POLISH JOURNAL OF ECOLOGY
(Pol. J. Ecol.)
61
2
233–239
2013
Regular research paper
Shou-Qin SUN 1 *, Gang HE 2, Yan-Hong WU 1, Jun ZHOU 1, Dong YU 1
1
Institute of Mountain Hazards and Environment, Chinese Academy of Sciences, Chengdu, 610041
China, *e-mail: [email protected] (corresponding author)
2
School of Life Sciences, Sichuan Normal University, Chengdu, 610101 China
STARCH AND NUTRIENT CONTENTS ARE KEY FOR MOSSES
ADAPTING TO DIFFERENT SUCCESSION STAGES ALONG
A RECEDING GLACIER
ABSTRACT: Mosses are the pioneer and the
first green land plants developed during the evolutionary process, they play an important role in
the development of soil, biogeochemical cycling
and facilitating plant colonization. Although species richness, composition, diversity and cover of
moss communities vary, they grow well almost in
all forests. Why mosses can grow in different conditions? What are the adaptive strategies of mosses in different forests along primary succession
sequences? It is not still completely clear. In order
to answer these questions, nutrient and carbohydrate accumulation in mosses were tested along
the primary succession following deglaciation of
Hailuogou glacier, Gongga Mountain, China. Nitrogen (N), phosphorus (P), potassium (K) content, total organic carbon (TOC), soluble sugar
and starch accumulated in the dominant moss
species were determined and compared. TOC increased insignificantly with forest age. N, P, K contents in mosses were significantly higher in forests
with dense shrubs, where N content was seperately 1.69% in A. hookeri and 1.35% in P. schreberi
in 30 yr aged forest, P content in 30 yr and 52 yr
aged forest was seperately 0.022% and 0.020% in
A. hookeri and 0.020% and 0.017% in P. schreberi,
and K content in 30 yr and 52 yr aged forest was
seperately 0.570% and 0.553% in A. hookeri and
0.490% and 0.493% in P. schreberi. Soluble sugar
was higher in the early stage of succession, but
the opposite was observed for starch and nonstructure carbohydrate content, which was lower
journal 34.indb 233
in early successional stage. Mosses adopted different adaptive strategies in different aged forests
along receding glacier, in which starch and N, P, K
contents were key for adaptiation. That is, mosses
accumulated much more starch in the severe environment of early succession stage. In more favourable environment, N, P, K was found to be
accumulated for plant growth.
KEY WORDS: glacier foreland, mosses, nutrient, primary succession, nonstructural carbohydrate
1. INTRODUCTION
As the pioneer and the first green land
plants developed during the evolutionary
process, mosses play an important role in the
development of soil, element biogeochemical cycling, and facilitating plant colonization (Uch i d a et al. 2002). They also play an
important role in seed germination, seedling growth and forest regeneration. Delach
and Ki mme re r (2002) found that the moss
Polytrichum piliferum C. Mull. had a positive
effect on germination of Melilotus officinalis Desr. C z ar ne cka (2004) and Tu re t sky
(2003) also found that a dense moss cover
may create a more humid microclimate with
smaller temperature amplitudes and thereby
2013-07-09 14:46:50
234
Shou-Qin Sun et al.
benefits the survival of seedlings. Although
species richness, composition, diversity and
cover of moss communities varied (Gust af ss om and Ha l l ingb äck 1988, B oudre au lt
et al. 2000), they grow well almost in all kinds
of forests, irrespective of forest age and forest
continuity. Why could mosses grow in various forests conditions?
It is widely accepted that higher plants
can adapt to different environment conditions by changes in morphology and physiology. In order to survive the nutrient deficient
environment, plants might decrease growth
rate, aboveground biomass, nutrient concentration and photosynthetic capacity of plant
(Vance et al. 2003, Hi l l et al. 2006). They
also can reprogram their metabolism and/
or restructure root system architecture to
maintain the growth rate as high as possible
(Vance et al. 2003, Jain et al. 2007, G ang
et al. 2012). Plants can even change their
net photosynthetic production allocation to
growth, defence, and storage (C hapin et al.
1990), for example, allocating more carbon to
storage to enhance plant survival from severe
environment (Myers and Kit ajima 2007,
Po or ter and Kit ajima 2007). However,
much of literature on adaptive mechanism of
Fig. 1. Maps of sampling sites.
journal 34.indb 234
plant were focused on vascular plants, particularly in juvenile plants (Ku rokaw a et
al. 2004, Mye rs and Kit aj i ma 2007). For
mosses, the nonvascular poikilohydric plants
with no root system and with totally different
morphological and physiological characters
of higher plants, what kind of growth strategies they adopt in different aged forests? It is
not still completely clear.
The forefield of a receding glacier represents a pristine environment and offers
an excellent opportunity to study vegetation succession (Nol l and Wel l i nge r 2008,
S ch ma l enb e rge r and Nol l 2010). On a
glacier foreland there are very heterogeneous
conditions regarding microclimate, soil conditions, and dominant vegetation types, which
makes it possible to study the successive and
adaptive mechanisms of microorganisms and
some vegetation, such as mosses. With an
area of 80.5 km2 and a length of 15 km, Hailuogou Glacier is in the east slope of Gongga
Mountain in Sichuan, China, the highest
mountain (7,556 m) in the eastern fringe
of the Tibetan Plateau and the Hengduan
Mountain region, and is the longest maritime
glacier in the Hengduan Mountain region.
With climate change, the retreat of glaciers in
Gongga Mountain area has been fast (Wang
and Z hang 1992). Various data indicate that
the glaciers retreated by >1.88 km during the
20th century, and mass balance records show
that it suffered a sustained mass loss of snow
and ice in the period 1959/60–2003/04, with
an accumulated mass balance of 10.83 m water equivalent (L i et al. 2010). On the other
hand, retreat of the glacier also left a long glacier foreland, which provides an ideal place to
study the adaptative mechanisms of mosses
in different forest types.
By comparing the nutrient and carbohydrate accumulation of mosses along primary
succession following deglaciation of Hailuogou glacier, Gongga Mountain, China, the
present study tested two hypotheses: (1) The
reasons for which mosses could grow in various forest conditions are that mosses have adopted different adaptive strategies in different
forest types. (2) Nutrient and nonstructure
carbohydrate are the key materials for mosses
adapting to different environments. This investigation will contribute to a better understanding of the adaptive mechanisms adopted
2013-07-09 14:46:50
Adaption mechanism of moss to environment
235
Table 1. Moss species along the foreland of Hailuogou glacier.
Sites
Site 1
Age (yr)
12
Site 2
30
Site 3
40
Site 4
52
Site 5
76
Site 6
122
Dominant moss species
Racomitrium ericoides
Racomitrium ericoides, Pleurojium schreberi,
Thuidium cymbifolium, Actinothuidium hooreri
Pleurojium schreberi, Actinothuidium hooreri,
Brachythecium homocladum
Pleurojium schreberi, Actinothuidium hooreri,
Brachythecium homocladum
Pleurojium schreberi, Actinothuidium hooreri,
Hylocomiastrum pyrenacium
Pleurojium schreberi, Actinothuidium hooreri,
Hylocomiastrum pyrenacium
by mosses in different succession stages or in
different vegetation types.
2. STUDY AREA
The study was conducted in the foreland of Hailuogou Glacier, Mt. Gongga
(29°20¢–30°20¢N, 101°30¢–102°15¢E), China,
where a well established chronological sequence of vegetation succession was observed
(L i and X iong 1995, He and Tang 2008).
The succession stages (Fig. 1) with increasing
ages are: (1) glacier stage 1998 – herbaceous
community dominated by pioneers such
as Astragalus mahoschanicus Hand.-Mazz.,
Anaphalis aureo-punctata Lingelsh Et Borza,
Epilobium hirsutum Linn., Chamaenerion angustifolium (Linn.) Scop. and a few leguminous plant species and Hippophae rhamnoides Linn. Seedlings (12 yr), (2) glacier stage
1980 – midium shrubs dominated by Hippophae rhamnoides Linn., Salix rehderiana
Schneid. and Populus purdomii Rehder saplings (30 yr), (3) glacier stage 1970 – PopulusBetula community dominated by medium
P. purdomii, Betula utilis D. Don and Betula
insignis Franch. (40 yr), (4) glacier stage 1958
– Populus-Betula community dominated
by tall P. purdomii, B. utilis, B. insignis, and
shrubs (52 yr), (5) glacier stage 1934 – mixed
forest dominated by tall P. purdomii and Picea brachytyla (79 yr), (6) glacier stage 1888
– conifer forest dominated by P. brachytyla
(122 yr).
The local climate is typical of monsoon
temperate regions with distinct rainy and
dry seasons. The mean annual precipitation
is 1949 mm, as most of which (over 70%)
falling between June and October, and an-
journal 34.indb 235
Grow status
erect
erect, creeping
creeping
creeping
creeping
creeping
nual potential evaporation averages 264 mm.
The mean monthly temperature ranges from
–4.5°C to 12.7°C.
3. MATERIAL AND METHODS
Six sites with increasing ages (site 1 – site
6) were selected along the chronological sequence in the glacier foreland, representing
the late 6 succession stages (Fig. 1). At each
site, each dominant moss species was collected from 5–6 plots sized 50 × 50 cm area
and combined to one collective sample. In the
laboratory, moss samples were first cleaned of
extraneous detritus and epiphytes, and the
apices of the shoots (2–3 cm) were cut from
the moss plants. The apices were then washed
with tap water and then with distilled water
to remove all the dusts and epiphytic organisms. After air dried, the moss samples were
dried at 40°C for 48 h, and then ground to
pass through a 2 mm mesh prior to analysis.
Organic carbon content in the mosses
was determined by using the dichromate
oxidation-sulphateferrous titration method
(B a o 1999). The methods used for the analysis of universal nutrients were the semi-micro
Kjeldahl procedure for N, vanadium molybdate colorimetric method for P, and flame
photometry for K (B a o 1999). Concentration of the macronutrients was expressed as
percent dry weight.
Tissue concentrations of soluble sugars
and starch were analyzed following Te ng et
al. (2006) and Tan et al. (2010) with minor
modifications. 0.1 g of the oven-dried powder
of each sample was extracted with 80% ethanol (v/v) at 85ºC for 1 h. The solutions were
then centrifuged at 12,000 g for 10 min. The
2013-07-09 14:46:50
Shou-Qin Sun et al.
236
Fig. 2. TOC (total organic carbon), total N, total P, and total K contents (mean ± SE) in mosses along
the 6 succession stages.
ethanol extraction step was repeated three
times. The three resulting supernatants were
combined and made up to a known volume
and then subjected to soluble sugar analysis using the anthrone-sulfuric acid method
(Tan et al. 2010). The residues after soluble
sugar extraction were oven-dried overnight
at 60ºC and retained for starch analysis according to the procedures described by Tan
et al. (2010). Total nonstructural carbohydrate (NSC) was calculated as the sum of
soluble sugar and starch.
All samples were analyzed in triplicate
and data were expressed as means ± standard
deviation (SD). The significant difference
among different succession stages was tested
by one-way ANOVA at P <0.05 or P <0.01
level. All the above mentioned statistical
analyses were performed with the SPSS 11.0
program.
4. RESULTS
Dominant moss species differed in forest
stands with different ages (Table 1). Along the
six succession stages, the mosses are seperately dominated by: site 1, Racomitrium ericoides (Hedw.) Brid. (12 yr); site 2, R. ericoides,
Pleurozium schreberi (Brid.) Mitt., Thuidium
cymbifolium (Doz. et molk.) doz. et molk. and
Actinothuidium hookeri (Mitt.) Broth (30 yr);
site 3, P. schreberi, A. hookeri and Brachythe-
journal 34.indb 236
cium homocladum C. Muell. (40 yr); site 4, P.
schreberi, A. hookeri and B. homocladum (52
yr); site 5, P. schreberi, A. hookeri and Hylocomiastrum pyrenacium (Spruce) Lindb. Ex
Broth (76 yr); site 6, P. schreberi, A. hookeri
and H. pyrenacium (122 yr). Table 1 also
shows that growth status of mosses in the
early stage of deglation was erect, with time
going, moss layer was dominated by species
with creeping status.
Organic carbon content increased insignificantly with successional stage (Fig. 2).
However, the impact of successional stage on
N, P, K concentrations in mosses was significant (P <0.01). N concentration was highest
in the stand aged 30 yr, which was seperately
1.69% in A. hookeri and 1.35% in P. schreberi,
then it decreased with increasing stand age
(Fig. 2). For P and K, there was a tendency
of higher concentrations in stage with many
shrubs, i.e., the forests aged 30 yr and 52 yr,
when P content was seperately 0.022% and
0.020% in A. hookeri and 0.020% and 0.017%
in P. schreberi, and K content was seperately
0.570% and 0.553% in A. hookeri and 0.490%
and 0.493% in P. schreberi. Contrarily, P and
K concentrations were significantly lower
in mixed broadleaf-conifer forest (76 yr and
122 yr) and herbaceous community (12 yr)
(P <0.01). Fig. 2 also indicates that nutrient
accumulation in R. ericoides was significantly
lower than in P. schreberi and A. hookeri.
2013-07-09 14:46:56
Adaption mechanism of moss to environment
Soluble sugar concentrations increased
significantly in mosses from 30 yr of stand
and then kept stable with time. However, concentration of starch and nonstructural carbohydrate (NSC) decreased in mosses from
30 yr of stand (Fig. 3). Fig. 3 also indicates
that the stand aged 30 yr, which was dominated by H. rhamnoides-P. purdomii, was one
key stage and was also the key point for moss
growth and succession, in which the nutrient
element contents and carbon and nitrogen
metabolizing products reached the maximum
or minimum, after this site, the values of the
parameters changed in the reverse direction.
5. DISCUSSION
Mosses are the pioneer and the first green
land plants developed during the evolutionary processes, they play an important role in
vegetation succession (Uch id a et al. 2002).
Many studies showed that the composition
of bryophyte communities varies with forest
age and that community diversity increases
with forest continuity (S elv a 1994, B ou d re au lt et al. 2000). In this study, moss species also changed with the succession processes. The dominant moss species changed
from erect form to creeping form. The covers of moss in the six succession processes
were 5%, 25%, 55%, 65%, 70% and 60%, respectively (He and Tang 2008). Although
Nic ol e and Yves (2006) deemed that succession of bryophyte community in an boreal forest after fire was driven by changes in
available moisture and light, we thought differences in moss community compositions,
diversities, and covers were related to both
the microclimate and the adaptive mechanisms of mosses.
In this study, mosses from different stages
differed in N, P, K, soluble sugar and starch
content, indicating different nutrient utilization patterns of mosses during succession
processes. N, P and K content was higher in
mosses from forest with dense shrubs, indicating that mosses accumulated more nutrients
for plant growth in suitable environment. As
consequent products of plant photosysthesis,
soluble sugar concentrations of mosses were
higher in the late stages of succession, indicating the higher photosynthetic activities of
mosses in stands older than 12 yr.
journal 34.indb 237
237
Contrarily, starch contents were substantially higher in the early stage of succession. As mosses are poikilohydric plants, the
growth of mosses was heavily influenced by
their water content and the relative humidity in the environment (St ark 1983). In the
present study, mosses grown in the early stage
would endure heavier water stress, because
stand 1 was rarely dominated by pioneer
herbaceous communities such as Astragalus
mahoschanicus, Anaphalis aureo-punctata
Anaphalis sp, Epilobium hirsutum Linn.,
Chamaenerion angustifolium, etc., the canopy
could not maintain a high humid environment for moss growth. Kit aj i ma (1996)
indicated that there are a trade-off between
plant growth and survival caused by a tradeoff between carbon allocation to growth and
allocation to storage and defense. Carbon allocation to storage enhances plant survival, as
it allows plants to overcome periods of stress
Fig. 3. Soluble sugar, starch and nonstructural
carbohydrate (NSC) (mean ± SE) accumulated in
mosses along the 6 succession stages (see Table 1).
2013-07-09 14:47:00
238
Shou-Qin Sun et al.
and disturbance (Po or ter and Kit aj i ma
2007, Myers and Kit ajima 2007). Therefore, the higher starch contents in site 1 in the
present study was one of the adaptive strategies of mosses to suvive environmental water stress. But site 2 to site 6 were covered by
thick forest, which could provide appropriate shade and temperature for moss growth,
due to the shade-loving property of mosses.
Additionally, the litterfall and infiltrated water from upper vegetation could provide sufficient nutrients for mosses, therefore it was
not necessary for mosses to accumulate much
starch for survival.
Compared with starch, soluble sugar
represented the smaller part of nonstructure
carbohydrate content, inducing a similar
trend of NSC with starch in different succession stages, in which a higher value of
NSC (nonstructural carbohydrates) content
at site 1 was observed. It was indicated that
NSC storage in plants generally allow plants
to overcome periods of stress and should
enhance survival (Po or ter and Kit aj i ma
2007). Soluble carbohydrates might function
as cryoprotectants, antioxidants and osmotic
regulators in drought–stressed plants (Popp
and Smir nof f 1995), acquisition of desiccation tolerance in some plant is also associated with the accumulation of carbohydrates
(Nor wo o d et al. 2000). Therefore, higher
NSC content in site 1 was also benefit for the
survival of mosses from the water–stressed
environmental conditions in site 1. However,
from the perspective of light requirement of
plant, our result was in contrast to previous
studies conducted on vascular plants, which
demonstrated that shade-tolerant species
tend to have greater carbohydrate reserves
(Venek l aas and den O uden 2005). For
example, Gaucher et al. (2005) found that
saplings of the shade-tolerant Acer saccharum
had higher NSC concentrations than the intermediate light-demanding Betula alleghaniensis. Po or ter and Kit ajima (2007) found
higher carbohydrate contents and pools in
shade-tolerant species than in shade-intolerant species in the moist forest. And, this phenomenon was also observed between other
shade–tolerate and shade–in-tolerate plants,
for example Quercus and Castanea (Imaj i
and S eiwa 2010). Our results were different
to others due to mosses were not only shade-
journal 34.indb 238
tolerant but shade-loving plants. Different
trends of soluble sugar and starch in mosses
were observed along the succession stages,
which disclosing the different contribution
of them to the moss metabolism. We deemed
that starch was more responsible for moss
survival from environmental stress.
ACKNOWLEDGMENTS: The present
work was supported by the “National Natural Science Foundation of China” (Grant No. 30900201)
and the “Knowledge Innovation Project of
the Chinese Academy of Sciences” (Grant No.
KZCX2–EW–QN310, KZCX2–YW–BR–20).
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Received after revision July 2012
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