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Published online 15 February 2008
Published in Soil Sci Soc Am J 72:500-506 (2008)
DOI: 10.2136/sssaj2007.0052N
© 2008 Soil Science Society of America
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SOIL CHEMISTRY NOTE

Sample Pretreatment Affects the Distribution of Organic Carbon in Aggregates of Tropical Grassland Soils

Sonja Paula,*, Guntars O. Martinsona, Edzo Veldkampa and Heiner Flessab

a Buesgen Institute, Soil Science of Tropical and Subtropical Ecosystems, Georg-August Univ. of Goettingen, 37077 Goettingen, Germany
b Buesgen Institute, Soil Science of Temperate and Boreal Ecosystems, Georg-August Univ. of Goettingen, 37077 Goettingen, Germany

* Corresponding author (spaul1{at}gwdg.de).


   ABSTRACT
TOP
 NOTES
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Soil aggregation is an important mechanism for the stabilization of soil organic C (SOC). The distribution of SOC among aggregate classes depends on sample pretreatment and on the applied method of aggregate fractionation. We examined the effect of soil pretreatment (air-dried vs. field-moist soil) on the yield and SOC content of aggregate size fractions (8000–2000, 2000–250, 250–53, and <53 µm). Aggregate size fractions were separated by wet sieving tropical soils of different parent material and mineralogy (volcanic ashes dominated by short-range-order aluminosilicates and marine Tertiary sediments dominated by smectitic clays), which were used as pastures for 13 to 50 yr after deforestation. In addition, the proportion of pasture- and forest-derived SOC in the aggregate fractions was determined using the 13C/12C isotope ratio. In volcanic ash soils, there was no clear effect of soil pretreatment on the distribution of aggregates into aggregate size classes. Furthermore, the SOC concentration and proportion of pasture-derived SOC of aggregates within each size class did not differ across treatments. In smectitic clay soils, however, the two pretreatments resulted in distinct differences in the distribution of dry matter yield and also of SOC among the aggregate fractions. Wet sieving of dry soil led to a separation of macroaggregates rich in pasture-derived SOC, whereas wet sieving of moist soil isolated microaggregates with high contents of pasture-derived SOC. This implies that soil organic matter plays a major role in both the formation and the stabilization of macroaggregates and in the early stage of microaggregate formation in sedimentary soils but not in volcanic ash soils.

Abbreviations: MWD, mean weight diameter • SOC, soil organic carbon.


   INTRODUCTION
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
SOIL AGGREGATION can decrease the accessibility of enzymes to substrate and thus contributes to the physical protection of SOC (Sollins et al., 1996). Several methods have been developed to fractionate soil into different aggregate size classes. Their results depend on water content in the field, sample pretreatment, and the sieving procedure (Gollany et al., 1991; Christensen, 1996; Beare and Bruce, 1993; Six et al., 2000b; Ashman et al., 2003). The most widely used approach to separate aggregate size classes is rapid immersion of air-dried samples in water with subsequent wet sieving of the soil (Kemper and Rosenau, 1986). When air-dried aggregates are rapidly immersed in water, water enters the pores of the aggregates and air gets trapped inside the aggregate. Increasing pressure may destroy the aggregate and air bubbles emerge, a process called slaking (Kemper and Rosenau, 1986). In addition, the combination of wet sieving of air-dried and rewetted soil is used to separate stable and unstable aggregates (Six et al., 2000b; Denef et al., 2002). Several methods have been suggested to rewet soil before aggregate size fractionation: rewetting by tension, vapor, under vacuum, or capillary wetting to field capacity plus 5% (Kemper and Rosenau, 1986; Beare and Bruce, 1993; Puget et al., 1995; Le Bissonnais, 1996; Six et al., 1998). Differences between these rewetting methods are comparatively small compared with the large differences found between rewetted and air-dried slaked treatments (Beare and Bruce, 1993). In temperate climate soils, wet sieving of air-dried and slaked soil is considered to be the most appropriate procedure to separate aggregate size classes that differ in SOC storage and stability (Puget et al., 1995; Six et al., 2000a).

Tisdall and Oades (1982) formulated the hypothesis that stable microaggregates (<250 µm) are bound together into larger units (macroaggregates, >250 µm) by labile organic material. This concept, which they called "soil aggregate hierarchy," was supported by subsequent studies that showed that macroaggregates had higher SOC contents, contained less decomposed organic material, and had faster SOC turnover than microaggregates in temperate climate soils with 2:1 clays (Jastrow et al., 1996; Six et al., 2002; John et al., 2005). This concept of aggregate hierarchy, which relies on organic matter as the main binding agent, may not be suitable for heavily weathered tropical soils with 1:1 clays or for volcanic ash soils, as in these soils rich in Fe and Al oxides, formation of aggregates by mineral–mineral bindings is more important (Oades and Waters, 1991; Hoyos and Comerford, 2005; Schwendenmann and Pendall, 2006). In addition, sample pretreatments like air drying can induce an irreversible flocculation in volcanic ash soils (Churchman and Tate, 1987; Wells and Theng, 1988). Studies determining the effect of drying on aggregate size distribution in volcanic ash soils are rare (Churchman and Tate, 1987), however, and its influence on the partitioning of SOC among aggregate classes is not clear.

The objective of our study was to determine the effect of sample pretreatment (air-dried vs. field-moist soil adjusted to 75% of field capacity) on: (i) the distribution of aggregate size fractions in different tropical pasture soils (volcanic ash soils dominated by short-range-order aluminosilicates and marine Tertiary sedimentary soils with smectitic clays); (ii) the distribution of total SOC among aggregate classes; and (iii) the proportion of recently incorporated SOC from pasture vegetation in aggregate size fractions.


   MATERIALS AND METHODS
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Sites and Soils
We selected four sites in northwest Ecuador with different soil textures and parent materials: two soils were developed on marine Tertiary sediments (Chonta Duro, a Haplustept, and Tazones, a Paleustalf) and two sites had soils developed from volcanic ashes (Maquipucuna and Pedro Viciente, both Hapludands; Soil Survey Staff, 1998). As the determination of clay content for allophane-containing soils reveals ambiguous results due to incomplete dispersion, we did not determine the clay content of the volcanic ash soils (Nanzyo et al., 1993). X-ray diffraction of the clay fraction of the sedimentary soils revealed that they were dominated by smectite with marginal contributions of illite, chlorite, and kaolinite. None of the investigated sites contained inorganic C. At each site, we selected a pasture plot dominated by C4 grasses and a natural forest plot as a C3 reference. Pasture plots had been established after cutting and burning natural forest. Natural forest plots with similar overall environmental characteristics of the pasture plots were selected as close as possible. The duration of the pasture period was 35 yr for both sedimentary soils, 50 yr for Maquipucuna, and 13 yr for Pedro Viciente. The duration of the pasture period influences the amount of pasture-derived SOC in soils. This has to be taken into account when comparing absolute amounts of pasture-derived SOC in different soils or comparing calculated turnover rates of SOC (Feigl et al., 1995). We evaluated the effect of pretreatment on SOC distribution among aggregate fractions for the same soils and we compared only relative differences of pasture-derived SOC between different soils. This data evaluation is not biased by the duration of the pasture period. Four soil samples (depth: 0–0.1 m, 0.09 m2) and root samples were taken at each site. Selective dissolution of all soil samples was done using acid ammonium oxalate extraction of Al, Fe, and Si, dithionite–citrate extraction of Fe, and pyrophosphate extraction of Al (Buurmann et al., 1996). Iron, Al, and Si concentrations in these extracts were measured by inductively coupled plasma emission spectroscopy (flame ICP, Spectro Analytical Instruments, Kleve, Germany). General soil properties of the plots are summarized in Table 1 .


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  		Table 1. Location and general site characteristics of the pasture soils. All values expressed as mean, with SD in parentheses, except pH, which is based on the soil profile (n = 1).

 
Aggregate Fractionation
Before wet sieving, field-moist samples were carefully broken into aggregates <8000 µm by hand. Initial gravimetric moisture content was 68 ± 15% for sedimentary soils and 75 ± 9% for volcanic ash soils (mean ± standard deviation). One subsample was air dried and one subsample was adjusted to 75% of the maximum field capacity by air drying or adding distilled water. Maximum field capacity was determined by saturation of the soils with distilled water and a subsequent draining of water until no further loss of water was measured (Schachtschabel et al., 1998). Fractionation of water-stable aggregates was done following Elliott (1986) in four size classes (8000–2000, 2000–250, 250–53, and <53 µm). In brief, a soil sample (equivalent to 100 g air-dried soil was used for both treatments) was submersed in distilled water for 5 min on top of a 2000-µm sieve and the sieve was manually moved 3 cm up and down 50 times. Aggregates of 8000 to 2000 µm were collected and sieving was repeated with sieves of 250 and 53 µm. Sand content (particles >53 µm) was determined in subsamples of all aggregate classes >53 µm by dispersion with sodium pyrophosphate and wet sieving at 53 µm. Organic C content of the aggregates is expressed as SOC in sand-free aggregates (Elliott et al., 1991). The relative contribution of SOC stored in an aggregate size class to the total SOC content of the bulk soil (F, in %) was calculated as follows:

Formula 1[1]
where Cagg is the absolute amount of SOC stored in an aggregate size fraction of 1 kg bulk soil (g kg–1) and Cbulk represents the amount of SOC stored in 1 kg bulk soil (g kg–1).

The mean weight diameter (MWD) of water-stable aggregates was calculated as:

Formula 2[2]
where Formula 2 is the mean diameter of each size fraction, and wi is the proportional weight of the corresponding size fraction (Kemper and Rosenau, 1986).

Amount and Proportion of Pasture-Derived Carbon
Carbon content was measured with a total C and N analyzer (Heraeus Elementar Vario EL, Hanau, Germany) and the 13C/12C isotope ratio was measured using an isotope ratio mass spectrometer (Finnigan MAT, DELTAplus, Bremen, Germany). The 13C/12C isotope ratios are expressed as {delta}13C values:

Formula 3[3]
with Rsam = 13C/12C isotope ratio of the sample and Rstd = 13C/12C isotope ratio of the reference standard V-PDB (Vienna PeeDee Belemnite). The proportion of SOC derived from pasture vegetation (C4–SOC) was calculated from the 13C abundance of samples from pasture and reference sites according to Balesdent and Mariotti (1996):

Formula 4[4]
where f is the proportion of soil C4–SOC, {delta}sam is the measured {delta}13C ({per thousand}) value of the pasture topsoil sample, {delta}ref is the {delta}13C value of the corresponding sample from forest soil, and {delta}pasture and {delta}forest are the {delta}13C values of roots from pastures and forests, respectively. The {delta}13C value of the roots from all pastures and forests differed by 15.5 ± 1.4{per thousand}. We used the {delta}13C values of roots for this calculation because all A horizons under pasture were intensively rooted and we assume that the pasture-derived SOC in these horizons originated mainly from grass roots. The contribution of pasture-derived SOC to total SOC in the soil aggregate size fractions was used to evaluate the partitioning of young pasture-derived SOC among different aggregate size classes.

Statistics
The significance of differences among aggregate size fractions was assessed by ANOVA and post hoc Fisher's LSD at P ≤ 0.05. Differences between treatments were tested with a paired t-test at a significance level of 0.05 with the STATISTICA 6.1 software package (StatSoft, Tulsa, OK).


   RESULTS
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Sample Pretreatment and Aggregate Size Distribution
For the sedimentary soils, pretreatment affected the distribution of dry matter yield of different aggregate size classes. Air drying and slaking of soil before the sieving procedure reduced the proportion of large macroaggregates (8000–2000 µm) by about 50%, whereas the proportion of small macroaggregates (2000–250 µm) and microaggregates (250–53 µm) increased (Table 2 ). The proportion of the fraction <53 µm that consisted of the smallest microaggregates and fine nonaggregated mineral particles was smaller for the moist pretreatment (4%) than for the air-dried pretreatment (13–16%). Large macroaggregates were the dominant aggregate size fraction (60–74%) of the moist pretreatment, whereas small macroaggregates were the most important fraction of the air-dried pretreatment. The MWD of soil aggregates was about 40% smaller for the air-dried pretreatment than for the moist pretreatment (Fig. 1 ).


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  		Table 2. Dry matter yield of aggregate size fractions, relative contribution of soil organic C (SOC) stored in the aggregate size fractions to total SOC storage of the bulk soil, and SOC concentration in aggregate size fractions of tropical pasture sites using either air-dried or moist soil before aggregate fractionation by wet sieving. Values are means (n = 4) with standard deviations in parentheses. The SOC concentration of the bulk soil before aggregate fractionation is 100% of total SOC (Table 1).

 

Figure 1
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  		Fig. 1. Box plots of the mean weight diameter (MWD) of aggregates of tropical pasture sites using either air-dried soil or moist soil before aggregate fractionation by wet sieving (median, upper and lower quartile, and extreme values, n = 4). Values within a site followed by different letters are significantly different (P < 0.05).

 
For volcanic ash soils, the order of dry matter yield of the aggregate size fractions was not changed by different pretreatments. Large macroaggregates were the most important aggregate fraction (41–53% of total yield). Drying and slaking resulted in a decrease of the smallest fraction (<53 µm) from about 10 to 2% at both volcanic ash sites (Table 2). There was no effect of sample pretreatment on the MWD of aggregates at the Pedro Viciente site, while air drying resulted in a slight increase (10%) in MWD at Maquipucuna (Fig. 1).

Sample Pretreatment and Soil Organic Carbon in Aggregate Fractions
In the moist pretreatment of the sedimentary soils, 54 to 70% of total SOC was stored in the large macroaggregates followed by the fractions <53 µm (11–24%), small macroaggregates (9–10%), and microaggregates (3–6%; Table 2). In contrast, the outcome of air drying and slaking was that most total SOC was found in the small macroaggregates (40–50%), followed by large macroaggregates (29–38%), microaggregates (9–14%), and the <53-µm fraction, which only contributed 3% to total SOC. Soil organic C concentration of sand-free aggregates was also influenced by pretreatment: air drying and slaking caused SOC concentrations to increase with aggregate size and SOC concentrations were highest (34–35 g kg–1) in the large macroaggregates. In contrast, wet sieving of moist soil resulted in the highest SOC concentration in the 53- to 250-µm fraction.

The partitioning of pasture-derived SOC among aggregate fractions was also influenced by soil pretreatment. The highest proportion of pasture-derived SOC of the total SOC was found in macroaggregates and decreased with decreasing aggregate size in the air-dried pretreatment. In contrast, the microaggregate class of the moist pretreatment showed the highest contribution of pasture-derived SOC to total SOC (Fig. 2 ). Most of the total pasture-derived SOC was stored in the large macroaggregate class (73–57% of total C4–SOC) using moist soil, while in the air-dried and slaked pretreatment, the highest proportion of the total pasture-derived SOC was found in small (47–48% of total C4–SOC) and large (38–41% of total C4–SOC) macroaggregate classes (Table 3 ).


Figure 2
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  		Fig. 2. Percentage (means n = 4, standard deviation) of pasture-derived soil organic C (C4–SOC) in aggregate classes produced by wet sieving of sedimentary soils from (a) Tazones and (b) Chonta Duro and volcanic ash soils from (c) Maquipucuna and (d) Pedro Viciente using moist soil (without prior drying) and air-dried soil before wet sieving. * Bars in the same aggregate size class are significantly different between treatments; bars within a treatment followed by a different lowercase letter are significantly different (P < 0.05). In one case (Chonta Duro, 250–53 µm), it was not possible to test significance due to insufficient sample replicates.

 

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  		Table 3. Partitioning of pasture-derived soil organic C (C4–SOC) and forest-derived soil organic C (C3–SOC) of aggregate size fractions of tropical pastures sites using either air-dried or moist soil before aggregate fractionation by wet sieving. Values are means (n = 4) with standard deviations in parentheses.

 
In the volcanic ash soils, pretreatment caused only slight differences in the SOC concentrations of different aggregate classes and the partitioning of SOC among aggregate sizes. If differences occurred, they were not consistent comparing the two sites. Air drying resulted in a higher contribution of small macroaggregates to total SOC storage at Maquipucuna and in a lower contribution of the <53-µm fraction at Pedro Viciente (Table 2). The lowest SOC concentrations were found in the <53-µm fraction of the air-dried pretreatment, while the moist pretreatment resulted in no differences between SOC concentrations of aggregate classes at this site (Table 2). At Maquipucuna, SOC concentration increased with decreasing aggregate size to the microaggregate class in the air-dried pretreatment, while a higher SOC concentration was found in the small macroaggregate class of the moist pretreatment.

Pasture-derived SOC storage was higher in the small microaggregate class and lower in the <53-µm fraction of the air-dried pretreatment compared with the moist pretreatment (Table 3). The relative proportions of pasture-derived SOC to total SOC within each fraction were equally distributed between all aggregates size classes and independent of pretreatment (Fig. 2).


   DISCUSSION
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
CONCLUSIONS
 REFERENCES
 
Sample Pretreatment and Aggregate Size Distribution
Sedimentary Soils
Published studies that report differences in the aggregate-size distribution of air-dried, slaked and rewetted, unslaked soil samples from temperate climate soils agree with our observation that air drying and slaking reduces the amount of macroaggregates and decreases MWD compared with moist pretreatment of sedimentary soils (Puget et al., 1995; Six et al., 2000a; Denef et al., 2002). Generally, in these studies the unslaked treatments were achieved by rewetting air-dried soil. A comparable decrease in the MWD of 42 to 65% was found by Six et al. (2000a) in temperate grassland soils. The use of moist or rewetted soil probably reduces the stress on aggregates because the pores are already partly filled with water and, consequently, also less stable macroaggregates survive the procedure, thereby increasing the MWD (Kemper and Rosenau, 1986).

The use of field-moist soil samples in our study resulted in a <53-µm fraction that was about three to four times higher than in the air-dried and slaked treatment. Comparable results have also been documented by others who compared the use of field-moist and air-dried soils from temperate areas (Haynes, 1993; Beare and Bruce, 1993). Rewetting of air-dried soil before aggregate fractionation did not result in an increase in the <53-µm fraction (Beare and Bruce, 1993; Six et al., 2000b). More specifically, Beare and Bruce (1993) analyzed the effect of rewetting by comparing the distribution of water-stable aggregates of air-dried, capillary-wetted and field-moist, capillary-wetted soil. Differences in the size distribution of macroaggregates were negligible, while a higher proportion of soil was recovered in the <53-µm fraction of the field moist than in the rewetted soil treatment. Precipitation of bonding agents and an increase in the solid-phase cohesion of aggregated particles was proposed to increase the aggregate stability of air-dried soil (Kemper and Rosenau, 1984). These additional intermolecular associations might be formed between organic macromolecules such as polysaccharides and mineral surfaces and might persist after rewetting and reduce dispersion and the release of particles <53 µm from the surface of aggregates (Haynes and Swift, 1990; Haynes, 1993). These processes may also explain the observed higher proportion of the <53-µm fraction recovered in the air-dried pretreatment than the moist pretreatment in the sedimentary soils.

Volcanic Ash Soils
In the volcanic ash soils, differences in aggregate size distribution among air-dried and moist pretreatment were minimal, which contrasts with other soil types that have 2:1 and 1:1 clay minerals (Six et al., 2000b; Denef et al., 2002). Moreover, rapid immersion in water of air-dried volcanic ash soils did not lead to a slaking process. Air drying of the soil resulted in a higher yield in macroaggregates compared with the moist soil pretreatment, a result that was also reported for allophanic soils from New Zealand (Churchman and Tate, 1987). Higher MWD of the air-dried pretreatment may be a result of irreversible flocculation that occurs on drying (Wells and Theng, 1988). Thus, it is not possible to define stable and unstable aggregates using this method in volcanic ash soils.

Sample Pretreatment and Soil Organic Carbon in Aggregate Fractions
Sedimentary Soils
The correlation of aggregate size with SOC concentration in sand-free aggregates and the proportion of recently incorporated SOC in air-dried and slaked soils can be explained by the stabilizing effect of fresh organic matter on macroaggregates (e.g., Jastrow et al., 1996; Six et al., 2002). Our finding, however, that in the moist pretreatment of smectitic clay soils microaggregates have a higher SOC concentration than macroaggregates contrasts with other studies where no differences in SOC concentration of rewetted or misted aggregate sizes were found (Elliott, 1986; Cambardella and Elliott, 1993; Six et al., 2000b). Other studies that reported the highest SOC concentration in the unslaked (soil was rewetted before sieving) microaggregate class were done in soils with mixed-clay mineralogy (2:1 and 1:1 clays; Six et al., 2000b) or soils with 1:1 clays (Beare et al., 1994). This led Six et al. (2000b) to conclude that the SOC enrichment in unslaked microaggregates was specific for soils containing 1:1 clays. Our results show that this effect can also be found in smectite-dominated soils by using moist soil.

Our finding that the use of moist soil resulted in microaggregates in which a higher SOC concentration correlated with a higher contribution of new SOC, while wet sieving of air-dried soil separated macroaggregates enriched in SOC and a higher proportion of new SOC has been reported also for arable soils (Gale et al., 2000). Differences, however, in the relative increase in recently incorporated SOC in stable macroaggregates were higher (89–27%) than in our tropical pastures (19–23%; Puget et al., 1995).

The observed results suggest that during slaking of air-dried soil, unstable macroaggregates not enriched in SOC disintegrate into smaller particles and are therefore recovered in the microaggregate class. Consequently, the microaggregate class of the air-dried and slaked treatment contained both stable microaggregates and also parts of the broken macroaggregates. In contrast, the moist pretreatment resulted in fewer broken macroaggregates recovered in the microaggregate fraction. Both the SOC content and 13C signal of the microaggregates in the moist pretreatment show that these microaggregates contained a higher proportion of pasture-derived SOC, which is characteristic of newly formed microaggregates. These results support the notion that the initial formation of microaggregates is caused by encapsulation of fresh plant residues (Oades, 1984; Oades and Waters, 1991), and that these newly formed aggregates should have higher SOC concentrations and proportions of recently incorporated SOC. In the air-dried pretreatment, the simultaneous increase of SOC concentration and the proportions of recently incorporated SOC with aggregate size supported the concept of aggregate hierarchy.

Volcanic Ash Soils
In contrast to sedimentary soils, pretreatment caused no systematic changes in the SOC concentration of macro- and microaggregates. In agreement with our results, no aggregate hierarchy was expressed by wet sieving of air-dried volcanic ash soils (Huygens et al., 2005; Hoyos and Comerford, 2005). In addition, soil pretreatment caused only slight differences in C4 proportions, which is in contrast to the sedimentary soils. As none of the previously applied aggregate fractionation methods found a relationship between aggregate size and SOC concentration and proportion of pasture-derived SOC, other binding agents such as metal–humus complexes and electrostatic forces dominate the aggregate stability in these soils (Nanzyo et al., 1993; Huygens et al., 2005). In addition, the even distribution of pasture-derived SOC among the aggregate size classes may indicate that disaggregation and reformation of aggregates is a relatively rapid process under field conditions.


   CONCLUSIONS
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
REFERENCES
 
Our results demonstrated that in smectitic clay soils, both soil sample pretreatments resulted in distinct aggregate fractions with different SOC contents and proportions of recently incorporated SOC. Wet sieving of air-dried soil provided information on the stabilizing effect of fresh organic matter on macroaggregates. In contrast, wet sieving of moist soil separated a microaggregate fraction that was characterized by a high proportion of microaggregates in an early stage of aggregate formation and fewer broken parts of unstable macroaggregates. In volcanic ash soils, neither of the pretreatments was able to separate aggregate size fractions with a distinct SOC concentration and proportions of pasture-derived SOC, illustrating that aggregates in these soils are not predominantly stabilized by soil organic matter.


   ACKNOWLEDGMENTS
 
We thank GTZ-Ecuador for institutional support, the Deutsche Forschungsgemeinschaft (Ve-219/6) for financial support, and the Center for Stable Isotopes Research and Analysis, University of Göttingen, for performing the isotope analyses.


   NOTES
TOP
 NOTES
ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
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Received for publication February 7, 2007.


   REFERENCES
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 





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