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: [email protected] (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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