Download Tree-ring elemental concentrations in oak do not necessarily

S CIE N CE OF T H E TOT AL E N V I RO N ME N T 3 9 0 ( 2 00 8 ) 2 7 5–2 86
a v a i l a b l e a t w w w. s c i e n c e d i r e c t . c o m
w w w. e l s e v i e r. c o m / l o c a t e / s c i t o t e n v
Tree-ring elemental concentrations in oak do not necessarily
passively record changes in bioavailability
Andrew R. Bukata⁎, T. Kurtis Kyser
Queen's Facility for Isotope Research (QFIR), Department of Geological Sciences and Geological Engineering, Queen's University, Kingston, ON,
Canada K7N 3N6
AR TIC LE I N FO
ABS TR ACT
Article history:
Elemental concentrations in tree-rings from red and white oak trees at six sites across
Received 2 April 2007
Southern Ontario, Canada, were assessed to determine whether they passively record
Received in revised form
changes in geochemical cycling in the presence of environmental stress. Periods of stress
6 September 2007
were defined as sustained periods with elevated δ13C values in tree-rings relative to
Accepted 7 September 2007
atmospheric CO2 during the same period. In some trees, nutrient concentrations (Ca, Mg,
Mn) were erratic during historic periods of stress while chemically similar non-nutrients (Ba,
Keywords:
Sr) and the anthropogenic pollutant Pb were not. Tree-ring concentrations of Ca and Sr were
Dendrogeochemistry
related to bedrock type and leachable concentrations in the soil. In contrast, tree-ring
Carbon isotopes
concentrations of Mg were not related to bedrock type, although Mg concentration in the soil
Tree-ring
leachate was. Tree-ring Mn, Ba and Pb concentrations were not related to bedrock type or
LA-ICP-MS
soil concentrations, but were inversely related to soil pH. Erratic behavior of nutrient
elements during historic periods of stress suggests that some nutrient concentrations in the
environment were not always passively recorded by tree-rings.
© 2007 Elsevier B.V. All rights reserved.
1.
Introduction
Proxy records of pollution are necessary when direct instrumental monitoring of the environment is not available.
Longevity, fixed location and visible annual growth rings
make trees attractive as potential sentinels of environmental
change. Chemical variations observed across tree-rings have
led to the suggestion they can potentially be used to generate
chronologies of changes in biogeochemical cycles (Watmough, 1997; Padilla and Anderson, 2002; Witte et al., 2004).
For tree-ring elemental concentrations to be effective proxies
for elemental bioavailability, trees must be passive monitors
and the physiological effects on uptake of elements should be
predictable. There must be minimal elemental mobility across
growth rings and the elemental concentrations in the tree-ring
must be proportional to bioavailability (Momoshima et al.,
1995; Watmough, 1997), which may not always be the case
(Watmough and Hutchinson, 2002). Failure to meet these
conditions means that tree-ring elemental concentrations are
not passive monitors and developing chronologies of environmental change based on tree-rings becomes difficult.
There has been considerable debate as to whether elemental concentrations of tree-rings passively record bioavailability
in their environment or whether concentration trends are
dominated by tree physiology (Chun and Hui-yi, 1992; Smith
and Shortle, 1996; Garbe-Schönberg et al., 1997; Watmough,
1999; Watmough and Hutchinson, 2003). The effect of stress
on tree-ring elemental concentrations has not been systematically studied, but could help assess whether tree-ring
chemistry passively records environmental conditions. This
study examines the relationship between stress and tree-ring
elemental concentration of nutrients (Ca, Mg and Mn), nonnutrients that are chemically similar to Ca (Ba, Sr) and the
anthropogenic pollutant Pb. Despite chemical similarity, these
⁎ Corresponding author. Department of Geology, University at Buffalo, Buffalo, NY 14260-3050, USA. Tel.: +1 716 645 6800x6100; fax: +1 716
645 3999.
E-mail address: [email protected] (A.R. Bukata).
0048-9697/$ – see front matter © 2007 Elsevier B.V. All rights reserved.
doi:10.1016/j.scitotenv.2007.09.005
276
SC IE N CE OF T H E TOT AL E N V I RO N ME N T 3 9 0 ( 2 00 8 ) 2 7 5–2 86
elements have been shown to display some dissimilar
behavior in tree-rings including differences in radial mobility
and uptake (Cutter and Guyette, 1993). If an environmental
stressor affects geochemical cycling, similar behavior should
be observed in both nutrients and chemically similar nonnutrients. Dissimilar response would indicate that environmental stress is affecting physiological functioning of the tree,
which in turn differentially affects uptake and distribution of
elements in the tree. Conversely, a lack of stress-related
variation in uptake would be consistent with trees passively
recording changes in their geochemical environment. Lead
was analyzed as an element with an approximately known
long-term pollution history in North America, with an
increasing input function during the twentieth century that
has been recorded in tree-rings with some success (Watmough, 1997, 1999; Watmough et al., 1998).
The carbon isotopic composition of cellulose in tree-rings is
affected by both the δ13C value of atmospheric CO2 and
physiological functioning of the tree (Farquhar et al., 1982;
O'Leary et al., 1992; Lajtha and Marshall, 1994; Panek and
Waring, 1997). Atmospheric CO2 concentration has been
increasing while its δ13C value has been decreasing since
1750, due primarily to the combustion of fossil fuels (Freyer,
1979; Freyer and Belacy, 1983; Leavitt and Long, 1989; O'Leary
et al., 1992; Lajtha and Marshall, 1994; February and Stock,
1999). Farquhar et al. (1982) modeled the δ13C value of plant
tissue with respect to atmospheric CO2 for C3 plants and found
the plant δ13C values were controlled by photosynthetic
pathway, diffusion related fractionation, and the ratio of the
partial pressure of CO2 inside the leaf to atmospheric CO2.
When stressed, decreases in stomatal aperture can occur
(Kozlowski and Pallardy, 1997). This decreases isotopic fractionation resulting in higher tree-ring δ13C values (Freyer,
1979; Martin and Sutherland, 1990; O'Leary et al., 1992; Lajtha
and Marshall, 1994; Panek and Waring, 1997; Sakata and
Suzuki, 2000; Savard et al., 2002). As a result, positive
deviations in tree-ring δ13C values from the long-term trend
of decreasing δ13C values of atmospheric CO2 were used
indicate periods of stress.
This study is divided into three parts: (1) an examination of
changes in tree-ring elemental concentration during periods of
stress, (2) an examination of the relationship among tree-ring
concentrations, site characteristics and soil leachate concentrations, and (3) an assessment of the cohesiveness of sitenormalized long-term non-nutrient elemental trends in treerings from sites with multiple trees analyzed. Together these data
are used to assess whether tree-ring elemental concentrations
passively record changes in their geochemical environment.
We characterize periods of stress in individual red oak
(Quercus rubra) and white oak (Quercus alba) based on increases
in δ13C values in cellulose of tree-rings from trees at sites
proximal and distal to urban areas in Ontario, Canada. Treering elemental concentrations during these periods of stress
are compared to long-term trends to assess the extent to
which variations in tree-ring chemistry may be physiological
responses to stress. Tree-ring elemental concentrations were
also considered with respect to soil characteristics such as soil
pH and leachable concentrations of each element. Comparing
tree-ring elemental concentrations to soil characteristics
examines the extent to which recent tree-ring chemistries
reflect soil characteristics and potentially may be reconstructed using historic tree-ring chemical compositions. In
addition, the normalized long-term trends in elemental
concentrations from multiple red oaks at three sites across
Southern Ontario were compared to examine whether the
normalization would be informative in developing sitespecific and regional chronologies.
2.
Materials and methods
Red and white oak trees were sampled at six sites across
Southern Ontario, Canada (Fig. 1). These sites were selected to
cover a broad range of soil and bedrock types as well as varying
distances from urban pollution sources such as Hamilton,
Toronto and Sudbury (Fig. 1 and Table 1). Forests at each site
are mixed coniferous and deciduous remnant second growth
stands. The sites are all located within the natural range for
red and white oak, and while not the dominant species at
every stand, they are abundant. When possible, white oak was
sampled preferentially to red oak because it has preferred
characteristics for dendrochemical analysis (Cutter and Guyette, 1993). Red oak is less preferred due to higher heartwood
permeability and moisture content (Cutter and Guyette, 1993).
Between three and ten dominant, visibly healthy trees
were sampled at each site for potential chemical analysis.
From each tree, eight cores were taken, two from each of four
positions located at 90° intervals around the tree at breast
height. Cores were taken using a 5 mm diameter increment
corer. The corer was washed with ethanol followed by
deionized water between trees and rinsed with deionized
water between cores from the same tree. From these sampled
trees, one to three trees from each site were selected for
chemical analysis after an examination of the extracted core.
Additional trees were sampled at each site for cross-dating
purposes. These cores were air-dried, mounted and sanded
with increasing grit number sandpaper until individual
growth rings were easily visible. Cores from the same site
were cross-dated according to the principles of Stokes and
Smiley (1968). Distinctive ring-width patterns were identified
in the cross-dated core at the same site and used to cross-date
trees among sites prior to dissection for chemical analysis.
For isotope analysis, cores from each position sampled
around the bole were grouped and dissected into annual
growth rings. The visibly distinct earlywood and latewood
were separated in each growth ring and a sub-sample of the
latewood from every even year was taken for carbon isotope
analysis. α-Cellulose was prepared using a modification of
the technique described by Loader et al. (1997) based on
Green (1963). The carbon isotopic composition (δ13C value) of
the α-cellulose fraction was measured using an Elemental
Analyzer (EA) coupled to an Isotope Ratio Mass Spectrometer
(IRMS) operating in Continuous Flow (CF) mode. EA-CF-IRMS
analyses were performed using either a Carlo Erba NCS 2500
EA coupled to a Finnigan MAT 252 IRMS or a Costech ECS 4010
coupled to a Finnigan MAT Delta Plus XP in the Queen's
Facility for Isotope Research. The δ13C values are reported in
units of permil (‰) (Faure, 1986) relative to V-PDB. Using
these techniques, NIST-19 returned a δ13C value of 1.95‰ and
NIST-21 gave a δ13C value of − 28.1 ± 0.2‰. Replicate analyses
S CIE N CE OF T H E TOT AL E N V I RO N ME N T 3 9 0 ( 2 00 8 ) 2 7 5–2 86
277
Fig. 1 – Map of Canada with inset map of Southern Ontario showing site locations and main pollution point sources of (Hamilton,
Toronto, Sudbury). Arrows in inset indicate prevailing wind direction.
of a laboratory α-cellulose standard (δ13C = − 24.3 ± 0.3‰) and
selected samples indicate an uncertainty of 0.3‰ (2σ).
Periods of stress were characterized as sustained intervals
of elevated (N1‰) tree-ring δ13C values corrected for long-term
changes in the δ13C values of atmospheric CO2. The temporal
trend towards lower tree ring δ13C values due to the trend in
atmospheric CO2 was removed by subtracting the δ13C values
of atmospheric CO2 from the tree-ring δ13C value. Changes in
tree-ring δ13C values relative to coeval atmospheric CO2 were
compared by calculating Δδ13C values using the method of
Freyer (1979). A time interval common to all sites was selected
and the Δδ13C value was calculated as the difference between
the measured tree-ring and the average δ13C value during that
time interval. Intervals where the running average of Δδ13C
Table 1 – Summary of the physical characteristics of the sampling sites in Ontario
Site
Location
Bedrock type
Soil type
North Bay
46.35N
79.40W
Granitic Gneiss
Orthic Humo-Ferric Podzol
Lake Opinicon
44.58N
76.32W
Granitic Gneiss
Monteagle Sandy Loam Podzol
Burlington
43.28N
79.80W
Shale/Mudstone
Grey Brown Luvisol
Peterborough
44.37N
78.30W
Carbonate
Orthic Melanic Brunisol
Kingston North
44.33N
79.60W
Carbonate
Humic Gleysol
Kingston East
44.26N
76.40W
Carbonate
Grey Wooded Podzol
Soil pH (range)
4.62
(4.22–5.15)
n = 10
5.07
(4.78–5.92)
n=7
6.43
(5.78–8.27)
n = 10
7.36
(6.62–7.93)
n=9
6.87
(6.48–7.26)
n=4
5.94
(5.69–6.65)
n=3
Species
Red oak
Red oak
Red oak
Red oak
White oak
White oak
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values exceeded 1‰ were identified as periods of stress. The
onset and termination of the period of stress were defined as
the beginning and end of the interval with elevated Δδ13C
values. A change greater than 1‰ in δ13C value can be real and
significant in plants (O'Leary et al., 1992) and as a result was
chosen as a threshold value for stress definition. Sustained
intervals of stress were used rather than individual measurements when the threshold value was exceeded to examine
whether prolonged stress intervals had an effect on tree-ring
elemental concentration. Short term stresses may lead to
annual variations and appear as high frequency variability in
the elemental concentration data. The exact timing of the
onset and termination of these identified periods of stress are
not rigid and as a result render the defined periods of stress
qualitative to semi-quantitative.
Individual cores were analyzed for elemental concentrations by Laser-Ablation Inductively Coupled Plasma Mass
Spectrometry (LA-ICP-MS) as described by Kyser et al. (2003).
All analyses were done with a Finnigan MAT Element High
Resolution ICP-MS and a New Wave Research 213 nm Nd–YAG
laser. The laser was operated in line or raster mode with a
beam width of 300 μm and frequency of 20 Hz to measure each
growth ring. Counts of each element were normalized to 13C to
account for variations in ablation and transport efficiency to
the plasma. Triplicate LA-ICP-MS analyses were done on at
least three samples per tree and the results were compared to
assure sample homogeneity and analytical reproducibility.
To quantify the intensities from the LA-ICP-MS analyses,
several tree-rings from each LA-ICP-MS run (60 rings total)
were acid digested and their elemental concentrations determined by solution ICP-MS. Samples for solution ICP-MS
analysis were selected to cover the widest range of machine
response by LA-ICP-MS for the greatest number of elements. In
a class-100 clean room, 0.020 to 0.100 mg of wood, all of the
latewood remaining in the ring after LA analysis, was sealed in
an acid washed Savillex container with 1–2 mL of high purity
concentrated nitric acid. The container was placed on a hot
plate (80 °C) for 3 days, five drops of ultra pure hydrogen
Fig. 2 – a) Non-stressed tree from North Bay (red oak); b) Stressed tree from Lake Opinicon (red oak). The top row of figures is the
carbon isotope (Δδ13C values), middle row is nutrients, and bottom row is non-nutrients. Hatched lines indicate the heartwood–
sapwood boundary in each tree. Stressed time interval is indicated as a filled box.
S CIE N CE OF T H E TOT AL E N V I RO N ME N T 3 9 0 ( 2 00 8 ) 2 7 5–2 86
peroxide added, and placed back on the hot plate for an
additional day. Once clear, the solutions were evaporated to
dryness in a laminar flow fume-hood and re-dissolved in 2%
HNO3 with a 1 ppb indium internal standard. Analysis of
standards and duplicates indicate a relative error of b5% for
most elements. The concentrations measured by solution ICPMS were used to generate a 13C-normalized ion count per unit
concentration for each element analyzed for each day of LA
analysis. Individual conversion figures and equations were
developed as in Watmough et al. (1998) and were plotted for
each element in each core for each day run. Using the
individual conversion equations, replicate laser-determined
concentrations were within 20% for all the elements measured.
The elemental concentrations were highly specific to
individual trees (Figs. 2–4). Therefore, it became clear that
comparing trends was of more interest than absolute elemental concentrations.
To evaluate common temporal trends in the elemental
concentrations of tree-rings for several trees from a specific
site, we developed a normalization technique wherein an
index value between 0 and 1 was calculated for each tree-ring
for the time period common among all trees sampled at that
site. For example, if three trees from one site covered the time
periods 1860–1998, 1920–2004 and 1910–2000, the common
time period for all three trees is 1920–1998. For each tree, the
highest concentration measured in the tree-rings from 1920–
1998 was assigned an index value of 1, the lowest a value of 0,
and the rest were given values between 0 and 1 scaled to their
relative concentration using the following equation:
Index value for year xðIx Þ
¼ ðconcx conclowest Þ= conchighest conclowest
ð1Þ
The calculated index value (Ix) for each tree-ring within the
common time period at the site will be between 0 and 1 and
those outside the common time period may be outside that
range. Normalizing each core to a dimensionless unit also has
the advantage that if the entire core is measured in a single
laser ablation run without changing tune parameters and
results are 13C-normalized to account for variations in ablation
efficiency, the data need not be converted to concentrations
prior to calculating index values.
At each site, 3 to 10 soil samples were taken from the top
5 cm of the A-horizon. The samples were air-dried in a fumehood, organic debris was manually removed and the soil was
passed through a 2 mm sieve. Soil pH was measured in a 1:1
soil/water slurry (Table 1). Leachable element concentrations
in the soils were determined using a modification of the
method described in Holk et al. (2003), wherein 0.5 g of soil and
5 mL of 2% HNO3 spiked with indium were placed in an
ultrasonic bath for 2 h, centrifuged and the supernatant
analyzed by ICP-MS. Such a harsh treatment was chosen to
extract the highest concentration of elements possibly available to the tree. This fraction would include most soluble
minerals as well as elements bound to amorphous oxides and
humic matter.
The strength of the relationships between soil pH, leachate
and tree-ring elemental concentration was examined by linear
regression in Microsoft Excel.
3.
279
Results
Periods of stress were identified in all but one red oak from the
North Bay site (Figs. 2–4). The periods of stress and the average
δ13C value during the common interval among sites (1918 to
1930) and within the Burlington site (1936 to 1998) are
summarized in Table 2.
3.1.
Comparison of tree-ring elemental concentrations in
the non-stressed and most stressed trees
A red oak from North Bay does not record any prolonged
periods of stress in its tree-ring Δδ13C values (Fig. 2a-i). The
most pronounced change in nutrient concentrations in this
tree occurs at the heartwood–sapwood transition, with a
smaller change in non-nutrient element concentrations
(Fig. 2a-ii and iii). There are shifts in Pb concentration
independent of stress and in 1988 there is a spike in all
elemental concentrations. In the heartwood of the nonstressed tree from North Bay, temporal trends in nutrient
contents are similar to those of non-nutrients (Fig. 2a-ii and iii).
The Δδ13C values in red oak from the Lake Opinicon site
record a period of stress from 1940 to 1976 (Fig. 2b-i). These
time intervals coincide with abrupt increases in the concentrations of nutrients Ca, Mn and Mg (Fig. 2b-ii). A concomitant
increase in non-nutrient element concentrations during this
period of stress is not observed, rather the tree-rings have Ba,
Sr, and Pb concentrations that steadily increase after 1920
(Fig. 2b-iii). That there is no abrupt change in the concentrations of non-nutrients suggests the increase in nutrient
concentrations represent a physiological response, rather
than a change in geochemical conditions in the soil.
3.2.
Stress coincident elemental variations in tree-rings
During the period of stress in a red oak from Burlington (1946 to
1960; Fig. 3a-i) there is a decrease in Ca and Mn concentration
(Fig. 3a-ii) unmatched by systematic changes in non-nutrient
concentrations (Fig. 3a-iii).
A second red oak from Burlington has two periods of stress,
1934 to 1938 and 1946 to 1958 (Fig. 3b-i). During the first period
of stress the concentration of Ca increases and Mn decreases
(Fig. 3b-ii) while the concentrations of non-nutrients Ba and Sr
both increased (Fig. 3b-iii). During the second period of stress,
overlapping spikes in Ca, Ba, Sr and Pb concentrations occur
(Fig. 3b-ii and iii). Therefore, during both periods of stress in
this tree there are shifts in the nutrient and non-nutrient
concentrations.
Nutrient and non-nutrient trends in the white oak from the
Kingston East site have similar features during the period of
stress from 1932 to 1966 (Fig. 3c). During the period of stress both
the Ca and Sr concentrations reach their lowest values and
begin to increase after the period of stress ends (Fig. 3c-ii and iii).
Also, there are concomitant increases in Mn and Pb concentrations during the period of stress (Fig. 3c-ii and iii). Like the
second red oak from Burlington (Fig. 3b), the white oak from the
Kingston East site is recording similar shifts in both nutrient and
non-nutrient concentrations during periods of stress. During a
non-stressed interval between 1878 and 1896 in the Kingston
280
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Fig. 3 – Stressed trees with elemental concentration shifts during period of stress from a) Burlington (red oak Burl4); b) Burlington (red oak Burl2); and c) Kingston East (white oak).
The top row the figures is carbon isotope (Δδ13C values), middle row is nutrients, and bottom row is non-nutrients. Hatched lines indicate the heartwood–sapwood boundary in
each tree. Stressed time interval is indicated as a filled box.
S CIE N CE OF T H E TOT AL E N V I RO N ME N T 3 9 0 ( 2 00 8 ) 2 7 5–2 86
Fig. 4 – Stressed trees without elemental concentration shifts during period of stress from a) Peterborough (red oak); b) Burlington (red oak Burl3); c) Kingston North (white oak).
The top row the figures is carbon isotope (Δδ13C values), middle row is nutrients, and bottom row is non-nutrients. Hatched lines indicate the heartwood–sapwood boundary in
each tree. Stressed time interval is indicated as a filled box.
281
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SC IE N CE OF T H E TOT AL E N V I RO N ME N T 3 9 0 ( 2 00 8 ) 2 7 5–2 86
Table 2 – Average δ13C values during normalization
periods for Δδ13C values and periods of stress
δ13C value (‰;
V-PDB) Avg.
1918–1930
Tree
Burlington 2
Burlington 3
Burlington 4
North Bay
Lake
Opinicon
Peterborough
Kingston
North
Kingston
East
− 22.9
− 24.1
− 24.7
δ13C value (‰;
V-PDB) Avg.
1936–1998
Period of
stress
−23.0
1934–1938
1946–1958
1956–1968
1946–1960
None
1940–1976
−22.6
−23.3
− 23.7
− 25.2
1932–1946
1952–1976
− 25.1
1932–1966
East white oak there are elevated nutrient (Ca, Mn and Mg) and
non-nutrient (Ba and Sr) concentrations (Fig. 3c-iii).
3.3.
No stress coincident variations in tree-rings elemental
concentration
While all three trees in Fig. 4 have periods of stress, in each
case the threshold Δδ13C value of 1‰ is not greatly exceeded
(Fig. 4a-i, b-i and c-i; Table 2). In particular, the Δδ13C in both
the third red oak from the Burlington site (Fig. 4b) and the
white oak from the Kingston North site (Fig. 4c) both have
prolonged periods between 1950 and 1980 where the Δδ13C
value is elevated near, but not exceeding the threshold value.
Any systematic shifts in elemental concentration related to
stress are not as clear in the three trees in Fig. 4 as they are in
the Lake Opinicon red oak (Fig. 2b).
After the period of stress in the Peterborough red oak
(Fig. 4a) there is a concomitant increase in the Ca and Sr
concentrations from 1950 to 1980, although the shift in Sr
concentration is much smaller (Fig. 4a-ii and iii). Indeed the
long-term Ca and Sr trends are similar to one another in both
the red oak from Burlingon (Fig. 4b-ii and ii) and the white oak
from Kingston North (Fig. 4c-ii and iii).
3.4.
Soil leaches
Elemental concentrations in soil leachates potentially reflect
the amount available for uptake by trees. The highly individualistic behavior of trees with respect to total elemental
concentrations (Figs. 2–4) and uptake, and possible relationships
between heartwood and sapwood concentration confound a
rigorous statistical treatment of soil chemistry here. Instead a
qualitative examination of common features was done.
Soils developed on carbonate bedrocks at Peterborough,
Kingston North and Kingston East have higher pH and leachate
Ca and Sr concentrations than low pH soils developed on
granites at North Bay and Lake Opinicon (Fig. 5). High Ca and Sr
concentrations in the soils are also reflected in relatively high Ca
and Sr concentrations in the tree-rings. Calcium has higher
concentrations in sapwood relative to heartwood concentrations, with the difference being more pronounced in trees over
soils with high pH on carbonate bedrock (Fig. 5a). In all but the
tree from Kingston East (pH = 5.94), heartwood and sapwood Sr
concentrations are equivalent (Fig. 5b).
Magnesium and Mn are both nutrients and are higher in
concentration in sapwood relative to heartwood at all sites.
Concentrations of Mg in soil leaches, like those of Ca and Sr,
are higher in soils over carbonate bedrock sites and with
higher soil pH, but sapwood Mg concentrations are similar at
all sites, as are heartwood Mg concentrations (Fig. 5c). In
contrast, soil leaches have similar Mn concentrations at all
sites whereas low soil pH sites generally have higher Mn
concentrations in both their sapwood and heartwood (Fig. 5e).
Heartwood and sapwood concentrations are similar for both
non-nutrient elements Ba and Pb at all sites (Fig. 5d and f). With
the exception of the low pH site at North Bay that has elevated
Ba concentrations in the soils, leachate concentrations of Ba are
similar across the soil pH range of the sites sampled (Fig. 5d).
However, tree-ring Ba concentrations vary with soil pH, with the
highest concentrations on acidic soils. A linear regression of Ba
concentration as a function of soil pH for the five sites with soil
pHb 7 has an r2 = 0.85 for heartwood, an r2 = 0.83 for sapwood,
whereas soil leach concentrations have an r2 = 0.30. This
suggests Ba concentrations in tree-rings may be related to soil
pH and not soil leachate concentration. Concentrations of Pb in
the tree-rings also increase with decreasing pH and do not vary
directly with Pb concentrations in the soils (Fig. 5f).
3.5.
Long-term trends in non-nutrients
Normalized index values were calculated for non-nutrients
(Ba, Sr, Pb) from three trees sampled at Lake Opinicon, North
Bay and Burlington (Fig. 6). Two of the three trees at Lake
Opinicon have Ba and Sr tree-ring concentrations that have
increased since 1940 whereas the third tree records decreasing
Ba and Sr concentrations with time (Fig. 6a). All three trees
have similar long-term Pb concentration trends towards
higher concentrations since 1940 (Fig. 6a).
Two trees from the North Bay site have identical temporal Ba
index values, with a trend of decreasing values expected for most
cations (Momoshima and Bondietti, 1990) until 1980, when the
values increase (Fig. 6b). Index values for Sr similarly decrease
until 1980 when they too increase (Fig. 6b). Two of the three trees
have similar long-term trends towards higher Pb concentrations
since 1940 and the third is consistent with the others until 1988,
when the concentrations abruptly decrease (Fig. 6b).
Trees from Burlington display the least temporal agreement among samples, except for Ba values which follow the
long-term cation trend (Momoshima and Bondietti, 1990)
(Fig. 6c). The Sr values are highly variable with no common
temporal trend and Pb shows no distinct increase in concentration (Fig. 6c) despite the proximity to multiple point sources
of pollution of this site (Fig. 1).
4.
Discussion
Environmental factors including climate, disease, pestilence and
pollution can stress trees and affect carbon isotope compositions
(Freyer, 1979; Martin and Sutherland, 1990; O'Leary et al., 1992;
Lajtha and Marshall, 1994; Panek and Waring, 1997; Sakata and
S CIE N CE OF T H E TOT AL E N V I RO N ME N T 3 9 0 ( 2 00 8 ) 2 7 5–2 86
283
Fig. 5 – Elemental concentrations in tree-rings and soil leachate concentrations plotted against soil pH for a) Ca, b) Sr, c) Mg, d) Ba,
e) Mn and f) Pb. Legend for all panels is in the bottom right panel. From left to right on each panel, the sites are North Bay, Lake
Opinicon, Kingston East, Burlington, Kingston North and Peterborough.
Suzuki, 2000; Savard et al., 2002). Significant positive deviation in
carbon isotopic composition can be used to define a period of
stress but cannot establish the cause of the stress. As a result,
variation in elemental concentration during these periods of
stress may be directly recording the effect of the stressor in the
geochemical environment, or may be recording a change in
elemental uptake as a result of change in physiology.
During periods of stress in some trees, nutrient concentrations in tree-rings become erratic, differing from long-term
temporal trends of non-nutrients (Figs. 2b and 3a). This was
particularly evident in the tree from Lake Opinicon (Fig. 2b). In
this tree, the periods of stress are coincident with concentration
increases in nutrients that are not shared by non-nutrient
elements (Fig. 2b). These observations are consistent with
stress-induced physiological changes in nutrient uptake or
allocation occurring within the tree. In some instances, such as a
red oak from Burlington (Fig. 3b) and a white oak from Kingston
East (Fig. 3c), the stress-coincident shifts in nutrient concentration are accompanied by shifts in non-nutrient concentration,
consistent with the stressor affecting the geochemical environment. In the Kingston East tree (Fig. 3c), there are concomitant
shifts in nutrients and non-nutrients during a non-stressed
interval (1878 to 1896). In other trees, there are no systematic
shifts in elemental concentration coincident with periods of
stress (Fig. 4). This may be due to chronic stress or may indicate
that the level of stress is not sufficient to affect the physiological
functioning of the tree or geochemical environment. Therefore,
unless it is established that a tree is non-stressed, tree-ring
nutrient concentrations cannot be considered exclusively
passive monitors of elemental bioavailability.
Differences between nutrient and non-nutrient behavior
are more pronounced in tree-rings than in soil leachate
concentrations or soil pH differences. With the exception of
Ca concentrations at the low pH granitic sites (Fig. 5a),
284
SC IE N CE OF T H E TOT AL E N V I RO N ME N T 3 9 0 ( 2 00 8 ) 2 7 5–2 86
Fig. 6 – Normalized non-nutrient concentrations (Pb top, Ba middle and Sr bottom row) for three trees from a) Lake Opinicon; b) North Bay; and c) Burlington.
S CIE N CE OF T H E TOT AL E N V I RO N ME N T 3 9 0 ( 2 00 8 ) 2 7 5–2 86
sapwood has higher nutrient concentrations than heartwood
regardless of soil pH or leachate concentration (Fig. 5a, c and
e). Calcium and Mg have higher soil leachate concentrations
above carbonate bedrock (Fig. 5a and c), and this appears to be
reflected in elevated Ca concentrations in tree-ring concentrations (Fig. 5a). In contrast, Mg concentrations in tree-rings
seem unrelated to soil leachate concentration or soil pH, with
heartwood Mg concentrations generally low and comparable
among sites, and sapwood Mg concentrations are high and
comparable among sites (Fig. 5c). Both Ca and Mg concentrations in sugar maple tree-rings were shown to be related to soil
leachate concentration (Watmough, 2002). The lack of relationship between soil leachate concentration and tree-ring
concentration of Mg suggests oak tree-rings do not passively
record the amount of this element available in the soil for
uptake; rather is controlled by the physiology of the tree.
Tree-ring Mn concentrations follow a pattern opposite that
of Mg. Soil leachate Mn concentration is similar among sites, but
tree-ring Mn concentrations vary with soil pH (Fig. 5e). Higher
tree-ring Mn concentrations occur in soils with low pH,
suggesting that soil pH affects tree-ring Mn concentrations, as
has been reported in previous studies (Watmough, 1997, 2002).
However, attempting to develop chronologies of soil pH using
tree-ring Mn concentration might be hampered by potentially
high radial mobility of Mn (Cutter and Guyette, 1993) and a
strong physiologically-controlled trend seen for nutrients in oak
with a decrease to the heartwood–sapwood boundary followed
by an increase to the outermost sapwood ring (Figs. 2–4).
Concentrations of Pb in oak tree-rings seem more related to
soil pH than soil leachate concentrations or bedrock type
(Fig. 5f), similar to previous observations in sugar maple
(Watmough, 2002). Soils with low pH have higher tree-ring Pb
concentrations than do soils with higher pH, independent of
leachate concentration. There is excellent agreement among
temporal trends in Pb concentrations in the three trees analyzed
at Lake Opinicon (Fig. 6a), a site distal to urban areas of Southern
Ontario, but with soils having low pH. Increasing Pb concentrations in these trees begin in 1940 and continue until the mid1990s, and the good agreement among trees suggests it may be
recording a site-wide process. Two of the three trees sampled at
North Bay, also a site with soils of low pH (Table 1), have
temporal Pb concentration trends similar to those at Lake
Opinicon. The third tree at North Bay shows the same trend
until 1988, when the concentration suddenly decreases (Fig. 6a
and b). The cause of this intriguing decrease is not clear. In
contrast, the high variability and lack of agreement among treering Pb concentration trends at the Burlington site (Fig. 6c)
suggest that either the circum-neutral soil pH is making the site
unsuitable for developing tree-ring based Pb pollution histories
or competing processes at the site are causing a variable signal
to be recorded. Proximity of the Burlington site to pollution
sources likely resulted in the relatively high soil leachate Pb
concentrations, but this is not reflected in tree-ring Pb
concentrations (Fig. 6f). The low radial mobility of Pb (Cutter
and Guyette, 1993) suggests tree-ring Pb concentrations can be
used to reconstruct site-wide changes in geochemical processes, but concentration trends may be complicated by soil pH.
Tree-ring Ba concentrations seem independent of bedrock
type or soil leachate concentration, but are inversely related to
soil pH (Fig. 5d), and thus may record an environmental signal.
285
For example, barium concentrations in trees measured at the
Lake Opinicon site, with low soil pH, have increasing or
constant trends since 1950 (Fig. 6a). The inverse correlation
between tree-ring Ba concentrations and soil pH (Fig. 5d)
suggests the temporal trend in these trees may be recording
the well-documented increased acid deposition in Canada
throughout the second half of the twentieth century (Environment Canada, 2004). Momoshima and Bondietti (1990)
demonstrated that tree-rings behave like ion exchange
columns with the number of binding sites per ring decreasing
radially from the pith. This can result in a trend of decreasing
tree-ring cation concentration from pith to outer most growth
ring, as is seen in the tree-ring Ba concentrations of the
Burlington trees (Fig. 6c). Tree-ring Ba concentrations at North
Bay similarly decrease outwards from the pith until 1960 when
concentrations increase (Fig. 6b). This may indicate a change
in Ba availability, possibly related to increased acid deposition
since 1960 (Fig. 6b). Given the low radial mobility of Ba (Cutter
and Guyette, 1993), tree-ring Ba concentration may be used to
reconstruct historic changes in soil pH or acidic deposition.
Barium and Sr are both alkaline earth elements and their
similar chemical behavior is likely responsible for the similarity
of their temporal trends at both the Lake Opinicon and North Bay
sites (Fig. 6a and b). However, the agreement among temporal Sr
concentration trends is not as good as for Ba at both sites. Lower
soil leachate Sr concentrations and a lack of relationship
between soil pH and tree-ring Sr concentration (Fig. 6b) may
have combined to make tree-ring Sr concentration shifts less
sensitive to environmental changes than Ba at Lake Opinicon
and North Bay. The lack of a common trend of Ba and Sr in trees
from Burlington is consistent with no site-wide environmental
change recorded in tree-ring Sr concentrations. The use of a site
normalization procedure for tree-ring elemental concentration
allows for the examination of potential site-wide responses to
environmental change recorded by tree-rings.
Changes in nutrient concentration can be examined in treerings, but without knowledge of the stress-status of the tree, any
changes not matched by chemically similar non-nutrients may
be due to physiological stress in the tree. The effects of stress on
tree-ring elemental concentrations may be partially mitigated
by analyzing multi-year segments of the tree rather than
individual rings. The potential effect of stress on elemental
concentration would be averaged over the segment and
minimized. The potential effect of stress and site characteristics
on tree-ring chemistry suggests that background or control trees
should be selected from sites that are as similar to the study area
as possible, differing in only the single variable being examined
such as in Witte et al. (2004) and Sheppard et al. (2007).
Replication will help establish the veracity of any temporal
patterns observed. Our results suggest that normalizing concentrations to a dimensionless index value can be useful in
detecting common patterns among trees even when absolute
concentrations are quite different.
5.
Conclusions
While nutrient concentrations in tree-rings from oak may be
used in pollution studies, they must be used with caution as
concentrations can be affected by physiological stress unrelated
286
SC IE N CE OF T H E TOT AL E N V I RO N ME N T 3 9 0 ( 2 00 8 ) 2 7 5–2 86
to the pollution. Non-nutrient concentrations are minimally
affected by physiological stress, but tree-ring concentrations can
be complicated by the interplay of site and soil characteristics in
addition to environmental change or pollution. Site characteristics such as soil pH, bedrock and soil type and stress history of a
tree should be taken into consideration when designing a
dendrogeochemical study of environmental change.
Acknowledgments
We are grateful to Don Chipley, April Vuletich and Kerry
Klassen at QFIR for their analytical and technical assistance.
This project was supported by OGS and Queen's University
Scholarships to A.R.B., and funding and support from NSERC
Discovery and MFA grants, Canadian Foundation for Innovation and Ontario Innovation Trust grants to T.K.K.
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