Nitrogen Uptake during Snowmelt by the Snow Buttercup

Nitrogen Uptake during Snowmelt by the Snow Buttercup, Ranunculus adoneus
Author(s): R. B. Mullen, S. K. Schmidt, C. H. Jaeger III
Source: Arctic and Alpine Research, Vol. 30, No. 2 (May, 1998), pp. 121-125
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Arctic and Alpine Research, Vol. 30, No. 2, 1998, pp. 121-125
Ranunculus
Snowmelt
adoneus
bytheSnowButtercup,
during
Nitrogen
Uptake
R. B. Mullen,
S. K. Schmidt, and
C. H. Jaeger III
Department of Environmental,
Population and Organismic Biology,
Campus Box 334, University of
Colorado, Boulder, Colorado 80309,
U.S.A. schmidts @spot.colorado.edu
Abstract
Seasonal patterns of nitrogen (N) uptake were measured to assess the ability of
the alpine herb Ranunculus adoneus to utilize the flush of N during snowmelt in
an alpine tundra ecosystem. Development of mycorrhizal and dark septate fungi
were also monitored within the roots of this snowbed plant in order to determine
the role of these fungi in N acquisition. In addition, soil temperature, moisture,
and inorganic N levels were measured to determine possible influences of edaphic
factors on plant N uptake. In contrast to P uptake, which occurs late in the growing season and corresponds with arbuscular mycorrhizal (AM) development, N
uptake occurred very early in the growing season before new roots and active
AM fungal structures were formed. Soils at this time were cold and wet and NH4+
was the predominant form of inorganic nitrogen. Our data indicate that R. adoneus
is able to take advantage of the early season flush of N by utilizing the previous
year's root system which is heavily infected with a dark septate fungus. Given
the high density of R. adoneus plants (135 plants per m2) in this snowbed system,
they are a significant sink (ca. 0.5 g N per m2) for nitrogen released from within
or beneath the alpine snowpack.
Introduction
Ranunculus adoneus (the snow buttercup) emerges in full
bloom through snow at the edges of long-lived snowbanks at
elevations of approximately3000 to 4000 m in the Rocky Mountains. The environment of these snowbanks is characterizedby
low soil temperaturesand a short growing season (Billings and
Bliss, 1959) and R. adoneus possesses a suite of attributeswhich
allow it to complete its life cycle in this environment (Stanton
and Galen, 1989; Mullen and Schmidt, 1993; Scherff et al.,
1994). For instance, flowers of R. adoneus are heliotropic, thus
receiving the most benefit of sunlight and therefore insect pollinators throughoutthe day (Stanton and Galen, 1989). In addition this plant accumulates phosphorus (P) after seed set when
soil temperaturesare relatively high. This P is then stored over
the winter and re-mobilized early in the following season allowing R. adoneus to begin growing while soil temperaturesare
close to 0?C and the plants are still covered with snow (Mullen
and Schmidt, 1993). Phosphorus uptake coincides with the development of arbuscularmycorrhizal (AM) fungi in the roots of
R. adoneus indicating that these fungi are important to the P
nutrition of wild populations of R. adoneus (Mullen and
Schmidt, 1993).
Nitrogen (N) can be an importantlimiting nutrientto plant
growth in tundra systems (Chapin, 1980; Giblin et al., 1991;
Kielland and Chapin 1992; Bowman et al., 1993; Jonasson et
al., 1993). Nitrogen levels in the soil beneath alpine snowpacks
are highest just prior to, and during, snowmelt (Brooks et al.,
1996). This flush of N is probably in large part due to over
winter release of N from organic matter and microorganisms
(Kielland, 1990; DeLuca et al., 1992; Chapin et al., 1993;
Brooks et al., 1996). However, the fate of this N in alpine systems has not been determined. Studies in more temperate systems indicate that early spring N can be immobilized by soil
microorganisms and to a lesser extent by plants (Zak et al.,
1990). In addition, it has recently been demonstratedon Niwot
? 1998 Regents of the Universityof Colorado
0004-0851/98 $7.00
Ridge, Colorado that the some of early season N pulse is immobilized by soil microorganisms (Brooks et al., 1996, 1997).
Before the present study, the role of plants in immobilizing this
early season pulse has not been examined in any high elevation
tundraecosystem.
Our goal was to determineto what extent R. adoneus could
accumulate N released during snowmelt. We hypothesized that
N uptake would not be dependent on new root growth or AM
fungi because these structuresdevelop after the initial flush of
N (Mullen and Schmidt, 1993). We followed the temporal patterns of N uptake, root development and fungal colonization of
new and old roots of R. adoneus. This was done in a wild population of R. adoneus while we simultaneously measurededaphic factors over an entire growing season. In addition to providing
information about the physiological ecology of R. adoneus and
its fungal partners,this study also provides valuable information
about the fate of the early season N pulse that occurs in many
alpine systems.
Methods
STUDY SITE
The site for this study was Niwot Ridge, a Long-TermEcological Research Site (LTER) in the Colorado Front Range
(40?03'N, 105?36'W). The saddle on Niwot Ridge contains an
east-facing snowbed (3510 m elevation) which remains partially
unmelted until mid-August. Ranunculus adoneus is common
throughout this snowbed and is one of the few plants that is
active during snowmelt (Mullen and Schmidt, 1993). The sampling sites are on a slope (ca. 20?) and snowmelt water runs
through the site for most of July. Snow usually starts to accumulate at this site in October. The snowbed soil was characterized as a typic cryumbreptwith 6 to 16% organic matter and a
pH of 4.5 to 5.0 (Bums 1980).
R. B. MULLEN ET AL. / 121
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FIGURE 1.
Patterns of N accumulation in R. adoneus during the 1991 growing season. (a, left) Total
N (mean per plant) in roots and shoots of R. adoneus, (b, center) % N in the same roots and shoots,
possibly showing net movement of N from roots to shoots and (c, right) total amounts of plant N.
PLANT AND SOIL ANALYSES
During June and July, when plants were growing most rapidly, plants were collected biweekly. Toward the end of the
growing season plants were collected monthly. Collections consisted of six plants which were chosen as randomlyas possible,
but also with the objective of selecting plants of approximately
the same size and therefore,age. Each plant was removed with
sufficient soil to ensure that the entire root system was obtained.
Once collected, plants and soil were transportedimmediatelyto
the laboratoryand were stored at 4?C for a maximum of 24 h
before processing. Processing consisted of washing and separating plants into new roots, old roots, and shoots. New roots were
placed in preservative(as below) and old roots and shoots were
dried, weighed, ground and analyzed for total Kjeldahlnitrogen
using a hydrogen peroxide and salicylic acid digest (Haynes,
1980) and colorimetric analysis by a flow-injection analyzer
(FIA) (LACHATInstruments,Mequon, Wisconsin, USA).
Soil temperaturewas measured at each sampling date at
depths of 5 and 10 cm using a LI-Cor dataloggerwith thermocouple probes. Soil moisture was measured gravimetricallyby
drying to constant weight at 60?C to determine water content.
In addition, soil NH4+and NO3- were determinedby extraction
of fresh soil in a 2M KCl solution followed by analysis using a
Lachat FIA.
Density of R. adoneus at the study sites was quantifiedusing 20 x 20 cm squares that were tossed randomly (N = 62)
within the study area. The mean numberof plants per quadrant
was used to calculate the density of plants per square meter.
Time-course data were analyzed using ANOVAs. Bonferonni multiple comparisonswere performedto test for significant
differences among data (Judd and McClelland, 1989).
QUANTIFICATION OF MYCORRHIZAL DEVELOPMENT
New roots from each plant were measuredfor length, and
stored in F.A.A. (90% formalin,5% acetic acid, 5% ethanol).On
three sampling dates old roots from previous years were collected and also placed in F.A.A. Roots were stainedas described
in Mullen and Schmidt (1993). Roots were clearedin 10%KOH
in a boiling water bath for at least 1 h, acidified in 1% HCl for
20 min, and stained in cold lactophenoltrypanblue (0.05%) for
at least 12 h. Quantificationof fungal infection was done in a
manner similar to that of McGonigle et al. (1990). Roots were
cut into 2-cm sections and arrangedlengthwise on microscope
slides. Passes were made vertically across the slide at regular
intervals using a compound microscope (160x). When roots
were crossed an ocular crosshair was aligned perpendicularto
the long axis of the root and the presence or absence of fungi
122 / ARCTIC AND ALPINE RESEARCH
was recorded for the area directly under the crosshair. If the
crosshair intersected fungal structures,the type of fungus and
fungal structureswere recorded.The magnificationused was primarily 160X, althoughidentificationof specific structuressometimes required using a magnification of 400x. Using this approach it was possible to quantify the stages of mycorrhizaldevelopment in addition to total infection levels for each type of
fungus in the root. Infection is expressed as a percent of total
root length infected for each type of fungal structure.
Results
Preliminarymeasurementsfrom 1990 indicatedthat N uptake occurredvery early in the growthcycle of R. adoneus, prior
to our earliest samplingdates (datanot shown). Thus, duringthe
1991 season we began sampling when flowers of R. adoneus
first appearedthrough the melting snowpack in June. Seasonal
patternsof N accumulationand depletion in the shoots and roots
of R. adoneus during 1991 are presentedin Figure 1. During the
early part of the growing season a net uptake of N into plant
tissues was observed in both roots and shoots of R. adoneus
(Fig. 1). Some N also appears to have been translocatedfrom
roots to shoots. PercentN in the shoots of R. adoneus increased
significantly(P < 0.05) from late June to early July and this rise
coincided with a drop in percent N in the roots (Fig. lb). Even
accountingfor this translocationof N from roots to shoot a large
increase in N uptakewas observed from 25 June to 8 July (Fig.
ic). This early season uptake of N for the most part preceded
net shoot growth by R. adoneus. Shoots continued to increase
in mass until late July (Fig. 2) whereas net N accumulationhad
ceased by 8 July (Fig. 1).
Edaphic factors may have influenced N uptake by R. adoneus. N uptake occurred when soil temperaturewas rising and
soil moisture was declining (Fig. 3). In addition, NH4+was the
dominantinorganicN species in the soil duringthe early season
(Fig. 3c).
Because of the unique rooting phenology of R. adoneus
(Mullen and Schmidt, 1993), we were able to follow the patterns
of new root and mycorrhizal development in the same plants
from which the shoot N data were taken (Fig. 4). New root
growth reached its peak duringmid-July(Fig. 4a) at which time
arbuscularmycorrhizal(AM) infection was just beginning to increase (Fig. 4b). Thus, N accumulationoccurredbefore significant new root growth and well before AM fungi developed in
these new roots (Figs. lb, lc).
Arbuscularmycorrhizal and other fungal infection levels
also were monitored in old roots (i.e. roots that had over-wintered) of R. adoneus plants collected on three of the same dates
melt from the upper part of the snowbed was still flowing
through our site. In comparison, other alpine plants accumulate
N somewhat later in the growing season although they also tend
to accumulate more N in the first half of the growing season
than in the second half (Jaegeret al., 1997). Of the plants studied
to date on Niwot Ridge, however, R. adoneus seems to be alone
in its ability to exploit the very early flush of N associated with
snowmelt.
Our data indicate that early season N uptake by R. adoneus
may significantly impact N losses from this alpine system. Our
estimate that R. adoneus can immobilize approximately 0.53 g
N m-2 is similar to the level of N removal by a spring ephemeral
community in a deciduous forest of 0.55 g m-2 (5.5 kg ha-')
(Blank et al., 1980) and higher than the early season immobilization of N (0.1 g m-2) noted by Muller and Bormann (1976)
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for Erythronium americanum at Hubbard Brook.
In order to investigate the mechanism of early season N
uptake by R. adoneus, we quantifiedthe developmental patterns
of roots and mycorrhizalfungi associated with this plant. A number of studies have examined the presence of mycorrhizaein the
genus Ranunculus (Mullen and Schmidt, 1993; Read and Haselwandter, 1981; Vare et al., 1992, 1997), but none of these
studies examined the functional role of these fungi in the nitrogen nutrition of Ranunculus spp. In addition, there have been
very few previous studies relating the development of root systems to functioning of alpine plants (Barnolaand Montilla, 1997;
Mullen and Schmidt, 1993). In the present study, maximal N
accumulationin the field occurredat a time when almost no new
roots were observed on R. adoneus plants. Thus, we concluded
that new roots were not involved in early season N uptake by
R. adoneus. It is also possible to rule out a significant role for
AM fungi in the early season N nutrition of R. adoneus. The
peak in arbuscule levels in new roots of R. adoneus occurred
well after the period of maximal N accumulation. Although the
old roots of R. adoneus contained AM hyphae (data not shown),
arbuscules were very scarce in these roots early in the season
(Fig. 5). Because arbuscules are the site of nutrient transferbetween the fungus and plant (Smith and Smith 1989), a lack of
arbuscules is a strong indication that no nutrient transfer was
taking place between AM fungi and R. adoneus early in the
growing season.
In contrast to arbuscules, there were high levels of a dark
septate (DS) fungus in the over-wintered roots of R. adoneus
early in the season. Dark septate fungi are very common in high
elevation plants, but very little work has been done to determine
the functional role of these fungi and their role in N nutritionof
wild plants remains unknown (Haselwandter and Read, 1982;
Stoyke and Currah,1991; Wilcox and Wang, 1987). Haselwand-
FIGURE 2.
Biomass of shoots of R. adoneus during the 1991
growing season.
that the N measurements were made. Extremely low levels of
arbuscules were found in these old roots at all sampling dates,
but a dark septate (DS) fungus (Haselwandterand Read, 1982;
Trappe, 1988; Vare et al., 1992; Mullen and Schmidt, 1993) was
present at high levels early and late in the growing season (Fig.
5).
Discussion
Our interest in R. adoneus stemmed from our curiosity
about nutrient acquisition by plants as alpine snowbeds melt.
Ranunculus adoneus begins growth prior to other snowbed
plants, thus we hypothesized that N uptakeby R. adoneus would
occur at the beginning of its growing season during the early
season N flush observed by Brooks et al. (1996) at this site. In
addition, we also hypothesized that N uptake, in contrast to P
uptake (Mullen and Schmidt 1993) would not be dependent on
new root growth or AM fungi because these structuresdevelop
well after the initial flush of N. These hypotheses were substantiated in the present study.
Our results show that R. adoneus is able to take advantage
of the seasonal pulse of N availability. Recent studies at our site
indicate that N availability is very high just prior to and during
snowmelt (Brooks et al., 1996). Our results show that N accumulation occurred very early in the life cycle of R. adoneus,
tripling the amount of total N in plant tissues within 2 wk of
emergence. This net accumulationof N occurredwhen soil temperatures ranged between 0 and 8?C (Fig. 3a) and when soils
were still wet from snowmelt (Fig. 3b). During this time snow14
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FIGURE 3.
Edaphic factors during 1991. Measurements were taken in soil near sample plants. Soil
temperatures at depths of 5 and 10 cm (a, left), gravimetric soil moisture (b, center), and soil inorganic
N concentrations (c, right).
R. B. MULLEN ET AL. / 123
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FIGURE 4.
Development of new roots (a, left) and AM fungi in new roots (b, right) of R. adoneus
during the 1991 growing season. (data re-drawn from Mullen and Schmidt, 1993).
ter and Read (1982) showed that DS fungi can significantly increase P uptake and growth of the alpine sedge, Carex firma,
but they did not test the effects of the DS fungus on N nutrition
of that plant. In another alpine sedge, C. sempervirens,however,
Haselwandter and Read (1982) showed no effect of the fungus
on plant growth and speculated that a nutrientother than P may
have been limiting the growth of this plant in the P-deficient
sand system that they used.
The extent to which DS fungi may take up N or impart
nutrients to host plants is not known. At our site, N and P are
usually the limiting nutrients for plant growth (Bowman et al.,
1993). Thus, at a time when soils are relatively cold, new roots
are not yet functional, old roots are highly suberized (indicating
a decrease in nutrient uptake efficiency), and active AM structures are absent, R. adoneus is taking up large amounts of nitrogen from surroundingsoils. One explanation for this uptake is
that the DS fungus contributes to uptake of inorganic and organic N by this plant. Mycorrhizalfungi have been shown to aid
in uptake of organic N (Abuzinadahand Read, 1986; Bajwa and
Read, 1986) but this has not been demonstrated for DS fungi.
We have recently isolated the DS fungus from R. adoneus and
have shown that it can take up and utilize both NH4+and organic
forms of N at temperaturesas low as 2?C (Mullen and Schmidt,
unpublished data). Thus, the DS fungus has the potential to act
v)
O,
35--C,-
30
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-
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Dark septate fungi
VAMArbuscules
as a conduit for both organic and inorganic forms of N at temperaturesexperienced by early season roots of R. adoneus. They
also produce sclerotia, fungal storage structures,within the cortical cells of R. adoneus roots, which could be digested by the
plant cells. The role of these fungi deserves more investigation
given that these they are extremely common in plant roots and
soil and rarely cause pathogenic effects.
In conclusion, R. adoneus takes up the majority of its N
early in the season when snowmelt is occurring at andjust uphill
from the plants. These results may help explain why very little
N is lost from vegetated sites in the alpine even early in the
growing season (Brooks et al., 1996). The role that fungal endophytes play in this early season retention of N needs more
study.
Acknowledgments
We thank D. Lipson, T. Raab, and A. Yen for field and
technical assistance and Chris Schadt for comments on the
manuscript. This research was supported by EPA grant R823442-01, NSF grant IBN95-14123 and grants from Sigma Xi
and the Spokane Mushroom Club.
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124
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