seed banks of temperate deciduous forests during secondary succession
TRANSCRIPT
Seed banks of temperate deciduous forests during secondary succession
Jan Plue, Kris Verheyen, Hans Van Calster, Damien Marage, Ken Thompson, Rein Kalamees,
Malgorzata Jankowska-Blaszczuk, Beatrijs Bossuyt & Martin Hermy
AbstractQuestion: (i) How does former land use and land useintensity affect seed bank development during post-agricultural succession? (ii) How does time since thelast clear-cut change seed bank composition duringpost-clear-cut succession?Methods: One data set was compiled per successiontype using the following selection criteria: (i) thedata set included a successional series, (ii) plots werelocated in mesotrophic forest plant communitiesand (iii) vegetation data were available. The post-agricultural succession data set comprised 76 recentforest plots (eight studies); the post-clear-cut succes-sion data set comprised 218 ancient forest plots(three studies). Each data set was analysed sepa-rately using either linear mixed models orgeneralized linear models, controlling for both en-vironmental heterogeneity and variation betweenstudy locations.
Results: In the post-agricultural succession data set,land use and time significantly affected nearly all thestudied seed bank characteristics. Seed banks onformer arable land recovered poorly even after 150year of restored forest cover, whereas moderate landuse intensities (grasslands, heathlands) yielded morerapid seed bank recovery. Time was a significantdeterminant of all but two soil seed bank character-istics during post-clear-cut succession. Seed banks inmanaged ancient forest differed strongly in theircharacteristics compared to primary forest seedbanks.Conclusions: Forest seed banks bear the marks offormer land use and/or forest management andcontinue to do so for at least 150 years. Never-theless, time since the last major disturbance, beingeither former land use or clear-cutting, remains asignificant determinant of the seed bank.
Keywords: Ancient forest; Former land use; Landuse intensity; Post-agricultural succession; Post-clear-cut succession; Recent forest.
Nomenclature: Lambinon et al. (1998); Gleason &Cronquist (1991).
Introduction
Seed bank dynamics during secondary forestsuccession are of interest because of the role thatpersistent seed banks fulfil in successional vegeta-tion dynamics. Especially in the earliest stages ofsecondary forest succession, a persistent seed bankwill be a dominant driver in community assembly(e.g. Marks & Mohler 1985), second only to the ex-tant vegetation and seed input via (long-distance)dispersal. Despite a declining input from the seedbank (increasing vegetation-seed bank dissimilarity(Dolle & Schmidt 2009)), the seed bank remains im-portant for the herbaceous community long afterthe forest canopy closes. Indeed, seeds may germi-nate from the persistent seed bank and theirseedlings may subsequently be recruited into forestswith recurrent short-interval disturbances (e.g. cop-piced forests; Brown & Oosterhuis 1981), forestcanopy gaps (Mladenoff 1990; Naaf & Wulf 2007)
Plue, J. (corresponding author, [email protected])
& Hermy, M. ([email protected]): Divi-
sion Forest, Nature and Landscape Research, KU
Leuven, Celestijnenlaan 200E, Leuven, Belgium.
Verheyen, K. ([email protected]) Laboratory
of Forestry, Ghent University, Geraardsbergsesteen-
weg 267, Melle-Gontrode, Belgium.
Van Calster, H. ([email protected]): Institute
for Forest and Nature Research, Kliniekstraat 25, 1070
Brussels, Belgium.
Marage, D. ([email protected]): AgroPar-
isTech, ENGREFNancy, UMR 1092, F-54000 Nancy,
France.
Thompson, K. ([email protected]): De-
partment Animal and Plant Sciences, The University
of Sheffield, Western Bank, Sheffield S10 2TN, U.K
Kalamees, R. ([email protected]): Department of Botany,
Institute of Ecology and Earth Sciences, University of
Tartu, 40 Lai, 51005 Tartu, Estonia.
Jankowska-Blaszczuk, M. ([email protected]):
Botany Department, The Jan Kochanowski University
of Humanities and Sciences, 15 �Swietokrzyska Street,
Kielce, Poland.
Bossuyt, B. ([email protected]): Terrestrial
Ecology Unit, Ghent University, K. L. Ledeganck-
straat 35, Ghent, Belgium.
Journal of Vegetation Science 21: 965–978, 2010DOI: 10.1111/j.1654-1103.2010.01203.x& 2010 International Association for Vegetation Science
or small gaps in the herbaceous canopy (Rydgrenet al. 2004; Jankowska-Blaszczuk & Grubb 2006;Hautala et al. 2008). In particular, the third phe-nomenon increasingly adds to the view of seedbanks as a functional part of non-successional com-munities (Kalamees & Zobel 2002), includingtemperate deciduous forests. Unfortunately, manyseed bank studies are a snapshot at a single momentin time, with little thought as to how seed bankcomposition or characteristics arose and/or arechanging (Fenner & Thompson 2005). Hence, athorough understanding of temporal seed bankchanges and their determinants over the course ofsecondary forest succession is required; this willprovide insights into the role that seed banks couldplay in the dynamics of understorey populationsand communities.
The initial form of the seed bank at the start ofsecondary forest succession, in terms of compositionand characteristics, will depend on the type/intensityof the former land use (Thompson & Grime 1979),rendering it a key determinant of the persistent seedbank during succession (Bossuyt & Hermy 2001).Indeed, the seed bank generally reflects the severityand predictability of the disturbance regimes asso-ciated with specific land use types. Small-seeded,high-density and diverse seed banks in arable landwith regular ploughing (e.g. Roberts & Vankat1991) and low-density, species poor seed banks inforests with long-rotational timber harvesting (e.g.Bossuyt et al. 2002; Van Calster et al. 2008a; Plueet al. in press) present the two extremes of the seedbank spectrum. Furthermore, there is a strong as-sociation between seed persistence and habitat type,triggered by the typical spatial and temporal pat-terns of the disturbance regime (Thompson et al.1998). Consequently, one might hypothesize thatsuccessional forest seed banks may bear the legaciesof former land use for a longer time as land use in-tensity increases (Plue et al. 2009), analogous topatterns observed in the herbaceous understoreyforest vegetation (Dupouey et al. 2002; Dambrineet al. 2007). Yet, the majority of seed bank studieshave so far indicated that former land use, beingpasture, grassland or heathland, no longer had asignificant effect on recent forest seed banks, onceforest stands exceeded an age of 50 years (Bossuyt &Hermy 2001). Hence, time since disturbance is per-ceived as a second major determinant of forest soilseed banks, in post-agricultural, recent forests (Ro-berts & Vankat 1991; Bossuyt et al. 2002) and inpost-clear-cut, ancient forests (Plue et al. in press).Indeed, seed predation, seed senescence, failed ger-mination and changing input from the herb layer
during succession are but a few of the seed bank andvegetation processes that will affect and change theseed bank composition through time.
However, despite some generalizations on suc-cessional seed bank dynamics, most establishedpatterns and processes concerning seed banks oftemperate deciduous forests are far from clear.Therefore, we aimed to establish common under-lying patterns in seed bank dynamics in the course ofsecondary succession, through a plot-based quanti-tative review of post-agricultural and post-clear-cutforest succession in NW Europe and N America.The two main goals of the review were: (1) unravel-ling both the effects of former land use intensity andtime since former land use during post-agriculturalsuccession in recent forests, and (2) understandingthe effect of time since disturbance during post-clear-cut succession in ancient forests.
Methods
Data collection and description
Data setsStudies containing suitable data sets were lo-
cated in the ISI Web of Knowledge& via queriesusing the keywords ‘‘recent forest’’, ‘‘ancient for-est’’, ‘‘soil seed bank’’, ‘‘land use history’’ and‘‘succession’’, in various combinations. The numberof studies was further narrowed by carefully check-ing the manuscript, as each data set had to meet anumber of criteria. The final selection of data sets(for characteristics, see Table 1) was based on thefollowing criteria: (i) each study included a second-ary successional series from either old-fields or clear-cuts in ancient forest; (ii) studies were located intemperate deciduous forest with mesotrophic plantcommunities, and rich alluvial forests and (con-iferous) forests on poor sandy soils were excluded;and (iii) preferably, vegetation data were available.Raw seed bank and vegetation data were extractedfrom the manuscript, or were retrieved throughcontacting the corresponding author(s). Seed bankdata were retrieved from the individual studies inseed number per species per forest plot. All studiesused germination trials to estimate seed bank char-acteristics and composition, thus working with asubset of viable, germinated seeds. Detailed in-formation on sampling and germination protocolscan be found in Appendix S1. Vegetation and seedbank data were transformed to presence–absencedata to overcome differences in sampling intensity(plot size) and to be able to perform Raup & Crick
966 Plue, J. et al.
dissimilarity analysis. The data set of Bossuyt et al.(2006) lacked vegetation data and was not in-corporated in analyses requiring vegetation data.This resulted in a post-agricultural succession dataset containing 76 recent forest plots from eight in-dividual studies, and a post-clear-cut successiondata set containing 218 plots from four individualstudies, of which one plot was omitted as it con-tained no species.
Seed bank characteristicsSeed bank characteristics were calculated per
plot: species richness, Shannon–Wiener diversity in-dex, the presence–absence-based share of ancientforest species in the seed bank (sensu Hermy et al.1999; only for the European data sets), the CSR seedbank signature (only for the European data sets;Hunt et al. 2004) and the Raup and Crick vegeta-tion–seed bank dissimilarity (Vellend et al. 2007).The probabilistic Raup and Crick dissimilaritymeasure was chosen as it is unbiased by the large a-diversity differences between the seed bank and theherbaceous understorey forest vegetation (Vellendet al. 2007). Seed density from European studies wascalculated without Juncus effusus (Bossuyt et al.2002) because of the vast abundance of this species,which could possibly confound the results. Ad-ditionally, two seed bank-related traits werecompiled for all recorded seed bank species: meanseed weight (mg) and life span (annual, biennial orperennial). Seed weight was analysed because lighter(smaller) seeds (e.g. seed banking species from ara-
ble land) may persist longer, keeping overall seedweight equally low as forest succession progresses.Life span was analysed as arable lands almost ex-clusively contain annual and biennial seed bankingspecies, whereas grassland seed banks yield moreperennial species, both persistently altering seedbanks during forest succession. Traits from Eur-opean species were gathered from the LEDAtraitbase (Kleyer et al. 2008) and, if necessary, sup-plemented with data from Grime et al. (2007) or theEcological Flora of the British Isles (http://www.ecoflora.co.uk/). American species traits were col-lected from (i) the Seed Information Database at theKew Royal Botanical Garden (seed weight; http://data.kew.org/sid/), (ii) the USDA plant database(life span), (iii) Gleason & Cronquist (1991) (lifespan) and (iv) online American floras (life span;http://efloras.org). Plant synonyms were identifiedusing the IPNI database (http://www.ipni.org/) torecover the correct plant traits. Using the presence–absence seed bank composition, either the mean va-lue (seed weight) or the relative contribution to theplot seed bank of a trait value (annuals; biennials)was calculated.
Data analysis
As detailed environmental data were lacking formost studies, we used soil acidity (pH H2O) as aproxy for the overall abiotic soil conditions. Soilacidity was incorporated into both analyses as afixed factor, with levels corresponding to the various
Table 1. Main characteristics of the 13 collected datasets. 4100/150/250 Ancient forest (stand age is approximate); wAllstands are ancient forest; �Primary forest; 1Old-growth forest Background information on sampling and germinationprotocols can be found in Appendix S1.
Location Former land use Time since disturbance n Reference
Old Field succession Time since former land useEurope
Vlaams Brabant, Belgium Arable fields 55/97/116/4250 8/8/8/12 Bossuyt et al. (2002)Viroin, Belgium Grassland 41/133/4250 2/2/1 Bossuyt et al. (2006)Southern Black Forest, Germany Pasture/Grassland 150/4250 6/7 Ludemann (1994)Durham County, United Kingdom Arable fields 50/80/100/4150 1/1/1/1 Donelan & Thompson (1980)Southern Alps, France Arable fields/Pasture/
Heathland50/75/115/4250 2/3/3/8 Marage et al. (2006)
Laelatu, western Estonia Wooded meadow 20/4100 10/10 Kalamees & Zobel (1998)USA
South-western Ohio, USA Arable fields 10/50/90/42501 1/1/1/1 Roberts & Vankat (1991)North Carolina, USA Arable fields 33/58/85/112/42501 2/2/2/2/2 Oosting & Humphreys (1940)
Forest successionw Stand ageEurope
Montargis, central France Forest 20/40/70/100/120 8/16/6/12/6 Van Calster et al. (2008a, b)Hasbruch forest, northern Germany Forest 40/80/120/4250 12/12/12/12 Plue et al. (in press)Hasbruch forest, northern Germany Forest 40/80/120/4250 12/12/12/12 Plue et al. (in press)Hasbruch forest, northern Germany Forest 120/4250 12/12 Plue et al. (unpublished data)Bialowieza forest, eastern Poland Forest 80/4250� 25/25 Jankowska-Blaszczuk
& Grubb (1997)
Seed banks in temperate forest succession 967
soil buffer ranges (as defined by Ulrich 1983). Eachlevel contained a sufficiently large number of plotsto allow meaningful statistical inference (four levelsin post-agricultural succession data set; three levels inpost-clear-cut succession data set). This procedureenabled us to account for environmental variation inboth data sets. The two data sets were analysed sepa-rately to establish a posteriori whether or not post-agricultural and post-clear-cut forest succession in soilseed banks would be similar, and would conform tothe same processes and driving factors.
Post-agricultural succession data setTo test whether the various seed bank char-
acteristics changed significantly with land useintensity and time since former land, a linear mixedmodel was applied. Land use intensity [high: arableland; moderate: grassland, pastures, (wooded) mea-dows, heathland (these four land use types were incasu only moderate in their disturbance intensity)and a reference state: managed ancient forest] andtime since former land use (0–50; 51–100; 101–150;250 yr) were incorporated into the mixed model asone integrated fixed factor (Land use�Time). Thisfixed factor counted seven levels. The first six factorlevels were defined by the interaction term betweenland use intensity and time since former land use,with managed ancient forest as the seventh factorlevel. This procedure was applied because the post-agricultural data set lacked young stands in mana-ged ancient forests. This would have stronglyconfounded the mixed model, should we have optedto apply a full-factorial model with fixed factorsland use intensity and time since disturbance. Forsimilar reasons, the fixed factor pH class (four levels:pH H2O 3.8–4.2, 4.2–5.0, 5.0–6.2, 46.2) was onlyincorporated as a main effect, as not all levels werepresent at each level of the land use–time factor,preventing correct modelling of their interactionterm. Location was incorporated into the mixedmodel as a random factor to eliminate variation be-tween studies. Non-significant model terms wereprogressively omitted, omitting the most insignif-icant term first and subsequently re-running thereduced model at each step. We are aware that thissimplified mixed model structure may have elimi-nated significant effects; therefore, its results will bediscussed with caution.
Post-clear-cut succession data setSeed bank characteristics were analysed using
generalized linear models (GzLMs), with fixed fac-tors being time since disturbance (0–50; 51–100;101–150; 151–250 yr), pH (three levels: pH H2O 3.8–
4.2, 4.2–5.0, 45.0) and location. Location was in-cluded as fixed factor in the GzLMs and not as arandom factor in a linear mixed model (cf. post-agricultural succession data set), as three locationsare too few to accurately estimate a random inter-cept in a linear mixed model. The interaction termbetween the fixed factors, time since disturbance andpH, was included in the model. The interactionterms including location were omitted as not all lo-cations contained all levels of time since disturbanceor pH data. Moreover, we were only interested ifthere was an overall effect of study location on seedbank characteristics. Non-significant model termswere progressively omitted from the GzLMs, whichwere re-run at each occasion after first omitting themost insignificant model term. The plots from un-disturbed primary forest (4500 yr; Jankowska-Blaszczuk & Grubb 1997) were not included in theGzLMs, as these plots only occurred over a narrowsoil acidity range, confounding the results of theGzLMs (Gotelli & Ellison 2004).
The random/fixed effect of location in both ana-lyses will not be presented or discussed here because wewere only interested in excluding this variation fromthe data sets. However, the main effect of the random/fixed factor ‘location’ is presented in Appendix S2 toallow readers to assess the amount of variation re-presented by this factor in the various models.
Results
Post-agricultural succession: the effects of formerland use and time
Eight (1–39 species) was the median number ofspecies recovered from the seed bank. Seed density perplot (without Juncus effusus) ranged from 10 to26 750 seedsm� 2, with a median plot seed density of3261 seedsm� 2. Recent forest seed banks contained amedian of 15% ancient forest species (0–50%) and25% annuals and biennials (0–75%). Themedian seedweight of the seed bank species was 0.72mg (0.08–2.39mg). The vegetation was relatively similar to theseed bank (only 43%median dissimilarity; 0–99%).
All linear mixed models successfully modelledthe ten seed bank variables (Table 2), excluding be-tween-study variation. Apart from the ruderal seedbank signature, the integrated Land use�Time fac-tor had a significant effect on all remaining seedbank characteristics. The explanatory power wasonly moderate for modelling of the Shannon–Wi-ener diversity index and the percentage of ancientforest species. Particularly in the latter case, pH ap-
968 Plue, J. et al.
peared to be of great importance (Table 2). Soil pHhad a significant effect on six seed bank character-istics (Table 3). Additionally, pH was the onlysignificant parameter in the ruderal seed bank sig-nature model. The boxplots illustrating the maineffect of soil pH on seed bank characteristics can befound in Appendix S3.
Seed bank species richness declined with time,mainly due to high species richness in the youngestforest stands (0–50 yr) on former arable land (Fig.1a). Seed bank species richness on former arableland was consistently higher compared to the speciesrichness of ancient forest seed banks, irrespective ofstand age. Recent forest seed banks of grasslandscontained similar amounts of species as ancient for-est seed banks. Only the seed banks of the youngeststands on former arable land had the highest speciesdiversity compared to ancient forest seed banks,when correcting for seed number (Shannon–Wienerdiversity index; Fig. 1b). Seed banks in recent forestson (mostly) former grasslands contained a similarseed number to seed banks of ancient forests. Seedbanks of recent forests on former arable land stillcontained more seeds than ancient forest seedbanks, independent of stand age (Fig. 1c). Thecompetitive seed bank signature was consistentlylower in recent forests with an intermediate level offormer land use intensity compared to ancient for-ests (Fig. 1d). Recent forest seed banks on formerarable land had a share of competitive species thatappeared to decrease with age, but this share wassimilar to ancient forest from stands over 100 yearsold (Fig. 1d). The stress-tolerant seed bank sig-nature was significantly lower and higher,respectively, on former arable land and formergrasslands/pastures compared to the stress-tolerant
seed bank signature of ancient forests. The ruderalseed bank signature remained relatively constantover land use class and time (Fig. 1f). Contrary toour expectations, a high percentage of ancient forestspecies was present in the seed bank of former arableland. Average seed weight increased significantlywith time in all recent forests, although it appearedto recover faster on former grasslands/pastures (50years; Fig. 1h). Recent forest stand seed banks weremore dissimilar to the vegetation than seed banks ofancient forests. This dissimilarity became of similarmagnitude once recent forest stands had reached theage of 100 years (Fig. 1i). Seed banks of (mostly)former grasslands had a vegetation–seed bank dis-similarity that was rather erratic (Fig. 1i). Thepercentage of annuals and biennials was high in an-cient forests, whereas in recent forests it appearedconsistently higher on former arable lands, andpersistently lower on former grasslands (Fig. 1j.),irrespective of stand age.
Post-clear-cut succession: the effect of time
The plot seed bank yielded a median of ninespecies, with plot species number ranging from oneto 27 species. Seed density per plot (without Juncuseffusus) ranged from 0 to 26 308 seedsm� 2, with amedian plot seed density of 3872 seedsm� 2. Theplot seed bank had a median contribution from an-cient forest species of 17% (0–50%) and fromannuals and biennials of 20% (0–67%). The medianseed weight was high: 0.81mg (0.02–4.82mg). Theseed bank was highly dissimilar to the standing ve-getation (91% median dissimilarity; 0–94%).
Time since the last clear-cut significantly anddirectly affected eight out of ten seed bank char-
Table 2. Main effects of the fixed factors in the Linear Mixed Models applied on the seed bank characteristics of the post-agricultural succesion dataset. ���P � 0.001; ��0.001oP � 0.01; �0.01oP � 0.05; AIC Akaike’s Information Criterion, ameasure of the goodness of fit for the final estimated model; DAIC observed change in the goodness of fit through modelsimplification compared to the full model; 2Square root transformed; 3Ln(X11) transformed; 4Only on the European data;An extended table including the random effect of Location can be found in Appendix S2.
n AIC DAIC Land use�Time pH
df F df F
Species richness 110 620.42 – 6 8.55��� 3 7.26���
Shannon-Wiener Diversity Index 108 196.64 20.63 6 2.29� – –Seed density (#/m2)2 108 340.08 – 6 9.86��� 3 16.13���
Competitive signature4 95 127.89 6.16 6 8.37��� 3 4.60��
Stress-tolerant signature2,4 95 143.84 17.51 6 5.66��� – –Ruderal signature2,4 95 96.67 17.81 – – 3 3.98��
% Ancient forest species2,4 95 678.57 – 6 3.01� 3 17.69���
Raup and Crick dissimilarity (%) 101 214.07 21.43 6 3.89�� – –Weight (mg)3 110 126.64 – 6 3.53�� 3 6.4��
(Bi)Annuals (%) 110 79.64 18.26 6 16.48��� – –
Seed banks in temperate forest succession 969
acteristics. Soil pH contributed significantly in ex-plaining variation in seven out of ten seed bankcharacteristics. On the one hand, the percentage of
ancient forest species and the Raup and Crick dis-similarity solely depended upon time since the lastclear-cut. On the other hand, the ruderal seed bank
a Species richness b Shannon-Wiener diversity Index
c Seed density without Juncus effusus d Competitive seed bank signature
e Stress-tolerant seed bank signature f Ruderal seed bank signature
Fig. 1. The integrated effect ‘‘land use intensity� time since former land use’’ during post-agricultural succession on seed bankcharacteristics: (a) species richness, (c) seed density without Juncus effusus, (d) competitive, (e) stress-tolerant and (f) ruderal seedbank signatures, (g) percentage of ancient forest species, (h) average seed weight, (i) the Raup and Crick vegetation–seed bankdissimilarity and (j) percentage of annuals and biennials in the seed bank. ���P � 0.001; ��0.001oP � 0.01; �0.01oP � 0.05;(�) 0.05oPo0.10; �Indicates significant differences opposed to the ‘‘Ancient forest’’ category.
970 Plue, J. et al.
signature solely depended upon soil acidity. Averageseed weight remained constant throughout the dataset, as a function of both time since the last clear-cutand soil pH.
Species richness increased with increasing habitatproductivity, but decreased consistently with ageacross the environmental gradient, as did seed densityfor themost part (Fig. 2a and c). The Shannon–Wienerindex was significantly higher on richer soil conditions,while simultaneously showing a significant decreaseover time, notably in the oldest stand age category(151–250yr) (Fig. 2b). The share of competitive speciesin the seed bank declined during post-clear-cut forestsuccession, yet the consistent decline in competitivecharacteristics with increasing stand agewas eliminatedin the most fertile environments (Fig. 2d). The share ofruderal species in the seed bank increased with soil pH(Fig. 2f). The stress-tolerant seed bank increased as theforest environment became less productive, except for
the 0–50-year-old stands with constant stress-tolerantcharacteristics. Stress-tolerance increased with age inthe most acid conditions, while this pattern wasreversed in the fertile environments (Fig. 2e). The shareof annual and biennial species differed significantlybetween age classes, being lowest in the oldest stands(151–250yr). The relation to soil pH was quite erratic(Fig. 2j). The vegetation-seed bank dissimilarity andpercentage of ancient forest species increased withtime, notably rising once forest stands mature beyond50 years of age (Fig. 2g and i).
Discussion
Time over land use or land use over time?
Former land use does leave a persistent markon the forest seed bank (Bossuyt & Hermy 2001;
g Percentage of ancient forest species h Average seed weight
i Raup & Crick dissimilarity j Percentage of annuals and biennials
Fig. 1. Continued.
Seed banks in temperate forest succession 971
a Species richness b Shannon-Wiener diversity index
c Seed density without Juncus effusus d Competitive seed bank signature
e f Ruderal seed bank signature Stress-tolerant seed bank signature
Fig. 2. The effects of time since disturbance and pH during post-clear-cut succession on seed bank characteristics: (a) speciesrichness, (b) Shannon–Wiener diversity index, (c) seed density without Juncus effusus, (d) competitive, (e) stress-tolerant and(f) ruderal seed bank signatures, (g) percentage of ancient forest species, (h) average seed weight, (i) Raup–Crick vegetation–seed bank dissimilarity and (j) percentage of annuals and biennials in the seed bank. 4500 yr Age Class A seed bank re-ference state from Bialowieza primary forest (Poland). This age category was not included in the data analysis, but wasincluded here for comparison.
972 Plue, J. et al.
Table 2; Fig. 1) and does dependent on the formerland use intensity (Bossuyt & Hermy 2001; Plueet al. 2009;Fig. 1) and stand age (Bossuyt & Hermy2001; Fig. 1). However, our findings only correspondin part to those of Bossuyt & Hermy (2001). One oftheir main conclusions relates to a stand age thresholdof 50 years. Bossuyt & Hermy (2001) – supportedby the results of e.g. Hill & Stevens (1981), Warr et al.(1994) and Dougall & Dodd (1997) – consider theimpact of former land use on the forest seed bankshould start to diminish with time, but can thisbe confirmed?
On the one hand, the review of Bossuyt & Hermy(2001) did not incorporate former arable land – itcontained only former grasslands and heathlands –with highly persistent, high-density and diverseseed banks (Roberts & Vankat 1991). These specificcharacteristics (e.g. increased seed density, speciesrichness) and even particular species (e.g. Verbascumthapsus) have recently been shown to persist in 1600-
year-old ancient forests with regular disturbanceregimes (Plue et al. 2009). Indeed, typical seed bankcharacteristics of former arable lands, i.e. increasedspecies richness, increased seed density and a largershare of annuals and biennials, remained alteredcompared to ancient forest seed banks after 150 years(Fig. 1a, c, h and j). Given the high overall persistenceof annuals and biennials (Thompson et al. 1998), thisneed not be surprising (Plue et al. 2008, 2009). Othercharacteristics (e.g. Shannon–Wiener diversity index,CSR signature, seed weight, vegetation–seed bankdissimilarity) did differ significantly compared toancient forests, but significantly recovered within50–150 yr (Fig. 1b, d, e, f, h and i). These seed bankfeatures may possibly be more responsive to processessuch as e.g. density-dependent and/or preferentialseed predation and seed senescence, which may trig-ger a faster decline in species richness as opposed toseed density effects (Fig. 1a and c). Hence, speciesdiversity may recover within 50 years. The CSR
g Percentage of ancient forest species h Average seed weigth
i Raup-Crick dissimilarity j Percentage of annuals and biennials
Fig. 2. Continued.
Seed banks in temperate forest succession 973
signature, seed weight and vegetation–seed bank dis-similarity may additionally reflect increased seedinput from the forest vegetation (Bossuyt et al. 2002).Indeed, the seed input from typical herbaceous forestunderstorey species (Fig. 1g), which are less competi-tive (Fig. 1d), more stress-tolerant (Fig. 1e; Hermyet al. 1999) and bear heavier seeds (Fig. 1h; Verheyenet al. 2003), may equally induce a swifter recovery ofthese characteristics, lowering the vegetation–seedbank dissimilarity (Fig. 1i).
On the other hand, forest plots labelled as‘‘medium’’ disturbed, containing in casu mostly for-mer grasslands, did not differ markedly in speciesrichness, species diversity and seed density from an-cient forest seed banks, irrespective of stand age(Fig. 1a–c). In this respect, our results largely parallelthe findings of Bossuyt & Hermy (2001). However,beyond the species level, the competitive and stress-tolerant seed bank signatures were, respectively, sig-nificantly lower and higher independent of stand age,in contrast to ancient forests (Fig. 1d and e). Yet, noobvious explanation was at hand. Indeed, annualsand biennials were present in low amounts (Fig. 1j),while seeds appeared similar in weight (except forlow seed weight in 50-year-old recent forest stands),compared to ancient forest seed banks (Fig. 1h).
Nevertheless, all the above information seems tosuggest that, despite partial recovery of the seed bankwith time since former land use, the seed bank stillyields typical characteristics of that former land use.Our results confirm that the influence of the formerland use diminished beyond the threshold of 50 yearssuggested by Bossuyt & Hermy (2001) (see e.g.Granstrom 1988). However, several seed bank char-acteristics had not yet returned to their state inmanaged ancient forest, even after 150 years of forest
cover. Moreover, there is little reason to assume thatthe seed bank may ever recover (Plue et al. 2008, 2009)if frequent natural or man-made disturbances allowfor seed bank replenishment (VanCalster et al. 2008a).
Will managed ancient forests ever resembleprimary forests?
Duffy &Meier (1992) questioned whether the for-est herb layer could ever recover after clear-cutting ofthe forest canopy. The results on the successional seedbank dynamics in ancient forests compared to primaryforest seed banks, put forward a similar hypothesis.
Let us assume that all ancient forests have neverknown a land use other than managed forest, whichis rather likely for the studies in this review (Jan-kowska-Blaszczuk & Grubb 1997; Van Calsteret al. 2008a; Plue et al. in press). Hence, naturalsteady-state canopy dynamics (e.g. Emborg et al.2000) have been replaced by modern silviculturalsystems, encompassing tree harvest cycles of 100–150 yr. Hence, small-scale, patchy canopy gap dy-namics (�shifting mosaic), which maintainstructurally diverse forest stands in which all devel-opmental stages are present, are replaced byinfrequent, stand-scale disturbances (clear-cuts inthis case) to yield even-aged forest stands. Indeed,during this 100–150-yr period between large stand-scale disturbances, the forest is in a relatively stableaggradation phase (Bormann & Likens 1979; Em-borg et al. 2000), characterized by few natural gapdisturbances and prolonged low-light levels. Atmost, foresters return every 5–15 yr to thin stands,creating temporary increased light levels. This severechange in canopy cover dynamics induces the seedbank of light-demanding early-successional species
Table 3. Main effects of the fixed factors Time and pH in the Generalized Linear Models applied on the seed bankcharacteristics of the post-clearcut succession dataset. ���P � 0.001; ��0.001oP � 0.01; �0.01oP � 0.05; AIC Akaike’sInformation Criterion, a measure of the goodness of fit for the final estimated model; DAIC observed change in the goodnessof fit through model simplification compared to the full model; 2Only variable with significant Time�pH interaction term (df6, F 32.43, P � 0.001); An extended table including the main effect of Location can be found in Appendix S2.
n AIC DAIC Time pH
df F df F
Species richness 193 950.07 32.45 3 54.82��� 2 48.33���
Shannon-Wiener Diversity Index 192 238.77 2.77 3 18.91��� 2 14.38��
Seed density (#m� 2) 193 600.32 5.11 3 37.68��� 2 22.53���
Competitive signature 191 309.75 7.35 3 9.31� 2 18.90���
Stress-tolerant signature2 191 452.76 – 3 11.12� 2 27.02���
Ruderal signature 191 271.87 8.98 – – 2 59.88���
% Ancient forest species 192 1499.39 13.52 3 7.98� – –Raup and Crick dissimilarity (%) 168 587.07 4.69 3 9.93� – –Weight (mm) 191 32.17 11.96 – – – –(Bi)Annuals (%) 189 175.97 6.44 3 14.76�� 2 29.35���
974 Plue, J. et al.
to become depleted as the absence of light for ex-tended periods inhibits seed bank replenishment.This is reflected by declining seed bank species rich-ness and seed density with time, independent of theabiotic conditions (Fig. 2a and c). Furthermore, theseed bank depletion during successional series oc-curs predictably through elimination of increasinglypersistent seed banking species (Van Calster et al.2008a; Plue et al. in press). Seed senescence, on theone hand, and inability to replenish the seed bankon the other, thus appear to be the principal driversof post-clear-cut successional seed bank dynamics(Van Calster et al. 2008a; Plue et al. in press). Ad-ditionally, few forest herb layer species invest in apersistent seed bank (Bossuyt & Hermy 2001), yettheir contribution does grow with time (cf. increas-ing stress-tolerance with age, rise in percentage ofancient forest species (Fig. 2d and g; Bossuyt et al.2002; Plue et al. in press).
Nevertheless, comparing these findings to the pri-mary forest seed bank of Bialowieza forest (Poland)(4500 yr; Fig. 2) reveals a big contrast with thesuccessional ancient forest series, very similar to thefindings of another unique study in a tract of remnantprimary deciduous forest in Quebec, Canada (Leckieet al. 2000). Although only in the highest soil pHcategory (Fig. 2) plots in the natural forest of Bialo-wieza contain considerably more species than theoldest managed ancient forest stands (Fig. 2a) (Jan-kowska-Blaszczuk & Grubb 1997; Leckie et al. 2000).Including the considerably larger seed weight (Fig. 2g)and the larger share of ancient forest species (ca. 30%on average; Fig. 2e) likely responsible for the increasedspecies richness, the ecological seed bank profile – i.e.the collection of all seed bank characteristics – in aprimary forest seems to be quite different from theobserved seed bank profile in managed ancient forest(Leckie et al. 2000). Could the lack of steady-statecanopy conditions be responsible for this observation?Possibly, as the unpredictable temporal and spatialcanopy gaps, characteristic of steady-state canopyconditions, seem most adequately colonized by early-successional species via a persistent seed bank. Hence,early-successional, light-demanding species (4500yr;Fig. 2j) occupy their own narrow niche in naturaltemperate forests. Yet, the large share of ancient forestspecies in these primary forests (ca. 30%; Fig. 2e), alsorecorded and thought to be quite exceptional byLeckie et al. (2000), does not fit common theories,which consider ancient forest species do not need, andtherefore do not form, a significant persistent seedbank (Hermy & Verheyen 2007). However, the shift-ing mosaic pattern of the forest canopy locally allowsmore light to filter through, triggering enhanced
population fitness and growth (Valverde & Silvertown1998; Van Calster et al. 2008b). As a result, typicalforest species may produce larger amounts of moreviable seeds, being either more likely to persist or morelikely to be retrieved via sampling. In any case, thishypothesis, supported by the increased ancient forestspecies seed bank share in a forested series (Bossuytet al. 2002; Plue et al. in press), seems to suggest thatancient forest species do form a small functioning seedbank (Jankowska-Blaszczuk & Grubb 1997; Leckieet al. 2000) as a buffer against temporary adverseenvironmental conditions or stochastic extinctionevents. However, given the 100–150-yr rotation cycles,with succession being set back each time, it remainsdoubtful whether seed banks may return to a statecomparable to that of the primary forest (Duffy &Meier 1992).
Conclusions
Forest seed banks can indeed be considered a‘‘memory’’ of human interference in temperatedeciduous forests (Bakker et al. 1996), and our find-ings suggest that forest seed banks bear the scars ofa former land use and/or forest management for atleast 150 years, mostly irrespective of environmentalconditions. Hence, our results imply that the influ-ence of a former land use does not necessarily dimi-nish as a forest stand matures beyond 50 years(Bossuyt & Hermy 2001).
Inherent to succession, time – a substitute forprocesses such as seed senescence, seed predation,secondary seed dispersal, failed germination and/orchanging input from the herb layer – is anotherimportant determinant of soil seed banks in bothpost-agricultural and post-clear-cut forest succes-sion. Yet temporal effects diverge. Indeed, despitethe same series of detrimental processes experiencedby the soil seed bank in recent and ancient forests,time induces a partial recovery of some seed bankcharacteristics in recent forests, yet it inhibits an-cient forest seed banks from returning to their initialstate in primary forests.
Hence, this study adds to the already substantialbody of literature illustrating the persistent impact thatman has had on the natural environment, and en-courages an increasing awareness among researchersto incorporate land use history into ecological studies,including seed bank studies.
Acknowledgements. J.P. wishes to thank Carol Baskin for
help with collecting American seed traits and Dr. Thomas
Ludemann for sending his paper. Two anonymous refer-
Seed banks in temperate forest succession 975
ees are acknowledged for their constructive critiques,
which significantly improved the manuscript.
References
Bakker, J.P., Bekker, R.M., Poschlod, P., Strykstra, R.J.
& Thompson, K. (1996). Seed banks and seed
dispersal: important topics in restoration ecology.
Acta Botanica Neerlandica 45: 461–490.
Bormann, B.D. & Likens, G.E. (1979). Pattern and process
in a forested ecosystem. Springer-Verlag, New York,
NY, US.
Bossuyt, B. & Hermy, M. (2001). Influence of land use
history on seed banks in European temperate forest
ecosystems: a review. Ecography 24: 225–238.
Bossuyt, B., Heyn, M. & Hermy, M. (2002). Seed bank
and vegetation composition of forest stands of varying
age in Central Belgium: consequences for regeneration
of ancient forest vegetation. Plant Ecology 162: 33–48.
Bossuyt, B., Butaye, J. & Honnay, O. (2006). Seed bank
composition of open and overgrown calcareous
grassland soils – a case study from southern Belgium.
Journal of Environmental Management 79: 364–371.
Brown, A.H.F. & Oosterhuis, L. (1981). The role of buried
seeds in coppicewoods.Biological Conservation 21: 19–38.
Dambrine, E., Dupouey, J.-L., Laut, L., Humbert, L.,
Thinon, M., Beaufils, T. & Richard, H. (2007). Present
forest biodiversity patterns in France related to former
Roman agriculture. Ecology 88: 1430–1439.
Dolle, M. & Schmidt, W. (2009). The relationship between
soil seed bank, above-ground vegetation and disturbance
intensity on old-field successional permanent plots.
Applied Vegetation Science 12: 415–428.
Donelan, M. & Thompson, K. (1980). Distribution of
buried viable seeds along a successional series.
Biological Conservation 17: 297–311.
Dougall, T.A.G. & Dodd, J.C. (1997). A study of species
richness and diversity in seed banks and its use for the
environmental mitigation of a proposed holiday village
development in a coniferized woodland in south-east
England. Biological Conservation 6: 1413–1428.
Duffy, D.C. & Meier, A.J. (1992). Do Appalachian
herbaceous understories ever recover from clear-
cutting? Conservation Biology 6: 196–201.
Dupouey, J.-L., Dambrine, E., Lafitte, J.D. & Moares, C.
(2002). Irreversible impact of past land use on forest
soils and biodiversity. Ecology 83: 2978–2984.
Emborg, J., Christensen, M. & Heilmann-Clausen, J.
(2000). The structural dynamics of Suserup skov, a
near-natural temperate deciduous forest in Denmark.
Forest, Ecology and Management 126: 173–189.
Fenner, M. & Thompson, K. (2005). The ecology of seeds.
Cambridge University Press, Cambridge, UK.
Gleason, H.A. & Cronquist, A. (1991).Manual of vascular
plants of northeastern United States and adjacent
Canada. The New York Botanical Garden Press, New
York, NY, US.
Gotelli, N.J. & Ellison, E.M. (2004). A primer of ecological
statistics. Sinauer Associates Inc., Sunderland,MA,US.
Granstrom, A. (1988). Seed banks at six open and
afforested heathland sites in southern Sweden.
Journal of Applied Ecology 25: 297–306.
Grime, J.P., Hodgson, J.G. &Hunt, R. (2007).Comparative
plant ecology: a functional approach to common British
species. Castlepoint Press, Dalbeattie, UK.
Hautala, H., Tolvanen, A. & Nuortila, C. (2008). Recovery
of pristine boreal forest floor community after selective
removal of understorey, ground and humus layers.
Plant Ecology 194: 273–282.
Hermy, M. & Verheyen, K. (2007). Legacies of the past in
the present-day biodiversity: a review of past land-use
effects on forest plant species composition and
diversity. Ecological Research 22: 361–371.
Hermy, M., Honnay, O., Firbank, L., Grashof-Bokdam,
C. & Lawesson, J.E. (1999). An ecological comparison
between ancient and other forest plant species of
Europe, and the implications for forest conservation.
Biological Conservation 91: 9–22.
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.
Hunt, R., Hodgson, J.H., Thompson, K., Bungener, P.,
Dunnett, N.P. & Askew, A.P. (2004). A new practical
tool for deriving a functional signature for herbaceous
vegetation. Applied Vegetation Science 7: 163–170.
Jankowska-Blaszczuk, M. & Grubb, P.J. (1997). Soil seed
banks in primary and secondary deciduous forest in
Bialowieza, Poland. Seed Science Research 7: 281–292.
Jankowska-Blaszczuk, M. & Grubb, P.J. (2006). Changing
perspectives on the role of the soil seed bank in northern
temperate deciduous forests and in tropical lowland rain
forests: parallels and contrasts. Perspectives in Plant
Ecology, Evolution and Systematics 8: 3–21.
Kalamees, R. & Zobel, M. (1998). Soil seed bank composi-
tion in different successional stages of a species rich
wooded meadow in Laelatu, western Estonia. Acta
Oecologia 19: 175–180.
Kalamees, R. & Zobel, M. (2002). The role of the seed
bank in gap regeneration in a calcareous grassland
community. Ecology 83: 1017–1025.
Kleyer, M., Bekker, R.M., Knevel, I.C., Bakker, J.P.,
Thompson, K., Sonnenschein, M., Poschlod, P., van
Groenendael, J.M., Klimes, L., Klimesova, J., Klotz, S.,
Rusch, G.M., Hermy, M., Adriaens, D., Boedeltje, G.,
Bossuyt, B., Dannemann, A., Endels, P., Goetzenberger,
L., Hodgson, J.G., Jackel, A-K., Kuehn, I., Kunzmann,
D., Ozinga, W.A., Roemermann, C., Stadler, M.,
Schlegelmilch, J., Steendam, H.J., Tackenberg, O.,
Wilmann, B., Cornelissen, J.H.C., Eriksson, O.,
Garnier, E. & Peco, B. (2008). The LEDA traitbase: a
database of life-history traits of the Northwest European
flora. Journal of Ecology 96: 1266–1274.
Lambinon, J., De Langhe, J.-E., Delvosalle, L. &
Duvigneaud, J. (1998). Flora van Belgie, het
Groothertogdom Luxemburg, Noord-Frankrijk en
976 Plue, J. et al.
de aangrenzende gebieden (Pteridofyten en
Spermatofyten). Nationale plantentuin van Belgie,
Brussels, BE. [In Dutch].
Leckie, S., Vellend, M., Bell, G., Waterway, M.J. &
Lechowicz, M.J. (2000). The seed bank in an old-
growth, temperate deciduous forest. Canadian Journal
of Botany 78: 181–192.
Ludemann, T. (1994). Zum Samenvorrat von Waldboden
im Feldberggebiet. Carolinea 52: 45–60.
Marage, D., Rameau, J.C. & Garraud, L. (2006). Soil seed
banks and vegetal succession in the Southern Alps:
effects of historic and ecological factors. Canadian
Journal of Botany 84: 99–111.
Marks, P.L. & Mohler, C.L. (1985). Succession after
elimination of buried seeds from a recently plowed
field. Bulletin of the Torrey Botanical Club 112: 376–382.
Mladenoff, D.J. (1990). The relationship of the soil seed
bank and understorey vegetation in old–growth
northern hardwood-hemlock treefall gaps. Canadian
Journal of Botany 68: 2714–2721.
Naaf, T. & Wulf, M. (2007). Effects of gap size, light and
herbivory on the herb layer vegetation in European
beech forest gaps. Forest, Ecology and Management
224: 141–149.
Oosting, H.J. & Humphreys, M.E. (1940). Buried viable
seeds in a successional series of old field and forest soils.
Bulletin of the Torrey Botanical Club 67: 253–273.
Plue, J., Hermy, M., Verheyen, K., Thuillier, P., Saguez,
R. & Decocq, G. (2008). Persistent changes in forest
vegetation and seed bank 1600 years after human
occupation. Landscape Ecology 23: 673–688.
Plue, J., Dupouey, J.-L., Verheyen, K. &Hermy, M. (2009).
Forest seed banks along an intensity gradient of ancient
agriculture. Seed Science Research 19: 103–114.
Plue, J., Van Gils, B., Peppler-Lisbach, C., De Schrijver, A.,
Verheyen, K. & Hermy, M. (in press). Seed bank
convergence under different tree species during forest
development. Perspectives in Plant Ecology, Evolution
and Systematics, doi: 10.1016/j.ppees.2010.03.001.
Roberts, T.L. & Vankat, J.L. (1991). Floristics of a
chronosequence corresponding to old field deciduous
forest succession in southwestern Ohio. 2. Seed
banks. Bulletin of the Torrey Botanical Club 118:
377–384.
Rydgren, K., Økland, R.H. & Hestmark, G. (2004).
Disturbance severity and community resilience in a
boreal forest. Ecology 85: 1906–1915.
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.
Thompson, K., Bakker, J.P., Bekker, R.M. & Hodgson,
J.G. (1998). Ecological correlates of seed persistence in
soil in the NW European flora. Journal of Ecology 86:
163–169.
Ulrich, B. (1983). Effects of accumulation of air pollutants
in forest ecosystems. Kluwer, NL.
Valverde, T. & Silvertown, J. (1998). Variation in the
demography of a woodland understorey herb (Primula
vulgaris) along the forest regeneration cycle: projection
matrix analysis. Journal of Ecology 86: 545–562.
Van Calster, H., Chevalier, R., Van Wyngene, B., Archaux,
F., Verheyen, K. &HermyM, . (2008a). Long-term seed
bank dynamics in a temperate forest under conversion
from coppice-with-standards to high forest manage-
ment. Applied Vegetation Science 11: 251–260.
Van Calster, H., Endels, P., Antonio, K., Verheyen, K. &
Hermy, M. (2008b). Coppice management effects on
experimentally established populations of three
herbaceous layer woodland species. Biological
Conservation 141: 2641–2652.
Vellend, M., Verheyen, K., Flinn, K.M., Jacquemyn, H.,
Kolb, A., Van Calster, H., Peterken, G., Graae, B.J.,
Bellemare, J., Honnay, O., Brunet, J., Wulf, M.,
Gerhardt, F. & Hermy, M. (2007). Homogenization
of forest plant communities and weakening of species–
environment relationships via agricultural land use.
Journal of Ecology 95: 565–573.
Verheyen, K., Honnay, O., Motzkin, G., Hermy, M. &
Foster, D.R. (2003). Response of forest plant species
to land-use change: a life-history trait-based approach.
Journal of Ecology 91: 563–577.
Warr, J.S., Kent, M. & Thompson, K. (1994). Seed bank
composition and variability in five woodlands in south-
west England. Journal of Biogeography 21: 151–168.
Supporting Information
Additional supporting information may befound in the online version of this article:
Appendix S1. Sampling and germination proto-cols applied by the various studies.
Appendix S2. Extensions of Tables 2 and 3,showing the main effect of the random/fixed factor lo-cation in the linear mixed models/generalized linearmodels.
Appendix S3. Boxplots illustrating the fixed effectof pH during post-agricultural succession on seedbank characteristics: (a) species richness, (c) seeddensity without Juncus effusus, (d) the competitive, (e)stress-tolerant and (f) ruderal seed bank signature, (g)percentage of ancient forest species, (h) average seedweight, (i) the Raup and Crick vegetation–seed bankdissimilarity and (j) the percentage of annuals andbiennials in the seed bank.
Photo S1. Seedling of Potentilla sterilis (L.)Garcke. A typical ancient forest species (sensu Hermyet al. 1999) with the capacity to build up a persistentseed bank. Potentilla sterilis (L.) Garcke wasrecovered in several seed bank studies, such as VanCalster et al. (2007), Plue et al. (in press), and con-tributes to the overall rise in ancient forest species
Seed banks in temperate forest succession 977
with time since the last disturbance in managedtemperate deciduous forest.
Photo S2. Seedling of Gnaphalium sylvaticum L.A typical early-successional forest species appearingon forest clear-cuts and forest road verges, withthe capacity to build up an apparently long-termpersistent seed bank. Gnaphalium sylvaticumwas recovered in several seed bank studies, such asLudemann (1994), Van Calster et al. (2007) andPlue et al. (in press), and may be considered a speciesthat seems adequately adapted to the naturaldisturbance regime in temperate deciduous forest,
occupying its own narrow temporal niche in forestsuccession.
Please note: Wiley-Blackwell is not responsiblefor the content or functionality of any supportingmaterials supplied by the authors. Any queries(other than missing material) should be directed tothe corresponding author for the article.
Received 15 December 2009;
Accepted 26 May 2010.
Co-ordinating Editor: Dr. Martin Zobel.
978 Plue, J. et al.