Download Nutrient resorption of wetland graminoids is related to the type of

Functional
Ecology 2005
19, 344–354
Nutrient resorption of wetland graminoids is related to the
type of nutrient limitation
Blackwell Publishing, Ltd.
S. GÜSEWELL*†‡
†Utrecht University, Department of Geobiology, PO Box 80084, NL-3508 TB Utrecht, the Netherlands, and
‡Geobotanisches Institut ETH Zürich, Zürichbergstrasse 38, CH-8044 Zürich, Switzerland
Summary
1. Nitrogen or phosphorus limits plant growth in many wetlands. If specific mechanisms reducing losses of the growth-limiting nutrient have been favoured by selection,
the N and P resorption efficiency (RE) during leaf senescence (NRE, PRE: the fraction
of N or P resorbed) might depend on the type of nutrient limitation.
2. The size, mass, and N and P concentrations of green and senesced leaves were determined for 10 graminoid species at Dutch and Swiss wetland sites, with N : P ratios in
leaves (6–27 by mass) indicating N or P limitation.
3. During senescence, leaf area decreased by 8–19%, and leaf mass by 8–38%; NRE
ranged from 0 to 87%, and PRE from 30 to 96%. PRE correlated strongly with NRE
(r = 0·91) but was, on average, 17% higher. Within the Swiss or Dutch sites, NRE and
PRE did not correlate with foliar N : P ratios, indicating that RE was not directly adjusted
to the type of nutrient limitation.
4. NRE and PRE were, on average, higher at the P-limited Swiss sites than at the Nlimited Dutch sites. Because PRE exceeded NRE, high RE would be most beneficial
when P limits plant growth. This may have contributed to the dominance of graminoids
with high RE in P-limited wetlands.
Key-words : Carex, leaf senescence, nutrient limitation, nutrient retention, resorption efficiency
Functional Ecology (2005) 19, 344–354
doi: 10.1111/j.1365-2435.2005.00967.x
Introduction
Nutrient resorption from senescing leaves enables
plants to reduce the losses of nutrients associated with
leaf turnover (Bleecker 1998; Aerts & Chapin 2000;
Escudero & Mediavilla 2003), but it also entails costs
(Field 1983; Chapin, Schulze & Mooney 1990). Therefore plants might optimize their resorption efficiency
(RE, the fraction of a leaf’s nutrient content withdrawn
from senescing leaves) to balance the relative costs and
benefits of nutrient conservation (Wright & Westoby
2003). Because small nutrient losses are most important
for survival and competitive ability under nutrient-poor
conditions (Aerts & van der Peijl 1993; Aerts 1999),
particularly efficient resorption would be expected
to have evolved at nutrient-poor sites. Furthermore,
plasticity in RE might optimize the cost–benefit relationship under varying nutrient availability (Enoki &
Kawaguchi 1999).
Yet species from nutrient-poor sites do not always
resorb nutrients more efficiently than those from
nutrient-rich sites (Eckstein, Karlsson & Weih 1999),
© 2005 British
Ecological Society
*Correspondence should be addressed to the Geobotanisches
Institut ETH Zürich. E-mail: [email protected]
nor does RE change consistently according to nutrient
availability in soil (Escudero et al. 1992; Wright &
Westoby 2003) or nutrient concentrations of leaves
(Del Arco, Escudero & Garrido 1991; Aerts 1996). It
has therefore been proposed that selection at nutrientpoor sites does not promote high RE, but rather a long
life span (Escudero et al. 1992; Eckstein et al. 1999)
or low nutrient concentrations in litter (‘resorption
proficiency’, Killingbeck 1996).
Other evidence does suggest that efficient nutrient
resorption is important as a nutrient-conserving strategy.
A meta-analysis of leaf-level data revealed phosphorus
resorption efficiency (PRE) to be the main determinant
of P residence time in plant foliage (Aerts & Chapin
2000). A review of changes in leaf area and mass during senescence suggested that high RE (= 80%) is more
common than previously thought, especially for P (van
Heerwaarden, Toet & Aerts 2003). Wright & Westoby
(2003) argued that nutritional control of RE does not
necessarily imply negative correlations with nutrient
availability, and is therefore not refuted by inconsistent
changes along nutrient gradients.
The question remains as to whether and how RE is
optimized in response to variation in nutrient availability. The type of nutrient limitation might be important.
344
345
Nutrient resorption
in graminoids
© 2005 British
Ecological Society,
Functional Ecology,
19, 344–354
Either N or P (and sometimes K) can be limiting for
plant growth in terrestrial ecosystems (Aerts & Chapin
2000; Olde Venterink et al. 2003). The type of nutrient
limitation is approximately indicated by the N : P
ratios (ratio between N and P concentration) of plant
biomass: N : P mass ratios above 16 suggest P limitation, whereas N : P mass ratios below 13 suggest N
limitation (Güsewell & Koerselman 2002; Tessier &
Raynal 2003). Plants are likely to benefit most from an
efficient use of the growth-limiting nutrient (Koide,
Dickie & Goff 1999). If selection has optimized the
benefits of RE (Wright & Westoby 2003), high nitrogen
resorption efficiency (NRE) should have been favoured
under N-limited conditions, and high PRE under Plimited conditions, even at relatively productive sites.
As a result, PRE would increase in relation to NRE as
plants become more P-limited, that is, as their foliar
N : P ratios increase (Güsewell & Koerselman 2002).
Alternatively, if nutrient resorption is not regulated by
nutrition, but only by the flow of solutes from senescing leaves (Chapin & Kedrowski 1983), NRE and PRE
should strongly correlate with each other. N and P
would then be resorbed in direct proportion to foliar
N : P.
Patterns and determinants of nutrient resorption
have been investigated mostly for woody plants, and
much less is known for herbaceous plants (Chapin &
Kedrowski 1983; Aerts 1996; Eckstein et al. 1999; van
Heerwaarden et al. 2003). This scarcity of data contrasts with the fact that nutrient resorption can be very
important in the nutrient economy of herbaceous plants,
especially graminoids, because of their short leaf life
span, sequential leaf growth, and potentially high RE
(Jonasson & Chapin 1985; Aerts 1996; Aerts & Chapin
2000; Bausenwein, Millard & Raven 2001). Several
studies revealed plastic adjustments of RE to nutrient
availability in graminoids (e.g. Rejmánková 2001). In a
growth experiment with five Carex species from wetlands, Güsewell (2005) found that, within each species,
NRE was greatest in plants with low to intermediate
N : P ratios, while PRE was greatest in plants with
intermediate to high N : P ratios (Güsewell 2005).
Relationships between RE and biomass N : P ratios
(as indicators of N or P limitation) have not yet been
tested in field experiments.
This study investigates how leaf size, leaf mass and
foliar nutrient concentrations change during leaf
senescence in graminoids from N- and P-limited wetlands. Two main questions are addressed: first, do
patterns of nutrient resorption in graminoids parallel
those in woody plants? Second, is there evidence that
plants adjust NRE and PRE to the type of nutrient
limitation? While most previous studies focused either
on interspecific differences (e.g. Wright & Westoby
2003) or on intraspecific variation (e.g. Vitousek 1998),
this study considered both by sampling 10 species at
several locations in Swiss fen meadows and in Dutch
floating fens, to include plants with a broad range of
biomass N : P ratios.
Methods
 
The four Swiss sites are fen meadows near Zürich
(47°25′ N, 8°40′ E) at 430–550 m a.s.l. The long-term
mean annual temperature is 7·9 °C, and the mean annual
precipitation is 1144 mm. Soils of the study sites are
base-rich loamy gleysols; they are waterlogged or
flooded in winter but relatively dry in summer; the soil
pH is about 7 (Brülisauer & Klötzli 1998; S.G., unpublished data). All sites are mown annually in autumn.
The vegetation belongs to the phytosociological
alliance Molinion (Ellenberg 1996). It is moderately
species-rich and reaches a peak above-ground biomass
of 300–600 g dry matter m−2 in August (Güsewell &
Klötzli 1998). Five Carex species and the grass Molinia
caerulea were included in this study (nomenclature,
Halliday & Beadle 1983). Three of the species occurred
at all four sites, and the three other species at only two
or three sites. A given species at a given site is hereafter called a ‘plant population’.
The three Dutch sites are floating fens near Utrecht
at sea level (52°9′ N, 5°7′ E). The long-term mean
annual temperature of the area is 9·0 °C, and the mean
annual precipitation is 732 mm. Floating fens have
developed through the terrestrialization of ponds
created by peat excavation (van Wirdum, den Held &
Schmitz 1992). The substrate is a floating mat of partly
decomposed plant roots and rhizomes and Sphagnum
mosses (Bakker, Jasperse & Verhoeven 1997). The pH
of the sites ranges from 4 to 6, and the vegetation belongs
to the phytosociological alliances Caricion davallianae
and Caricion nigrae (Schaminée, Stortelder & Westhoff
1995). All sites have been mown every year in July or
August for ≈30 years. Peak above-ground biomass
ranges from 300 to 700 g m−2, of which up to 70% may
be bryophyte mass.
The Dutch sites were fertilized experimentally in
1999 and 2000 (Güsewell, Koerselman & Verhoeven
2002). At each site 16 plots of 50 × 50 cm2 were assigned
to 16 different treatments resulting from the factorial
combination of: +N or –N in 1999; +N or –N in 2000;
+P or –P in 1999; +P or –P in 2000. Thus some plots
received the same element in both years, while others
received different elements (Güsewell et al. 2002). In
the +N treatments 20 g N m−2 year−1 were supplied as
NO3NH4, and in the +P treatments 5 g P m−2 year−1
were supplied as NaH2PO4. The main purpose of the
experiment was to investigate the effects of fertilization
on vegetation biomass; therefore the vegetation was
clipped within the central 40 × 40 cm2 of each plot in
July 2000 (Güsewell et al. 2002). For this study the 10-cmwide strips bordering the central quadrat were sampled
in November 2000; this marginal zone was visibly
influenced by fertilizer treatments. Study species were
Anthoxanthum odoratum, Carex acutiformis, Carex
curta, Carex diandra and Eriophorum angustifolium,
the five most abundant graminoid species at these sites.
346
S. Güsewell
 
Swiss sites
On 24 – 25 May 2000, a line 3 – 6 m long was laid out
within each site at a spot where the studied species cooccurred, and 24 shoots of each species were selected
along the line. Twelve shoots were tagged with numbered plastic labels, and their youngest fully expanded
leaf (usually the third visible leaf from the top of the
shoot) was tagged with a small piece of red or yellow
plastic foil. The length of this leaf (from the tip of the
ligule to the tip of the leaf ) was measured to the nearest millimetre, and the maximum width was measured
to the nearest 0·2 mm. On each of the 12 other shoots,
the youngest fully expanded leaf was measured similarly, then removed and taken to the laboratory. Leaf
mass was determined after 48 h drying at 70 °C, and
leaves were kept for nutrient analyses.
Tagged leaves were monitored after 4, 8 and
13 weeks. Once they had fully senesced up to the ligule
(grey-brown colour and dry appearance), they were cut
off, taken to the laboratory, dried and weighed. The
length and width of those senesced leaves harvested at
week 13 (end of August) was measured again in the
field to determine whether leaf area changed during
senescence.
For nutrient analyses of green and senesced leaves,
four to six leaves of the same species and site were always
pooled to obtain a sufficient amount of material. They
were digested with a modified Kjeldahl procedure (1 h
at 200 °C and 2 h at 340 °C in a mixture of concentrated
sulphuric acid, salicylic acid, copper and selenium).
Concentrations of total N and P in the digests were
determined colorimetrically on a continuous-flow analyser (Skalar SA-40, Skalar, Breda, the Netherlands).
A second set of leaves were measured, weighed and
analysed in July 2000 (same sample size and procedure
as in May), but only few tagged leaves senesced before
the end of August, when the study had to stop due to
the mowing of sites. To obtain a measure of nutrient
concentrations in senesced leaves for the July cohort,
the youngest fully senesced leaf blade from five shoots
per species and site was also collected at the end of
August and analysed for N and P as described above;
these leaves had approximately the same age as the
tagged ones.
Dutch sites
© 2005 British
Ecological Society,
Functional Ecology,
19, 344–354
Sampling at the Dutch sites was restricted to a single
harvest in November 2000, after completion of the fertilization experiment. Despite the late sampling date,
nutrient concentrations in mature leaves did not differ
significantly from those of the same plots in July 2000
(Güsewell et al. 2002). Plant shoots were divided into
mature green and entirely senesced leaves or leaf parts;
young (expanding) leaves and material in an intermediate state were discarded. The length and width of 15
mature and 15 recently senesced leaves of each species
were measured. The mass of these leaves was determined after 48 h drying at 70 °C. The other material
was dried and analysed for N and P.
 
Swiss sites
Changes in leaf size during senescence were estimated
for individual tagged leaves as the percentage difference
between the length, width and area of the leaf when it
was green (LG, WG, AG) and after senescence (LS, WS,
AS). In these calculations, leaf area was estimated by
the product of length and width (AG ≈ PG = LGWG;
AS ≈ PS = LSWS), after checking that the two variables
were proportional to each other on a separate set of
leaves (PG = 1·1AG). As the size of senesced leaves was
measured only for some of the tagged leaves (those
senesced in August), data from the four sites were
pooled for each species, and two-sided paired t-tests
were used to test whether the average size changes
differed significantly from zero.
Changes in leaf mass during senescence were determined for each species and site as the percentage
difference between the mean mass of the 12 leaves
harvested when they were green (MG) and of those harvested after senescence (MS). To obtain accurate means
despite variation in leaf size, the mass of each leaf (MG
or MS, in g) was first standardized by the product of its
length and width (PG). MS was divided by PG and not
by PS so that mass loss would not be underestimated if
leaf size decreased during senescence (van Heerwaarden
et al. 2003). For a given species and site, both MG and
M S were proportional to P G (r 2 = 0·90), so that the
ratios MG /PG and MS /PG were independent of leaf size.
Thus, for each species and site, mass loss was estimated
accurately as:
Mean mass loss =
( M G / PG ) − ( M S / PG )
( M G / PG )
eqn 1
where horizontal lines above symbols indicate means
per species and site. Differences among species and
sites were tested with two-way .
Leaf-level nutrient resorption efficiencies (NRE, PRE)
were estimated for each species and site as the relative
changes in the mean N and P contents of a leaf (NC,
PC, in mg leaf−1):
NRE =
NC G − NC S
PC G − PC S
and PRE =
eqn 2
NC G
PC G
As NCG = [N]GMG and NCS = [N]SMS, with [N] (in
mg g−1) being the mean N concentration per species
and site, the formula for NRE can be rewritten as:
NRE =
[ N ]G − [ N ]S ⋅ ( M S / M G )
[ N ]G
eqn 3
Again, the ratio MS /MG was estimated for each species
and site from means of leaf mass standardized by leaf
347
Nutrient resorption
in graminoids
size: M S /M G ≅ ( M S / PG )/( M G / PG ) . The mean NRE per
species and site was therefore given by:
NRE =
[N ]G − ([N ]S ⋅ ( M S / PG )/( M G / PG ))
[ N ]G
eqn 4
Calculations were identical for PRE, replacing [N]
with [P]. As the ratio MS /PG could not be determined
accurately for the July cohort (too few tagged leaves
senesced before the last sampling), values for MG /PG
and MS /PG from the May cohort were used to calculate
NRE and PRE for both leaf cohorts. As RE was generally
≥ 80%, possible differences in mass loss between May
and July would hardly have affected the results (van
Heerwaarden et al. 2003). Finally, the N : P resorption
ratio was calculated for each species and site as the ratio
of the mean amounts of N and P resorbed per leaf:
N : P resorption =
[N ]G − ([N ]S ⋅ ( M S / PG )/( M G / PG ))
[ P ]G − ([ P ]S ⋅ ( M S / PG )/( M G / PG ))
eqn 5
Differences among species, sites and leaf cohorts
in nutrient concentrations (log-transformed) as well as
NRE and PRE were tested with repeated-measures
.
Dutch sites
At the Dutch sites the length and width of senesced
leaves were measured only after senescence. The change
in leaf size during senescence therefore could not be
determined. Mass loss was estimated using equation 1
and NRE and PRE using equation 4, but MS /PG was
replaced with MS /PS. This corresponds to the usual
calculations of NRE and PRE based on N or P concentrations per leaf area, which slightly underestimate
the true values if leaf area decreases during senescence
(van Heerwaarden et al. 2003).
Relationships among nutrient concentrations in
green and senesced leaves and nutrient resorption were
represented by scatter plots and quantified with Pearson’s
correlation coefficients (r), based on log-transformed
data for nutrient concentrations and N : P ratios. Four
types of relationship were considered. (1) Overall correlations were calculated from individual data points,
separately for Swiss sites (two cohorts) and Dutch
sites. (2) Interspecific correlations were calculated
from species means. For the Dutch sites, species means
across all plots were always closely similar to those across
unfertilized plots, so that results were not affected by
including fertilized plots. For C. acutiformis, the only
species sampled in both countries, means for Swiss and
Dutch sites were calculated separately. (3) Intraspecific
correlations were calculated after verifying that, for all
relevant pairs of variables, model-I regression slopes of
one variable against the other did not differ significantly among species (i.e. no interaction in an analysis
of covariance). All variables were then adjusted by
subtracting species means, and Pearson’s correlation
coefficients were calculated from the adjusted data. (4)
The relationship between NRE and PRE was further
described with a model-II regression, which corresponds to the principal axis of the distribution of the
two variables (Sokal & Rohlf 1995). Model-II regressions minimize error variation in both x and y dimensions, and therefore describe bivariate data more
accurately than ordinary regressions. Data from Swiss
sites (July cohort) and Dutch sites were included in the
calculation. All analyses were carried out with the
statistical package  ver. 3·2·2 (SAS Institute 1993–
2000). Pairwise significance levels are reported for
correlations because each tested for a different type of
relationship.
Results
      
 
The six species investigated in Swiss fen meadows
differed considerably in leaf size and mass, whereas
differences among the four sites were small (data not
shown). During senescence, leaf length (May cohort)
changed by <6% in all species, whereas leaf width
decreased by 3–17%, and estimated leaf area by 6–
19% (Table 1). The decrease in leaf area was significant
(P < 0·05) in five of six species.
Leaves from the May cohort lost 17 – 38% of their
initial dry mass during senescence. Species means
(20–34%; Table 1) differed (two-way , P < 0·05),
whereas site means did not (P > 0·05). In Dutch
fens, leaf mass loss was 33·5% in A. odoratum, 17% in
C. curta, and 8·5–9% in the three other species.
Table 1. Changes in size and mass of leaf blades during senescence, as a percentage of initial values, for six graminoid species
in Swiss fen meadows
© 2005 British
Ecological Society,
Functional Ecology,
19, 344–354
Carex acutiformis
Carex elata
Carex flacca
Carex flava
Carex panicea
Molinia caerulea
nL
Length
Width
Area
nS
Dry mass
11
14
5
9
13
11
− 2·2 ± 0·3*
− 5·6 ± 5·8°
0·5 + 1·6
2·3 ± 5·4
− 1·2 ± 0·7°
0·9 ± 1·3
− 6·6 ± 3·7°
− 12·8 ± 3·9***
− 6·6 ± 7·7
− 2·9 ± 3·2°
− 16·9 ± 6·3***
− 6·2 ± 4·2***
− 8·7 ± 5·4***
− 16·0 ± 7·4***
− 6·1 ± 8·5
− 5·7 ± 5·0*
− 19·3 ± 11·5***
− 7·2 ± 5·3***
4
4
2
3
4
4
− 30·2 ± 6·6**
− 27·1 ± 3·6***
− 25·2 ± 4·7°
− 28·0 ± 4·3**
− 33·8 ± 3·0***
− 20·3 ± 3·3**
Figures are means ± SD of nL leaves (for size) or of nS sites (for mass) and the significance of the change (two-sided paired t-tests;
***, P < 0·001; **, P < 0·01; *, P < 0·05; °, P < 0·1).
348
S. Güsewell
Table 2. N and P concentrations (mg g−1) in green and recently senesced leaf blades of six graminoid species, determined for two
leaf cohorts (May and July 2000) in Swiss fen meadows
Nutrient concentrations (mg g−1)
Resorption (%)
Species
NG
NS
PG
PS
N
P
May cohort
Carex acutiformis
Carex elata
Carex flacca
Carex flava
Carex panicea
Molinia caerulea
17·2 ± 2·4
18·3 ± 2·4
16·1 ± 3·1
19·9 ± 2·5
17·2 ± 2·0
18·5 ± 0·7
5·5 ± 0·4
7·1 ± 1·4
5·1 ± 0·4
7·1 ± 1·3
4·7 ± 1·8
3·9 ± 1·2
0·78 ± 0·08
0·78 ± 0·09
1·10 ± 0·41
1·18 ± 0·12
0·81 ± 0·21
0·79 ± 0·05
0·12 ± 0·07
0·09 ± 0·10
0·19 ± 0·02
0·25 ± 0·02
0·12 ± 0·05
0·06 ± 0·03
78·0 ± 3·9
72·3 ± 7·1
77·9 ± 5·8
75·1 ± 2·7
82·2 ± 3·9
82·6 ± 3·4
88·0 ± 3·2
88·3 ± 9·3
88·4 ± 3·7
84·4 ± 1·2
90·6 ± 4·1
93·5 ± 2·9
July cohort
C. acutiformis
C. elata
C. flacca
C. flava
C. panicea
M. caerulea
11·0 ± 0·8
10·3 ± 0·4
12·4 ± 0·1
12·2 ± 1·8
11·7 ± 0·8
12·6 ± 0·6
5·2 ± 1·1
6·3 ± 1·0
4·3 ± 0·1
6·7 ± 0·3
4·4 ± 0·7
4·0 ± 1·2
0·61 ± 0·12
0·40 ± 0·07
1·11 ± 0·02
0·96 ± 0·09
0·71 ± 0·09
0·64 ± 0·05
0·14 ± 0·06
0·11 ± 0·07
0·15 ± 0·01
0·26 ± 0·05
0·10 ± 0·08
0·06 ± 0·07
65·9 ± 3·3
50·3 ± 11·1
71·9 ± 2·7
59·5 ± 1·2
74·1 ± 5·3
74·7 ± 3·6
84·7 ± 2·7
74·3 ± 15·2
88·7 ± 0·2
80·7 ± 2·2
89·3 ± 4·6
92·1 ± 3·2

Species (df = 5)
Site (df = 3)
Month (df = 1)
Month × species
Month × site
1·13
0·18
307·8 ***
2·4
0·7
5·5**
0·4
1·3
0·2
0·7
21·4***
4·0*
31·3***
3·2
0·8
5·1*
1·5
0·03
0·9
3·1
5·7**
0·4
409·3***
12·2**
0·5
3·0
0·7
38·6***
7·2**
1·2
rMay–July
0·47 *
0·70 ***
0·73 ***
0·72 ***
0·91***
0·89***
Figures are means ± SD of nS sites (see Table 1 for nS), F ratios and significance levels from repeated-measures , and
correlations (Pearson’s r) between the two leaf cohorts, calculated across species and sites. Significance levels are as in Table 1.
Table 3. N and P concentrations (mg g−1) in green and in recently senesced leaf blades of five graminoid species in Dutch fens
Nutrient concentrations (mg g−1)
Resorption (%)
Species
n
NG
NS
PG
PS
N
P
Anthoxanthum odoratum
Carex acutiformis
Carex curta
Carex diandra
Eriophorum angustifolium
25
15
21
4
12
18·8 ± 3·4
11·8 ± 1·7
15·3 ± 2·9
12·5 ± 1·6
15·7 ± 2·4
12·0 ± 2·3
10·0 ± 1·9
8·9 ± 2·2
8·8 ± 1·1
8·6 ± 3·6
2·82 ± 0·91
1·20 ± 0·52
2·18 ± 0·66
1·77 ± 0·77
1·97 ± 0·96
1·36 ± 0·48
0·59 ± 0·24
1·04 ± 0·56
1·08 ± 0·55
0·52 ± 0·36
56·9 ± 8·8
20·9 ± 18·1
49·2 ± 8·0
36·0 ± 5·5
51·3 ± 16·8
67·9 ± 9·1
52·0 ± 10·5
60·8 ± 11·9
47·2 ± 8·6
73·7 ± 17·0
Figures are means ± SD of n plots which had been partly fertilized with N and /or P during the two preceding years.
  
 
© 2005 British
Ecological Society,
Functional Ecology,
19, 344–354
In Swiss fen meadows, the N concentration of green
leaves ([N ]G) differed between May and July cohorts
(on average 45·5% lower in July), but not among species or sites (Table 2). The P concentration ([P]G) differed among species, sites and cohorts (18·5% smaller
in July; Table 2). Nutrient concentrations of senesced
leaves differed among species but not among sites or
cohorts (Table 2). As a result, NRE and PRE were
higher in the May cohort than in the July cohort. NRE
differed among species while PRE did not, and there
were no consistent differences among sites (Table 2).
In Dutch fens, nutrient concentrations of green and
senesced leaves varied more among species than at the
Swiss sites, and the P concentration was generally
higher (Table 3). The estimated NRE and PRE were
more variable and, on average, lower than at the Swiss
sites (Table 3).
  
Nutrient concentrations of green and senesced leaves
correlated positively with each other, except for [N ]G
and [N]S in the Swiss fen meadows (Fig. 1a,b). Interand intraspecific relationships were similar: both were
stronger for P than for N (Table 4a). NRE correlated
positively with [N]G in the Dutch fens but not in the
Swiss ones (Fig. 1c). PRE and [P]G did not correlate
with each other within the data sets (Fig. 1d), but a
weak negative interspecific correlation (Table 4a) reflected
the above-mentioned differences in PRE and [P]G
between Swiss and Dutch sites.
349
Nutrient resorption
in graminoids
Fig. 1. Relationships between N or P concentrations in green leaves and (a,b) N or P concentrations in senesced leaves
(resorption proficiency); (c) NRE; and (d) PRE. Each symbol refers to a ‘population’, i.e. one species in one of the Swiss fen
meadows (for two leaf cohorts) or one species in one of the experimental plots in the Dutch fens. Pearson’s correlation
coefficients (r) and their significance are given for each graph, separately for the Dutch sites and the two leaf cohorts from the
Swiss sites. Significance levels: ***, P < 0·001; **, P < 0·01; *, P < 0·05; °, P < 0·1.
Table 4. Inter- and intraspecific correlations among nutrient
concentrations in green and senesced leaves and nutrient
resorption, as shown in Figs 1–3
© 2005 British
Ecological Society,
Functional Ecology,
19, 344–354
Interspecific
Intraspecific
(a) Fig. 1
[N ]G − [N ]S
[P]G − [P]S
[N ]G − NRE
[P]G − PRE
0·57°
0·88***
− 0·02
− 0·54°
0·48***
0·69***
0·22*
− 0·01
(b) Fig. 2
[N ]G − [P]G
[N ]S − [P]S
NRE − PRE
0·87***
0·93***
0·93***
0·30*
0·56***
0·75***
(c) Fig. 3
N : PG − N : PS
N : PG − N : Pres
N : PG − NRE
N : PG − PRE
0·95***
0·89***
0·43
0·62*
0·78***
0·81***
− 0·08
− 0·03
Pairs of variables correlated are indicated in the first column.
Correlations (Pearson’s r) were calculated for Swiss sites (July
cohort) and Dutch sites together, first from species means
(interspecific correlations, n = 11), then from data adjusted
for species means (intraspecific correlations, n = 94).
Abbreviations: [N ], [P] = N or P concentrations in mg g−1;
[ ]G = green leaves; [ ]S = senesced leaves; NRE, PRE = N
or P resorption efficiency in percentage; N : P = N : P ratio;
N : Pres = ratio of amounts of N and P resorbed.
Pairwise significance levels are indicated by symbols as
in Table 1.
Resorption efficiency correlated positively with leaf
mass loss in the Dutch fens (r = 0·52 for NRE; 0·23 for
PRE). In the Swiss fen meadows there was no correlation across species, but within species NRE and PRE
were also positively related to mass loss (,
P < 0·01).
N and P concentrations correlated positively with
each other in green leaves (Fig. 2a) and senesced leaves
(Fig. 2b). An even stronger correlation occurred between
NRE and PRE (Fig. 2c). This was most apparent at
the intraspecific level: although [N]G and [P]G correlated poorly within species, NRE and PRE were still
strongly correlated (Table 4b). However, PRE was
always greater than NRE, as the relationship between
NRE and PRE (model-II regression line) was given by
PRE = 1·003NRE + 17·1%, r = 0·91.
The N : P ratios of green leaves, senesced leaves and
nutrient resorption correlated strongly with each other
in all types of comparison (Fig. 3; Table 4c). Because
PRE generally exceeded NRE, N : P was mostly greater
in senesced leaves than in green leaves (Fig. 3a), whereas
the N : P resorption ratio (equation 5) was slightly
smaller than the N : P ratio of green leaves (Fig. 3b).
Nutrient resorption efficiency (NRE and PRE) did
not generally correlate with the N : P ratios of green
leaves within the Swiss or Dutch data sets (Fig. 3c,d),
nor did the ratio of NRE to PRE (P > 0·05, not shown).
However, positive interspecific correlations between
350
S. Güsewell
Fig. 2. Relationships between (a) N and P concentrations in
green leaves; (b) N and P concentrations in senesced leaves;
and (c) NRE and PRE. Symbols and codes as in Fig. 1.
N : PG and NRE or PRE (Table 4c) reflected the fact
that all three variables had larger values in Swiss fen
meadows than in Dutch fens. The absence of intraspecific correlations (Table 4c) indicates that individual
species did not directly adjust their NRE and PRE to
the relative degree of N vs P limitation.
Discussion
   
    
© 2005 British
Ecological Society,
Functional Ecology,
19, 344–354
Nutrient resorption during senescence has been studied mainly for woody plants. This study has shown a
close similarity between graminoids and woody plants
Fig. 3. Relationships between N : P mass ratios of leaves and
(a) N : P of senesced leaves; (b) N : P resorption ratio (based
on amounts resorbed per leaf ); (c) NRE; and (d) PRE.
Diagonal lines in (a,b) indicate where x = y; all N : P axes
have a logarithmic scale. Symbols and codes as in Fig. 1.
regarding changes during leaf senescence. Leaf mass
loss in the graminoids ranged from 8 to 38%, which is
close to the range of 3–37% reported for woody species
by van Heerwaarden et al. (2003). An even broader
range of mass loss (0–60%) was found by Chapin &
Kedrowski (1983) for boreal trees, but only few values
exceeded 40%. The 5–19% decrease in leaf area found
351
Nutrient resorption
in graminoids
here for graminoids compares well with the 4–22%
area loss reported by van Heerwaarden et al. (2003)
and Peng & Wang (2001) for woody species. Leaf area
decreased mainly through a shrinkage of leaf width,
whereas leaf length changed little. This supports the
proposal of van Heerwaarden et al. (2003) that, in
graminoids, nutrient concentrations per leaf length
may be a good basis for calculating RE if the change
in leaf size during senescence cannot be monitored.
Nutrient concentrations per needle length have also
been used to calculate nutrient resorption in coniferous trees (Enoki & Kawaguchi 1999).
Nutrient resorption efficiency varied widely among
and within species, with a range from 0 to nearly 100%.
The uppermost values exceeded the maximal RE (about
80% of N and 90% of P) reported for woody plants
(Walbridge 1991; Wright & Westoby 2003). However,
only leaf blades were sampled here for practical
reasons (part of the sheaths were in the soil or waterlogged moss layer, and senesced later than blades).
Leaf sheaths have a lower RE than blades (Aerts 1989).
Based on entire leaves, Güsewell (2005) found ≈10%
lower RE than in the present study for five of the Carex
species. This suggests that maximal RE from entire
leaves does not differ between graminoids and woody
plants. Nevertheless, the average RE of graminoids is
higher (Aerts 1996), which may reflect contrasting
selective forces. The main adaptation of woody plants
to low nutrient availability is an increased leaf life
span (Escudero et al. 1992; Wright & Westoby 2003).
In contrast, most graminoids have short-lived leaves
(Aerts & de Caluwe 1995; Ryser & Urbas 2000), so that
RE plays a greater role than life span for their nutrient
conservation (Aerts & Chapin 2000).
   
   
© 2005 British
Ecological Society,
Functional Ecology,
19, 344–354
Resorption efficiency was not consistently related to
nutrient concentrations in green leaves, as has often been
demonstrated for trees (Del Arco et al. 1991; Wright
& Westoby 2003). In particular, high N or P concentrations in green leaves did not result in low NRE or PRE,
as should be expected if plants adjusted their RE to
their nutrient status. Downregulation of PRE from
P-rich leaves has often been observed in trees grown
on very P-rich soils or after P fertilization (Chapin &
Moilanen 1991; Uliassi & Ruess 2002). In a glasshouse
experiment with five wetland Carex species, PRE was
also strongly reduced when foliar P concentrations
exceeded 2 mg g−1 (Güsewell 2005). The same did not
hold here for the Dutch fens, where even plants with P
concentrations of 3 – 4 mg g−1 had a relatively high PRE.
Likewise, the forest herb Claytonia virginica had a
PRE of 87% with a foliar P concentration of nearly 6%
(Anderson & Eickmeier 2000). Thus even extremely high
P concentrations do not necessarily downregulate PRE.
Although N and P concentrations in green leaves
correlated only moderately with each other, there was
a strong positive correlation between NRE and PRE
(Fig. 2). An equally strong correlation between NRE
and PRE was obtained by Aerts (1996) in a meta-analysis
of published data. The present study shows that this
relationship holds among and within species (Table 4b)
and for N- and P-limited plants, as indicated by the
broad range of biomass N : P (Fig. 3). Contrary to my
initial hypothesis, N-limited plants (with low N : P)
did not specifically increase their NRE (in absolute
terms or relative to PRE), nor did P-limited plants
(with high N : P) specifically increase their PRE.
Apparently, RE was not regulated by the type of nutrient
limitation as reflected by foliar N : P ratios. Instead,
nutrient concentrations of senesced leaves correlated
positively with those of green leaves. This nutritional
control was stronger for P than for N (to judge from
correlation coefficients), but not stronger at the Plimited Swiss sites than at the N-limited Dutch sites, so
that it was not specific to the type of nutrient limitation
either.
The positive correlation between leaf N concentration and NRE at the Dutch sites might be interpreted
as indicating that NRE was determined by the fraction
of the leaf’s N allocated to labile, metabolically active
compounds such as photosynthetic enzymes and pigments (Nordell & Karlsson 1995). However, there was
no correlation at the Swiss sites, and other studies that
considered the fractions of N involved in resorption
concluded that most of the leaf’s N and P can be solubilized, so that RE is generally not limited by the availability of labile compounds (Chapin & Kedrowski
1983; Cartaxana & Catarino 2002; Yasumura et al.
2005). In those studies RE rather appeared to depend
on the flow of solutes from senescing biomass, and
thus on the duration of the senescent stage (Del Arco
et al. 1991; Silla & Escudero 2004), or on the strength
of sinks for assimilates (growing parts or storage tissues:
Chapin & Moilanen 1991; Yasumura et al. 2005). The
high RE and low nutrient concentrations in litter
found at the Swiss sites further indicate that most N
and P contained in green leaves of graminoids can
potentially be resorbed. Moreover, RE correlated positively with leaf mass loss, supporting control by the
total outflow of solutes (Chapin & Kedrowski 1983).
    

Resorption efficiency was generally greater at the
Swiss than at the Dutch sites. Despite similar aboveground biomass production, plants at the Swiss sites
had lower P concentrations and higher N : P than
plants at the Dutch sites, suggesting that they were
more P-limited. Fertilization experiments directly
demonstrated N or N + P limitation at the Dutch sites
(Güsewell, Koerselman & Verhoeven 2003) and P
limitation at Swiss sites similar to those investigated here
(Egloff 1983). Aerts & Chapin (2000) hypothesized
that nutrient resorption is more important for nutrient
352
S. Güsewell
© 2005 British
Ecological Society,
Functional Ecology,
19, 344–354
conservation at P-limited than at N-limited sites. Indeed,
reports of very high RE (>80%) mainly concern vegetation
with high N : P ratios, suggesting growth limitation by
P (Walbridge 1991; Wright & Westoby 2003; McGroddy,
Daufresne & Hedina 2004). Could this explain the
difference in RE between Swiss and Dutch sites?
It is first necessary to examine whether the difference in RE might simply reflect the different sampling
methods. Changes in leaf area during senescence
were not accounted for at the Dutch sites. If leaf area
decreased by 5 – 20% at the Dutch sites, similar to the
Swiss ones, RE would have been underestimated by 5–
20% in plant populations with an apparent RE of 0%,
but only by 1 – 4% in plant populations with an apparent RE of 80% (van Heerwaarden et al. 2003). Thus
accounting for leaf area loss would only marginally
reduce differences between Swiss and Dutch sites.
Plant material was sampled later in the year at the
Dutch sites, but nutrient concentrations in biomass did
not differ between July and November (see Methods).
The lower RE of Dutch plants therefore could not be
explained by export of nutrients from leaves during the
autumn while they were still green. The oceanic climate of the Netherlands enables plants to grow during
most of the winter, but photosynthesis is certainly
restricted by the low irradiation. A seasonal reduction
in photosynthesis and growth would affect RE if the
current carbon assimilation determines the sink effect
of growing plant parts (Chapin & Moilanen 1991).
Insufficient data are available to assess how important this effect might be. Shading of birch (Betula
papyrifera) leaves to prevent photosynthesis caused a
20 – 30% decrease in RE (Chapin & Moilanen 1991),
whereas RE did not differ between sun and shade
leaves in a beech forest (Yasumura et al. 2004).
Despite a possible seasonal bias, differences between
Swiss and Dutch sites probably reflected inherent differences among the species or populations sampled in
each region. Indeed, similar interspecific differences
were also found in other studies without differences in
sampling time. In a glasshouse experiment, RE was
greatest in Carex panicea and Carex flacca, intermediate in Carex flava, and lowest in C. curta and Carex
elata, which corresponds to their ranking in the
present study (Güsewell 2005). In a Dutch heathland,
RE of M. caerulea (foliar N : P = 33) between September and November (NRE = 74 –75%, PRE = 80–87%)
resembled that between July and August in the Swiss
fen meadows (Aerts 1989). Conversely, in a Swiss fen
meadow the RE of A. odoratum (foliar N : P = 19)
estimated from nutrient concentrations in August 2004
(NRE = 73%, PRE = 54%) resembled that found in
November 2000 at the Dutch sites (unpublished data).
Among these species, those that dominate in P-limited
wetlands (e.g. Carex panicea, Molinia caerulea) consistently had a higher RE than those that dominate in
N-limited wetlands (C. curta, C. elata, A. odoratum).
Carex acutiformis had a much higher RE at the
Swiss sites than at the Dutch ones, in apparent contra-
diction with the suggestion of inherent differences
among species. It is possible that genetic differences
exist between populations from Swiss and Dutch sites.
A comparable difference was observed for C. flacca: at
the P-limited Swiss sites: its N and P concentrations
decreased by 65 and 86%, respectively, during senescence (Table 2). In a Dutch dune slack, where biomass
production is generally N-limited (Güsewell et al. 2003),
N and P concentrations decreased by only 33 and 50%,
respectively, indicating lower NRE and PRE (unpublished data). For several evergreen woody species,
genetically determined differences in NRE were found
among populations from sites with contrasting types
of nutrient limitation (Treseder & Vitousek 2001) or
with differing productivity (Oleksyn et al. 2003). In
outcrossing species such as many graminoids, populations from geographically distant areas may be required
for genetic differentiation to become apparent
(Vellend & Waterway 1999; Stenström et al. 2001).
Even if NRE and PRE are not directly regulated by
the type of limitation (no correlation with foliar N : P),
differences in RE may have had contrasting implications for plant fitness at N- and P-limited sites. PRE
exceeded NRE by, on average, 17% throughout the
range of foliar N : P. Given the nonlinear relationship
between RE and nutrient retention by plants with a
given leaf life span (assuming that resorbed nutrients
are effectively recycled; Escudero et al. 1992), the difference between NRE and PRE suggests that a parallel
increase of NRE and PRE (e.g. by extending the senescent stage) would enhance P retention more than N
retention (Fig. 4). Accordingly, plants at Swiss and
Dutch sites differed only slightly in N retention, but
differed greatly in P retention (Fig. 4). Graminoids
that dominate in P-limited wetlands typically have
long-lived below-ground storage organs (rhizomes,
basal internodes), which act as sinks for solutes during
leaf senescence (Aerts 1989; Güsewell 2005). In contrast, graminoid species typical of N-limited wetlands
Fig. 4. Relationship between nutrient resorption efficiency
(RE) and nutrient conservation, measured as the residence
time of leaf N or P relative to leaf life span. Due to the close
correlation between N and P resorption (cf. Fig. 2c), the xaxis represents RE for both nutrients jointly, with PRE =
NRE + 17%. Means ± SD of NRE (and PRE) are shown for
the Dutch fens (NL) and Swiss fen meadows (CH, two leaf
cohorts). Curves were calculated as: nutrient retention time =
leaf life span × (1 − RE)−1.
353
Nutrient resorption
in graminoids
produce more fine roots below ground, and their
leaves senesce rapidly when the plants are P-deficient
(Güsewell 2005 and unpublished data), reducing
sink strength and the duration of nutrient resorption.
These contrasting traits may give a selective advantage
to different graminoid species (or ecotypes) at N- and
P-limited sites, as suggested by Aerts & Chapin (2000).
Conclusions
This study of nutrient resorption in wetland graminoids addressed two questions. First, are patterns of
nutrient resorption found in woody plants also valid
for graminoids? The results show that changes in leaf
area, leaf mass and nutrient concentrations during
senescence vary over a similar range in graminoids to
that in woody plants. Second, is there evidence that
plants adjust their RE to the type of nutrient limitation? At first sight, the answer is negative: NRE and
PRE correlated strongly with each other, but not with
foliar N : P. However, high RE appeared to improve
P retention more than N retention, suggesting that
plants benefit most from high RE when P limits their
growth. This may have contributed to the dominance
of graminoids with high RE in P-limited wetlands.
Acknowledgements
I thank I. Wright, J. Oleksyn, D. Uliassi and one anonymous
referee for their helpful comments on a draft of the
manuscript, J.T.A. Verhoeven and W. Koerselman for
advice on the fertilization experiments, G. Rouwenhorst
and P. van der Ven for assistance with nutrient analyses,
P. van Bodegom for sampling C. flacca in a dune slack,
and the landowners and conservation authorities (Amt
für Natur und Landschaft Zürich, Staatsbosbeheer
Utrecht) for access to the study sites. The research
was funded by TMR grant ENV4-CT97-5075 from
the Commission of the European Communities.
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Received 1 December 2004; accepted 4 January 2005