is discussed. In functional terms, the role of the mycorrhiza in
nutrient mobilization is evaluated on the basis of experiments with ericaceous plants. The considerable saprotrophic
potential of endophytes such as Hymenoscyphus ericae is demonstrated and the signiﬁcance of this for nitrogen (N)
and phosphorus (P) nutrition of plants growing in sclerophyllous litter of high C:N and C:P ratios is discussed. The
need to carry out experiments using epacrid hosts is stressed. It is considered that the selective provision, by ericoid
mycorrhizal fungi, of access to recalcitrant organic sources of N and P facilitates niche diﬀerentiation and so
contributes to the maintenance of species diversity which is a feature of heaths with a signiﬁcant component of epacrid
or ericaceous plants particularly in the southern hemisphere. # 1996 Annals of Botany Company
Key words: Ericoid mycorrhiza, hair root, heathland, nitrogen mobilization, Epacridaceae.
INTRODUCTION
In 1979 Specht described the heathlands of the world as
being united by their evergreen sclerophyllous nature, by
the presence, but not necessarily the dominance of the
families Diapensiaceae, Empetraceae, Epacridaceae,
Ericaceae, Grubbiaceae, Prionotaceae and Vacciniaceae,
and by their ecological restriction to soils very low in plant
nutrients.
It has subsequently been argued (Read, 1983; Read and
Kerley, 1995) that emphasis upon phenology of aboveground
parts has diverted attention from a below-ground
structure, the ericoid mycorrhizal root, which has even
greater uniformity through the families listed by Specht,
than any aspect of the shoots. This structure, long known to
be a characteristic feature of ericaceous genera of the
northern hemisphere (Rayner, 1915, 1925, 1929), was ﬁrst
described in the Epacridaceae by McLennan (1935). It is
characterized by reduction of its vascular and cortical
tissues, by the absence of root hairs, and by the presence in
what would be the piliferous zone of a conventional plant
root, of swollen epidermal cells occupied by mycorrhizal
fungi (Fig. 1). Ericoid mycorrhizal roots have now been
observed in a large number of epacrid genera (Table 1). The
individual roots, as a result of their anatomical simpliﬁcation,
are delicate structures, often referred to as ‘hairroots’
usually each having a diameter in the distal regions of
less than 100 µm (Fig. 2A, B). Collectively, the hair-roots
form a dense ﬁbrous root system the bulk of which is
concentrated towards the surface of the soil proﬁle (Dodd et
al., 1984; Pate, 1994).
While the soils in which plants with ericoid mycorrhizal
roots ﬂourish are rightly characterized by their impoverished
nutrient status, they cover such a broad latitudinal range
that they show a great diversity of hydrological conditions.
Thus in the southern hemisphere epacrids are found on the
permanently moist soils of the Magellanic tundra complex
of Patagonia (Pisano, 1983) and the Sphagmum mires of
New Zealand (Wardle, 1991) as well as on the dry sandplains
of Australia. Each of these very diﬀerent moisture
regimes causes a distinctive pattern of seasonal development
of the essentially ephemeral ericoid root system, it being
active in the moist winter season in the sand-plain heath
environment (Read, 1983; Bell, Pate and Dixon, 1994) but
in the drier summer season in peat dominated systems of
high latitudes.
It is important to bear this diversity of habitat type in
mind when considering functions of the ericoid root. While
there is an apparent logic and appeal in the assumption that
a structure as uniform as this should also be uniform in its
function, it will be shown below that such structures have a
wide range of functional attributes. At the very least it
would be wise to determine which, if any, of these attributes
are important in a given ecological circumstance, and to
bear in mind that the ericoid mycorrhizal root is part of an
overall adjustment of epacridaceous or ericaceous species to
the extreme nutritional impoverishment of heathland soils.
Only by evaluating the above and below ground attributes
of these plants in an integrated manner will we eventually
achieve a realistic understanding of what provides ‘ﬁtness’
in their peculiarly harsh environments.
The fungi forming ericoid mycorrhiza
It has now been ﬁrmly established that fungi isolated from
epidermal cells of hair roots of the Ericaceae (Fig. 3)
typically produce dark coloured slow growing sterile and
dematiaceous mycelia in agar cultures. Many such isolates
0305-7364\96\040365j10 $18.00\0 # 1996 Annals of Botany Company
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366 Read—Structure and Function of the Ericoid Root
F. 1. The ericoid mycorrhizal root of Epacris impressa as originally
depicted by McLennan (1935). Epidermal cells heavily colonized by
hyphal complexes are seen to enclose narrow cells of the exodermis,
endodermis and the monarch stele.
form zig-zag chains of arthroconidia in culture (Burgeﬀ,
1961; Pearson and Read, 1973) a feature which has led
Dalpe! , Litten and Sigler (1989) to assign them to the genus
Scytalidium (Fig. 4). Some of these isolates also produce
apothecia which has enabled them to be identiﬁed as the
ascomycete Hymenoscyphus ericae (Read) Korf and Kernan
(Read, 1974). Comparative analysis of ribosomal DNA
sequences of an isolate of Vaccinium identiﬁed as being
Scytalidium accinii and of H. ericae suggest that there is an
anamorph-teleomorph relationship between these two fungi
(Egger and Sigler, 1993).
Until recently the question of the identity of fungi
forming ericoid mycorrhiza in Epacridaceae had not been
addressed. Two studies, one carried out in eastern (Reed,
1987) the other in western Australia (Hutton, Dixon and
Sivasithamparam, 1994) have now added considerably to
our knowledge. They indicate that isolates obtained from
epidermal hyphal complexes (Fig. 5) have broadly similar
culture characteristics to those seen in their ericaceous
counterparts of the northern hemisphere. Again, they are
dark coloured slow growing sterile dematiaceous fungi. It is
apparent on the basis of light (Reed, 1989; Hutton et al.,
1994) and electron (Allen et al., 1989) microscope studies
revealing the presence of simple septa that they are of
ascomycetous rather than basidiomycetous aﬃnity. These
observations coupled with that of Reed (1989), subsequently
conﬁrmed by Read and Reed (unpubl. res.), that fungal
isolates of Epacridaceae readily form typical root ericoid
T 1. Records of epacrid genera that ha e been reported
to ha e ericoid mycorrhiza
Epacrid genus Reference
Acrotriche Reed, 1987
Andersonia Reed, 1987; Hutton et al., 1994
Astroloma Hutton et al., 1994; Bell et al., 1994
Brachyloma Reed, 1987; Hutton et al., 1994
Conostephium Reed, 1987; Hutton et al., 1994
Cyathodes McNabb, 1961
Dracophyllum McNabb, 1961; Allen et al., 1989;
Logan et al., 1989
Epacris McLennan, 1935; Reed, 1987
Leucopogon McNabb, 1961; McGee, 1986; Reed, 1987, 1989;
Brundrett and Abbott, 1991; Logan et al., 1989;
Hutton et al. 1994; Bell et al., 1994
Lissanthe Reed, 1987
Lysinema Reed, 1987; Hutton et al., 1994
Melichrus Reed, 1987
Monotoca Reed, 1987
Needhamiella Reed, 1987
Oligarrhena Reed, 1987
Pentachondra McNabb, 1961; Reed, 1987
Richea Reed, 1987
Rupicola Reed, 1987
Sphenotoma Reed, 1987; Hutton et al., 1994
Sprengelia Reed, 1987
Styphelia Reed, 1987
Trochocarpa Reed, 1987
Woollsia Reed, 1987
mycorrhiza in hair roots of Ericaceae, and ice ersa, are
strongly suggestive of close relationships between the fungi.
However, on the basis of pectic zymogram analysis it was
reported (Hutton et al., 1994) that none of the isolates
obtained from 14 genera of Western Australian epacrids
produced banding patterns which perfectly match those of
ericaceous isolates. Notwithstanding this, the similarities
between published zymograms of some of the isolates,
notably Ec2 and Ec3 obtained from Andersonia and those of
ericaceous isolates 100 and 101 are striking. The appearance
of these two epacrid isolates in culture is also very
reminiscent of H. ericae.
There is a need for DNA sequence analysis of these
isolates to be run in parallel with studies of their functional
attributes or when grown with epacrid or ericaceous hosts.
The work of Perotto et al. (1995) is moving in this
direction.
Some workers have reported the isolation of Oidiodendron
spp. from mycorrhizal hair roots of ericaceous species
(Burgeﬀ, 1961; Couture, Fortin and Dalpe! , 1983; Dalpe! ,
1986, 1991; Douglas, Heslin and Read, 1989; Xiao and
Berch, 1992). To date there appear to be no reports of these
fungi being isolated from epacrid roots. The banding
patterns produced in pectic zymograms by a series of
European at North American isolates of Oidiodendron were
shown by Hutton et al. (1994) to be distinct from those of
fungi obtained from epacrid mycorrhiza.
In addition to these records of fungi isolated from typical
ericoid mycorrhiza, there are a few reports in the literature
of colonization of epacrid and ericaceous roots by arbuscular
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Read—Structure and Function of the Ericoid Root 367
A B
F. 2. A, Transverse section of ericoid hair root of Leucopogon ericoides Smith R. Br. ﬁxed in glutaraldehyde and embedded in Spurrs resin. Root
diameter approx. 67 µm. Material ﬁxed sectioned for TEM and photographed by Suzanne Bullock. This section is taken in a mature region of
the hair root and shows relatively light colonization. B, Transverse hand section of young hair root of Calluna ulgaris indicating very heavy
colonization of all of the epidermal cells by a mycorrhizal endophyte. Root diameter approx. 70 µm.
(VA) and ectomycorrhizal (ECM) fungi. Bellgard (1991),
without mention of ericoid colonization, reports the
presence of VA associations in Brachyloma, Epacris and
Leucopogon growing on Hawkesbury sandstone, while
McGee (1986) observed ericoid colonization in the latter
genus but VA and ectomycorrhiza in Astroloma. Similarly
in Ericaceae, plants which would normally have ericoid
infection have been reported to be colonized by ectomycorrhizal
(Largent, Sugihara and Wishner, 1980; Dighton
and Coleman, 1991) and VA (Johnson, Joiner and Crews,
1980; Koske, Gemma and Englander, 1990; Dighton and
Coleman, 1991) fungi. Since in none of these reports were
attempts made to determine the functional status of the
fungal colonization, their status remains uncertain. There is
increasingly evidence that when growing from a true ‘host’
mycorrhizal fungi of the VA type have suﬃcient inoculum
potential to enable penetration of nearby plants which are
not normally colonized (Francis and Read, 1995). The
outcome of such colonization can, however, be detrimental
to the ‘non-host’ and under these circumstances any
suggestion that the occurrence represents a mycorrhizal
symbiosis should be treated with caution.
Leake and Read (1991) have stressed the need to satisfy
the requirements of Koch’s (1912) postulates when assessing
the status of any putative mycorrhizal association. This
requires not only that a healthy structural relationship
between host and fungal inoculant is produced under
conditions which are free of exogenous sources of simple
sugars, but also that some measures of host response be
obtained. By growing seedlings of Calluna ulgaris under
deﬁned conditions in the presence of a range of fungal
isolates of ericoid roots, they showed that while some
including H. ericae, S. accinii and to a lesser extent O.
griseum gave a positive growth response in the seedlings,
others were inhibitory. Ideally these studies should be
carried out in natural soil but the complication associated
with the need to sterilize such substrates makes this
problematical.
It is arguable also that to challenge the delicate hair roots
of an epacridaceous or ericaceous seedling with vigorous
inoculum of a single fungus is unrealistic, since in nature the
emerging radical immediately enters a complex community
of microorganisms. The use of mixed inocula of putative
endophytes and saprotrophes would enable determination,
either by use of in situ immunocytochemical identiﬁcation,
or by sequence analysis following subsequent re-isolation,
of which fungi gained access to and formed compatible
associations with a particular host species. Such studies if
carried out in a range of hosts and substrates would help to
provide answers to the challenging question of the relative
importance of host and ecological speciﬁcity in determining
the outcome of host-fungus interactions.
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368 Read—Structure and Function of the Ericoid Root
F. 3. Individual epidermal cell of Calluna released from the root axis
by maceration after serial washing in distilled water, showing emergence
of mycorrhizal fungus from hyphal complex occupying the cell. Such
direct observation of fungal growth from the cell is desirable if
prerequisite for any claim of mycorrhizal status.
What we know about functional aspects of the ericoid
mycorrhiza
It arises from the essentially superﬁcial pattern of distribution
of ericoid mycorrhizal roots in the soil proﬁle that
they are in intimate contact with the detrital material
produced as the above and below ground parts turnover. In
an environment characterized by extremes of nutrient
impoverishment it is clearly important to determine the
extent to which these roots are directly involved in turnover
processes.
The conventional view of the function of a root as a
nutrient absorbing organ is that it provides eﬀective
interception of minerals released from organic polymers or
insoluble salts by the activities of a decomposer population.
Within this scenario mycorrhizal colonization has been
interpreted simply as providing greater eﬀectiveness in such
mineral scavenging activities. There is, indeed, evidence that
H. ericae can assimilate nitrate, ammonium (Bajwa and
Read, 1986) (Fig. 6A) and phosphate (Pearson and Read,
1975) ions, and the importance of this should not be
overlooked, in particular in sandy heathland soils of warmer
regions. Signiﬁcant amounts of nitriﬁcation can, for
example, occur in these soils (Hannon, 1956) and in view of
the very low nitrate reducing ability of ericaceous (Havill,
Lee and Stewart, 1974) and epacridaceous (Stewart, Pate
and Unkovich, 1993) plants themselves, access to the nitrate
ion may be largely dependent upon mycorrhizal colonization.
Experiments have shown, however, that the fungi
forming ericoid mycorrhiza also have saprotrophic capabilities
suﬃcient to enable competition with decomposers,
and so have exposed the possibility of direct involvement of
the mycorrhizal root in mobilization of N and P from the
organic residues which are the major repository of both of
these elements in most heathland ecosystems (Read, 1983;
Read and Kerley, 1995).
The ﬁrst indication of this type of activity came from a
study in which "&N labelled ammonium was fed to
mycorrhizal (M) and non-mycorrhizal plants of Vaccinium
growing in sterile heathland soil (Stribley and Read, 1974).
It was observed that despite having signiﬁcantly greater
yields and total nitrogen contents the M plants had lower
"&N enrichment, indicating that dilution of label by
alternative N sources had occurred. In the absence of
nitriﬁcation, organic residues were the only realistic candidates.
This observation led to a series of analyses in which
the saprotrophic potential of ericoid endophytes was
examined in pure culture and in association with their host
plants. In addition to an ability readily to use ammonium or
nitrate as sole source of N H. ericae used amino-acids,
(Bajwa and Read, 1986) (Fig. 6B, C) peptides (Bajwa and
Read, 1985) of a range of chain lengths, and protein, the
polymeric forms of organic N being broken down by the
activities of an acid carboxy-proteinase enzyme (Leake and
Read, 1989a, 1990a). When these experiments were repeated
using plants grown in the M or NM condition, it was shown
that substantial quantities of N assimilated from organic
sources by ericoid fungi were transferred to the autotroph
(Stribley and Read, 1980; Bajwa and Read, 1985, 1986;
Bajwa, Abuarghub and Read, 1985).
The thrust of work in recent times has been towards
evaluating the extent to which the saprotrophic capabilities
revealed in studies using model N compounds, might be
expressed also in natural environments where the element is
likely to be contained in more complex polymers or to be
precipitated with polyphenolic compounds.
Of the naturally occurring polymers which are a signiﬁcant
repository of N, chitin, particularly in soil horizons heavily
exploited by mycorrhizal fungi, is likely to be amongst the
most important. It is known to be a major constituent of the
hyphal walls of H. ericae itself (Bonfante-Fasolo and
Gianinazzi-Pearson, 1982). Leake and Read (1990b) showed
that chitin, when supplied as sole N source to H. ericae in
pure culture was able to support growth of the fungus.
More recently Kerley and Read (1995) have grown H.
ericae, which is likely itself to be the main potential source
of fungal N in heathlands dominated by ericaceous plants,
under aseptic conditions, and used its dead mycelium as a
sole source of N for Vaccinium plants grown with and
without mycorrhizal colonization. Mycorrhizal plants
gained suﬃcient access to N contained in this substrate to
enable signiﬁcant increases of yield and N concentration
(Figs 7, 8). Puriﬁed hyphal wall fractions can also provide N
sources for H. ericae the culture ﬁltrates of which after
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Read—Structure and Function of the Ericoid Root 369
F. 4. Segmentation of hyphae of an isolate of H. ericae to zig-zag chains of arthroconidia which are characteristic of Scytalidium.
growth on such substrates reveal evidence of chitinolytic
activity in the form of glucosamine residues (Kerley and
Read, 1995).
Soluble protein released from plant and fungal tissues on
senescence would also be accessible to fungi with well
developed proteolytic potential, but the half-life of protein
as a free component in mor-humus litters of the kind
produced under polyphenol-rich heathland plants is likely
to be short. Experiments using aqueous extracts of these
materials, or tannic acid as a model polyphenolic compound,
over a pH range characteristic of the soil produced from
them, demonstrate the eﬀectiveness with which protein is
co-precipitated by tannins. Bearing in mind the very high
concentrations of polyphenols typically found in sclerophyllous
tissues of the ericaceous type (Jalal, Read and
Haslam, 1982), it is probable that such precipitation will
occur during breakdown of cellular compartmentation as
senescence proceeds so largely removing free protein from
circulation. Under these circumstances the key question
would concern the extent to which the ericoid endophytes
have access to protein-N that is precipitated in this way.
Answers to these questions are beginning to emerge for
ericaceous hosts but remain to be sought in the case of
epacridaceous mycorrhiza.
It has been shown (Leake and Read, 1989b; Bending and
Read, unpubl. res.) that H. ericae has considerable potential
to mobilize protein N even when the source polymer is
co-precipitated with polyphenols such as tannic acid. Its
biomass yield is unrestricted (Fig. 9) and N is acquired from
such sources in amounts greater than those obtained when
NH
%
-N is supplied at the same concentration (Fig. 10). This
N can eventually be transferred to the host in suﬃcient
quantity to enhance its growth and its release appears to be
achieved by a combination of polyphenol-oxidase (PPO)
and proteinase activities (Bending and Read, unpubl. res.).
Assays of the latter (Fig. 11) suggest inhibition of the
enzyme in the presence of tannic acid (Fig. 12) but part of
this may be attributable to co-precipitation of protein and
product in the presence of the phenolic compound.
The ability to degrade polyphenols, perhaps combined
with ligninolytic activity (Haselwandter, Bobleter and Read,
1990) enables the fungus to achieve a broadly based attack
upon the scleroplyllous residues which protect the scarce
nutrient resources in heathland soils. While nitrogen may be
quantitatively the most important of these, others notably
phosphorus (P) may also be released by activities of this
kind. H. ericae has been shown to release P from ferric and
aluminum phytates which are thought to be the major
sources of the element in acid organic soils (Mitchell and
Read, 1986).
There have as yet been relatively few studies of the
functional aspects of ericoid mycorrhiza in epacrids and
these are clearly much needed. However, a recent examination
of the responses of seedlings of four epacrid species
(Andersonia gracilis, Astroloma xerophyllum, Leucopogon
conostephiodes, and Leucopogon kingianus, now Croninia
kingianus) (Bell et al., 1994) lends general support to the
view established from studies, reported above, of their
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370 Read—Structure and Function of the Ericoid Root
F. 5. Endophyte emerging from epidermal cell of Leucopogon
juniperinus after serial washing of the hair root and plating on water
agar (from Reed, 1987).
50
0
Days
Endophyteyield(mg)
40
30
20
10
10 20 30
A
pH
8
6
4
2
50
0
Days
40
30
20
10
10 20 30
B
pH
8
6
5
4
7
50
0
Days
40
30
20
10
10 20 30
C
pH
5
4
3
2
F. 6. Dry weight yields (——) of H. ericae and changes of pH (---) of media after growth of the fungus on nitrate, ammonium or a series of
acidic and basic amino-acids as sole sources of N. (A) Mineral (>, NH
%
; $, NO
$
) or minus N (#, control) treatments, (B) acidic amino acids
($, Aspartic acid; #, Glutamic acid) and (C) basic amino acids ($, 2 Amino-butyric; #, Arginine). (From Bajwa and Read, 1986.)
10
0
Day of harvest
Plantdryweight(mg)
6
4
2
24 6012 36 48
***
***
***
8
F. 7. Yield of V. macrocarpon grown in the mycorrhizal (M) and nonmycorrhizal
(NM) condition with dead intact mycelium of H. ericae
(IHE) as sole N source. Vertical bars represent l.s.d. P l 0n05.
*** Indicates signiﬁcant diﬀerence between MjIHE and NMjIHE at
P 0n001 according to one way ANOVA. (From Read and Kerley,
1995.)
ericaceous counterparts, that the symbiosis plays a primary
role in the acquisition of nitrogen for the plant. Seedlings of
these species were transferred in minimally disturbed soil
cores from the ﬁeld to pot cultures in a glasshouse where
they were supplied with distilled water, with complete
nutrient solutions or with solutions containing only nitrogen
or only phosphorus.
Three of the species showed signiﬁcant positive responses
of shoot height and plant dry weight to N added as
NH
%
NO
$
whereas addition of P as PO
%
led to little or no
such growth response. Addition of complete nutrient
solution resulted in dry matter yields not signiﬁcantly
greater than those observed in the N only treatment, a
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Read—Structure and Function of the Ericoid Root 371
0.2
0
Day of harvest
PlanttotalN(mg)
0.15
0.10
0.05
24 6012 36 48
***
***
***
F. 8. Whole plant nitrogen content (mg plant dry weight) of V.
macrocarpon grown and analysed as described in Fig. 7. (From Read
and Kerley, 1995.)
42
35
Time (d)
Mycelialdryweight(mg)
25
30
20
15
10
5
14 280
a* b** c*
F. 9. Dry weight yield of mycelium of H. ericae grown with pure
protein ( ), protein precipitated with tannic acid (=), or with basal
medium containing ammonium (#) (control) N, as sole N sources.
Letters indicate signiﬁcance of diﬀerences between treatments at a
given harvest as determined by one-way ANOVA. a, Treatments
signiﬁcantly diﬀerent except pure protein s. precipitated protein. b,
Signiﬁcant diﬀerence between control and precipitated protein. c, All
treatments signiﬁcantly diﬀerent. ** Indicates diﬀerences signiﬁcant at
P 0n01. * Indicates diﬀerences signiﬁcant at P 0n05. (From Bending
and Read, unpubl. res.)
further feature suggestive of a pivotal role of this element in
determining plant responses. L. kingeanus failed to respond
to any of the treatments. Labelling of the complete or N
treatments with "&NH
%
or "&NO
$
showed that both forms of
N were taken up and incorporated into plant insoluble N.
While apparently conﬁrming the importance of nitrogen
acquisition for epacridaceous plants these experiments do
not inform us as to the role of the mycorrhiza in qualitative
or quantitative aspects of N assimilation and leave unanswered
the important question of the extent to which
colonization provides the plant with access to organic
residues in the ﬁeld.
600
0
C
Treatment
TotalmycelialNcontent(µg)
BSA TA–BSA
500
400
300
200
100
a**
F. 10. Total nitrogen content of harvested mycelium of H. ericae at
ﬁnal harvest after growth with pure protein (BSA), protein precipitated
with tannic acid (TA-BSA), or on basal medium with ammonium as
N source (C). a**, Indicates all treatments signiﬁcantly diﬀerent at
P 0n01 according to one-way ANOVA. (From Bending and Read,
unpubl. res.)
42
35 000
Time (d)
Proteaseactivity
(fluorescenceunitsper3h)
25 000
30 000
20 000
15 000
10 000
5000
14 280
a** b* c*
F. 11. Extracellular protease activity of H. ericae measured over a
time-course in media containing pure protein ( ), pure protein
precipitated with tannic acid (W), the culture ﬁltrate of protein-tannic
acid treatment (=), and the basal medium without protein (#). a**,
Indicates activity in protein treatment signiﬁcantly diﬀerent from
protein-tannic acid and control at P 0n01. b*, Indicates both protein
and protein tannic acid treatments signiﬁcantly diﬀerent from control
at P 0n05. c*, Indicates all treatments signiﬁcantly diﬀerent except
protein-tannic acid and culture ﬁltrate of protein-tannic acid at P
0n05. (From Bending and Read, unpubl. res.)
DISCUSSION
Both in the managed Calluna-type heathlands of the
northern hemisphere (Gimingham, 1972) and in the natural
heaths of Australasia (Bell, Hopkins and Pate, 1984) ﬁre is
an important factor in the nutrient economy of the
ecosystem. In both types of community burning has a
particular impact upon the N economy of the system, up to
80% of the fund of nitrogen that has accumulated between
burns being lost (Pate and Dell, 1984). Similar ﬁgures have
been suggested in Europe (Allen, 1964). Chapman (1967)
showed that volatilization of N during a burn in Calluna
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372 Read—Structure and Function of the Ericoid Root
Ericoid mycorrhizal dwarf
shrubs, e.g. Erica, Calluna,
Epacris, Leucopogon. Fungal
mobilization of plant litter
and microbial protein N.
Insectivores, e.g.
Drosera, Sarracenia
capture and release of
insect protein N.
Legumes, e.g. Ulex,
Daviesia, Dillwynia.
Nodulated for
atmospheric N fixation.
Cyperaceous or restionaceous
plants, e.g. Eriophorum, Restio, with
aerenchymatous roots tapping
deep N and dauciform or cluster
roots scavenging surface mineral N
—latter also in Proteaceae.
COMPARTMENTATION OF NITROGEN ACQUISITION IN HEATHLAND ECOSYSTEMS
F. 12. Diagrammatic view of possible processes whereby niche separation in heathlands of northern and southern types might arise through
mutualistic or structural modiﬁcations which provide access to qualitative diﬀerent sources of the major element nitrogen.
heathland was equivalent to 173 kg ha−" and that because
cumulative inputs from rainfall in the 12 year period
between ﬁres was only 62 kg serious N deﬁcits occurred. In
Europe concerns over deﬁcits in the N budget have been
replaced in recent times by considerations of excess
deposition, inputs of pollutant N in the form of NH
%
and
NO
$
having reached in excess of 30 kg ha−" in some
heathlands (INDITE, 1994). Nitrogen saturation is now
thought to be promoting the process whereby ericaceous
plants are being progressively replaced in what were the
heathlands of north-west Europe by grasslands (Heil and
Diemont, 1983). In eﬀect, N saturation removes the
advantages of nutrient conservation associated with sclerophylly,
as well as those derived from the ericoid mycorrhiza
which, it is proposed, has evolved to provide selective access
to the conserved resource. Instead it favours those species
able rapidly to respond to surges of mineral N availability.
Epacrids still ﬂourish in the relatively unpolluted heathlands
of Australasia, and it is reasonable to hypothesize that
they do so in some measure as a result of those attributes
shown above to be features of ericoid mycorrhizas. There is
clearly a need to explore further the functional relationships
between the mycorrhiza of epacrid and ericaceous species.
Amongst the attributes of particular interest in the naturally
ﬁre-prone epacrid habitat are the nature and distribution of
fungal propagules in the post ﬁre environment, the
relationship between seedling establishment and mycorrhizal
colonization, and the role of the mycorrhiza in the
processes of nutrient acquisition through the inter-ﬁre cycle.
In an attempt to evaluate the possible contribution of
mycorrhiza to the determination of the structure of wet
heathland communities of the northern hemisphere Read
(1993) presented a schematic view of the manner whereby
distinctive mutualisms, together with modiﬁcations of root
distribution and anatomy, might promote species diversity
by enabling exploitation of diﬀerent sources of the critical
growth limiting element nitrogen. In this, the co-existence of
ericaceous, leguminous and carnivorous species typically
seen in heaths of moderate acidity, was facilitated by their
abilities to use sources of N derived respectively, from soil
organic matter, the atmosphere and captured animals.
Structural modiﬁcations, in particular production of aerenchyma,
enables cyperaceous species to penetrate waterlogged
horizons where they exploit N sources, including
organic forms (Chapin, Morilanen and Keilland, 1993),
untapped by the other groups that are essentially surface
rooting.
The species diversity seen in heathlands containing
epacrids is generally greater than that seen in those
dominated by ericaceous species but it appears that there is
a commensurate increase in the range of specialisms which
they exhibit (Lamont, 1982, 1984; Pate, 1994). It can
atMasarykUniversityonApril25,2016http://aob.oxfordjournals.org/Downloadedfrom
Read—Structure and Function of the Ericoid Root 373
therefore be hypothesized that the same niche separation
occurs (Fig. 12). Amongst the distinctive families of southern
heaths the Proteaceae and Restionaceae are characterized
by the production of cluster roots. These structures are
formed in the same superﬁcial horizons of the soil proﬁle as
are ericoid roots, where they also exploit the region of
actively decomposing litter (Lamont, 1984). Though spatial
segregation appears not to occur there remains the possibility
of functional diﬀerentiation between ericoid and
cluster-root systems. As far as is known the main function
of cluster roots is to enhance the capture of available
phosphate ions (Malajczuk and Bowen, 1974), although
they and their associated bacteria may also be involved in
the mobilization of these ions. If this is the case while
proteoid roots will scavenge for nutrients, including N, in
mineral form, ericoid roots in the same substrate should
have the potential to exploit organic nitrogen residues.
Evidence to support functional segregation comes from the
study of Stewart et al. (1993) who observed suﬃcient nitrate
reducing ability (NRA) in shoots and roots of three
proteaceous genera (Banksia, Petrophile and Stirlingia) to
suggest that they would assimilate nitrate in nature. In
contrast the two epacrid species Astroloma macrocalyx and
Conostephium pendulum showed barely detectable NRA
even after feeding of nitrate via the transpiration stream.
Other plant families with widespread representation in
epacridaceous heaths but which are absent or of little
importance in the northern hemisphere are Rutaceae,
Dilleniaceae and Compositae, most members of which
would be expected to be colonized by VA fungi. This type
of mycorrhiza has been reported, for example, in Boronia
(Rutaceae), Hibbertia (Dilleniaceae) and Helichrysum
(Compositae) (Lamont, 1984). It appears that the less
ﬁbrous root system of plants such as these penetrate soil
more deeply being of Types I and 4 (Dodd et al., 1984) or
Type R3 (Pate, 1994) a feature providing spatial separation
from epacrids. In addition, while VA colonization will
enhance their ability to scavenge for P, members of two of
these genera Helichrysum and Hibbertia have been shown to
develop signiﬁcant NRA (Stewart et al., 1993), again
suggesting the likelihood of nutritional as well as spatial
niche diﬀerentiation between these plants and those with
ericoid mycorrhiza.
Recognition of these patterns leads to the suggestion that
selection favouring a range of specialisms has been
important in enabling the co-existence of taxonomically
distinct species in Australian heathland systems, where the
greatest diversity is found on the least fertile soils (Pate and
Hopper, 1993). This situation contradicts Tilman’s equilibrium
model of plant competition (Tilman, 1982, 1988)
which predicts that in resource poor environments diversity
will be low because few species can survive such impoverishments.
Rather, it suggests that over very long periods,
evolutionary selection of distinctive mutualisms has facilitated
co-existence of species in diverse assemblages. It is a
measure of the success of the ericoid mycorrhizal mutualism
within this range of specialisms that it is uniformly present
across all the families which ecologists such as Specht (1979;
Specht and Rundel, 1990) have recognized as being most
characteristic of impoverished heathland ecosystems.
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