Embed Size (px)
Citation preview
Soil seed bank dynamics in hay®eld succession
RENEÂ E M. BEKKER, GEURT L. VERWEIJ, JAN P. BAKKER and
LATZI F. M. FRESCO
Laboratory of Plant Ecology, University of Groningen, P. O. Box, 14 A. A. Haren 9750, the Netherlands
Summary
1 Changes in the species composition of the soil seed bank were determined in a
dry and a more species-rich wet chronosequence. Each sequence represented a 25-
year hay®eld succession following cessation of fertilizer application in the Drentse
A Nature Reserve (NL), where the vegetation has been studied since 1972.
2 The number of seeds of many late successional species showed a signi®cant
increase during succession with only two characteristic late species present in the
seed bank of the early stage of each series. Most of the early successional species
showed a decrease in the number of seeds, which paralleled their relative frequency
within the vegetation. Overall, seed density and species diversity of the seed bank
was higher in the wet than the dry chronosequence.
3 Mean values for seed longevity were calculated for each successional phase in
each series using a published seed bank data base. When based simply on the pre-
sence of species, the seed longevity index decreased signi®cantly during the wet-ser-
ies succession in both surface and deeper seed banks and in the vegetation. When
based on the relative frequency of species present, the index decreased signi®cantly
in both series but only in the surface seed bank and the vegetation.
4 Comparison with data for an ancient undisturbed wet hay meadow in England
suggests that seed longevity of hay®eld species is generally low. Similarity between
seed bank and established vegetation was low in both the undisturbed British mea-
dow (only 47%) and in the relatively young Dutch study sites (c. 50%).
5 The soil seed bank is unlikely to determine hay®eld succession in the Drentse A
Nature Reserve, since the composition of the soil seed bank tended to follow that
of the above-ground vegetation. Increases in plant species richness following the
cessation of fertilizer application, the main goal of restoration management, there-
fore depend to a large extent on an in¯ux of the seeds of most species from outside
the site.
Key-words: chronosequence, Junco-Molinion, Nardo-Galion, species-rich grassland,
seed longevity
Journal of Ecology (2000) 88, 594±607
Introduction
Nature conservationists often manipulate succession
in grassland ecosystems to increase plant species
diversity. To this end, low intensity management of
former agricultural grasslands has, in many cases,
been successful (Van Altena & Van Minderhoud
1972; Grime 1979; Symonides 1986; Bakker 1989;
Hutchings & Booth 1996; Oomes et al. 1996; Bekker
et al. 1997). It is often suggested that some of the
(re)colonizing species establish from the soil seed
bank, where they exist as a relict from the highly
diverse communities that were present at the site
before intensi®cation of land use. Much research,
however, suggests that seed longevity of grassland
plant species is low (Rice 1989; Milberg 1995;
Thompson et al. 1997; Bekker et al. 1998), thus
arguing against the seed bank as an important fac-
tor in secondary succession within these commu-
nities (Van Andel et al. 1993).
The relation between seed banks and successional
series has been studied in woodlands (Livingston &
Allessio 1968; Hill & Stevens 1981; GranstroÈ m 1982;
Koniak & Everett 1982; Pickett & McDonnell 1989)
old ®elds and forests (Oosting & Humphrey 1940;Correspondence: Rene e Bekker (fax �31 50 3632273; e-
mail [email protected]).
Journal of
Ecology 2000,
88, 594±607
# 2000 British
Ecological Society
Symonides 1986; Roberts & Vankat 1991), heath-
land (GranstroÈ m 1988; Hester et al. 1991) and
Mediterranean pastures (Levassor et al. 1990).
However, the majority of these studies focus on
long-term successions where there are large di�er-
ences in plant communities between the stages (as in
a dune succession from bare sand to forest) and lack
detailed information on the relation between the
established vegetation and the seed bank.
Detailed repeated studies on seed bank develop-
ment in a single area are very rare (Leck & Leck
1998; Willems & Bik 1998; Falinska 1999).
Moreover, community processes, such as species
replacement, speed of colonization and accumula-
tion of seeds, are di�cult to study in seed banks.
The availability of a well studied grassland succes-
sion and a complementary chronosequence gave us
the opportunity to study species dynamics in the
seed bank in more detail.
Since its establishment in 1965, the Drentse A
Nature Reserve (NL) has aimed to return intensively
used agricultural grassland to species-rich hay®elds
by elimination of fertilization. Soil nutrient avail-
ability and peak standing crop has decreased and
changes in canopy structure and species composition
could be detected that varied with soil moisture
(Willems 1983; Bakker 1989; Ol� & Bakker 1991;
Pegtel et al. 1996). It takes about 5±10 years of
impoverishment by cutting and removal of the hay
for su�cient change to occur to allow new species
to become established in the sward. The target is to
(re)establish Nardo-Galion communities at the drier
sites (although not yet restored, these were present
over a large area at the beginning of the century)
and Junco-Molinion communities at the wetter sites
(a community resembling this is developing at the
oldest successional site) (alliances according to
Schamine e et al. 1996). Most of the target species,
such as Succisa pratensis and Nardus stricta for the
dry series, are known to have been present before
the intensi®cation of land use 20±50 years ago
(Grootjans 1980). Although the fragmented land-
scape outside of the reserve provides few seed
sources for re-establishment of these species, a sig-
ni®cant rise in species number still occurred during
the ®rst 25 years of management. It is important to
know whether restoration requires only the pre-
viously accumulated seed bank to permit re-estab-
lishment of the plant communities, or whether
succession depends upon input via seed dispersal.
The aim of this study was to determine the impor-
tance of the seed bank and its dynamics in dry and
wet areas within this well described successional
sequence. We asked whether the composition of the
seed bank in the early stage of succession contri-
butes to the above-ground replacement of species
and if there are any generalizations that can be
made regarding seed bank strategies or longevity of
hay meadow species through time. We also com-
pared our secondary succession with an ancient,
well developed, undisturbed hay®eld.
Materials and methods
STUDY AREAS
The study areas are situated at the Drentse A
Nature Reserve, the Netherlands (53�N, 6�420 E). Aset of ®elds along the AnloeÈ rdiepje brook valley
have been acquired by the State Forestry
Department individually over a period of 30 years.
These sites therefore di�er in `age' and soil fertility
due to the di�erent dates at which fertilizer applica-
tion ceased and the original hay-cutting regime (cut
once a year at the end of July) was resumed (Bakker
1989), and comprise a chronosequence representing
a successional series of soil impoverishment in a wet
and a dry area. The dry sequence on sandy soil, situ-
ated on the edge of the valley, consisted of four
®elds managed for 7, 15, 20 or 26 years. The wet
sequence situated on peaty soil adjacent to the
brook, had four ®elds where the hay cutting was
resumed 7, 15, 20 and 25 years ago. None of the
®elds was grazed. In both series, the youngest most
nutrient enriched ®eld was designated site A, with
sites B, C and D progressively older and more impo-
verished. The vegetation development at the 20-
year-old sites (C) has been studied by Bakker & Ol�
(1995) and comparison with data from permanent
quadrats at these sites was used to con®rm the suc-
cessional age of the other sites and thus validate the
chronosequence.
Within the dry series, the vegetation ranged from
a Holcus lanatus dominated community to a
Agrostis capillaris-Luzula campestris community
(nomenclature of plant species follows Van der
Meijden 1990). The wet series ranged from a PooÈ-
Lolietum to a Juncus acuti¯orus dominated commu-
nity, both representing retrograde successions in
response to impoverishment. Soil fertility has now
been restored to values typical of the hay®elds at the
beginning of this century before the application of
both arti®cial fertilizer and large amounts of cattle
manure had started. However, the species composi-
tion in each series has not yet returned to that of the
target communities and is still changing.
Previous research has shown that, in addition to
di�ering soil type, species composition and location
relative to the brook, the wet and the dry series dif-
fered in the type and extent of macro-nutrient lim-
itation (Ol� & Pegtel 1994; Pegtel et al. 1996).
Indicator values for soil moisture and soil nutrient
levels for individual plant species in our vegetation
were obtained from Kruijne et al. 1967. These indi-
cator values, like those of Ellenberg, are often used
to derive a mean value over all species present in
each releve , which gives an indication of soil moist-
595Bekker et al.
# 2000 British
Ecological Society
Journal of Ecology,
88, 594±607
ure and soil fertility at that location (see also
Melman et al. 1988 and Meerts 1997).
The undisturbed hay meadow used for compari-
son, Oxey Mead, is an ancient ¯ood plain meadow
beside the river Thames, north-west of Oxford
(UK). Exploitation practices have not changed since
the 13th century, and the ®eld, never arti®cially fer-
tilized, contains an Alopecurus pratensis±Sanguisorba
o�cinalis association. It provides a stable baseline
with which the seed bank and the established vegeta-
tion of our wet sequence can be compared. All data
for Oxey Mead are derived from McDonald et al.
1996.
SAMPLING
Seed bank samples were collected in March 1993 to
allow natural strati®cation to have taken place over
the winter. Ten 5� 5m quadrats were laid out in an
area of homogeneous vegetation in the middle of
each of the eight sites. Ten soil cores (diameter 4
cm) were taken from each quadrat and subdivided
into two layers: 0±5 cm and 5±10 cm. The total area
sampled at each site was 0.125m2.
The samples were treated according to the seed
bank sampling method of Ter Heerdt et al. (1996).
Seeds were concentrated by washing the soil over a
®ne sieve (mesh width 0.212mm) before being
spread out in a very thin layer (less than 3mm) on
trays ®lled with sterile potting soil topped with a
thin layer of sterilized white sand and allowed to
germinate in a glasshouse for 12 weeks. The germi-
nation regime consisted of a 12-h photoperiod with
night and day temperatures of 15/25 �C and daily
watering.
When there was no further emergence and all
seedlings had been identi®ed, counted and removed,
the samples were recollected from the trays, dried
and stored cold (5 �C) and dark until sorted for the
remaining seeds.
Hand-sorting of the seeds under a binocular
microscope revealed those that were viable (i.e.
those with a healthy appearance that were ®rm
when pressed against a hard surface); these viable
seeds belonged to only four taxa. In total, these
seeds amounted to only 3.5% of the number that
had germinated and three of the species, Juncus
spp., Holcus lanatus and Rumex spp., had already
germinated in large numbers. Only for Trifolium
spp. were more viable seeds found through sorting
than through germination. This is most likely caused
by enforced dormancy due to a hard seed coat that
had not been completely broken by strati®cation
and the washing pretreatment. Overall, germination
was a very e�ective method for assessing viable seed
numbers in the soil: due to their negligible number,
seeds found by sorting were excluded from subse-
quent analyses.
The same quadrats were reused for vegetation
analysis in June 1994. Quadrats were divided into 10
subplots of 2.5� 1m and plant species present in
each subplot were noted; this gave a total of 100
vegetation recordings per site.
DATA ANALYSIS
A total of 102 species were present in both the seed
bank and the established vegetation. Our germina-
tion method, however, did not provide reliable
information on taxa such as orchids that produce
spores or very small seeds that are di�cult to germi-
nate. Consequently, such taxa were excluded from
the data set. A few species that were very di�cult to
identify at the seedling stage were pooled into spe-
cies groups for both vegetation and seed bank ana-
lysis. These were, Agrostis spp., Betula spp.,
Callitriche spp., Carex spp., Epilobium spp.,
Ranunculus repens�R. acris, Rubus spp. Salix spp.,
Taraxacum agg. and Juncus bufonius (including the
taxa J. bufonius, J. e�usus and J. conglomeratus).
The last group was excluded from most analyses
because of its heterogeneity, but it was included as a
single species in the analysis of numbers of species
and individuals over the sites because it made a sig-
ni®cant contribution to the seed bank. To avoid
contamination, species occurring in the seed bank
but not in the vegetation were included only when a
total of three or more seeds were found within the
series under consideration, while species occurring
only in the vegetation were included only if their
cumulative frequency was r 5%. The total number
of species used in the analyses was 51 for the dry
series and 56 for the wet series (summarized in
Table 1; full details in Appendix 1 in the Journal of
Ecology archive on the World Wide Web; see the
cover of a recent issue of the journal for the WWW
address).
Signi®cant di�erences between the mean number
of seeds per site were tested using a one way
ANOVA and a Tukey range test. Prior to this,
homogeneity of variance was tested with a Levene's
test. If no homogeneity of variance occurred, a non-
parametric Kruskal±Wallis test was used instead of
the ANOVA, and contrasts were calculated with a
Student Newman Keuls test (Zar 1984).
To detect successional trends in seed bank devel-
opment, the quantitative seed bank data for the dif-
ferent soil layers were analysed separately using
Detrended Correspondence Analysis (DCA) with
the software package CANOCO (Ter Braak 1988).
The vegetation of the eight sites was analysed by
Canonical Correspondence Analysis (CCA). The
environmental factors used were indicator values for
nitrate, potassium and phosphorus derived from
Kruijne et al. (1967), available for nearly all species
present in the vegetation. The program SPECT in
the software package VEGROW (Fresco 1991) was
596Seed bank
dynamics
# 2000 British
Ecological Society
Journal of Ecology,
88, 594±607
used to obtain an average value per releve , taking
account of the presence or absence of individual spe-
cies.
Logistic response curves were ®tted where species
had enough seeds (seven and eight for the dry and
wet successional series, respectively). The program
CURVE (VEGROW package Fresco 1991) was used
to generate curves for the 0±5 cm seed bank, the 5±
10 cm seed bank and vegetation for each series. The
abundance of species in the vegetation is expressed
as the mean of their relative frequency over all
releve at a site, whereas in the seed bank we used
the total number of germinated seeds per site stan-
dardized relative to the maximum number of seeds
of that species observed in any of the 40 quadrats in
that series.
To investigate trends in seed longevity during the
succession, we analysed the recently published seed
bank data base of Thompson et al. (1997) and
counted the number of transient, short-term and
long-term persistent records for each of the species
we found in the seed bank to calculate the longevity
index.
At least ®ve records are needed to calculate a seed
longevity index for a species according Bekker et al.
(1998) and thus to enable a con®dent identi®cation
of the seed bank type. For each species which ful-
®lled this criterion, we followed the method of
Thompson et al. (1998) and Bekker et al. (1998b)
and estimated the proportion of the total number of
transient and persistent records for the species that
were persistent (short- plus long-term records).
This index could be compared with the presence
(a qualitative description of the species composition)
and the abundance (a quantitative description of the
species composition) of species in both seed bank
layers. The resulting estimates of the qualitative and
quantitative weights of seed longevity for each quad-
rat of each site could be tested for di�erences
between means, as it could for di�erences in seed
numbers.
Results
CHRONOSEQUENCES REPRESENTING
SUCCESSION
The indicator values of the individual species con-
®rm that the established vegetation in the two series
is characteristic of di�erent moisture regimes. This
main factor (the `moisture' vector in Fig. 1a) clearly
separates the wet and dry chronosequences on the
®rst axis of the canonical correspondence analysis
(Fig. 1a). The second axis represents di�erences in
soil nutrient richness, and therefore di�erences in
biomass production. Each series separately shows
that increasing age of the ®elds (the `time' vector in
Fig. 1) correlates with decreasing levels of nitrogen,
potassium and phosphorus. Altogether, 70% of the
variance in the data set was explained by the ®rst
two axes of the analysis, which comprised four fac-
tors.
The CCA also enables a positioning of the species
present in the two successional series (Fig. 1b), and
demonstrates their subdivision into four vegetation
groups. The ®rst axis divides late and early succes-
sional species and the second forms the border
between the wet and dry series. Each grassland spe-
cies could then be allocated to an early (E) or late
(L) successional group. The few extra species that
occurred only in the soil seed bank were allocated
manually and all woody taxa and ruderal species of
ditches, hedgerows or arable habitats (beyond the
main focus of this study) were designated R (the
`rest' group; see Table 1).
SPECIES
It is remarkable that hardly any late successional
species were found in the seed bank of the early
stages of either succession. Of the species character-
istic of the `target' communities, only Luzula cam-
pestris and Calluna vulgaris seeds were present at
younger sites in the dry series and only those of
Juncus acuti¯orus and Carex spp. were present in the
wet series (Table 1).
Many late successional species show a signi®cant
increase in the number of seeds during succession
while most of the early successional species show a
peak or early decrease in the number of seeds that
parallels their frequency in the established vegeta-
tion. In both series, `rest' species, such as Urtica
dioica and Betula spp., occur with very low frequen-
cies in the vegetation but vary widely in seed abun-
dance (Table 1). Although the two series contained
fairly similar total numbers of species, many more
showed signi®cant di�erences in mean seed numbers
between the four stages at both soil depths in the
wet than in the dry series (32 vs.15) (for statistics of
individual species see Appendix 1, WWW).
Figure 2 shows the performance during the
course of the succession of the species for which suf-
®cient seed was present to allow analysis. Of the
early successional species in the dry series, Holcus
lanatus and Rumex acetosa had high frequencies in
the vegetation for all sites but vegetation coverage
decreased with time (not shown), whereas their
abundance in the seed bank declined signi®cantly.
Calluna vulgaris, one of the two species present in
the target community for this dry series, was found
only in the deeper soil layer and was absent from
the vegetation. Although the late successional spe-
cies, such as Anthoxanthum odouratum and Carex
spp., showed a clear increase in the vegetation, their
seed bank patterns varied. A. odouratum, for exam-
ple, was not found in the deeper soil layer even after
25 years of succession. The ruderal species Urtica
dioica has a typical persistent seed bank pattern and
597Bekker et al.
# 2000 British
Ecological Society
Journal of Ecology,
88, 594±607
was present in the seed bank at all sites but did not
occur in the vegetation. Rumex obtusifolius can be
considered to be a local guest and is most likely
expanding from the ®eld edge where it was common.
This species shows peaks in the vegetation and
within both seed bank layers at the same single site.
In the wet series, one of the early successional spe-
cies, Agrostis spp., showed initially high abundances
in the seed bank, followed by a decline that paral-
leled its frequency of occurrence within the vegeta-
tion. Another early species, Holcus lanatus, showed
similar seed bank patterns, but with no decrease in
vegetation frequency. Percentage cover of H. lanatus
decreased signi®cantly, as it was also observed to do
in the dry series (data not shown) where seed bank
changes were less obvious. The late successional spe-
cies (Juncus acuti¯orus, Anthoxanthum odouratum
and Caltha palustris) showed increasing relative fre-
quency within the vegetation, paralleled by an
increase in seed abundance in both seed bank layers.
A. odouratum, like H. lanatus, occurred in both ser-
ies but the patterns for this species were very similar
under wet and dry conditions. Glyceria ¯uitans,
although not of great importance within the vegeta-
tion, showed a peak in seed abundance at one site.
Gnaphalium uliginosum, a ruderal species, did not
occur in the vegetation at all.
The mean number of species in the seed bank rose
and then dropped signi®cantly during the succession
with a maximum at site B (15 years of restoration
management) in both layers of both series (Table 2).
The surface layer of the dry series contained more
species than the deeper layer, whereas the wet
sequence showed no di�erences between layers. The
number of species in the wet series was, however,
higher than in the dry sequence. In the dry series,
the number of individuals also showed a maximum
at site B in both layers if the exceptionally high
value for the surface layer of site D (due mainly to
many Juncus bufonius seeds) is disregarded. In the
wet series, both seed bank layers showed a maxi-
mum of individuals at site C (20 years). Many more
Fig. 1 The ®rst two axes from a canonical correspondence analysis. (a) Positions of the vegetation releve s in the two suc-
cessional series and their relationship to the important habitat variables based on indicator values and shown as vectors.
Sites A to D represent a gradient of increasing successional age and decreasing nutrient status. (b) Ordination of species fre-
quencies showing groupings of early and late successional species in both dry and wet chronosequences. EV, eigenvalue.
Abbreviations and full species names are given in Table 1.
598Seed bank
dynamics
# 2000 British
Ecological Society
Journal of Ecology,
88, 594±607
Table1Totalseed
numbersandvegetationfrequency
ofspeciespresentin
dry
andwet
series
combined
andwithin
thedry
series
only
andthewet
series
only
(!and!!indicate
target
speciesoftherespective
communities).Speciesweredesignatedascharacteristicofearly(E)orlate
(L)successionalstages
orassigned
toa`rest'group(R
)containingmainly
ruderalsandtree
species.L.I.,LongevityIndex
calcu-
latedafter
Thompsonet
al.(1997);±,data
notavailable.Speciesare
inalphabeticalorder
within
successionalgroup(E/L/R
)within
each
locationcategory
L.I.
Species
Dry
series
Wet
series
Seedbank0±10cm
Vegetationfrequency
Seedbank0±10cm
Vegetationfrequency
AB
CD
AB
CD
AB
CD
AB
CD
E0.73
Alopecurusgeniculatus(A
g)
00
00
025
01
00
00
90
20
0
E0.14
Alopecuruspratensis(A
p)
00
00
55
00
00
00
00
10
0
E0.49
Cardaminepratensis(C
pra)
00
00
12
12
00
141
126
151
134
94
100
100
100
E0.65
Cerastium
fontanum
(Cf)
20
34
90
98
56
69
3138
35
33
10
056
17
70
E0.27
Deschampsiacespitosa
(Dc)
00
00
012
00
00
34
10
15
98
0
E±
Epilobium
spp.(Esp)
14
10
10
00
29
67
053
100
3
E0.08
Festuca
pratensis(Pp)
00
00
124
20
00
10
76
95
93
50
E0.54
Glyceria¯uitans(G
f)0
00
20
11
00
156
375
1609
375
68
876
3
E0.56
Holcuslanatus(H
l)443
249
51
37
100
98
99
91
900
73
464
169
100
100
100
100
E0.2
Lolium
perenne(Lp)
00
00
90
10
00
00
45
20
0
E0.28
Phleum
pratense
03
20
00
00
40
42
20
00
0
E0.9
Poaannua(Pann)
31
117
51
00
00
49
19
12
25
00
E0.39
Poapratensis(Pp)
11
67
38
10
78
99
79
0272
362
409
253
100
98
100
99
E0.68
Ranunculusrepens(R
r)8
313
258
157
66
98
80
6860
1407
2127
487
100
100
100
100
E0
Rhinanthusangustifolius(R
ha)
00
00
51
47
27
00
00
075
100
98
97
E0.29
Rumex
acetosa
(Rua)
69
21
22
8100
99
99
87
46
57
564
100
95
100
E0.67
Rumex
obtusifolius(R
o)
022
1874
01
732
02
26
40
00
0
E0.75
Stellariamedia
(Sm)
00
00
13
51
01
57
10
00
60
1
E0.3
Taraxacum
agg.(Tagg)
10
00
100
37
57
013
00
123
53
14
45
E0.4
Trifolium
repens(Tr)
04
12
11
30
00
00
043
16
9
E0.55
Veronicaarvensis(V
a)
95
40
25
00
01
00
80
00
0
L±
Agrostisspp.(A
sp)
10
371
584
1022
55
99
100
100
1103
116
272
12
100
34
93
0
L0.45
Ajugareptans(A
r)2
03
50
00
01
11
00
01
018
L!!
0.29
Anthoxanthum
odouratum
(Ao)
02
212
172
98
100
01
43
89
097
100
100
L!!
±Carexspp.(C
sp)
299
5259
022
442
331
38
29
015
71
49
L0.14
Festuca
rubra
(Fr)
00
00
053
100
100
00
00
00
740
L!!
0.7
Juncusacuti¯orus(Ja)
07
21
31
00
020
108
436
97
1401
065
692
L0.35
Plantagolanceolata
(Pl)
01
30
960
59
00
011
96
197
100
99
L0.62
Stellariauliginosa
(Su)
74
30
00
00
30
70
891
10
14
08
L!
0.88
Callunavulgaris
90
12
00
00
01
023
015
595
R0.3
Alnusglutinosa
20
627
10
00
010
33
00
00
0
R±
Betula
spp.(Bsp)
10
18
34
130
02
26
33
33
30
02
0599Bekker et al.
# 2000 British
Ecological Society
Journal of Ecology,
88, 594±607
L.I.
Species
Dry
series
Wet
series
Seedbank0±10cm
Vegetationfrequency
Seedbank0±10cm
Vegetationfrequency
AB
CD
AB
CD
AB
CD
AB
CD
R0.91
Gnaphalium
uliginosum
21
13
00
00
10
22
41
10
00
0
R±
Juncusbufonius-group
320
7378
485
9867
069
072
2739
13935
18538
8908
21
60
84
49
R±
Rorippapalustris
00
04
00
00
311
21
00
00
R0.87
Saginaprocumbens(Sp)
00
04
00
00
171
32
70
10
0
R±
Salixspp.
22
15
10
00
013
13
00
00
00
R0.78
Urticadioica(U
d)
25
625
116
00
07
610
30
00
0
E0.21
Anthryscussylvestris(A
s)0
00
097
12
24
0
E0.33
Bromushordeaceus(Bh)
00
00
55
00
E0.2
Dactylisglomerata
(Dg)
00
00
68
12
55
0
E0.24
Galium
aparine(G
a)
00
00
012
50
E0.17
Glechomahederacea(G
h)
00
50
00
13
0
E0
Holcusmollis(H
m)
00
00
11
24
15
5
L0.32
Hypochaerisradicata
(Hr)
00
00
00
13
11
L0.35
Stellariagraminea
(Sg)
00
00
111
41
0
L!
0.37
Luzula
campestris(Lc)
10
03
10
15
85
R0.46
Galeopsistetrahit(G
t)0
01
00
07
0
R0.24
Lythrum
salicaria
07
20
00
00
R0
Quercusrobur(Q
r)0
00
011
13
838
R±
Rubusspp.(R
sp)
01
00
00
50
E±
Callitrichespp.
370
86
40
00
0
E0.16
Leontodonautumnalis(La)
00
00
010
40
E±
Lycopuseuropaeus
00
35
00
00
E0.23
Menthaaquatica
(Ma)
00
34
09
00
E0.25
Potentillaanserina(Pans)
03
00
031
00
E0.29
Veronicascutellata
00
08
00
00
L0.26
Cirsium
palustre
(Cip)
00
21
02
740
L0.02
Cynosuruscristatus(C
c)0
00
00
55
62
88
L0.11
Filipendula
ulm
aria(Fu)
00
00
011
452
L0.26
Galium
palustre
(Gp)
00
24
018
23
38
L0.12
Galium
uliginosum
(Gu)
08
00
05
03
L0.15
Myosotispalustris(M
p)
051
842
444
12
19
L0.63
Ranunculus¯ammula
(Rf)
265
32
14
00
02
L0.32
Trifolium
pratense
(Tp)
00
00
08
11
56
L!!
0.11
Calthapalustris(C
pal)
01
023
015
595
L!!
±Lotusuliginosus(Lu)
00
00
021
430
L!!
0.56
Lychnis¯os-cuculi(Lf)
09
2245
025
154
R1
Lythrum
portula
14
23
00
00
0
R0.35
Polygonum
hydropiper
00
13
10
00
0
Totalnumber
ofspecies
21
25
28
22
27
29
29
16
30
34
37
38
16
40
31
32
Totalnumber
ofindividuals
1003
8742
3482
11562
6665
17408
25035
12360
individuals as well as more species were seen in the
wet series and this can only partly be explained by
the greater density of Juncus spp.
SEED BANK DEVELOPMENT
Detrended Correspondence Analysis of the quantita-
tive seed bank data (seed abundance) for the surface
soil layer of the dry series showed a clear succes-
sional trend from sites A to D relative to the ®rst
two axes (Fig. 3a). The anomalous position of site C
was due to the occurrence of several atypical species
in its seed bank (e.g. Glechoma hederacea, Galeopsis
tetrahit and high abundances of Rumex obtusifolius).
A similar separation of the sites holds for the species
composition of the deeper soil layer (Fig. 3b). In the
Fig. 2 Logistic curves of the performance of early (E) and late (L) successional species represented in the vegetation and in
both seed bank layers (0±5 cm and 5±10 cm) of the four stages in the two successional series, supplemented with a few spe-
cies from the `rest' group (R). Seed abundance was standardized to the species maximum found in one quadrat of a series
(in parentheses). Curves were statistically signi®cant (P<0.05) when species were present in a layer, except for Holcus lana-
tus (5±10 cm) and Glyceria ¯uitans (vegetation) as shown by the horizontal line.
601Bekker et al.
# 2000 British
Ecological Society
Journal of Ecology,
88, 594±607
wet series (Fig. 4a, b) the successional sequence was
more clearly seen in the surface layer, although sites
B and C did not show a clear separation along
either axis. In the deeper soil layer, the four sites
form clearly distinct groups but their positions are
not related to successional age. The eigenvalues of
the axes were smaller in the wet series than in the
dry series, indicating that the di�erences between
Fig. 3 Ordination of seed bank data relative to the ®rst
two axes of a detrended correspondence analysis of the
four sites of the dry series. (a) 0±5 cm and (b) 5±10 cm.
Symbols for sites are as in Fig. 1. EV, eigenvalue.
Table 2 Species and individuals (x-�SE) in seed banks of the dry and wet chronosequences. Di�erent symbols within a row
indicate signi®cantly di�erent means using a one-way ANOVA followed by a Tukey's range test or di�erences in mean
ranks using a Kruskal±Wallis test (npar) followed by a Student Newman Keuls test. Sites A to D represent a gradient of
increasing successional age and decreasing nutrient status
Signi®cance A B C D
Mean number of species
Dry series 0±5 cm P<0.001 (npar) 8.3a�0.8 12.5b�0.9 11.7b�1.0 9.4a�0.9
Dry series 5±10 cm P<0.01 6.1a�0.9 8.9b�0.8 8.2b�0.9 6.1a�0.6
Wet series 0±5 cm P<0.01 13.5a�1.1 17.3c�1.2 16.1bc�0.8 14.0ab�1.2
Wet series 5±10 cm P<0.05 13.3a�1.6 17.2b�0.9 16.0ab�1.1 13.9a�1.5
Mean number of individuals
Dry series 0±5 cm P<0.001 68.7a�13.3 583.3bc�135.7 189.9ab�28.8 984.0c�218.6
Dry series 5±10 cm P<0.001 31.6a�6.3 285.9c�21.7 158.3b�27.0 172.2b�38.0
Wet series 0±5 cm P<0.001 380.3a�62.5 1006.9b�115.5 1344.7c�138.2 566.3a�93.5
Wet series 5±10 cm P<0.001 286.2a�30.1 737.5b�43.6 1092.7c�97.7 669.7b�62.9
Fig. 4 Ordination of seed bank data relative to the ®rst
two axes of a detrended correspondence analysis of the
four sites of the wet series. (a) 0±5 cm and (b) 5±10 cm.
Symbols for sites are as in Fig. 1. EV, eigenvalue.
602Seed bank
dynamics
# 2000 British
Ecological Society
Journal of Ecology,
88, 594±607
the four sites were smaller. This pattern is similar to
that observed for the vegetation communities, where
the ®rst and last sites (A and D) also di�ered more
in the dry than in the wet series (see also Fig. 1a).
SEED LONGEVITY
The analyses of the average seed longevity index,
based only on species present in the seed bank for
which this could be calculated (Table 3), showed
that there were no signi®cant di�erences through
time in the dry series, whereas in the wet series the
mean seed longevity index decreased with increasing
successional age at both soil depths. When calcu-
lated for species present in the vegetation, the long-
evity index decreased signi®cantly for both series as
the stage of succession and species-richness
increased. It is clear, however, that basing the analy-
sis on species present in the vegetation gives a far
lower value for the mean index than analysis of
either seed bank layer.
The frequency-adjusted analyses of mean seed
longevity indices revealed signi®cant increases with
age from sites A to B in both series, after which the
index remained constant (dry sites) or fell (wet
sites). The deeper soil layer did not show signi®cant
trends in either series. The established vegetation,
however, showed a signi®cant decrease through the
succession at both series (Table 4). Values for the
mean seed longevity index were never found to di�er
signi®cantly between the two series, regardless of
whether they were adjusted for species frequency.
Data from an undisturbed wet hay meadow
(Oxey Mead, Table 5), suggest that both unadjusted
and adjusted indices are considerably lower at Oxey
Mead than in our wet chronosequence.
RELATIONSHIP BETWEEN SEED BANK AND
VEGETATION
The composition of the vegetation was relatively
similar to the total seed bank (0±10 cm). Similarity
indices of c. 50% for all sites (Sùrensen 1948; Table
6). Although site B of the wet series had the highest
similarity, values tended to increase slowly with suc-
cession age. The higher value was probably
explained by seed input from the disturbed edges,
leading to greater abundance in the seed bank of
Table 4 Mean seed longevity index (�SE) of species in the seed bank and the vegetation across the dry and wet succes-
sional series, weighted by species relative frequencies in each layer. See also Table 3
Stages in the chronosequence
Signi®cance A (7 years) B (15 years) C (20 years) D (25/26 years)
Dry series
Seed bank 0±5 cm P<0.001 (npar) 0.53a (�0.01) 0.61b (�0.01) 0.64b (�0.01) 0.60b (�0.02)
Seed bank 5±10 cm NS 0.65 (�0.03) 0.67 (�0.02) 0.67 (�0.00) 0.65 (�0.01)
Vegetation frequency P<0.001 0.37b (�0.00) 0.38b (�0.01) 0.36b(�0.01) 0.32a (�0.01)
Wet series
Seed bank 0±5 cm P<0.001 0.58b (�0.00) 0.62c(�0.01) 0.57b (�0.01) 0.54a (�0.01)
Seed bank 5±10 cm NS 0.59 (�0.01) 0.60 (�0.01) 0.60 (�0.00) 0.59 (�0.01)
Vegetation frequency P<0.001 (npar) 0.43b (�0.02) 0.36a (�0.00) 0.34a (�0.00) 0.34a (�0.00)
Table 3 Mean seed longevity index (�SE) of species in the seed bank and vegetation across the dry and wet successional
series; index calculated according to Bekker et al. (1998) for each species with more than ®ve records in Thompson et al.
(1997). All species counts are equal. Di�ering letters within a row indicate signi®cant di�erences using a one-way ANOVA
followed by a Tukey's range test or di�erences of mean ranks using a Kruskal±Wallis test (npar) followed by a Student
Newman Keuls test. NS � no signi®cant di�erences
Stages in the chronosequence
Signi®cance A (7 years) B (15 years) C (20 years) D (25/26 years)
Dry series
Seed bank 0±5 cm NS 0.51 (�0.02) 0.56 (�0.02) 0.53 (�0.02) 0.54 (�0.02)
Seed bank 5±10 cm NS 0.63 (�0.03) 0.63 (�0.02) 0.61 (�0.02) 0.63 (�0.02)
Vegetation frequency P<0.05 (npar) 0.37b (�0.01) 0.35ab (�0.01) 0.34a (�0.01) 0.31a (�0.01)
Wet series
Seed bank 0±5 cm P<0.001 0.55cb (�0.01) 0.59c(�0.01) 0.53ab (�0.02) 0.48a (�0.01)
Seed bank 5±10 cm P<0.001 0.60c (�0.01) 0.61c (�0.01) 0.56b (�0.01) 0.49a (�0.01)
Vegetation frequency P<0.001 (npar) 0.42c (�0.02) 0.36b (�0.01) 0.32a (�0.00) 0.34ab (�0.00)
603Bekker et al.
# 2000 British
Ecological Society
Journal of Ecology,
88, 594±607
species which appear sparsely in the vegetation. The
Sùrensen index for Oxey Mead (Table 5) falls within
the range of similarities that we found in the wet
series. This similarity (47% between seed bank and
vegetation) was lower than expected for a site with
long-term stable management and low disturbance
intensity.
Discussion
The seed bank dynamics of the grasslands studied
are mainly governed by input from the established
vegetation with unidirectional trends in species
replacement in both wet and dry series. The deeper
soil layer is, however, not expected to contribute sig-
ni®cantly to species replacement in the above-
ground vegetation. The longevity of the species in
the seed bank declines with successional time in
most analyses, and even the lower levels in the dry
series are still higher than in an ancient meadow
where succession has continued for centuries.
SEED BANK COMPOSITION AND
SUCCESSION
The number of species in the seed bank often
decreases during secondary succession, e.g. from old
®elds to deciduous forest (Roberts & Vankat 1991),
from grazed calcareous grassland to Juniper scrub
(Bakker et al. 1996) and in temperate deciduous for-
ests (Pickett & McDonnell 1989). This is usually
associated with a decline in the density of seeds. The
succession from fertilized grassland to semi-natural
grassland showed similar patterns with both species
richness and density of the seed bank decreasing sig-
ni®cantly after having reached a maximum at inter-
mediate sites of both series. In contrast, Milberg
(1995) found no decrease in seed numbers and seed
density in grassland succession following cessation
of grazing. This was most likely due to the e�ect of
grazing animals manipulating seed input and seed
incorporation into the soil in the early stages of the
succession. Conclusions from studies on changes in
seed banks and vegetation in chronosequences
depend on the assumption that history, soil condi-
tions and availability of propagules are similar at all
sites (Pickett & McDonnell 1989; Glenn-Lewin &
Van der Maarel 1992), and the results of this study,
where site management and vegetation development
are very well known, support the use of this
method.
LONGEVITY OF SEEDS DURING
SUCCESSION
According to the seed bank classi®cation of
Thompson (1993) and Thompson et al. (1997), most
of the dry and wet hay-meadow species observed in
this study have a transient or short-term persistent
seed bank. According to our depth distribution
data, only Agrostis spp., Ranunculus repens,
Cardamine pratensis, Poa annua, Callitriche spp.,
Juncus acuti¯orus, Lychnis ¯os-cuculi, Myosotis
palustris, Stellaria uliginosa, and Gnaphalium uligino-
sum could be classi®ed as having a long-term persis-
tent seed bank. The non-grassland `rest' (R) group
Table 6 Sùrensen similarity indices between the established vegetation and the seed bank (0±10 cm) in each site
Stages in the chronosequence
A (7 years) B (15 years) C (20 years) D (25/26 years)
Index for dry series (%) 44 46 43 50
Index for wet series (%) 40 62 40 59
Table 5 Characteristics of Oxey Mead, an ancient ¯ood-meadow along the River Thames (UK). Its management has not
been changed since the 13th century and is therefore an example of an undisturbed species-rich hay meadow (data after
McDonald et al. (1996), indices calculated as in Tables 3 & 4
Total number of species in the vegetation 55
Total number of species in the seed bank 0±10 cm 32
Sùrensen similarity index between vegetation and seed bank 47%
All species count equally Weighted after relative frequency
Seed longevity index of the seed bank 0±5 cm 0.36 0.40
Seed longevity index of the seed bank 5±10 cm 0.38 0.41
604Seed bank
dynamics
# 2000 British
Ecological Society
Journal of Ecology,
88, 594±607
contains species with a mix of strategies. It includes
tree species known to have a transient seed bank,
such as the specialized wind dispersers Betula spp.
and Salix spp., as well as Alnus glutinosa and
Quercus robur. Ruderal herbs, the majority of which
have a long-term persistent seed bank, are also
included and typically show low vegetation frequen-
cies and hence low input into the soil seed bank
(Table 1).
Long-lived seeds would be expected to accumulate
in high numbers during succession but the number
of ruderal and pioneer species decreased signi®cantly
over time at both series at both soil depths (see also
Bekker et al. 1997). However, the input of these
long-lived seeds stopped when restoration manage-
ment began. They therefore also disappeared from
the seed bank and were replaced by a few late suc-
cessional species, such as Carex spp. and Juncus acu-
ti¯orus, that produce many long-lived seeds. There
is evidence that grassland species, which are mainly
perennial, have not generally been exposed to evolu-
tionary selection towards persistent seeds: vegetative
propagation throughout a long life-span appears to
be a successful survival strategy in relatively stable
grassland habitats (such as Oxey Mead). Late suc-
cessional species tend to exhibit little dormancy and
to germinate readily in the open sward of later suc-
cessional phases (Ol� et al. 1994). Juncus acuti¯orus
might be exceptional in that its success involves
being able to spread e�ectively in space and time,
both vegetatively and generatively.
The di�erences in mean longevity between the
two series could be associated with the di�erences in
soil type and moisture content. It has recently been
shown that seed longevity may be higher under
anoxic or waterlogged conditions, especially for
those species that show optimum growth in rela-
tively wet grasslands (Bekker et al. 1998a).
RELATIONSHIP BETWEEN SEED BANK AND
VEGETATION
The poor correlation between the ¯oristic composi-
tion of the established vegetation and the seed bank
agrees with previous ®ndings (Thompson & Grime
1979; Graham & Hutchings 1988; Vira gh &
Gerencse r 1988; Russi et al. 1992), although an
ancient undisturbed calcareous grassland with a
similarity of 77% (Willems 1995) and annual-domi-
nated Mediterranean pastures that exhibited 80%
similarity (Levassor et al. 1990) are known. Because
of the low similarity (46±50%) between the vegeta-
tion and the seed bank, we propose that changes in
the seed bank of both dry and wet series follow,
rather than cause, changes in the vegetation. Only
two of the target species in each series (Calluna vul-
garis and Luzula campestris in the dry series and
Juncus acuti¯orus and a Carex sp. in the wet series)
were found in the seed bank of the youngest sites,
suggesting that the addition of species depends on
dispersal. Hay-making machinery is known to be an
important dispersal vector within the nature reserve
where all ®elds are interconnected by the annual
mowing scheme (Strykstra et al. 1996; Strykstra &
Verweij 1997). This mowing is likely to be an impor-
tant factor in the rapid and predictable succession
within the wet ®elds. The levelling o� in the number
of target species in the dry series may well be due to
the fact that species such as Succisa pratensis and
Nardus stricta are not present in either other mown
®elds within the nature reserve or in the surrounding
area. Although possible, dispersal by wind or water
into the reserve is unlikely due to the long distances
involved (Strykstra et al. 1998).
Oomes (1990) has also reported a decrease in bio-
mass production during succession similar to that
seen in our sites (Bakker 1989; Ol� & Bakker 1991;
Pegtel et al. 1996). This indicates that in both cases
sites increasingly become suitable for mesotrophic
species. Oomes (1990) found no signi®cant increase
in species number, although his sites were not con-
nected to any nearby species-rich sites through the
use of farm machinery. Vegetation succession accel-
erates under an active mowing regime (Strykstra
et al. 1996), although the development of the seed
bank may di�er due to its dependence on the time
of mowing (e.g. if late ¯owering species are mown
before seeds are shed). Juncus acuti¯orus is therefore
only present in the seed bank at a fraction of its
potential density as a large part of its seed produc-
tion is removed with the hay each year. Although
25 years of succession is associated with dramatic
changes in the soil seed bank, the importance of
seed dispersal increases in both wet and dry series as
seed longevity decreases. This study shows that
restoration is possible to a certain extent in intercon-
nected hay meadow reserves, but it also suggests
that a lack of seed sources will impede restoration if
hay meadows are isolated.
Acknowledgements
The authors would like to thank the State Forestry
Commission for their permission to sample in the
Drentse A Nature Reserve. Many thanks go to
Yzaak de Vries, Jacob Hogendorf, Sieze Nijdam
and Willem van Hal for their help and care during
the seed bank sampling, the germination period in
the greenhouse and the identi®cation of the many
seedlings. Two anonymous referees contributed sig-
ni®cantly to the improvement of the manuscript.
This study was ®nancially supported by a grant
(SLW-DWT 805.35.855) of the Netherlands
Organization of Scienti®c Research (NWO) to RMB
and of the European Community programme
(AIR3-CT920079) to GLV.
605Bekker et al.
# 2000 British
Ecological Society
Journal of Ecology,
88, 594±607
References
Bakker, J.P. (1989) Nature Management by Grazing and
Cutting. Kluwer Academic Publishers, Dordrecht, the
Netherlands.
Bakker, J.P., Bakker, E.S., Rose n, E., Verweij, G.L. &
Bekker, R.M. (1996) Soil seed bank composition along
a gradient from dry alvar grassland to Juniper scrub.
Journal of Vegetation Science, 7, 165±176.
Bakker, J.P. & Ol�, H. (1995) Nutrient dynamics during
restoration of fen meadows by hay-making without
fertilizer application. Restoration of Temperate
Wetlands (eds B.D. Wheeler, S. Shaw, W. Fojt &
R.A. Robertson), pp. 143±166. Wiley, Chichester, UK.
Bekker, R.M., Oomes, M.J.M. & Bakker, J.P. (1998a) The
impact of groundwater level on soil seed bank survival.
Seed Science Research, 8, 399±404.
Bekker, R.M., Schamine e, J.H.J., Bakker, J.P. &
Thompson, K. (1998b) Seed bank characteristics of
Dutch plant communities. Acta Botanica Neerlandica,
47, 15±26.
Bekker, R.M., Verweij, G.L., Smith, R.E.N., Reine, R.,
Bakker, J.P. & Sneider, S. (1997) Soil seed banks in
European grasslands: does land use a�ect regeneration
perspectives? Journal of Applied Ecology, 34, 1293±
1310.
Falinska, K. (1999) Seed bank dynamics in abandoned
meadows during a 20-year period in the Bialowieza
National Park. Journal of Ecology, 87, 461±475.
Fresco, L.F.M. (1991) VEGROW (Version 4.0):
Processing of Vegetation Data. S-BEES, Haren, the
Netherlands.
Glenn-Lewin, D.C. & Van der Maarel, E. (1992) Patterns
and processes of vegetation dynamics. Plant
Succession: Theory and Prediction (eds D.C. Glenn-
Lewin, R.K. Peet & T.T. Veblen), 11±59. Chapman &
Hall, London, UK.
Graham, D.J. & Hutchings, M.J. (1988) Estimation of the
seed bank of a chalk grassland ley established on for-
mer arable land. Journal of Applied Ecology, 25, 241±
252.
GranstroÈ m, A. (1982) Seed banks in ®ve boreal forest
stands originating between 1810 and 1963. Canadian
Journal of Botany, 60, 1815±1821.
GranstroÈ m, A. (1988) Seed banks at six open and a�or-
ested heathland sites in southern Sweden. Journal of
Applied Ecology, 25, 297±306.
Grime, J.P. (1979) Plant Strategies and Vegetation
Processes. Wiley, Chichester, UK.
Grootjans, A.P. (1980) Distribution of plant communities
along rivulets in relation to hydrology and manage-
ment. Epharmonie (eds O. Wilmanns & R. TuÈ xen), pp.
143±170. Cramer, Vaduz, Liechtenstein.
Hester, A.J., Gimingham, C.H. & Miles, J. (1991)
Succession from heather moorland to birch woodland.
III. Seed availability, germination and early growth.
Journal of Ecology, 79, 329±344.
Hill, M.O. & Stevens, P.A. (1981) The density of viable
seed in soils of forest plantations in upland Britain.
Journal of Ecology, 69, 693±709.
Hutchings, M.J. & Booth, K.D. (1996) Studies on the fea-
sibility of re-creating chalk grassland vegetation on ex-
arable land. I. The potential roles of the seed bank and
the seed rain. Journal of Applied Ecology, 33, 1171±
1181.
Koniak, S. & Everett, R.L. (1982) Seed reserves in soil of
successional stages in pinyon woodlands. American
Midland Naturalist, 108, 295±303.
Kruijne, A.A., De Vries, D.M. & Mooi, H. (1967).
Bijdrage Tot de Oecologie Van de Nederlandse Grasland
Planten (with English summary). Verslagen van
Landbouwkundige Onderzoekingen 696. PUDOC,
Wageningen, the Netherlands.
Leck, M.A. & Leck, C.F. (1998) A ten-year seed bank
study of old ®eld succession in central New Jersey.
Journal of the Torrey Botanical Society, 125, 11±32.
Levassor, C., Ortega, M. & Peco, B. (1990) Seed bank
dynamics of Mediterrenean pastures subjected to
mechanical disturbance. Journal of Vegetation Science,
1, 339±344.
Livingston, R.B. & Allessio, M.L. (1968) Buried viable
seed in successional ®eld and forest stands, Harvard
Forest, Massachusetts. Journal of the Torrey Botanical
Society, 95, 58±69.
McDonald, A.W., Bakker, J.P. & Vegelin, K. (1996) Seed
bank classi®cation and its importance for the restora-
tion of species-rich ¯ood meadows. Journal of
Vegetation Science, 7, 157±164.
Meerts, P. (1997) Foliar macro-nutrient concentrations of
forest understory species in relation to Ellenberg's
indices and potential relative growth rate. Plant and
Soil, 189, 257±265.
Melman, Th.C.P., Clausman, P.H.M.A. & Udo de Haes,
H.A. (1988) The testing of three indicator systems for
trophic state in grasslands. Vegetatio, 75, 143±152.
Milberg, P. (1995) Soil seed bank after eighteen years of
succession from grassland to forest. Oikos, 72, 3±13.
Ol�, H. & Bakker, J.P. (1991) Long-term dynamics of
standing crop and species composition after the cessa-
tion of fertilizer application to mown grassland.
Journal of Applied Ecology, 28, 1040±1052.
Ol�, H. & Pegtel, D.M. (1994) Characterization of the type
and extent of nutrient limitation in grassland vegeta-
tion using a bioassay with intact sods. Plant and Soil,
163, 217±224.
Ol�, H., Pegtel, D.M., van Groenendael, J.M. & Bakker,
J.P. (1994) Germination strategies and vegetation
structure during grassland succession. Journal of
Ecology, 82, 69±77.
Oomes, M.J.M. (1990) Changes in dry matter yield during
the restoration of species-rich grasslands. Journal of
Vegetation Science, 1, 333±338.
Oomes, M.J.M., Ol�, H. & Altena, H. (1996) E�ects of
vegetation management and raising the water table on
nutrient dynamics and vegetation changes in a wet
grassland. Journal of Applied Ecology, 33, 576±588.
Oosting, H.J. & Humphrey, M.E. (1940) Buried viable
seeds in a successional series of old ®eld and forest
soils. Journal of the Torrey Botanical Society, 67, 253±
273.
Pegtel, D.M., Bakker, J.P., Verweij, G.L. & Fresco,
L.F.M. (1996) N, K and P de®ciency in chronosequen-
tial cut summer-dry grasslands on gley podzol after
cessation of fertilizer application. Plant and Soil, 178,
121±131.
Pickett, S.T.A. & McDonnell, M.J. (1989) Seed bank
dynamics in temperate deciduous forest. Ecology of
Soil Seed Banks (eds M.A. Leck, V.T. Parker &
R.L. Simpson), pp. 123±147. Academic Press, San
Diego, USA.
Rice, K.J. (1989) Impacts of seed banks on grassland com-
munity structure and population dynamics. Ecology of
Soil Seed Banks (eds M.A. Leck, V.T. Parker &
R.L. Simpson), pp. 211±230. Academic Press, San
Diego, USA.
Roberts, T.L. & Vankat, J.L. (1991) Floristics of a chrono-
sequence corresponding to old ®eld-deciduous forest
succession in southwestern Ohio. II. Seed banks.
Journal of the Torrey Botanical Society, 118, 377±384.
606Seed bank
dynamics
# 2000 British
Ecological Society
Journal of Ecology,
88, 594±607
Russi, L., Cocks, P.S. & Roberts, E.H. (1992) Seed bank
dynamics in a Mediterranean grassland. Journal of
Applied Ecology, 29, 763±771.
Schamine e, J.H.J., Stortelder, A.H.F. & Weeda, E.J.
(1996) De Vegetatie van Nederland 3.
Plantengemeenschappen van graslanden, zomen en droge
heiden. Opulus, Uppsala, Sweden, and Leiden, the
Netherlands.
Sùrensen, T. (1948) A method of establishing groups of
equal amplitude in plant sociology based on similarity
of species content. Kongelige Danske Videnskabernes
Selskab Biologiske Skrifter (Kopenhagen), 5, 1±34.
Strykstra, R.J., Bekker, R.M. & Bakker, J.P. (1998)
Assessment of dispersule availability: its practical use
in restoration management. Acta Botanica Neerlandica,
47, 45±56.
Strykstra, R.J., Bekker, R.M. & Verweij, G.L. (1996)
Establishment of Rhinanthus angustifolius in a succes-
sional hay®eld after seed dispersal by mowing machin-
ery. Acta Botanica Neerlandica, 45, 557±562.
Strykstra, R.J.G.L. & Verweij, & Bakker, J.P. (1997) Seed
dispersal by mowing machinery in a Dutch brook val-
ley system. Acta Botanica Neerlandica, 46, 387±401.
Symonides, E. (1986) Seed bank in old-®eld successional
ecosystems. Ekologia Polska, 34, 3±29.
Ter Braak, C.J.F. (1988) canoco, a FORTRAN Program
for Canonical Community Ordination by [Partial]
[Detrended] [Canonical] Correspondence Analysis,
Principal Component Analysis and Redundancy Analysis
(Version 2.1). Agricultural Mathematics Group,
Wageningen, the Netherlands.
Ter Heerdt, G.N.J., Verweij, G.L., Bekker, R.M. &
Bakker, J.P. (1996) An improved method for seed
bank analysis: seedling emergence after removing the
soil by sieving. Functional Ecology, 10, 144±151.
Thompson, K. (1993) Persistence in the soil. Methods of
Comparative Plant Ecology (eds G.A.F. Hendry &
J.P. Grime), pp. 194±196. Chapman & Hall, London,
UK.
Thompson, K., Bakker, J.P. & Bekker, R.M. (1997) Soil
Seed Banks of North West Europe: Methodology,
Density and Longevity. Cambridge University Press,
Cambridge, UK.
Thompson, K. & Grime, J.P. (1979) Seasonal variation in
the seed banks of herbaceous species in ten contrasting
habitats. Journal of Ecology, 67, 893±921.
Thomspon, K., Bakker, J.P., Bekker, R.M. & Hodgson,
J.G. (1998) Ecological correlates of seed persistence in
soil in the NW European ¯ora. Journal of Ecology, 86,
163±169.
Van Altena, S.C. & Van Minderhoud, J.W. (1972)
KeimfaÈ hige Samen van GraÈ sern und KraÈ utern in der
Narbenschicht der NiederlaÈ ndische Weiden. Z. Acker
P¯anzen B., 136, 95±109.
Van Andel, J., Bakker, J.P. & Grootjans, A.P. (1993)
Mechanisms of vegetation succession: a review of con-
cepts and perspectives. Acta Botanica Neerlandica, 42,
413±33.
Van der Meijden, R. (1990) Heukels' Flora Van Nederland.
21st edn. Wolters-Noordho�, Groningen, the
Netherlands.
Vira gh, K. & Gerencse r, L. (1988) Seed bank in the soil
and its role during secondary successions induced by
some herbicides in a perennial grassland community.
Acta Botanica Hungaria, 34, 77±122.
Willems, J.H. (1983) Species composition and above-
ground phytomass in chalk grassland with di�erent
management. Vegetatio, 52, 171±180.
Willems, J.H. (1995) Soil seed bank, seedling recruitment
and actual species composition in an old and isolated
chalk grassland site. Folia Geobotanica et
Phytotaxonomica, 30, 141±156.
Willems, J.H. & Bik, L.P.M. (1998) Restoration of high
species density in calcareous grasslands: the role of
seed rain and soil seed bank. Applied Vegetation
Science, 1, 91±100.
Zar, J.H. (1984) Biostatistical Analysis. Prentice Hall,
London, UK.
Received 29 June 1999
revision accepted 14 December 1999
607Bekker et al.
# 2000 British
Ecological Society
Journal of Ecology,
88, 594±607
