Resource allocation to vegetative and reproductive growth in relation to mast seeding in Fagus crenata
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Forest Ecology and Management 229 (2006) 228–233
Resource allocation to vegetative and reproductive growth in
relation to mast seeding in Fagus crenata
Yuko Yasumura a,*, Kouki Hikosaka a, Tadaki Hirose b
a Laboratory of Plant Ecology, Graduate School of Life Sciences, Tohoku University, 6-3 Aoba, Aramaki, Sendai 980-8578, Japanb Department of International Agriculture Development, Tokyo University of Agriculture, Sakuragaoka 1-1-1,
Setagaya-ku, Tokyo 156-8502, Japan
Received 28 October 2005; received in revised form 12 March 2006; accepted 3 April 2006
Abstract
Year-to-year variation in vegetative and reproductive growth was studied in Fagus crenata dominating a forest in Northeast Japan. Trees
synchronously produced abundant nuts in 2 mast years during 6 years of study. Nut production was absent or very sparse in the other 4 non-mast
years. Annual leaf production estimated from the amount of leaf litter did not differ between mast and non-mast years. Similarly, radial stem growth
evaluated from tree ring width was not necessarily reduced in mast years compared with non-mast years. Radial growth decreased only in 1 of the 2
mast years. Trees also invested a substantial amount of nitrogen into reproductive growth in mast years, but mast seeding did not reduce nitrogen
investment into the foliage or enhance nitrogen resorption from senescing leaves. We conclude that mast seeding does not place a strong impact on
the canopy of F. crenata trees, probably owing to resources stored in perennial tissues.
# 2006 Elsevier B.V. All rights reserved.
Keywords: Fagus crenata; Mast seeding; Resource allocation; Litterfall; Tree ring; Nitrogen resorption
1. Introduction
Many forest trees show high year-to-year variation in seed
production at the population level, a habit called mast seeding
or masting (Kelly, 1994). Mast years occur at irregular
intervals, and are followed by a year or years of poor seed
production (Fenner, 1991). Masting has been interpreted as an
evolved reproductive strategy that enhances the efficiency of
pollination and/or satiates seed predators in mast years (Kelly
and Sork, 2002).
Many species show switching in resource allocation between
vegetative and reproductive growth through successive mast and
non-mast years (see Kelly and Sork, 2002). If plants are to divert
part of carbohydrates from vegetative to reproductive growth in
mast years, then what aspect of vegetative growth is sacrificed?
Some studies reported a reduction in radial stem growth in a year
of mast seeding (Eis et al., 1965; Norton and Kelly, 1988; Selas
* Corresponding author. Present address: Department of Plant Ecology,
Forestry and Forest Products Research Institute, Tsukuba, Ibaraki 305-8687,
Japan. Tel.: +81 29 873 3211; fax: +81 29 873 1542.
E-mail address: yukes@affrc.go.jp (Y. Yasumura).
0378-1127/$ – see front matter # 2006 Elsevier B.V. All rights reserved.
doi:10.1016/j.foreco.2006.04.003
et al., 2002) and in the subsequent years (Silvertown and Dodd,
1999), while other studies reported a reduction in leaf growth in a
year of mast seeding (Pregitzer and Burton, 1991; Caritat et al.,
1996; Alley et al., 1998). These studies examined the effect of
seed production only on either aspect of vegetative growth, and it
remains unclear whether both are sacrificed at the same time.
Moreover, the studies were often conducted during a short period
without replication of mast and non-mast years.
Trees would require a large amount of N, as well as
carbohydrates, for mast seeding because fruits generally contain
a substantial amount of N (Sinclar and de Wit, 1975). Some
species have shown to draw N from senescing leaves for
reproductive growth (Chapin and Moilanen, 1991; Pugnaire and
Chapin, 1992). Do masting species also translocate N directly
from leaves to reproductive growth, and thus enhance N
resorption in response to mast seeding? Or do they draw N from
storage organs, as has been suggested by Pregitzer and Burton
(1991)? In the latter case, the extent of N resorption would be
unaffected by the occurrence of mast seeding.
The objective of the present study was to assess resource
allocation to vegetative and reproductive organs in a masting
species, Fagus crenata Blume (Siebold’s beech). We examined
year-to-year variation in: (1) carbon allocation to leaf, stem and
Y. Yasumura et al. / Forest Ecology and Management 229 (2006) 228–233 229
reproductive growth, (2) N allocation to leaf and reproductive
growth, and (3) N resorption from senescing leaves. Carbon
allocation to leaf and reproductive growth was evaluated by the
amount of leaf litter and reproductive tissues recovered in litter-
traps, and stem growth by the width of tree rings. N cost
associated with leaf and reproductive growth was evaluated by
the amount of N in their structures. The extent of N resorption
from senescing leaves was evaluated with canopy leaves
sampled in summer and autumn.
2. Materials and methods
2.1. Study site
The study was carried out in a natural beech forest located on
Hakkoda Mountains in Northeast Japan (408390N, 1408510E,
800 m a.s.l.) during the growing seasons in 1999–2005. The site
characteristics have been described previously (Yasumura
et al., 2002). The forest canopy is dominated almost exclusively
by F. crenata. The density of F. crenata trees was 778 trees/ha
and the diameter at breast height was 21.6 � 14.3 cm
(mean � S.D.) in a 30 m � 30 m plot. According to Suzuki
et al. (2005), F. crenata trees showed mast seeding in 1995 for
the last time before 1999. Therefore, years 1996–1998 were
non-mast years. Climatic data for 6 study years are given in
Table 1. They were recorded at the meteorological station
<2 km away from the forest.
2.2. Litter-trap sample
Ten litter-traps were established at the beginning of the
growing season (early June) in 1999 under a closed canopy of
mature trees (�16 m). The traps had a mouth of 0.81 m2 and
were fixed ca. 1 m above the ground. Plant litter (we use the
term ‘litter’ to include both dead plant materials and live nuts)
that fell into the traps were collected monthly, and sorted into
leaf, reproductive tissues (flowers, husks, and nuts), and woody
tissues (including bark and bud scales) in the laboratory. Litter
that fell from species other than F. crenata was discarded. The
traps were removed in mid November after the period of
autumnal leaf-fall, because they do not withstand the weight of
snow that can accumulate more than 4 m. Eight to ten traps
were established in spring and removed in winter in the
Table 1
Climatic condition during 6 years of study
Precipitation (mm) Solar radiation (h)
February–Novembera May–October January–December May–Octob
1999 1649 1293 1250 833
2000 M 1491 914 1108 791
2001 1457 1135 1235 771
2002 1400 965 1115 667
2003 M 1296 959 1173 751
2004 1367 941 1162 744
Six months from May to October are the growing season; M denotes a mast year.a Total precipitation for the entire year was not available.
following five growing seasons. Though traps were relocated
each year to minimize the impact on forest floor, they were
always under similarly closed canopies and were within the
same small plot (50 m � 50 m). Bud scales, leaves, and flowers
that fell in early spring before the establishment of traps were
collected from the ground and added to the sample. The
samples were brought to the laboratory, where they were dried
in an oven at 70 8C for at least 72 h and weighed. The samples
were then ground with a mill (EFDU-KT; Hitachi Ltd., Tokyo,
Japan) and their N concentration was determined with an NC
analyzer (SUMIGRAPH NC-80; Shimadzu Ltd., Kyoto,
Japan). The total amount of N in the sample was calculated
as the product of dry mass and N concentration.
2.3. Stem core sample
Stem cores were sampled at the breast height (135 cm) from
16 mature trees on September 6–7, 2005. The diameter at the
breast height of these trees ranged 30.6–55.7 cm and averaged
40.5 � 8.6 cm. In the laboratory, the cores were scraped and
ring widths were measured to the nearest 0.01 mm with a slide
caliper under a binocular microscope. Radial growth index was
calculated as the percentage difference between ring width in
year i (wi) and ring width averaged over 6 years between 1999
and 2004 (w):
Radial growth index ¼ wi � w
w:
Therefore, a positive or negative value indicates growth
larger or smaller than the 6-years mean, respectively. Possible
variation associated with tree age was not considered because
the short 6-years period was focused in the present study, and
because tree ring width was very small (around 1 mm) in light
of the large stem diameter (around 40 cm).
2.4. Canopy leaf sample
Seasonal changes in leaf N content per area (Narea) were
examined from June (expanding leaves) to November (dead
leaves) in leaves belonging to the lowermost position (4–5 m
above the ground) of mature trees in 2000 (n = 20–30; 5–10
leaves from each of 2–3 trees). The data revealed that leaf N
content is relatively stable during summer, and declines sharply
Mean temperature (8C) Wind velocity (m/s)
er January–December May–October January–December May–October
5.5 14.1 3.0 2.5
5.3 14.2 2.9 2.2
4.5 13.2 2.9 2.3
5.0 12.9 2.7 2.2
5.1 12.7 2.6 2.1
5.9 14.0 2.8 2.2
Y. Yasumura et al. / Forest Ecology and Management 229 (2006) 228–233230
Table 2
Dry mass of litter (kg/(ha year)) released annually by Fagus crenata
Leaf Reproductive tissues Woody tissues
1999 2805 � 174 a 33 � 53 a 461 � 231
2000 M 2210 � 137 b 1527 � 458 b 267 � 156
2001 2339 � 345 b 40 � 23 a 563 � 371
2002 2113 � 188 b 135 � 108 a 487 � 410
2003 M 2820 � 245 a 873 � 246 c 343 � 251
2004 2125 � 114 b 28 � 19 a 730 � 655
Different letters (abc) indicate significant yearly variation at P < 0.05 (Tukey–
Kramer test); M denotes a mast year.
Fig. 1. Seasonal changes in nitrogen content in Fagus crenata leaves in 2000.
in autumn with leaf senescence (Fig. 1). N resorption efficiency
was calculated as the percentage difference in mean Narea
between green leaves sampled in summer and dead leaves
sampled at the end of autumn (Aerts, 1996):
N resorption efficiency ð%Þ
¼ green-leaf Narea � dead-leaf Narea
green-leaf Narea
� 100:
Leaf area was determined with an area meter (Li-3100; LI-
COR, Lincoln, NA, USA) and dry mass and N concentration
were determined as described above. In 1999, green leaves
were obtained from six canopy positions in a mature tree and
dead leaves were collected from the ground (n = 30). In 2000,
2001, 2003, and 2004, green and dead leaves were sampled
from the same lowest canopy position (n = 15–30; 5–10 leaves
from each of two to three trees). Dead leaves could not be
sampled in 2002 due to early snowfall.
Fig. 2. Dry mass (bar) and nitrogen concentration (line) of: (a) leaf, (b) reproductive
1999–2004. An arrow indicates a day when wind velocities over 8 m/s was record
2.5. Statistical analyses
Statistical tests were performed using Stat View Version 5.0
(SAS Institute Incorporation, Cary, IN). Differences among
different years were analyzed by ANOVA. When the difference
was significant at P < 0.05, post hoc multiple comparison was
made using Tukey–Kramer test.
3. Results
3.1. The occurrence of mast seeding
F. crenata trees synchronously produced a substantial
amount of nuts in 2000 and 2003 (Table 2). Therefore, these 2
years were regarded as mast years. On the other hand, there
were little or no reproductive activities (flowering and nut
production) observed in 1999, 2001, 2002, and 2004. These 4
years were regarded as non-mast years.
3.2. Seasonal pattern of litterfall
Leaf-fall was concentrated in autumn (from early October
until early November) in all years (Fig. 2a). Leaf litter N
tissues, and (c) woody tissues recovered in litter-traps during growing seasons of
ed. M denotes a mast year.
Y. Yasumura et al. / Forest Ecology and Management 229 (2006) 228–233 231
Table 3
The amount of nitrogen in litter (kg/(ha year)) released annually by Fagus
crenata
Leaf Reproductive tissues Woody tissues
1999 40.3 � 2.7 a 0.2 � 0.2 a 2.1 � 0.9
2000 M 30.2 � 3.8 bc 23.8 � 6.9 b 1.7 � 1.0
2001 27.7 � 4.4 b 0.1 � 0.1 a 3.8 � 2.3
2002 26.1 � 2.5 b 1.6 � 1.4 a 3.0 � 2.0
2003 M 30.6 � 5.5 bc 11.2 � 3.6 c 2.5 � 1.9
2004 34.9 � 2.6 c 0.2 � 0.2 a 4.2 � 2.6
Different letters (abc) indicate significant yearly variation at P < 0.05 (Tukey–
Kramer test); M denotes a mast year.
Fig. 3. Radial growth index of 16 mature trees. Each bar represents one tree,
arranged from left (the smallest) to right (the largest) by diameter at breast
height (dbh). Means (�S.D.) of 16 trees are given in the graph. Different letters
indicate significant yearly variation at P < 0.05 (Tukey–Kramer test). M
denotes a mast year.
concentration had been reduced by this time due to N resorption
in the course of leaf senescence. Green, pre-senescent leaves
fell occasionally in summer during the sampling intervals when
strong wind velocities (>8 m/s) were recorded (arrows in
Fig. 2). Summer leaf-fall occurred in a small quantity, but
leaves had relatively high N concentrations. There was no
apparent difference in the seasonal pattern of litterfall between
mast and non-mast years.
Large part of reproductive tissues was released in autumn in
2 mast years (Fig. 2b). N concentration of total reproductive
tissues was high at this time, reflecting the N concentration of
mature nuts (2.62%) being dispersed. Husks, which also
accounted for a major part of reproductive tissues, had
considerably a low N concentration (0.43%).
In most cases, fall of woody tissues was observed in the
sampling intervals with strong winds (Fig. 2c). Therefore, no
apparent seasonal trend was found. N concentration of woody
tissues was generally low, except in spring in some years.
3.3. Yearly variation in dry mass and N in litter
Leaf litter accounted for 78–85 and 56–70% of total litter in
non-mast and mast years, respectively. Dry mass, the amount of
N, and N concentration in total leaf litter varied significantly
among years (P < 0.0001, ANOVA; Tables 2–4). However, leaf
dry mass was not necessarily smaller in mast years. In fact, the
largest leaf dry mass was found in a mast year (2003) and in a
non-mast year (1999). Similarly, changes in the amount of N or
N concentration were not correlated with the occurrence of
mast seeding.
Table 4
Nitrogen concentration of litter (%dry mass) released annually by Fagus
crenata
Leaf Reproductive tissues Woody tissues
1999 1.44 � 0.05 a 0.59 � 0.26 a 0.46 � 0.06 a
2000 M 1.37 � 0.13 a 1.56 � 0.20 b 0.66 � 0.09 b
2001 1.19 � 0.05 bc 0.39 � 0.15 a 0.73 � 0.13 b
2002 1.24 � 0.04 b 1.32 � 0.36 b 0.68 � 0.09 b
2003 M 1.08 � 0.16 c 1.28 � 0.16 b 0.75 � 0.11 b
2004 1.64 � 0.08 d 0.67 � 0.38 a 0.68 � 0.14 b
Different letters (abcd) indicate significant yearly variation at P < 0.05 (Tukey–
Kramer test); M denotes a mast year.
Reproductive tissues accounted for 0–5 and 22–38% of
total litter in non-mast and mast years, respectively. Dry mass,
the amount of N and N concentration in reproductive tissues
varied significantly among years (P < 0.0001; Tables 2–4).
Apparently, they were larger in the 2 mast years (2000 and
2003) than in the non-mast years, except for N concentration
in 2002. Dry mass and the amount of N differed also between 2
mast years; the magnitude of nut production was larger in
2000 than in 2003.
Woody tissues accounted for 7–18% of total litter. Dry mass
and the amount of N in woody tissues did not differ
significantly among years (P = 0.2126 and 0.0523; Tables 2
and 3). There was significant yearly variation in N concentra-
tion (P = 0.0002; Table 4), which was lower in 1999 than in the
other years.
3.4. Stem radial growth
Radial growth index differed significantly among years
(P < 0.0001, ANOVA). Radial growth was largest in 1999 and
second largest in 2004 (Fig. 3). Most trees showed positive
values in these 2 non-mast years, but there were also a few trees
that showed negative values. Compared with 1999 and 2004,
radial growth was smaller in the other 4 years. Though the
difference was not significant among these years, radial growth
tended to be smaller in 2000, a mast year with more nut
production than the other mast year, 2003.
Fig. 4. N resorption efficiency in Fagus crenata leaves in 5 years. NA: data not
available; M denotes a mast year.
Y. Yasumura et al. / Forest Ecology and Management 229 (2006) 228–233232
3.5. N resorption from senescing leaves
Narea changed seasonally (Fig. 1). Narea declined during the
period of leaf expansion in May, stabilized in summer, and
declined sharply during the period of leaf senescence in
October. The efficiency of N resorption was similar among
years 1999–2003 irrespective of the magnitude of nut
production (Fig. 4). N resorption efficiency was exceptionally
low in 2004.
4. Discussion
Resource-matching hypothesis explains mast seeding as a
response of plants to weather conditions that influence resource
availability (Kelly and Sork, 2002). However, precipitation,
solar radiation, and temperature were relatively invariant
among study years (Table 1) and the occurrence of mast seeding
was not associated with favorable conditions in F. crenata.
Previous studies showed that many mast species sacrifice part
of their vegetative growth for reproduction (Pregitzer and Burton,
1991; Caritat et al., 1996; Alley et al., 1998; Eis et al., 1965; Selas
et al., 2002). In Fagus crenta, however, neither annual leaf
production nor stem growth was apparently reduced in mast
years compared with non-mast years. Firstly, the amount of leaf
litter was not correlated with the magnitude of nut production
(Table 2). F. crenata trees produced similar amounts of leaf in the
canopy among mast and non-mast years. Secondly, radial growth
index did not show a consistent change with the occurrence of
mast seeding (Fig. 3). Radial growth varied among non-mast
years, being largest in 1999. Such variability may be related to the
length of interval between 2 mast years. F. crenata trees had not
produced abundant nuts for 4 years in 1999 (Suzuki et al., 2005),
compared with 1–2 interval years in other non-mast years
(Table 2). Radial growth seemed to be reduced markedly in one
of the mast years (2000), but not in the other (2003). Nut
production was larger in 2000 than in 2003 (Table 2). Radial
growth may be sacrificed only when the extent of nut production
exceeds a certain level. It must be noted that even in 2000, not all
mature trees reduced radial growth (Fig. 3). The results suggest
that mast seeding does not necessarily place a pronounced impact
on the radial growth in F. crenata.
The amount of leaf plus reproductive tissues increased
considerably in mast years (154–155% compared with the
mean for non-mast years). The reduction in radial growth, if
any, may not be able to fully account for such a large increase in
dry mass. Some species can assimilate a substantial amount of
carbon with their leaf-like infructescence organs (Hoch, 2005).
However, F. crenata lacks such organs that would self-support
development of nuts. Therefore, it is unlikely that F. crenata
obtain extra carbon with their reproductive organs in a mast
year. Generally, tree species build up carbohydrate storage in
perennial tissues (Chapin et al., 1990; Kozlowski, 1992).
Previous studies suggested that some masting species draw
such reserves for reproductive growth. For example, Miyazaki
et al. (2002) reported that the amount of storage starch was
smaller in reproductive shoots than in non-reproductive shoots
of Styrax obassia. Hoch et al. (2003) reported that the
concentration of storage carbohydrates in branch and stem was
decreased at the time of nut maturation in F. sylvatica. It is
possible that also in F. crenata, increased carbon demand was
met partially with the reserves in mast years.
A substantial amount of N was used for reproductive growth in
mast years (Table 3). Chapin and Moilanen (1991) suggested that
reproductive organs draw N from senescing leaves in Betula
papyrifera. In F. crenata, however, N resorption efficiency was
not enhanced in response to mast seeding (Fig. 4). N resorption
efficiency was comparably high among 4 years (1999–2001,
2003) irrespective of the magnitude of nut production. Although
N resorption efficiency was determined only in the lowest canopy
positions in most of the years, similar values may apply to the
whole canopy because there was no significant vertical variation
in N resorption efficiency in F. crenata in the same forest
(Yasumura et al., 2005). N resorption efficiency was exception-
ally small in 2004. Year-to-year variation may arise from climatic
factors (Nordell and Karlsson, 1995), but precipitation, solar
radiation and temperature were similar among the 6 years
(Table 1). It remains unclear what caused a reduction in N
resorption in 2004.
The results suggest that F. crenata trees did not retranslocate
N from the foliage to reproductive tissues. This is probably
because the timing of nut maturation was not coupled with the
timing of N resorption. Nuts started falling earlier than the
completion of autumnal leaf senescence, making it difficult for
trees to directly transport N from the foliage to nuts. In F.
crenata, N resorption may be important in conserving N for the
next year growth rather than in supporting current reproductive
growth. N that is resorbed from senescing leaves would be
stored in perennial tissues, and retranslocated when in need
(Stepien et al., 1994). Undoubtedly, N storage as well as
carbohydrate storage plays an important role in supporting
reproductive growth in a mast year.
Because N was not recycled from the foliage to nuts within a
year, the amount of N released through litterfall was increased
by the amount of N in reproductive tissues in mast years
(Table 3). Pregitzer and Burton (1991) reported a similar
increase in N return in Acer saccharum. As seeds and seedlings
of F. crenata have high mortality (Akashi, 1997), large part of N
in reproductive tissues would eventually be incorporated in N
cycling in the forest (Zackrisson et al., 1999).
The seasonal pattern of leaf or woody tissue fall was not
influenced by the occurrence of mast seeding (Fig. 2). In contrast,
the timing of leaf-fall was affected by reproductive growth in
Nothofagus truncata (Alley et al., 1998). In F. crenata, most of
the leaves were released from mid October to mid November
every year. Some leaf-fall occurred in summer due to strong
winds, and caused loss of N that would otherwise be resorbed in
autumn. Fall of woody tissues was associated with strong winds
(see Fig. 2) and similar phenomena have been observed in other
forests (Enright, 1999; Lebret et al., 2001).
5. Conclusions
The present study showed that F. crenata trees allocated a
substantial amount of carbohydrates and N into reproductive
Y. Yasumura et al. / Forest Ecology and Management 229 (2006) 228–233 233
growth in mast years. However, leaf production, radial growth,
or N investment in the foliage was not reduced markedly in
mast years compared with non-mast years. Nor did trees
enhance N resorption from senescing leaves in response to mast
seeding. Therefore, trees did not sacrifice a large part of annual
vegetative growth for reproduction. These results suggest that
mast seeding relies on stored resources in F. crenata. Without
such resources, trees would not be able to sustain a sufficient
amount of leaves and abundant nuts in the canopy at the same
time. It may be critical for F. crenata trees to produce enough
leaves in the canopy every year, because they can photo-
synthesize only in a short growing season.
Acknowledgements
We thank T. Ozaki and Y. Matsumoto for their help with the
fieldwork and the Mt. Hakkoda Botanical Laboratory of Tohoku
University for logistic support. We also thank N. Kamata for
information on the Hakkoda forest, and anonymous reviewers for
their valuable comments. This work was supported by Grants-in-
aid of the Japan Ministry of Education, Science, Sports, and
Culture and by Research Fellowships of the Japan Society for the
Promotion of Science for Young Scientists.
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