Annals of Botany 77, 477–486, 1996
Central Die-back of Monoclonal Stands of Reynoutria japonica in an Early Stage
of Primary Succession on Mount Fuji
N A O K I A D A C H I*†, I C H I R O T E R A S H I M A‡ and M A S A Y U K I T A K A H A S H I*
* Department of Plant Sciences, Faculty of Science, The UniŠersity of Tokyo, Hongo, Bunkyo-ku, Tokyo,
113 Japan and † Institute of Biological Sciences, UniŠersity of Tsukuba, Tsukuba, Ibaraki, 305 Japan
Received : 21 June 1995
Accepted : 23 November 1995
Reynoutria japonica is a common perennial pioneer species on Japanese volcanoes. In a volcanic desert (1500 m above
sea level) on Mount Fuji (3776 m), central Japan, this species forms circular stands (patches). As a patch develops,
shoot density decreases in its centre (‘ central die-back ’). The central die-back has been considered a key process in
the early stages of primary succession, though its mechanism has been unknown.
The pattern of patch development, population dynamics of aerial shoots, and growth patterns of below-ground
organs were analysed in order to investigate the mechanism of die-back, and the following traits are clarified : (1)
central die-back areas occur in most small patches (approx. 1 m#) without later successional species ; (2) shoot
characteristics are dependent both on their position within a patch and on patch size ; (3) despite the large differences
in shoot density, neither time course of shoot growth nor their mortality differs between the centre and periphery of
patches ; and (4) rhizomes of R. japonica grow outwards with regular sympodial branching.
From these results, it is concluded that neither interspecific nor intraspecific competition is likely to be a primary
cause of the die-back phenomenon, but that central die-back is brought about intrinsically by the growth pattern of
the rhizome systems. We also discuss the importance of the central die-back in facilitating establishment of later
successional species in the early stages of primary succession.
# 1996 Annals of Botany Company
Key words : Clonal plant, central die-back, competition, facilitation, Japanese knotweed, Mount Fuji, primary
succession, Reynoutria japonica, rhizome growth, volcanic desert.
INTRODUCTION
Reynoutria japonica Houttuyn (The species shows wide
geographical variations and our plant agrees with var.
compacta Hiyama. Voucher specimen is kept in TI.)
(Polygonaceae, syn. Polygonum cuspidatum Sieb. et Zucc.),
a dioecious perennial, usually grows on sunny bare ground
or slopes and along roads or railways (Kitakawa, 1982). It
is also a dominant primary colonizer in many volcanic
deserts in Japan (Tezuka, 1961 ; Ohba, 1969, 1975).
On the southeast slope of Mount Fuji, an early stage of
primary succession has been underway since the last eruption
in 1707. Reynoutria japonica Houttuyn var. compacta
Hiyama is dominant on this volcanic desert as a pioneer
species (Ohga and Numata, 1971 ; Ohsawa et al., 1971 ;
Ohba, 1975 ; Maruta, 1981 ; Hirose and Tateno, 1984).
While the aerial shoots of R. japonica only survive for one
growing season, rhizomes remain alive for more than a
decade. Rhizomes of R. japonica extend horizontally from
the centre of the plant forming circular monoclonal stands
(Maruta, 1981). The stand is referred to as a patch here.
As a patch develops, the aerial shoot density in its centre
gradually decreases (Masuzawa and Suzuki, 1991). We call
this phenomenon ‘ central die-back ’. Herbaceous species
such as Miscanthus oligostachyus Stapf and Aster ageratoides
Turcz. subsp. oŠatus (Franch. et Savat.) Kitam. occur in the
central areas of these large R. japonica patches (Ohga and
Numata, 1971 ; Ohsawa et al., 1971 ; Maruta, 1981 ; Hirose
and Tateno, 1984 ; Tateno and Hirose, 1987 ; Chiba and
Hirose, 1993). Since these invading species are not observed
in stands of other pioneer species or on bare ground, but
only in the centres of large patches of R. japonica, central
die-back of R. japonica patches probably facilitates primary
succession on Mount Fuji.
Replacement of species in successions is often caused by
interspecific competition (e.g. Horn, 1981 ; Tilman, 1982,
1985 ; Huston and Smith, 1987 ; Bazzaz, 1990). This suggests
the hypothesis that interspecific competition occurs between
R. japonica and later successional species, and that the
central die-back is brought about because R. japonica is
eliminated through competition. Even for individuals of the
same species, severe competition frequently occurs for
resources such as light, water and nutrients (for reviews see
Harper, 1977 ; White, 1980 ; Weiner and Thomas, 1986 ;
Firbank and Watkinson, 1990). Since R. japonica forms a
dense canopy, intraspecific competition could also contribute to central die-back.
Architecture and growth pattern of below-ground organs
greatly affect the structure and dynamics of the aerial shoots
in clonal plants (for reviews see Bell, Roberts and Smith,
1979 ; Waller and Steingraeber, 1985 ; Sutherland and
Stillman, 1990). Thus, the distribution and growth traits of
* Present address : Global Environment Division, National
Institute for Environmental Studies, Tsukuba, Ibaraki, 305 Japan.
0305-7364}96}050477­10 $18.00}0
# 1996 Annals of Botany Company
478
Adachi et al.—Central Die-back of Reynoutria japonica
the below-ground organs may be responsible for the central
die-back.
Although some hypotheses have been suggested, the
mechanism for the central die-back remains unknown. The
objectives of the present study are : (1) to describe central
die-back in R. japonica with reference to its role in primary
succession ; and (2) to reveal the mechanism of central dieback. We first examined the relationship between patch
development and the central die-back processes by comparing patches of different sizes. Second, biomass and shoot
characteristics, including phenology and demography, were
compared in detail between the central and peripheral areas
of several patches of different sizes. Third, we excavated the
below-ground organs and investigated the growth pattern
of the whole patch. The results are discussed in relation to
primary succession and the significance of central die-back.
MATERIALS AND METHODS
Study site
The study site is located on the southeast slope of Mount
Fuji (3776 m), central Japan, at 1500 m above sea level
(35° 20« N, 138° 48« E). At this site, the ground is covered
with a thick basaltic scoriae layer which was formed by the
eruption of Mount Hoei (2702 m), a parasite volcano of
Mount Fuji, in 1707. The scoriae layer reaches 5 m at its
deepest. The vegetation present before the eruption was
completely destroyed (Tsuya, 1971). The dune of volcanic
gravel is about 2–3 km in width from 1400 m above sea level
to the summit of Mount Hoei. The study was carried out in
an area about 500 m wide, from 1440 to 1550 m.
The annual mean temperature measured in a nearby
forest (at Tarobo Meteorological Observatory, 1350 m
above sea level, 1±5 km from the study site) is 8±6 °C, and the
monthly means of daily maximum and minimum temperatures are 22±3 °C and 15±8 °C, respectively in August, and
2±2 °C and ®5±9 °C in January (Huzimura, 1971). Mean
annual precipitation is 4849 mm, and the climate is seldom
dry except for a short period following the summer rainy
season (Maruta, 1976). In winter, strong winds blow from
the west. There are snowfalls from midwinter to early spring
and sometimes avalanches destroy the vegetation in spring.
In the study site, the dominant pioneer species is R.
japonica. Other pioneers such as Pleuropteropyrum weyrichii
(Fr. Schm.) H. Gross var. alpinum (Maxim.) H. Gross,
Cirsium purpuratum (Maxim.) Matsum., Arabis serrata
Franch. et Savat. and Carex doenitzii Bo$ cklr. also establish
on the bare ground, forming small patches less than 1 m#.
However, later successional species such as Miscanthus
oligostachyus Stapf, Aster ageratoides Turcz. subsp. oŠatus
(Franch. et Savat) Kitam., Calamagrostis hakonensis
Franch. et Savat. and Artemisia princeps Pamp. grow only
in the centres of R. japonica patches. These pioneers and
successional herbs are all perennials and, except for the
rosettes of Arabis serrata, their aerial shoots wither in
autumn and the remaining below-ground parts overwinter.
In large patches of R. japonica, woody species like Salix
reinii Franch. et Savat. and Spiraea japonica L. fil. are also
observed. Plant nomenclature follows Satake et al. (1981,
1982 a, b, 1989).
Plant materials
Discrete clonal patches of R. japonica are distributed
throughout the study site. Since aerial shoots within a patch
possess similar characteristics such as leaf size and colour of
flower, each patch can be regarded as homogeneous, and
distinguished from other patches. Excavation of ten patches
confirmed that almost all the aerial shoots within each patch
were connected by rhizomes. Excavated materials were used
for further analysis (see Analysis of below-ground organs).
Since patches are clonal individuals, large patches can be
assumed to be older than small ones (Maruta, 1981 ; Hirose
and Tateno, 1984). Patches of 1±6, 5±9, and 29±7 m# were
estimated from the accumulated nitrogen and supply rate of
nitrogen (approx. 1±2 g m−# year−" in precipitation) to be
approx. 30, 80, and 140 years old, respectively (Tateno,
1983). There are no apparent differences in morphological
and growth characteristics between male and female patches.
Thus, the data from the different genders were pooled.
Field census and examination of aerial shoots
One hundred and twenty clonal patches of R. japonica
were selected arbitrarily to cover the whole range of the
patch sizes from 1450 to 1550 m above sea level on 1 and
2 Oct. 1993. For each of the patches, lengths of axes were
measured along the slope and at right angles to the slope.
Central die-back areas were determined by observation
from above. When there were successional species within a
patch, the area dominated by the invading species was
assumed to be the die-back area. On the basis that the patch
and die-back area are ellipses, the ratio of the die-back area
to the whole patch area was calculated. When the shape of
die-back or invaded area was irregular, the ratio of the
central area was estimated by eye. In order to investigate the
relationship between patch development and invasion of
successional species, a 50¬50 m sample area was established
at 1440 m above sea level and the number of the species
contained in each of the patches was counted.
Morphological characteristics of aerial shoots and leaf
nitrogen content were analysed for three patches of
diameters 2, 4, and 8±5 m. In each of these patches, a belttransect 50 cm wide was established through the centre of
the patch along the slope. The transects were divided into
50¬50 cm quadrats. All the aerial shoots in each of the
quadrats of the small and medium patches were harvested
and brought back to the laboratory on 3 Aug. 1990, and
those of the large patch on 7 Sep. 1990. Height, basal
diameter, number of leaves, number of primary branches
and height of the lowest attached leaf were measured for
each shoot in the quadrats of the small and the medium
patches. Average stem diameter was the mean of diameters
measured in two directions at the centre of the first internode
above the ground level. The materials were dried at 80 °C in
an oven for more than 72 h, and weighed. Subsamples of
finely ground leaves were combusted in a N-C analyser
(Sumigraph NC-80, Sumitomo Chemical Co., Osaka, Japan)
to determine nitrogen and carbon contents of the leaves.
The number of aerial shoots of R. japonica per unit area
was compared between the peripheral area where only R.
Adachi et al.—Central Die-back of Reynoutria japonica
For each of ten patches of 4–6 m in diameter with central
die-back, two 50¬50 cm areas were excavated in the centre
and at the upper end of the patch. In the peripheral areas of
the patches, rhizomes had not developed deeply, thus all the
rhizomes in the areas were collected by excavating to 30 cm.
In the centre, where litter and newly formed soil had
accumulated, some rhizomes were deeper than 30 cm.
Although they possessed a few old lateral buds, rhizomes
deeper than 30 cm had neither aerial shoots nor fresh winter
buds. The soil was, therefore, excavated to 30 cm from the
surface to collect rhizomes with winter buds. Collected
samples were brought back to the laboratory and carefully
washed. The numbers of all the remaining aerial shoots
(including those which had emerged in the previous years),
winter buds formed at the bases of aerial shoots, terminal
buds of the rhizome branches, and dormant lateral buds on
the rhizomes were counted. The fresh weight of the rhizomes
was also measured.
A quarter of a patch of 4±6¬4±0 m was excavated in Nov.
1990, and the positions and directions of apices of rhizome
branches were mapped in situ. The excavated rhizomes and
shoots were returned to the laboratory for subsequent
investigation.
Observation of the below-ground organs revealed that
aerial shoots sprout at almost the same positon for several
years, forming a small cluster of shoots. We call such a
cluster a ‘ shoot clump ’. The age of each shoot clump was
estimated by counting the repeated number of shoot
production at the clump, then the life-span of shoot clumps
was estimated with subsamples of the rhizomes excavated in
Nov. 1990.
RESULTS
The process of central die-back
The central die-back area is plotted against the area of
whole patches of R. japonica in Fig. 1. The relative cover of
the central die-back area tended to increase with the whole
patch area. All patches smaller than 0±1 m# were pure stands
without any invaders, while all patches greater than 10 m#
showed central die-back. In most patches greater than
20 m#, the central die-back area accounted for more than
50 % of the whole patch. In patches without central dieback areas, seedlings or very small plants of invading species
were sometimes found under R. japonica canopies. On the
contrary, there were central die-back patches without any
invading species. In the patch size class from 0±1 to 1±0 m#,
12 out of 25 had die-back centres. Of these 12 patches, nine
contained no later successional species. In the 1±0–10 m# size
class, 12 out of 45 die-back patches had not been invaded.
Die-back area (%)
Analysis of below-ground organs
100
80
60
40
20
0
0.01
0.1
1
10
Patch area (m2)
100
F. 1. Changes in the percentage of the central die-back area expressed
as a fraction of the whole patch area of R. japonica clones. (E) Pure
stands without any invaders, (D) patches invaded by successional
species.
Number of species per patch
japonica grew, and the central area dominated by other
species. Five patches of approx. 4 m diameter were chosen,
and two 50¬50 cm quadrats were set up in each of the
patches ; one was at the periphery, at the upslope location of
the patch, and the other in the centre. Every aerial shoot
exceeding 5 cm in height was tagged and its fate was
followed till the end of the growth season. The numbers of
newly emerged aerial shoots were counted.
479
20
15
10
5
0
0.01
0.1
1
10
Patch area (m2)
100
1000
F. 2. Relationship between the number of invading species and patch
area. (E) Number of invading woody and (D) herbaceous species.
Herbaceous species were observed to invade patches greater
than approx. 1±0 m# and woody species patches greater than
approx. 10 m#. The numbers of invading successional species
of both categories increased as patch size increased (Fig. 2).
Changes in the density of aerial shoots of R. japonica and
biomass along the belt-transects across the patches are
shown for three patches of different sizes (Fig. 3). The small
patch of 2 m diameter was a pure stand of R. japonica
without any other species. Central die-back had already
occurred in this small patch without any invaders (Fig. 3 A).
Both above-ground biomass and aerial shoot density of R.
japonica were less in the centre than in the peripheral
quadrats. In some small patches (similar size as one analysed
in Fig. 3 A), areas of bare soil without any aerial shoots were
apparent at the centre (for example, see Fig. 4).
In the 4 m diameter patch, the density of aerial shoots and
biomass of R. japonica were also smallest in the centre (Fig.
3 B). In this patch, the perennials such as Miscanthus
oligostachyus and Aster ageratoides subsp. oŠatus were
present in the die-back areas. Shoot biomass of R. japonica
decreased gradually from the quadrat at one end (left end in
the figure) towards the centre. However, the biomass of
Shoot biomass
(g d.wt per 50 × 50 cm2)
Shoot density
(No. per 50 × 50 cm2)
480
Adachi et al.—Central Die-back of Reynoutria japonica
60
A
B
C
40
20
0
200
150
100
50
0
1
2 0
1
2
3
4 0
1
2
3
Distance from the upper end of patch (m)
4
5
6
7
8
F. 3. Profiles of shoot biomass and shoot density along belt-transects across : A, small (2±0 m) ; B, medium (4±0 m) ; and C, large (8±5 m) patches
of R. japonica. (*) Aerial shoot biomass per quadrat (50¬50 cm#) of R. japonica, (8) herbaceous invaders and (+) woody invaders. (E – E)
Shoot density of R. japonica in each quadrat. Distance was measured along the slope from the upper end of each patch. Horizontal bars in (A)
and (B) indicate the central areas referred to in Table 1.
F. 4. Central die-back area in a small patch of R. japonica. The scale on the ground is 1 m.
successional species compensated for the decrease in biomass
of R. japonica. Thus, the total biomass per unit area was
almost constant across the patch.
In the large patch (8±5 m diameter), both shoot biomass
and density were much less than in the medium one. The
central area was also dominated by later successional
species (Fig. 3 C). Compared with the 4 m patch, the
number of later successional species was greater (two and
six species for these medium and large patches, respectively).
Besides the herbaceous species there were some plants of the
shrub, Salix reinii, in the lower peripheral part of the patch.
The abundance of such later successional species in this
patch was much greater than in the medium patch in most
quadrats.
Adachi et al.—Central Die-back of Reynoutria japonica
481
T     1. Comparisons of shoot characteristics of Reynoutria japonica between peripheral and central areas of patches
Small patch
Medium patch
Morphological parameters compared
Periphery
Mean³s.e.
Centre
Mean³s.e.
Dunnett’s
t-test
Periphery
Mean³s.e.
Centre
Mean³s.e.
Dunnett’s
t-test
Basal diameter (mm)
Height (cm)
Height of the lowest leaf (cm)
Leaf number
Primary branch number
Aerial shoot biomass (g d.wt)
Ratio of shoot with leaves (%)
Leaf nitrogen content (mg N g−" d.wt)
4±17³0±31
35±0³2±2
13±0³1±6
11±8³2±7
1±5³0±6
3±49³0±58
62±4³4±0
2±48³0±02
5±22³0±54
47±6³3±9
18±4³2±7
24±4³4±8
3±4³1±1
5±59³1±03
60±3³6±7
2±78³0±02
ns
*
ns
ns
ns
ns
ns
*
4±11³0±18
47±3³2±1
21±9³1±3
17±6³1±9
2±6³0±3
2±57³0±31
52±4³2±4
3±08³0±03
3±28³0±27
46±1³3±1
29±3³1±9
9±0³2±9
1±2³0±5
1±78³0±47
34±4³3±6
2±74³0±03
*
ns
*
*
ns
ns
*
*
These characteristics were compared among quadrats by one-way ANOVA and multiple comparisons between each pair were executed by
Dunnett’s t-test. Means only for the periphery and the centre are presented.
* Shows the statistically significant differences (P ! 0±05) between means of aerial shoots in the periphery and in the centre. ns denotes the
difference not significant (P " 0±05).
80
Aerial shoot characteristics
60
Cumulative number of shoots per 50 × 50 cm2
Table 1 summarizes morphological characteristics of the
aerial shoots and leaf nitrogen content of R. japonica in the
small and medium patches analysed in Fig. 3. In the small
patch (see Fig. 3 A), the height of aerial shoots in the centre
was greater than in the periphery. The means of the basal
diameter, aerial shoot dry weight, and the mean height of
the lowest attached leaf were greater in the centre than at the
periphery, though the differences were not significant. The
ratios of stem length with leaves to the whole length were
approx. 60 % both for the shoots in the peripheral and those
in the central quadrats. The means of leaf number and
primary branch number in the centre were more than twice
those in the periphery, but neither difference was significant.
Nitrogen content of leaves was significantly higher in shoots
from the centre.
In the medium patch (see Fig. 3 B), shoot basal diameter
was smaller in the centre, and the shoots in the central area
of the patch had only half as many leaves as those in the
peripheral area. Height of the shoots, biomass, or number
of primary branches per shoot did not differ significantly
between the areas. However, there was a weak but consistent
tendency for shoots to be smaller in the centre. The lowest
leaf level was significantly higher and the ratio of shoot
length with leaves was, thus, much smaller for shoots from
the centre of the patch. Significantly higher leaf nitrogen
content was observed in the periphery.
A
40
20
0
15
B
12
9
6
3
0
0
20
40
60
Days from the first census
80
100
Aerial shoot dynamics
F. 5. Changes in the cumulative number of emerged shoots (E, D)
and of dead shoots (+, *) in : A, the periphery (E, +) ; and in B, the
centre (D, *) of a medium-sized patch. The first census was carried out
on 26 May 1990.
Five medium-sized patches were selected arbitrarily, and
changes in the number of aerial shoots of R. japonica were
followed from emergence to flowering. These patches were
similar in appearance in that the central parts of them had
died back and were dominated by herbaceous species. The
changes in cumulative emergence (including the shoots
which withered) and death of aerial shoots in one of these
patches are shown in Fig. 5. On 26 May (the first census),
65 % of aerial shoots had already emerged in the periphery,
while only 27 % had appeared in the centre, indicating
delayed emergence in the centre. Figure 5 also indicates that
the flush of emergence occurred at the beginning of the
growing season in both quadrats. In the periphery, the last
emergence of an aerial shoot was observed on 23 Jun. (28 d
from the start of the census), whereas emergence of aerial
shoots lasted until 25 Jul. (after 60 d) in the centre. The
death of the tagged shoots was first observed on 6 Jul. (after
41 d) both in the centre and the periphery, and the number
of dead shoots gradually increased. A similar pattern was
482
Adachi et al.—Central Die-back of Reynoutria japonica
ds
Survivorship (%)
100
5 cm
80
lb
as
as
wb
wb
60
40
lb
20
0
0
20
40
60
Days from the first of the census
80
F. 6. Changes in the percentage of surviving shoots with time. (——)
Values in the centres and the (– – –) peripheries. Five patches are shown
using different symbols. The number of observed patches depends on
the census date. The first census was carried out on 26 May 1990.
rb
sc
F. 8. Formation of aerial shoots and buds along a rhizome branch.
as, Current aerial shoot ; ds, dead aerial shoot of previous or earlier
year ; rb, rhizome branch ; sc, shoot clump ; lb, lateral bud along a
rhizome ; and wb, winter bud formed at base of an aerial shoot.
was weak (r# ¯ 0±280, n ¯ 15, P ¯ 0±0427). This result
suggests that there was only weak density dependence on
mortality, if any. Moreover, density dependence in survivorship between the central areas and the peripheral ones
did not differ significantly (one-way analysis of covariance,
P " 0±05).
Final survivorship (%)
100
Below-ground organs
80
60
40
20
0
20
40
60
80
2
Total number of emerged shoots per 50 × 50 cm
F. 7. Relationship between the cumulative number of emerged shoots
and their final survivorship. (D) Values in the centres and the (E)
peripheries of patches.
observed in the other four patches, though the absolute
numbers of the shoots differed from patch to patch.
Changes in survivorship of the shoots in these five patches
are shown in Fig. 6. Survivorship did not differ significantly
between the central and peripheral areas on any observation
date (Mann–Whitney U-tests, P " 0±05). The aerial shoots
which died during the growing period were exclusively those
which emerged far behind the first cohort and had remained
beneath the canopy, and the mortality of the shoots that
emerged early in the growing season was practically nil
(data not shown).
Since the shoot density was different between quadrats
within a patch and from patch to patch, the dependence of
the final survivorship of shoots on the total number of
emerged shoots was also examined (Fig. 7). Excluding the
one quadrat which had a large number of emerged shoots
(71 shoots in the quadrat ¯ 284 shoots m−#), the survivorship did not show significant regression with the total
number of emerged shoots (r# ¯ 0±061, n ¯ 14, P ¯ 0±397).
Even if this quadrat was taken into account, the regression
Examination of excavated materials, together with the
field observations, indicated the following. In the peripheral
part of a patch, rhizomes grew almost horizontally, while
some rhizomes grew obliquely in the central area. No
rhizomes grew vertically downward. Rhizome diameter
varies between 5 and 10 mm near the apex of rhizome
branch, but in the central parts of the patches the diameters
of old rhizomes sometimes exceed 50 mm. The rhizome has
a thick, hard, suberized cortex except at its apex. Most of
the nodes of the rhizome bear lateral buds, and the
divergence of these buds follows a 2}5 pattern of phyllotaxis
(see Bell, 1991 for terminology). Most of these lateral buds
are covered with thick black bud scales. There also are
latent buds buried in the cortex of rhizomes. The dormancy
of buds appears to be regulated by the apical activity (apical
dominance) : lateral buds sprout when the rhizome is severed
or damaged. The aerial shoot is annual and produces
subterranean winter buds at its basal part by the end of the
growth period. These buds are covered with thin red scales
and are easily distinguished from dormant lateral buds on
the rhizomes. To distinguish these two types of buds, we call
the buds at the bases of aerial shoots and those on the
rhizomes winter buds and lateral buds, respectively (Fig. 8).
Rhizome growth pattern
By observations of below-ground organs, the following
pattern of growth of below-ground structures was determined. (1) For any patch, a tap root grows directly
downward in or near the centre of the patch. Rhizomes
extend centrifugally from the basal part of the tap root. (2)
The apex of the rhizome branch eventually becomes an
aerial shoot (Fig. 9 A). (3) The annual aerial shoot produces
a variable number of subterranean winter buds at its basal
part by the end of the growth period (Fig. 8), though small
Adachi et al.—Central Die-back of Reynoutria japonica
A
as
483
×
× ×
D
×
×
×
×
rb
arb
dc
E
B
× × ×
× ×
×
×
×
×
×
×
ds
×
rb
sc
C
×
rb
×
×
as
F. 9. Schematic diagram of rhizome branching and growth pattern. dc, Dead shoot clump ; and arb, apex of a rhizome branch. See the legend
of Fig. 8 for other abbreviations.
shoots and those which die during the growth period fail to
produce any subterranean winter buds. (4) One or more
winter buds at the aerial shoot base sprout in the following
spring to form new aerial shoots close to the mother shoot
(Fig. 9 B). Aerial shoots are produced in almost the same
position for several years, forming a small cluster of shoots
(a shoot clump) (Fig. 9 C). (5) When the shoot clump ceases
to produce new aerial shoots and dies, some lateral buds
break dormancy and begin to grow horizontally as new
rhizome branches (Fig. 9 D). New rhizome branches
sometimes extend more than 1 m. The apex of the new
rhizome develops into a new aerial shoot and forms a new
shoot clump (Fig. 9 E). The whole patch develops by
iterating these steps from (2) to (5).
Distribution of buds
Table 2 summarizes the numbers of aerial shoots and
excavated buds in peripheral and central areas of ten
patches. Since fresh weight of rhizomes per unit area varied
from quadrat to quadrat, the values are shown on both area
and weight bases. Numbers of the winter buds and terminal
buds of rhizome branches were less in the centre both on an
area and weight basis, while lateral buds were greater in the
periphery only on a weight basis. The number of terminal
buds of rhizome branches was much less than that of winter
buds. There were 2±2 times as many aerial shoots in the
peripheral compared to the central areas ; peripheral areas
also had 3±7 times as many aerial shoots as central areas
when compared on a rhizome weight basis (P ! 0±01).
T     2. Comparisons of fresh weight of excaŠated rhizomes
and number of shoots and buds of Reynoutria japonica
between peripheral and central areas of ten patches
Periphery
Mean³s.e.
Centre
Mean³s.e.
P
Comparison by area
(Number per 50¬50 cm#)
Fresh weight (kg)
0±486³0±054 0±924³0±219 ns
Shoot
54±2³13±2
24±7³5±9
**
Winter bud
64±0³14±6
40±9³10±7
*
Terminal bud of rhizome branch
7±5³2±3
3±0³1±0
*
Lateral bud
13±8³2±8
15±4³5±2
ns
Comparison by weight
(Number per kg f.wt)
Shoot
108±7³21±0
29±1³5±1
**
Winter bud
132±7³24±8
46±4³8±2
**
Terminal bud of rhizome branch 15±4³3±5
4±3³1±5
*
Lateral bud
31±9³6±2
19±0³5±5
*
Only winter buds exceeding 5 mm were counted, while the other buds
were counted irrespective of size. Not only current shoots but all the
remaining shoots were counted. The values were compared between
quadrats by Wilcoxon signed-ranks test. Number of quadrats were ten
for each area. * and ** show the statistically significant differences
(P ! 0±05 and 0±01, respectively) between the means. ns denotes the
difference not significant (P " 0±05).
The directions of apices of rhizome branches are shown in
Fig. 10 A. The plan clearly shows that the apices were
generally directed outwards. Figure 10 B shows the distribution of differences in angle between each apex direction
484
Adachi et al.—Central Die-back of Reynoutria japonica
A
7
slope
N
B
6
2.0
Frequency
5
1.0
4
3
2
1
1.0
2.0
Distance from the centre (m)
0.0
0
–160 –120 –80 –40
0
40
80
Angle difference (deg.)
120
160
Number of current aerial shoots per clump
F. 10. A, Distribution map of apices of rhizome branches. Arrows show the directions of apices of rhizome branches. The starting point of each
arrow indicates the location of an apex. The hatched area indicates the clonal stand of R. japonica. B, Frequency distribution of differences
between each apex direction and radial direction at its site.
formation is shown in Fig. 11. No shoot clumps were
observed producing aerial shoots more than six times. Since
some winter buds may remain dormant for more than a year
before emergence, clumps repeating shoot formation n
times might be older than n years. However, it is certain that
shoot clumps have shorter life-spans than patches.
3
2
DISCUSSION
1
0
Mechanism of central die-back
1
2
3
4
5
6
7
Number of iterated shoot formation
F. 11. Relationship between mean number of current aerial shoots
per clump and number of iteration of shoot formation. Vertical bars
indicate the 95 % upper confidence intervals of the means. Number of
samples are from three to 18, different for each group.
and radial direction at its site. The mean difference was 7±9°,
which is not significantly different from 0° (V-test, u ¯ 4±79,
P ! 0±0001, see Batschelet, 1981 for the statistical calculation). The difference would converge to zero if the buds
were directed radially. Only three of 32 apices directed
inwards (difference angle was smaller than ®90° or greater
than ­90°) (Fig. 10 B).
Life-span of shoot clumps
Since new shoots sprout from winter buds at the bases of
their mother shoots, the number of iterations of aerial shoot
formation at the clump can be estimated by examining
morphology of shoot clumps. For example, the number of
iterations of aerial shoot formation at the clump illustrated
in Fig. 8 is two. The relationship between the current shoot
number per shoot clump and number of iterations of shoot
Although the phenomenon of invasion of successional
species into R. japonica patches is well-known, the beginning
of the central die-back or the mechanism for it have not
been investigated. However, the present study shows that
central die-back occurs in the absence of other species (Figs
1, 3 A and 4). Therefore, central die-back is not caused by
interspecific interactions, but by intrinsic factors.
Mortality of shoots observed during the growth period
was low (Fig. 6). Although there was a weak density
dependence of shoot mortality (Fig. 7), as far as our census
was concerned, even the lowest survivorship was 67 % by
the end of the growth season (Figs 6 and 7). Moreover, most
of the shoots that died were those which sprouted late in the
season and remained below the leaf canopy. Therefore, it
appears that intraspecific or intraclonal competition was
not severe. Furthermore, there were no consistent effects of
shoot position in a patch on shoot survivorship (Figs 6 and
7). This suggests that shoot mortality is not affected by
differences in environmental factors such as light and
nitrogen availability. Therefore, it is difficult to ascribe
central die-back to the increased mortality of the shoots in
the central area caused by intraspecific competition.
For some clonal plants, it has been shown that aerial
shoots are not independent of each other, but that they are
to some degree physiologically integrated (for reviews,
Harper, 1985 ; Pitelka and Ashmun, 1985 ; Hutchings and
Bradbury, 1986 ; Marshall, 1990). For such ramet populations of clonal perennials, Hutchings (1979) suggested that
the ®3}2 power law may operate only during colonization
Adachi et al.—Central Die-back of Reynoutria japonica
in new habitats and that, once colonized, the biomass and
the number of shoots are internally regulated and remain
fairly constant. Low shoot mortality of R. japonica
throughout the growth period (Fig. 6) suggests the involvement of similar regulation. However, this simple
intraclonal regulation would result in the formation of a
uniform patch, in which density of aerial shoots would be
equal both in the centre and the periphery.
The present results consistently indicate that central dieback is brought about by the characteristics of growth of
below-ground organs. First, the number of winter buds was
greater in the peripheral areas than in the central areas
(Table 2). Since sprouting rate does not differ greatly
between the periphery and the centre, the number of shoots
is most likely to be determined by the number of buds.
Fewer winter buds in the central area could result in a lower
density of shoots in the next season.
Furthermore, the number of terminal buds of rhizome
branches was greater in the peripheral areas (Table 2) and
they generally grew outwards (Fig. 10). Since the terminal
buds of rhizome branches will become aerial shoots, the
clumps will extend outwards as a whole. In addition, the
growth pattern of the rhizome systems showed that the
rhizomes grow sympodially and that they have active shoot
clumps only at the tips of the rhizomes (Fig. 9), because
shoot clumps have only limited life-span (Fig. 11). As a
natural consequence of this growth pattern, the population
of aerial shoots proceeds gradually outwards. Therefore, we
conclude that the central die-back of R. japonica is brought
about by the growth pattern of its rhizome systems.
Central die-back and primary succession
Interspecific competition has been considered as a major
process in succession (e.g. Horn, 1981 ; Tilman, 1982, 1985 ;
Huston and Smith, 1987 ; Bazzaz, 1990). For example,
Tilman (1985, 1988) claimed that competition for both light
and nutrients among dominant species is a major mechanism
in succession and predicted that a pioneer species which is
a better competitor in nutrient-poor but high-light habitat
will be replaced by species which are better competitors in
nutrient-rich but low-light conditions. The volcanic bare
ground on Mount Fuji lacks nutrients. Nitrogen, which is
a major limiting factor of plant growth in this habitat,
increased in the course of patch development, accumulating
especially in the central part of the patches (Hirose and
Tateno, 1984). Two of the species colonizing die-back areas
are Aster ageratoides and Miscanthus oligostachyus. Under
nitrogen limiting conditions these species do not grow so
well as R. japonica (Chiba and Hirose, 1993). In this
volcanic desert, however, the central die-back takes place
without interspecific competition and the invasion of later
successional species follows. Moreover, they establish only
within the patches of R. japonica, and the number of those
species increases with patch development (Fig. 2). These
results demonstrate that R. japonica facilitates establishment
of later successional species (facilitation sensu Connell and
Slatyer, 1977). A similar facilitation by an initial colonizer
Dryas drummondi was observed in primary succession
following deglaciation at Glacier Bay (Chapin et al., 1994).
485
However, it is worth noting that R. japonica is not N-fixing,
while D. drummondi is.
Facilitation was sometimes considered as a premise for
intraspecific competition as a mechanism for the replacement of dominant species (Tilman, 1982, 1985). However,
we propose that facilitation is distinct from competition as
a promoting factor of succession, and suggest that facilitation is more influential in the early stages of primary
succession on Mount Fuji. This may be partly because the
availability of resources is strictly limited in this habitat.
Ecological significance of the central die-back
Similar die-back phenomena have been reported for some
clonal plants ; e.g. Agrostis tenuis and A. canina (Watt,
1947), Anemone nemorosa (Shirreffs and Bell, 1984), and
Solidago altissima (Cain, Pacala and Silander, 1991). In all
these species, however, connections between ramets (aerial
shoots) only persist for a few years, and the whole shoot
population is often composed of a mixture of shoots of
different clones. Thus, in spite of the similar appearance in
aerial shoot distributions, central die-back of R. japonica
results from a different mechanism, and its persistent
rhizome connections and the shape of the whole patch could
have some ecological significance specific to R. japonica and
the enviroment. Here, we discuss the significance of the
phenomenon in reference to acquisition of light.
Detailed comparison of the aerial shoots revealed that the
shoots have different features depending both on their
position within the patch and on the developmental stage of
the patch (Table 1). The medium patch had thinner and
rather smaller shoots in the centre than in the periphery.
The leaf nitrogen content was much lower in the centre of
the medium patch compared to the peripheral area (Table 1)
despite the higher amount of organic nitrogen in the soil
(Hirose and Tateno, 1984). All these features of the central
shoots are typical of shaded plants (Givnish, 1988), which
suggests that the light energy available to the aerial shoots
was less in the centre of the medium-sized patch where the
die-back had proceeded and later successional species
already dominated. Actually, the relative photon flux density
(in the range 400–700 nm) at 30 cm above the ground was
one quarter in the centre of that in the periphery (data from
three medium-sized patches different from the one analysed
in Table 1). The opposite tendency was the case in the
shoots of the small patch (Table 1), suggesting that
irradiance was higher in the centre than in the periphery. If
the whole patch were covered by the closed canopy, most
shoots would suffer from mutual shading except for those at
the circumference of the patch. As long as there are no
successional species, therefore, central die-back may be an
effective way to allow better light penetration into the
canopy and higher productivity in the whole clone.
A C K N O W L E D G E M E N TS
We are grateful to Dr E. Maruta of Toho University who
gave useful advice throughout the study and to Drs H. Yura
of Natural History Museum and Institute, Chiba and
M. Tateno of Gumma University for field assistance and
486
Adachi et al.—Central Die-back of Reynoutria japonica
useful discussions. Thanks are also due to Dr N. Kachi of
Tokyo Metropolitan University and Drs A. Takenaka and
R. Hooper of National Institute for Environmental Studies
who gave critical comments on the draft. We are indebted to
colleagues in the laboratory and postgraduates of the
Department for their help in field survey and census. We
also thank to Ms M. Kouri of University of Tsukuba for an
illustration. This study was partly carried out during N A’s
tenure of the Fellowships of the Japan Society for the
Promotion of Science for Japanese Junior Scientists and
supported in part by a Grant-in-aid from the Ministry of
Education, Science, and Culture, Japan.
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