Effect of tree mixture on the humic epipedon andvegetation diversity in managed beech forests(Normandy, France)

Michaël Aubert, Fabrice Bureau, Didier Alard, and Jacques Bardat

Abstract: Using a space-for-time substitution procedure, we assessed the patterns of variation during stand develop-ment of the humic epipedon and vegetation diversity in a pure European beech (Fagus sylvatica L.) forest and in amixed beech–hornbeam (Carpinus betulus L.) forest. The humic epipedon was investigated through macromorpho-logical characteristics (thickness of the OL, OF, OH, and A horizons) and pH measurements (pHKCl, pHH O2

, and ∆pH).Vegetation diversity was assessed using correspondence analysis and hierarchical cluster analysis to identify the mainplant community succession groups. The groups were compared using three diversity measures (species richness, Shan-non index, and evenness index) and three indices describing the community composition (similarity index betweenstands and index of heterogeneity at the stand and herbaceous layer levels). The pH measurements revealed an acidifi-cation of the A horizon during pure beech stand maturation. Macromorphological characteristics showed an alternationof an organic matter accumulation phase and organic matter disappearance along the two silvicultural cycles. Vegeta-tion diversity measures showed small differences between the two forests. Indices accounting for community composi-tion revealed a homogenizing effect of the pure beech silvicultural type on species composition of plant communitiesoccurring during stand development. They also revealed a strong heterogeneity at the herbaceous level. Comparison ofspecies composition indicated an increasing occurrence of acidophilous species in the pure beech forest. We discuss theinterest of these results for future sustainable management decisions.

Résumé : Au moyen d’une approche synchronique, nous avons observé la variabilité de l’épisolum humifère et de ladiversité végétale dans une hêtraie (Fagus sylvatica L.) pure et une hêtraie–charmaie (Carpinus betulus L.). L’épisolumhumifère a été décrit à l’aide de variables morphologiques (épaisseurs des horizons OL, OF, OH et A) et chimiques(pHKCl, pHH O2

et ∆pH). La diversité végétale fut appréhendée au moyen d’une analyse factorielle des correspondancesassociée à une classification ascendante hiérarchique afin de caractériser les principales communautés de plantes se suc-cédant au cours des cycles sylvicoles. Les groupes furent comparés à l’aide de trois mesures de diversité (richesse spé-cifique, indices de Shannon et indice d’équitabilité) et trois indices rendant compte de la composition des communautés(indice de similarité et indices d’hétérogénéité à l’échelle du peuplement et à l’échelle de la strate herbacée). L’étudede l’épisolum humifère montre l’alternance de phases d’accumulation et d’incorporation de la matière organique dansles deux forêts ainsi qu’une acidification de l’horizon A au cours de la maturation des peuplements purs. Les patronsde variation de la diversité floristique sont sensiblement équivalents pour les deux forêts. La composition spécifique descommunautés végétales se succédant au cours du cycle sylvicole de la hêtraie pure varie peu. Les indices rendantcompte de la composition des communautés indiquent également une très forte hétérogénéité à l’échelle de la strateherbacée pour les deux forêts. La comparaison de la composition floristique révèle une plus forte occurrence des espè-ces acidiphiles dans la hêtraie pure. L’intérêt de ces résultats pour l’élaboration de règles de gestion sylvicole durableest discuté.

Aubert et al. 248Introduction

In the current debate on the relationships betweenbiodiversity preservation and sustainable ecosystem manage-ment, it is largely recognized that management and harvest-

ing practices have a negative impact on the organization, di-versity, and functioning of managed forests (Bo Larsen1995; Gilliam and Roberts 1995; Graae and Heskjaer 1997).Concerning temperate beech forests, the main criticisms area simplification of the stand vertical structure, a modifica-

Can. J. For. Res. 34: 233–248 (2004) doi: 10.1139/X03-205 © 2004 NRC Canada

233

Received 13 August 2002. Accepted 28 August 2003. Published on the NRC Research Press Web site at http://cjfr.nrc.ca on30 January 2004.

M. Aubert and F. Bureau.1 Université de Rouen, Laboratoire d’Écologie, Unité Propre de Recherche et d’Enseignement - Équiped’Accueil 1293, F-76821 Mont Saint Aignan CEDEX, France.D. Alard. Institut National de la Recherche Agronomique, Toulouse, Unité Mixte de Recherche-1201 DYNAFOR, B.P. 27, F-31326Castanet Tolosan CEDEX, France.J. Bardat. Muséum National d’Histoire Naturelle, Institut d’Écologie et de Gestion de la Biodiversité, 57, rue Cuvier, F-75231Paris CEDEX 05, France.

1Corresponding author (e-mail: Fabrice.Bureau@univ-rouen.fr).

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tion of the forest cycle by truncating succession before thelate biostatic phase (Christensen and Emborg 1996), and or-ganic matter accumulation resulting in topsoil acidification(Cochet 1977). As beech is considered to be a late-successional species, forestry based on planted beechmonoculture does not also allow the expression of early-successional tree species in young phases (Carbiener 1991).Thus, the absence of early-successional species throughoutthe forest cycle could potentially mean the loss of functionalgroups, which may alter the ecosystem functioning in thelong term.

In Upper-Normandy (France), beech forests developed onloamy soil are mainly managed as monospecific even-agedforests. Under this kind of forest, Brêthes (1984) reportedthe systematic development of moder humus forms as a re-sult of the triple effect of the poor litter quality of beech, theAtlantic climate, and the acidic parent rock. This humus ho-mogenization leads to an impoverishment of forest floracaused by topsoil acidification. In a previous study on the di-versity of plant communities in an even-aged pure beech for-est in Upper-Normandy (Aubert et al. 2003), we reported thedevelopment of a moder humus form under a mature standwith closed canopy, confirming Brêthes (1984) findings.

In this study, we compare the same even-aged pure Euro-pean beech (Fagus sylvatica L.) forest with a mixed beech–hornbeam (Carpinus betulus L.) forest at the stand level. Incontrast with beech, hornbeam is an early-successional spe-cies (Koop and Hilgen 1987) with a soil-improving litter,i.e., characterized by a low C/N ratio (Mangenot and Toutain1980). Thus, it stimulates the biological activity of thehumic epipedon and increases litter decomposition rates(Duchaufour 1997; Gobat et al. 1998). This study aimed atassessing the consequences of the presence of hornbeamwithin a beech-dominated stand on (i) the humic epipedon(“episolum humifère” according to the French classificationof AFES (1998)) and (ii) plant communities along thesilvicultural cycle. Throughout a beech-dominated stand ro-tation, we assume that the only presence of an early-successional mull-forming species (such as hornbeam) couldreduce the negative impact of beech monoculture by improv-ing decomposition processes and thereby diversity of herba-ceous plant assemblages.

Materials and methods

We used a space-for-time substitution (SFTS) procedureadded to multivariate and cluster analysis. This approach al-lows us to elaborate an empirical silvicultural cycle of thepure and mixed forests. Silvicultural or harvesting practicesmay strongly influence plant community composition(Becker 1979; Deconchat and Balent 2001). We first identi-fied the main floristic gradients structuring plant communi-ties during stand development with a correspondenceanalysis (CA) and checked their similarity throughout thepure and the mixed forest cycle. The intensity of thinningoperations can vary between stands of the same age. Thiscan lead to the occurrence of different species assemblageswithin two stands exhibiting the same age. So, the character-ization of dynamic stages was based on the similarity ofstand species composition and not on their age. This wasdone with a cluster analysis performed on stand scores pro-

vided by the CA. Thus, for each stage (for both forests), wecompared the humic epipedon and the diversity of plant as-semblages.

Study sitesOur research was conducted in the state forests of Eawy

(pure beech forest) and Lyons (mixed beech–hornbeam for-est) located in Upper-Normandy in northern France. Themean annual precipitation and temperature are 800 mm and10 °C, respectively (Brêthes 1984). The French NationalForestry Office manages the two forests. Timber harvestingis their most important output. They have been managed aseven-aged beech forest since 1830 for Eawy and since 1856for Lyons. The silvicultural cycle occurs on a 170-year basis(see Aubert et al. (2003) and Lanier (1994) for details abouteven-aged forest management). The differences between thepure and mixed forests are as follows. (i) Eawy stands aremonospecific, while hornbeam occurs at a low abundance(30% in young stands to 1% in regeneration ones) in Lyonsstands (Table 1). (ii) All Eawy stands come from artificialplantations, while those of Lyons come from natural regen-eration. (iii) In regeneration stands at Eawy, the soil is pre-pared by mechanically scraping the superficial layers, andherbicides are used to facilitate the regeneration process andlimit herbaceous competition. At Lyons, the regenerationcategory is composed of old stands intended as a regenera-tion phase before the December 1999 windstorm. Except forwindfall harvest, no site preparation has been performed.

Thirty-seven stands (Table 1) were selected in the twoforests to reconstitute the silvicultural cycle. According toSamuels and Drake (1997), communities that develop undersimilar environmental conditions are likely to converge to asimilar structure. Nonetheless, historical differences (Samuelsand Drake 1997) or changes in disturbance regime (Alardand Poudevigne 2002) can lead to successional divergence.Thus, the sampling procedure was designed so that suc-cessional changes and stand management were the mainfactors explaining the recorded variations in vegetation andhumic epipedon. Three precautions were taken as follows.(i) According to the phytosociological classification of Durinet al. (1967), all stands belong to the Endymio–Fagetum.(ii) All stands were characterized by the same parent materi-als (loess >60 cm thick lying on clay with flints) and thesame topographic position (plateau). From previous workconducted in this region (Lautridou 1985), the plateauloesses are lamellated silts in both forests. Moreover, bothare situated on the same type of clay with flints (Laignel etal. 1998, 1999). In each forest, physicochemical analyseswere performed on the soil profile in one stand. These haveconfirmed the similarity of the silt and clay quality in bothforests (F. Bureau and M. Aubert, unpublished data). (iii) Allthe soils were Luvisols according to the “Référentiel pédo-logique” (AFES 1998) and were equivalent to Luvisols inthe world reference base (FAO et al. 1998).

Soil samplingSoil characteristics were assessed through a description of

the humic epipedon corresponding to “épisolum humifère”,defined as the sequence of organic horizons (O horizons)and organomineral horizon (A horizon) (AFES 1998). Thisprovides an indicative value of nutrient availability and or-

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234 Can. J. For. Res. Vol. 34, 2004

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ganic matter turnover in forested ecosystems (Duchaufour1997; Ponge et al. 1998).

Soil cores were obtained with an auger in the 400-m2

plots situated at the centre of the sampling design (Fig. 1) tocheck the type of soil and the loess layer thickness. Humusform characteristics were sampled near the centre of each400-m2 vegetation plot. Sampling sites were selected so thatthey were not disturbed by traffic (no vehicle tracks) andwere situated as far as possible from tree trunks to avoid or-ganic matter accumulation and acidification (Beniamino etal. 1991). The macroscopic morphological characteristics ofhumus forms (sensu AFES 1998) recorded were the depth ofthe OL, OF, and OH organic horizons and the depth of theorganomineral A horizon. This horizon nomenclature corre-sponds to U.S. Department of Agriculture nomenclature asfollows: OL is Oi, OF is Oe, and OH is Oa. The pHKCl and

pHH O2of the A horizon were measured at the laboratory

(1:2.5 soil–liquid mixture) with a 1 M KCl solution and dis-tilled water, respectively. ∆pH (∆pH = pHH O2

– pHKCl) wasdetermined. For a given soil type, this index is positivelycorrelated with exchangeable acidity (Baize 1988).

Vegetation samplingIn each stand, five 20 m × 20 m (400 m2) plots and twelve

2 m × 2 m (4 m2) quadrats were used for vegetation record-ing (Fig. 1). They were considered to be of a suitable sizefor describing stand-scale and fine-scale vegetation hetero-geneity. Plots and quadrats were systematically located inthe stands according to a constant design. For each 400-m2

plot, a floristic inventory was performed for four vegetationstrata according to plant species height at time of sampling:(i) the herb stratum (plants <0.5 m height including seed-

© 2004 NRC Canada

Aubert et al. 235

StandAge of stand(years) Last year cut

Silviculturalphase

Hornbeam(%)

PureP1 25 1998 CleaningP2 25 1997 First thinningP3 27 1996 First thinningP4 31 1996 First thinningP5 58 1997 AmeliorationP6 58 1997 AmeliorationP7 62 1998 AmeliorationP8 114 1992 AmeliorationP9 115 1995 AmeliorationP10 120 1995 AmeliorationP11 133 1994 AmeliorationP12 133 1994 AmeliorationP13 133 1995 AmeliorationP14 144 1997 AmeliorationP15 176 1991 AmeliorationP16 174 1996 AmeliorationP17 179 1998 RegenerationP18 179 1998 RegenerationP19 194 1997 RegenerationP20 194 1997 Regeneration

MixedM1 24 1993 Amelioration 10M2 28 1999 Amelioration 30M3 40 1997 Amelioration 20M4 45 1992 Amelioration 30M5 52 1992 Amelioration 20M6 71 1990 Amelioration 30M7 82 1994 Amelioration 10M8 86 1994 Amelioration 15M9 92 1990 Amelioration 16M10 112 1998 Amelioration 11M11 114 1990 Amelioration 5M12 141 1995 Amelioration 5M13 142 1991 Amelioration 3M14 148 1990 Amelioration 3M15 182 Windthrow (1999) Regeneration 3M16 195 Windthrow (1999) Regeneration 1

Table 1. Description of the 37 stands (20 pure European beech stands and 17 mixedbeech–hornbeam stands).

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lings of tree and shrub species), (ii) small shrub stratum(0.5–2 m), (iii) shrub stratum (2–8 m), and (iv) tree stratum(>8 m). The cover of all vascular plant species was esti-mated using a seven-point scale: i = species represented byonly one individual, + = species with a very small cover, 1 =species with a cover of <5%, 2 = 5%–25%, 3 = 25%–50%,4 = 50%–75%, and 5 = 75%–100%. As well, the total per-centage cover of each stratum was estimated. For everystand, an overall inventory was made by listing all speciesrecorded in the five 400-m2 plots and attributing to them anaverage abundance and dominance score. On the 4-m2 vege-tation quadrats, a floristic inventory was performed usingpresence–absence data. Nomenclature of species followsLambinon et al. (1992). The 37 stands comprised a total of185 (400 m2) plots and 444 (4 m2) quadrats that were sur-veyed in May and June 1999 for pure Eawy stands, June2000 for Lyons mixed stands, and July 2001 for Lyons re-generation stands.

Data analysisVegetation records of pure and mixed stands were first

analysed with CA and hierarchical clustering (Roux 1991) toidentify the floristic gradients and interpret the ecologicalfactors structuring species assemblages with the help of aut-ecological species data from Grime et al. (1988), Rameau et

al. (1989), and Brêthes (1984) and to reconstruct the empiri-cal silvicultural cycle and identify the successional stages.Subsequently, the stages were compared to examine the suc-cessional changes and the effect of canopy composition onthe diversity pattern of plant assemblages and humicepipedon characteristics.

CAs were performed on pure (CA1: 20 stands × 99 spe-cies) and mixed (CA2: 17 stands × 94 species) stands usingADE software (Thioulouse et al. 1997) to check the equiva-lence of ecological factors structuring species assemblages.Prior to the analysis, species found in less than 3% of standswere removed from the data set. Hierarchical clustering wasperformed on stand CA scores on the two first axes (Roche1994; Roux 1985) using Ward’s (1963) method to identifyclusters, i.e., groups of stands that are characterized by simi-lar species assemblages.

For the different stands, six different measures of diversitywere investigated.

� Diversity (species richness (SR))This refers to the number of species within a given habitat

or quadrat (Palmer 1990). It was calculated from the numberof species recorded in the four vegetation strata: herbs, smallshrubs, shrubs, and the tree stratum.

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236 Can. J. For. Res. Vol. 34, 2004

Fig. 1. Sampling design used for description of vegetation and soil characteristics. The letters C, N, S, E, and W correspond to thefive 400-m2 plots used for both vegetation and humic epipedon sampling. The numbers 1–12 correspond to the 4-m2 quadrats used forvegetation records.

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Shannon diversity index (H′)This takes into account the variation in species abundance

within a given record (Pielou 1975; Blondel 1995):

H p pii

i′ ==∑

12

SR

log

where pi is the relative frequency of species i in a plot andpi = ni/∑ni where ni is the percentage cover of species i in aplot.

Evenness index (J′)This reflects the relative dominance of species within a

given record (Smith and Wilson 1996).

JH

H

H

′ = ′′

′ =max

max log2 SR

Similarity index (SI)Pairwise similarities among all stands were determined

using the Jaccard (1901) index and mean similarities foreach successional group of stands were computed (Scheiner1992; Alard and Poudevigne 2000):

Jaccard Index =+ −

ca b c( )

where c is the number of species shared between a pair ofstands and a and b are the total number of species occurringin the two stands.

Medium-scale heterogeneity (MSH)Pairwise similarities among all five 400-m2 plots of a

given stand were determined using the Jaccard index andmean plot-level similarity for the stand was computed.

Fine-scale heterogeneity (FSH)Pairwise similarities among all twelve 4-m2 quadrats of a

given stand were determined using the Jaccard index andmean quadrat-level similarity for the stand was computed.

For each cluster, the mean and standard error of each di-versity and similarity index and the soil variables were com-puted. Conformity with a normal distribution was testedusing a Wilk–Shapiro test at the significance level of p =0.05. When necessary, a logarithmic transformation was per-formed to homogenize the variance. To evaluate the effectsof succession on diversity pattern and humus form character-istics, we used a Tukey HSD test (significant level of p =0.05) to test the difference between means of clusters be-longing to each forest. One-way ANOVA was used to testthe effect of silvicultural treatment between clusters belong-ing to the equivalent successional stage in the two foresttypes. Tukey HSD tests and ANOVAs were performed at theplot scale (400 m2). These statistical analyses were per-formed with STATISTIX software (Statistix 1998).

Results

Floristic gradients and silvicultural dynamicsThe two CAs indicated that the major factors structuring

plant communities were similar along the silvicultural cycleof both pure and mixed forests.

For the pure beech stands (CA1, Fig. 2), the total inertiawas 1.65, and the first four eigenvalues (and associated rela-tive inertias) were 0.54 (32.77%), 0.34 (20.84%), 0.15(9.14%), and 0.14 (8.25%). The small eigenvalues and lowinformation provided by axes 3 and 4 allowed us to interpretonly the first two axes. The ordination diagrams show thataxis 1 separated woody species belonging to the shrub stra-tum (Fagus sylvatica 2) from those belonging to the treestratum (Fagus sylvatica 1, Quercus robur 1), suggestingthat this axis may be related to a gradient of stand matura-tion. Axis 2 distinguished a group of stands characterized bysciaphilous (i.e., shade-tolerant) species (Galium odoratum,Hyacinthoides non-scripta, Circaea lutetiana) from a groupcharacterized by heliophilous (i.e., shade-intolerant) species(Teucrium scorodonia, Calamagrostis epigejos, Lotus uligino-sus). This axis may be interpreted as a canopy-opening gra-dient.

For the mixed beech–hornbeam stands (CA2, Fig. 3), thetotal inertia was 1.90, and the first four eigenvalues (and cor-responding relative inertias) were 0.50 (26.52%), 0.44(23.19%), 0.21 (11.23%), and 0.15 (8.15%). As for CA1, thesmall eigenvalues and presumably low information providedby axes 3 and 4 allowed us to interpret only the two firstaxes. Axis 1 opposed species belonging to the shrub stratum(Quercus robur 2, Acer pseudoplatanus 2, Fagus sylvatica 2)to those belonging to the tree stratum (Acer pseudoplatanus1, Fagus sylvatica 1, Carpinus betulus 1). As with axis 1 ofCA1, it reflected a gradient of stand maturation. Axis 2 sepa-rated shade-tolerant species (Melica uniflora, Polygonatummultiflorum, Hedera helix) from shade-intolerant species(Epilobium angustifolium, Senecio erucifolius, Digitalis pur-purea). As for CA1, this axis reflected a gradient of canopyopening.

Hierarchical clustering performed on CA1 (Fig. 2) andCA2 (Fig. 3) plot scores distinguished five groups of standscharacteristic of five successional stages for each forest.These groups ranged from young stands (PI, MI) to oldstands (PIII, PIV, PV, MIII, MIV, MV) and from stands witha high canopy cover (PIII, MIII) to regeneration stands (PV,MV).

The humic epipedon

Relationships with silvicultural dynamicsThe normality of the different variables was checked us-

ing a Wilk–Shapiro test. Except for OF and OH thickness,all variables had a normal distribution (p > 0.05). After loga-rithmic transformation, only OH thickness did not reach nor-mality. Nevertheless, the transformed values were still usedto perform the Tukey HSD test and one-way ANOVA.

During the silvicultural cycle of the pure beech forest, themacromorphological characteristics of humus form indicatedthat regeneration stands were significantly different from theothers (Table 2). The lower OL, OF, and OH thicknessshowed by this stand group indicated the development of amull phase during this successional stage. Total litter thick-ness did not vary significantly between the other groups, butthe thickness of the OL horizon was significantly higher inPI than in PII–PIV. In addition, the greater OH thickness inold mature stands with open canopy (PIV), added to a thin Ahorizon, indicated that a moder phase developed when thestand became older. Stand maturation of pure beech forest

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238 Can. J. For. Res. Vol. 34, 2004

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was associated with a significant acidification of the organo-mineral horizon. The pHH 02

values were lowest in PII–PIVand highest in young and regeneration stands.

In the mixed beech–hornbeam forest, the A horizon thick-ness did not vary significantly along the silvicultural cycle.The Tukey HSD test revealed two kinds of stands, youngand regeneration stands (MI–MV), which had a significantlylower total litter thickness, and the other stands. Among thelatter category, old mature stands (MIV) had the highest OHthickness. These differences between stand groups indicatemechanisms of litter accumulation during stand maturation(development of moder humus forms) and of litter disap-pearance during the regeneration phase (development ofmull humus forms). Except for ∆pH, which was lowest inyoung stands, the other pH measurements did not vary sig-nificantly between the different clusters. Stand maturationwas not associated with any acidification of the A horizon.

Comparisons of pure and mixed forestsYoung pure beech stands had a significantly higher total

litter (p < 0.001), OL thickness (p < 0.001), and OF (p <0.001) thickness than young mixed stands (Fig. 4). The op-posite trend was observed in regeneration stands (p < 0.05).The thickness of the A horizon was greater in pure standsthan in mixed stands (p < 0.01 for PIV, p < 0.001 for theothers). Pure mature stands with a closed canopy (PIII)showed a higher OH layer thickness than mixed ones (MIII)(p < 0.01).

Strong pH differences were observed between pure andmixed forest stands. Except for regeneration stands, wheremeans were not significantly different, pHH O2

and pHKClwere higher in mixed stands than in pure stands (p < 0.01 orp < 0.001). In the same way, the exchangeable acidity (∆pH)was greater under pure stands than under mixed ones (p <0.01 or p < 0.001) except for PII and PIV.

Diversity of plant assemblages

Relationships with silvicultural dynamicsAll diversity measures had a normal distribution (Wilk–

Shapiro test, p > 0.05). The three indices accounting forcommunity similarity (SI, MSH, FSH) did not show signifi-cant variations between successional stages for either forest(Table 3). Nonetheless, the nested sampling scales revealed a

higher heterogeneity at the herbaceous scale (FSH) than atthe stand level (MSH).

In the pure beech forest, young plantations and regenera-tion stands had a significantly higher SR than old standswith a closed canopy (PIII). PII and PIV had intermediateSR values. The H′ reached its highest values in old standswith an open canopy and its lowest in young plantations andold closed stands. Three groups were identified on the basisof significant differences in J′ values: highest mean values inold stands with an open canopy, lowest values in youngstands, and intermediate values in PII and PIII.

In the mixed beech–hornbeam forest, regeneration standshad significantly higher SR than the other old stands, whileyoung stands exhibited intermediate mean values. The H′and J′ showed the same pattern of variations. They con-trasted MI and MIII with a low diversity and strong domi-nance of some species from MII, MIV, and MV.

Comparisons of pure and mixed forestsFor SR, MSH, and FSH (Fig. 5), no significant differences

were observed between the two forests. MII exhibited higherH′ (p = 0.022) and J′ (p = 0.007) than PII, whereas PIII,PIV, and PV had a significantly higher SI than did MIII,MIV, and MV (p < 0.001, p < 0.05, and p < 0.01, respec-tively). Although the diversity indices showed small differ-ences between the two silvicultural practices, the speciescomposition of pure stands seemed to show a tendency to in-clude more acidophilous species (see Appendix Table A1) inaccordance with the ecological groups of Brêthes (1984).

Discussion

The SFTS procedure and the silvicultural cycleTo reconstitute empirically a silvicultural cycle, we used

the SFTS procedure combined with multivariate analysis.The main criticism of such a procedure is that ecologistscannot be in control of all environmental parameters for allstudied stands, as can be the case for laboratory experiments.Caution must be taken when interpreting the axes of multi-variate analyses to avoid confusion between environmentalgradients and temporal gradients. In our study, the samplingprocedure was designed so that differences between the twoecosystems were mainly the result of stand canopy composi-

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240 Can. J. For. Res. Vol. 34, 2004

ClusterO thickness(cm)

OL thickness(cm)

OF thickness(cm)

OH thickness(cm)

A thickness(cm) A pHH O2 A pHKCl ∆pH

PI 3.95 (0.82)a 2.3 (0.42)a 1.55 (0.55)a 0.1 (0)b 5.12 (1.42)a 3.86 (0.23)a 2.78 (0.16)b 1.08 (0.18)aPII 2.79 (0.74)a 1.53 (0.67)b 1.21 (0.43)a 0.12 (0.06)b 3.68 (2.17)a 3.63 (0.18)b 2.85 (0.22)b 0.78 (0.21)bPIII 3.25 (1.24)a 1.62 (0.68)b 1.5 (0.87)a 0.26 (0.39)b 1.94 (1.77)b 3.66 (0.15)b 2.79 (0.21)b 0.86 (0.19)bPIV 3.24 (1.14)a 1.43 (0.6)b 1.33 (0.76)a 0.48 (0.4)a 2.29 (1.97)b 3.68 (0.18)b 2.84 (0.22)b 0.84 (0.2)bPV 1 (0.49)b 0.53 (0.23)c 0.45 (0.4)b 0.02 (0.04)b 3.15 (1.2)ab 4.03 (0.16)a 3.12 (0.26)a 0.9 (0.14)abMI 1.74 (0.53)b 1.11 (0.57)bc 0.51 (0.29)b 0.12 (0.13)b 0.62 (0.3) 3.92 (0.32) 3.34 (0.31) 0.58 (0.08)bMII 2.94 (0.58)a 2.04 (0.56)a 0.82 (0.34)ab 0.08 (0.09)b 0.71 (0.29) 3.94 (0.22) 3.19 (0.16) 0.76 (0.11)aMIII 2.58 (0.7)a 1.58 (0.56)ab 0.89 (0.32)a 0.1 (0.1)b 0.73 (0.35) 3.97 (0.3) 3.25 (0.29) 0.73 (0.13)aMIV 3.09 (0.8)a 1.58 (0.62)ab 1.2 (0.73)a 0.32 (0.17)a 0.61 (0.33) 3.87 (0.26) 3.13 (0.25) 0.74 (0.13)aMV 1.66 (0.74)b 0.89 (0.49)c 0.72 (0.42)ab 0.05 (0.08)b 0.89 (0.65) 4.02 (0.26) 3.28 (0.25) 0.73 (0.12)a

Note: Data are mean and standard error (in parentheses) of organic horizon thickness (total litter thickness O, OL, OF, and OH), organomineral horizon(A) thickness, and pH measures (pH H O2

, pHKCl, and ∆pH). Different letters indicate significant differences between clusters for each forest type at p =0.05 (Tukey HSD test).

Table 2. Pattern of variations of humic epipedon along the silvicultural cycle of the pure European beech and mixed beech–hornbeam forests.

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tion: the climate, parent rock, and forestry practices weresimilar; however, a bias may still exist in stand history. Nev-ertheless, because of the long duration of the forest cycle,the SFTS procedure appears to be the only way to assesstemporal changes in vegetation composition and diversity.

The results revealed that species turnover along the silvi-cultural cycle was similar for both pure beech and mixedbeech–hornbeam forests. Stand maturation (i.e., canopy de-velopment and closure) and canopy opening are the maingradients structuring species assemblages. This supports thegeneral model of Bormann and Likens (1979) of vegetationdevelopment during secondary forest succession.

The humic epipedonDuring the past decade, the occurrence of similar changes

in vegetation and humic epipedon throughout the life cycleof forest ecosystems has been demonstrated (Arpin et al.1998). More precisely, studies by Bernier and Ponge (1994)in a mountain spruce forest (France) and Ponge and Delhaye(1995) in a natural beech forest (Northern France) haveshown an alternation between phases of accumulation (i.e.,moder phase) and incorporation (i.e., mull phase) of litter.

The present results also indicate that changes occur in hu-mus form during silvicultural cycles of pure and mixed for-ests. The humic epipedon exhibited similar patterns of

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Fig. 4. Comparisons of humic epipedon characteristics between pure European beech and mixed beech–hornbeam forest. I–V correspondto the successional stages. Significant differences (one-way ANOVA): *, p < 0.05; **, p < 0.01; ***, p < 0.001; ns, not significant.

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242 Can. J. For. Res. Vol. 34, 2004

Clusters SR H′ J′ FSH MSH SI

PI 38.5 (3.54)a 1.81 (0.42)c 0.34 (0.07)c 0.40 (0.05) 0.44 (0.04) 0.57 (0.02)PII 47.67 (2.52)ab 3.06 (0.19)b 0.55 (0.03)b 0.21 (0.02) 0.48 (0.08) 0.57 (0.07)PIII 36.4 (5.03)b 2.69 (0.25)c 0.52 (0.06)b 0.34 (0.1) 0.55 (0.06) 0.56 (0.02)PIV 45.65 (8.98)ab 3.87 (0.5)a 0.70 (0.07)a 0.32 (0.07) 0.56 (0.05) 0.56 (0.02)PV 57.5 (2.12)a 4.52 (0.07)a 0.77 (0.01)a 0.29 (0) 0.51 (0) 0.50 (0.04)MI 41 (7.07)ab 2.73 (0.59)b 0.51 (0.09)b 0.22 (0.1) 0.54 (0.1) 0.41 (0.02)MII 43.5 (4.95)ab 3.69 (0.09)a 0.68 (0)a 0.33 (0.19) 0.48 (0.05) 0.44 (0)MIII 32.57 (6.24)b 2.67 (0.16)b 0.53 (0.03)b 0.39 (0.06) 0.51 (0.07) 0.46 (0.02)MIV 36.33 (11.50)b 3.63 (0.36)a 0.71 (0.02)a 0.39 (0.05) 0.54 (0.02) 0.43 (0.09)MV 57 (1.73)a 3.93 (0.31)a 0.67 (0.06)a 0.33 (0.07) 0.49 (0.02) 0.37 (0.02)

Note: Data are mean and standard error (in parentheses) of species richness (SR), Shannon index (H′), evenness in-dex (J′), fine-scale heterogeneity (FSH), medium-scale heterogeneity (MSH), and similarity index (SI). Different lettersindicate significant differences between clusters for each forest type at p = 0.05 (Tukey HSD test).

Table 3. Patterns of variation of diversity and similarity indices for plant communities (clusters) alongthe silvicultural cycle of the pure European beech and mixed beech–hornbeam forests.

Fig. 5. Comparisons of diversity indices between pure European beech and mixed beech–hornbeam forest. I–V correspond to thesuccessional stages. FSH, fine-scale heterogeneity; MSH, medium-scale heterogeneity. Significant differences (one-way ANOVA): *,p < 0.05; **, p < 0.01; ***, p < 0.001; ns, not significant.

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changes during the mixed forest and pure forest cycles. Bothreveal the development of moder humus forms (OH devel-opment) during the amelioration phase. Moder developmentreflects a low rate of organic matter incorporation (Brêtheset al. 1995). But the higher OH thickness in the pure maturestand with a closed canopy (PIII) than in mixed ones (MIII)indicates that decomposition processes are slower in purebeech forest.

The morphological description of humus profiles indicatesthat the mull humus form characterizes the regenerationphase (low litter thickness and thicker A horizon than otherold stands). The regeneration phase is characterized by amore open canopy, with lower amounts of litterfall. We as-sume that the occurrence of mull humus forms in the regen-eration phase is due to the lower litterfall and the activationof organic matter mineralization resulting from canopy thin-ning (Duchaufour 1997) rather than from macroinvertebrateactivity (mainly earthworms) as reported by Ponge andDelhaye (1995) in natural beech forest. More investigationsare thus needed to check for the ecological processes of mullhumus forms in regeneration stands.

It can be noticed that litter is thicker and A horizon thin-ner in mixed regeneration stands than in pure ones. Weassume that this is the consequence of mechanical soil prep-aration occurring in the pure regeneration stands wherebyorganic matter is mixed with upper mineral horizons leadingto a thicker A horizon.

The pH fluctuations during the silvicultural cycle showedthat there was an acidification of the A horizon throughoutpure stand maturation. Moreover, pHKCl and pHH O2

were al-ways higher for the mixed forest stages than for the purebeech forest. Soil acidification results from a reduction inthe acid-neutralizing capacity of the soil (Duchaufour 1997).It is the consequence of proton inputs of external or internalecosystem origin (Bonneau et al. 1987). Among internal in-puts, soil nutrient uptake by roots is considered as a proton-producing process. On the other hand, mineralization oforganic matter (Van Breemen et al. 1984) and mineral weath-ering (Bonneau et al. 1987) are proton-consuming processes.In forest ecosystems, tree growth results in soil acidificationbecause proton production resulting from nutrient uptake ex-ceeds proton consumption (Binkley and Richter 1987; Ulrich1986). In contrast with pure forest, mixed beech–hornbeamforest did not exhibit a tendency toward acidification duringstand maturation. This agrees with the results of other studies,as tree species with a litter that decomposes at a high rate,such as hornbeam, are considered to be able to reverse acidifi-cation (Ponge et al. 1998; Tamm 1990).

Vegetation diversityThe assessment of diversity changes along successional

gradients was performed using several indices describingcommunity structure and composition. Except for SI, diver-sity and heterogeneity indices exhibited the same patterns ofvariation throughout the silvicultural cycle for both the pureand mixed forests. This result suggests that community as-sembly rules occurring throughout silvicultural cycles aresimilar for both forests (see Aubert et al. 2003). The otherdifference between the two silvicultural cycles concerns thevegetation composition, which showed a higher occurrenceof acidophilous species in the pure beech forest. We assume

that the effects of silvicultural practices on successionalchanges are likely to be quantitative (changes in speciesdominance) rather than qualitative (loss of species) (Van derMaarel 1988). Along the succession gradient, the lack ofvariation in SI between stages indicates that a majority ofspecies are not strongly associated with a given successionalstage. A similar result has been reported by Halpern andSpies (1995) for natural forests in the United States. Never-theless, the highest SI values observed in the pure foreststages probably indicate a homogenizing effect of thissilvicultural type (pure planted forest) on species assem-blages.

The results also showed that heterogeneity was higher atthe herbaceous layer scale (FSH) than at the stand level(MSH). This suggests that changes in light availabilitycaused by thinning operations are a disturbance occurringuniformly at a broader scale than soil disturbance inducedby harvesting methods (Deconchat and Balent 2001). This isan important fact for management decisions that address di-versity conservation. According to Nakashizuka (2001), dis-turbance regimes occurring at fine scales may favour speciesco-occurrence, while those occurring at coarse scales mayfavour colonization-competition processes. We assume thatsilvicultural practices based on a long rotation and canopyhomogeneity may favour community organization based oncolonization-competition processes. Such practices shouldalso allow for the establishment of late-successional speciessuch as Gymnocarpium dryopteris, which is absent in thestands of this study. In Upper-Normandy, its scarcity makesit a species of high conservation value found on embank-ments but never within stands, unlike its reported occurrenceunder the closed canopy of a German beech forest at thedegradation phase (Otto 1998).

Conclusion

The approach used (SFTS procedure with multivariateanalysis) provides empirical evidence that the presence of anearly-successional mull-forming species (such as hornbeam)leads to an improvement in decomposition processes in for-est managed for the production of beech. Nevertheless, theimpact of hornbeam on the diversity of herbaceous plantassemblages is only moderate, being simply a lower occur-rence of acidophilous species within mixed forests. Al-though both systems showed only small differences invegetation diversity throughout their silvicultural cycle, theydid not have similar functioning in terms of organic matterturnover. This suggests that sustainable management prac-tices cannot be based solely on the assessment of diversityusing classical approaches. In fact, the functional character-istics of component species are likely to be at least as impor-tant as the number of species to maintain critical ecosystemprocesses and services (Hooper and Vitousek 1997).

Within the study region, most pioneer and postpioneertree species such as Fraxinus excelsior, Acer sp., Betula sp.,Alnus glutinosa, and Carpinus betulus are characterized bytheir soil-improving litter (Duchaufour 1997; Gobat et al.1998). In terms of life history traits and pioneer status, theyform a functional group (Lavorel et al. 1997). Throughoutthe cycle of the pure beech forest, silvicultural practices de-prive the ecosystem of this entire functional group with ex-

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pected strong impacts on ecosystem processes and long-termproductivity (Diaz and Cabido 2001). The same applies tothe absence of species occurring in old forest phases. Thus,long silvicultural rotation (Aubert et al. 2003; Christensenand Emborg 1996; Halpern and Spies 1995) and mainte-nance of early-successional species even at a low abundanceappear to be relevant propositions for future sustainablemanagement decisions.

Finally, it is generally agreed that the relationship betweenspecies composition and ecosystem function needs to be in-vestigated at a variety of spatial and temporal scales(Lacroix and Abbadie 1998). A given scale of biodiversitymeasurement is not necessarily relevant for both the func-tional eco-unit (Oldeman 1990) and the management unit(Alard et al. 1998). The stand level appears to be the rele-vant scale for assessing this relationship from a managementviewpoint. Nevertheless, because of the strong heterogeneityoccurring within a stand and the scale at which the litter de-composition processes occur, fine-scale studies (below thestand level) are necessary. These studies may provide under-standing of functional changes caused by tree species mix-ture and guidelines for recommended species mixture withinstands.

Acknowledgements

This work was possible thanks to the financial support ofthe GIP-ECOFOR for the study and the “Conseil régional deHaute-Normandie” for a research grant given to M. Aubert.The authors would like to acknowledge Julie Baudet,Mickaël Hedde, and Vianney Drouet for their help in datarecording. We thank the French National Forestry Office forits help in site selection, Benoit Laignel (Laboratoire deGéologie, Université de Rouen) for his help in soil charac-terization (loess and clay), and Hen Britton for English cor-rections. We also acknowledge our colleague ThibaudDecaens for statistical analysis and manuscript correctionsand Dr. W. Jan A. Volney as well as two anonymous review-ers for their useful comments.

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Appendix A

Appendix appears on the following page.

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Mixed forest Pure forest

Species MI MII MIII MIV MV PI PII PIII PIV PV

AcidophilousPteridium aquilinum IV IV IV V IV V V V V IVIlex aquifolium III IV III IV II IV III IV IV IVCarex pilulifera IV V IV IV IV III V IV V IVHolcus lanatus II III II IV IV II II III V IIIDigitalis purpurea III III II II V III IV III V IVDeschampsia flexuosa II II II IV V III V IVSalix caprea II II III IV IVBetula alba II III III IIIHypericum perforatum II IIICytisus scoparius III II III IV IIITeucrium scorodonia II III IIGalium saxatile III II II IIICalamagrostis epigejos III IV

MesoacidophilousHolcus mollis III IV III II IV V IV III IV VJuncus effusus II IV III IV V IV IV IV V VLonicera periclymenum IV III IV IV IV IV IV IV IIJuncus conglomeratus II V IV III III V VDactylis glomerata III III II IIIBlechnum spicant II IIICastanea sativa III II

Wide amplitudeRubus fruticosus V V V V V V V V V VMilium effusum V V V V V V IV V IV VDryopteris filix-mas III V III III IV V IV V III IVLuzula pilosa III III III III IV IV IV III IVPrunus avium IV IV II II IV IV II IIIEpilobium angustifolium II III IV V III III II V IVHypericum pulchrum III III II III III IV IV V IVPoa nemoralis II II IV II IIICarpinus betulus V V V V V

MesotrophicAthyrium filix-femina V IV III V IV II III IV III VPolygonatum multiflorum V II III II II IV III III III IIIOxalis acetosella III IV IV IV II II IV III III IIICarex remota V IV IV IV V V V V V VDeschampsia cespitosa IV II III III IV II II II IV IVMelica uniflora IV II III V II II II III IIICarex sylvatica V IV IV III III III III III IIGaleopsis tetrahit II IV III II III IV II IIIHedera helix IV IV IV IV III III IV IVHyacinthoides non-scripta V II IV II IV IV II IVStellaria holostea III III II III III IILysimachia nemorum II II II III V III IIIPoa trivialis III II II II III IIFestuca gigantea II II

Neutrophilous with wide amplitudeCircaea lutetiana III III III II II II IILamium galeodolon III III III II II IIIGalium odoratum III II II IIEpilobium montanum IV III IIRuscus aculeatus IV IIAnemone nemorosa IV VVeronica montana II

Table A1. Species occurrence in the 400-m2 vegetation plots for each succession group.

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Aubert et al. 247

Speciesabbreviation Species name

Tree stratumApse 1 Acer pseudoplatanus 1Cbet 1 Carpinus betulus 1Csat 1 Castanea sativa 1Fsyl 1 Fagus sylvatica 1Fexc 1 Fraxinus excelsior 1Qpet 1 Quercus petraea 1Qrob 1 Quercus robur 1

Shrub stratumApse 2 Acer pseudoplatanus 2Balb 2 Betula alba 2Cbet 2 Carpinus betulus 2Csco 2 Cytisus scoparius 2Fsyl 2 Fagus sylvatica 2Iaqu 2 Ilex aquifolium 2Ptre 2 Populus tremula 2Qrob 2 Quercus robur 2Sauc 2 Sorbus aucuparia 2

Small shrub stratumBalb3 Betula alba 3Cbet3 Carpinus betulus 3Cmon 3 Crataegus monogyna 3Csco 3 Cytisus scoparius 3Fsyl 3 Fagus sylvatica 3Iaqu 3 Ilex aquifolium 3Qrob 3 Quercus robur 3Rfru 3 Rubus fruticosus 3Sauc 3 Sorbus aucuparia 3

Herbaceous stratumApse Acer pseudoplatanusAcap Agrostis capillarisAsto Agrostis stoloniferaAfil-fem Athyrium filix-feminaAnem Anemone nemorosaAela Arrhenatherum elatiusBalb Betula alba

Table A2. Correspondence between species abbrevi-ations and species names.

Mixed forest Pure forest

Species MI MII MIII MIV MV PI PII PIII PIV PV

Strict neutrophilousStachys sylvatica II III II II IIIGeranium robertianum III II III IIScrophularia nodosa IV II III IIFraxinus excelsior IV II IICardamine pratensis II IIGalium aparine III IIUrtica dioica IV IICrataegus monogyna II III II

Note: V, species present in 75%–100% of the records; IV, 50%–75%; III, 25%–50%; II, 5%–25%; I, <5%. Species classi-fication is according to the ecological groups of Brêthes (1984).

Table A1 (concluded).

Speciesabbreviation Species name

Bspi Blechnum spicantBsyl Brachypodium sylvaticumCepi Calamagrostis epigejosCsp Callitriche sp.Cpra Cardamine pratensisCova Carex ovalisCpal Carex pallescensCpil Carex piluliferaCrem Carex remotaCsyl Carex sylvaticaCbet Carpinus betulusCsat Castanea sativaClut Circaea lutetianaCmaj Conopodium majusCmon Crataegus monogynaCsco Cytisus scopariusDglo Dactylis glomerataDces Deschampsia cespitosaDfle Deschampsia flexuosaDpur Digitalis purpureaDcar Dryopteris carthusianaDdil Dryopteris dilatataDfil-mas Dryopteris filix-masEang Epilobium angustifoliumEmon Epilobium montanumEcan Eupatorium cannabinumEsyl Euphorbia sylvaticaFsyl Fagus sylvaticaFgig Festuca giganteaFhet Festuca heterophyllaRacu Ruscus aculeatusFexc Fraxinus excelsiorGtet Galeopsis tetrahitGapa Galium aparineGodo Galium odoratumGsax Galium saxatileGrob Geranium robertianumHhel Hedera helixHsp Hieracium sp.

Table A2 (continued).

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248 Can. J. For. Res. Vol. 34, 2004

Speciesabbreviation Species name

Hlan Holcus lanatusHmol Holcus mollisHnon-scr Hyacinthoides non-scriptaHper Hypericum perforatumHpul Hypericum pulchrumIaqu Ilex aquifoliumJbuf Juncus bufoniusJcon Juncus conglomeratusJeff Juncus effususLgal Lamium galeodolonLcom Lapsana communisLper Lonicera periclymenumLuli Lotus uliginosusLfor Luzula forsteriLmul Luzula multifloraLpil Luzula pilosaLnem Lysimachia nemorumMuni Melica unifloraMeff Milium effusumMtri Moehringia trinerviaOace Oxalis acetosellaPsp Phleum sp.Pann Poa annuaPcha Poa chaixiiPnem Poa nemoralisPtri Poa trivialisPmul Polygonatum multiflorumPhyd Polygonum hydropiperPper Polygonum persicariaPavi Prunus aviumPaqu Pteridium aquilinumQpet Quercus petraeaQrob Quercus roburRrep Ranunculus repensRfru Rubus fruticosusRacu Ruscus aculeatusRace Rumex acetosaRsan Rumex sanguineusScap Salix capreaSnod Scrophularia nodosaSeru Senecio erucifoliusSauc Sorbus aucupariaSsyl Stachys sylvaticaSals Stellaria alsineSgra Stellaria gramineaShol Stellaria holosteaSmed Stellaria mediaSnel Stellaria nemorumTsco Teucrium scorodoniaUdio Urtica dioicaVmon Veronica montanaVriv Viola riviniana

Table A2 (concluded).

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