The Emerald Lake Basin provides a long-term site for research on hydrology, ecology, and biogeochemistry, as well as baseline data for a representative subalpine watershed in the Sierra Nevada of California. Field studies provided quantitative data on the biomass, net primary production, and nutrient allocation of major subalpine shrub and meadow communities. Measurements carried out over two growing seasons found aboveground biomass per unit canopy area was 3857 g m-2 in Chrysolepis sempervirens, 3360 g m-2 in Salix orestera, and 1614 g m-2 in Phyllodoce breweri. The biomass for Chrysolepis and Salix canopies were high compared to other published data for subalpine and alpine shrublands, but the Phyllodoce biomass was comparable to values for ericaceous heath in the Rocky Mountains and European Alps. Wet and dry meadows had 377 and 98 g m-2, respectively, in aboveground living tissues, comparable to values from the Rocky Mountains and European Alps. Belowground biomass for shrub communities was the highest for Phyllodoce (3670 g m-2), followed by Chrysolepis (2400 g m-2) and Salix (2070 g m-2). The wet meadow community had a surprisingly high belowground biomass of 2897 g m-2, reflecting the dominance of large perennial herb species. This resulted from a root:shoot ratio of 8.21 compared to 5.72 in the dry meadow community. Canopies of Chrysolepis and Salix had root:shoot ratios of 0.62 and 0.61, respectively, and Phyllodoce a ratio of 2.27.
Introduction
The biologically rich subalpine and alpine basins of the Sierra Nevada have had a long history of descriptive study, but more recently have served as important areas for quantitative research on the ecology and ecosystem processes in subalpine watersheds. These high mountain ecosystems are sensitive to small changes in growing season conditions of temperature and water availability, and their stability impacts hydrological conditions that provide a critical resource for downstream agriculture and urban development in California (Bales et al., 2006; Maurer, 2007; Trujillo et al., 2012). Despite a number of detailed studies of hydrology, and biogeochemical cycles of high mountain systems in the Sierra Nevada (Millar and Rundel, 2014), there has been relatively little study of the biomass and primary productivity of subalpine and alpine shrublands and meadows communities.
The Emerald Lake Basin in Sequoia National Park has served for more than three decades as a primary study site to understand the hydrology, ecology, and biogeochemistry of a representative subalpine watershed in the southern Sierra Nevada (Fig. 1). This work began in 1984 with funding from the California Air Resources Board to address concerns related to the influence of atmospheric inputs of nutrients to basin processes and ecosystem structure (Tonnessen, 1991). The ecological communities and floristic diversity of the Emerald Lake Basin have been described (Rundel et al., 2009). Watershed studies have continued up to the present day and have provided detailed and in many cases long-term and continuing databases to understand hydrologic flow and water balance (Kattelmann and Elder, 1991; Huth et al., 2004), nutrient enrichment (Sickman et al., 2003a, 2003b), solute chemistry of snowmelt and runoff (Williams and Melack, 1991; Sadro and Melack, 2012), nitrogen fluxes and transformations (Williams et al., 1995; Miller et al., 2009), and models of hydrochemical response (Wolford et al., 1996; Wolford and Bales, 1996; Meixner et al., 2004).
Relatively little is known about patterns of biomass distribution and rates of productivity for subalpine and alpine communities in the Sierra Nevada. Although there have been numerous studies in the Rocky Mountains and Europe describing the biomass and productivity of alpine and subalpine fellfield, sedgeland, and grassland meadow communities, there has been relatively little comparative study of subalpine shrublands, which often dominate extensive areas near treeline. Moreover, most of the existing subalpine and alpine meadow studies from Europe and the Rocky Mountains have focused on areas with a dominance of summer rainfall regimes where summer drought is not a strong limiting factor for growth.
The high mountains of California offer very different conditions, as late summer drought often limits growth before cold fall temperatures (Rundel et al., 2005). The objective in this paper has been to quantify the biomass, net primary production and nutrient allocation of major shrub and meadow communities of the Emerald Lake Basin, and compare and contrast these values with those for the summer-rainfall high mountain areas of the Rocky Mountains and Europe.
Methods and Materials
STUDY SITE
Field studies were carried out in the Emerald Lake Basin (Fig. 1), a subalpine watershed about 120 ha in area in the upper drainage of the Marble Fork of the Kaweah River above Tokopah Falls in Sequoia National Park (36°35′49″N, 118°40′30″W). The watershed is roughly triangular in shape trending northwest to southeast, with elevations ranging from 2804 m at Emerald Lake at the lower end of the basin to the apex of the triangle at the summit of Alta Peak at 3416 m (Rundel et al., 2009).
FIGURE 1.
Map of the 120-ha Emerald Lake watershed, Sequoia National Park, California, U.S.A. Small map of California shows latitude and longitude.
The Emerald Lake Basin is a glacial cirque (Fig. 2), carved from granitic parent material and representative of many subalpine and alpine basins in the Sierra Nevada, with lakes exhibiting weakly buffered calcium bicarbonate surface waters (Williams and Melack, 1991). The climate of the Emerald Lake Basin is typical of the mediterranean-type regime of the southern Sierra Nevada, with 75%–90% of the annual precipitation falling as snow in the winter months (Stephenson, 1990). At this site specifically, rainfall composes only about 10% of annual precipitation and occurs predominantly in the autumn, with winter snows the predominant form of precipitation. Based on limited long-term data on precipitation levels, mean annual precipitation is about 1600 mm, but amounts are highly variable between years (Sickman et al., 2003a). Snowmelt typically begins in April with peak flow of runoff water occurring in June (Sickman et al., 2003b). Summers are generally dry except for an occasional convective storm associated with monsoonal air masses from the east (Sadro and Melack, 2012).
Because bedrock exposed by glacial scouring and frost action covers nearly half of the surface area of the Emerald Lake Basin, with the remaining half covered by talus and thin soils in approximately equal proportions, with soils present over only about 20% of the watershed surface (Sisson and Moore, 1984; Tonnessen, 1991), vascular plant cover is relatively sparse. Thin soils and fractures in the granite surface, however, do support a wide distribution of both wet and dry meadow communities throughout the basin as well as extensive woody shrub growth in local areas of the lower basin with more soil development and in rocky fracture lines across the basin where soil and moisture are available.
A low-growing ericaceous heath dominated by Phyllodoce breweri (Ericaceae) is widely distributed in the basin, but covers only about 0.73 ha of area. Also present in these heath stands are the evergreen Arctostaphylos nevadensis (Ericaceae) and the winter deciduous Amelanchier utahensis, Prunus emarginata, and Sorbus californica (all Rosaceae). However, Phyllodoce is the major element of this community and forms relatively extensive local populations in granite fracture zones across the basin. Species names used in this paper follow those in Baldwin et al. (2012).
Willow thickets are widespread and cover 8.55 ha within the basin. Along with Salix orestera, the dominant species, which reaches 1-2 m in height, there are a characteristic set of understory shrubs that typically cover 100% of the ground surface. These species include evergreen ericaceous shrubs such as Rhododendron columbianum (formerly Ledum glandulosum), Kalmia polifolia, Phyllodoce breweri, and Vaccinium cespitosum (Rundel et al., 2009).
The understory of open conifer forest stands in the lower elevations of the Emerald Lake Basin is locally dominated by an open shrubland of Chrysolepis sempervirens (Fagaceae), an evergreen shrub 1–1.5 m in height. This shrubland may locally exhibit dense ground cover up to 80%–100%, but is also present in more open stands with an understory of typical dry meadow herbs such as Achillea millefolium (Asteraceae) and Ivesia santalinoides (Rosaceae).
Wet meadows form diverse communities in the watershed and cover 4.1 ha of area. These include a number of distinctive associations largely distributed in relatively flat areas on west-facing slopes above Emerald Lake where soils accumulate to moderate depths and remain moist for much or all of the growing season (Rundel et al., 2009). Variations in soil texture, soil organic matter content, and soil moisture dynamics appear to be the primary physical factors separating different wet meadow associations.
Dry meadow communities occupy about 7.7 ha of the Emerald Lake watershed, most notably in the relatively flat plateau and benches below the northeast ridge and boundary of the basin. In these sites, soils are formed of shallow layers of decomposed granite with low organic matter, and typically dry early in the growing season, as indicated by the early senescence of herbaceous species (Rundel et al., 2009).
SAMPLING BIOMASS AND PRODUCTIVITY
Detailed measurements of stand biomass and productivity were carried out over two growing seasons (1985–1986) in three shrub species and wet and dry meadow communities in the Emerald Lake Basin. These shrubs were Chrysolepis sempervirens, Phyllodoce breweri, and Salix orestera. The differing structure and composition of each community type required the use of multiple sampling methodologies. Both Salix and Chrysolepis are large shrubs. For canopies of these species, we utilized a series of nine 1 m2 canopy plots located in three different sites within the basin. For each plot, all biomass was clipped and sorted, separating current growth, previous year growth, and standing dead biomass. Understory herbs were harvested and surface litter collected. A standardized root core of 20 cm diameter (0.0314 m2) and 30 cm deep was taken from the center of each of these plots. Because of the shallow granitic soils, this depth of core was sufficient to sample virtually all roots.
FIGURE 2.
Emerald Lake watershed, looking southeast toward Alta Peak (3416 m). Emerald Lake (2800 m) is in the foreground, with willow thickets along the far end of the lake and wet meadows beyond.
For the Phyllodoce heath and wet meadow communities, three canopy areas of 20 cm diameter in each of three sites were clipped and tissues separated by species and by biomass categories of current and older growth. Surface litter was collected in the same plots. A root core of 20 cm diameter was taken from each of these nine plots, as above.
Biomass samples collected at the end of the growing season in the first year of the study were separated into categories of current-year foliage, old foliage, reproductive tissues, current year twigs, older woody tissues, and dead biomass. In order to determine the increment of current-year woody tissue growth on older stems, woody tissues were first cut and separated into a series of diameter size classes. For the larger Salix and Chrysolepis, up to ten size classes were used. Only a single size class was necessary for the small and relatively uniform stems of Phyllodoce. The total length (L) and mean diameter of each stem size class were measured to 0.1 and 1.0 mm accuracy, respectively. Ten twigs of each size class were subsampled, and measurements were made using a dissecting microscope of overall branch diameter, total wood diameter (Dn), and wood diameter beginning with the previous year (Dn-1). The volume of current-year wood increment (Vn) was calculated as:
The biomass increment of current-year woody growth on these stems was then the product of this volume calculated and summed for all of the sampled length of stems, times the mean wood density. Experimental trials demonstrated that wood density was not a function of stem diameter. Current-year bark biomass was included in the current-year twig pool, while bark on older twigs was included in the pool of older wood tissues. The reproductive pool for Salix and Phyllodoce included only current-year tissues, and with sampling occurring after some of the tissues had senesced. For Chrysolepis, the great bulk of the reproductive tissues were matured fruits from the previous growing season.
Prostrate rooted stems were commonly encountered in both Salix and Chrysolepis, apparently the result of snow compaction and subsequent layering of the tissues. For the purposes of this study, these rooted stems were classified as root tissues. Such stems formed the major part of the >20 mm diameter root pool as well as a smaller portion of the 10–20 mm diameter pool of roots.
The distribution of dead tissues on the aboveground stems was highly variable between species and within communities. Virtually all of this pool consisted of dead stem material from the growth of previous years, but small amounts of dead foliage and dried reproductive structures from previous years were also included when encountered. For Salix, dead aboveground tissues formed by large dead branches were uncommon and highly scattered in occurrence. The situation was very different in Chrysolepis, where large areas of dead canopy were localized in distribution.
NUTRIENT CONTENT AND ALLOCATION
The nitrogen, phosphorus, potassium, calcium, and magnesium contents of each major aboveground tissue were analyzed from individual biomass samples for Phyllodoce breweri and Salix orestera. These samples were divided into two groups, which were analyzed separately to provide replication in analyses for nitrogen and phosphorus. Samples of root tissues in three size classes were collected and analyzed for Salix, while only fine roots 0–2 mm in diameter were collected and analyzed for wet meadow canopies. Total nitrogen and total phosphorus were analyzed by the plant tissue laboratory of the University of Alaska, Anchorage, using Kjeldahl digestions and a Technicon colorimetric autoanalyzer using standard procedures and calibration, with mean values reported here. Cations (K, Ca, and Mg) were analyzed by optical emission spectroscopy at the then Laboratory of Biomedical and Environmental Sciences at UCLA, following procedures described by Alexander and McAnulty (1981) with subsamples run with ten replicates.
Results
BIOMASS
Shrub cover in the Emerald Lake basin totaled about 9% of the surface area, with willow thickets making up the great majority of this cover. The total aboveground biomass per unit canopy area of shrub cover, including both living and dead tissues, was highest among the canopies studied for Chrysolepis sempervirens, with a mean biomass of 3857 g m-2, with 2747 g m-2 (71%) of this in living tissues. Thickets of Salix orestera were a close second, with 3360 g m-2, and 2230 g m-2 (66%) of this in living tissues. Stands of the less woody and smaller stature Phyllodoce breweri had 1614 g m-2 in aboveground tissues, with 1409 g m-2 (87%) of this in living tissues (Table 1). Wet and dry meadow communities had 377 and 98 g m-2 in aboveground living tissues, respectively.
Despite these differences in aboveground biomass, belowground biomass was much more consistent between communities. Estimated values of belowground biomass were high in the Phyllodoce heath, with an estimated 3670 g m-2. The woodier Chrysolepis and Salix stands had a lower belowground biomass of 2400 and 2070 g m-2, respectively. Including all tissues, living and dead, these values gave mean root:shoot ratios of 0.62 and 0.61 for the Chrysolepis and Salix stand canopies, respectively, and 2.27 for Phyllodoce. The wet meadow community, reflecting the dominance of large perennial herb species, had a root:shoot ratio of 7.68, while this ratio was lower at 5.72 for the dry meadow community.
Litter biomass was highest in the Chrysolepis stands, with a mean of 4553 g m-2, a value three times higher than that of any other community (Table 1). The Phyllodoce and Salix stands had 1618 and 1441 g m-2, respectively, while the wet and dry meadow communities had much smaller amounts of litter. These values produced a ratio of aboveground biomass to litter of 0.85 and 1.00 in the Chrysolepis and Phyllodoce canopies and 2.33 in the Salix canopy (Table 1).
The woody growth of Chrysolepis and Salix did not allow for the survival of a significant biomass of herbaceous species below their canopies. However, we sampled a mean aboveground herb biomass of 54 g m-2 below the more open canopy of Phyllodoce heath.
NET PRIMARY PRODUCTION AND BIOMASS ALLOCATION
Annual patterns of net primary production in the four study communities showed a different pattern than that seen in the biomass data. Despite its lower stature, the aboveground net primary production was highest in the Phyllodoce heath, with a mean of 499 g m-2 y-1 (Table 1). The Chrysolepis canopies were a close second in productivity, with 443 g m-2 y-1, followed by the Salix thickets with a relatively low annual productivity of 227 g m-2 y-1. The wet and dry meadow communities had rates of aboveground productivity very close to that of their biomass, reflecting the herbaceous growth forms that dominate these communities and die back to ground level each winter. A small amount of perennial aboveground tissues in wet meadow community was contributed by low-growing perennials such as Vaccinium cespitosum, Penstemon heterodoxus, Eriogonum incanum, and Kalmia pohlifolia.
The biomass accumulation ratio, aboveground living biomass divided by productivity, was relatively high in the woody Chrysolepis and Salix stand canopies, with values of 6.2 and 9.8, respectively. This ratio was 2.8 in the Phyllodoce heath, and only about 1.1 in the wet and dry meadow communities.
As expected, the proportion of dry weight biomass within new tissues was lowest in the woody Chrysolepis and Salix canopies, with 12.7% and 8.5%, respectively (Table 2). In Phyllodoce canopies, new growth for the current year made up 32.9% of the biomass. The relative allocation of new growth to leaves in the evergreen Chrysolepis and Phyllodoce was quite similar, with a relative allocation to leaf production of 49.8% and 50.6%, respectively. Deciduous Salix canopies allocated a significantly lower 30.9% of new growth to leaves, but a higher fraction to new twigs. The three species did not differ significantly in allocation to new wood on old branch tissues (Table 2).
NUTRIENT CONTENT AND ALLOCATION
Nutrient contents on a dry weight basis for each tissue type of Phyllodoce breweri, Salix orestera, and wet and dry meadows are presented in Appendix Table A1. New leaves of Salix had a relatively high nitrogen content of 28.2 mg g-1, compared to only 14.9 mg g-1 in Phyllodoce. Phosphorus concentration levels in new leaves were less different with 1.9 mg g-1 in Salix and 1.7 mg g-1 in Phyllodoce.
The relative amount of aboveground nitrogen pools contained in new tissues of Phyllodoce closely matched the proportional biomass of these tissues. The situation was very different in Salix where current year tissues composed less than 10% of the total plant biomass, but held 44% of the nitrogen (Table 3). This pattern is repeated in concentrations of phosphorus, potassium, calcium, and magnesium. Among new tissues, Phyllodoce with evergreen leaves allocated 60% of its nitrogen to leaf tissues compared to a biomass proportion of 51%, while Salix with deciduous leaves allocated 55% of nitrogen compared to a proportional biomass of 31% for leaf tissues. Similarly, Salix allocated proportionally larger relative amounts of phosphorus, potassium, calcium, and magnesium to new leaf tissues than to biomass, although the proportion is less for phosphorus.
Table 1
Biomass and productivity parameters for three subalpine shrubs species and wet meadows in the Emerald Lake Basin of Sequoia National Park. All values are based on units of canopy cover for the shrub species. For wet meadows, cover was taken as 100% of the mapped community, while for more open dry meadows cover was measured as 38% of the mapped community. NP indicates tissue not present.
TABLE 2
Relative aboveground biomass allocation (%) and relative allocation of new aboveground growth (%) in three species of subalpine shrubs in the Emerald Lake Basin, Sequoia National Park. Values shown in parentheses are standard deviations of measurements.
Discussion
Data on the biomass and productivity of subalpine and alpine shrubland communities are relatively few in the literature. The shrub tundra at Niwot Ridge in Colorado, a community of low willows less than 50 cm in height, has an aboveground biomass of about 1500 g m-2, an aboveground net primary production of about 300 g m-2, and a belowground biomass of about 5000 g m-2, for a root:shoot ratio of 3.3 (May and Webber, 1982). More parallel with our research are data collected on mountain heath communities dominated by Phyllodoce empetriformis, Cassiope metensiana, and Vaccinium deliciosum in the Cascade Range of Washington by Grier (1973) who looked at patterns of organic matter and nitrogen distribution in three differing areas of geomorphic condition. The standing crop of aboveground biomass ranged from 740 to 2380, and root:shoot ratios were 0.37 and 0.38, respectively, in organic-rich and colluvial soils but 1.00 in residual soils. Our results for aboveground biomass in Phyllodoce breweri lie within this range, but we found greater biomass in Castanopsis sempervirens and Salix orestera. The relatively high biomass of these latter two species likely results from the more moderate conditions of winter temperatures in the Sierra Nevada and the heavy snowpack that protects soils from deep frosts and canopies from winter desiccation.
There have been numerous studies of subalpine Vaccinium and Rhododendron heaths in the European Alps, and these have generally reported aboveground biomass of 1200–1900 g m-2 (Körner, 2003; Gerdol et al., 2004). Another synthesis reported a mean of 1163 g m-2 (Elzein et al., 2011), while similar values have been published for dwarf shrub communities on both acidic and calcareous soils from the eastern Alps (Tappeiner et al., 2008). Belowground biomass for dwarf shrub communities in the European Alps range from 2400 to 2800 g m-2, giving root:shoot ratios of 2.0–2.3 (Tappeiner et al., 2008).
TABLE 3
Relative allocation of macronutrients in total aboveground biomass and the relative allocation of these nutrients to aboveground new growth in Phyllodoce breweri and Salix orestera. NP indicates tissue not present; ND = no data.
Studies of aboveground production in alpine and subalpine shrublands in the central Rocky Mountains and the European Alps have generally found rates of 100–400 g m-2 yr-1, with typical values closer to 200 g m-2 yr-1 (see Bowman and Fisk, 2001; Körner, 2003). However, these mean values mask the high spatial heterogeneity in rates of aboveground net primary productivity, with plot level values ranging from as low as 50 g m-2 yr-1 to as much as 500 g m-2 yr-1 or more (Bowman et al., 1993; Walker et al., 1994). This heterogeneity is strongly influenced by topographic controls on microclimate conditions as well as biotic impacts from grazers and burrowing animals (Scott and Billings, 1964). Interannual variation in productivity is also characteristic with summer temperatures, patterns of snowmelt, and levels of summer drought having a strong influence on the length of growing season (Billings and Bliss, 1959).
Extensive studies on aboveground biomass and primary production of alpine meadows have been carried out at Niwot Ridge in Colorado, with net aboveground primary production of herbaceous alpine communities varying between about 120 and 171 g m-2 yr-1 (Bowman and Fisk, 2001). These values for herbaceous communities are similar to those reported for other herbaceous subalpine and alpine communities in North America (Billings and Bliss, 1959; Scott and Billings, 1964; Klikoff, 1965; Bliss, 1966, 1985; Kuramoto and Bliss, 1970; Anderson et al., 1979). Higher values with means of 542-684 g m-2 have been described for alpine meadows in the European Alps (Tappeiner et al., 2008). Older data on aboveground biomass are in subalpine and alpine Carex heath and wet meadows in Europe present values from 240 to 800 g m-2 (Brzoska, 1973; Wielgolaski, 1975; Rehder, 1976; Rehder and Schäfer, 1978). These values are lower than what we have measured in our subalpine wet meadow where large upright herbaceous perennials contain significant amounts of biomass, but higher than our low-growing dry meadow community (Table 1).
Belowground biomass has also been quantified in a number of alpine meadow studies. Research at Niwot Ridge has reported total root biomass in herbaceous alpine communities from about 1500 to 5700 g m-2, with associated root:shoot ratios of 2.5–5.6 (May and Webber, 1982; Fisk et al., 1998). The Emerald Lake belowground biomass for wet and dry meadows lies within this range for belowground biomass. However, while the root:shoot ratios in dry meadows at Emerald Lake lie at the upper end of values for Niwot Ridge, the wet meadow ratios are higher at 7.68. The relative absence of deep soil freezing in the Sierra Nevada likely leads to the ability to form larger amounts of storage tissue, a beneficial trait under conditions of summer drought. Root:shoot ratios for alpine meadows in the European Alps have been reported to average about 2.2–2.4 (Tappeiner et al., 2008). Root:shoot ratios are expected to increase with decreasing temperature (Körner, 2003; Friend and Woodward, 1990) and with decreasing availability of water or nutrients (Chapin, 1980; Fonseca et al., 2000).
Conclusions
Despite extensive research on alpine meadows in both North America and Europe, there remain relatively few published data on biomass, primary production, and nutrient pools and fluxes in shrublands, communities that cover significant areas of subalpine watersheds in the Sierra Nevada. The existing data come largely from older studies in the European Alps (e.g., Rehder, 1976; Larcher, 1977; Rehder and Schäfer, 1978; see summary in Tappeiner et al., 2008). Ericaceous subalpine shrublands in the Sierra Nevada have comparable values of biomass and productivity to those in the Pacific Northwest and European Alps. However, willow shrublands in the Sierra Nevada contain far more biomass and higher productivity than low-growing alpine willow stands in the Rocky Mountains. Subalpine meadows in the Sierra Nevada have biomass and productivity relationships similar to those found in subalpine and alpine meadows of the Rocky Mountains at Niwot Ridge, but wet Sierran meadows possess higher biomass and root:shoot ratios than those reported for Niwot Ridge and the European Alps.
Subalpine shrublands and meadows appear to be highly sensitive to small alterations in the seasonality of temperature and hydrology, and thus play a major role in biogeochemical cycles. There have been clear indications for the Sierra Nevada that there has been a significant upward elevational shift in range over the past century for a number of species of birds and mammals (Moritz et al., 2008; Tingley et al., 2009). Subalpine and alpine ecosystems will likely be impacted by other attendant factors as declining snowpack, earlier spring runoff, and earlier phenology (Cayan et al., 2001; Mote et al., 2005; Stewart et al., 2005; Maurer, 2007; Millar and Rundel, 2015). The structure and stability of these high mountain biotic systems form critical components of alpine and subalpine ecosystems in a world with rapid global change (Theurillat and Guisan, 2001; Millar and Rundel, 2015).
Acknowledgments
I thank the California Air Resources Board for funding this research. Peter Rabenold, Mike Neuman, Gail Baker, Evan Edinger, Carmen Crivellone, and Karen Poulin provided major assistance in carrying out the field work for the project. The support of Kathy Tonnessen, Dave Parsons, the staff of Sequoia and Kings Canyon National Parks, and colleagues from many universities working in the Emerald Lake Basin is gratefully acknowledged with thanks.
