Dynamics of seedling banks in beech forest: results of a 10-year study on germination, growth and...

Dynamics of seedling banks in beech forest: results of a10-year study on germination, growth and survival

Jerzy Szwagrzyk, Janusz Szewczyk*, Jan BodziarczykDepartment of Forest Botany and Nature Conservation, Agricultural University,

Al. 29 Listopada 46, 31-425 Cracow, Poland

Received 4 November 1998; received in revised form 4 August 1999; accepted 20 December 1999

Abstract

The dynamics of a seedling bank was studied in four plots located in the Krynica Experimental Forest, southern Poland.

Each sample plot was divided into eight sectors, in which germinants and seedlings were mapped, measured, and labelled;

their survival was checked twice a year between 1989 and 1996. Maps of relative light intensities on the forest ¯oor in sample

plots were produced on the basis of measurements conducted in June and August 1991. During the entire period of study,

European beech (Fagus sylvatica L.) made up over 96% of germinants and seedlings. Numbers of beech germinants varied

strongly (from 0 to 1178) among plots and years. Each year of abundant germination was followed by one or two years of

scarce germination, and there was an increasing trend in the number of germinants in three plots between 1989 and 1996.

Seedling emergence was almost independent of relative light intensity and ®rst-season survival was positively, but weakly

correlated with it. Long-term survival of seedlings was low and strongly related to relative illumination. Results of analyses of

spatial patterns in seedlings suggested that some microsites were more conducive than others to germination and early survival

of seedlings. Survival among taller germinants was greater than among shorter ones. A true seedling bank was observed only

in two plots, where relative light intensities were 9 and 15% of full sunlight. In a plot with relative light intensity of 4%, the

seedling bank was unstable and in the least illuminated plot (<3% of full sunlight) no seedling bank was formed. Results

indicate that, even in a strongly shade-tolerant species like beech, formation of a seedling bank requires the occurrence of

canopy openings in the close proximity. # 2001 Elsevier Science B.V. All rights reserved.

Keywords: Fagus sylvatica; Natural regeneration; Seedling demography; Shade tolerance; Western Carpathians

1. Introduction

Natural regeneration in temperate forests, domi-

nated by shade-tolerant tree species, has been thor-

oughly studied for many decades, especially in Central

Europe (Burschel et al., 1992; Korpel, 1995; Madsen

and Larsen, 1997), North America (Woods, 1984;

Canham, 1989; Houle, 1994; Boerner and Brinkman,

1996) and Japan (Nakashizuka, 1988; Washitani and

Tang, 1991; Peters et al., 1992). However, the mechan-

isms involved in natural regeneration are still poorly

understood, because the whole process is usually

prolonged and complex (Streng et al., 1989; Peterken,

1996; Gray and Spies, 1996). When a tree stand

reaches the understorey re-initiation phase (Oliver

and Larson, 1990), seedlings start to appear on the

forest ¯oor; however, this does not necessarily mean

that they will eventually form the next generation of

Forest Ecology and Management 141 (2001) 237±250

* Corresponding author. Tel.: �48-12-4119044.

E-mail address: [email protected] (J. Szewczyk).

0378-1127/01/$ ± see front matter # 2001 Elsevier Science B.V. All rights reserved.

PII: S 0 3 7 8 - 1 1 2 7 ( 0 0 ) 0 0 3 3 2 - 7

canopy trees (Madsen and Larsen, 1997). Mortality

among germinants is high (Harper, 1977; Nakashi-

zuka, 1988; Boerner and Brinkman, 1996; Ida and

Nakagoshi, 1996) and the growth rates of seedlings

can be extremely low (Davis, 1991; Madsen and

Larsen, 1997). The changeability in sapling growth

rates (due to the emergence and closure of canopy

gaps) makes the species composition and structure of

the next generation of canopy trees dif®cult to predict

(Runkle and Yetter, 1987; Canham, 1989; Streng et al.,

1989; Gray and Spies, 1996).

This problem is specially pronounced in situations

where several shade-tolerant tree species share domi-

nance in a given forest type (Klinka et al., 1992; Latham,

1992; Takyu and Ohsawa, 1997). In such a case, dom-

inance can easily change from one species to another

between two consecutive generations (Lertzman, 1992;

Szewczyk and Szwagrzyk, 1996); this phenomenon is

frequently referred to as `reciprocal replacement' of tree

species (Woods, 1984). However, the mechanisms

behind that phenomenon are still unclear.

The important role of a seedling bank in natural

regeneration of forests has been stressed by many

authors (Oliver and Larson, 1990; Klinka et al.,

1992; Peterken, 1996). Some other authors have

shown the signi®cant role played by sprout banks

(Hara, 1987; Ohkubo et al., 1996) in that process.

With the creation of canopy gaps, seedlings waiting

under the canopy in the form of a seedling bank are

likely to respond with more vigorous growth (Can-

ham, 1989; Oliver and Larson, 1990), usually after a

period of acclimation to the changed light environ-

ment (Tucker et al., 1987). The fact that they do not

need to start as germinants give them an initial com-

petitive advantage over tree species which do not form

seedling banks (Shugart, 1984). Unfortunately, quan-

titative data concerning the processes of establishment

and persistence of a seedling bank are scarce.

The main goal of this research was to examine the

processes of formation of a seedling bank in a forest

dominated by shade-tolerant tree species. To follow

the fate of many individual seedlings for a number of

years, we restricted our study to four plots represent-

ing various stages of stand development within a forest

tract which was almost homogeneous in respect to

topography, elevation and species composition of tree

stands. The study extended over 11 years. The speci®c

questions asked by us were: how big is the spatial and

temporal variation in numbers of seedlings and their

survivorship? How are the density of seedlings and

their survival related to relative light intensities? Do

the seedlings appear more frequently in some places

than in the others, and how is that related to their

survival in those places? What is the age structure of a

seedling bank? Although the duration of our research

was less than the average length of time spent by

suppressed seedlings under forest canopy (Morin and

Laprisse, 1997), compared to other studies it seems

long enough to obtain some valuable information

about the dynamics of the seedling bank.

2. Study area

The study was conducted in the Jaworzyna Kry-

nicka range, the highest part of the Krynica Experi-

ment forest in the north-western Carpathians

(498170N, 208580E). The area is covered with exten-

sively managed stands of European beech Fagus

sylvatica L. and silver ®r Abies alba Mill., with an

admixture of Norway spruce Picea abies (L.) Karst.

and rowan Sorbus aucuparia L. Although these stands

have been subjected to various kinds of silvicultural

treatment, they do regenerate naturally, and some parts

of the forest still display old-growth characteristics.

Four research plots were established in the upper

part of the Czarny Potok catchment; their elevation

ranged from 960 to 1025 m. Aspect ranged from E

through NE to N, and maximum slope inclination

varied between 8 and 118. Three plots (A, B and C)

were located in old, extensively managed beech and

mixed beech-®r-spruce stands; the fourth site (D) was

situated in a mature (around 80-years old) stand.

Species composition, number of trees, basal area

and maximum tree heights (all calculated on the basis

of measurements conducted in, 1986) are given in

Table 1. Between 1986 and 1996, no timber cutting

took place. A few ®rs, beeches and one rowan were

snapped by wind during that decade, but none of them

were closer than 10 m to the study plots.

3. Methods

3.1. Field measurements

Four circular plots, 6 m in diameter, were estab-

lished in 1986: the plots had been chosen from a

238 J. Szwagrzyk et al. / Forest Ecology and Management 141 (2001) 237±250

regular 100 m�100 m grid covering a larger part of

the Krynica Experiment Forest (Szwagrzyk, 1990). In

July 1986, all seedlings within the circular plot were

mapped and measured; measurements were repeated

in June 1987, except that plot B was omitted from

measurements in 1987. Each seedling was located

using a theodolite and measuring tape. Heights of

seedlings were measured to the nearest 1.0 cm. Height

increments in seedlings which had survived more than

one growing season were measured to the nearest

0.1 cm. In total, our study spanned 11 years, but no

data were collected in 1988.

In June 1989, each circular plot was divided into

sectors (see Fig. 1) to avoid the potential in¯uence of

trampling on seedling emergence and survival. Seed-

lings in wide sectors (without trampling) were

mapped, measured, and given plastic labels with

numbers. Seedlings in narrow sectors (trampled ones)

were also mapped and measured, but not labelled. For

the labelled seedlings, censuses were repeated in

September to determine their survival.

In years 1991±1992 as well as measurements con-

ducted in June and September, two censuses of seed-

ling survival were conducted in July and August in

addition to the ones done in June and September. In

years 1993±1996, the number of censuses was again

reduced to two per year.

In 1991, a series of measurements of light intensity

on the forest ¯oor was conducted using a set of ®ve

light-meters calibrated in Lux. Measurements were

repeated twice: on 20 June, soon after beech leaf

development, and on 21 August, between 11 a.m.

and 2 p.m. June 20 was a bright sunny day with some

clouds, so the light intensity in the open varied; 20

August was an overcast day, with very little variation

in light intensity in the open. In each permanent plot,

the light intensity was measured at 36 points distrib-

uted regularly at the intersections of a 2 m�2 m grid,

covering the circular plot and its immediate environs

(Fig. 1). Light intensity was measured simultaneously

at four points randomly selected from the grid and at

one place in the open (a clearing at a forest road). The

series of light measurements at each point consisted of

15 measurements at 5-s intervals. After completing the

series at a set of four points, light meters were moved

to the next set of four points and the whole procedure

Table 1

Characteristics of the tree stands in the analyzed plots (1986) in the Krynica Experiment Forest

Plot

A B C D

Basal area (m2/ha)

Beech 16.77 16.20 34.10 31.27

Fir 0.00 0.00 5.28 0.00

Spruce 5.28 0.00 0.00 0.00

Rowan 0.00 0.00 0.00 1.20

Total 22.05 16.20 39.38 32.47

Number of trees 1±7 cm DBH per ha

Beech 2405 390 0 65

Number of trees over 7 cm DBH per ha

Beech 829 452 490 791

Fir 0 0 38 0

Spruce 38 0 0 0

Rowan 0 0 0 38

Total 867 452 528 829

Maximum tree height (m)

Beech 26 28 33 34

Fir ± ± 29 ±

Spruce 27 ± ± ±

Rowan ± ± ± 23

Maximum tree DBH (cm) 67 66 77 57

J. Szwagrzyk et al. / Forest Ecology and Management 141 (2001) 237±250 239

was repeated until measurements for the entire set of

36 points were completed.

4. Data analysis

4.1. Seedling number and survival

Statistical analyses of seedling numbers and survi-

val were con®ned to beech, because numbers of

seedlings of all other species were too small. Kendall's

coef®cient of rank correlation (t, Sokal and Rohlf,

1981) was used to compare the consistency of ranking

of sectors with respect to the number of seedlings in

different years. To get an overall measure of agree-

ment among the ranking of seven variables (numbers

of seedlings in the years: 1986, 1989, 1991, 1992,

1993, 1995 and 1996), Kendall's coef®cient of con-

cordance (W, Sokal and Rohlf, 1981) was calculated.

Signi®cance of the values of W was determined with a

w2-test. The years 1990 and 1994 were excluded from

the calculations because of extremely small numbers

of seedlings, and the year 1987 was excluded because

of the lack of data for plot B.

Similar procedures were applied to the data on

seedling survival. Coef®cients t and W were calcu-

lated for data on ®rst-season seedling survival during

four years: 1989, 1991, 1993 and 1996 (seedling

numbers in other years were too small). First-season

survival was computed by dividing the number of the

®rst-year seedlings remaining in September by the

number present in June of the same year. In Sector 8 of

plot D, more germinants were found in September

than in June of 1996, apparently due to additional late

germination of beech in July. In that case, we assumed

the number of germinants in June to be equal to that in

September.

In order to assess long-term seedling survival, the

1993 cohort was chosen because of the large number

of beech germinants in that year. Survivorship of the

1993 cohort in various sectors was compared using tcoef®cient for the ®rst, second, third and fourth growing

seasons, and W was calculated to get an overall measure

of agreement among the ranking of those four seasons.

4.2. Spatial patterns

Fine-scale patterns of seedling distribution within

plots were analyzed using Ripley's K function (Dig-

gle, 1983). This method allowed us to relate spatial

patterns to the spatial scale (range of inter-plant dis-

tances) at which they had been observed. To eliminate

edge effects, each circular plot was divided into an

inner circle and buffer zone (Szwagrzyk, 1992). The

radius of the inner circle was 1.5 m, and the buffer

zone was 1.5 m wide. Thus, our analyses spanned the

range of distances from 0.01 to 1.5 m.

Analyses of spatial patterns were conducted for the

distribution of seedlings (including germinants) in the

years 1986, 1987 and 1989. For the years 1991, 1992

and 1995, we analyzed spatial patterns of germinants.

In the years 1990 and 1994, we did not conduct spatial

Fig. 1. Design of the research plots for monitoring seedling

demography in the Krynica Experiment Forest. A, sizes and

distributions of sectors; and B, distribution of points where the light

intensity measurements were conducted in the year 1991.


analyses, because numbers of germinants were too

small. In 1993, we did not conduct spatial analysis,

because of the lack of data on exact distribution of

germinants; the number of germinants in that year was

extremely large, so we only counted them. Mapping,

measurements and labelling of surviving individuals

was done in 1994.

In years when seedlings were abundant, we also

conducted separate analyses of spatial pattern for

beech seedlings and germinants. In cases when seed-

lings of the other species were numerous enough, we

carried out separate analyses for those species.

Bivariate Ripley's K analysis (Diggle, 1983) was

employed to analyze spatial relationships between

beech seedlings and seedlings of other species (only

when the number of seedlings of the other species

exceeded 10 per plot) and to analyze relationships

between the distributions of seedlings in different

years. The latter analysis was made for all seedlings

(including germinants) in 1987 and 1989. In all other

combinations of years (1987±1991, 1987±1992,

1989±1991, 1989±1992, 1991±1992), analyses were

conducted only for germinants, so the results repre-

sented mainly spatial relationships between cohorts.

4.3. Calculating relative light intensities

The absolute light intensity recorded at each point

beneath the forest canopy was divided by the light

intensity recorded at the same time in the open to

obtain relative light intensity. The mean relative light

intensity was calculated for each point as an average

from values ascertained for 20 June and for 21 August.

On the basis of data from 36 regularly distributed

points per plot, contour maps of relative light intensity

were produced for each 10 m �10 m square using

linear interpolation. The map of sectors was then

superimposed upon each of the contour maps of

relative light intensity, and the mean relative light

intensities for each sector were determined as

weighted averages of relative light intensities as read

from the map.

4.4. Relationship between seedling number and

relative light intensity

The simple coef®cient of correlation was employed

to determine the relationship between light intensity

and seedling number or seedling survival. Light inten-

sity was represented by average values for sectors

calculated for the growing season 1991. Seedling

survival was de®ned in two different ways: as an

average ®rst-season survival for all cohorts in a given

sector, and as four-year survival of the 1993 cohort in a

given sector. The relationship between those two

estimators of seedling survival was examined using

t coef®cient.

5. Results

5.1. Numbers of beech germinants

Numbers of germinants varied strongly, both among

plots and among years (Fig. 2), from 0 to 1178

germinants per plot. During the analyzed decade, each

year of good or moderate germination was separated

from another by one (or two) years of almost no

germination. There was also an increasing trend in

numbers of germinants in three plots; only in plot A

did the highest number of germinants occur in 1993.

The big variation among plots and among years was

accompanied by a large variation among sectors

within one plot. This variation was especially pro-

nounced in the years of abundant germination, when

two sectors situated next to each other could differ in

number of germinants by an order of magnitude.

Coef®cient t, calculated on the basis of germinant

numbers by sector, yielded several signi®cant correla-

tions; most of them were positive (Table 2). The most

signi®cant correlation was ascertained for the rankings

of germinant numbers in 1993 and 1995. Only the

ranking in June 1992 failed to be correlated with the

rankings in other years. Coef®cient W for all seven

years of data on number of germinants by sector

amounted to 0.7375 (p<0.0001)

5.2. First-season survival of beech germinants

Average ®rst-season survival of beech germinants

varied from 0 to 100% per plot (Table 3), and the

average from four plots for the eight years (1989±

1996) was 51%. However, when only initial numbers

of germinants, �30 individuals per plot were taken

into account, the range of ®rst-season survival was

much narrower (1±67%).


Variation among plots for the whole period of study

was rather small (42±59%). Much bigger differences

occurred among years; the highest survival occurred in

years when numbers of germinants were very small

(100 and 80% for 1994 and 1990, respectively). Low-

est survival occurred when the number of germinants

were moderately small (19 and 39% for 1991 and

1989, respectively). In years with very large numbers

of germinants (1996 and 1993) average survival

amounted to 59 and 58%, respectively.

The survival in individual sectors was much more

variable than the averages per plot. Even in years when

average survival was above 40% in all plots (e.g. see

the year 1996 in Table 3), survival in some sectors was

zero. However, that occurred only in sectors where

initial numbers of germinants were small (1±5 indi-

viduals). In years, when average survival was poorer

(e.g. in 1991) no single sector showed exceptionally

good survival of germinants.

Most of the rank correlations (calculated for the

years 1989, 1991, 1993 and 1996) were positive. Two

of them (between years 1989 and 1991 and between

1991 and 1993) were statistically signi®cant at the

0.05 level. Coef®cient W for all four years of data on

®rst-season survival of germinants by sector was

0.3377 (p<0.0001).

Fig. 2. Numbers of germinants in circular plots for monitoring seedling demography in the years 1986±1996 in the Krynica Experiment

Forest; there are no data for the year 1988.

Table 2

Rank correlations between the numbers of beech germinants on 32 sectors in different years

Year Kendall's coefficient of rank correlation (probability)

1989 1991 1992 1993 1995 1996

1986 ÿ0.254 (0.041)* 0.032 (0.796) 0.045 (0.716) ÿ0.122 (0.328) 0.053 (0.672) 0.259 (0.037)*

1989 0.318 (0.010)* ÿ0.037 (0.767) 0.370 (0.003)** 0.360 (0.004)** ÿ0.135 (0.276)

1991 0.193 (0.121) 0.207 (0.096) 0.222 (0.075) ÿ0.072 (0.564)

1992 0.031 (0.804) 0.192 (0.122) ÿ0.102 (0.412)

1993 0.569 (0.000)*** 0.270 (0.030)*

1995 0.149 (0.230)

*p, 0.05; **p<0.01; and ***p<0.001.


5.3. Spatial patterns of seedlings and germinants

Spatial patterns of seedlings were variable; patterns

not differing signi®cantly from a random distribution

existed, as well as various kinds of aggregated and

regular patterns. In general, random patterns prevailed

in 13 out of 21 cases. Aggregated patterns were found

®ve times, and regular patterns three times. Patterns

were varied, both within plots and within years,

especially in plot C, where all types of pattern were

found in different years. In 1986 and 1992, random

patterns existed in all plots. In all other years, spatial

patterns of seedlings were less consistent.

In some cases, the results obtained by analyzing

single species or age classes separately were different

from those for all seedlings pooled together. For

instance, in plot D in 1989, all seedlings together

displayed a regular spatial pattern (Table 4); when

only germinants were taken into account did the

spatial pattern change to an aggregated distribution

(at distances 0.20, 0.25 and 0.35 m). In plot C, the

distribution of all seedlings, taken together was sig-

ni®cantly regular in 1989; however, when beech and

®r were analyzed separately, both displayed random

spatial patterns.

5.4. Comparison of seedling distribution in different

years

The analysis of spatial relationships between seed-

lings (including germinants) in 1989 and germinants

in 1991 revealed a signi®cant àttraction' in plot A

(individuals tended to occur closer to one another than

when there was no spatial relationship between them).

Similar results were obtained for germinants in 1987

and 1991: there was a statistically signi®cant àttrac-

tion' between seedlings of both cohorts at distances

�1.0 m. However, for the same plot the àttraction'

between germinants in the years 1991 and 1992 was

statistically insigni®cant.

The signi®cant àttraction' between germinants

(beech and ®r) in 1991 and 1992 was ascertained in

plot C. However, this relationship for beech germi-

nants alone was insigni®cant. In the majority of cases,

Table 3

First season survival of beech germinants in different years

Plot Survival (%)a

1989 1990 1991 1992 1993 1994 1995 1996 Weighted

average

A 23 (31) ±b (0) 1 (155) 0 (11) 59 (562) ± (0) 57 (14) 44 (147) 43

B 63 (12) ± (0) 13 (45) 67 (6) 56 (201) 100 (3) 67 (3) 64 (456) 59

C 48 (25) 100 (3) 33 (98) 82 (11) 45 (51) 100 (1) ± (0) 59 (133) 49

D 67 (49) 50 (2) 32 (149) 36 (11) 64 (192) ± (0) 50 (4) 58 (453) 55

Weighted average 39 80 19 44 58 100 57 59 ±

a Initial numbers given in parentheses.b Not defined.

Table 4

Spatial patterns in seedling distribution (including germinants) in the Krynica Experiment Forest (all species pooled)

Year Type of pattern (distance)

Plot A Plot B Plot C Plot D

1986 Random Random Random Random

1987 Aggregated (0.40±0.50 to 0.75±1.50 m) ±a Regular (1.50 m) Random

1989 Aggregated (0.55±1.50 m) Random Regular (1.40±1.50 m) Regular (1.50 m)

1991 Aggregated (0.20±0.25, 0.45±0.55

to 0.85±1.50 m)

Aggregated

(1.45±1.50 m)

Aggregated (0.5 m) Random

1992 Random Random Random Random

1995 Random ± ± Random

a Not defined.


seedlings and germinants in different years were dis-

tributed independently of one another. This indepen-

dence was especially pronounced when comparing the

distribution of seedlings in 1989 with the distribution

of germinants from the 1992 cohort; no signi®cant

spatial relationships were found.

5.5. Correlation between incident light and beech

seedling number and survival

Average light intensities varied between plots. In

plot A, average relative light intensity was 3% of full

sunlight, in plot D about 4%, in C about 9% and in plot

B about 15%. There was also a lot of variation between

sectors within plots, especially in B and C (Table 5).

Plot B was situated close to a moderately big canopy

gap. Canopy openings around plot C were more

numerous, but smaller. Plot A was the most uniform

with respect to relative light intensity on the forest

¯oor, probably due to the well-developed lower

canopy of younger beeches (see Table 1).

The correlation between relative light intensity

and initial number of germinants was negative, but

statistically insigni®cant (r�ÿ0.15, p�0.398). The

correlation coef®cient between light intensity and

average ®rst-season survival was 0.3813 (p�0.031).

Table 5

Characteristics of sectors (light intensity and seedling survival) in plots A±D in the Krynica Experiment Forest

Plot and sector

number

Relative light

intensity (%)

Average first season

survival (%)a

Four year survival

of the 1993 cohort (%)

A-1 2.5 26.9 0.0

A-2 2.5 39.9 0.0

A-3 2.5 28.6 0.0

A-4 2.5 23.9 0.0

A-5 3.1 50.0 1.8

A-6 3.8 60.7 2.6

A-7 3.3 41.9 0.0

A-8 2.5 17.0 0.0

B-1 8.2 64.2 16.0

B-2 12.4 40.5 0.0

B-3 33.7 54.4 35.0

B-4 32.5 74.8 43.2

B-5 14.7 57.3 0.0

B-6 6.8 56.3 5.0

B-7 6.7 39.0 0.0

B-8 9.2 70.3 0.0

C-1 12.0 42.4 12.5

C-2 12.9 34.1 0.0

C-3 8.1 54.0 0.0

C-4 11.9 65.5 0.0

C-5 10.0 50.0 0.0

C-6 10.4 52.9 ±

C-7 5.1 47.5 0.0

C-8 4.2 53.6 0.0

D-1 3.5 18.2 0.0

D-2 4.5 53.3 0.0

D-3 4.7 45.9 0.0

D-4 4.5 24.3 0.0

D-5 4.5 57.4 1.8

D-6 4.9 48.0 25.0

D-7 3.5 54.1 0.0

D-8 2.5 75.9 0.0

a Calculated for the years 1989±1996.


Correlation between light intensity and four-year sur-

vival of the 1993 cohort was 0.7159 (p<0.0001). The

relationship between average ®rst-season survival and

four-year survival of the 1993 cohort was statistically

signi®cant (t�0.3345, p<0.0001).

5.6. Long-term survival of beech seedlings

Survival after 4 years was usually low. In 22 of the

32 sectors, all seedlings from the 1993 cohort died. In

plots D and C, relatively high survival was found in

Fig. 3. Survival of beech cohorts between 1989 and 1996 in plots A±D in the Krynica Experimental Forest.


sectors where the initial number of germinants was

low (<10 individuals). However, in plot B, high sur-

vival occurred in sectors where initial numbers of

germinants had been over 20.

Plot A was characterized by a very rapid decline in

numbers of surviving seedlings (Fig. 3). In contrast,

mortality in plot B was more gradual, and more

seedlings survived for more than 2 growing seasons.

Survival curves for plots C and D were similar Ð

mortality rates were moderate, and ®nal numbers of

survivors very low (Fig. 3). However, there were

essential differences in survival between the latter

plots. Initial numbers of germinants in plot D were

usually higher; thus, mortality was in fact more rapid

in plot D than in plot C.

Coef®cient t was calculated for four-year survival

of the 1993 cohort. All rank correlations were positive

and signi®cant. Three (between 1993 and 1994, 1995

and 1996) at the 0.05 level, and three (1994±1995,

1994±1996 and 1995±1996) at the 0.001 level. Coef-

®cient W for the whole set of four-year survival data of

the 1993 cohort was 0.78333 (p<0.0001).

5.7. Growth rates of beech seedlings which survived

more than 3 years

In plots A and D, growth rates of all seedlings,

including those which had survived more than 3 years,

were very small. During the study, none of the seed-

lings surviving for more than 3 years had achieved a

height of 10 cm, and annual height increment was in

the 0.1±0.5 cm range. In plot D, all seedlings died

before the fall of 1996 (Fig. 3). In plot A, a few

seedlings from the 1993 cohort survived until fall 1996

(Fig. 3), despite their very poor growth rates.

Among the seedlings established after 1989 in plot

C, the survival and growth rates were slightly greater.

One seedling was almost 23 cm tall in its ®fth year of

growth, and in plot B one seedling was even 35 cm tall

in its sixth year of growth. However, other seedlings in

plot B grew poorly and died within ®ve years.

5.8. The age structure of the seedling bank

Large numbers of beech germinants were a general

feature during the period of study. However, that was

not the case for older seedlings. In plot A, there were

no seedlings older than 2 years (until 1995). Later,

survivors of the 1993 cohort formed a small but

declining group of older seedlings which survived

four growing seasons (Fig. 4). In plot D, where

survivorship was slightly better, a `seedling bank'

of a few individuals which survived at least 5 years

was formed between years 1992 and 1995 (Fig. 4).

However, in 1996 this tiny `seedling bank' disap-

peared. Permanent seedling banks occurred in plots

C and B. During the whole period of study, seedlings

older than 5 years were present in these plots (Fig. 4).

The density of older seedlings in plot B was about 1

individual/m2, which declined slightly between 1989

and 1995. In 1996, it started to grow at a very slow

pace. In plot C (Fig. 4), density of older seedlings was

about 0.5 individual/m2, and followed a similar pattern

of gradual decline in the years 1989 to 1995, with a

slight increase in 1996.

Apart from beech, silver ®r was the only species that

formed a `seedling bank'. In plot C a few ®r seedlings

established in 1991 survived through six growing

seasons and in 1996 they formed a tiny seedling bank

(along with seedlings established in 1992 and 1993).

In other plots, silver ®r germinants appeared in very

small numbers and none of them survived for longer

than a few years. The only exception was a single ®r

seedling in plot A, which in 1986 was 10 cm tall and

attained a height of 33 cm in 1996.

6. Discussion

The relative light intensities on the forest ¯oor in

this study correspond well with the earlier ®ndings in

European beech forests (Burschel et al., 1992; Madsen

and Larsen, 1997) as well as with results in forests

dominated by Fagus crenata Bl. in Japan (Nakashi-

zuka, 1988) or composed of several shade-tolerant tree

species in eastern North America (Messier and Belle-

¯eur, 1988; Reader et al., 1995). Extremely low levels

of relative light intensity (in some cases even below

1% Ð see also Minotta and Pinzauti, 1996; Emborg,

1998) were found in a single series of our measure-

ments, but these extreme values were not evident when

average relative light intensities were calculated.

Average ®rst-season survival of beech seedlings

(around 50%) was slightly higher than most of the

results obtained in other investigations (Nakashizuka,

1988; Boerner and Brinkman, 1996; Emborg, 1998).


Fig. 4. Age structures of seedlings. Explanations: (1) seedlings at least 5-years old; (2) 4-year-old seedlings; (3) 3-year-old seedlings; (4) 2-

year-old seedlings; (5) 1-year-old seedlings; and (6) germinants. Remark: In years 1991 and 1992, four censuses (in June, July, August and

September) per year were made. In other years, the first census was made in June, the second in September.


However, it is within the range of survival found in the

study by Streng et al. (1989) for numerous species

with various regeneration strategies. Even in sectors

with the lowest light intensities, average ®rst-season

survival was >10% and agreed with earlier ®ndings

that relative light intensities below 1% of full sunlight

permit ®rst-season survival of seedlings of large-

seeded species (Welander and Ottosson, 1998). Thus,

like in Chen (1997), the ®rst-season survival was not a

good estimator of the likely formation of a seedling

bank.

Although we did not record the proximate causes of

®rst-season beech seedling mortality, damping-off as a

result of fungal pathogen activity (Nakashizuka, 1988;

Burschel et al., 1992) can play an important role

during the growing season. Mortality in winter, espe-

cially in species with small germinants, like spruce,

rowan and silver ®r, may have been caused by detri-

mental effects of beech litter (Facelli and Pickett,

1991). Herbivory did not seem to be a signi®cant

factor in seedling mortality, although saplings, espe-

cially of rowan and silver ®r, were heavily browsed by

deer in the locality.

Out of more than 6000 beech seedlings observed in

the course of the study, only two grew taller than

20 cm and both were situated in plots with a partly

open canopy. Thus, the fraction of seedlings which

could eventually enter the sapling class is very small.

Our results also indicate that, in places with no large

openings in the canopy, there is little chance of

germinants attaining sapling size irrespective of

how many seedlings exist on the forest ¯oor and

how many survive the ®rst growing season.

As long-term survival of seedlings of all tree species

is generally low (even in plots with relatively high

light intensities), the occurrence of numerous germi-

nants is a prerequisite for the formation of a seedling

bank (Burschel et al., 1992; Reader et al., 1995).

Species composition of germinants almost perfectly

re¯ects species composition of the overstorey and the

spatial limitation of seedling recruitment (Ribbens

et al., 1994) probably plays an important role in this

community. Because shade-tolerant species domi-

nated the overstorey, they also dominated the seed

rain and contributed numerous germinants to the pool.

Species of smaller stature (like rowan) or light-

demanding species which do not occur in the immedi-

ate vicinity (like goat willow) are marginalized

because of their small number of germinants, probably

re¯ecting the scarcity of seed rain.

The role of the microsite mosaic in shaping the

`seedling bank' can be evaluated indirectly on the

basis of results from the spatial analyses. In general,

there are places where numbers of germinants were

high and others where they were low, and ranking was

quite consistent among many years, as shown by the

results of the test of concordance. On the other hand,

aggregated spatial patterns and mutual `attraction'

between germinants in consecutive years are not a

rule, and they did not occur in some plots (plot D).

Thus, the role of microsites for the formation of a

seedling bank seems only locally important.

The results of our study suggest that shade-toler-

ance of seedlings is not a guarantee of their success in

tree stands dominated by shade-tolerant tree species,

which cast very deep shade (Messier and Belle¯eur,

1988; Ribbens et al., 1994; Emborg, 1998). In the plot

where relative light intensity was lowest (plot A), no

seedling bank formed. In plot D, where relative light

intensity was around 4%, the seedling bank was

unstable, appearing and disappearing within few

years. Permanent seedling banks formed only in plots

where relative light intensities were much higher (9

and 15%) due to the occurrence of canopy gaps in

close proximity. Thus, contrary to some widespread

opinions (Shugart, 1984), canopy openings are also

essential for the regeneration of shade-tolerant spe-

cies. This fact is often overlooked in short-term studies

in which the occurrence of numerous seedlings on the

forest ¯oor is considered proof that natural regenera-

tion is actually taking place (Emborg, 1998). In fact,

very often it is only a `ephemeral' pulse of regenera-

tion with virtually no chance of ever attaining the

sapling stage.

The conclusion of this work is that it is impossible

to fully comprehend the dynamics of seedling banks

on the basis of short-term studies. Therefore, long-

term demographic studies on tree seedlings (Streng

et al., 1989; Houle, 1994) are necessary for under-

standing the processes of natural forest regeneration.

Acknowledgements

We would like to express our grateful thanks to

Anna Gazda and to Wieslaw Klimek for their


assistance in the ®eld. Douglas A. Maguire (Oregon

State University) and an anonymous referee provided

useful comments on the manuscript. This work was

supported by the research grant 6 P205 009 07

funded by the Committee of Scienti®c Research

(KBN).

References

Boerner, R.E.J., Brinkman, J.A., 1996. Ten years of seedling

establishment and mortality in an Ohio deciduous forest

complex. Bull. Torrey Bot. Club 123 (4), 309±317.

Burschel, P., El, Kateb, H., Mosandl, R., 1992. Experiments in

mixed mountain forests in Bavaria. in: Kelty, M.J., Larson,

B.C., Oliver, C.D. (Eds.), The Ecology and Silviculture of

Mixed-Species Forests). Kluwer Academic, Dordrecht, pp. 183±

216.

Canham, C.D., 1989. Different responses to gaps among shade-

tolerant tree species. Ecology 70, 548±550.

Chen, H.Y.H., 1997. Interspecific responses of planted seedlings to

light availability in interior British Columbia: survival, growth,

allometric patterns, and specific leaf area. Can. J. For. Res. 27,

1383±1393.

Davis, W.C., 1991. The role of advance growth in regeneration of

red spruce and balsam fir in the East-Central Maine. In:

Simpson, C.M. (Ed.), Proceedings of the Conference on Natural

Regeneration Management. Forestry Canada Ð Maritime

Region, Fredericton, pp. 157±168.

Diggle, P.J., 1983. The Statistical Analysis of Spatial Point

Patterns. Academic Press, London, 148 pp.

Emborg, J., 1998. Understorey light conditions and regeneration

with respect to the structural dynamics of a near-natural

temperate deciduous forest in Denmark. For. Ecol. Manage.

106, 83±95.

Facelli, J.M., Pickett, S.T.A., 1991. Plant litter: its dynamics

and effects on plant community structure. Bot. Rev. 57, 1±32.

Gray, A.N., Spies, T.A., 1996. Gap size, within-gap position and

canopy structure effects on conifer seedling establishment. J.

Ecol. 84, 635±645.

Hara, M., 1987. Analysis of seedling banks of a climax beech

forest: ecological importance of seedling sprouts. Vegetatio 71,

67±74.

Harper, J.L., 1977. Population Biology of Plants. Academic Press,

London, 892 pp.

Houle, G., 1994. Spatiotemporal patterns in the components of

regeneration of four sympatric tree species Ð Acer rubrum,

Betula alleghaniensis and Fagus grandifolia. J. Ecol. 82, 39±

53.

Ida, H., Nakagoshi, N., 1996. Gnawing damage by rodents to the

seedlings of Fagus crenata and Quercus mongolica var.

grosserata in a temperate Sasa grassland±deciduous forest

series in southwestern Japan. Ecol. Res. 11, 97±103.

Klinka, K., Wang, Q., Kayahara, G.J., Carter, R.E., Blackwell,

B.A., 1992. Light-growth response relationships in Pacific

silver fir (Abies amabilis) and subalpine fir (Abies lasiocarpa).

Can. J. Bot. 70, 1919±1930.

Korpel, S., 1995. Die Urwaelder der Westkarpaten. Gustav Fisher

Verlag, Stuttgart, 310 pp.

Latham, R.E., 1992. Co-occurring tree species change rank in

seedling performance with resources varied experimentally.

Ecology 73, 2129±2144.

Lertzman, K.P., 1992. Patterns of gap-phase replacement in a

subalpine, old-growth forest. Ecology 73, 657±669.

Madsen, P., Larsen, J.B., 1997. Natural regeneration of beech

(Fagus sylvatica L.) with respect to canopy density, soil

moisture and soil carbon content. For. Ecol. Manage. 97, 95±

105.

Messier, C., Bellefleur, P., 1988. Light quantity and quality on the

forest floor of pioneer and climax stages in a birch±beech±

sugar maple stand. Can. J. For. Res. 18, 615±622.

Minotta, G., Pinzauti, S., 1996. Effects of light and soil fertility on

growth, leaf chlorophyll content and nutrient use efficiency of

beech (Fagus sylvatica L.) seedlings. For. Ecol. Manage. 86,

61±71.

Morin, H., Laprisse, D., 1997. Seedling bank dynamics in boreal

balsam fir forests. Can. J. For. Res. 27, 1442±1451.

Nakashizuka, T., 1988. Regeneration of beech (Fagus crenata)

after the simultaneous death of undergrowing dwarf bamboo

(Sasa kurilensis). Ecol. Res. 3, 21±35.

Ohkubo, T., Tanimoto, T., Peters, R., 1996. Response of Japanese

beech (Fagus japonica Maxim.) sprouts to canopy gaps.

Vegetatio 124, 1±8.

Oliver, C.D., Larson, B.C., 1990. Forest Stand Dynamics.

McGraw±Hill, New York, 467 pp.

Peterken, G.F., 1996. Natural Woodland. Cambridge University

Press, Cambridge, 522 pp.

Peters, R., Nakashizuka, T., Ohkubo, T., 1992. Regeneration and

development in beech-dwarf bamboo forest in Japan. For. Ecol.

Manage. 55, 35±50.

Reader, R.J., Bonser, S.P., Duralia, T.E., Bricker, B.D., 1995.

Interspecific variation in tree seedling establishment in

canopy gaps in relation to tree density. J. Veg. Sci. 6,

609±614.

Ribbens, E., Silander, J.A., Pacala, S.W., 1994. Seedling recruit-

ment in forests: calibrating models to predict patterns of tree

seedling dispersion. Ecology 75, 1794±1806.

Runkle, J.R., Yetter, T.C., 1987. Treefalls revisited: gap dynamics

in the southern Appalachians. Ecology 68, 417±424.

Shugart, H.H., 1984. Forest Dynamics. Springer, New York, 278

pp.

Sokal, R.R., Rohlf, J.F., 1981. Biometry. W. H. Freeman, New

York, 859 pp.

Streng, D.R., Glitzenstein, J.S., Harcombe, P.A., 1989. Woody

Seedling Dynamics in an East Texas floodplain Forest. Ecol.

Monogr. 59, pp. 177±204.

Szewczyk, J., Szwagrzyk, J., 1996. Tree regeneration on

rotten wood and on soil in old-growth stand. Vegetatio 122,

37±46.

Szwagrzyk, J., 1990. Natural regeneration of forest related to the

spatial structure of trees: A study of two forest communities in

Western Carpathians, southern Poland. Vegetatio 89, 11±22.


Szwagrzyk, J., 1992. Small-scale spatial patterns of trees in a

mixed Pinus sylvestris±Fagus sylvatica forest. For. Ecol.

Manage. 51, 301±315.

Takyu, M., Ohsawa, M., 1997. Distribution and regeneration

strategies of major canopy dominants in species-rich subtropi-

cal/warm temperate rainforests in south-western Japan. Ecol.

Res. 12, 139±151.

Tucker, G.F., Hinckley, T.M., Leverenz, J., Jiang, S., 1987.

Adjustment of foliar morphology in the acclimation of

understory Pacific silver fir following clearcutting. For. Ecol.

Manage. 21, 249±268.

Washitani, I., Tang, Y., 1991. Microsite variation in light

availability and seedling growth of Quercus serrata in

a temperate pine forest. Ecol. Res. 6, 305±

316.

Welander, N.T., Ottosson, B., 1998. The influence of shading

on growth and morphology in seedlings of Quercus robur L.

and Fagus sylvatica L. For. Ecol. Manage. 107, 117±

126.

Woods, K.D., 1984. Patterns of tree replacement: canopy effects on

understory pattern in hemlock-northern hardwood forests.

Vegetatio 56, 87±107.


Dynamics of seedling banks in beech forest: results of a 10-year study on germination, growth and...

Documents

Transcript of Dynamics of seedling banks in beech forest: results of a 10-year study on germination, growth and...