Soil Science Society of America Journal 65:111-117 (2001)
© 2001 Soil Science Society of America
DIVISION S-3-SOIL BIOLOGY & BIOCHEMISTRY
Microbial Biomass Levels in Barren and Vegetated High Altitude Talus Soils
Ruth E. Ley,
David A. Lipson and
S.K. Schmidt
Dep. of Environmental, Population and Organismic Biology, Univ. of Colorado, Boulder, CO 80309-0334 USA
Corresponding author (schmidts{at}spot.colorado.edu)
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ABSTRACT
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Microbial biomass generally increases with organic matter accretion in soils, but little is known about the relative proportion of specific microbial functional groups that compose the biomass. We measured the biomass of two microbial functional groups in soils of a high altitude talus slope (3700 m) in the Colorado Rocky Mountains. Talus slopes are composed of boulders, with occasional patches of soil in the rock matrix. Because of the severity of the physical conditions, many soil patches are barren. Carbon inputs to barren talus soils are thought to be predominantly eolian deposition. The soils we studied all had the same parent material, aspect and climate, but ranged in soil organic matter (SOM) content from 6 to 250 g kg-1. Total soil C and N, silt, clay, and SOM all increased linearly as sand content decreased. Using the substrate-induced growth response (SIGR) assay and a most-probable number (MPN) assay, we estimated the general microbial biomass (glutamate mineralizers) and the biomass of a microbial group capable of degrading more complex carbon compounds (salicylate mineralizers). In vegetated soils, both groups were positively correlated with SOM. In barren soils, however, silt content was the best predictor of total biomass, which showed no trend at all with SOM. In contrast, the relationship between the biomass of salicylate mineralizers and SOM was the same in vegetated and barren soils, although it was not significant in barren soils. In addition, the proportion of salicylate mineralizers in the total biomass was higher in barren soils than in vegetated soils, which is possibly as a result of different carbon quality inputs to the soils. This research represents the first in-depth description of the biology and soil characteristics of barren high elevation talus soils.
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INTRODUCTION
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STUDIES HAVE SHOWN levels of SOM to correlate with general microbial biomass levels in most soils (Anderson and Domsch, 1989; Wardle, 1992). Most studies of the relationship between SOM and microbial biomass have been conducted in vegetated systems. Whether the trends observed for the general biomass apply to more specialized microbial functional groups, and whether these trends apply to barren soils with very little SOM, is uncertain. We used a gradient of soils from barren to vegetated encompassing a wide range of SOM to assess these questions. The soils came from high elevation mountain talus slopes, which are a poorly studied extreme environment.
Mountain talus slopes are composed of unconsolidated boulders of various sizes where fine material (sand and clays) accumulates among the boulders, forming soils (Williams et al., 1997). Climatic conditions are extreme, with mean annual temperatures below zero, strong winds, high levels of solar radiation, and snow cover much of the year. The duration of the snowpack and the position of water channels on the slopes are important in determining whether plants can establish (Caine, 1995) and many soil patches are barren. While plants supply carbon to the vegetated soils, carbon inputs to the barren patches include eolian deposition of plant matter and soil particles (Litaor, 1987), and possibly CO2 fixation by soil algae and lichens. The resulting pattern on the slope is a mosaic of different soils with different SOM contents. Yet, the aspect, the climate, and the parent material, all state factors in soil formation (Jenny, 1941), are the same for the soils.
To describe the soils, we measured soil texture, SOM content, %C and %N, and pH. We quantified the biomass of the general microbial population (glutamate mineralizers) and the population of a specialized functional group that can degrade more recalcitrant plant detritus and humic materials (salicylate mineralizers). We estimated the biomass of these microbial groups using the substrate-induced growth response (SIGR) method (Schmidt, 1992; Colores et al., 1996) and a most-probable number (MPN) method. We hypothesized that cold temperatures characteristic of talus soils would constrain the mineralization of C inputs by the microbial biomass, resulting in the build-up of SOM, and that SOM accretion and microbial biomass in soil would both reflect the levels of C input. We therefore predicted that the total microbial biomass and salicylate mineralizer biomass would both be positively correlated with SOM.
MATERIALS AND METHODS
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Study Site and Sampling Regime
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We conducted this research in Green Lakes Valley, part of the City of Boulder, CO, watershed in the Front Range of the Colorado Rocky Mountains (40°03' N, 105°35' W). Green Lakes Valley drains the eastern slope of the continental divide and the southern aspect of the Niwot Ridge Long Term Ecological Research/UNESCO Biosphere Reserve. Green Lakes Valley is a typical high elevation valley, but it is closed to the public and therefore minimally affected by human activity. Our study site is a south-facing talus slope extending from approximately 3600 to 3750 m. Barren soils were snow covered from late October 1997 to the beginning of August 1998, and vegetated soils were covered from late October 1997 to the end of June 1998. During the snow-free period of 1998, soil temperatures measured every 4 h at 5-cm depth ranged from 0.3°C to 20.0°C (mean of 6.9°C) in vegetated soil, and 0°C to 33.2°C in barren soil (mean of 9.8°C). During the snow-covered period of the year, soil temperatures stayed between -1.3°C and 0°C in both vegetated and barren soils. About 80% of the 930-mm mean annual precipitation occurs as snow (Caine, 1996).
Soils referred to as "barren" in this study are fine patches on the surface of the talus slope with no plant cover. Soils referred to as "vegetated" have plant communities similar to those found on nearby Niwot Ridge (Fisk et al., 1998; Walker et al., 1994). These include soils dominated by cushion plants [such as Trifolium dasyphyllum T & G and Minuartia obtusiloba (Rydberg) House], soils dominated by sedges (Carex ebenea, Carex misandra), and wetter soils with mixed graminoids and forbs (such as Acomastylis rosii R. Brown).
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Soil Collection and Analyses
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Because of the remoteness of the talus slopes and the difficulty of the terrain, we constrained our sampling to a 1-ha area of talus that extended from the floor of Green Lakes Valley to just under the ridge top of Niwot Ridge (a vertical distance of about 100 m). Within this area, we sampled each patch of barren and vegetated soil that was present, amounting to a total of 12 sites. We sampled four vegetated and four barren soils in July 1997 and July and August 1998; in August 1997 we sampled the same ones plus an additional four barren soils. We collected three randomly located soil cores per site, each with a volume of about 100 cm3, to a depth of 10 cm. Soil was kept on ice and immediately returned to the laboratory the same day of collection. All soil was stored at 3°C and processed within 48 h of sampling. We homogenized the replicate cores for each soil and sieved the soils to 8 mm. All of the soils collected were used in the biomass and SOM assays. For the SIGR assays, two replicate assays were performed for each soil. Nine of the 1997 soils from July and August were randomly chosen for texture analysis, 17 were randomly chosen for %C and %N analysis, and 16 were randomly chosen for pH analysis. Soil organic matter content was estimated by loss on combustion at 550°C (Nelson and Sommers, 1996), and pH was measured after equilibrating a 1:1 soil:water mixture for 1 h. For %C and %N analysis, 60-g subsamples of sieved homogenized soils were dried at 60°C, and of this about 10 g was finely ground (to pass through a 250-µm sieve) by placing steel rods in 20-mL scintillation vials, and tumbling the vials for 3 wk. Subsamples were analyzed for %C and %N at the Stable Isotope Ratio Facility for Environmental Research (SIRFER) at the University of Utah. Nine soils (four vegetated and five barren) were analyzed for particle size distribution. The soils were treated with hot hydrogen peroxide to remove organic matter, then wet sieved to 63 µm to remove the sand fraction (63–8000 µm). The silt (2–63 µm) and clay (<2 µm) were determined by the pipette method of particle size distribution (Burke et al., 1986; Day, 1965).
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Microbial Biomass Measurements
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We estimated heterotrophic microbial biomass using two methods: (i) the substrate-induced growth-response (SIGR) method and (ii) a most probable number (MPN) enumeration technique. The SIGR method (Colores et al., 1996; Schmidt, 1992) provides an estimate of the microbial biomass capable of mineralizing specific carbon compounds in soil without extraction of the biomass. Another advantage of the SIGR method is that it does not rely on conversion factors that confound the interpretation of chloroform fumigation-extraction (CFE) and substrate-induced respiration (SIR) results when different soils are compared (Smith et al., 1995; Ohtonen, 1994; Wardle and Ghani, 1995; Wardle and Parkinson, 1991). When glutamate is used as a substrate, the SIGR method correlates well with these (SIR, CFE) methods (Colores and Schmidt, 1999; Lipson et al., 1999) and was therefore used to estimate total microbial biomass in this study. We chose the amino acid glutamate instead of a simple sugar such as glucose in the SIGR assay because glutamate typically results in the highest population estimates in tundra soil (Lipson et al., 1999). Salicylate is mineralized by the same general pathways as breakdown products from lignin and detrital (poly)phenols. We thus used glutamate in the SIGR assay to measure the general population and salicylate to measure the specialized population that can mineralize the more recalcitrant plant detritus and humic materials.
For the SIGR measurements, replicate soil samples of 10 g for vegetated soils and 20 g for barren soils were added to sterilized biometer flasks. Glutamic acid was added to the soils in concentrations of 2 mg C g-1 for vegetated soils, and 0.1 mg C g-1 for barren soils. Salicylic acid was added to concentrations of 0.1 mg C g-1 and 0.05 mg C g-1 of soil for vegetated and barren soils, respectively. These concentrations had been previously determined to promote maximum respiration rates in these soils. The substrates added were spiked with uniformly 14C-labeled glutamic acid and salicylic acid (Sigma Biochemical Co., St. Louis, MO) so that the final radioactivity was 150 000 dpm and 250 000 dpm per flask, respectively. All incubations were performed at 22°C (± 2°C). The CO2 evolved during the assay was trapped in 1 mL of 0.5 M NaOH in the sidearm of the biometer flask. Every 2 to 3 h, the NaOH was removed, mixed with 2.5 mL of scintillation fluid (Scintiverse, Fisher Scientific, Pittsburgh, PA) and the disintegrations per minute counted. Fresh NaOH was added back to the sidearm after each sampling. The length of the entire assay was typically 30 to 50 h for vegetated soils and 200 to 300 h for barren soils. Of this duration, the exponential growth phase used in the derivation of the biomass estimates was about the first third. Respiration data were analyzed with Kaleidograph software using equations derived by Colores et al. (1996). To convert the units of mg C-CO2 g-1 to mg C-biomass g-1, empirically derived yields (Yc) of 0.11 for salicylic acid and 0.50 for glutamic acid were used in the equation 
, where Xa is the actual biomass in mg C-biomass g-1, and X1 is the biomass in units of mg C-CO2 g-1 (Colores et al., 1996; Lipson et al., 1999).
The MPN biomass estimates were obtained by a microtiter plate assay (Lipson et al., 1999). Dilution series of soil blended with sterile buffer 
were prepared and eight replicate 0.05-mL samples of each dilution series was added to 0.15 mL of a salts solution 
and either glutamic acid or salicylic acid in concentrations equivalent to those used in the SIGR assay, in 96-well plates. The plates were checked for growth (turbidity) after an incubation period of 2 to 3 wk, or until no new wells developed growth. The number of positive wells per dilution was used in a computer program written in C++ to estimate cell number per gram of soil (Lipson et al., 1999).
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Statistical Analyses
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All analyses of variance were conducted by a model comparison approach based on linear regression (Judd and McClelland, 1989). The relationships between biomass and soil attributes were determined by multiple regression and analysis of covariance (ANCOVA). The mean biomass of the two microbial groups in vegetated or barren soil were compared by t-tests, as were the ratios of the salicylate mineralizers to the total biomass. Data not normally distributed were log transformed to fit normal distributions prior to analysis, no outliers were omitted. All statistical tests were performed with the "proc reg" command in SAS software.
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RESULTS
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Soil Attributes
The soils ranged in organic matter content from 0.6 to 25% (Fig. 1) . The barren soils all had organic matter contents of less than 3%. One sparsely vegetated soil had an SOM content of 2%, making the vegetated and barren soil categories overlap in SOM content. Percent total C and N were highly correlated with SOM (Fig. 1a). The correlation between %C and %N was 0.99 (
, P < 0.0001) across the soil organic matter gradient. The pH of the soils overall was not significantly related to SOM. The percentages of organic matter, carbon, nitrogen, silt and clay all increased as sand content decreased in all soils (Fig. 1). Silt and clay content of the soils increased with increasing SOM across all soils 
and 
respectively) (Fig. 1b). Fine particles in soil are the result of chemical weathering that is typically driven by the presence of plants; barren soils had the coarsest texture and the lowest SOM.
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Fig. 1. Properties of talus soils along the SOM gradient. A: %N and %C in soils along the SOM gradient. B: Silt, clay, and sand content of soils along the SOM gradient
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Microbial Biomass Measurements
Total Microbial Biomass
The SIGR total biomass values are highly reproducible, the regression of replicate biomass estimates against each other has a slope of 1.04 and an r2 of 0.98. Total microbial biomass estimated by the SIGR method ranged from 0.028 µg C g-1 to 38.6 µg C g-1 (mean = 3.7 µg C g-1) in barren soils, and from 0.5 µg C g-1 to 207 µg C g-1 (mean = 63 µg C g-1) in vegetated soils (Fig. 2a)
. This variation was remarkable in barren soil particularly, since the range of SOM values for these soils was just a few percent (0.6–3%). When all the soils were considered together as an SOM gradient, the total biomass was positively correlated with SOM (Table 1). The relationship between total biomass and SOM is different in barren and vegetated soils, however, since the slope of the regression is significantly different between barren and vegetated soils (see "interaction", Table 1). Furthermore, when vegetated soils were considered alone, the total biomass was highly correlated with SOM (Fig. 3a)
, but in barren soils alone, total biomass was not correlated with SOM, instead total biomass was positively correlated with the percent silt of the soil 
(Fig. 4)
. The total biomass estimated by the MPN method showed generally the same trends as the SIGR total biomass estimates but the relationships with SOM and pH were weaker (data not shown). The total biomass estimated by the MPN method was related to SOM across all soils 
controlling for pH.
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Fig. 2. Mean biomass values in vegetated and barren soils. A: total biomass; B: salicylate mineralizers. C: the ratio of salicylate mineralizer biomass to total biomass. Error bars are standard errors, * denotes statistically significant difference between means
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Table 1. Analysis of covariance of total biomass and salicylate mineralizer biomass regressed against SOM and soil type (barren or vegetated). The "interaction" tests whether the relationship (slope) between the biomass and the SOM is the same or changes significantly between barren and vegetated soils
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Fig. 3. A. Total biomass (circles) and salicylate mineralizers (squares) measured by the SIGR in vegetated soils. B. Total biomass (circles) and salicylate mineralizers (squares) measured by the SIGR in barren soils
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Salicylate Mineralizer Biomass
The salicylate mineralizer biomass values estimated with the SIGR are accurate, the slope of the regression line of replicates against each other is 0.88 and the 
. Salicylate mineralizer biomass (measured by SIGR) ranged from 0.005 µg C g-1 to 1.5 µg C g-1 (mean = 0.1 µg C g-1) in barren soils, and from 0.002 µg C g-1 to 3.0 µg C g-1 (mean = 0.8 µg C g-1) in vegetated soils (Fig. 2b). The biomass of salicylate mineralizers mirrored the total biomass in its relationship with SOM, but the values were lower than those for total biomass. Like the total biomass, the salicylate mineralizer biomass was positively related to SOM when all the soils were considered together as an SOM gradient (Table 1). The relationship (as described by the slope of the regression line) is the same in both vegetated and barren soils (Table 1), although this relationship is not significant in barren soils alone. In vegetated soils alone, the salicylate mineralizer biomass could be predicted very accurately with both pH and SOM 
(Fig. 3a). The salicylate mineralizer biomass measured by MPN showed the same trends as the SIGR estimates (data not shown). The MPN estimates were positively related to SOM and pH 
. For the salicylate mineralizer biomass as with the total biomass, the MPN assay showed the same trends as the SIGR assay, but the biomass values were more variable, and the correlations with SOM were weaker.
Salicylate Mineralizer Biomass in Relation to Total Biomass
The total biomass was highly correlated with salicylate mineralizer biomass in vegetated soils 
. But surprisingly, the total biomass was not correlated with salicylate mineralizer biomass in barren soils. Another interesting observation was that the ratio of salicylate mineralizer biomass to total biomass was higher in barren soils than vegetated soils 
(Fig. 2c). In vegetated soils, the ratio of salicylate mineralizer biomass to total biomass did not change as a function of SOM. There appears to be a shift that occurs with the absence of plants, such that a greater proportion of the total biomass can mineralize salicylate.
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DISCUSSION
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This is the first in-depth study of the microbial communities and soils of one of the most extreme terrestrial environments for life on Earth. Organisms living in the rocky slopes of the high reaches of mountains must contend with extremely low temperatures and very little free water much of the year. Where vegetation has not taken root there is also minimal C input to the soil. The result is a cold, dry, oligotrophic environment. In a talus slope of Green Lakes Valley of the Colorado Rocky Mountains, we examined the biomass of two microbial functional groups in relation to physical factors of the soils.
The Soils
We found that the physical properties that we measured in these soils allowed us to order them into a gradient of increasing SOM content. Our gradient of soils probably does not constitute a successional gradient, however, because the differences in the soils are due to their positions on the slope and the resulting water courses and snow pack, not the length of time since their formation which defines chronosequences in similar studies (Insam and Domsch, 1988; Ohtonen et al., 1999). The texture of the soils correlated well with SOM; as SOM increased in the soils, the percentages of silt and clay also increased, and sand content decreased. This is consistent with the process of chemical weathering in soil that progressively converts larger soil particles (sand) to smaller ones (silts and clays). Chemical weathering is typically the result of organic acid production by plants and associated microbes (Gerrard, 1992), so it is not surprising that the vegetated soils in our system had the greatest percentages of silts and clays.
The Microbial Biomass
As we had predicted, the total biomass and the biomass of salicylate mineralizers correlated with SOM across all the soils. But the proportion of salicylate mineralizers did not stay constant. Instead, there were more salicylate mineralizers relative to the total biomass in the barren soils than in the vegetated soils. The nature of C inputs to the soils may help explain these patterns.
Plants supply C to microbes in most soils, so it is not surprising that microbial biomass is greater under plant canopies than in open areas (Herman et al., 1994) and in the rhizospheres relative to bulk soil (Clarholm, 1981). In alpine soils close to our sites (Niwot Ridge), the greater the plant production, the greater the microbial biomass (Fisk et al., 1998). We expected the same relationships to be present in the talus soils, and we did observe a positive correlation between microbial biomass and SOM. So it seems reasonable that in the vegetated soils of talus slopes, the positive relationship that we observed between SOM and microbial biomass is the result of increasing levels of plant production.
What we did not expect was the change in the proportion of salicylate mineralizers in the total biomass from barren to vegetated soils. This change was not gradual, instead the ratio decreased abruptly, reflecting the presence of vegetation in the soils rather than the steady increase in SOM along the gradient. The higher proportion of salicylate mineralizers in the total biomass in barren soils could be a reflection of the chemistry of the C inputs to barren soils. The salicylate breakdown pathway is typical of (poly)phenol mineralization, which suggests that the barren soil organic matter is likely to contain either transported resistant plant residues (fiber or acid-insoluble fractions) or humic materials sorbed to clay and silt surfaces, rather than the more labile in situ products of cyanobacterial or algal communities. Indeed, eolian deposits constitute an important input of materials to talus slopes (Litaor, 1987; Blank et al., 1996; Dahms and Rawlins, 1996). Dust falling in Green Lakes Valley has been found to contain up to 22% organic C (Litaor, 1987). The organic components of the dust could very well have a composition different from that of the plant inputs to vegetated soils which is reflected in the shift in the proportion of salicylate mineralizers in the total biomass.
Whereas in vegetated soils the correlations between the total microbial biomass, SOM, and texture were very striking, the almost total lack of relationship between the same soil components in barren soils was equally striking. This could be a sampling artifact: the range of SOM values for barren soils is much smaller than the range for barren soils, making it harder for significant relationships to emerge; however, the lack of any trend between the general biomass and SOM in barren soils suggests a lack of relation between the two. The associations and positive correlations between SOM, microbial biomass, and fine particles are well documented in vegetated soils (Gupta and Germida, 1988; Schnitzer and Kodama, 1992; Hassink et al., 1993; Kiem and Kandeler, 1997). In the absence of plants, these associations considered typical of (vegetated) soils do not occur. In contrast, the more specialized salicylate mineralizers show the same relationship with SOM across the whole gradient of soils, although the relationship is not as strong in barren soils as in vegetated soils. The similar slopes imply similar relations for salicylate mineralizers with SOM. This supports the notion that salicylate mineralizers are relying on SOM as a source of energy, instead of labile photosynthetic inputs from algae or cyanobacteria.
In conclusion, this is the first in-depth description of the biology of soils found in one of the most common extreme environments on Earth, the highest reaches of continental mountains. The soils and microbiological properties of vegetated soils in talus were very similar to those of alpine tundra soils of nearby Niwot Ridge (Fisk and Schmidt, 1995; Fisk et al., 1998; Lipson et al., 1999). The total biomass and the biomass of a specific functional group both increased consistently with increasing SOM content. In contrast, there was no relationship between total microbial biomass and SOM in barren soils. Instead, the silt content of the soils could predict total biomass. The relationship between SOM and salicylate mineralizer biomass was the same, although weaker, in barren soils. Additionally, the proportion of salicylate mineralizers in the total biomass was higher in barren soils than in vegetated soils. This difference in functional composition of the biomass in barren and vegetated soils could be the result of very different C inputs. Sources of C for barren soils are most likely eolian, which are possibly very different in quality from plant C inputs to vegetated soils. More research is needed to characterize the unique microbiological properties and carbon inputs of these oligotrophic cold soils.
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ACKNOWLEDGMENTS
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This work was funded by the NSF LExEn (DEB-9809348) grant to S.K. Schmidt. Logistical support was provided by the Niwot Ridge LTER program and the Mountain Research Station. Support was also received from the Biosphere/Atmosphere Research Training Program. We'd like to thank Kirsty Johnston for field and laboratory assistance, and Margie Krest for help with preparation of the manuscript.
Received for publication January 13, 2000.
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TOP
ABSTRACT
INTRODUCTION
