Biodiversity and Conservation 13: 2485–2509, 2004. # 2004 Kluwer Academic Publishers. Printed in the Netherlands.
Soil seed bank composition and diversity in a managed temperate deciduous forest GUILLAUME DECOCQ1,*, BERTILLE VALENTIN2, BENOIT TOUSSAINT2, FRE´DE´RIC HENDOUX2, ROBERT SAGUEZ1 and JACQUES BARDAT3 1 De´partement de Botanique, Universite´ de Picardie Jules Verne, 1 rue des Louvels, F-80037 Amiens Cedex, France; 2Centre re´gional de Phytosociologie=Conservatoire Botanique National de Bailleul, Hameau de Haendries, F-59270 Bailleul, France; 3Institut d’Ecologie et de Gestion de la Biodiversite´, Service du Patrimoine naturel, Muse´um National d’Histoire Naturelle, 57 rue Cuvier, F-75231 Paris Cedex 5, France; *Author for correspondence (e-mail:
[email protected]; fax: þ33-322827-469)
Received 9 April 2003; accepted in revised form 1 September 2003
Key words: Agestochory, Disturbance regime, Forest management, Seed bank, Seed dispersal, Spatial variation, Succession, Temperate deciduous forest Abstract. Little is known about the influence of forest management on the interaction between seed bank and aboveground vegetation. We surveyed seed banks and vegetation in 10 forest stands under similar abiotic conditions but submitted either to a coppice-with-standards treatment (n ¼ 5) or to a selective-cutting system (n ¼ 5). We analyzed species composition and diversity, community ecological profile, and distribution of taxa among different life forms, strategy, morphology and functional type categories. A total of 2085 seedlings (8296 seeds m2) germinated, corresponding to 28 species, among which Juncus effusus was the most abundant. Fifty-seven percent of the species were also recorded in the aboveground vegetation, the dominant species being Rubus fruticosus agg., but only 28% of the aboveground species were present in the seed bank. Our results suggest that (1) vernal geophytes and shade-tolerant perennials, which group most true forest species, are not incorporated in the seed bank, (2) parent plants of most seeds were present either in the stand in an earlier dynamic stage or apart from the stand and long-distance dispersed, (3) as expected, early-successional species are well represented in the seed bank, (4) forestry vehicles seem to be a major means of dispersion for stress-tolerant species normally found in forest lanes and wheel tracks. We conclude that seed banks contain species that have a potentially negative impact on the true forest flora and, thus, forest management should minimize soil disturbance and retain remnants of old-coppice woods to conserve disturbance-sensitive true forest species. Nomenclature: Lambinon et al. (1992). Abbreviations: CWS – coppice-with-standards treatment; PFT – plant functional type; SC – selectivecutting system.
Introduction Under the influence of management, most European temperate deciduous forests have undergone large changes in vegetation composition for many centuries (Arnould et al. 1997; Kirby and Watkins 1998). Forest management, particularly silviculture, is often cited as the main determinant of forest vegetation (e.g., Volpers 1989; Aude and Lawesson 1998). It can be viewed as a complex of anthropogenic
2486 disturbances with a periodicity and intensity that depend on the silvicultural system applied (e.g., Picket and White 1985). Whatever the silvicultural treatment, tree harvesting represents a major disturbance, since it is responsible for the removal of a more or less important part of the biomass. Post-harvest recovery of forest stands depends on the recruitment from diaspore banks (including seeds, spores and vegetative propagules), seed rain (either from residual vegetation on the site or from surrounding vegetation), residual vegetation not destroyed by harvesting and eventually planting of tree species. Over the last few decades, there is a growing interest in the composition of forest soil seed banks (e.g., Milberg 1995; Buckley et al. 1997; Dougall and Dodd 1997; Kalamees and Zobel 1998; Mitchell et al. 1998; Falinska 1999; Leckie et al. 2000; Bossuyt and Hermy 2001; Bossuyt et al. 2002) because they have been found to be important in forest regeneration and post-disturbance recovery (e.g., Nakagoshi 1985; Pickett and McDonnell 1989; Mladenoff 1990; Peterson and Carson 1996) and to strongly influence post-harvest species composition and diversity (Roberts 1981). Whereas vegetative propagules and transient seed banks enable certain species of the pre-harvest forest to maintain themselves, persistent seed banks may allow new species to establish in the immediate post-harvest stands (Grime 1989; Wilson et al. 1993; Brown 1998; Hyatt 1999). It is largely recognized that most typical shade-tolerant species do not form a persistent seed bank (Brown and Oosterhuis 1981; Halpern et al. 1999; Bossuyt and Hermy 2001), which results in a poor correspondence between forest vegetation and seed bank composition (Thompson and Grime 1979; Staaf et al. 1987; Beatty 1991; Warr et al. 1994; Eriksson 1995). Most seed bank species are rather early-successional species of former forest stages (i.e., species of forest edges and clearings) and ruderal species (Halpern et al. 1999; Bossuyt and Hermy 2001; Bossuyt et al. 2002), and even sometimes exotic species (Halpern et al. 1999). Since both transient and persistent seed banks are likely to be the major source of the plant community following environmental changes such as forest harvesting (Grime 1989; Wilson et al. 1993; Brown 1998; Hyatt 1999), similarity between soil seed banks and aboveground vegetation is expected to be greater in post-harvest stands. However, this hypothesis has rarely been tested. Moreover, the potential role of silviculture in influencing seed bank composition through harvesting methods requires further investigations (Qi and Scarrat 1998), particularly in temperate forests where it remains unexplored. A better understanding of soil seed bank dynamics in temperate deciduous forest will thus increase our knowledge of postharvest vegetation succession patterns. This may help to design appropriate strategies to manage forest effectively for biodiversity conservation. Within this framework, we designed a study to explore the variability of the persistent soil seed bank in forest stands under similar abiotic conditions, but submitted to two contrasting silvicultural systems. The research questions were: 1. What is the persistent seed bank density and composition in managed forest systems? 2. Are there differences in seed bank attributes between adjacent stands submitted to different silvicultural treatments?
2487 3. What is the relation between seed bank and understory vegetation? 4. How can the variations observed be explained?
Study area The study was undertaken in the ancient forest of Le Nouvion, located in northern France (508000 N, 38500 E, 180–220 m altitude), which covers ca. 4000 ha. The climate is of suboceanic type. Mean annual temperature reaches 9.1 8C. Precipitation is high (annual total of 950 mm on average), with 190 rainy days well distributed all along the year. The geological substrate mainly consists of cretaceous marls and clays (Turonian), largely covered by a thick layer of Quaternary loess. Soils are leached brown earths with a moderate internal drainage (Luvisol). The vegetation consists of a temperate deciduous forest affiliated to the Querco roboris–Carpinetum betuli Tu¨ xen 1930 (Decocq 1998). The dominant tree species in the area is oak, Quercus robur L., which is associated mainly with hornbeam (Carpinus betulus L.), ash (Fraxinus excelsior L.) and sycamore (Acer pseudoplatanus L.). This private – formerly royal – forest was managed as hornbeam Coppice-With-oak Standards (CWS) from the mid-17th to the late 20th century (Dubois 1996). At the end of the 1970s part of the forest has been converted into a selective-cutting system (SC). In SC, pre-commercial thinning treatments are conducted every 4 years (removal of almost all shrubs and unsuitable trees at 23 m3 ha1) and commercial fellings every 8 years (selective cutting of mature trees at 10 m3 ha1). Harvested products are hauled by heavy vehicles that drive through forest stands, frequently using different paths. In CWS, commercial felling usually occurs every 30 years, removing the whole coppice timber and about three quarters of the standards (i.e., from 150 to 250 m3 ha1). Harvested products are also hauled by heavy vehicles, which always use the same trails.
Methods Field sampling Ten forest stands submitted either to CWS (n ¼ 5) or to SC (n ¼ 5) were randomly selected within parts of the forest providing similar abiotic conditions, characterised by the same substrate (loess, thickness exceeding 5 m) and topographic position (plateau), all the soils being haplic luvisol according to the FAO classification. In each stand a 20 m 20 m square plot was randomly positioned. Aboveground vegetation was recorded between early May and late June 1999 by compiling a phytosociological releve´ including all vascular plant species present in each plot. Cover-abundance values were estimated in the field using the Braun– Blanquet scale. Field investigations were also conducted in the whole forest as well as in the immediate surrounding landscape, in order to evaluate the local species pool.
2488 Soil sampling was done in early June 1999 by collecting five soil cores by plot. The first one was taken at the plot center and the others at a distance of 10 m from the center toward the four cardinal points. Woody material (twigs, cones, branches) and leaf litter were removed before sampling. We used a 8-cm diameter auger, which was meticulously cleaned between two samples to avoid contamination. Each sample consisted of a 20-cm depth soil core, which was immediately bagged and labeled in the field and then transported to the laboratory.
Seedling emergence technique On arrival at the laboratory each soil core was cut into six layers (0–2, 2–5, 5–8, 8– 12, 12–15 and 15–20 cm) using a clean sharpened blade. Each individual layer was crumbled and placed in a 16 8C darkroom for 28 days to desiccate the samples and facilitate germination (Vanesse 1977). All root fragments and vegetative propagules were then removed. The residual material was placed as a ca. 1-cm thick layer superposed on a ca. 1.5-cm thick layer of sterilized potting soil in labeled plastic L15 W13 H7-cm containers for germination. Potting soil served as a moisture reservoir to facilitate germination. Ten control containers only filled with sterilized potting soil were randomly added to test for eventual contamination. Containers were transferred in a culture chamber where they were submitted to a 12-h photoperiod and a 20/16 8C (day/night) thermoperiod. All samples were kept moistened with demineralized water and treated with 0.2% KNO3 every 3 weeks to stimulate germination. After 2 months containers were temporarily placed in a darkroom and submitted to a humid cold stratification during 4 weeks to favor germination of still dormant seeds. Seedling emergence in the containers was checked weekly from July to late December 1999. Color-coded and labeled toothpicks marked new emergent taxa in each container, and the total number of individuals of each taxon was recorded weekly. Seedlings were removed from the containers as identifications were made. When necessary, seedlings identification was facilitated by transplanting individuals to be grown to maturity under greenhouse conditions. We did not take into consideration fern species since they could not be identified at the prothallus stage, but just noted for presence.
Data analysis To characterize the soil seed bank we calculated the seed density (viable seed m2 soil surface), species richness (S), Shannon diversity (H0 ), Pielou equitability (J0 ), specific contribution of the dominant species (number of seedlings of the dominant species/total number of seedlings), and proportion of ancient and interior forest species (following the list of Hermy et al. 1999). For this purpose the values obtained for the five soil cores were cumulated for each plot. Further calculations were made on presence–absence data because one species (Juncus effusus) accounted for more
2489 than 70% of the total number of viable seeds. Intra-plot similarity was calculated by averaging values of Sørensen’s similarity index between each pair of samples within a plot. Relations between these different parameters were investigated with Spearman rank correlations (p < 0.1). Differences between the two silvicultural systems were tested using the non-parametric Mann and Whitney U-test (p < 0.1). To estimate sampling efficiency we drew (i) the species richness–number of cores curve by displaying the cumulative number of species found as a function of the number of cores taken in a plot, and (ii) the species richness–soil depth curve by displaying the cumulative number of species found as a function of the depth of the cumulative soil cores taken in a plot. The similarity of species composition between the seed bank and the aboveground vegetation was assessed at each plot using Sørensen’s index. The ecological profile of both seed bank and aboveground vegetation was estimated using Ellenberg’s system for light (L), soil moisture (F), soil reaction (R) and soil nutrient (N) indicator values (Ellenberg et al. 1991). In order to make the diagrams clearer and facilitate comparisons, the nine indicator values of Ellenberg’s scale have been grouped into three (R, N) or four (L, F) classes. We also examined the distribution of taxa among (i) life forms (Raunkiaer 1934), (ii) CSR strategies, (iii) seed dispersal attributes, (iv) seed weight classes (Grime et al. 1988), (v) morphological types (Barkman 1988), and (vi) plant functional types (PFTs) as previously defined for the vegetation studied in an earlier work (Decocq et al., in press). In this earlier study 10 PFTs were derived from a multivariate analysis of a data matrix describing the 73 species of the local species pool in terms of 14 traits. These PFTs were found to be particularly relevant for evaluating functional response of vegetation to forest management. All calculations used the values of the cumulative five soil cores per plot. Differences in attributes between seed banks and aboveground vegetation were assessed using the Mann and Whitney test (p < 0.1). Relations between seed bank attributes and aboveground vegetation characteristics were explored with Spearman rank correlations (p < 0.1). Finally, to test whether between-plot variation in seed bank composition was related to between-plot variation in vegetation composition, we conducted a Mantel test on matrices of similarity among plots for the two data sets (Mantel 1967). All statistical analyses used Statview1 version 4.5 software (Sager and Rocco 1992), except for the Mantel test, which used PC-Ord1 version 3.0 software (McCune and Mefford 1997).
Results Seed bank characteristics A total of 2085 seedlings were recorded for the cumulated soil samples, of which 138 died before they could be identified, which corresponded to an overall seed density of 8296 seeds m2 and a total species richness of S ¼ 28 taxa. No germination occurred in the control containers. Seedling density was highly variable within plots, reaching a range from 30 to 171 seedlings from one core to another in
9.62.5
0.317ns
9.82.4
9.42.9
11 10 7 6 13 13 11 8 10 7
1.360.51
1.567ns
1.120.49
1.590.46
1.16 1.43 2.19 1.22 1.97 0.79 1.29 0.89 0.71 1.91
Shannon diversity (H0 )
0.4330.193
1.567ns
0.3560.169
0.5100.188
0.336 0.430 0.780 0.471 0.531 0.214 0.373 0.298 0.215 0.680
Pielou equitability (J0 )
16 26 24 31 33 14 19 21 26 14
1.681* 0.5400.116 22.46.7
2.611**
0.4500.045 18.85.1
0.2710.163
1.048ns
0.3260.188
0.2160.128
0.296 0.167 0.387 0.054 0.174 0.296 0.533 0.207 0.500 0.095
Aboveground Sørensen’s species index richness between seed bank and vegetation
0.6290.093 266.7
0.501 0.607 0.740 0.696 0.600 0.477 0.384 0.475 0.425 0.491
Intra-plot similarity of the seed bank
CWS: coppice-with-standards; SC: selective-cutting system; sd: standard deviation. z: result of the Mann and Whitney U-test between CWS and SC (ns: non significant; *0.1 > p 0.01; **0.01 > p 0.001).
69.819.6
208.5125.7
All plots
meansd
1.567ns
60.320.0
82.2 67.9 28.0 63.8 59.8 89.8 74.7 87.2 90.6 54.0
0.731ns
221.690.4
229 350 103 244 182 475 158 108 184 52
z
27 25 24 15 40–50 4 2 4 8 8
Proportion Species of Juncus richness effusus in (S) the seed bank (%)
79.315.5
meansd
CWS CWS CWS CWS CWS SC SC SC SC SC
Total number of viable seeds per plot
195.4164.2
meansd
CWS
SC
Forest stands 1 2 3 4 5 6 7 8 9 10
Silvicultural Time system since the last logging (years)
Table 1. Features of seed bank (all viable seeds per plot obtained from the cumulative five soil cores) and aboveground vegetation (all species recorded in the 400 m2 quadrat).
2490
2491 plot 6, as well as between plots (minimum: 52 viable seeds in plot 10, maximum: 475 viable seeds in plot 6). Other characteristics of the soil seed bank are reported in Table 1 for each plot. Although the difference was not significant, CWS stands tended to support a higher and less variable seed density than SC stands. H0 and J0 tended to be higher for CWS compared to SC stands while S was in the same range. We found no correlation between seedling density and either S, H0 or J0 . For 9 of the 10 stands assessed, more than 50% of the seedlings corresponded to J. effusus, which was always the dominant species in the seed bank. The other frequent species were Agrostis canina, Betula alba, Rubus idaeus and R. fruticosus agg. (Table 2). The genera Hypericum and Carex were also well represented, with a number of different species. The proportion of J. effusus in the seed bank tended to be higher in SC stands compared to CWS ones. As this proportion increased, species richness also increased (r ¼ 0.667, p ¼ 0.06) but evenness (J0 ) decreased (r ¼ 0.988, p ¼ 0.003). It is noteworthy that plot 4, which corresponded to the CWS stand with the most recent logging and coppice cutting, supported a seed bank composition very close to those of SC stands, while plot 9, which corresponded to one of the two oldest SC stands, had a soil seed bank composition close to those of CWS. Intra-plot similarity of species composition reached 0.540 on average but was significantly higher for CWS stands (0.629) than for SC stands (0.451) (Table 1). It was very close to the mean value of 0.504 for between-plot similarity (0.551 and 0.591 for CWS and SC, respectively). Seed density sharply decreased from the 0–2 cm (15.8 seeds per core and 62.5 seeds per plot on average) to the 15–20 cm layer (2.7 seeds per core and 8.1 seeds per plot on average), without significant difference between the two systems. Species richness strongly decreased from the top to the bottom layer so that the cumulative species richness curve rapidly reached an asymptote (Figure 1a). As of the 5–8 cm layer, S did not increase significantly. There was no significant difference between the two systems. Conversely, species richness linearly increased with the number of sample cores (Figure 1b). All species but one (Hypericum perforatum) had their highest abundance in the most superficial soil layer, particularly J. effusus, A. canina and B. alba, but these three species were also present in the deepest layer (Figure 2). Abundance of R. fruticosus agg. and R. idaeus seeds was quite low but constant throughout the seed bank. Depth distribution of species did not differ significantly between the two systems. The seed bank included mainly herbaceous taxa. Four tree or shrub species were recorded but B. alba was the only species constant throughout the samples. Among the species recorded, only four (14.3%) were ancient forest species (C. pallescens, C. sylvatica, Hypericum pulchrum, Lysimachia nemorum), but all except Carex sylvatica were open-forest habitat species rather than interior forest species in our study area.
Relation between seed bank and vegetation A total of 57 species were identified in the aboveground vegetation, ranging from 14 to 33 species per plot, of which 16 (28.1%) were also found in the seed bank
Hedera helix Lonicera periclymenum
R. idaeus
Woody undershrubs and climbers Rubus fruticosus agg.
Sambucus racemosa S. nigra S. sp. Corylus avellana Populus tremula Sorbus aucuparia Crataegus monogyna Viburnum opulus Prunus avium Fagus sylvatica Salix caprea
Acer pseudoplatanus Quercus robur Fraxinus excelsior Betula alba subsp. alba
Alnus glutinosa
Tree and shrub species Carpinus betulus
Species
AV SB AV SB AV AV
AV SB AV SB AV AV AV AV SB AV AV SB AV AV AV AV AV AV AV AV
11 +
2 2
1 + +
1
4 + 1
3 7
+ 2
3
2 3 2 3 2 1 2 + +
3
3
4 1 2 1 2 3 + 1 10 1
8
5 15
+
1
1 + 1 2 36 1 1 5 1
2
4
2
+
+
12
2 2
+ +
5 1
4 +
3 + 1 3 +
1 2 1
1
2
5
2 + 3
2
1
4
5 4 0 5 2 1
5 1 5 2 5 5 5 3 5 4 3 2 5 2 2 2 2 1 2 2
F
4 8 + 9
2
3 2 + 19
2 +
+ 2 +
3 2 +
2 3
1 1 2 4
2
2
1
7
6
3
1
2
SC stands
CWS stands
Table 2. Species composition of seed bank (number of viable seeds) and aboveground vegetation (cover-abundance index).
3 3
2
1
1
+
2 1 +
2
+
8
3 1 + 1
+
+ 1
4 6
+
1
11
3
2 1 1 + 1
2
2
4
10
2 2 1
1
9
5 5 3 3 1 1
5 0 5 2 5 3 3 2 4 4 1 4 2 2 1 0 0 1 0 0
F
2492
Stachys sylvatica Valeriana repens Filipendula ulmaria Festuca gigantea Epilobium angustifolium
Clearing and edge species Senecio ovatus Silene dioica Moehringia trinervia
Impatiens noli-tangere Viola reichenbachiana Paris quadrifolia Ranunculus ficaria Arum maculatum Adoxa moschatellina
Anemone nemorosa Polygonatum multiflorum Oxalis acetosella Milium effusum Circaea lusetiana Lysimachia nemorum
Understory true forest species Lamium galeobdolon Hyacinthoides non-scripta Carex sylvatica
Species
Table 2. (Continued).
AV AV AV SB AV AV AV AV AV
AV AV AV SB AV AV AV AV AV AV SB AV AV AV AV AV AV
4
5
F
2 3
+ +
+
+ 2
+ 3
1
2
1 2 + 2 +
+
+
2 + +
1 2 1 +
4 1 2
1 1
1
+ + 1 + +
1
1
3 3 1 3 1 + 1
4 2 1 0 1 1 1 1 0
5 5 3 2 3 3 4 1 1 1 1 0 1 1 1 1 1 +
6
3
1
2
SC stands
CWS stands
+
+
+ 1
1
7
+
2
1
1
4 1 +
8
+
2 + + 1 +
1
1 +
+
2
9
1 1
+ 2
10
3 1 2 1 1 0 0 0 1
4 2 3 1 1 1 0 3 2 0 1 1 0 0 0 0 0
F
2493
Holcus mollis Geum urbanum Carex ovalis C. demissa Juncus bufonius Luzula multiflora Scirpus setaceus Agrostis capillaris
Poa trivialis
Carex pallescens
Carex remota
Agrostis canina
Deschampsia cespitosa
Species of moist-compacted soils Juncus effusus
Hypericum perforatum H. humifusum Carex pilulifera Eupatorium cannabinum Hypericum pulchrum Hypericum sp.
Species
Table 2. (Continued).
AV SB AV SB AV SB AV SB AV SB AV SB AV AV SB SB SB SB SB SB
SB SB SB SB SB SB 3
4
5 7
F
4 5
1
+
+
1
76
222
1
2
4
166 +
3
+
+ 1
+ 26 +
+
2
+
146 4 4
73
2
+ 1
+
33 +
101 3 1
1
1 5 4 2 1 4 2 1 0 0 3 0 2 2 2 0 2 0 3 0
2 2 0 1 0 0
1
2
5
2
3
+
405 1 1
1 10
1
3
6
3
1
2
SC stands
CWS stands
1
+
1
+ 118 2 3
7
1 2
+
2 +
+
82
2 2
8
2 3
2 1
2 163 + 6
9
1
+
1
27
3
10
2 5 3 3 1 0 3 1 1 3 2 1 3 0 3 1 0 1 0 1
3 1 2 0 1 1
F
2494
AV AV AV AV AV SB
Fern species Athyrium filix-femina Dryopteris carhusiana D. dilatata D. filix-mas D. affinis Unidentified prothallus
4
5
F
.
1 1 +
27
1
.
2 1 + +
23
1
.
+ +
10
+
+
.
3 2 + 2
15
+ 1 +
+ 3
.
+
2 1
13
+
1 1 +
5 5 3 3 0 5
5
4 2 1 2 1 2 1
.
3 2 1 1 +
24
+
6
3
1
2
SC stands
CWS stands
.
3 2 1 + +
6
1
7
.
4 + 2 1
14
+ 2 1 1 +
8
.
3 1 1 1
4
1
+ 2
9
.
2 2 + 1
2
+
10
5 5 5 5 2 5
5
5 2 1 1 2 0 0
F
CSW: coppice-with-standards; SC: selective-cutting system; F: frequency (number of occurrences in the five plots), AV: aboveground vegetation (cover-abundance indices: +: scarce; 1: 75%), SB: seed bank (number of viable seeds per plot except .: presence (ferns)).
SB
AV AV SB AV AV AV AV
Unidentified seedlings
Urtica dioica Galium aprine Cardamine pratensis Stellaria media
Other species Galeopsis tetrahit Glechoma hederacea
Species
Table 2. (Continued).
2495
2496
Figure 1. Evolution of species richness as a function of the soil depth (a) and the number of soil cores taken (b). CWS: coppice-with-standards treatment; SC: selective cutting system.
(Table 2). Of the 28 taxa recorded in the seed bank, 16 (57.1%) were also present in the vegetation. On average, CWS stands supported a higher species richness than SC ones. Although the difference was not significant, the proportion of species present in both the aboveground vegetation and the seed bank tended to be higher in SC stands than in CWS stands (Figure 3). Of the 12 taxa only recorded in the seed bank, all but two (Scirpus setaceus and Eupatorium cannabinum) were observed in
2497
Figure 2. Vertical distribution of viable seed density and most frequent species in the seed bank of 10 managed forest stands (average of the values obtained by cumulating the five soil cores per plot).
Figure 3. Similarity between the seed bank and the aboveground vegetation species composition. CWS: coppice-with-standards treatment; SC: selective cutting system; SI: Sørensen’s similarity index. Values in the bars are mean number of species per plot. Total number of species per plot, including both seed bank and vegetation species, is taken as 100%.
2498 the surrounding vegetation, mainly in forest trails and clearings. None of these species were interior forest species. Species richness was always higher in the aboveground vegetation than in the seed bank, the correlation being weakly significant and negative (r ¼ 0.599, p ¼ 0.09). The dominant species in vegetation was always R. fruticosus agg. The other abundant constant species were A. pseudoplatanus, C. betulus, Q. robur, Corylus avellana, Lamium galeobdolon and Hyacinthoides non-scripta (see Table 2). There were considerable differences among stands. The contribution of true forest species was more important in CWS than in SC stands. Similarity of species composition between seed bank and aboveground vegetation was very low since Sørensen’s index reached 0.271 on average. Although the difference was not significant, SC stands tended to support a higher similarity than CWS ones (Table 1). We found a significant negative relationship between the plots within aboveground vegetation and seed bank Sørensen’s indices (Mantel test: t ¼ 9.34, p < 108), though the Mantel correlation was low (r ¼ 0.105). Between-plot similarity was 0.544 for aboveground vegetation and 0.504 for seed bank on average. Ellenberg indicator values show that the seed bank ecological profile strongly differed from that of vegetation (Figure 4). The major part of seed bank species were much more heliophilic, hygrophilic, acidophilic and oligotrophic than those of aboveground vegetation. There were also substantial differences between the two silvicultural systems. SC stands supported a more heliophilic vegetation than CWS stands (z ¼ 1.928, p ¼ 0.05), but this was the contrary for seed bank species (z ¼ 1.909, p ¼ 0.06). More hygrophilic species were found in the seed bank of CWS stands compared to SC stands (z ¼ 1.786, p ¼ 0.07), although the difference was not significant for vegetation. Distributions of indicator values for soil reaction were similar between seed bank and vegetation in SC stands, whereas vegetation was more neutrophilic than the seed bank in CWS stands. Nearly the same trend was observed for soil nutrient. Whatever the treatment, oligotrophic species dominated the seed bank but a higher proportion of mesotrophic species was found in CWS stands (z ¼ 1.886, p ¼ 0.06). Conversely, most vegetation species were mesotrophic or eutrophic in the two types of stands. Comparison of plant attributes between seed bank and aboveground vegetation is shown in Figure 5. As for the vegetation, seed banks were largely dominated by hemicryptophytes and phanerophytes. Geophytes were lacking from the seed bank and both therophytes and chamaephytes were very rare, particularly in SC stands, although these three biological types were well represented in the vegetation. The biological spectrum tended to be better preserved in the seed bank of CWS stands compared to SC stands. Plant strategy spectra were quite similar between seed bank and vegetation. Surprisingly, ruderals were very rare in the seed bank and restricted to CWS stands. Conversely, stress-tolerant species were more frequent in the seed bank than in vegetation, particularly in SC stands. The dispersal mode slightly differed between seed bank and vegetation, zoochoric species being dominant. Species with unspecialized seeds were better
2499
Figure 4. Comparison of Ellenberg indicator values between aboveground vegetation (left side) and seed bank (right side) species. Ellenberg indicator values have been grouped into three or four categories for statistical comparisons. Number in brackets is the number of species used for calculation of the percentages. Differences between the seed bank and the vegetation have been tested with the Mann and Whitney U-test (ns: non-significant; * 0.1 < p 0.01; ** 0.01 < p 0.001; *** 0.001 < p 0.0001).
represented in the seed bank than in vegetation, particularly for SC stands. We also observed a strong contrast between the seed bank and vegetation for seed weight spectra. Although heavy-seed species largely dominated aboveground vegetation, light-seed species represented almost 50% of the total number of species in the seed bank, while heavy-seed species were rather rare. This result was particularly marked for CWS stands whose seed banks include more numerous light-seed species than SC ones (z ¼ 1.886, p ¼ 0.06), although their vegetation supports a higher number of heavy-seed species (z ¼ 1.853, p ¼ 0.06). Morphological spectra also differed between seed bank and vegetation. Climbers (except R. fruticosus agg.) and species with a basal rosette were lacking in the seed
2500
2501 bank. Herbs with an erected-leafed stem and graminoids were much more numerous in the seed bank than in the vegetation. There was no significant difference between CWS and SC stands. Comparison of the distribution of taxa among PFTs showed that three PFTs were completely lacking from the seed bank: ruderal annuals, vernal geophytes and shade-tolerant perennials. Conversely, cespitous graminoids and prostrated ruderals were more frequent in the seed bank than in vegetation. Despite significant differences in the vegetation between CWS and SC stands (ruderal annuals more frequent in SC stands: z ¼ 2.095, p ¼ 0.04; shade-tolerant perennials more frequent in CWS stands: z ¼ 1.676, p ¼ 0.09), the two PFT spectra did not significantly differ for seed banks.
Discussion Methodological considerations Our study was designed to be mainly explorative and thus careful interpretation of the results is required. Due to limited laboratory capacities we restricted our investigations to 10 forest stands divided over two management types, and the sampling design to five soil cores per plot. However, all stands were selected under similar abiotic conditions to avoid large variability in vegetation and seed bank composition. We found rather low values of intra-plot similarity and a strong linear increase of species richness from the first up to the fifth soil core within plots. These results suggest that the five cores per plot-sampling scheme was not optimal and that sampling efficiency would gain if the within-plot number of samples is increased. On the contrary, the species richness–soil depth curve showed that the number of species did not increase significantly beneath 8cm depth. All species corresponding to the deepest buried seeds were also found in the most superficial layer with a higher density. Consequently, an 8-cm depth soil core would be sufficient to sample seed banks in such managed forests. Between-plot
Figure 5. Comparison of species attributes between aboveground vegetation (left side) and seed bank (right side) species. CWS: coppice-with-standards treatment, SC: selective-cutting system. Life forms (Raunkiaer 1934). Th: therophytes; H: hemicryptophytes; G: geophytes; Ch: chamaephytes; Ph: phanerophytes. CSR strategies (Grime et al. 1988). C: competitors (incl. C, C/CR, C/CSR, C/SC); S: stress-tolerators (incl. S, S/SR, S/CSR, S/SC); R: ruderals (incl. R, R/CR, R/SR, R/CSR); CSR: ruderal, stress-tolerant competitors (incl. CSR, CR, CR/CSR, SC, SC/CSR, SR, SR/CSR). Morphological types (Barkman 1988). W: woody species, S: herbs with an erected-leafed stem; P: prostrated creeping species; G: graminoids; Others: erected herbs with a basal rosette, herbs with both a basal rosette and an erectleafy stem, equisetoids, climbers. Plant functional types (Decocq et al., in press). TS: tree seedlings; WC: woody climbers: CG: cespitous graminoids; RA: ruderal annuals; VG: vernal geophytes; TlF: tall lightrequiring forbs; LfG: late-flowering graminoids; PR: prostrated ruderals; StP: Stress-tolerant perennials. All percentages have been calculated with 53 and 26 species for vegetation and seed bank, respectively, for which attributes were available from the literature. Differences between the seed bank and the vegetation have been tested with the Mann and Whitney U-test (ns: non-significant; * 0.1 < p 0.01; ** 0.01 < p 0.001; *** 0.001 < p 0.0001).
2502 similarity was moderate whatever the silvicultural system, suggesting that the number of stands included was nearly adequate. Nevertheless, this low number of plots associated with the high variance of the values recorded made statistical comparisons between the two silvicultural treatments difficult, even using non-parametric tests. Moreover, we were not able to take ferns into consideration in the data analysis though they represented an important taxonomic group in the plant communities studied. Finally, although the seedling emergence method is the most commonly used technique for investigating seed banks, a number of methodological limitations have been recognized (e.g., Ingersoll and Wilson 1989; Brown 1992; Holderegger 1996; Thompson et al. 1997). Consequently, in the following discussion we mainly address some trends, further investigations being needed to draw definitive conclusions.
Seed bank density and diversity The seed bank density recorded is within the range previously reported for similar deciduous forests: from 1391 to 21,514 seeds m2 in mature beech forests (Staaf et al. 1987), 12,426 seeds m2 in an oak–beech forest of Belgium (Bossuyt et al. 2002), 6500 seeds m2 in an oak–lime forest (Petrov and Palkina 1983), from 475 to 16,700 seeds m2 in an old-growth temperate deciduous forest of Quebec (Leckie et al. 2000). The high spatial variability of seed bank density observed has often been reported (Major and Pyott 1966; Leck et al. 1989; Halpern et al. 1999) and usually related both to the patchy distribution of parent plants and to the patterns of seed dispersal. The dominance by J. effusus has also been frequently observed (Brown and Oosterhuis 1981; Kjelsson 1992; Warr et al. 1994; Augusto et al. 2001; Bossuyt et al. 2002). This species has been found to provide large stocks of long-living seeds, reaching 30,600 seeds m2 according to Warr et al. (1994). Moreover, it is probably largely dispersed during harvesting operations (i.e., agestochory, sensu Bossuyt et al. 2002). J. effusus was always present in the deepest layer. This result is in accordance with several studies, pointing to the exceptional life span of J. effusus of up to 200 years according to Kjelsson (1992). Among the other frequent species, R. fruticosus agg. and Hypericum spp. were also noted by Bossuyt et al. (2002), and Carex species from one of the main components of the seed bank for a number of ecosystems (Leckie et al. 2000). Our results are in full agreement with the forest seed bank typology recently proposed by Bossuyt et al. (2002). J. effusus is the species reaching the highest density whatever the soil layer considered. Hypericum spp. (mainly H. perforatum in our study, instead of H. hirsutum) is well represented in the seed bank, particularly at mid-depth, although it may lack in the aboveground vegetation. R. fruticosus agg. occurs both in the seed bank, with a quite regular distribution among the different horizons, and in the understory, where it usually reaches high densities. True forest species as well as tree species are rare in the seed bank, with the previously reported exception of L. nemorum and Moehringia trinervia, which are restricted to the most superficial horizon. Finally, the recent-forest species mentioned by Bossuyt et al. (2002), such as Urtica dioica, Chenopodium polyspermum or Conyza canadensis, were lacking
2503 in our study. This is an expected result, since we sampled an ancient forest. Surprisingly, these authors did not mention the case of graminoid species (including grasses and sedges) for which we found relatively high densities in the seed bank. It should be outlined that all the species recorded were forest species in our study area, that is, species that naturally occur either in forest stands or in associated open habitats. This result has often been reported for ancient forests (see Bossuyt and Hermy 2001) but with notable exceptions (e.g., DeFerrari and Naiman 1994; Halpern and Spies 1995; Halpern et al. 1999). This suggests that weedy seeds as well as exotic species from surrounding landscapes are poorly able to enter the forest seed banks.
Why are true forest species so rare in the seed bank? We found a large discrepancy between aboveground vegetation and seed bank composition. The similarity tended to be higher in SC stands where the disturbance regime allows many light-demanding species to persist. Most of the species present in both vegetation and seed bank were not interior forest species but species of open forest habitats. This is consistent with numerous previous studies on viable seeds in forest soils that have shown a poor correspondence between species present in the flora and in the seed bank (e.g., Thompson and Grime 1979; Warr et al. 1994; Eriksson 1995; Bossuyt and Hermy 2001), as well as the scarcity of true forest species in the seed bank. In our study, C. sylvatica may be considered as the only true forest species. Other species, such as M. trinervia, L. nemorum, C. pallescens, C. pilulifera, H. pulchrum, have been cited as ancient forest species (Hermy et al. 1999) but in the study area all have their optimum not in closed-canopy stands but in open areas, like forest lanes or edges. The scarcity of true forest species in forest soil seed banks is often attributed to seed size. Our results show that though most species of the aboveground vegetation have rather heavy seeds, small-seeded species formed the largest contribution in the seed bank. This may be explained by the negative correlation between seed size and seed longevity (Bekker et al. 1998). As true forest species usually have large, heavy seeds for successful recruitment in stress-associated forest environments (Eriksson and Ehrle´ n 1992; Eriksson 1995), they are not able to incorporate the persistent seed bank. It is noteworthy that of the three PFTs which are completely lacking in the seed bank, two, vernal geophytes and shade-tolerant perennials, are almost exclusively composed of true forest species (Decocq et al., in press). A number of studies have shown the lack of persisting seed banks for spring ephemerals (Brown and Oosterhuis 1981; Schiffman and Johnson 1992). It has been suggested that these species do not need to incorporate the seed bank since they possess alternative modes of propagation (e.g., rhizomes or bulbs) and already develop a shadeevading strategy (Rogers 1982; Pickett and McDonnell 1989). Shade-tolerant perennials would not need to incorporate the seed bank either since they mainly reproduce vegetatively. However, it has been recently demonstrated that they also regenerate by seeds (Eriksson 1995; Holderegger 1996), suggesting rather a methodological problem in detecting seeds (Holderegger 1996; Leckie et al. 2000).
2504 Where do seed bank species come from? Only 57.1% of the seed bank species were recorded in the aboveground vegetation. This value is close to those previously reported (Warr et al. 1994; Eriksson 1995; Bossuyt and Hermy 2001), which indicates that parent plants do not belong to the current aboveground plant community. Two hypotheses may explain this result. A first hypothesis may be that buried seeds originated from parent plants growing in the stand in the past and maintained as a result of extended longevity (e.g., Qi and Scarratt 1998). This ‘temporal segregation’ hypothesis is supported by a number of previous studies which have demonstrated that most species of the seed bank are light-demanding species, that is, early-successional species, which appear profusely in the gaps as soon as the trees are blown down or cut. Next they disappear from the aboveground vegetation as tree canopy develops and shade increases (e.g., Jankowska-Blaszczuk 1998). In our study, seed banks were largely dominated by heliophilic species, particularly in CWS stands. Comparison of seed bank composition with aboveground vegetation observed in postlogged stands confirms the hypothesis that forest seed banks are partly composed of early-successional species of former forest stages. A persistent seed bank allows them to respond immediately after silviculture-induced disturbances, particularly to the increasing light availability (Brown and Oosterhuis 1981). This induces the regeneration of early successional species from buried seeds and thus the replenishment of the seed bank (Staaf et al. 1987). B. alba was the only tree species to be constant in the soil seed bank. Previous studies have already reported that Betula species (including B. alba and B. pendula) were quite frequent in the seed bank of European temperate forest (see Bossuyt and Hermy 2001). To a lesser degree, Alnus glutinosa and Sambucus racemosa were also recorded in the seed bank. All the tree or shrub species of the seed bank were light-demanding early-successional species. This confirms the assumption that only shade-intolerant woody species are able to show durable seed-banking (Halpern et al. 1999; Leckie et al. 2000). In our study, seed banks also included a high amount of hygrophilic species, particularly in CWS stands. This may be related to soil and climate properties in the study area. As soils are moderately drained, they often become waterlogged after forest harvesting as a result of both soil compaction and water table elevation. Several seed bank species are characteristic of wheel tracks microhabitats (e.g., J. effusus, J. bufonius, S. setaceus, Deschampsia cespitosa, L. nemorum), which often associate compacted waterlogged soils with temporary micro-ponds. As forestry vehicles always use the same trails in CWS stands, such amphibious microhabitats are well differentiated and thus may persist during a few years, allowing these hygrophilic species to establish and massively enter the seed bank. Conversely, in SC stands, wheel tracks are scattered throughout the stand and are less deep, and thus the induced microhabitats may be too ephemeral to allow a durable establishment of hygrophilic species. A second explanation is that buried seeds originated apart from the stand and have been imported during harvesting operations. This ‘spatial segregation’ hypothesis is supported by several arguments. Firstly, Ellenberg indicator values for soil reaction and soil nutrient were much lower for the seed bank than for vegetation, particularly in SC
2505 stands. Almost all the seed bank species responsible for this difference (e.g., A. canina, C. demissa, C. ovalis, C. pallescens, Luzula multiflora) characterize the Carici demissae–Agrostietum caninae association, which is the most largely distributed plant community of forest lanes in the study area (Decocq 1997). These species may be dispersed into forest stands by means of the mud carried by forestry vehicles used for harvesting operations. This hypothesis would explain the fact that SC stands provide higher seed densities of acidophilic, oligotrophic species, since they support denser tracks and more frequent passages of vehicles than CWS stands, and thus are more exposed to seed inputs from adjacent open areas. Secondly, in the seed bank the positive correlation between the proportion of the dominant J. effusus and species richness suggests that this species does not exclude others. As J. effusus is widely recognized as an agestochoric species (see Bossuyt et al. 2002), its abundance in the seed bank could be interpretated as an indicator of management intensity and even may be a good predictor for the agestochoric species richness of seed banks. The fact that the abundance of J. effusus in the seed bank is higher in SC stands than in CWS stands is consistent with this hypothesis. Thirdly, the Mantel test indicated that the variability in seed bank composition was related to vegetation heterogeneity. Surprisingly, this correlation was negative. This is apparently a conflicting result, since in a similar study Leckie et al. (2000) have reported a positive – but also low – relationship. We suspect that this significant relationship may be linked to a third factor (i.e., confounding), which would be forest management and its associated disturbance regime. Due to the stronger disturbance regime, SC stands support a lower species richness and a more homogeneous vegetation, compared to CWS stands (Decocq et al., in press). Another consequence is the increased probability for seeds produced apart from the stand (particularly in adjacent open habitats) to incorporate the forest stand seed bank due to agestochory. The fact that the variability of seed bank composition is greater in SC stands than in CWS stands tends to confirm this hypothesis. This may also explain the lack of correlation between aboveground species richness and seed bank density or richness. This is also in accordance with previous studies which have shown that the size and diversity of seed banks depend not on the diversity of aboveground vegetation but on the disturbance regime to which a forest community is submitted (Whipple 1978; Staaf et al. 1987; Picket and McDonnel 1989). The fact that the soil seed bank composition of the CWS stand with the most recent coppice cutting was closer to those of SC stands, and oppositely for the oldest SC stand, also suggests an important role of the duration since the last disturbance event in patterning soil seed banks.
Management implications An important question in sustainable forestry concerns the potential role of seed banks in the conservation of the forest flora in forests submitted to more or less intensive management. Yet a total of 28 species has been recorded in the soilpersistent seed bank and perhaps more could have been found with a more intensive
2506 sampling design. Nevertheless we think that soil seed banks could not be considered as an important source of interior forest species diversity, but early-successional species are involved in the forest regeneration. However, seed banks also contain species which have a potentially negative impact on the true forest flora like competitive-ruderal light-demanding blackberries (R. fruticosus agg.) or graminoid species (e.g., J. effusus, Carex spp., D. cespitosa). This result is consistent with previous studies (Chambers and McMahon 1994; Hermy 1994; Halpern et al. 1999). Some management practices like soil mixing or scarification to expose mineral soil may thus release unwanted vegetation, such as the large seed reserve of graminoids. The light-resource increase associated with forest harvesting may enhance the negative effects that species like R. fruticosus agg. have towards true forest species in managed forests, as confirmed by the strong dominance of blackberries in SC stands. Following previous authors we conclude that the characteristics of forest seed banks are largely affected by the silvicultural system (Augusto et al. 2001), and that plot to plot variation in the seed bank as well as in aboveground vegetation can be explained not only by direct environmental variation but also by variation in forest management. These results have two main implications for sustainable forest management. Firstly, soil disturbance should be minimized to avoid the strong spread of blackberries or graminoids. Secondly, always following the same trails (as in CWS in our study) is probably a more suitable way to haul logs and timber from forest stands than each time using a different path (as in SC) to prevent forest stands from both extended soil compaction and spread of agestochoric species in the seed bank. Thirdly, as most true forest species do not have mechanisms for long-distance dispersal, successful reestablishment requires source populations in the direct vicinity of the degraded stands. Post-harvesting recruitment or expansion of the true forest flora rather depends on mechanisms like clonal spread and/or sexual reproduction of surviving plants than recruitment from the seed bank (Halpern et al. 1999). If rotation lengths are too short or silvicultural activities too frequent, disturbance-sensitive species with limited dispersal may be eliminated locally from the understory (Busing et al. 1995; Halpern and Spies 1995). The difference in aboveground vegetation observed between CWS and SC stands, particularly the lower abundance of shade-tolerant perennials and vernal geophytes, tends to confirm this hypothesis. Consequently, following Brown (1981) we think that it is essential to retain remnants of the original shade flora within old coppice woods, because the species involved were neither likely to survive in the seed bank nor able to re-migrate rapidly in disturbed stands.
Acknowledgements We thank the French Office National des Foreˆ ts and the ‘Compagnie Forestie`re du Nouvion’ for providing facilities during experimentation, and Fre´ de´ ric Dupont and Annie Wattez-Franger for assistance during field work. We are very grateful to the two anonymous referees for their very helpful comments on the initial draft. This
2507 research was supported financially by the GIP ECOFOR (‘Biodiversity and Forest management’ program).
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