~C>SCIENCE
4 (2): 170-178 (1997)
Growth responses of Carex ramenskii to defoliation,
salinity, and nitrogen availability: Implications for
geese-ecosystem dynamics in western Alaska!
Roger W. RUESS, Institute of Arctic Biology, University of Alaska, Fairbanks, Alaska 99775, U.S.A., e-mail: [email protected]
Daniel D. ULIASSI, Christa P. H. MULDER & Brian T. PERSON, Department of Biology and Wildlife, University of
Alaska, Fairbanks, Alaska 99775, U.S.A.
Abstract: The Yukon-Kuskokwim River Delta in western Alaska is the principal nesting area for several species of geese,
including Pacific black brant. Grazing by geese on Carex ramenskii, one of the most abundant plant species throughout
much of this region, appears to have increased in recent years. The purpose of this study was (i) to evaluate the effects of
early-season defoliation and fertilization on plant growth and nutrient cycling processes within field plots of C. ramenskii
over a 3-year period, and (ii) to study the interactive effects of defoliation, N availability, and salinity stress on growth, and
biomass and N allocation in C. ramenskii under controlled, greenhouse conditions. Relative to control plots, clipped-fertilized
plots showed significant increases in aboveground net primary production (AGNPP) and leaf N concentration, resulting in
significant increases in offtake biomass and offtake N during both 1991 and 1992. In the greenhouse, total production of
clipped and unclipped plants did not differ, but clipped plants had significantly higher offtake biomass, and biomass and N
allocation to offtake compared to unclipped plants. Both field and laboratory experiments found that rapid regrowth following
defoliation was dependent on soil nutrient availability. Fertilization increased soil respiration rates each year, but tended to
decrease rates of net N mineralization, indicating that the soil microbial biomass is a strong nutrient sink in this ecosystem.
In addition to the direct positive effects that goose feces have on plant growth, nitrogen recycled through feces may be an
important source of nitrogen contributing to salinity tolerance in C. ramenskii. Our results also suggest that the observed
increase in grazing pressure on patches of C. ramenskii early in the growing season may in.crease forage quality and quantity
within these swards, and have important implications for geese-ecosystem interactions at a time of rapid goose population
increase.
Keywords: goose grazing, nitrogen cycling, salt marsh, Alaska.
Resume: Le delta forme par les rivieres Yukon et Kuskokwim (ouest de l' Alaska) est Ie principal site de nidification de
plusieurs especes d'oies, dont la bemache cravant. Le broutage par les oies de Carex ramenskii, une des especes vegetales
les plus abondantes de la region, semble avoir ete plus intensif au cours des dernieres annees. Cette etude poursuivait deux
objectifs. En premier lieu, nous voulions evaluer, au cours d'une periode de trois ans et au sein de parcelles contenant des
individus de C. ramenskii, les effets de la defoliation hiitive des Carex et de la fertilisation sur la croissance des plantes et sur
Ie processus de recyclage des elements nutritifs. En second lieu, nous voulions etudier, en conditions controlees (serre), les
effets interactifs de la defoliation, de la disponibilite en azote et du stress dil 11 la salinite sur la croissance, la biomasse et
I' allocation en azote de C. ramenskii. Les parcelles defoliees et fertilisees ont une production primaire nette au-dessus de la
surface du sol et une concentration en azote des feuilles significativement superieures 11 celles des parcelles temoins. Cela a
entraine une hausse significative de la biomasse et d' azote consomme par les oiseaux en 1991 et en 1992. En serre, la pro­
duction totale des plantes defoliees et non defoliees n'a pas varie de fal<0n significative. Par ailleurs, les plantes defoliees
avaient une biomasse consommee et un taux de biomasse et d'azote disponible significativement plus eleves par rapport aux
plantes non defoliees. Les experiences sur Ie terrain et en serre montrent que la reprise de croissance rapide des plantes 11 la
suite de la defoliation depend de la disponibilite des elements nutritifs du sol. La fertilisation augmente les taux de respira­
tion du sol, mais tend 11 diminuer les taux de mineralisation de I'azote. Cela indique que la biomasse microbienne du sol
represente un puits important pour les elements nutritifs dans cet ecosysteme. En plus des effets positifs directs des feces
d'oie sur la croissance des plantes, I'azote recycle via les feces peut s'averer une source importante d'azote contribuant a
augmenter Ie niveau de tolerance 11 la salinite de C. ramenskii. Nos resultats suggerent egalement que I' augmentation de la
pression de broutage sur les communautes de C. ramenskii au debut de la saison de croissance peut augmenter la qualite et la
quantite du broutage au sein de ces communautes. Cela peut avoir des consequences importantes en ce qui a trait aux interac­
tions entre I'ecosysteme et les oies lors d'une periode caracterisee par une augmentation rapide du troupeau d'oies.
Mots-des: broutage par les oies, cycle de I'azote, marais sale, Alaska.
Introduction
The Yukon-Kuskokwim River (Y-K) Delta encompasses
a large expanse of coastal saltmarsh and inland wet meadow
ecosystems in western Alaska. The coastal landscapes of
this region, bounded on the north by Kokechik Bay (61 0 40' N,
166 0 7' w), and on the south by Hazen Bay (61 0 0' N, 165 0
15' w), are the principal nesting areas for black brant geese
lRec. 1996-04-26; acc. 1996-11-06.
(Branta bernicla nigricans), cackling Canada geese (B.
canadensis minima), greater white-fronted geese (Anser
albifrons frontalis) and emperor geese (A. canagicus). The
region is characterized by subtle elevational changes over
an area of approximately 160 000 km2 , and landscape patterns
in elevation, permafrost depth, and salinity are important
determinants of plant community distribution, and the asso­
ciated landscape selection and vegetation use by geese
(
ECOSCIE~E, VoL. 4 (2),
(Kincheloe & Stehn, 1991; Babcock & Ely, 1994).
Carex ramenskii (Kom) is the most abundant plant
species within river and slough levee meadows, and tidal
flat meadow communities. Together they constitute the
largest percentage of the coastal salt-marsh landscape in the
Y-K Delta (Tande & Jennings, 1986; Kincheloe & Stehn,
1991; Babcock & Ely, 1994). On average, the intensity and
frequency of goose grazing in these communities is substan­
tially less than that in Carex subspathacea swards, which
occur as monospecific grazing lawns along coastal mudflats
and along some inland ponds and slough margins. These are
similar to grazing lawns studied on the Hudson Bay lowlands
(Cargill & Jefferies, 1984 a,b; Bazely & Jefferies, 1985;
1989; Hik & Jefferies, 1990). However, in specific areas or
at certain times of the year, C. ramenskii is intensively
grazed. A common example of this is at the abrupt interface
between C. ramenskii and C. subspathacea-dominated
communities, where C. ramenskii is intensively grazed
throughout the growing season, and has a short, dwarfed
growth form strikingly similar to that of C. subspathacea.
Another habitat where C. ramenskii is frequently grazed
throughout the growing season is along the margins of
inland ponds, particularly in the vicinity of nesting brant
geese. Finally, during spring ice break-up, uneven patterns
of ice and snowmelt expose patches of C. ramenskii to grazing
by geese prior to nest initiation. In all these instances, it
appears that once grazed, repeated grazing shifts the growth
form of C. ramenskii to a shorter and potentially more palat­
able, rapidly-growing form that leads to repeated grazing
(pers.observ.).
Our observations, and those of other researchers working
on the Y-K Delta (C. Babcock, J. Sedinger, P. Flint, pers.
comm.), suggest that brant geese have begun to rely more
on C. ramenskii, particularly during ice break-up, and
during summer in swards close to the boundary with C.
subspathacea. The number of breeding pairs of black brant
at the Tutakoke River colony, one of the four major colonies
of the Y-K Delta, has increased recently from an estimated
1100 in 1986 to 4601 in 1993 (Sedinger et at., 1993), and
distribution of C. subspathacea grazing lawns in the region
may actually be limiting relative to this population increase.
One of the purposes of this study was to begin to evaluate
the consequences of this early-season grazing on C. ramen­
skii meadows, by examining plant growth characteristics
and nitrogen cycling processes in response to defoliation
and fertilization within C. ramenskii swards over 3 years.
An additional purpose of this study was to determine
the importance of soil nitrogen availability to salinity
tolerance in C. ramenskii. Along the Bering Sea coast and
inland slough levees, the average elevation above mean
high tide of Carex ramenskii communities ranges from 5 to
20 cm above that of C. subspathacea swards. This results in
C. ramenskii communities being flooded less frequently
than C. subspathacea, which can be subjected to daily sea
water inundation (Kincheloe & Stehn, 1991). However,
along the upper margins of C. subspathacea swards, where
C. ramenskii is subjected to more frequent flooding and
intensive grazing, higher rates of nitrogen cycling by geese
(Jefferies, 1988; Ruess, Hik & Jefferies, 1989) may improve
salinity tolerance in C. ramenskii by increasing the avail-
1997
ability of nitrogen for the synthesis of nitrogen-based
osmoregulators. We tested this hypothesis by examining the
interactive effects of defoliati.on, N availability, and salinity
stress on growth, and biomass and N allocation in C.
ramenskii under controlled greenhouse conditions.
Our results indicate that grazing may indeed increase
the productivity and nutrient content of C. ramenskii swards,
and create the potential for C. ramenskii swards to serve as
alternative foraging habitats for geese.
Material and methods
FIELD EXPERIMENT
Twelve plots (1 m2 in a grid separated by 1 m walkways)
were established in a large wet meadow of Carex ramenskii
in early June 1991. We recognize that plots separated by
such short distances do not represent true replicates; never­
theless, we assume that these plots are representative
vegetation and ecosystem responses of the surrounding
landscape. Plots were assigned to one of 4 experimental
treatments in a factorial design that included clipping (+/-)
and fertilization (+/-). Clipped plots were clipped once at
the beginning of the growing season each year to a height of
3 cm to simulate spring time grazing. Fertilized plots
received slow release fertilizer in early spring each year that
supplied 10 g m-2 each of N, P, and K. Standing biomass
was sampled in all plots at the time of clipping, and again at
the peak of the growing season in late July by clipping all
vegetation within one 15 cm x 15 cm quadrat placed random­
ly within each plot. Samples were dried in a field laboratory,
then taken to Fairbanks and redried at 60°C, weighed, and a
subsample analyzed for total N on a LECO CNS 2000 auto­
analyzer. Net aboveground primary production (AGNPP)
was calculated as the difference between biomass harvest­
ed in late July minus that harvested in early June. We used
the term total offtake biomass to refer to the total above­
ground biomass clipped above the 3 cm height. Total off­
take biomass in unclipped plants was material clipped at
final harvest, while total offtake biomass in clipped plants
was the sum of material clipped in the spring and that
clipped at the final harvest. AGNPP was measured at inter­
vals of 45, 48, and 43 days during 1991, 1992, and 1993,
respectively. In 1993, depth of thaw was measured at 3
points within each plot on 4 June, 15 June, and 30 June
using a 1.5 m steel rod.
One soil core (5 cm diameter x 10 cm depth) .was
collected from each plot at the time of final harvest each
year, stored in a polyethylene bag in a portable cooler, and
sent within 24 hours to the laboratory in Fairbanks. Each
core was split vertically into 2 laboratory replicates, and
approximately 25 g dry weight of soil was incubated in a
497 mL mason jar in the dark at 12°C for 30 days. Soil
respiration was measured every 10 days with the use of a
Shimadzu 8A gas chromatograph. Net N mineralization rate
was taken as the difference in mineral N (NH 4+ + N0 3-)
extracted with 2N KCI at day 30 and day 0 of the incuba­
tion. Total soil Nand C were measured on the LECO CNS
2000 autoanalyzer.
LABORATORY EXPERIMENT
Small plugs of Carex ramenskii (10 cm diameter x 15 cm
171
\.
RUESS ET AL.: GROWTH RESPONSES IN CAREX RAMENSKII
depth) were removed over a 100 m2 area from a wet meadow
near the Tutakoke River in late July and sent to Fairbanks
where they were kept outside in 15 cm deep tubs and
allowed to senesce and winter harden. Plants were moved
into the greenhouse in early winter, sub-divided into small
plugs (approximately 10 tillers per plug) and placed in 20 cm
pots containing equal amounts of perlite, vermiculite, and
peat moss. All plants were treated with distilled water
(every 2 days) and a dilute nutrient solution (113 Hoagland's
every 4 days) for 2 weeks as a preconditioning treatment.
Eighty pots were randomly assigned to one of 8 treatments
in a full 23 factorial design that included 2 levels each of
nitrogen, clipping, and salinity. Plants were grown for 12
weeks under an 18-hour photoperiod and PPFD of approxi­
mately 600 ,umol m- 2 s-1 provided by HPS lighting. High
(14 mM) or low (1 mM) N was provided every 6 days as a
balanced mixture of NH 4 + and N0 3 -; each solution had
equal proportions of other macro- and micro-nutrients.
Nutrient solutions were adjusted to a pH of 6.7 with either
HCI or NaOH. Salinity treatments consisted of either 0 or
19.5 g NaCI per liter (0 and 19.5 %0 salinity), mixed as a
component of the nutrient solution. Plants were either
unclipped or clipped every 3 weeks to a height of 3 cm. All
pots were flushed with distilled water every 10 days to
prevent salt and/or nutrient accumulation. Plant water
potential was determined on a similarly aged, fully-expanded
leaf from 6 randomly selected pots from each treatment at
mid-day prior to harvest using a Pressure Bomb (PMS
Instrument Co., Corvallis, Oregon). It is likely that because
of restricted pot volume at the end of the experiment, plants
were more water stressed at this time than would be expected
in the field; nevertheless, we believe treatment differences
among plant water potential measurements are reflective of
plant responses to actual field conditions.
At harvest, all aboveground biomass was clipped to a
3 cm height on all plants, and the total number of tillers was
counted. Roots were washed free of potting mixture, and all
tissues were dried at 60°C for 48 hours, and weighed to the
nearest mg. Total offtake biomass in unclipped plants was
material clipped at final harvest, while total offtake bio­
mass in clipped plants was the sum of material clipped
throughout the experiment including that at the final harvest.
Aboveground biomass below 3 cm height was termed
aboveground residual biomass. Root to shoot ratio was
calculated as the ratio of root to aboveground biomass, the
latter being the' sum of offtake and aboveground residual
biomass.
After weighing, tissues were ground in a Wiley Mill
and analyzed for total N as described above. Tissue N mass
was the product of tissue weight and %N. Total plant N
uptake was the ratio of total plant N mass to root mass
(Ruess, 1988).
Field and greenhouse data were analyzed by ANOVA
using a general linear models procedure, and a repeated
measures ANOVA was used to evaluate interannual effects
for the field experiment (SAS, 1985). Biomass data were
log transformed and proportional data were arcsin square
root transformed where necessary to meet ANOVA assump­
tions. In the greenhouse experiment, five plants from various
treatments died during the experiment and were omitted
172
from the analyses. Data presented from both experiments
represent true means ± standard errors. Treatment effects
expressed as a percent change in the mean use true means
for the field experiment, but for the greenhouse experiment,
use least squares means derived from PROC GLM for
unbalanced designs (SAS, 1985).
Results
FIELD EXPERIMENT
In the first year of treatments (1991), addition of nutrients
significantly increased peak season biomass (+ 64%), off­
take biomass (+ 46%), and AGNPP (+ 96%) compared with
corresponding values for untreated plants (Figures 1 and 2).
Although clipping did not significantly affect peak season
biomass (P = 0.10), both offtake biomass (+ 31 %, P < 0.05)
and AGNPP (+ 57%, P < 0.05) were higher in clipped versus
unclipped plots. The highest values of offtake biomass
(891.1 ± 36.4 g m- 2) and AGNPP (488.4 ± 36.4 g m-2 48 d- 1)
were measured in plots which were both clipped and
fertilized.
In 1992, treatment differences in standing biomass
early in the season paralleled patterns of AGNPP measured
in 1991. The addition of nutrients had similar effects on
plant growth in 1992 as in the previous year, increasing
peak season biomass (+ 66%), offtake biomass (+ 81 %),
and AGNPP (+ 73%, p = 0.11). Clipping significantly
decreased peak season biomass, although less so when
plants received high amounts of nutrients (P = 0.08), but it
had no significant effect on offtake biomass or AGNPP.
Overall, 1992 was a more productive year, particularly for
unclipped plots. Peak season biomass averaged 58%
greater, while AGNPP (when expressed per day) was more
than double values for unclipped plots in 1991. However,
increases in offtake biomass (+ 27%) and AGNPP (+ 18%)
in 1992, relative to values for 1991, were less in plots that
were both clipped and fertilized, and clipped plots showed a
22% decline in offtake biomass and a 2% decline in
AGNPP in 1992 compared to values for 1991. Unfortunately,
several plots were grazed by geese in the early spring of
1993, and all plots were grazed heavily by geese prior to
final harvest in 1993, preventing reliable estimates of
AGNPP.
Fertilization increased the N concentration in peak
season biomass each year (Figure 3), but there were no
significant carry-over effects on early season plant N
content the following year. Clipping had no overall effect
on N content of early or peak season biomass in any year.
However, during 1991 and 1993, clipping tended to
increase plant N content on unfertilized plots, and decrease
the plant N content on fertilized plots.
Treatments had no effect on total soil C or N content,
and no differences were detected in these soil variables
among years. Averaged across years and treatments, these
values (%DWT) were: C = 4.95 ± 0.24, and N = 0.266 ±
0.012. In 1991, clipping significantly reduced soil water
content when measured in late July (- 7%, P < 0.05), while
fertilizer additions tended to increase soil water content
(+ 5%, P = 0.12). No treatment effects on soil water were
found in 1992, but in 1993 fertilization increased soil water
\
"~
ECOSCIENCE,
VOL.
4 (2), 1997
1991
1200 ....
i 1D
1000
NUT·"
_NUT·"CLP"
800
600
400
200
0
1992
1400
]
1200
---
~
FIGURE 2. The effects of clipping (± CLP) and fertilization (± NUT) on
aboveground net primary production (AGNPP) during 1991 and 1992.
Abbreviations follow Figure 1.
DNUT·"
_ NUP" ··CLP
_NUp··
1000
800
'-'
~
600
Q
400
e
=
200
0
FIGURE I. The effects of clipping (± CLP) and fertilization (± NUT) on
aboveground biomass at the beginning of the growing season (open bars),
aboveground peak season biomass in late July (solid bars), and offtake
biomass (gray bars) during 1991-1993. Data represent means ± SE (n =3).
Legend bars indicate primary (NUT or CLP) and interactive (CLPNUT
clipping x fertilization interaction) treatment effects, where asterisks
following abbreviations indicate +NUT > -NUT, or +CLP > -CLP at p <
0.10·, 0.05", 0.01 ..•. Asterisks preceding abbreviations indicate the
opposite effect.
=
in unclipped plots (+ 15%, p < 0.05), and tended to decrease
soil water in clipped plots (- 11 %, p = 0.11). During 1991,
1992, and 1993, mineral N (NH4 + + N0 3-) was significantly
higher in fertilized plots (27.5, 54.10, and 23.82 Jig g-I dry
weight of soil) compared with unfertilized plots (9.72, 9.65,
and 3.04 Jig g-l dry weight of soil, respectively), as was
extractable phosphorus (0.08 versus 0.02 Jig g-l dry weight
of soil, measured in 1993 only).
Fertilization stimulated soil respiration rates every year
(Figure 4). Clipping had no significant effect on soil respi­
ration rates overall. Soil respiration in all years was posi­
tively correlated with soil water content (Figure 5). Soil
respiration rates did not vary among years, and there were
no differences in treatment effects on respiration rates
between years.
Rates of net N mineralization varied significantly
among years (P < 0.0001). Net N mineralization was
unaffected by treatments in 1991, and averaged 0.34 ± 0.10
Jig N g-l dry weight of soil dol across all plots. Fertilization
significantly reduced net N mineralization in 1992 (p <
0.0001), and caused a slight decline in net N mineralization
in 1993 (Figure 6).
In 1993, depth of thaw was similar across all plots in
early June, averaging 28.7 ± 0.8 cm. By 15 June, depth of
thaw of fertilized plots (38.7 ± 1.4 cm) was significantly
less than that in unfertilized plots (43.0 ± 0.9 cm, p < 0.01),
and clipped plots (42.2 ± 1.0 cm) showed a slight increase
in depth of thaw compared with unclipped plots (39.3 ±
1.7 cm, p = 0.06). These patterns continued until 30 June,
and although statistical differences among treatments disap­
peared, fertilized only plots still showed the least depth of
thaw (58.3 ± 2.6 cm) and clipped/fertilized plots the great­
est depth of thaw (76.3 ± 17.3 cm).
LABORATORY EXPERIMENT
PLANT GROWTH AND BIOMASS ALLOCATiON
Among the three treatments, salinity had the largest
effect on plant growth, decreasing total plant mass an aver­
age of 40% (p < 0.0001, Tables I and II) at high salinity
compared to growth in the absence of sodium chloride.
Salinity reduced root mass (- 39%), aboveground residual
mass (-18%), offtake mass (- 60%), biomass allocation to
offtake (- 21%) (allp < 0.0001), and tiller production (- 22%,
p < 0.05). The water potential of high salt plants (-4.2 ± 0.2
MPa, n = 30) was significantly less than that of low salt
plants (-2.3 ± 0.2 MPa, n = 30). Salinity had no overall
173
RUESS ET AL.: GROWTH RESPONSES IN CAREX RAMENSKII
~
TABLE I. The effects of clipping, salinity, and nitrogen (N) availability on biomass (g), biomass allocation (%), tissue N content (%), total
plant N uptake (mgN g roor l ) and leaf K+ and Na+ content (mg g-l) of Carex ramenskii. Data represent means ± 1 SE (n = 10)
Unclipped
Clipped
-SALT
-N
-SALT
+SALT
+SALT
+N
-N
+N
-N
+N
GROWTH AND BIOMASS ALLOCATION
1.21 ±0.11
Offtake
Aboveground residual
2.10 ± 0.17
12.19 ± 1.37
Root
15.50 ± 1.32
Total
Allocation to offtake
8.0 ± 0.6
Root: shoot ratio
3.8 ± 0.5
Number of tillers
121 ± 10
6.60 ± 0.28
4.46 ± 0.24
10.78 ± 0.61
21.84 ± 0.92
30.3 ± 0.9
1.0 ± 0.1
209 ± 27
0.78 ± 0.11
2.07 ± 0.21
7.39 ± 1.11
10.24 ± 1.06
8.2 ± 1.1
2.8 ± 0.5
94± 8
2.49 ± 0.19
3.56 ± 0.30
7.32 ± 1.21
13.38 ± 1.38
19.5 ± 1.5
1.2 ± 0.2
172±19
1.53 ± 0.09
2.08 ± 0.16
10.37 ± 1.30
13.99 ± 1.40
11.4±0.7
2.9 ± 0.3
134 ± 10
8.82 ± 0.24
4.90 ± 0.42
10.89 ± 1.07
24.61 ± 1.31
36.6 ± 1.9
0.8 ± 0.1
230 ± 25
1.28 ± 0.15 2.66 ± 0.20
2.30 ± 0.10 3.14 ± 0.15
7.29 ± 1.65 4.72 ± 0.80
10.87 ± 1.57 10.53 ± 0.95
14.0 ± 2.7
26.4 ± 2.2
2.2 ± 0.6
0.8 ± 0.1
105±9
159 ± 15
NUTRIENT RELATIONS
Plant N uptake
Offtake N
Aboveground residual N
RootN
LeafK+
LeafNa+
31.5
2.08
1.87
1.07
33-.58
0.59
14.1 ± 1.4
1.60 ± 0.05
1.30 ± 0.03
0.75 ± 0.03
21.91 ± 0.52
43.79 ± 5.88
37.0 ± 2.9
2.26 ± 0.06
1.95 ± 0.04
1.73 ± 0.11
27.73 ± 0.90
20.70 ± 2.03
10.0 ± 0.4
1.66 ± 0.05
1.06 ± 0.04
0.54 ± 0.01
34.44 ± 1.18
0.05 ± 0.02
43.5 ± 4.6
2.80 ± 0.07
1.73 ± 0.05
1.32 ± 0.15
39.19 ± 0.62
0.32 ± 0.02
18.7 ± 2.6
50.1 ±
2.02 ± 0.09 2.94 ±
1.21 ± 0.07
1.79 ±
0.90 ± 0.07
1.63
37.16 ± 1.16 37.35
1.48 ± 0.42
1.68
8.9 ± 0.5
1.31 ± 0.03
1.04 ± 0.01
0.54 ± 0.01
33.74 ± 0.43
1.05 ± 0.12
± 1.3
± 0.05
± 0.07
± 0.03
± 0.91
± 0.04
effect on root to shoot ratio.
High N increased total plant mass by 39% (p < 0.0001).
This was primarily a function of significant increases in
aboveground tissues, resulting in an increase (+ 173%) in
biomass allocation to offtake (all p < 0.0001). While N had
no significant effect on root mass, high N plants had signifi­
cantly lower root: shoot ratios compared with low N plants
(p < 0.0001). High N also increased total number of tillers
(+ 68%, p < 0.001). Nitrogen had no effect on plant water
potential.
Clipping had no overall effect on total plant biomass,
although clipping significantly affected patterns of biomass
allocation. For example, clipping increased offtake mass
(+ 27%, P < 0.0001) and biomass allocation to offtake
(+ 32%, P < 0.0001). Clipping had a minor effect on root
mass (- 10%, p = 0.18), but reduced root:shoot ratio (- 22%,
p < 0.05) due to an allocation shift that favoured above­
ground growth. Clipping had no effect on tiller production
(+ 3%, P = 0.50).
-N
+N
6.2
0.05
0.06
0.13
0.60
0.26
The largest number of significant treatment interactions
occurred between salinity and N, due to the fact that high
levels of salinity reduced plant responses to N. For example,
N increased total plant mass by 57% under low salt condi­
tions (p < 0.0001), but by only 14% (p = 0.27, n.s.) under
high salt. Similarly, N-induced increases in offtake biomass
were over twice as high at low salt compared with values
under the high salt treatment. Nevertheless, when grown
under high salt concentrations, N availability had a signifi­
cant positive effect on plant growth. Of particular relevance
to herbivory was the response of offtake biomass to added
N, which more than doubled in high salt plants (p < 0.05).
High N caused a slight improvement in plant water potential
in clipped plants grown on high salt (+ 10%, n.s.).
Clipping increased offtake mass more when plants
were grown at low salinity (+ 33%, P < 0.0001) compared
to when plants were grown at high salinity (+ 23%, P =
0.07). No other significant interactions between salinity and
clipping were found, although there were some interesting
TABLE II. ANOVA results listing percentage of significant variance explained by primary and interactive effects of clipping, salinity, and
N availability on components of growth allocation, and nutrient relations in Carex ramenskii (P < 0.05*,0.01 **,0.001 ***)
GROWTH AND BIOMASS ALLOCATION
Offtake
Aboveground residual
Root
Total
Allocation to offtake
Root shoot ratio
Number of tillers
NUTRIENT RELATIONS
Total plant N uptake
Offtake N
Aboveground residual N
RootN
LeafK+
LeafNa+
a Low salt> high salt.
b HighN > low N.
c Clipped> unclipped.
174
Salt
Nitrogen
24.4***a
5.9***a
28.2***a
39.1 ***a
4.5***a
49.6***b
54.7***b
9.8**a
3.4**
4.6***
3.5***
14.5***
15.9***a
28.9***
15.9***b
65.4***b
45.0***
36.4***b
63.5***b
62.1 ***b
62.8***b
8.2***b
5.4***
Clip
2.2**c
6.4***c
2.9*
Salt x N
18.0***
7.5***
Salt x clip
0.7**
N x clip
0.5**
7.8**
7.3***
2.7*
5.0**c
23.1 ***c
1.1 *c
0.6*
1.1*
41.6***c
19.7***
1.3*
5.9***
Salt x N x clip
1.0**
2.5*
2.0*
0.9*
14.5***
19.4***
2.7**
1.4*
5.0***
2.8***
\
\
ECOSCIENCE, VOL. 4 (2),1997
1991
2.5
120
110
100
QI ....
~-c 90
80
~ 70
60
,~~
Q..
'"QlO.... 50
40
30
's
0.0
VJ~
'-'
20
10
D
•
NUT·..·CLp..
1991 0 NUT' CLPNUT*
1992 • NUT'
1993 • NUT'
~
2.0
......
.g=.:. 1.5
.:U
1.0
0.5
o
o
-CLP
-CLP
+CLP
-NUT
[~
~
-=
g
2.0
+NUT
=
1.5
1.0
....'2~
0.5
I
I
+CLP
-CLP
-CLP
-NUT
+CLP
+NUT
1993
2.5
D
•
CLP'
NUT····
2.0
1.5
1.0
Nitrogen availability accounted for the largest increases
in tissue N concentrations and total plant N uptake
(TPNUP) (Tables I and II). Clipping had substantial effects
also, significantly increasing N concentrations in offtake
biomass and TPNUP compared with corresponding values
for unclipped plants. These clipping effects were greater
when plants were grown on high N, and N-induced increases
in both offtake N concentration and TPNUP were greater in
clipped plants compared with unclipped plants (both nitro­
gen x clipping interactions p < 0.001) (Tables I and 11),
Salinity also increased aboveground and belowground N
concentrations, and total plant N uptake (all p < 0.001).
These concentration increases were offset by reduced plant
size, resulting in a 58% reduction in offtake N mass in high
salt versus low salt plants. However, increases in plant N
uptake and tissue N concentrations were not simply a func­
tion of reduced plant size, since plant size, when used as a
covariate, did not significantly influence the positive effects
of salt on plant N accumulation.
0.5
o
+NUT
FIGURE 4. The effects of clipping (± CLP) and fertilization (± NUT) on
soil respiration rates during 1991-1993. Abbreviations follow Figure I.
NITROGEN UPTAKE AND ALLOCATION
..:l
o
+CLP
clipped plants (- 16%, p < 0.05) than in unclipped plants
(- 28%, P < 0.001). These interactive responses to clipping
and salinity were, in general, independent of N treatment.
NUT··..
C.l
g~
-CLP
-NUT
+CLP
'-'
~
+CLP
1992
2.5
~
-CLP
_'L...----I_
200
---.-1991 r2 =0.43,p<0.001
-A-1992r2 =0.41,p<0.0011
--+- -1993 r2 = 0.33, p < 0.01
180
I
I
-CLP
+CLP
·NUT
-CLP
+CLP
+NUT
FIGURE 3. The effects of clipping (± CLP) and fertilization (± NUT) on
nitrogen content of aboveground shoots sampled peak season 1991-1993.
Abbreviations follow Figure 1.
~;;- 160
~'Z. 140
~~ 120
.Q..
~~ 100
'" ...
1:8
~~
trends. For example, clipping reduced root growth and
root:shoot ratios more when plants were grown on high
salinity (- 18% and - 26%, respectively) compared to when
plants were grown at low salinity (- 7%, and - 23%, respec­
tively), The result of these responses was that biomass allo­
cation to offtake biomass was less sensitive to salinity in
..
~"CI
••
.
•
._ -------­
.... ...... ~~-.
.~
..~~'i.! •
80
60
40
20
•
1
~-----.\
~""'-"".--
"""'T'"
40
45
.
i i i
50
55
60
65
70
Soil water content (g H 20 gdwt"l)*l00
FIGURE 5. Relationship between soil respiration rate and soil water
content for 1991-1993.
175
\
RUESS ET AL.: GROWTH RESPONSES IN CAREX RAMENSKII
...
,­
-0
~
"'Cl
ZO!l ­ 1
~
I
.5
1
l'-2l
-3
1991 0
1992 . . *NUT
1993 . . *NUT
...1'''''""--
_
-CLP
+CLP
-NUT
-CLP
+CLP
+NUT
FIGURE 6. The effects of clipping (± CLP) and fertilization (± NUT) on
net nitrogen mineralization rates during 1991-1993. Abbreviations follow
Figure 1.
Na+ AND K+ CONTENT
Salinity markedly increased leaf Na+ content (p <
0.0001), and decreased, but to a lesser degree, leaf K+
content (p < 0.0001; Tables I and II). Clipping decreased
leaf Na+ content (- 95%, p < 0.0001), and increased leaf K+
content (+ 27%, P < 0.0001). High N also decreased leaf
Na+ content (- 58%, p < 0.0001) and increased leaf K+
content (+ 11 %, P < 0.0001). When grown on high levels of
salt, clipped plants maintained lower Na+ concentrations
and higher K+ concentrations compared with corresponding
values for unclipped plants (both interactions p < 0.0001).
High N significantly reduced leaf Na+ content (- 61 %, p <
0.0001) and increased leaf K+ content (+ 17%, P < 0.0001)
when plants were grown on high salt. Among all high salt
high N plants, clipped plants had significantly lower leaf
Na+ concentrations (1.68 ± 0.26 mg g-I) and higher K+/Na+
ratios (26.14 ± 3.36 mg mg- I g-I) compared with unclipped
plants (20.70 ± 2.03 mg g-I and 1.42 ± 0.14 mg mg- I g-I,
respectively).
Discussion
Our field experiment suggests that intensive, early­
season grazing by geese may significantly increase the
aboveground production and nitrogen content of C. ramen­
skii swards. Relative to control plots, clipped-fertilized plots
showed significant increases in AGNPP and leaf N concen­
tration, which resulted in significant increases in offtake
biomass and offtake N during both 1991 and 1992. When
grown in the greenhouse, total production of C. ramenskii
clipped every three weeks did not exceed that of unclipped
plants, but clipped plants had significantly higher offtake
biomass, and biomass and N allocation to offtake compared
to unclipped plants. Similar growth responses following
goose grazing in the field would suggest that forage quantity
could be increased without any net change in primary
production, by geese modifying patterns of plant biomass
allocation.
Both field and laboratory experiments demonstrate that
rapid regrowth of C. ramenskii following defoliation is
176
dependent on soil nutrient availability. These results are
consistent with a large number of other greenhouse
(McNaughton & Chapin, 1985; Georgiadis et aI., 1989) and
field studies (Bazely & Jefferies, 1985; Maschinski &
Whitham, 1989; Hik & Jefferies, 1990). We recognize that
our fertilization treatment (10 g N m-2 year-I) exceeded the
expected N deposition by geese during a single grazing
event. For example, if 65% of the N removed (309.8 g m-2
of early season biomass, containing 1.04% N) was returned
in a plant available form (1. Sedinger, unpubl. data), we would
expect approximately 2 g N m- 2 deposited. Nevertheless,
clipping without fertilization substantially increased
AGNPP (+ 42%), foliage N content (+ 14%), offtake
biomass (+ 36%), and offtake nitrogen (+ 53%) relative to
corresponding values for untreated plots during 1991.
Although this response was not observed in 1992, AGNPP,
offtake biomass, foliage N content, and offtake N were all
significantly higher in clipped/fertilized plots compared
with plots only fertilized during both 1991 and 1992. These
results support the notion that canopy removal alone stimu­
lates aboveground growth, and that grazed plants are more
capable of responding to added nutrients than ungrazed
plants. Mechanisms responsible for these responses have
been reviewed by Hik & Jefferies (1990), who found that
total aboveground N uptake by grazed swards of Puccinellia
phryganodes exceeded the sum of the amount of N returned
in feces plus that taken up by ungrazed plants.
In addition to removing older, slower growing tissues,
canopy removal in Carex ramenskii swards likely increases
light, and in particular, heat flux to emerging shoots. The
tendency for greater depth of thaw on grazed plots, and
reduced depth of thaw on fertilized plots supports this latter
idea. Increased soil heat flux may be particularly important
in arctic and subarctic ecosystems, where net N mineraliza­
tion rates have been shown to be highly temperature sensi­
tive above a given threshold (Nadelhoffer et al., 1991).
Although higher soil temperatures may reduce soil moisture
content, and thus soil microbial processes later in the season
(Figure 5), we suspect soil moisture does not limit microbial
processes in early spring, and that increased soil heat flux
following canopy removal by geese may notably inqease
soil nutrient turnover.
Fertilization increased soil respiration rates each year,
but tended to decrease rates of net N mineralization, indi­
cating that the soil microbial biomass is a strong nutrient
sink in this ecosystem. Relative to arctic tundra north of the
Brooks Range, Carex ramenskii meadows have an order of
magnitude less percentage soil C and lower C:N ratios, but
similar respiration rates per gram C. For example, Kielland
(1990) found that soils from Carex aquatilis/Eriophorum
vaginatum wet meadows (39.4% soil C, C:N ratio = 34.6)
had respiration rates averaging 65.8 pg CO 2-C g soil C-I
hour 1. In 1993, soil respiration rates from our unfertilized
and fertilized plots averaged 49.4 and 76.8 pg CO 2.:Cg soil
C-I hour-I, respectively. Thus, while Carex ramenskii
meadows overlay younger surfaces with less organic matter
accumulation, the physical, chemical, and biological
constraints controlling soil C turnover are similar to those in
arctic tundra. The high ratio of C respiration to net N miner­
alization we found, particularly on fertilized plots, suggests
ECOSCIENCE, VOL. 4 (2),1997
.-/
that nutrient availability may be more important than
substrate quality in regulating soil microbial processes.
Using a buried bag method, Giblin et al. (1991) also found
negative net N mineralization during the growing season
(July-August) in several arctic ecosystems, including wet
sedge tundra. Primary production is strongly limited by
nutrient availability in Carex ramenskii meadows, as indi­
cated by the dramatic response to fertilization. For example,
in 1991, 83% of the N added to unclipped plots was
recovered in aboveground biomass at the end of the season.
If our N mineralization rates are representative of mineral N
production in the field, then clearly other sources of N
would be required to meet plant demand. It is likely that
direct uptake of amino acids by Carex ramenskii plays an
important role in N cycling in these ecosystems, as has been
shown for Carex aquatilis and Carex bigelowii growing in
arctic wet meadow and tussock tundra (Kielland, 1990;
1994).
We found that higher N concentrations in both shoots
and roots, and higher total plant N uptake of high salt plants
were due to factors other than simply reduced growth
relative to N uptake, suggesting nitrogenous osmotic solutes
may be important for osmoregulation and/or enzyme osmo­
protection in this species (Blits & Gallagher, 1991; Hasegawa
et aI., 1994). Because these compounds often constitute a
significant portion of the total nitrogen budget (Jefferies &
Rudmik, 1991), increased plant nitrogen uptake or changes
in nitrogen allocation patterns are often required. This may
partially explain why clipping, which increased plant N
uptake and tissue N concentrations, also increased plant
water potential. Of particular relevance to herbivory was the
response of offtake biomass to added N, which more than
doubled in high salt plants (p < 0.05). Throughout western
and southwestern Alaska, C. ramenskii occupies moderately
saline marshes and wet meadows (Snow & Vince, 1984;
Vince & Snow, 1984; Kincheloe & Stehn, 1991; Babcock
& Ely, 1994). Given the high nitrogen demands associated
with N-based osmoregulation, the nitrogen recycled through
goose feces may be an important source of nitrogen con­
tributing to salinity tolerance in C. ramenskii throughout
these coastal saltmarsh regions. We suspect that such an
indirect effect of geese on plant salt tolerance may also
contribute to the observed growth stimulation of the more
salt-tolerant and more heavily grazed species Carex sub­
spathacea within dense grazing lawns along the Bering Sea
coast (Person, unpubl. data) and in eastern Canadian salt
marshes (Hik & Jefferies, 1990).
In addition to the potential importance of organic solute
accumulation, Carex ramenskii may mediate osmotic
adjustment through changes in ion accumulation. Elevated
leaf K+/Na+ is one mechanism associated with reducing ion
toxicity in salt-tolerant species, although it is not entirely
clear whether K+/Na+ selectivity occurs within the root or at
the level of the leaf plasmalemma, or both. Nor is it under­
stood if such selectivity is mediated by increased K+ and/or
reduced Na+ influx, or how the process affects ion compart­
mentation within the leaf (Hasegawa et al., 1994). We
found that defoliation and fertilization independently
contributed to elevated leaf K+/Na+ concentrations, and that
when grown on high salt, the highest values were found in
plants that were both clipped and fertilized. Given that
greater soil surface evaporation may exacerbate soil salin­
ization on grazed swards (Srivastava & Jefferies, 1995),
physiological adjustments in mechanisms for salt tolerance
are likely essential for maintaining rapid rates of growth by
C. ramenskii when grazed.
While plant communities on the Y-K Delta occupy
topographic zones with distinct edaphic characteristics
(Kincheloe & Stehn, 1991; Bab<;:ock & Ely, 1994), grazing
by geese strongly influences the dominance among Carex
species within a community. For example, within the C.
subspathacea grazing lawns surrounding inland ponds,
exclusion of geese for 2 years resulted in complete domi­
nance of the sward by C. ramenskii (J. Sedinger, unpubl.
data). In contrast, when a C. ramenskii sward is subjected to
frequent, intensive grazing, C. subspathacea can become
dominant within a growing season (pers. observ.). During
spring snowmelt, exposed islands of C. ramenskii are often
grazed heavily by early-arriving breeding and non-breeding
Pacific black brant geese. The present experiments suggests
such intensive, but infrequent defoliation may improve forage
quantity and quality to geese, particularly if accompanied
by increased soil nitrogen availability. Such plant responses
to grazing likely explain why these patches are in many
instances regrazed throughout the growing season. Moreover,
tolerance of C. ramenskii to salinized soils, resulting from
greater surface evaporation on trampled surfaces defoliated
by geese, may be linked to improved plant nitrogen balance
derived from goose feces.
The number of nesting pairs of black brant at the
Tutakoke River colony increased dramatically between
1986 and 1993 (Sedinger et al., 1993; 1994). Our field
observations and results from the present experiments
indicate that increased grazing pressure on patches of C.
ramenskii may provide high rates of biomass and N offtake
to geese, which in tum may lead to further grazing and the
eventual conversion to more preferred C. subspathacea
habitat. This apparent pattern of vegetation change has
important consequences for goose population dynamics at
the landscape scale, and offers an interesting contrast to the
coastal lowlands of west Hudson Bay, where grubbing by
lesser snow geese on the roots and rhizomes of graminoid
plants causes irreversible destruction of grazing habitat
through erosion and hypersalinization of devegetated
sediments (Kerbes, Kotanen & Jefferies, 1990).
Acknowledgements
We wish to thank K. Barber and L. Oliver at the UAF Forest
Soils Lab for assistance in laboratory analyses. R. L. Jefferies and
two anonymous reviewers provided many helpful suggestions to
the manuscript. This research was funded by the Department of
Biology and Wildlife at the UAF and by NSF OPP 92-14970.
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