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Long-term records of strontium isotopic composition in
tree rings suggest changes in forest calcium sources in the
early 20th century
THOMAS DROUET
*
, JACQUES HERBAUTS
*
and D A N I E L D E M A I F F E w
*
Laboratoire de Ge
´ne
´tique et d’Ecologie Ve
´ge
´tales, Universite
´Libre de Bruxelles, 1850 chausse
´e de Wavre, B-1160 Bruxelles,
Belgium, wLaboratoire de Ge
´ochimie Isotopique, Universite
´Libre de Bruxelles, CP 160/02, 50 av. F.D. Roosevelt,
B-1050 Bruxelles, Belgium
Abstract
Many studies made in Europe and North America have shown an increasing depletion of
exchangeable base cations that may cause tree nutritional deficiencies in sensitive soils.
We use radial variation of strontium isotope in tree-rings (
87
Sr/
86
Sr ratio) to monitor
possible changes in Ca sources for tree nutrition (Sr is used as an analog to Ca). The two
main sources of Ca in forest stands are mineral weathering release and atmospheric
inputs. Measurements in several forest stands in temperate regions show a steep
decrease from pith to outer wood of the Sr isotope ratio from 1870 to 1920 except for
stands developed on soils with a higher Ca status. This suggests a decrease of the
weathering contribution (high
87
Sr/
86
Sr ratio) when cations are displaced from the soil
exchange complex by acid deposition at a rate faster than the replenishment of the cation
pool by mineral weathering. This displacement enhances the atmospheric contribution,
which is characterized by a low
87
Sr/
86
Sr ratio. Tree-ring chronologies are an exceptional
historic-timing record of chemical changes in the soil environment induced by
atmospheric pollution. The reliability of the tree-ring recorder has been verified with
a well-controlled nutritional perturbation in the context of a limed forest stand (with a
known liming Sr isotopic signature). Our data suggest that forest ecosystems were
affected by atmospheric inputs of strong acids earlier than previously thought.
Keywords: acid deposition, atmospheric deposition, calcium, dendrochemistry, Fagus sylvatica, forest
ecosystem, natural Sr isotopes, Quercus robur, strontium, weathering
Received 14 March 2005; revised version received 15 May 2005; accepted 20 April 2005
Introduction
The two main sources of Ca delivered to trees in forest
ecosystems are mineral weathering release and atmo-
spheric inputs. The measurement of natural variations
of the Sr isotopic composition, expressed by the
87
Sr/
86
Sr ratio, constitutes a useful tool to determine
the origin and the fluxes of Ca in forest stands because
there is no significant chemical or biological fractiona-
tion (Gosz et al., 1983; Miller et al., 1993; Blum et al.,
2002; Kennedy et al., 2002; Drouet et al., 2005).
Strontium is used as a proxy for Ca because the ions
Ca
21
and Sr
21
have a similar chemical structure and
hence, behave similarly in the soil–plant system. Over
the past century, increased acidic deposition (Falkeng-
ren-Grerup et al., 1987; Schulze, 1989; Likens et al., 1996;
Thimonier et al., 2000; Tomlinson, 2003) and reduction
in atmospheric base cations (Hedin et al., 1994;
Wesselink et al., 1995) have caused detrimental effects
on forest ecosystems in temperate regions of Europe
and North America. Acidic deposition is suspected to
have a negative effect on the Ca status of sensitive
forest ecosystems (i.e. forest stands growing on very
acid soils with low weatherable mineral reserve),
because of both depletion of soil exchangeable Ca and
mobilization of monomeric and phytotoxic aluminum
species (Ulrich, 1980; Lawrence et al., 1995).
However, very few data present a historical and
continuous record of the soil acidification process, and
its impact on tree nutrition. Tree-ring analysis of Sr
isotopes provides information on past conditions and
Correspondence: Thomas Drouet, tel. 132 2 650 91 60,
fax 132 2 650 91 70, e-mail: tdrouetd@ulb.ac.be
Global Change Biology (2005) 11, 1–15, doi: 10.1111/j.1365-2486.2005.001034.x
r2005 Blackwell Publishing Ltd 1
on the evolution of Ca availability over time (A
˚berg,
1995; Poszwa et al., 2003; Bullen & Bailey, 2005).
Dendrochemistry assumes that a change in tree-ring
chemistry reflects the historical pattern of change in the
soil solution.
The main objective of the present study is therefore to
evaluate the contribution over time of mineral weath-
ering and atmospheric deposition to soil exchange Sr
and Ca pools. To this end, strontium isotope ratios were
measured in tree-ring chronologies higher than 100
years of beech (Fagus sylvatica L.) and oak (Quercus
robur L.) growth rings from four forest stands located in
Central and High Belgium. These stands were chosen
because they grow on soils with contrasting Ca
contents. Moreover, the soil mineral Sr isotopic compo-
sition (
87
Sr/
86
Sr40.712) is well separated from atmo-
spheric inputs (
87
Sr/
86
Sr0.709) in all the studied sites,
providing a good opportunity to apply the Sr isotope
method to sites that are more or less susceptible to Ca
depletion under acid atmospheric deposition (Drouet et
al., 2005). A parallel is also drawn between our own
data and those published previously by A
˚berg (1995)
and, more recently, by Bullen & Bailey (2005), with the
intention to detect: (1) whether general trends are
revealed on a large geographic scale in sensitive forest
ecosystems affected by acidic deposition; and (2)
whether temporal trends of these long-term chronolo-
gies show evidence of a similar historic timing. In
addition, we analyze the radial Sr isotopic composition
of a beech forest stand of Central Belgium, which has
experienced a controlled nutritional perturbation (ad-
dition of calcareous improvement of known
87
Sr/
86
Sr
ratio in 1972). The aim is to test the reliability of the
tree-ring record and to determine the importance of the
lateral re-equilibration process of base cations in tree
trunks (Houle et al., 2002; Momoshima & Bondietti
1990), which could have a foredating effect on the
historic timing.
Materials and methods
Study area
Seven forest stands were selected for this study. Five are
located in the loess belt of Central Belgium (Soignes
Regional Forest), and the two others in the Palaeozoic
Ardenne massif of High Belgium (Herbeumont State
Forest and Smuid Wood) (Table 1).
The Soignes Regional Forest, southeast of Brussels,
covers 4400 ha of a loessic plateau at about 120 m above
sea level. The natural vegetation is a deciduous forest
with oaks (Quercus robur L. and Q. Petraea (Mattuschka)
Lieblein) and European beech (Fagus sylvatica L.) as
codominant species, but beech has been extensively
introduced since the end of the 18th century. The study
sites are even-aged beech high forests: Me
´sanges site
(MES) planted between 1860 and 1865; Comte de Flandre
(CTE) planted between 1810 and 1820; Tir aux pigeons
(PIG) planted in 1967; Tambour (TAM) planted in 1976;
and Bonne Odeur (ODE) planted between 1830 and 1835.
The last forest stand (ODE) was experimentally limed
in 1972 by foresters to determine the growth response
of the beech to enrichment. Around 12 t ha
1
of crushed
limestone, containing 96% of CaCO
3
and 2.3% of
MgCO
3
, were applied. In all the stands, the ground
layer consists mainly of Pteridium aquilinum (L.) Kuhn,
Dryopteris dilatata (Hoffm.) A. Gray, Carex pilulifera L.,
and Milium effusum L.; Lamium galeobdolon (L.) L., an
indicator of a mull humus type, is locally present in the
limed stand. Prevailing soils are acid-leached soils
(FAO-UNESCO: Podzoluvisols), with an A
h
EB
t(g)
Csoil
profile. These soils are characterized by a clay-enriched
B
t
horizon. The parent material is a Pleistocene niveo-
eolian loess that is composed of more than 70% of
2–50 mm silt-size particles. In the studied sites, the loess
deposit is at least 3.5 m thick and dated from the end of
the Wu
¨rm glaciation (‘Brabantian’ loess,20,000 years
BP: Haesaerts & Bastin, 1977). The loess sheet is
underlain by Tertiary marine sediments (Oligocene
clayey sands). The soil profiles are mainly composed of
quartz (60%), muscovite, K-feldspar, plagioclase,
chlorite, and both 1 : 1 and 2 : 1 clay minerals. The
unweathered loess contains around 13% CaCO
3
, but is
decarbonated down to 250 cm (MES site) or 350 cm
(CTE site) in depth. As a result, in the upper 2 m of the
soil, the pH-H
2
Oiso5.0 and in the upper 80 cm, the
effective base cation saturation is very low (o25%);
correlatively, aluminum saturation is high (475%)
(Table 1). The humus type is a moder-mor (pH-
H
2
Oo4.0, C/N18, base cation saturationo30%). In
the limed beech stand (ODE), the pH-H
2
O and the
effective base cation saturation of the humic layer
(A
h
) are, on average, higher (4.9 1.2 and 78 23,
respectively, n520); the C/N ratio and the aluminum
saturation rate are lower (15.0 0.8 and 20 20,
respectively; n55 and 20, respectively). Very locally,
where residues of the 1970s liming remain, the pH-H
2
O
of the humic layer is around 7.5. In the underlying E
horizon, the differences with the non-amended sites are
still well marked and decrease only in the B
t
horizons
(Table 1).
The Herbeumont State Forest covers 1543 ha of a
400 m high plateau between the Semois and Vierre
river valleys in the southern Belgian Ardenne region.
The forest stand studied is a selection high-forest of
European beech (F. sylvatica L.) and pedunculate oak
(Q. robur L.) (Poursumont site, hereafter POUR). Beech is
the dominant species (90%) and the floristic composi-
2T. D ROU ET et al.
r2005 Blackwell Publishing Ltd, Global Change Biology, doi: 10.1111/j.1365-2486.2005.001034.x
Table 1 General characteristics and selected soil properties of the forest stands used in dendrochemical analyses
Study area
Latitude
longitude
Elevation
(m a.s.l.)
MAT
*
(1C)
MAP
w
(mm)
Stand
species
Tree age
class
z
Tree
87
Sr/
86
Sr
2s10
6
Stand
age
(year)
Soil
type
§
BS
e}
(%)
Ca
21
SR
k
(%)
Total soil
Ca reserve
(kg ha
1
0.5 m
1
)
Total soil
Ca reserve
(kg ha
1
m
1
)
Exchangeable
Ca reserve
(kg ha
1
m
1
)
Central Belgium
Me
´sanges (MES) 5014701300 N 115 9.8 780 Fagus sylvatica M (1879–84) 0.711227 6 170–175 Dd 31.3 20.3 14 700 29 800 3300
412700100 E M (1969–74) 0.711104 9
Tir aux Pigeons (PIG) 5014904100N 110 9.8 780 Fagus sylvatica M 0.711663 5
ww
40 Dd 42.1 20.5 14900 30 800 3600
412801100E
Tambour (TAM) 5014703700 N 105 9.8 780 Fagus sylvatica M 0.711348 5
ww
30 Dd 30.8 15.2 – – 3000
412604100 E
Comte de Flandre (CTE) 5014800600 N 95 9.8 780 Fagus sylvatica M (1824–28) 0.712032 5 180–190 Dd 63.5 33.8 15 600 31 400 2900
412603400 E M (1949–53) 0.712109 5
Bonne Odeur (ODE) 5014700700 N 120 9.8 780 Fagus sylvatica M (1915–19) 0.711237 10 170–175 Dd 48.5 30.6 – – 4700
412605800 E M (1975–79) 0.710083 7
High Belgium
Poursumont (POUR) 4914705700 N 410 7.8 1200 Fagus sylvatica M 0.714599 6160 Bd 5.1 1.7 1700 2100 50
511602600 E Y 0.713532 6
ww
P 0.713679 6
ww
Quercus robur M (1985–89) 0.714570 5
Smuid (SMD) 5010200700 N 360 8.2 1100 Fagus sylvatica M 0.715591 5160 Bd 9.4 1.8 3000 4200 80
511505200 E P 0.714958 5
ww
Quercus robur M 0.715422 9
European Nordic countries (A
˚berg, 1995)
Stockholm 591210N 0–100 3 500–750 Quercus robur M– Bv–––– –
181040E
Oslo 591560N 100–200 3 750–1000 Pinus sylvestris M – Po – – – – –
101440E
USA, New Hampshire (Bullen & Bailey, 2005)
Cone Pond 431540N 480–650 5 1300 Picea rubens M–185 Po 8.9–27.6
**
0.8–5.8
**
800–1200 – –
711360W
*
MAT, mean annual temperature.
w
MAP, mean annual precipitation.
z
M, mature tree ; Y, young tree ; P, plantlets. The 5-year growth intervals analyzed are given between parentheses.
§
Dd, Dystric Podzoluvisol ; Bd, Dystric Cambisol ; Bv, Vertic Cambisol ; Po, Orthic Podzol.
}
BSe, mean effective soil base saturation for the upper meter depth.
k
Ca
21
SR, mean soil calcium saturation rate for the upper meter depth.
**
Calculated for four sites using the data in Bullen & Bailey (2005) and Bailey et al. (1996).
ww
Foliar samples; other measurements are made on wood (recent growth increment samples).
LONG-TERM RECORDS OF STRONTIUM ISOTOPIC COMPOSITION 3
r2005 Blackwell Publishing Ltd, Global Change Biology, doi: 10.1111/j.1365-2486.2005.001034.x
tion of the herbaceous layer is characteristic of the
climax forest association (Luzulo-Fagetum typicum) with
acidity indicators including Luzula luzuloides (Lam.)
Dandy et Wilmott, Deschampsia flexuosa (L.) Trin., C.
pilulifera L., and Polytrichum formosum Hedw. The soil,
with an A
h
B
w
CR profile, is an ochreous brown earth
(FAO-UNESCO: Dystric Cambisol). The humus is a
moder (pH-H
2
O53.7, mean C/N 516.8). The soil is
developed in a 1 m thick loamy and stony solifluction
sheet in which weathering products of the bedrock were
mixed with added loess in a periglacial environment
during the Pleistocene. The bedrock is composed of
Lower Devonian clastic rocks, mainly Praguian shales
and siltstones. The main minerals in the soil are quartz,
muscovite, chlorite, K-feldspar, plagioclase, and both
1 : 1 and 2 : 1 clay minerals. Silt-size particles (2–50 mm)
are dominant, amounting to more than 50% in all
horizons. Because of physical weathering of the shales,
the clay content (o2mm) increases from the C horizon
(10%) to the upper layers (30%), whereas the sand
fraction decreases. The gravel fraction (42 mm) is
around 80% by weight close to the bedrock and
decreases slightly towards the topsoil (60%). Soil acidity
is strong in B
w
and C horizons (pH-H
2
O around 4.5) and
very strong in the organic horizons (A
h
and A
h
B; pH-
H
2
Oo4.0), corresponding to a very low effective cation
saturation (mostlyo10%) and a very high exchangeable
aluminum saturation (mostly 480%) (Table 1).
The Smuid Wood covers 250 ha of a 360 m high
plateau near the Lomme river valley in the middle west
of the Belgian Ardenne region. The forest management
of the stand studied is very similar to that of the POUR
site, (i.e. a selection high-forest of European beech) (F.
sylvatica L.) and pedunculate oak (Quercus robur L.)
where beech predominates (90%) (Smuid site, hereafter
SMD). The forest association (Luzulo-Fagetum festuceto-
sum) is characterized by the presence of both L.
luzuloides (Lam.) Dandy et Wilmott and Festuca altissima
All. The soil, which is also developed in an 1 m thick
loamy and stony solifluction material, has nearly the
same textural, chemical, and mineralogical properties
as the ochreous brown earth of the POUR site (Table 1).
The bedrock is composed of Lower Devonian rocks,
mainly Lochkovian shales and sandstones.
Very low levels of total Ca in the parent material and
bedrock of the two High Belgium forest sites (CaO
0.03% and0.07% in POUR and SMD sites, respec-
tively) are critical in explaining the deficiency of this
base cation in the soil. Forest decline is well documen-
ted in this region and related to Ca and Mg deficiencies
(Weissen et al., 1992). Additional information on site
and stand characteristics is provided in Herbauts et al.
(1996), Penninckx et al. (1999, 2001), and Drouet et al.
(2005).
Sampling
Beech trees (130–160 years old) were randomly
sampled in the MES, ODE, POUR, and SMD sites (five,
six, four, and six boles, respectively) and oak trees
(160 years, four boles) in the mixed stand of the
POUR site, during forest clearings in the winter period,
between 1995 and 1997. In the CTE site, only one old
beech (planted around 1815) was sampled in 2004.
Discs about 20 cm thick were cut from the top of the
boles (30 and 20 m height of the ground in Central
Belgium and High Belgium, respectively) and were
used previously for dendroecological and dendrochem-
ical measurements (Penninckx et al., 1999, 2001;
Herbauts et al., 2002). Leaves were also collected in
beech crowns in MES (n54), PIG (n55), TAM (n55),
CTE (n55), ODE (n55), POUR (n55), and SMD
(n55) sites. In addition, in the POUR stand, foliage of
one adult beech (160-year old), of younger beech
(10-year old; composite sample, n510), and of beech
plantlets (2 years old; composite sample, n55) were
collected. A composite sample of beech plantlets (2-year
old; n550) was also collected in the SMD forest stand.
Soil profiles were sampled within each forest site. Soil
samples were taken at different levels corresponding to
the major soil horizons (Table 1). Soil samples collected
Fig. 1 Comparison between Sr isotope signal in tree-rings and estimates of acid deposition since 1820. (a) Mean
87
Sr/
86
Sr ratio SE in
beech tree-rings of the Poursumont stand (POUR), High Belgium. (b) Oak chronology in the same stand. (c) Beech chronology of the
Smuid stand (SMD), High Belgium. (d) Spruce chronology of Cone Pond watershed, New Hampshire, USA (Bullen & Bailey, 2005) (with
the permission of Springer Science). (e) Oak chronology in the Stockholm area (A
˚berg, 1995). (f) Pine chronology near Oslo (A
˚berg, 1995)
(with the permission of Springer Science). (g) Estimation of acid deposition in Germany (Ulrich, 1987). (h) Estimates of non-marine SO
4
2
deposition, inferred from the GISP2 ice core record (Mayewski et al., 1990), unsmoothed (thin line) and smoothed with a 10-point
moving window (bold line) (with the permission of Nature). (i) Beech chronology of the Me
´sanges stand (MES), Brussels, Central
Belgium. (j) Beech chronology of the Comte de Flandre stand (CTE), Brussels, Central Belgium. Symbol (#) indicates an SE bar smaller than
the symbol size; nis the number of individual tree measurements by date (gray squares) and/or the number of samples constituting a
composite sample (white circles). White triangles represent measurements on foliar samples. The gray circle in (d) indicates a singletree
sample. Vertical dotted lines enclose the time scale of rapid evolution of the Sr isotope ratio. Note the difference in scale for the Sr isotope
ratio. All chronologies are displayed on the same time axis (1820–2000). Roman numerals indicate the estimation of Ca percentage
derived from the atmospheric source; see text for details.
4T. D ROU ET et al.
r2005 Blackwell Publishing Ltd, Global Change Biology, doi: 10.1111/j.1365-2486.2005.001034.x
0.7142
0.7146
0.7150
0.7154
0.7158
0.7162 Quercus robur
POUR
High Belgium
P = 0.004**
n = 4
(b)
0.7142
0.7146
0.7150
0.7154
0.7158
0.7162
87Sr/86Sr
87Sr/86Sr
87Sr/86Sr
87Sr/86Sr
87Sr/86Sr
87Sr/86Sr
87Sr/86Sr
87Sr/86Sr
Fagus sylvatica
POUR
High Belgium #
0.7154
0.7156
0.7158
0.7160
0.7162
0.7164
0.7166
0.7168
Fagus sylvatica
SMD
High Belgium
(c)
0.7188
0.7190
0.7192
0.7194
0.7196
0.7198
0.7200
0.7202
(d) Picea rubens
New Hampshire.
(Bullen & Bailey, in press)
P < 0.001***
n = 7
0.7220
0.7240
0.7260
0.7280
0.7300
0.7320
0.7340
0.7360
(e)
Quercus robur
Stockholm,
(Åberg, 1995)
0.7204
0.7206
0.7208
0.7210
0.7212
0.7214
0.7216
0.7218
(f)
Pinus sylvestris
Oslo (Åberg, 1995)
P = 0.015*
n = 4
(a)
45%
66%
44%
31%
70%
21%
56%
45%
44%
64%
0
20
40
60
80
100
120
140
1820 1840 1860 1880 1900 1920 1940 1960 1980 2000
SO42− (ppb)
(h)
0.00
0.05
0.10
0.15
0.20
0.25
0.30
1820 1840 1860 1880 1900 1920 1940 1960 1980 2000
Annual deposition
(mol m−2 yr−1)
(g)
0.7106
0.7108
0.7110
0.7112
0.7114
0.7116
0.7118
0.7120
1820 1840 1860 1880 1900 1920 1940 1960 1980 2000
Year Year
Year Year
(i)
Fagus sylvatica
MES
Central Belgium
P > 0.05 NS
n = 5
0.7114
0.7116
0.7118
0.7120
0.7122
0.7124
0.7126
0.7128
1820 1840 1860 1880 1900 1920 1940 1960 1980 2000
(j)
Fagus sylvatica
CTE
Central Belgium
LONG-TERM RECORDS OF STRONTIUM ISOTOPIC COMPOSITION 5
r2005 Blackwell Publishing Ltd, Global Change Biology, doi: 10.1111/j.1365-2486.2005.001034.x
at MES and POUR sites have been previously discussed
in Drouet et al. (2005).
Analytical methods
The tree discs were polished with a Si carbide abrading
band to reveal annual growth rings. For each disc,
dated stemwood samples representing 5-year growth
intervals were cut off with a band saw and a chisel, and
the extremities of these wood ‘sticks’ were cut off to
avoid contamination of rings from the abrasive material
and to ensure that interring contamination did not
occur. The samples were dried at 65 1C and ground in a
centrifugal mill ZM100 (Retsch, Haan, Germany) to
pass a 750 mm screen. In four of the five studied stands,
composite samples were prepared for the determina-
tion of the Sr isotope composition by mixing 5-year
growth increment of 4 (POUR site), 5 (MES site), or 6
(SMD and ODE sites) individual trees (shown in Figs 1
and 2). Subsequently, in the MES and the POUR sites, a
limited number of quintet of five and four trees,
respectively, were individually analyzed to observe
the intertree variability and allow statistical analyses.
Mineralization of about 2 g of ground wood or leaves
was performed by dry ashing in covered zirconium
crucibles (16 h at 450 1C). Ashes were dissolved with
1 mL suprapure HCl and heated on a hot plate for
10 min, avoiding boiling. This solution was brought to a
final volume of 50 mL.
Soil chemical and physical analyses
Soil samples were air-dried, crushed, and sieved to a
particle size of o2 mm. Common methods were used
for the determination of soil pH (stiff paste soil-H
2
O),
exchangeable acidity and exchangeable aluminum (1 M
KCl extraction; derivative titration curve for H
1
and
Al
31
), exchangeable cations (1 MCH
3
COONH
4
pH 7
extraction), carbon (dry combustion; Stro
¨hlein dosi-
meter), and nitrogen (semi micro Kjeldahl method).
Particle-size distribution was determined by the pipette
method after H
2
O
2
pre treatment and dispersion with
Na-citrate. Total chemical analysis was carried out by
fusion of 100 mg finely ground soil (planetary micro
mill Retsch), at 700 1C in Pt–Au crucibles (Claisse-
Fluxer) with LiBO
2
(Spectroflux 100 A, Johnson
Matthey, Paris, France); fused samples were dissolved
in a 5% HNO
3
solution and major elements were
determined by ICP-OES. Bulk soil samples used for
isotope analysis were totally digested in sealed Teflon
vessels using a HF-HNO
3
(10 : 1) acid mixture. The
‘acid-extractable’ soil fraction was obtained from
preconditioned soil samples by suprapure 1 M
CH
3
COONH
4
leaching to eliminate the exchangeable
Sr. Surface horizons containing substantial amounts of
organic matter (A
h
and Ehorizons) were at first treated
with hot suprapure H
2
O
2
and afterwards with supra-
pure 1 MCH
3
COONH
4
to eliminate exchangeable and
organically bound Sr. The acid extract consists of four
successive extracts, obtained by shaking 5 g of soil with
50 mL suprapure 0.1 MHCl for 2 h. The aim is to
simulate natural Sr release by weathering (Miller et al.,
1993; Blum et al., 2002, Bullen & Bailey, 2005). The
carbonated fraction of the C
k
horizon of the loessial soils
was leached using 0.5 MCH
3
COOH (only a partial
dissolution was carried out to prevent against possible
acid attack of the silicate residue); this extract is
evaporated to dryness, dry ashed, and re-dissolved
with HCl in a similar way as for plant material. All
elemental analyses of soil (Ca, Mg, K, Na, Ba, Al, Fe,
and Sr) and vegetation (Ca, Mg, K, Ba, and Sr) were
determined by ICP-OES.
Isotope analyses
Chemical separation of Sr from tree core and foliage
digests, total soil, 0.1 MHCl, and CaCO
3
dissolutions
was carried out by cation exchange chromatography. Sr
isotopic compositions were measured on a VG Sector 54
multicollector thermal ionization mass spectrometer
housed at the ‘Laboratoire de Ge
´ochimie isotopique,
Universite
´Libre de Bruxelles.’ The measured
87
Sr/
86
Sr
ratios were normalized to
86
Sr/
88
Sr 50.1194. Measure-
ments of the NBS-987 Sr standard yielded on average
an
87
Sr/
86
Sr value of 0.710270 0.000009 (2s,n525).
Additional details on the analytical procedure can be
found in Ashwal et al. (2002).
Calculations
Because of their geochemical similarities, Sr is often
used as a proxy for Ca in ecosystem studies (e.g.
Graustein & Armstrong, 1983; A
˚berg et al., 1990; Capo
et al., 1998). Sr isotopes are useful tracers in biological
systems because there is no significant fractionation by
geochemical or biochemical processes and any small
mass-dependent fractionating is eliminated via the
normalization procedure during measurement. As
long as the proportion of each cation in the source
materials is known, Sr isotope ratios allow calculation
of the proportion of Ca derived from each source. The
proportion of Sr in a mixture (in this case, the
vegetation) derived from two sources (atmosphere
and weathering) is calculated using a two-component
mixing equation (Capo et al., 1998):
XðSrÞAtm ¼ð87Sr=86 SrÞVeg ð
87Sr=86 SrÞWea
ð87Sr=86 SrÞAtm ð
87Sr=86 SrÞWea
;ð1Þ
6T. D ROU ET et al.
r2005 Blackwell Publishing Ltd, Global Change Biology, doi: 10.1111/j.1365-2486.2005.001034.x
where Veg, Wea, and Atm subscripts denote the
vegetation, weathering, and atmospheric component,
respectively.
The calculated Sr contribution cannot directly be
related to the Ca contribution to vegetation uptake
because the proportion of these elements (Sr/Ca ratio)
is not the same in the two sources. Nevertheless, the
fraction of Ca contributed by the atmospheric end-
member (X(Ca)
Atm
) in a two-component system can be
calculated from the Sr isotope data, provided the Sr/Ca
concentration ratio is known for each component (Capo
et al., 1998). The Sr/Ca ratios of the two sources are
incorporated into Eqn (1) to determine the proportion
of Ca derived from each source. The relative contribu-
tion of Ca from soil mineral weathering and atmo-
spheric sources to vegetation is given by a mixing
equation :
where X(Ca)
Atm
represents the mass fraction of Ca
derived from the atmospheric source.
Statistical analyses
To test whether the date or tree factors are determinant
in explaining the wood Sr isotopic distribution, we
performed an analysis of variance (ANOVA). For the
POUR site, four singletree samples at five and three
dates, for beech and oak, respectively, were used for the
test. In the MES site, five single beech trees at two dates
were used. In addition, for the MES chronology, we
calculated the amount of change that would be
detectable by a t-test at a value a50.05, assuming
equal sample size and standard deviations. The
87
Sr/
86
Sr ratio of the most recent tree-ring of each tree
was successively incremented in proportion to an
increasing Ca atmospheric contribution and compared
with the
87
Sr/
86
Sr ratio of the oldest tree-ring. No tests
were applied for chronologies based on composite
samples.
Results and discussion
Radial trends of Sr isotopic composition recorded in
growth rings
Dendrochemical curves clearly show a decrease of the
87
Sr/
86
Sr ratio from inner to outer wood in the forest
sites of High Belgium (POUR and SMD sites), for both
beech and oak (Fig. 1a–c). Dated wood ranges from ca.
1870 to 1990 for beech and ca. 1850 to 1970 for oak. By
contrast, the Sr isotopic signal shows a very low
variation over the recorded chronologies in the MES
beech stand and, to a lesser extent, in the CTE beech
stand of Central Belgium (Fig. 1i and j) where dated
wood ranges from ca. 1890 to 1990 and ca. 1830 to 1950,
respectively. There is a great inter-tree variability in the
range of
87
Sr/
86
Sr values for beech in the POUR High
Belgium stand, which is probably because of the
varying depth at which the basement rock or its
weathering products with high
87
Sr/
86
Sr ratios come
out in the relatively shallow soil profiles (Drouet et al.,
2005). By contrast, the variability is slight in the MES
beech stand of Central Belgium where loessial soil
profiles are deeper and developed in a much more
homogeneous parent material. Nevertheless, the two-
way ANOVA test shows that the influence of the date
factor on the variation of the Sr isotopic ratio is
significant in the High Belgium POUR site (Fagus:
F
4, 12
54.78, P50.015; Quercus:F
2, 6
516.17, P50.004);
the test is not significant in the MES site of Central
Belgium (F
1, 4
50.15, P50.716). The influence of the tree
factor is not significant for the two sites except for Fagus
in the POUR site (Fagus POUR: F
3, 12
582.36, Po0.001;
Fagus MES: F
4, 4
54.66, P50.083; Quercus POUR:
F
3, 6
51.57, P50.291).
0.7100
0.7102
0.7104
0.7106
0.7108
0.7110
0.7112
0.7114
1880 1900 1920 1940 1960 1980 2000
Year
87Sr/86Sr
Limed stand (ODE)
Control (MES)
Fig. 2 Sr isotope signal of a limed beech stand (Bonne Odeur,
Brussels, Central Belgium). Circles indicate the limed stand
chronology; squares indicates
87
Sr/
86
Sr values of a control stand.
The stand was limed by a blower in 1972 with 12 t ha
1
of
crushed Frasnian limestone (
87
Sr/
86
Sr ratio 50.707857). The
dotted line indicates the liming year.
XðCaÞAtm
¼
ð87Sr=86 SrÞVeg ð
87Sr=86 SrÞWea
hi
ðSr=CaÞWea
ð87Sr=86 SrÞVeg ð
87Sr=86 SrÞWea
hi
ðSr=CaÞWea þð
87Sr=86 SrÞAtm ð
87Sr=86 SrÞVeg
hi
ðSr=CaÞAtm
;ð2Þ
LONG-TERM RECORDS OF STRONTIUM ISOTOPIC COMPOSITION 7
r2005 Blackwell Publishing Ltd, Global Change Biology, doi: 10.1111/j.1365-2486.2005.001034.x
Patterns of decreasing Sr isotope ratio with time in
bole wood (similar to those recorded in beech and oak
trees of the forest sites of High Belgium) were also
observed for Q. robur and Pinus sylvestris in Scandinavia
(A
˚berg, 1995) (Fig. 1e and f), for Picea abies in France
(Poszwa et al., 2003), and for Picea rubens in New
Hampshire, USA (Bullen & Bailey, 2005) (Fig. 1d). A
decrease of the
87
Sr/
86
Sr ratio between the core and the
outer wood for P. abies in Sweden was also pointed out
by A
˚berg et al. (1990). Most of these published data
cover long-term chronologies (100–160 years), except
for the growth ring records of Picea abies, which are
limited to a growth period of only about 40 years. Data
showing no radial variation of the Sr isotopic composi-
tion in tree-rings (as those observed in beech trees of
Central Belgium) have not been published up to now.
Reliability of the tree-ring recorder
The reliability of the tree-ring recorder was verified
using a well-controlled nutritional perturbation, in-
duced 30 years ago in a forest stand by a liming
operation with a known liming Sr isotopic signature.
The radial Sr isotopic composition could be an artifact
because of lateral re-equilibration of base cation in the
tree-rings. This process, pointed out by Momoshima &
Bondietti (1990) and more precisely described by Houle
et al. (2002), implies that ring activity can last tens of
years after the ring formation. The conducting cross-
section is continuously reequilibrated with cation from
the mineral sap (influenced by current soil solution)
until the inactivity of the ring. For example, using the
radial distribution of fallout
90
Sr in tree-rings of red
spruce, Bondietti et al. (1989) have shown that its stem
wood may continue to conduct nutrients for up to 30
years following its formation. To assess the importance
of the reequilibration process in European beech and to
determine more precisely how many growth rings this
process affected, we measured the
87
Sr/
86
Sr ratio in
growth rings of six beeches in a forest stand of Central
Belgium (ODE site), similar to the MES site, but limed
in 1972 with Frasnian limestone (
87
Sr/
86
Sr 50.707857).
The Sr isotopic dendrochemical pattern (Fig. 2) shows
that the wood isotopic ratio was influenced about 50
years before the liming application date. Furthermore,
this time period is in good agreement with 40 active
rings detectable on a fresh disc cut from the bole of a
living beech by the IKI method recommended by
Hagemeyer & Scha
¨fer (1995). It is also in good
agreement with the radial distribution of
90
Sr measured
in the American beech (Fagus grandifolia Ehrh.) by
Momoshima & Bondietti (1994), which shows that the
tree-ring record is foredated by around 35 years before
the atmospheric deposition of
90
Sr in the northern
hemisphere. Concerning the pedunculate oak of the
High Belgium sites, dendroecological and dendrochem-
ical observations (Penninckx et al., 2001) have shown
that the active sapwood is composed of around 30
active growth rings. So, lateral reequilibration could
foredate by several decades the period of Sr iso-
tope ratio decrease observed in stands growing on
sensitive soils.
Origin of the radial trends of Sr isotopic composition in
tree-rings
Long-term chronologies suggest that a decreasing trend
could be a general feature in forest trees of Europe and
North America. Change in the radial
87
Sr/
86
Sr ratio can
be ascribed to: (i) the variation over the tree growth
period of the Sr isotope signal of the two main sources
of Sr delivered to trees (i.e. atmospheric inputs and
mineral weathering release) or (ii) a temporal change of
the respective contribution to tree nutrition of these two
primary sources.
Two modifications over time of the Sr isotope ratio
can be considered: (i) a modification of the atmospheric
source and (ii) a modification of the weathering source.
An evolution in the
87
Sr/
86
Sr ratio of the atmospheric
source over time can be discarded given that the
current Sr isotope measurements on bulk precipitation
in Central and High Belgium (Drouet et al., 2005) are
similar to those of present-day seawater (0.70923,
constant value for the o200-year interval) (e.g. Capo
et al., 1998). This is in good agreement with the
monitoring network of wet deposition on a European
scale (Van Leeuwen et al., 1996), which shows that
nearly the whole Belgian territory is under an oceanic
influence as clearly proved by the distribution pattern
in precipitation of elements from marine origin, mainly
Cl and Na. Bain & Bacon (1994) had already pointed
out in Scotland that the isotopic composition of the
precipitation in regions situated only 300 km or less
from the sea coast is strongly controlled by sea-salt
aerosols with constant marine
87
Sr/
86
Sr values. It can
also be concluded that the Sr atmospheric source is not
substantially influenced by human activities, knowing
that most of the industrial and agricultural sources of
Ca contributing to atmospheric pollution (and, by
inference, of Sr) generate strontium with an isotope
ratio lower than that of the present-day seawater
(Straughan et al., 1981; Simonetti et al., 2000; Bo
¨hlke &
Horan, 2000). It would also be very surprising that
regional industrial activities had the same effect, at the
same time, in countries as far as North America,
Scandinavia and High Belgium. Moreover, if we
assume that the whole modification of the tree-ring
87
Sr/
86
Sr ratio is because of a change of the isotopic
8T. D ROU ET et al.
r2005 Blackwell Publishing Ltd, Global Change Biology, doi: 10.1111/j.1365-2486.2005.001034.x
signal of the atmospheric source, we can estimate what
could be the value of the Sr isotopic ratio in precipita-
tion in the 1870s. This calculation is possible if we
consider that the proportion of Sr originatign from the
atmospheric source and stored in the forest biomass
(calculated from Eqn. (1)) has not changed over time.
Based on the
87
Sr/
86
Sr ratios of the weathering source,
the
87
Sr/
86
Sr ratios in recent and old tree-rings, and the
current proportion and Sr isotopic ratio of the atmo-
spheric source, the
87
Sr/
86
Sr ratio of the 1870s pre-
cipitation was modeled and gave values of 0.7093,
0.7074, 0.7128, 0.7145, and 0.7148, for the MES, CTE,
POUR (beech), POUR (oak), and SMD forest stands,
respectively. A similar calculation was extended to the
data published for a forest site of central Sweden
(A
˚berg et al., 1989, 1990), for a Norway spruce forest of
northeast France (Probst et al., 2000; Poszwa et al., 2003),
and for the red spruce forest studied by Bullen & Bailey
(2005) in New Hampshire. Modeled
87
Sr/
86
Sr precipita-
tions are 0.7230 in Sweden, range from 0.719 to 0.721 in
France, and from 0.7130 to 0.7193 (n57) in North
America. Most of these values are clearly too high to be
consistent with an oceanic or even continental origin of
the precipitation in all these areas. In addition, the
calculated
87
Sr/
86
Sr values are different between
stands, which could only be explained by different
local or regional human influences. Our view is that
these results are not compatible with the similar
decreasing patterns of tree-rings
87
Sr/
86
Sr ratio re-
corded in forest stands with a wide geographic
distribution. The lack of evidence of changes over time
of the Sr isotopic composition of atmospheric deposi-
tion was also suggested by A
˚berg et al. (1990), Dijkstra
et al. (2002), Poszwa et al. (2003) and Bullen & Bailey (in
press). Also unlikely is the hypothesis that the steep
declines in the atmospheric concentrations of base
cations over the past 20 years in Europe and North
America (Hedin et al., 1994) could have an effect upon
the Sr isotope signal in tree-rings: the consequence
would have been a proportional increase of the weath-
ering source in tree nutrition and hence, an increase
of the
87
Sr/
86
Sr ratio of the growth rings during this
time period.
Change of the weathering isotopic signal by a
variation of the relative weathering contributions is
also unlikely, as already pointed out by Bailey et al.
(1994). Laboratory kinetics, budget studies, and recon-
struction of historic weathering by modeling in
Swedish catchments over the 12 000 years following
the last glaciation have shown that no variation of the
chemical weathering has been reconstituted for the last
century, even if the modeled soil chemistry (e.g.
depletion of base cations and decrease of soil solution
pH) has changed very rapidly during the same time
period, because of acid deposition effects (Sverdrup &
Warfvinge, 1995). But change of the isotope signal of the
weathering source could also be explained by changes
in the soil layers prospected by tree roots during their
growth period, the different horizons forming a soil
profile showing generally contrasting isotope composi-
tions (A
˚berg et al., 1989, Blum & Erel, 1997; Kennedy
et al., 2002; Poszwa et al., 2003; Drouet et al., 2005; Bullen
& Bailey, 2005). Forest aging (Hamburg et al., 2003) or
limitations of nutrient availability in specific soil
horizons in response to modifications of environmental
factors – e.g. drought stress (Poszwa et al., 2003) or acid
deposition inducing aluminum toxicity (Ulrich 1989;
Poszwa et al., 2003; Bullen & Bailey, 2005) – have been
hypothesized to explain a deepening or a shallowing of
the effective depth of root uptake over the forest growth
period. But forest stand development implying change
in soil rooting depths or difference in organic acid
production enhancing as suggested by Hamburg et al.
(2003) may, however, be ruled out in the forest stands of
High Belgium in view of an increasing isotope ratio
from young trees and/or plantlets to mature trees of
Fagus sylvatica in the POUR and SMD sites (Table 2).
Such an increase of the
87
Sr/
86
Sr ratio with tree growth
goes against the observed temporal trend. On the other
hand, an extensive study of beech and oak growth
curves in High Belgium (Penninckx, 2001) has not
shown increased drought stress contemporary to the
change in tree-ring Sr isotope composition, suggesting
that the isotopic pattern is not related to climatic
factors. The third hypothesis, the ‘aluminum toxicity’
hypothesis, which was specially developed by Bullen &
Bailey (2005) to explain the decreasing temporal trend
in the stemwood Sr isotopic ratio of a north-American
red spruce forest by progressive shallowing of the
effective depth of alkaline earth elements uptake by fine
roots during the past 130 years, is open to discussion.
Using
87
Sr/
86
Sr and Sr/Ba ratios of spruce tissues and
soil fractions together in a multi-tracer approach, Bullen
and Bailey hypothesized that the preferential growth
and expansion of the fine root network in the upper
forest floor is a consequence of acid deposition and a
response to Ca depletion and/or mobilization of
‘monomeric Al’, which induces aluminum toxicity in
the lower forest floor and the upper mineral soil
horizons. Hence, the nutrient uptake by roots is
transferred from soil horizons with high
87
Sr/
86
Sr ratios
(characteristic of mineral weathering) to the uppermost
and organic soil horizons with lower isotopic ratios. A
nearly similar scenario was proposed by Ulrich (1989)
to explain an increasing sensitivity of forest to drought:
low concentrations of basic cations and high levels of
exchangeable Al in mineral horizons, resulting from
soil acidification, could promote the development of
LONG-TERM RECORDS OF STRONTIUM ISOTOPIC COMPOSITION 9
r2005 Blackwell Publishing Ltd, Global Change Biology, doi: 10.1111/j.1365-2486.2005.001034.x
Table 2 Physical and chemical properties of soil profiles in the forest stands studied
Horizon
Sampling
depth (cm)
Soil
texture
*
Stoniness
(wt%)
OM
(%) C/N pH-H
2
O
CaCO
3
(%)
Exchangeable
acidity
w
(cmol
c
kg
1
)
Exchangeable cations
z
Exchange-
able
w
Al
31
(cmol
c
kg
1
)
Effective base
saturation
(BS
e
)(%)
Al
31
satura-
tion (%)
Ca
21
satura-
tion (%)
Ca
21
Mg
2
K
1
(cmol
c
kg
1
)
Central Belgium
MES site acid-leached soil (Dystric Podzoluvisol), Soignes Regional Forest
A
h
0–5 Loam 0 21.3 18.3 3.7 0.0 3.28 0.73 0.29 0.29 2.69 28.5 58.6 15.9
E5–25 Loam 0 2.2 4.0 0.0 2.59 0.14 0.06 0.09 2.59 10.1 89.9 4.9
B
1t
25–35 Loam 0 1.8 4.1 0.0 2.98 0.14 0.06 0.13 2.98 10.0 90.3 4.2
B
21t
55–75 Clay loam 0 0.2 4.2 0.0 3.05 0.55 0.18 0.15 3.05 22.4 77.8 14.0
B
22t
80–90 Clay loam 0 0.1 4.4 0.0 2.26 1.97 0.93 0.21 2.26 57.9 42.1 36.7
B
3t
175–200 Clay loam 0 4.9 0.0 1.29 4.19 1.35 0.22 1.29 81.7 18.3 59.4
C230–240 Loam 0 5.3 0.0 0.00 10.32 2.80 0.18 0.00 100.00 0.0 77.6
C
k
300–320 Loam 0 7.4 15.1 0.00
CTE site, acid-leached soil (Dystric Podzoluvisol), Soignes Regional Forest
A
h
0–5 Loam 0 32.4 22.2 3.4 0.0 6.35 0.67 0.83 0.50 4.35 25.1 52.1 8.0
E5–25 Loam 0 4.5 0.0 2.75 0.04 0.03 0.05 2.44 5.3 85.1 1.2
B
21t
55–75 Clay loam 0 4.9 0.0 0.36 1.32 0.87 0.18 0.14 87.1 4.9 48.2
B
3t
175–200 Clay loam 0 5.2 0.0 0.73 3.69 1.80 0.17 0.61 88.6 9.5 57.8
C260–270 Loam 0 5.2 0.0 0.23 4.59 1.33 0.10 0.14 96.4 2.3 73.5
C
k
295–305 Loam 0 7.5 13.2 0.00
ODE site, acid-leached soil limed in 1972 (Dystric Podzoluvisol), Soignes Regional Forest
§
A
h
0–5 Loam 0 17.3 14.7 4.9 1.2 nd 1.78 1.89 15.2 19.3 0.75 0.57 0.31 0.16 1.60 1.59 78 23 20 20 70 24
E5–25 Loam 0 4.7 0.9 nd 1.53 1.22 2.20 2.11 0.13 0.03 0.09 0.03 1.53 1.22 59 34 41 34 52 33
B
1t
25–35 Loam 0 4.3 0.1 nd 3.88 0.74 0.74 0.42 0.10 0.07 0.13 0.04 3.88 0.74 19 6816156
B
21t
60–70 Clay loam 0 4.2 0.0 5.83 0.80 2.69 0.09 5.83 38.0 62.0 8.5
B
22t
100–120 Clay loam 0 4.8 0.0 1.62 4.99 2.88 0.13 1.62 83.2 16.8 51.9
High Belgium
POUR site, Ochreous brown earth (Dystric Cambisol), Herbeumont State Forest
A
h
0–3 Silty clay 28.5 29.8 19.9 3.7 0.0 8.41 0.69 0.48 0.33 6.75 15.1 68.1 7.0
A
h
/B3–10 Silty clay 39.5 13.7 22.7 3.9 0.0 6.94 0.14 0.19 0.18 5.75 6.8 77.2 1.9
B
1w
10–25 Sandy clay loam 46.6 6.4 4.5 0.0 3.37 0.05 0.05 0.07 2.99 4.8 84.5 1.4
B
2w
30–40 Sandy clay loam 59.2 4.7 4.4 0.0 2.44 0.05 0.03 0.06 2.27 5.4 88.0 1.9
B
2w
/C 45–55 Sandy clay loam 77.2 2.5 4.5 0.0 1.74 0.03 0.02 0.05 1.66 5.4 90.2 1.6
C70–85 Sandy clay loam 75.9 0.6 4.4 0.0 2.68 0.04 0.02 0.06 2.53 4.2 90.4 1.4
SMD site, Ochreous brown earth (Dystric Cambisol), Smuid wood
A
h
0–3 Silty clay nd 22.0 14.1 3.7 0.0 4.98 0.82 0.36 0.65 4.14 28.1 59.8 12.0
A
h
/B 3–10 Silty clay nd 7.6 15.3 4.0 0.0 4.46 0.09 0.09 0.18 3.82 9.2 77.8 2.0
B
1w
10–25 Sandy clay loam nd 4.5 4.4 0.0 2.36 0.05 0.03 0.07 2.13 9.2 82.0 2.2
B
2w
25–40 Sandy clay loam nd 1.3 4.4 0.0 1.71 0.04 0.02 0.06 1.57 11.6 81.2 2.3
B
2w
/C 40–50 Sandy clay loam nd 0.5 4.5 0.0 3.94 0.03 0.03 0.09 3.73 5.8 89.2 0.7
C60–70 Sandy clay loam nd 0.4 4.5 0.0 2.78 0.03 0.04 0.08 2.57 8.4 84.6 1.2
*
Belgian soil classification (all soil are silt loam after the FAO classification, except the silty E horizons).
w
1 M KCl extraction.
z
1MCH
3
COONH
4
pH 7 extraction.
§
Mean values standard deviation show the heterogeneity of some chemical data caused by the liming in the upper horizons.
MES, Me
´sanges; CTE, Comte de Flandre; ODE, Odeur; POUR, Poursumont;SMD,Smuid; nd, not determined.
10 T. DROUET et al.
r2005 Blackwell Publishing Ltd, Global Change Biology, doi: 10.1111/j.1365-2486.2005.001034.x
roots in the organic layers. A shallowing of the effective
depth of element uptake under the influence of acid
deposition could also be put forward in the forest
stands of High Belgium (POUR and SMD sites) and
could explain the outward decreasing trend of the Sr
isotopic ratio observed in beech and oak tree-rings: the
soil Sr isotopic ratios increase with depth and the
lowest
87
Sr/
86
Sr ratios are measured in the humic layers
(Table 3). However, in addition to the fact that an
alternative explanation can be formulated, it must be
emphasized that the whole of our set of data does not
totally agree with this hypothesis. Firstly, it is surpris-
ing that in the forest stands of Central Belgium (MES
and CTE sites) the isotopic signal recorded in beech
tree-rings is stable over time, while: (1) the
87
Sr/
86
Sr
ratio of the soil exchangeable fraction decreases in the
uppermost, organic-rich forest floor, in the same way as
in the High Belgium sites; and (2) the gradient with
depth of the soil chemical parameters are also favorable
to a shallowing of the effective depth of base cation
Table 3 Isotopic compositions, Sr, Ca, Ba concentrations and Sr/Ca, Sr/Ba ratios of the atmosheric and the weathering
endmembers and of the soil exchangeable fraction in the Belgian studied stands
Atmospheric precipitation
Sampling
date
87
Sr/
86
Sr
2s10
6
Sr (mgL
1
)Ca(mgL
1
) Sr/Ca (g g
1
)
Central Belgium
*
28-XI-2001 0.709026 10 1.3 250 0.0052
Central Belgium
*
29-XII-2002 0.709175 7 1.4 292 0.0048
High Belgium
*
23-I-2003 0.709238 7 2.4 1112 0.0021
Central Belgium mean bulk
precipitation (n517;
mean SD)
1.6 1.3 510 465 0.0032 0.0008
High Belgium mean
precipitation (Offagne,
n536; mean SD)
3.2 1.7 1490 1250 0.0024 0.0006
Soil Soil
horizon
Sampling
depth (cm)
87
Sr/
86
Sr
2s10
6
Sr (mg kg
1
)Ca(mgkg
1
) Sr/Ca (g g
1
)
Weathering endmember (0.1 MHCl leaching)
POUR site A
h
0–3 0.714070 6 0.71 69 0.0104
A
h
/B3–10 0.716204 6 0.42 37 0.0116
B
1w
10–25 0.717617 6 0.46 35 0.0132
B
2w
/C45–55 0.717027 5 0.48 35 0.0137
SMD site A
h
0–3 – – – –
A
h
/B3–10 – 0.25 26 0.0097
B
1w
10–25 0.717099 6 0.22 20 0.0110
B
2w
45–55 – 0.11 10 0.0114
MES site A
h
0–5 0.713643 7 0.37 32 0.0117
E10–25 0.713114 6 0.14 8 0.0179
B
21t
55–75 0.712067 7 0.39 15 0.0257
Exchangeable fraction (1 MCH
3
COONH
4
extract)
POUR site A
h
0–3 0.714509 9 0.69 135 0.0051
A
h
/B3–10 0.715634 9 0.12 12 0.0098
B
1w
10–25 0.715427 13 0.05 5 0.0101
B
2w
/C 45–55 0.717020 5 0.03 4 0.0075
SMD site A
h
0–3 0.714809 5 0.75 164 0.0046
A
h
/B3–10 0.715857 7 0.12 19 0.0061
B
1w
10–25 0.716250 5 0.06 11 0.0054
B
2w
45–55 0.714920 17 0.05 9 0.0055
MES site A
h
0–5 0.712138 6 0.89 190 0.0047
E10–25 0.712888 7 0.12 19 0.0062
B
21t
55–75 0.715291 6 0.48 66 0.0073
*
Data from Drouet et al. (2005).
MES, Me
´sanges; CTE, Comte de Flandre; ODE, Odeur; POUR, Poursumont;SMD,Smuid.
LONG-TERM RECORDS OF STRONTIUM ISOTOPIC COMPOSITION 11
r2005 Blackwell Publishing Ltd, Global Change Biology, doi: 10.1111/j.1365-2486.2005.001034.x
uptake by tree roots (i.e., a strong Ca depletion and very
high aluminum saturation rates in the upper mineral
soil horizons, in contrast with the overlying humic
layer) (Table 2). Secondly, the ‘shallowing hypothesis’ is
not confirmed in all our studied forest stands when, as
suggested by Bullen & Bailey (2005), the Sr/Ba ratio is
used as a complementary tracer. These authors have
shown that in the Cone Pond red spruce forest, the Sr/
Ba ratio of stemwood samples tends on average toward
values that are characteristic of the ‘plant available’
fraction of the uppermost forest floor. By contrast, in all
our studied forest sites, the radial evolution of the Sr/
Ba ratio in growth rings of both beech and oak shows
no marked trend.
Changes of atmospheric vs. weathering source ratio in
tree nutrition
If the Sr isotopic composition of neither the atmo-
spheric nor the weathering source has changed with
time, only a temporal change in their respective mass
contributions to tree nutrition can explain the decreas-
ing trends of the
87
Sr/
86
Sr ratio in growth rings
observed in long-term chronologies of both beech and
oak trees of the High Belgium forest stands and,
generally speaking, the similar decreasing trend de-
tected in different tree species of Scandinavia (A
˚berg,
1995) and North America (Bullen & Bailey, 2005). The
use of a two-member mixing equation (Eqn. (2)) allows
to calculate the proportion of Ca atmospheric input for
each stand in the course of time, assuming that Sr is a
proxy for Ca and that the vegetation cation pool is a
mixture of Sr derived from mineral weathering (weath-
ering endmember) and from atmospheric input (atmo-
spheric endmember) (respective Sr/Ca and
87
Sr/
86
Sr
ratios are given in Table 3). The atmospheric end-
member was measured in bulk precipitation samples,
and the weathering endmember was determined by
dissolution of soil samples from different soil horizons
using 0.1 MHCl (Table 3). Between 1850 and 2000,
atmospheric contributions increased from21% to
56% in the SMD beech stand, and from 45% to
66% for beech and from44% to70% for oak trees
in the POUR stand (Fig. 1). So, in both stands and
whatever the tree species, the contribution of the
weathering source has decreased by around 30%
during a 150-year time interval. How can this decrease
be explained? The supply of available Ca for a forest
stand depends mainly on the soil exchangeable reserve.
The Sr isotopic composition of this cation pool is
controlled by weathering processes and by the input of
Sr from atmospheric deposition and organic restitu-
tions. In the High Belgium forest sites, calculation
(based on Eqn. (2)) indicates that around 65% of the soil
exchangeable Ca of the B
1w
horizon (10–25 cm depth)
originates from atmospheric inputs. The steep decrease
of the Sr isotope ratio in tree-rings can therefore be
related to: (1) a fall of the soil base saturation (BS) and
of the Ca saturation rate; (2) a modification of the Sr
isotopic composition of this exchange pool because of
an increasing contribution of cations originating from
the atmospheric source. Both soil BS decrease and Ca
depletion from the soil exchange pool originating from
the weathering source lead to a decrease of the plant-
available elements what display mainly the Sr isotopic
signature of the weathering endmember and, accord-
ingly, a significant increase of the atmospheric con-
tribution. A decrease of the soil BS during different
periods of the last century has been highlighted in
Europe and North America by several methods (e.g.
soil resampling) (Falkengren-Grerup et al., 1987; Thi-
monier et al., 2000) and long-term site observations
(Likens et al., 1998; Blake et al., 1999). As early as 1995,
in order to see whether the decrease over time of the Sr
ratio in growth rings of two Scandinavian trees was a
general feature, A
˚berg looked for another independent
system and used the freshwater pearl mussel Margar-
itifera that grows in Central Swedish rivers. The results
show that there is a distinct decrease in Sr isotope ratio
in the Margaritifera shells over the studied time interval
(1901 to 1990) and that the trend is the same as those
recorded in tree-rings in the same region; this also
suggests an ongoing acidification of the environment
and a leaching of exchangeable base cations because of
acid deposition (A
˚berg, 1995; A
˚berg et al., 1995).
Historic timing of the temporal trend of long-term
chronologies and causal mechanisms
The similar isotopic patterns, which are observed for
different tree species with contrasting wood structure
in different world countries (from North America to
North and Western Europe) (Fig. 1), could arguably
point to a common environmental effect.
The decrease of the Sr isotope ratio in trees of
sensitive sites occurs in a very narrow period of time
(Fig. 1), from ca. 1870 to 1890, with a major impact on
the Ca sources available for root uptake. Interestingly,
there is a striking parallelism between the beginning of
the
87
Sr/
86
Sr decrease and the beginning of the increase
of sulfur emission because of industrial activities at the
end of the 19th century. This is highlighted by SO
4
2
deposition estimations (Ulrich, 1987) and by a record of
nonmarine SO
4
2
deposition in an ice core from South-
Central Greenland (Mayewski et al. 1990) (Fig. 1g and
h). A similar interpretation was already proposed by
A
˚berg et al., (1995) and, recently, by Bullen & Bailey
(2005). The latter concluded that the timing of den-
12 T. DROUET et al.
r2005 Blackwell Publishing Ltd, Global Change Biology, doi: 10.1111/j.1365-2486.2005.001034.x
drochemical changes, which suggest a response to soil
acidification in red spruce stemwood, is consistent with
the established history of inorganic acid deposition in
northeastern North America. Deposition of sulfates is
known to increase the loss of basic cations from the
rooting zone by leaching (Reuss, 1983). This soil
acidification process leads to the mobilization of
cationic Al competing with Ca, eventually reducing
Ca availability for root uptake (Lawrence et al., 1995;
Tomlinson, 2003). As a result, the Sr isotope composi-
tion of the soil water taken up by trees moves toward
that of the atmospheric source. The regular decrease of
the Sr isotopic signal in tree-rings (Fig. 1a and 1c), from
ca. 1870 to 1890, could be interpreted as a gradual effect
of acid deposition over this time period. However, it
must be kept in mind that this trend is influenced by a
radial reequilibration process in beech rings, which
implies that ring activity can last about 50 years after
the ring formation. It may therefore be expected that the
effect of acid deposition has not occurred gradually
from 1870 to 1920, but more abruptly around the 1920s.
Our opinion is that the steep decrease of the Sr isotope
ratio in tree-rings is a consequence of a broken
equilibrium caused by the change of the dominant acid
in soil (Wesselink et al., 1995). In the not highly acidic
context of a preindustrial forest ecosystems, the
dominant anion was either bicarbonate (HCO
3
)or
organic. In the 1870s, the combustion of fossil fuel
caused the substitution of the dominant carbonic acid
by sulfuric acid, which has a higher dissociation
constant (Tomlinson, 2003). The result is a substantial
increase in nutrient cations transferred from the
exchangeable pool to the soil solution. This explanation
reconciles the rapidity of the phenomenon with a
subsequent slower evolution, when a new Ca weath-
ering–leaching–uptake equilibrium has been reached.
After 1920, the Sr isotopic signal of the tree-rings
reaches a more or less constant value (except in the case
of oak trees in the High Belgium POUR stand and in the
New Hampshire spruce forest studied by Bullen &
Bailey (2005) corresponding to a maximum change in
the Ca source contributions of 12%, despite a contin-
uous increase of acid deposition until the beginning of
the 1980s (the amounts of acid loads in 1980 are two
times higher than those around 1920). Atmospheric
contribution of Ca continues to grow from 45% to 70%
in only one oak time series of High Belgium until the
1980s (Fig. 1).
Why an unvarying tree-ring Sr isotopic composition over
time in the forest sites of Central Belgium ?
The lack of a decrease of the Sr isotopic ratio in the tree-
rings of beech in the Central Belgium sites (MES and
CTE sites: Fig. 1i and j) is a very instructive cases to
complete the explanation of the above-discussed
process. Even if the difference of
87
Sr/
86
Sr ratios
between the two endmembers (0.709 and 0.713) in
these sites is 1.5 times lower than in the High Belgium
stands, they are well separated and not overlapping.
The conditions for applying the isotopic method are
then well respected (Capo et al., 1998). We have
calculated that an increase of 3% and 9% of the Ca
atmospheric contribution in Central Belgium should be
detectable at a significant to highly significant level,
respectively (paired t-test). So, a change in the Ca
sources proportion of 20–30%, as in the High Belgium
stands, would have been detectable.
The stability of the Sr isotopic signature in the beech
wood of Central Belgium could be explained by a soil-
effective base saturation BS
e
, on average higher than the
critical value of 20% (or a Ca saturation higher than
15%) in the upper meter (Table 2). Above these values,
the soil solution is considered to be buffered mainly by
release of base cations from the exchange complex
(Reuss, 1983).
Moreover, the acid-leached soils developed on loess
of Central Belgium (MES and CTE sites) contain 12
times more total Ca and 30 times more exchangeable Ca
in their upper meter than the ochreous brown earths on
Devonian shales of High Belgium (POUR and SMD
sites) (Table 2). Even if only the upper 50 cm of the soil
is taken into account (i.e. the depth mainly prospected
by beech roots), the Ca contents are still clearly distinct:
the loessial soils contain seven times more total Ca and
15 times more exchangeable Ca than the soils of High
Belgium. In other words, the Central Belgium forest
stands are growing on soils that can be considered as
slightly sensitive to acid deposition.
Conclusions
Our results show that long-term records of strontium
isotopic composition in tree-rings are an exceptional
historic-timing record of chemical changes in the soil
environment. An accurate interpretation of the tree-ring
records however, needs, to take into account the
influence of the lateral reequilibration of base cation
in the tree-rings. The opportunity to verify the
reliability of the tree-ring recorder was provided by a
well-controlled nutritional perturbation in the context
of a limed forest stand induced 30 years ago by addition
of crushed limestones with a known Sr isotopic
signature. In the ‘sensitive’ forest sites of High Belgium
(i.e. forest stands growing on very acid soils with low
Ca reserve), the dendrochemical curves show a
decrease of the
87
Sr/
86
Sr ratio in growth rings from
inner to outer wood, for both beech and oak, suggesting
LONG-TERM RECORDS OF STRONTIUM ISOTOPIC COMPOSITION 13
r2005 Blackwell Publishing Ltd, Global Change Biology, doi: 10.1111/j.1365-2486.2005.001034.x
that these forest ecosystems were abruptly affected by
atmospheric inputs of strong acids around the 1920s. By
contrast, the forest sites of Central Belgium, growing on
Ca-richer soils, are slightly sensitive to acid deposition
and, consequently, show a stability of the Sr isotopic
signature. The steep decrease of the Sr isotope ratio in
tree-rings is thought to be a consequence of a broken
equilibrium induced by the massive input of SO
4
through atmospheric pollution. The nearly similar
radial patterns of decreasing Sr isotope ratio recorded
in long-term chronologies of F. sylvatica and Q.
peduncalata in High Belgium, of Q. peduncalata and P.
sylvestris in Scandinavia (A
˚berg, 1995), and of P. rubens
in North America (Bullen & Bailey, 2005), associated
with a clear evidence of a similar historic timing, reveal
a general trend on a large geographic scale in sensitive
forest ecosystems affected by acidic deposition.
Acknowledgements
This research was financially supported by the ‘Fonds pour la
Recherche Fondamentale et Collective’ FRFC (Belgium) to J.
Herbauts and D. Demaiffe. Th. Drouet is a fellow of the FRIA
(Fonds de Formation pour la Recherche dans l’Industrie et
l’Agriculture). We gratefully acknowledge Wolf Gruber for
assistance in the laboratory. Patricia Hermand is warmly
thanked for the maintenance of the mass spectrometer and
supervision of the isotopic measurements. Th. D. is grateful to
Prof. Go
¨ran A
˚berg for constructive correspondence. The authors
are extremely grateful to the two anonymous reviewers for their
critical comments on the manuscript. Thanks are because of
Springer Science and to Nature for their permission to reproduce
some figures.
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