Journal of

Ecology 2000,
88, 506515
Nitrogen retention by Hylocomium splendens in a
subarctic birch woodland

R. L. ECKSTEIN

Department of Plant Ecology, Evolutionary Biology Centre, Uppsala University, Villava gen 14,
SE-752 36 Uppsala, Sweden


Summary

1 Nutrient dynamics and growth of the feathermoss Hylocomium splendens were
studied in a subarctic birch woodland. My aims were to estimate the species' nutri-
ent use strategy (and its determinants: mean residence time (MRT) and annual
nutrient productivity (aNP)) and to unravel possible traits related to nutrient con-
servation and their implications for ecosystem nitrogen ux. Three methods to esti-
mate nutrient losses in bryophytes were evaluated: a conventional growth analysis
technique, a retrospective analysis and a
15
N-tracer approach.
2 Estimates for nitrogen retention varied between 3 and 10 years as a result of the
dierent N pools considered by the three methods. Growth analysis results
depended on the distinction between live and dead tissues, whereas retrospective
analysis gave valuable information on N release from decaying segments but did
not measure MRT within the living segments. Valid estimates of MRT were
obtained by a
15
N-tracer approach.
3 MRT and aNP of H. splendens were similar to values typically found in woody
evergreen vascular plants. Ecient nutrient recycling and a relatively long segment
life span were responsible for the long residence time of nitrogen. Feathermosses
show ecient nutrient acquisition, nutrient recycling and acropetal transport; nutri-
ent losses will therefore be small.
4 Dominant bryophytes may retard the nutrient turnover at the forest oor
through their production of acidic nutrient-poor organic matter and their negative
eect on soil temperature, and they may therefore function as autogenic ecosystem
engineers.

Key-words: mean residence time, nutrient productivity, phosphorus, plant strate-
gies, transport mechanisms.

Journal of Ecology (2000) 88, 506515





















# 2000 British
Ecological Society
Introduction

Low temperatures and a short growing season limit
plant performance at high altitudes and latitudes.
Low temperatures reduce mineralization rates and
this together with a strong microbial competition
for free mineral nutrients (Michelsen et al. 1995;
Jonasson et al. 1996) leads to the growth of plants
of cold regions generally being nutrient limited.
Nevertheless, gradients of nutrient availability exist
even within the tundra (e.g. Shaver & Chapin 1991;
Giblin et al. 1991; Weih 1998; Weih & Karlsson
1999) and the various combinations of traits exhib-
ited by higher plants in response to such contrasts
can be characterized as dierent strategies of nutri-


Correspondence: Lutz Eckstein (tel. 46-(0) 18
4712880;
fax 46-(0) 18 553419; e-mail
lutz.eckstein@ebc.uu.se).
ent use (Eckstein & Karlsson 1997). The extremes
are represented by fast growing species (herbs and
graminoids) with a short retention time of growth
limiting nutrients and by slow growing species
(mainly evergreens) with a long residence time of
these nutrients. The relative performance of plants
can be expressed by the index of nutrient use e-
ciency (NUE) (Berendse & Aerts 1987), which is
dened as the annual amount of dry matter pro-
duced per unit of nutrient lost. Berendse & Aerts
(1987) partitioned NUE into two components: (i)
the mean annual nutrient productivity (aNP), which
measures the annual dry matter production per unit
nutrient in the plant, and (ii) the mean residence
time (MRT). Nitrogen productivity depends on
photosynthetic nitrogen use eciency and nitrogen
allocation within the plant (Garnier et al. 1995) and
represents a measure of the species' productivity.
507
R.L. Eckstein
MRT, which is estimated as the ratio between the
annual average nutrient pool and the annual nutri-
splendens, an important bryophyte of boreal and
subarctic woodlands. My aim was to characterize
ent losses, is an index of nutrient conservation and this species in terms of its nitrogen (N) use strategy
depends on tissue life span and nutrient resorption and to compare its nitrogen productivity and its
(Escudero et al. 1992; Aerts 1995; Eckstein & ability to conserve N with that of various types of
Karlsson 1997; Garnier & Aronson 1998). vascular plants. I addressed the following questions:
Bryophytes are important components in ecosys- 1 What is the mean residence time of growth lim-
tems within the polar regions with respect to cover, iting nutrients in H. splendens? Mosses characteristic
diversity, biomass, and production (Longton 1982). of nutrient-poor habitats should be conservative in
When they gain dominance in the understorey, pin- terms of their nutrient use. Therefore, I hypothesize
nately branched feathermosses such as Hylocomium that H. splendens will show a long mean residence
splendens (Hedw.) Br. Eu. and Pleurozium schreberi time of growth limiting nutrients (high nutrient
(Brid.) Mitt. may signicantly reduce soil tempera- retention) similar to evergreen vascular plants. Since
ture (Van Cleve et al. 1983) and hence primary MRT and aNP make conicting demands on plant
productivity (Oechel & Van Cleve 1986). Large, performance, a high MRT in H. splendens will be
acrocarpous and pleurocarpous mosses are able to paid for by a low annual productivity per unit nutri-
acquire and retain large proportions of nutrients ent.
from precipitation or other atmospheric sources 2 If H. splendens shows a long MRT, what
(Tamm 1953; Weber & Van Cleve 1981; Bates 1987, mechanisms enable it to retain nutrients over
1989a,b; Bowden 1991; Jonsdottir et al. 1995; extended periods? Nutrients may be conserved
Eckstein & Karlsson 1999) and therefore may also within the shoots by recycling and transport of
directly control nutrient ux through the ecosystem nutrients from senescing parts to new tissues and/or
(Weber & Van Cleve 1981, 1984; Chapin et al. 1987; by a long ramet life span (Escudero et al. 1992;
Bowden 1991; Jonsdottir et al. 1995; Svensson Aerts 1995; Garnier & Aronson 1998; Eckstein et al.
1995). 1999).
The few available data on the NUE of bryophytes Furthermore, given the problems of growth
suggest that these plants are either very ecient analysis in bryophytes, I used three dierent meth-
(Chapin & Shaver 1989) or are intermediate (Oechel ods for estimating the losses and the retention time
& Van Cleve 1986) as compared to various vascular of N. A traditional growth analysis based on
plant life-forms. To my knowledge, there has been
no attempt to characterize the nutrient use eciency
sequential harvests over 2 years was compared with
a
15
N-tracer approach where the fate of an initial
sensu Berendse & Aerts (1987) of any individual amount of label was followed through time, and
bryophyte species. There are three reasons why with a retrospective analysis of growth and N and
bryophytes do not lend themselves easily to the phosphorus (P) content of interconnected annual
growth analysis needed for ecophysiological studies. segments.
Firstly, the annual dry matter productivity, a central
variable in growth analysis, is dicult to estimate in
the vast majority of species because they lack innate




































































# 2000 British
Ecological Society
Journal of Ecology,
88, 506515
annual markers of growth. Second, there is no clear-
cut distinction between live and dead tissues in bryo-
phytes, nor can these states be dened unambigu-
ously. Third, due to the origin of the gametophytic
shoots from microscopic protonema, followed by
intense ramication, clonal growth and an unknown
degree of clonal integration, it is often dicult to
dene functional growth units. Therefore, the col-
ony rather than the `individual' is regarded as the
functional unit in many bryophyte species (Bates
1998).
Despite these problems, information on the nutri-
ent use strategy of bryophytes is essential in order to
understand the role of bryophytes in terrestrial eco-
systems. An increasing body of evidence suggests
that traits of plants adapted to nutrient-poor or
nutrient-rich habitats may have feedback eects on
decomposition and ecosystem nutrient turnover (e.g.
Hobbie 1992; Berendse 1998) and thus have a stabi-
lizing eect on ecosystem development (Aerts 1999).
I studied growth and nutrient use of Hylocomium
Materials and methods

THE S PECI ES

The pleurocarpous, perennial H. splendens, is a
characteristic element of the understorey vegetation
at high latitudes (Oechel & Van Cleve 1986). Unlike
many mosses, H. splendens shows clear innate mar-
kers which correspond to its annual growth (e.g.
Callaghan et al. 1978; kland 1995, 1997), and thus
distinct annual segments of known age can be iden-
tied. A number of interconnected annual segments
will be termed a `segment chain' and individual seg-
ments designated either according to the year they
started to grow (e.g. S 98 for shoots originating in
1998) or according to their age (S 0 for current-year
shoots), depending on the analysis.
Each segment of H. splendens is the product of
one meristem and therefore represents a ramet.
Earlier studies suggest strongly that there is clonal
integration among adjacent interconnected ramets
and that considerable acropetal transport of nitro-
508
Nitrogen retention
by Hylocomium
splendens






























































# 2000 British
Ecological Society
Journal of Ecology,
88, 506515
gen occurs under eld conditions (kland 1995;
Eckstein & Karlsson 1999).


STU D Y S I T E

The present study was carried out in an open, bryo-
phyte dominated birch forest in subarctic Sweden in
the vicinity of the Abisko Scientic Research
Station (68

21
0
N, 18

49
0
E, 360 m a.s.l.). The
region- al climate is subarctic: the average annual
tempera- ture is 0.8

C (196190) and there is
an annual total of c. 300 mm precipitation
(Andersson et al.
1996). The vegetation can be classied as an
Empetro-Betuletum hylocomietosum Nordh. 1943
(Dieren 1996) with the feathermosses H. splendens
and Pleurozium schreberi dominating in the bryo-
phyte layer. Within this forest type, I selected 20
apparently undisturbed populations of H. splendens,
all of which had a very low abundance of vascular
plants or other mosses. For the
15
N study, 30 10
10 cm plots with a cover of H. splendens of > 80%
and a low abundance of vascular plants were estab-
lished within an area of about 15 15 m adjacent
to the 20 study populations.


HAR V EST PROCEDURE

Growth analysis

This analysis was carried out in 1996 and 1997 and
H. splendens was harvested on six occasions during
each year (at about three-week intervals from early
June to late October). On each of the 12 occasions,
two to four segment chains were taken from each of
the 20 populations, selecting intact, mainly
unbranched, sympodial segment chains to reduce
the variation in nutrient content due to dierent
modes of ramication (kland et al. 1997). The
chains were divided into their component annual
segments (ramets) in the laboratory. The oldest
ramets were 5 years old (S 5) and had started
growth during 1992. All material was dried at 70

C
for 24 h and weighed to the nearest 0.1 mg.
The average dry weight of the segments of each age
class was calculated for each population. Variation
in the data thus expresses spatial variation among
popula- tions.


15
N-tracer approach

The labelling and harvesting procedure for the
15
N-
tracer study is described in detail in Eckstein &
Karlsson (1999). In short, the mosses were activated
by wetting with distilled water before H. splendens
in half of the selected plots was labelled with an
ammonium-sulphate solution on two consecutive
days (6 and 7 June 1997) using a simple spraying
bottle. Each labelled plot received 0.15 mg
15
N (15
mg
15
N m
2
) in total, which accounted for about
1% of the average total N pool per plot while the
remaining (control) plots received only distilled
water. Ammonium was chosen as the N source
because in the study area it is present in larger
amounts in precipitation and wet deposition than is
nitrate (Kindbom et al. 1994). Furthermore, ammo-
nium is more important as a source of mineral soil
nitrogen than is nitrate in dry to mesic heath birch
forests (Weih 1998).
Three harvests of all the segment chains within a
study plot were carried out: (i) 12 June 1997
(n
CONTROL
12, n
LABEL
12), (ii) 8 September 1997
(n
CONTROL
8, n
LABEL
9) and (iii) 22 September
1998 (n
CONTROL
8, n
LABEL
8). From each
sampled plot, 30 segment chains were selected and
divided into segments that were current-year
growth, 1-year-old growth, other green (usually only
2 to 3-year-old) growth and brown growth. The
remaining H. splendens segment chains from each
plot were also kept but not separated. All material
was dried at 70

C for 24 h and weighed to the
near- est 0.1 mg. During the 1998 harvest all
annual seg- ments were separated and only brown
segments originating from 1993 and older were
pooled. The mass of each segment type per plot
was then esti- mated using the ratio of the total dry
weight of H. splendens per plot and the dry weight
of the selected segment chains (see Eckstein &
Karlsson 1999).



Retrospective analysis

On 26 September 1998, three to ve segment chains
were collected from each of 16 of the 20 populations
used in the growth study. Segment chains were
selected as for the earlier analysis but were also cho-
sen to include as many ramets as possible. Each
chain was separated into annual segments, dried and
weighed. The oldest ramets originated from 1989
and were thus 9 years old. After weighing, ramets of
the same age from each population were pooled and
homogenized. The dry weights of all segments of the
same age class were averaged for each population.



CHEMI CAL ANALYSES

Samples from the growth study and from the retro-
spective approach were analysed after digestion with
concentrated sulphuric acid for total Kjeldahl nitro-
gen using a ow injection analyser (Fia-star 5012
system, Foss Tecator AB, Hoganas, Sweden).
Samples from the retrospective study were also ana-
lysed for phosphorus with a ow injection analyser
using the ammonium-molybdate method.
Samples from the
15
N study were analysed for
total N and
15
N by the Waikato Stable Isotope Unit
(Hamilton, New Zealand) using an ANCA-MS
(Europe Scientic Ltd, Crewe, UK).
509
R.L. Eckstein
Table 1 Summary table of the basic study unit, the denition of nutrient pool and loss related to the dierent methods
applied in this study. The annual nutrient losses are an estimate for nutrient transfer out of the bryophyte. MRT is dened
as the ratio between average nutrient pool and annual nutrient loss

Method Basic study unit Nutrient pool Nutrient loss
Growth analysis Segment chain Sum of green segments Segments turning brown during

(S 0, S 1, S 2, S 3 the season (S 3 in autumn)

[S3 only until August])

Retrospective analysis Annual segment Average green segment Segments during degeneration

(ramet) during growth phase phase (linear regression)

15
N technique

Plot
(S 0, S 1, S 2)
Initial amount of label

Amount of label not recovered




















































# 2000 British
Ecological Society
Journal of Ecology,
88, 506515
CALCULATI ONS AND S TATI STI CS

Dierences among the three methods applied in this
study with respect to the basic study unit and deni-
tions of nutrient pools and losses used to calculate
MRT are summarized in Table 1. According to the
concept of Berendse & Aerts (1987), nitrogen ux is
measured as N losses and the MRT of nitrogen is
dened as the ratio between the average N pool and
annual N losses.


Growth analysis

Dry matter productivity was calculated based on the
minimum and maximum mean dry weight of each
segment age class (S 0, S 1, etc.) per year, if these
were signicantly dierent (P < 0.05) using
Tukey's test after one-way analysis of variance with
harvest as a xed factor. In the current-year
segments, pro- ductivity was assumed to equal the
maximum dry matter reached during the year
concerned.
N and P pools were calculated based on the mean
dry matter and mean N and P concentration
summed over all green ( living) segment
types (Table 1).


15
N technique

The fate of the added
15
N label was followed by cal-
culation of the excess
15
N content of dierent seg-
ments, i.e. the total amount of
15
N reduced for the
natural abundance of this isotope (0.366% of the
total N). By denition, the pool of
15
N was the
amount of tracer recovered during September 1997,
while the dierence in
15
N between September 1997
and September 1998 was designated as N losses
(Table 1).


Retrospective analysis

The retrospective analysis is an approach that diers
from both growth analysis and the
15
N technique in
one important respect: each annual segment is
assumed to represent the result of past periods of
growth and decay accumulated during its lifetime
(cf. Callaghan et al. 1997). All calculations have
therefore to be expressed per ramet. Dry matter pro-
ductivity refers to the maximum average dry weight
attained divided by the segment's age. The N and P
pool was calculated as the average N and P content
of green segments, i.e. S 98 through S 96 (Table 1).
Using the plot of nutrient pool vs. segment age,
nutrient losses are expressed as the slope of a linear
regression through the degeneration phase (cf.
Callaghan et al. 1997), i.e. S 94 through S 89 (Table
1).


Results

DRY M ATTER PRODUCTI VI TY

Growth analysis showed that both current-year and
1-year-old segments (S 0 and S 1, respectively)
showed a signicant increase in dry weight over the
growing season (Fig. 1). Total dry matter
productiv- ity of these segment types was 9.4 and 7.2
mg during
1996 and 1997, respectively (Table 2). Dry matter
production of current year's segments in 1997 (2.7
mg) was only 52% of that of 1996 (5.2 mg).
Segments older than one year did not show signi-
cant variation in dry weight with time (Tukey's test,
P > 0.05).
Retrospective analysis revealed that H. splendens
segments achieved a maximum dry weight at an age
of 4 years (Fig. 2). The average annual
productivity per segment during the growth phase
estimated using the retrospective analysis was 2.7 mg
(Table 3).


NI TR OG EN P OOL SI ZE

The average N pool was calculated as the average N
content of live segments, i.e. S 0 through S 3, during
the season. The assumption that these segments
were still alive was based on their green colour and
on the observation that net photosynthesis becomes
negative at an age of about 3 years (Callaghan et al.
1978; Oechel & Van Cleve 1986). Since S 3 segments
turn brown during autumn this segment type was
counted as alive from June to August. The N pool
510
Nitrogen retention
by Hylocomium
splendens



Fig. 1 Dry matter of annual segments of Hylocomium
splendens in a subarctic birch woodland during 1996 and
1997. S 0 through S 5 denote current-year to 5-year-old
segments. Data are mean SE; n 1520.



was slightly smaller in 1997 as compared with 1996
(Table 2).
The retrospective analysis revealed an average N
and P pool size of 4.6 and 0.49 mmol per ramet,
respectively (Table 3).



N I TROGEN LOSSES

Estimation of nitrogen losses using the growth ana-
lysis method were based on the above distinction
between live and dead segments and yielded a loss
per segment chain per year of about 4 mmol (Table
2).
Using the
15
N approach, losses averaged 1.1 mmol
N per 100 cm
2
plot per year between
September
1997 and September 1998 (Table
2).
The retrospective analysis used variation in the N
and P pool size of dierently aged segments in the
degeneration phase sensu Callaghan et al. (1997) as
an indicator of N and P losses. Both linear regres-
sions were signicant: nitrogen pool size 6.99
0.446 segment age, R
2
0.819, P 0.0096, n
6; phosphorus pools size 0.60940.0454
segment age, R
2
0.952, P 0.0015, n 6. Thus,
ramets lost
an average of 0.446 mmol N and 0.045 mmol P per
segment per year during the rst 6 years of the
degeneration phase (Fig. 3, Table 3).


NI TROGE N TRANSLO C ATI O N I N
H. SPLENDENS

15
N analyses suggested that considerable acropetal
transport of added label occurred during the 1997
growing season (Fig. 4). Current-year segments
(S
97) increased their relative share from 2 to 20% of
the recovered
15
N from June to September 1997.
However, N recycling among ramets continued at
about the same rate from September 1997 through
September 1998 (Fig. 4). Tissues not existing when
the labelling was carried out (S 98), had accumu-
lated 1.7 mmol
15
N per plot (29% of the total
15
N
recovered) in September 1998 (Fig. 4). Current seg-
ments for that year and 1-year-old segments
together contained 61% of the label recovered dur-
ing autumn 1998, as compared with 71% in autumn
1997 (Fig. 4). The amount of
15
N in brown
segments increased from 0.3 mmol per plot (4%) in
September
1997 to 0.9 mmol (15%) in September 1998.


N I TROGEN P RODUCTI VI T Y AND M EAN
RESI DENCE T I ME
Values for mean annual nitrogen productivity (aNP)
were similar when determined by growth analysis
and by the retrospective approach (means of 615



Table 2 Dry matter productivity, average nitrogen (N) pool, N losses, annual N productivity (aNP) and mean residence
time of N (MRT) of Hylocomium splendens in a subarctic woodland during two study years (1996 and 1997) determined
using dierent methods: a conventional growth analysis (GA) and a
15
N-tracer technique (
15
N). nd not determined


Variable and method 1996 1997
Dry matter productivity (mg year
1
); GA 9.4 7.2
N pool (mmol); GA* 14.4 12.5
N pool (mmol plot
1
);
15
N nd 7.0
aNP (g mol N
1
year
1
); GA 653 576
N losses (mmol segment chain
1
year
1
); GA
N losses (mmol plot
1
year
1
);
15
N
3.8
nd
4.0
1.1{
MRT (years); GA 3.8 3.1
# 2000 British MRT (years);
15
N nd 6.4{
Ecological Society

Journal of Ecology, *Refers to `living' segments, cf. Table 1.

88, 506515 {Calculated from September 1997 to September 1998.

511
R.L. Eckstein



Fig. 2 Retrospective analysis of the dry weight and nitrogen (N) concentration of segments of Hylocomium splendens with
increasing age. Segment chains were harvested on the 26 September 1998. Data are mean SE; n 16 for dry weight and
N concentration of 0 to 6-year-old shoots, n 15, 10 and 7 for dry weight, and n 9, 4 and 2 for N concentration of
pro- gressively older segments.

and 587 g mol N
1
year
1
, respectively) (Tables 2
&
3).
Estimates of mean residence time of N in H.
splendens ranged between c. 3 and 10 years, depend-
ing on the method used (Tables 2 & 3). The lowest
MRT was estimated using the growth analysis and
the highest using the retrospective approach;
the
15
N-tracer technique gave an intermediate value.


Discussion

RECYCLI NG A ND TRA N SP ORT OF NI TROGEN
AMONG R AMETS OF H. SPLENDENS
The distribution of
15
N among ramets of H. splen-
dens presents evidence of considerable acropetal


Table 3 Average dry matter production, nitrogen (N) and
phosphorus (P) losses, average N and P pool size, annual
nutrient productivity (aNP) and mean residence time
(MRT) of N and P of Hylocomium splendens from a sub-
arctic woodland determined by retrospective analysis
transport of nitrogen in this species (Fig. 4).
Transport of carbon, phosphorus and metal cations
has been found in H. splendens and other ectohydric
species (e.g. Rydin & Clymo 1989; Wells & Brown
1996; Bru melis & Brown 1997; Bates & Bakken
1998), i.e. species apparently lacking dierentiated
conducting tissue. The recycling of N from senescing
segments in favour of the growing points appears to
be a highly ordered process. All of the
15
N captured
by the two already expanded ramets that were pre-
sent near the tip of the segment chain during label-
ling (i.e. S 96 and S 95 in June 1997) was recovered
3 months later in the now expanded current ramets
(S 97), the 1-year-old ramets and the 2-year-old
ramets (Eckstein & Karlsson 1999). Similarly, the
label in the two topmost ramets in September 1997
(i.e. S 97 and S 96) accounted for all
15
N recovered
in current (S 98), and 1- and 2-year-old ramets 1
year later (Fig. 4). Similar patterns of translocation
of N during these two observation periods suggest
that transport may occur mainly internally, since it
appears to be largely independent of weather condi-
Variable Value

Dry matter production (mg segment
1
year
1
)* 2.7
N pool (mmol segment
1
){ 4.6
P pool (mmol segment
1
){ 0.49
N losses (mmol N segment
1
year
1
){
0.446
P losses (mmol P segment
1
year
1
){
0.045 aNPN (g mol N
1
year
1
)
587
aNP
P
(g mol P
1
year
1
) 5500
tions, which varied considerably between the study
years. The year 1997 was relatively warm and dry
with c. 77 mm precipitation during the growing
sea- son from June to August. In contrast, 1998
was much wetter than a normal year (148 mm
compared to 121 mm, based on the means from
1961 to 90). It therefore seems unlikely that patterns
of clonal inte-
gration in this species (Eckstein & Karlsson 1999)





# 2000 British
Ecological Society
Journal of Ecology,
88, 506515
MRT
N
(years) 10
MRT
P
(years) 11

*Refers to all segments during the growth period (S 0
through S 4).
{Refers to green segments during the growth period (S 0
through S 2).
{Refers to segments during the degeneration period (S 4
and older).
together with strong size relationships found
between mature ramets (kland 1995) are based
solely on external transport, which would be vulner-
able to leakage of nutrients during heavy rain
showers (R.H. kland, personal
communication). Furthermore, Bates & Bakken
(1998) present new experimental data which
indicate internal (symplast)
512
Nitrogen retention
by Hylocomium
splendens



Fig. 3 Retrospective analysis of the average N and P pool of segments of Hylocomium splendens with increasing age. Pools
were calculated using the average dry weight and nutrient concentrations of each segment type (see Fig. 2). Full lines are lin-
ear regressions (P < 0.01) of N and P pool vs. segment age during 6 years of the degeneration phase dened by the
growth curve in Fig. 2 (cf. Callaghan et al. 1997).



transport of phosphorus in Pseudoscleropodium
purum, another pleurocarpous moss. The recent dis-
covery of polarized conducting cells in ectohydric
mosses (Ligrone & Duckett 1994, 1996), possibly
capable of transporting relatively large volumes of
solutes, helps to explain internal transport mechan-
isms in ectohydric mosses. In peatmosses
(Sphagnum), Rydin & Clymo (1989) have demon-
strated the existence of acropetal transport and its
ultrastructural basis.








Fig. 4 Average amount of added
15
N (mmol
15
N plot
1
) in
dierent segment types of Hylocomium splendens during
three harvests (June 1997, September 1997 and September
1998). The area of the circles is proportional to the size of
15

COMPA R I SON OF DI FF ERENT M ETHODS T O
ESTI M A T E N U TRI EN T RETEN TI ON

There is considerable variation among estimates of
MRT obtained by the dierent methods (Tables 2
&
3). These dierences are probably related to dier-
ent nutrient pools and nutrient uxes estimated by
the various methods. The lowest MRT was found
using a growth analysis approach, where the estima-
tion of MRT is based on assumptions about the dis-
tinction between living and dead segments. This
method probably overestimates annual N losses and
underestimates MRT, since it appears doubtful that
all N in brown segments would be unavailable to
the clone. Changing the denition of live and dead
segments will signicantly alter the estimated N
pool, the annual N losses and, consequently, MRT.
The retrospective approach for estimation of
nutrient losses by H. splendens yielded a nutrient
retention of about 11 and 10 years for N and
P, respectively (Table 3). Up to an age of 4 years,
seg- ments show a net increase in dry weight (Fig.
2), which is not associated with an increase in N
pool size (Fig. 3). Retrospective analysis does not
take into account possible nutrient losses in these
most active segments and thus overestimates
MRT. Retrospective analysis therefore represents an
in situ decomposition assay rather than
measuring the MRT of nutrients within the living
parts of the seg- ment chain, but as such it may
provide interesting information at the ecosystem
level.
When following the fate of added
15
N, the
a segment's excess N pool and shading indicates brown
amount of label, which cannot be recovered in the
# 2000 British
Ecological Society
Journal of Ecology,
88, 506515
segments. Labelling was carried out in early June 1997, 5
days before the rst harvest. S 98 through S 93 denote seg-
ments originating in the respective years. Data for the rst
two harvests are from Eckstein & Karlsson (1999).
system, is considered as loss. In H. splendens, more
than 95% of the recovered
15
N was found in green
segments 5 days after labelling (Fig. 4). As a
conse-
513
R.L. Eckstein
































































# 2000 British
Ecological Society
Journal of Ecology,
88, 506515
quence, senescent ramets showed
15
N concentrations
only marginally above the natural abundance
(Eckstein & Karlsson 1999). The MRT of nitrogen
estimated from losses of
15
N through time was
about 6 years (Table 2). However, labelling in
the
eld may result in some variation in the total
amount of
15
N recovered per plot, which may inu-
ence the calculation of MRT. The accurate estima-
tion of the average pool of
15
N appears thus to be
of crucial importance. Weber & Van Cleve (1981,
1984) encountered similar variation in the amount
of label recovered during sequential harvests, but in
the absence of information on the size of
15
N pools
over time, MRT cannot be estimated.
Estimated annual N losses might also change if
the pulse of
15
N were monitored over the whole life-
time of the labelled segment cohorts. However, a
study in arctic Alaska showed that even 28
months after labelling feathermosses contained
more than
90% of the label recovered and still showed
15
N
concentrations signicantly larger than the natural
abundance of the isotope (Weber & Van Cleve
1981). Furthermore, since the label appears to be
thoroughly distributed among segments at the end
of the present experiment, an annual loss rate of 1.1
mmol
15
N plot
1
year
1
appears to be a robust
esti- mate. However, assuming a 36% increase after
September 1998, would only reduce MRT estimated
over a 4-year interval to 5 years. Therefore, I con-
clude that the
15
N-tracer technique appears to be a
valid method for determination of MRT, although a
long-term study on
15
N dynamics within mats of H.
splendens would be worthwhile.


TRAI TS R ELATED TO NUTRI ENT
CONS ERVATI ON
In owering plants, loss of nutrients is mainly deter-
mined by the life span of parts that are shed and the
eciency with which nutrients are resorbed from
these parts before abscission (Escudero et al. 1992;
Aerts 1995; Garnier & Aronson 1998; Eckstein et al.
1999). The same holds true for feathermosses like
H. splendens where, judging from changes in col-
ouration, ramet life span is about 3 years (a conser-
vative estimate since brown segments are not
necessarily dead). This is within the range of leaf life
spans found in woody evergreen shrubs (Karlsson
1992). Nutrient recycling is high, with as much as
78% of the N pool resorbed from senescing seg-
ments (S 95 S 94, Fig. 4).
An important dierence between vascular plants
and bryophytes is that in the latter dead segments
are not shed but remain an integral part of the seg-
ment chain. They allow living, assimilating ramets
to be maintained in a favourable position with
respect to incoming radiation and also act in the
capillary transport of water to new growing points,
thus maintaining a favourable water balance. Mean
size of mature H. splendens segments showed posi-
tive density dependence in boreal spruce forests
(kland & kland 1996). Dead moss segments may
thus serve similar functions to the stems of woody
plants. However, since mosses are growing close to
the ground, decomposition of dead material occurs
in situ.


NUTRI ENT U SE STRATEGY

This study presents the rst attempt to estimate the
mean residence times (MRT) and the nutrient pro-
ductivity (aNP) of a dominant bryophyte.
Previously, nutrient use eciency (NUE) of bryo-
phytes has often been estimated simply as the
inverse of tissue nutrient concentration (Chapin &
Shaver 1989). In contrast to this, the concept of
Berendse & Aerts (1987) accounts for the recycling
of nutrients (cf. Garnier & Aronson 1998, p. 521).
Nutrient use eciency (i.e. the product of MRT and
aNP (Berendse & Aerts 1987) based on my
15
N
data) is therefore twice as high as the value pre-
sented for H. splendens by Chapin & Shaver (1989)
based on N concentration. The data presented here
strongly suggest that H. splendens shares a similar
nutrient use strategy to woody evergreen vascular
plants (Aerts 1990, 1995; Eckstein & Karlsson 1997;
Eckstein et al. 1999). MRT and aNP make conict-
ing demands on plant performance and there there-
fore appears to be a trade-o between them
(Berendse & Aerts 1987; Aerts 1990; Eckstein &
Karlsson 1997; Garnier & Aronson 1998). As a
result, nutrient productivity of H. splendens is low,
as it is for woody evergreen vascular plants (Tables
2 & 3; Aerts 1990; Eckstein & Karlsson 1997;
Garnier & Aronson 1998). Such a conservative
nutrient use strategy may enable these plants to sur-
vive and to dominate in chronically nutrient-poor
habitats (e.g. Aerts & van der Peijl 1993).


ECOSYSTEM EFFECTS

Large mosses acquire nutrients eciently from pre-
cipitation, throughfall and other atmospheric
sources. Between 30 and 100% of the total nitrogen
(Weber & Van Cleve 1981; Jonsdottir et al. 1995;
Eckstein & Karlsson 1999) and about half of the
phosphorus (Chapin et al. 1987) contained in simu-
lated rainfall may potentially be captured by bryo-
phytes. There is evidence for acropetal transport
and recycling of mineral nutrients and metal cations
in ectohydric mosses (Rydin & Clymo 1989; Wells &
Brown 1996; Bru melis & Brown 1997; Eckstein &
Karlsson 1999). Decomposition rates of bryophytes
are generally low owing to high C : N ratios in their
tissues (Russell 1990 and references therein).
Consequently, eux of nutrients will be small in
ecosystems with an intact bryophyte layer (Weber &
Van Cleve 1981; Bowden 1991).

Bates, J.W. (1987) Nutrient retention by Netherlands.
# 2000 British
Ecological Society
Pseudoscleropodium purum and its relation to growth.
Journal of Bryology, 14, 565580.
Garnier, E., Gobin, O. & Poorter, H. (1995) Nitrogen pro-
ductivity depends on photosynthetic nitrogen use e-
Journal of Ecology, Bates, J.W. (1989a) Interception of nutrients in wet deposi- ciency and on nitrogen allocation within the plant.
88, 506515 tion by Pseudoscleropodium purum: an experimental Annals of Botany, 76, 667672.

514
Nitrogen retention
by Hylocomium
splendens
Large forest oor mosses exert strong control on
ecosystem nutrient ux by capturing mineral nutri-
ents from canopy throughfall, incorporating them
into organic N compounds, recycling them over sev-
eral years and, after this time-lag, slowly releasing
nutrients through decomposition. By building a sur-
face layer of nutrient-poor, acidic organic substance
and as a result of the negative eects of a thick
moss cover on soil temperature (Van Cleve et al.
1983), bryophytes will maintain and reinforce the
infertility of the habitat. In this respect, large feath-
ermosses of the forest oor may act as `autogenic
ecosystem engineers' sensu Jones et al. (1994).
Likewise, the peatmoss Sphagnum fuscum has been
identied as small-scale ecosystem engineer in sub-
arctic peatlands (Svensson 1995). By capturing
mineral nutrients early in their circulation through
the ecosystem, and subsequent internal recycling,
this species retains growth limiting nutrients and
counteracts the spread of vascular plants.
Since mosses show a negative response to pertur-
bations that simulate climate change (Potter et al.
1995), accelerated nutrient turnover, increased eux
of mineral nutrients and changes in species composi-
tion may be anticipated as a consequence of global
warming, especially in boreal and subarctic regions.


Acknowledgements

I am much indebted to my supervisor, P. S.
Karlsson, for his support and encouragement during
this study. P. S. Karlsson, H. Rydin, R. Aerts and
two anonymous referees oered valuable comments
which improved the quality of the manuscript. L.
Haddon greatly improved the readability of the nal
version. K. Anton, J. Gaspar, M. Kardefelt and L.
Ericsson helped in the eld and during laboratory
work. Financial support was obtained from the
Swedish Natural Science Research Council and
from the Abisko Scientic Research Station.


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Received 9 September 1999
revision accepted February 2000