ECOSYSTEMS
Ecosystems (2002) 5: 11–22
DOI: 10.1007/s10021-001-0052-x
© 2002 Springer-Verlag
ORIGINAL ARTICLES
Increasing Feldspar Tunneling by
Fungi across a North Sweden
Podzol Chronosequence
Ellis Hoffland,1* Reiner Giesler,2 Toine Jongmans,1 and
Nico van Breemen1
1
Laboratory of Soil Science and Geology, Wageningen University, P.O. Box 37, 6700 AA Wageningen, The Netherlands; and
2
Department of Forest Ecology, Swedish University of Agricultural Science, 901 83 Umeå, Sweden
ABSTRACT
Tunnels in feldspar grains, assumed to be created by
fungal hyphae, were first discovered in a boreal
podzol. In this paper, we further describe the phenomenon of mineral tunneling by determining the
rate of feldspar tunneling across a north Sweden
podzol chronosequence. The chronosequence is a
result of ongoing land uplift, which started after the
retreat of glaciers about 9000 years ago. The sequence comprises a series of soils that began developing on glacial tills 190 –7800 years ago. Feldspar
tunneling was concentrated in the uppermost 2 cm
of the E horizon, and its frequency increased significantly with soil age. Although no tunnels were
found in feldspar grains from the youngest soil (190
years), they were seen more frequently in soils aged
2000 years and older. This lag phase in tunnel formation of about 2000 years coincided with the disappearance of the easily weatherable potassium-(K)
and calcium (Ca)-containing minerals biotite and
hornblende and with the appearance of etch pits on
feldspar grains. In the oldest soil (7800 y), about
25% of the feldspar grains in the upper 2 cm of the
E horizon were tunneled. Within site variation in
tunnel frequency was high, and we were able to
exclude spatial variations in mineralogy and texture
as a possible explanation. The shape of the tunnels,
their depth distribution, and the fungal hyphae
found inside them all offer support for the previous
assumption that their formation is mediated by biological activity involving fungi. The results of this
investigation also indicate that the bioavailability of
Ca and K may be a factor in tunnel formation.
INTRODUCTION
and others 1998, 1994). The chemical weathering
of feldspars (via water and its solutes) is accelerated
by low pH and the presence of cation-complexing
agents such as organic anions (Blum and Stillings
1995). Weathering on grains is usually initiated at
points of excess surface energy, such as cracks, corners, holes, and dislocations, and results in crystalographically controlled, square-shaped (cross section) and lens-shaped (longitudinal) etch pits
(Berner and Holdren 1979; Lee and others 1998).
These etch pits may eventually coalesce to form
sawtooth cavities.
Key words: weathering; feldspar; chronosequence; chronofunction; podzol; ectomycorrhiza;
hornblende; Sweden; Ca and K biogeochemistry;
micromorphology.
Feldspar minerals are the primary source of biologically available calcium (Ca) and potassium (K) in
most ecosystems. The weathering of feldspars
therefore contributes significantly to soil fertility
and is responsible for a major influx of Ca and K
into the element cycles of most ecosystems (Likens
Received 12 March 2001; accepted 9 July 2001.
*Corresponding author’s present address: Sub-department of Soil Quality,
Wageningen University, P.O. Box 8005, 6700 EC Wageningen, The Netherlands; e-mail: [email protected]
11
12
E. Hoffland and others
Biological activity can accelerate the weathering
of feldspars (Barker and others 1997). Research into
the biologically mediated weathering of feldspars
has focused on bacteria (Barker and others 1998),
lichens (Banfield and others 1999), and ectomycorrhiza (Jongmans and others 1997; Landeweert and
others 2001). Bacteria have been shown to colonize
open cleavages, within which they can enhance
weathering by the excretion of gluconic acid
(Welch and Ullman 1999). Hyphae of lichenous
fungi are thought to colonize intragranular pores
along these cleavages, where they may enhance the
formation of etch pits via the exudation of oxalate
(Lee and Parsons 1999).
Jongmans and others (1997) were the first to
describe tunnellike features inside feldspar and
hornblende grains. Their smooth sides, constant diameter (3–10 ␮m), and rounded ends distinguished
these tunnels from (coalesced) etch pits and cracks.
Some of the tunnels were colonized by fungal hyphae with similar diameters, which led to the hypothesis that the tunnels had been formed by ectomycorrhizal hyphae that dissolved the mineral via
the exudation of organic anions and protons (Jongmans and others 1997; Landeweert and others
2001). The tunnels were typically found in grains
from podzol E horizons of Fennoscandian boreal
forest soils (Van Breemen and others 2000b) and
were believed to offer the ectomycorrhizal tree a
unique source of basic cation nutrients via the external hyphae (Landeweert and others 2001; Van
Breemen and others 2000a).
To further elucidate this phenomenon, we studied mineral tunneling in a north Sweden podzol
chronosequence. Soil chronosequences have
proved to be valuable tools for the investigation of
slow processes (Huggett 1998), and the tunneling of
minerals is thought to be a slow process (Jongmans
and others 1997). The north Sweden chronosequence was formed through glacial rebound after
the Pleistocene ice sheet melted. The land rose from
the sea at a maximum rate of more than 50 mm y⫺1
(Renberg and Segerström 1981) and is still rising at
a rate of about 9 mm y⫺1, resulting in a series of
soils whose ages range from 0 to about 9000 years
old. Nyänget, one of the first sites where these
tunnels were found (Ilvesniemi and others 2000;
Van Breemen and others 2000b), is located near
this chronosequence. The bedrock (granite and
veined gneiss), which is poor in nutrients, and the
boreal climate and vegetation have favored podzolization in the tills throughout most of the chronosequence.
If, as hypothesized previously, mineral tunneling
is caused by ectomycorrhizal activity, it is likely that
the tunnels occur specifically in the upper part of
the mineral soil, since most ectomycorrhizal roots
are found in the organic horizon (Goodman and
Trofymow 1998). The aim of this study was to
provide a further description and explanation for
the newly discovered phenomenon of mineral tunneling and to explore its ecological significance. The
specific questions that it addressed were as follows:
(a) How does the percentage of tunneled minerals
increase with time? (b) How are tunneled minerals
distributed within a soil profile? and (c) What are
the ecosystem properties that affect mineral tunneling?
STUDY SITES
The Soil Chronosequence
Seven sites were selected in the vicinity of Umeå
(63°50⬘N, 20°17⬘E) in the Västerbotten province in
northern Sweden (Figure 1). The sites represent
different ages in a chronosequence that developed
as a result of land upheaval. The selected soils are
formed in sandy, gravely glacial till deposits. Drainage ranges from somewhat excessively drained to
moderately well drained (FAO 1990).
The age of the different sites was estimated using
the current elevation of the sites and a shoreline
displacement curve for southern Västerbotten based
on Renberg and Segerström (1981). Isostatic rebound of the crust since the melting of the Weichselian ice sheet is responsible for ongoing land uplift
at the current rate of about 9 mm y⫺1 in the coastal
areas of Västerbotten. The deglaciation started
about 8900 years ago and took about 250 years
(Bergström 1968). All of our sites are located below
the highest shoreline, at 260 –275 m above sea
level. We estimated site elevations using survey
marks with known elevations within 3 km from
each site. The elevation at the sites was determined
from the measured difference between the survey
mark and the site using a level (Leica NA820; Leica
AG, Heerbrugg, Switzerland). The exceptions were
the Bådelögern site, where the elevation was measured from the sea level, and the Baggöberget site,
where the elevation was estimated from a topographic map. The uncertainty in the age determinations of the data points of the displacement curve
of Renberg and Segerström (1981) was less than ⫾
200 years (70 –190 years). This corresponds to an
elevation of ⫾ 2 m using the current land uplift. In
all cases, the precision of the elevation estimates is
less than 1 m. Ages of parent material thus estimated ranged from 190 to 7800 years (Table 1).
The mean annual air temperature is 2.7°C, and
Feldspar Tunneling across a Chronosequence
13
Figure 1. The seven chronosequence sites around
Umeå in north Sweden. For
names of the sites corresponding to the numbers,
see Table 1.
Table 1. Estimates of Soil Age at the Seven
Study Sites
Site Name
Site
no.a
Elevation
(m)
Estimated
Soil Age
(y)
Bådelögern
Baggöberget
Oxtjärnsdiket
Bäcksjön Sör
Lappberget
Sör Grundbäck
Åkerbäck
1
2
3
4
5
6
7
1.7
11.0
24.6
44.8
67.5
95.5
126.6
190
1200
2700
4200
5600
6800
7800
a
See Figure 1.
annual precipitation is 662 mm (Alexandersson and
others 1991), of which about 40% occurs as snow.
Norway spruce (Picea abies) dominates the forested sites, with Scots pine (Pinus sylvestris) as an
associated species. Stand age was more than 70
years at all sites. The field layer consists mainly of
dwarf scrubs, Vaccinium myrtillus and V. vitis-idaea.
Mosses (Pleurozium schreberi and Hylocomium splendens) dominate the bottom layer.
Profile Descriptions
Freshly dug pits on flat to gentle sloping (less than
5%) positions, and FAO terminology (FAO 1990)
were used to describe the soil profiles.
The soil at Bådelögern (190 y) had an O horizon
of 11 cm, overlying a discontinuous 0 –2-cm-thick E
horizon. No Bs horizon was observed. The color of
the underlying C horizon was 10YR 7/4. Many
fresh stones and boulders were present. Roots were
concentrated in the upper 30 cm. The soil was
classified as a Typic Cryopsamment (Soil Survey
Staff 1998).
Soils aged 1200 y and older showed the characteristic podzol horizon development with depth (O,
E, and Bs horizons) and are classified as Typic Haplocryods (Soil Survey Staff 1998). The thickness of
the O horizon ranged from 4 to 10 cm. The E
horizon at Baggöberget (1200 y) was 2–5 cm thick.
In older soils, E horizons were generally thicker
(2–14 cm) but did not increase further with age.
The color of the E horizons was 10YR 8/1. The
thickness of the Bs horizon increased with soil age
from 22 cm at Baggöberget (1200 years old) to 51
cm at Åkerbäck (7800 years old). The color of the
Bs at Baggöberget (1200 years old) was 5YR 3/3.
The older soils had redder Bs horizons (2.5 YR 4/6
to 2.5 YR 3/4), with no age trend within this group.
The C horizons showed gray colors (10YR 5/1–2.5Y
6/2).
Mineralogy
Mineralogical composition was analyzed by x-ray
diffraction. Guinier exposures were made from
samples ground to a powder and mixed with glycerol (Van Doesburg 1996). No major differences
were found among the samples with respect to
mineralogy. All soil samples (from the E and C
horizons of all sites) contained mainly quartz and
about 20%–30% feldspars. Among the feldspars,
the majority were plagioclase feldspars, most likely
a Ca-rich oligoclase ((NaAlSi3O8)90(CaAl2Si2O8)10).
This was confirmed by the Becke test on plagioclase
feldspars with twins in thin sections: The indexes of
refraction of these plagioclase feldspars were lower
14
E. Hoffland and others
Table 2. Grain Size Distribution (vol. %) in C and E Horizons Classified according to FAO (1990)
C
Textural
Class (␮m)
Bädelögern
190 y
Baggöberget
1200y
Oxtsjärndiket
2700 y
Bäcksjön
Sör
4200 y
Lappberget
5600 y
Sör
Grundbäck
6800 y
Åkerbäck
7800 y
⬍2
2–20
20–63
63–125
125–200
200–630
630–1250
1250–2000
1
2
7
8
7
46
20
10
0
2
5
4
3
26
37
22
4
17
15
10
8
20
18
9
2
11
16
12
8
19
19
13
3
19
19
12
7
18
14
7
4
17
31
24
13
9
2
0
2
11
14
9
6
14
22
22
than the index of refraction of the resin (1.535).
This indicates that the mole % of anorthite is 10%
at most. The minority of the feldspars were alkali
feldspars. The Guinier diffraction pattern due to
alkali feldspars was most similar to that of pure
microcline (KAlSi3O8). Lines from micas and amphiboles (including hornblendes) were visible in
the Guinier exposures, but their concentrations
were estimated to be low.
In addition, two to four replicate subsamples
from cores taken from the uppermost 2 cm of the E
horizons from Lappberget (5600 years old), Sör
Grundbäck (6800 years old), and Åkerbäck (7800
years old) were analyzed to assess the spatial variation within sites. Guinier exposures showed no
differences among replicate samples from sites, indicating little within-site spatial variation in mineralogy.
Texture
Grain-size distributions in the range of 0.04 –2000
␮m were determined with a Coulter LS230 grain
sizer (Pape 1996). Bulk samples were homogenized
and sieved (2000 ␮m). Subsamples (less than 2000
␮m) were prepared by treatment with peroxide to
remove organic matter and sonication. Subsamples
of the same samples taken for determination of
mineralogical composition were used to determine
grain-size distribution (Table 2).
C horizons at all sites were low in clay (0%– 4%).
Six of the seven sites had a high (59%–93%) sand
content. C material from Sör Grundbäck (6800
years old) had a finer texture, with more silt (48%)
and less sand (48%). E horizon material from all
sites, including Sör Grundbäck, was very similar,
with little clay (1%–2%) and a high percentage
(78%–90%) of sand.
To check for within-site variation in texture,
small (⫾ 6 g) subsamples of samples taken with an
auger (2.5-cm diameter) from the uppermost 2 cm
of the E horizon of Lappberget, Sör Grundbäck, and
Åkerbäck were analyzed by subsequent sieving and
weighing. The duplicate samples from Lappberget
were very similar (Table 3). Replicates from the Sör
Grundbäck and Åkerbäck sites had somewhat different textures.
METHODS
Micromorphology
To study the micromorphology of the soil profiles,
undisturbed samples (7.5 ⫻ 7.5 ⫻ 2.9 cm) were
taken from pit walls and placed in cardboard boxes.
One series of samples was taken per site, from the O
horizon down into the C horizon.
For analyses of tunnel frequency throughout the
chronosequence, five disturbed replicate samples
per site were taken from the uppermost 2 cm of the
E horizon with an auger (diameter, 2.5 cm).
All samples were impregnated with polyester
resin (Synolyte 544-A-4). Thin sections (7.5 ⫻ 7.5
cm from undisturbed samples and 1.4 ⫻ 1.4 cm
from disturbed samples) were prepared according
to FitzPatrick (1970) and examined with a petrographic light microscope (Zeiss Axioskop) in crosspolarized and brightfield light at magnifications up
to ⫻ 400.
Undisturbed thin sections were described according to Bullock and others (1985). Different
types of minerals were identified optically in sofar
as possible. However, because of the relatively
high sodium (Na) content of the plagioclase
feldspars, it was not possible to distinguish between alkali and plagioclase feldspar grains with-
Feldspar Tunneling across a Chronosequence
15
Table 2. (Continued)
E
Baggöberget
1200 y
Oxtsjärndiket
2700 y
Bäcksjön
Sör
4200 y
Lappberget
5600 y
Sör
Grundbäck
6800 y
Åkerbäck
7800 y
1
3
6
5
4
43
25
13
2
5
6
6
11
38
20
12
1
6
10
8
5
20
27
22
2
8
10
8
5
20
27
22
1
7
9
7
4
10
32
30
2
9
11
8
7
30
18
15
out twinning patterns. Special attention was
given to alterations across the chronosequence,
including weathering phenomena such as tunneling, etch pit formation, and shifts in mineralogical
constitution.
Rough grain surfaces were studied with a scanning electron microscope (Philips, Eindhoven, The
Netherlands). Chemical mineralogy was determined by EDXRA.
Tunnel Frequency
For analyses of the distribution of tunnels by depth,
an imaginary grid was drawn on the thin section
from an undisturbed soil sample from Sör Grundbäck (6800 years old) with lines 2 mm apart. Fields
of view at each crossing were analyzed. The total
number of grains of a certain type of mineral was
counted in each field of view, as well as the number
of the grains containing tunnels. The magnification
used was ⫻100.
To analyze the frequency of tunnels in minerals
across the chronosequence, thin sections from
disturbed soil samples were examined. In each
field of view, the total number of grains was
counted, as well as the number of grains containing tunnels. For feldspars, a total of at least 200
grains were counted per replicate. Generally,
about 20 fields of view were sufficient to observe
200 feldspar grains. Five replicates were used per
site.
Only grains with a diameter between about 50
and 500 ␮m were taken into account when determining tunnel frequency. Grains measuring less
than 50 ␮m were too small to allow the detection of
tunnels; grains larger than 500 ␮m were usually
rock fragments consisting of different mineral components.
RESULTS
Chemical Weathering and Soil Formation
The micromorphological observations of site mineralogical composition and variation confirmed the
x-ray analysis. The presence or absence of biotite in
the upper mineral soil varied according to soil age.
At Bådelögern (190 years old), no alteration features were observed in the mineral grains and rock
fragments, except for iron staining of a few biotite
grains. At Baggöberget (1200 years old), biotite was
absent in the first cm of the E horizon. At Oxtjärnsdiket (2700 years old), biotite was absent in the
upper E horizon. In all soils aged 4200 years or
older, biotite was absent in the whole E horizon.
Biotite grains occurred immediately below the E
horizon and were frequently present in the Bs horizon; some were fresh and others were partially
stained by iron.
The degree of weathering of feldspars and hornblendes increased with soil age. In the younger soils
(1200 and 2700 years old), hornblende grains in the
upper cm of the E horizon showed sawtooth patterns at the outer surface due to the formation of
etch pits. In the older soils, feldspars and hornblende showed clear etch pit formation (Figure 2A,
B) and pellicular, parallel linear and dotted alteration (Delvigne 1999). In the Bs horizon, feldspars
and hornblendes lacked alteration. The Bs horizon
was stained by homogeneously distributed, dominantly isotropic iron oxides in the fine groundmass.
Although the E horizon does not deepen with soil
age, it was clear that the degree of weathering of
biotite, hornblende, and feldspars in this horizon
does increase with soil age. This continued weathering in the older E horizons caused an increased
thickness of the Bs horizon with soil age as a result
of increased iron accumulation.
16
E. Hoffland and others
Table 3. Within-Site Variation in Grain Size Distribution (Weight %) in the Uppermost 2 cm of the
E Horizon
Lappberget
(5600 y)
Mesh size
(␮m)
⬍63
63–150
150–300
300–600
600–2000
⬎2000
Sör Grundbäck (6800 y)
Åkerbäck (7800 y)
Tunnel Frequency (%)
2
5
26
4
17
13
32
19
31
11
15
17
22
29
6
17
15
16
20
26
5
14
28
17
12
25
4
9
17
22
18
31
4
3
6
8
14
67
1
10
14
11
13
38
14
3
8
60
27
1
0
10
9
11
12
38
19
2
10
50
30
7
1
Tunnel frequency as given in Figure 4
Tunnel Formation: Qualitative Aspects
Tunnels that had smooth and parallel-oriented
walls, constant diameters (3–10 ␮m), and rounded
ends were readily distinguishable from other
weathering phenomena inside the mineral grains
(Figure 2A–D). Tunnels were found exclusively in
feldspar and hornblende grains.
Tunnels in hornblendes started to occur in the E
horizon of the 2700-year-old soil. Tunneled
feldspars were scarce in this soil, but they were
regularly seen in soils older than 2700 years. Some
tunnels were partially filled with fungal hyphae.
The onset of tunnel formation was frequently observed on mineral edges where etch pits had
formed (Figure 2E, F). The presence of fungal hyphae (Figure 2G, H) inside tunnels and hyphae
penetrating feldspar grains (Figure 3) strongly implicated fungi in the tunneling phenomenon.
It was impossible to classify the majority of
feldspars as alkali or plagioclase feldspars. However,
a portion of the alkali feldspars were aligned such
that the tarting twins pattern characteristic of microcline was visible. Tunnels were rarely seen in
such grains, indicating that either microclines are
resistant to tunneling or that tunnels in microclines
are oriented such that they are invisible when the
tarting twins are visible.
There were other indications that the orientation
of tunnels within a mineral is not random. Frequently, several tunnels would be observed in one
mineral (Figure 2C, D), whereas there would be no
tunnels at all in a similar mineral from the same
site. This indicates that the tunnels are aligned in
planes along the crystallographic cleavage or twinning plane of a mineral (the zones of weakness).
In the 2700 –5600-year-old soils, the tunnels
were mainly present in the upper 2 mm of the E
horizon. In the older soils, tunneled minerals were
concentrated in the upper E horizon, but they were
also observed deeper in the E horizon. Especially in
the older soils (more than 5600 years), the tunnels
increased in diameter and their shape became more
irregular. The length of the tunnels in feldspar
grains increased with soil age, indicating a heavier
colonization of fungi.
Tunneling within a Soil Profile
Thin sections from Sör Grundbäck (6800 years old)
showed the highest tunnel frequency, expressed as
the percentage of feldspars containing tunnels, in
the uppermost centimeters of the E horizon (Figure
4). The percentage of grains containing tunnels decreased rapidly with depth. Very few minerals with
tunnels were found in the B horizon.
Tunnel Frequency across
the Chronosequence
The percentage of feldspar grains with tunnels increased with age from 0% in the two youngest sites
to about 25% in the 7800-year-old site (Figure 5).
Tunneled grains were almost exclusively feldspars
(more than 99%). The relationship between soil
age and mineral tunneling could best be described
by an exponential increase. After 10log transformation, the relationship between soil age and mineral
tunneling was highly significant (P ⬍ 0.001). Soil
age statistically explained 85% of the variance in
mineral tunneling.
All samples contained less than 1% hornblende,
of which an average of about 50% was tunneled
throughout the chronosequence. The total number
of hornblende grains detected (34 in total for all 35
Feldspar Tunneling across a Chronosequence
17
Figure 2. Thin-section micrographs in cross-polarized (A–G) and plain (H) visible light of plagioclase feldspars from
Åkerbäck (7800 y). A and B: Parallel-oriented, lens-shaped etch pits in a row, resulting in a sawtooth pattern. B also shows
a single etch pit (upper left corner). C and D: Typical nonparallel pattern of feldspar tunneling. Tunnels show a constant
diameter and a rounded end. E and F: Tunnel (t) formation at a mineral surface where etch pits (e) had been formed. G
and H: Detail of a tunnel colonized by a fungal hypha. The septae of the hypha are clearly visible (H).
samples analyzed) was too small to indicate any
trend of tunnel frequency with soil age.
Textural differences could not explain the variation in mineral tunneling. A stepwise multiple regression analysis was applied, using the soil age and
the percentage of grains smaller than 63 ␮m (Table
3) as independent variables and 10log of the per-
centage of tunneled feldspars as a dependent variable. The set of samples presented in Table 3 (n ⫽ 9)
was chosen because subsamples from the same core
from the uppermost 2 cm from the E horizon were
used to determine grain size distribution and another was used to determine mineral tunneling.
Also, for this subset of samples, there was a signif-
18
E. Hoffland and others
Figure 3. Scanning electon micrograph showing two
fungal hyphae penetrating a feldspar grain.
Figure 4. Percentage of tunneled feldspar grains as related to depth of mineral soil in Sör Grundbäck (6800 y).
For each data point, 13 fields of view from a thin section
(magnification ⫻100) were analyzed.
icant relationship between soil age and mineral
tunneling (P ⫽ 0.03), but there was no statistically
significant improvement of this relationship when
the percentage of grains smaller than 63 ␮m was
taken into account (P ⫽ 0.78).
Taking the thickness of the E horizon into account did not improve the relationship between soil
age and mineral tunneling either. Thickness was
recorded for each core taken for the analysis of
tunnel frequency. It varied strongly within each
site. The largest variation was found at Bäcksjön Sör
(4200 years old), where the thickness varied from 6
to 13 cm; the smallest variation was found at Lappberget (5600 years old), with a minimum thickness
of 2 cm and a maximum of 5 cm. To determine
whether the thickness of the E horizon was related
to mineral tunneling in its uppermost 2 cm, multiple regression analysis was performed with soil age
and thickness of the E horizon as independent variables and 10log of the percentage of tunneled
Figure 5. Percentage of feldspar grains with tunnels in
the first 2 cm of the E horizon. For each data point, 200
feldspar grains were considered. Five replicates per site
were used. Some data points may be obscured by the
overlap of markers. The solid line represents a fit (exponential increase) to all data (Y ⫽ 0.87 ⫻ 10(0.000188X)–1).
The dashed line represents a fit (exponential sigmoid) to
the maximum values only for each site (Y ⫽ 41/(1 ⫹
e⫺(X-5874)/1585). r2 represents the percentage of variation
statistically explained by soil age; n represents the number of observations considered; P ⬍ 0.0001 in both cases.
feldspars as a dependent variable. Using the thickness of the E horizon as an extra independent variable did not significantly improve the relationship
between soil age and mineral tunneling (P ⫽ 0.20).
DISCUSSION
This study clearly showed that mineral tunneling
(a) is concentrated in the upper mineral soil and (b)
increases with soil age.
The concentration of mineral tunnels in the uppermost centimeter of the mineral soil is in line
with our previous hypothesis that tunnel formation
is mediated by biological activity involving saprotrophic or mycorrhizal hypae. This vertical distribution pattern (Figure 4) has been observed in podzols
from all over the world (E. Hoffland unpublished).
The presence of hyphae in the tunnels (Figure 2G,
H) (Jongmans and others 1997) and hyphae penetrating feldspar grains (Figure 3) (Van Breemen and
others 2000a) also suggests that hyphal activity is
involved in the formation of mineral tunnels.
Our results do not allow us to determine whether
saprotrophic or ectomycorrhizal hyphae are responsible for feldspar tunneling. Both types of fungi
are known to exude organic anions (Ahonen Jonnarth and others 2000; Allen and others 1996;
Cumming and others 2001; Dutton and Evans
Feldspar Tunneling across a Chronosequence
1996; Gadd 1999). Ectomycorrhizal hyphae are the
more likely candidates, since ectomycorrhizal roots
are concentrated in the O horizon (Goodman and
Trofymow 1998) and ectomycorrhizal hyphal densities in the mineral soil would thus be expected to
be highest in the upper few centimeters. This would
coincide with the vertical distribution pattern of
tunneled feldspars (Figure 4). The total active fungal biomass (presumably mainly saprotrophs) in the
B horizon is smaller than that in the E horizon
(Bååth and Söderström 1982; Söderström 1979) but
still considerable, although tunneled minerals are
rare at this level (Figure 4).
The statistical relationship between soil age and
mineral tunnel formation suggested an exponential
increase in the tunneling frequency of feldspar
grains (Figure 5). The percentage of variance statistically explained by soil age is so high (85% after log
transformation) that it does not leave much room
for factors other than time to be involved.
Estimates of Mineral Tunneling
Due to the scoring method, the reported percentage
of tunneled grains is most likely an underestimate.
With this method, tunnels can only be recognized
as such when a longitudinal section longer than
about 10 ␮m is made through a tunnel. Other tunnels cannot be distinguished because the thickness
of the thin section (⫾ 30 ␮m) results in a small
depth of field at the required magnification (at
least ⫻ 100).
The fact that the tunnels occur along cleavage
and twinning planes (Figure 2C, D) suggests that
the crystallographic structure of a feldspar influences the tunnel’s orientation (Van Breemen and
others 2000a). Because of their crystallographically
determined orientation, only a limited number of
tunnels would be visible in a thin section, since
their visibility would depend on the planar alignment of the mineral in the sample.
Spatial Variation
The most likely explanation for the spatial variation
seen with mineral tunneling is the mechanical disturbance of the mineral soil. For instance,
windthrows are a natural feature that leads to the
uprooting of trees, which can then redistribute the
mineral soil (Jonsson and Dynesius 1993). These
and other disturbances (such as erosion and animal
activity) could create patches where fresh, nontunneled mineral soil is mixed with the uppermost
layer. This admixture would drastically reduce tunnel frequency, since the majority of tunneled feldspar grains are found in the uppermost mineral soil
19
(Figure 4). Selecting the maximum value of the
percentage of tunneled feldspars from the five replicates for each site (Figure 5) would reduce bias
caused by disturbance.
The thickness of the E horizon may be regarded
as a measure of the disturbances that have occurred
over the preceding centuries. The absence of any
significant relationship between the thickness of
the E horizon and the percentage of tunneled minerals is probably due to the fact that E horizons of
considerable thickness can develop within 400
years after windthrows (Bormann and others
1995). Because tunnel formation is a much slower
process, restoration of the minerals being tunneled
to the original level would require much longer, or
would never occur at all.
Texural differences may affect tunnel formation.
However, the absence of any statistically significant
relationship between the percentage of grains less
than 63 ␮m and tunneling may indicate that either
soil texture at such a small scale is not a suitable
parameter to quantify nutrient availability or that
mineral tunneling is not triggered by nutrient deficiency. As a confounding factor, a greater abundance of smaller grains could be caused by a higher
frequency of tunnels, which would cause the grains
to break up into particles so small that tunnels
would be impossible to distinguish. Fine texture
could thus be a consequence of more tunneling
rather than a cause of less tunneling activity.
Soil Age and Tunneling
Theoretically, a sigmoid curve would be the most
obvious way to describe the relationship between
soil age and the percentage of feldspars containing
tunnels. The plateau would be at 100%, unless part
of the feldspars were either resistant to tunneling or
invisibly tunneled.
If the maximum value of the percentage of
feldspars containing tunnels found among the five
replicates for each site is related to soil age, the
sigmoid curve is indeed the best fit. This sigmoid
relationship is highly significant (r2 ⫽ 0.997, P ⫽
7 ⫻ 10⫺7, n ⫽ 7). This fit results in a maximum rate
of mineral tunneling in soils aged between ⫾ 4000
years and 7000 years and a plateau of 41% (Figure 5).
We cannot exclude the possibility that microclines (alkali feldspars) are resistant to tunneling.
However, we consider it more likely that not all of
the tunnels are visible, because they are aligned
according to the crystallographic pattern of a mineral. A plateau at ⫾ 40% instead of 100% could
therefore suggest that 60% of the feldspars are
20
E. Hoffland and others
aligned in such a way that the tunnels are not
visible.
Lag Phase
There are at least three processes that could explain
the lag phase in the relationship between soil age
and mineral tunneling (Figure 5): (a) an absence of
ectomycorrhizas in the younger sites, (b) the time
of etch pit formation, and (c) a decreased availability of K and Ca due to losses of easily weatherable
minerals.
Early successional vegetation along the land-rising coast is dominated by vesicular–arbuscular mycorrhizal plant species (Ericson and Wallentinus
1979). However, within about 50 years, ectomycorrhizal species appear (for instance, Betula and Picea)
(Svensson and Jeglum 2000); and after about 200 –
300 years, ectomycorrhizal and ericoid mycorrhizal
species dominate. As soon as ectomycorrhizal plant
species appear, they can be colonized, although the
fungal species that form the symbiosis can change
(Helm and others 1996). Depending on which fungal species is responsible for mineral tunneling, tunneling activity can then be expected to begin. Thus,
the absence of ectomycorrhizas would explain a lag
phase of a few 100 years only.
Frequent observations similar to those depicted
in Figure 2E, F suggest that tunneling specifically
begins at feldspar surfaces where microscopically
visible etch pits were formed previously. Etch pit
formation occurs in soils aged 4200 years and older
and tunneling increases rapidly with age thereafter
(Figure 5). Etch pits may catalyze the tunneling
process by physically restraining the diffusion and
mass flow of the organic anions that have been
exuded by fungal hyphae into the bulk soil solution. If the concentration of mineral-dissolving organic anions on the mineral surface is prolonged, it
could facilitate tunneling. The lag phase would then
coincide with the period required for etch pit formation.
Alternatively, or additionally, the lag time could
have been caused by the presence of easily weatherable biotite and hornblende, which—like
feldspars,— contain K and Ca, respectively. Easily
weatherable biotite and hornblende are more abundant in younger soils (less than 4200 years old);
therefore, the bioavailability of K and Ca is probably
higher. Their presence could reduce the exudation
of organic anions by ectomycorrhizal hyphae in the
younger soils (Paris and others 1995, 1996), resulting in lower tunneling activity in these soils. Thinsection analysis demonstrated that the appearance
of mineral tunnels coincides with the disappearance
of biotite from the upper E horizon (Oxtjärnsdiket,
2700 years old), which is in line with the higher
bioavailability of at least K during the first few
thousand years of soil development.
Evaluation of the Chronosequence
The Swedish suite of soils has not been described
before as a chronosequence, so careful evaluation is
necessary. To be able to study the rate of mineral
tunneling, no soil-forming factor other than time
should vary across the selected series of soils (Jenny
1941). No differences among the entire set of samples were found with respect to the mineralogical
composition of the parent material. However, we
did find some differences in texture. C material
from Sör Grundbäck (6800 years old) had a higher
silt content than the other sites (Table 1). However,
the texture of E samples was very similar throughout the chronosequence. The E horizon of Sör
Grundbäck has probably been formed in material
with a texture different from what is now the C
horizon. Because we are studying tunnel formation
in the E horizon, all sites therefore meet the criterion of homogeneity of parent material.
Two other relevant soil-forming factors that
should be constant are climate (moisture and temperature) and vegetation. There is a gradient in
temperature and rainfall from the young sites near
the coast toward the older inland sites. Moreover,
climate has not been constant throughout the last
8000 years. The first 3000 years after deglaciation
were warmer than the last 5000 years. Pollen analysis from the investigated region showed that Alnus,
Betula, and Pinus were the major forest trees during
climatic optimum and that Picea abies expanded rapidly between 1400 and 1000 BC, establishing a
predominantly coniferous forest.
Because very little is known about factors affecting mineral tunneling, it is difficult to speculate
about the effect of these imperfections of the podzol
chronosequence on the chronofunction describing
mineral tunneling. For example, the fact that the
older soils (more than 5000 years old) have experienced a warmer period, presumably with increased mycorrhizal activity, may lead to an, overestimatation of the rate of mineral tunneling in
these sites.
CONCLUSIONS
The north Sweden podzol chronosequence on glacial tills can, despite some shortcomings, be considered a useful series of soils for the study of slow
soil-forming processes such as mineral tunneling.
Mineral tunneling increased significantly over
Feldspar Tunneling across a Chronosequence
time, starting at 0 in the younger soils. This progression indicates that mineral tunneling is caused
by some factor that only comes into play after the
emergence of the soils from below sea level. The
concentration of tunneled feldspars within the upper centimetres of the mineral soil and the presence
of hyphae inside the tunnels strongly suggest that
the tunneling is related to biological activity involving fungi.
The chronofunction describing mineral tunneling
shows a lag phase. This may indicate that the prior
formation of etch pits facilitates tunneling. Tunneling may also be driven by the bioavailability of Ca
and K. The lag phase is longer than would be expected after the appearance of ectomycorrhizas in
the chronosequence, but it coincides with the appearance of etch pits in feldspars and the disappearance, or strong weathering, of K- and Ca-containing minerals (biotite and hornblende, respectively)
in the upper mineral soil.
Further research is needed to quantify the contribution of mineral tunneling to weathering of the
soil profile and to ecosystem influx of Ca and K.
Given the fact that at least 25% of the feldspar
grains are tunneled after 7800 years of soil formation, mineral tunneling probably plays a significant
ecological role. The sigmoid curve is the most obvious fit to the chronofunction describing mineral
tunneling. This fit implies that mineral tunneling
contributes maximally to the ecosystem influx of Ca
and K in north Sweden soils aged between 4000
and 7000 years.
ACKNOWLEDGMENTS
We are grateful to Jan van Doesburg and Arie van
Dijk for technical assistance, to Prof. Dr. Leendert
van der Plas for expert advice on matters related to
optical mineralogy, and to Karin de Boer and Renske Landeweert for help during the field work. E.H.
received financial support from the Netherlands Organization for Scientific Research (NWO). R.G. was
supported by the Carl Trygger Foundation and the
Swedish Research Council for Forestry and Agriculture (SJFR).
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