Trait variations along a regenerative chronosequence in the herb layer of submediterranean forests

Acta Oecologica 43 (2012) 29e41

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Original article

Trait variations along a regenerative chronosequence in the herb layer of submediterranean forests Andrea Catorci a, Alessandra Vitanzi b, Federico Maria Tardella a, *, Vladimir Hrsak c a

School of Environmental Sciences, University of Camerino, Via Pontoni 5, IT-62032 Camerino, Macerata, Italy School of Advanced Studies, PhD Course in Environmental Sciences and Public Health, University of Camerino, Via Lili 55, IT-62032 Camerino, Macerata, Italy c Department of Botany, University of Zagreb, Marulicev trg 20/II, HR-10000 Zagreb, Croatia b

a r t i c l e i n f o

a b s t r a c t

Article history: Received 24 November 2011 Accepted 9 May 2012 Available online 8 June 2012

The aim of this paper is to assess the functional shifts of the herb layer in the submediterranean Ostrya carpinifolia coppiced forests (central Italy) along a coppicing rotation cycle. More specifically, the following questions were addressed: i) is there a pattern in functional trait composition of the herb layer along a regeneration chronosequence?; ii) which traits states differentiate each regeneration stage?; iii) are patterns of trait state variation related to the change of the environmental conditions? Species cover percentage was recorded in 54 plots (20 m
20 m) with homogeneous ecological conditions. Relevés, ordered on the basis of the time since the last coppicing event and grouped into three age classes, were analysed with regard to trait variation, based on species absolute and relative abundance. Differences in light, temperature, soil moisture, and nutrients bioindicator values between consecutive regeneration stages were tested using the non-parametric ManneWhitney U-test. Multi-response permutation procedures (MRPP) revealed statistically significant separation between young and intermediate-aged stands with regard to most traits. Indicator species analysis (ISA) highlighted indicator trait states, which were filtered, along the chronosequence, by changes in environmental conditions. Redundancy analysis (RDA) revealed that light intensity had the greatest effect on traits states variation from the first to the second regeneration stage, while variation from the second to the third age classes was affected by temperature. Young stands were differentiated by short cycle species with acquisitive strategies that only propagated by sexual reproduction, with light seeds, summer green and overwintering green leaves, and a long flowering duration. Intermediate-aged and mature stands were characterized by traits associated with early leaf and flower production, high persistence in time, and showing retentive strategies aimed at resource storage (e.g., geophytes, spring green leaves, rhizomes, and mesomorphic/hygromorphic leaves). Ó 2012 Elsevier Masson SAS. All rights reserved.

Keywords: Chronosequence Coppice Functional trait Ostrya carpinifolia

1. Introduction In temperate climate, management is a key factor driving the species composition of forest ecosystems (Bartha et al., 2008; Denslow, 1980; Pickett and White, 1985; van der Maarel, 1993), because it alters ecological parameters such as light, temperature, air humidity, and soil properties (Gondard and Deconchat, 2003; Rubio and Escudero, 2003). Species differ in their susceptibility to Abbreviations: MRPP, multi-response permutation procedures; ISA, indicator species analysis; RDA, redundancy analysis; DCA, detrended correspondence analysis; L, light intensity; T, air temperature; M, soil moisture; N, soil nutrients content. * Corresponding author. Tel.: þ39 0737404502; fax: þ39 0737404508. E-mail addresses: [email protected] (A. Catorci), alessandra.vitanzi@ unicam.it (A. Vitanzi), [email protected] (F.M. Tardella), vhrsak@ botanic.hr (V. Hrsak). 1146-609X/$ e see front matter Ó 2012 Elsevier Masson SAS. All rights reserved. doi:10.1016/j.actao.2012.05.007

stress and disturbance change, as their potential to establish or persist under any given set of environmental conditions is largely determined by their biological traits (Díaz and Cabido, 2001; Lavorel et al., 1997, 2007; McIntyre et al., 1999). Plant traits are considered as reflecting, not only adaptations to variation in the physical environment, but also trade-offs among different functions within a plant (Lavorel et al., 2007). Indeed, plants are constrained for performing alternative functions simultaneously, such as resource capture and conservation (Chapin et al., 1993; Grime, 1979, 2006; Poorter and Garnier, 1999), acquisition of several different resources (Smith and Huston, 1989; Tilman, 1988), or growth and reproduction (Silvertown et al., 1993; Solbrig, 1993). Thus, it is basic to select an appropriate trait set that synthesizes the main functions enabling plants to face competition, stress and disturbance, due to the variability in space and time of environmental conditions and resource availability, and to human impact.

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The trait-based functional grouping of the species that compose a plant community can also provide information on the mechanisms underlying species assemblages (Alard and Poudevigne, 2000; Kolasa and Rollo, 1991), simplifies the ecological interpretation of the complexity of a plant community (Díaz and Cabido, 2001; Hobbie et al., 1994), improving the understanding of ecological processes and the assessment of ecosystem functions (Díaz and Cabido, 1997; Garnier et al., 2004; Gondard et al., 2006; Hunt et al., 2004; Kirby and Thomas, 2000; Moola and Vasseur, 2004; Nagaike et al., 2003; Pillar, 1999). Trait-based approaches have improved the understanding of forest ecosystem responses to environmental constraints and human impact (e.g., Aubin et al., 2007, 2009; Decocq et al., 2004; Sammul et al., 2004; Verheyen et al., 2003). Previous research indicated that stable forest ecosystems are characterized by species with slow growth, stress-tolerator strategy, early and short flowering span, vegetative spread, large seeds, and transient seed bank. Moreover, the shaded conditions of dense forests affect seed size, plant height, and leaf phenology (Givnish, 1982; Graae and Sunde, 2000; Huston and Smith, 1987; Leishman et al., 1995; Venable and Brown, 1988). Disturbance, instead, favours the presence of therophytes with small seeds, and species with a ruderal strategy and flowering all year round (Givnish, 1982; Graae and Heskjaer, 1997; Graae and Sunde, 2000; Schmidt et al., 1991). As stated by Díaz et al. (2002), traits response to disturbance may depend on the regional context, so that results of local studies cannot be used to make inferences on wide scale. For this reason, it is necessary to analyse the relationships between forest management and the understory functional composition in different biogeographic areas throughout the world. From this point of view, there is a dearth of knowledge about the submediterranean climatic context, because there are no papers that deal with plant trait variation along post-coppicing regenerative sequences in forest ecosystems where winter cold stress alternates with summer drought stress. In these environmental conditions it is possible to hypothesize forest coppicing to have different and stronger effects on the understory vegetation than in those of temperate regions, because plants have to accomplish vegetative growth and reproduction in a short growing season, lasting from the end of winter cold stress to the beginning of summer drought period. On the other hand, the soil erosion due to forest coppicing can reduce the soil water availability enhancing the intensity of drought stress. Moreover, investigations of plant diversity in coppiced forests were mostly focused on limited areas, while landscape scale studies are largely lacking (Canullo et al., 2011). Such a crucial gap affects the quality of the management decisions, usually taken at landscape scale. The aim of our research was to assess the functional shifts of the herb layer in the submediterranean hop-hornbeam (Ostrya carpinifolia) forests, along a coppicing rotation cycle. Hence, the following questions were addressed: i) is there a pattern in functional trait composition of the herb layer along a regeneration chronosequence?; ii) which traits states differentiate each regeneration stage?; iii) are patterns of trait state variation related to the change of the environmental conditions?

The territory is characterized by calcareous substrata, on the border between Temperate and Mediterranean bioclimatic regions (RivasMartínez and Rivas-Saenz, 1996e2009). The main climatic features are typical of the submediterranean landscape: a mean annual temperature of 11e13  C; a mean annual precipitation of 900e1,100 mm; two or three months with a mean minimum temperature of below 0  C (mainly January and February); summer drought stress lasting more than one month (from mid-July to the end of August); a vegetative period of 180e210 days (Catorci et al., 2007b). The O. carpinifolia woods are managed as coppices with standards (mature trees retained through two or three coppicing rotation cycles) and cut down every 20e25 years. From a phytosociological point of view, they are referred to the Querco-Fagetea class, Quercetalia pubescenti-petraeae order and Carpinion orientalis alliance (Blasi et al., 2004; Catorci and Orsomando, 2001).

2. Materials and methods

2.3. Data collection

2.1. Study area

Data were collected during the period 2007e2008. In each sampling plot tree, shrub and herb layer cover were expressed as percent values based on a visual evaluation of vertically projected cover of vegetation layers on the forest floor. Similarly, the cover percentage of each species of the herb layer was evaluated as well. Relevés were carried out from mid-May to mid-June, because during this time it is possible to observe both the early spring

The study area consisted of over 80,000 ha of mountainous territory with altitudes ranging from 500 to 1,000 m a.s.l. in the Umbria-Marche Apennines (central Italy; coordinates range 43140 e42 570 N; 12 570 e13160 E), 2,500 ha of which covered by O. carpinifolia forests taken into consideration in the present research.

2.2. Sampling design To reduce the number of macro-environmental variables, only O. carpinifolia coppiced woods growing on limestone, at altitudes ranging from 600 to 900 m a.s.l., on north-facing slopes (NWeNE), and with a slope angle of 20e45 were considered and sampled based on the Marche Region plant landscape geodatabase (Catorci et al., 2007a; Pesaresi et al., 2007). Preliminarily, 120 stands (surface area ranging from 1 to 6 ha) were randomly selected. Stands were categorized into one of three eight-year intervals (young stands, up to 8 years; intermediateaged stands, 9e16 years; mature stands, 17e24 years) using stand age (time since the last coppicing) as stratifying criterion. Information about time since last logging was obtained from the felling registers of the Corpo Forestale dello Stato. For stands categorization we used a space-for-time substitution approach (Pickett, 1989). This approach has proven its validity to infer many aspects of vegetation dynamics, providing significant insights into the patterns and mechanisms of regeneration and succession (Bartha et al., 2008; Canullo et al., 2011; Foster and Tilman, 2000; Garnier et al., 2004). The categorization was possible for 80 stands, because for 40 of them no information was available about time since the last coppicing. In each of them a plot, covering 400 m2 (20 m
20 m), was randomly placed. To reduce the local environmental variability, plots were analysed with regard to soil physical-chemical conditions (rock fragment percent cover, visually evaluated; texture and pH, analysed by the Marche Region agrochemical analysis and research laboratories, according to the methodological standards established by Italian ministerial decree 13/09/1999). The ecological homogeneity of samples was tested by quartiles calculation for each variable. Plots in which the value of at least one of the above-mentioned variables falls outside the interquartile range (rock fragment cover 1e8%, soil skeleton content 10e50%, sand content 35e65%, and soil pH 5.5e6.5) were excluded. As a result of this selection procedure, 54 plots (16 in young stands, 19 in intermediate-aged as well as in mature stands), were considered for the subsequent analyses. Distance among plots was always greater than 2 km.

A. Catorci et al. / Acta Oecologica 43 (2012) 29e41

flowering species and the late spring/early summer flowering species. Following some authors (e.g., Diekmann, 1995; Ertsen et al., 1998; Persson, 1981; van der Maarel et al., 1985; Wittig and Durwen, 1982; Pignatti, 2005), the environmental effects of forest recovery after coppicing on the herb layer were investigated using Ellenberg indicator values for light intensity (L), air temperature (T), soil moisture (M), and soil nutrients content (N) (Ellenberg et al., 1991). As our aim was to assess the functional response of the herb layer during a coppicing rotation cycle, we considered the following traits, linked to the main plant functions, i.e. resource acquisition and conservation (vegetative traits), and sexual reproduction (reproductive traits): life form, vegetative propagation, storage organs, leaf persistence, leaf anatomy, flowering phenology, and seed weight. Bibliographic data on species traits (Grime et al., 1988; Klotz et al., 2002; Pignatti, 1982) were checked and supplemented by field observations with regard to life form, storage organs, vegetative propagation, leaf anatomy (punctual observations), flowering phenology and leaf persistence (checked during the year), and by the collection and weigh of the seeds in the laboratory. A description of each trait, with a list of the respective states and data sources, is reported in the appendix. 2.4. Data elaboration Traits states binary data (presence/absence) were transformed Ps in quantitative data using the formula Ta ¼ i ¼ 1 ðCi $IÞ, where Ta is the absolute weighted abundance of a trait state in a relevé; Ci is the cover value (%) of each herb species; s is the number of herb species; I may be either 0 or 1 (absence or presence of the considered trait state). The mean relative abundance of each trait state (percentage value) was calculated in each regeneration stage using the formula P Tr ¼ ðTa$100Þ= ni¼ 1 Tai , where Tr and Ta are, respectively, the relative and the absolute abundances of a trait state in a relevé; n is the number of trait states in a relevé. The Ta and Tr values were averaged for each age class and were used for further statistical elaborations. The mean of vegetation layers cover in the three regeneration stages was calculated as well. Ellenberg indicators were weighted using presence/absence data of herb layer species, disregarding species cover. The arithmetical mean of each indicator was calculated for each relevé, and averaged for each regeneration stage. Correlation between tree canopy cover and bioindicator values was examined using Spearman rank correlation coefficients. Normality distribution and variance homogeneity of vegetation layers cover, Ellenberg indicator values, Ta and Tr values for each trait state, were assessed using KolmogoroveSmirnov test and Levene test, respectively. Because data did not meet the assumptions required for parametric tests, non-parametric ManneWhitney U-tests were performed to understand which regeneration stages are significantly different (P < 0.05) from each other in relation to the tested variables. A Holm (1979) adjustment for multiple comparisons of ManneWhitney U-test results was used to avoid Type I error. The multi-response permutation procedure (MRPP), applied using Sørensen (BrayeCurtis) distance (McCune and Grace, 2002), was used to test the null hypothesis of no difference in the composition of traits states for each trait among the three regeneration stages. MRPPs were run for each trait on the matrix relevés
trait states (Ta, absolute weighted abundances), using age class (young, intermediate-aged, and mature stands) as grouping variable. The MRPP compares the observed intra-group average distance with the average distance that would have resulted from

31

all the other possible combinations of the data under the null hypothesis. The observed delta is determined by averaging the observed intra-group distances, weighted by the relative group size. The observed delta is compared to the probability delta, resulting from every permutation of all the observations among the groups. A probability value of a delta smaller than the observed is calculated from the position of the observed delta in the list of possible deltas. A test statistic T is calculated from Pearson type III distribution to derive the probability (Mielke and Berry, 1994). The statistic A (chance corrected within group agreement), calculated from the observed and expected deltas, is used to measure the homogeneity within the group. An A ¼ 1 indicates that all samples within each group are identical; an A equalling zero or lower than zero indicates that within-group heterogeneity is equal or greater, respectively, to that expected by chance. Pairwise comparisons between age classes were run. The Holm (1979) correction for multiple comparisons was used to avoid Type I error. Indicator species analysis (ISA) was run for each trait, on the matrix relevés
trait states (Ta, absolute weighted abundances), using age class (young, intermediate-aged, and mature stands) as grouping variable, to highlight indicator trait states of each regenerative step. The ISA is a non-parametric method for identifying those species that show significantly preferential distribution (frequency and abundance) with respect to a priori treatment group. An indicator value is calculated by multiplying the relative abundance of each species in a particular group and the relative frequency of the species occurrence in the sample of that group (Dufrêne and Legendre, 1997; McCune and Grace, 2002). The statistical significance of the observed maximum indicator values for trait states was evaluated through the Monte Carlo test, based on 4,999 permutations, where samples are reassigned and recalculated. The number of randomized indicator values higher than the observed ones are used to calculate the probability value (McCune and Grace, 2002). Trait states with an indicator value greater than 40 were considered to be of interest. We ran detrended correspondence analyses (DCA) to decide (on the basis of the gradient lengths depicted by axis 1 of DCA) whether the linear or unimodal model was more appropriate in the subsequent multivariate analyses. DCA results on trait data matrices (whole trait data set and partial data sets composed of the first and the second age classes, and of the second and the third age classes) showed short gradients (1.646 S.D., 1.734 S.D., and 1.630 S.D., respectively), suggesting that an ordination technique based on the linear model, such as Redundancy analysis, could be used (ter Braak, 1995). On the basis of these results, a canonical redundancy analysis (RDA) of trait matrix (Ta, weighted abundances of trait states), constrained by Ellenberg’s bioindicator values (L - light intensity, T - air temperature, M - soil moisture, and N - soil nutrients content) was performed to compute the percentage of variation explained by the combination of the four explanatory variables. Prior to RDA, cover data matrix has been Hellingertransformed to avoid considering double absence as a resemblance between sites (Legendre and Gallagher, 2001). To assess the contribution of each environmental variable to the total variability of trait data set, the total variance was partitioned into fractions explained by each of the predictor variables by partial RDAs (Borcard et al., 1992; Borcard and Legendre, 1994). Adjusted Rsquare values were calculated to produce unbiased estimates of the contributions of the independent variables to the explanation of the response variables (Peres-Neto et al., 2006). To test the significance of the adjusted R-squares (i.e., whether each independent fraction exhibits a significant influence on cover data), a permutation test with 1,000 permutations was applied, in accordance with Legendre and Legendre (1998). The same procedure was used to analyse the effects of environmental variables on two partial data

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sets, composed of relevés carried out in young and intermediateaged stands, and in intermediate-aged and mature stands. MRPP and ISA were run using PCORD 5.0 software (McCune and Mefford, 2006). Spearman correlation, KolmogoroveSmirnov, Levene, and Mann-Whytney U-tests, were performed using the SPSS software, version 8.0 (SPSS Inc., 1997). DCA, RDAs and variance partitioning were computed using decorana, rda, decostand, and varpart functions in R software, version 2.13.0 (R Development Core Team, 2011), and the vegan package, version 1.17e9 (Oksanen et al., 2011).

Table 1 shows the main structural and ecological features of the three regeneration stages along the considered chronosequence. Whereas tree layer cover shows an increasing trend, the opposite trend is shown for shrub layer and herb layer cover values. Light and temperature mean bioindicator values of the herb layer decreased from post-logged to mature plots, whereas soil moisture and nutrient values slightly increased in mature plots. The ManneWhitney U-test revealed a significant difference between plots of young and intermediate-aged stands for light bioindicator value, tree and shrub layer cover, and between plots of intermediate-aged and mature stands for temperature bioindicator value. Correlation analysis showed a negative correlation between tree canopy cover value and light bioindicator value of the herb layer (0.3974; P ¼ 0.0029), while temperature, soil moisture and nutrient bioindicator values of the herb layer did not show any significant correlation with tree canopy cover. The MRPP results showed a statistically significant separation among age classes for all the traits of the herb layer (Table 2). A significant difference was detected between plots of young and intermediate-aged stands with regard to life form, storage organs, leaf persistence and anatomy, and flowering phenology. Plots of intermediate-aged and mature stands differed in leaf anatomy (Table 2). The indicator plant functional trait states highlighted by ISA are shown in Table 3. Trait states mean cover percentage values in each step of the chronosequence are reported in Table 4. The comparison between plots of young and mature stands revealed a significant increase in abundance along the coppicing rotation cycle of species with rhizomes (functioning as storage organs) and mesomorphic/hygromorphic leaves (Table 4), indicator trait states of mature stands. Conversely, a significantly decreasing abundance was shown for the indicator trait states of young stands;

Table 1 Mean values of structural variables and of bioindicator values of the herb layer for light intensity (L), air temperature (T), soil moisture (M), and soil nutrients content (N) in the three age classes since the last coppicing event (standard deviation values are given in parentheses). Equal letters indicate no statistical difference as determined by ManneWhitney U-test, after Holm correction (1 - young stands; 2 intermediate-aged stands; 3 - mature stands).

Structural variable Tree layer cover (%) Shrub layer cover (%) Herb layer cover (%) Bioindicator value L T M N

Trait

Age classes comparison

T

A

P

Life form**

1 1 1 1 1 1 1 1 2 1 1 1 1

5.480 3.441 3.976 4.442 3.484 3.363 4.492 6.780 3.824 7.502 7.594 5.036 3.103

0.063 0.039 0.036 0.043 0.037 0.049 0.066 0.091 0.044 0.094 0.091 0.059 0.031

0.001 0.008 0.003 0.001 0.006 0.010 0.003 0.000 0.004 0.000 0.000 0.000 0.010

Storage organs***

3. Results

Variable

Table 2 Pairwise comparison between age classes since the last coppicing event, with regard to plant trait composition, as performed by multi-response permutation procedures. The level of significance of differences in trait composition among age classes is indicated by asterisks (1- young stands; 2 - intermediate-aged stands; 3 - mature stands; T - test statistics; A - Chance-corrected within-group agreement; P - probability of a smaller or equal weighted mean within-group distance). Only significant differences in trait composition between age classes after Holm correction are reported.

Age class 1

2

3

47.9a (35.9) 55.6a (15.4) 66.7a (38.4)

95.6b (5.2) 31.3b (14.5) 63.7a (24.8)

96.2b (4.6) 26.2b (13.4) 52.4a (24.2)

5.5a 5.9a 4.5ab 4.8a

5.1b 5.8a 4.5bc 4.8a

(0.5) (0.2) (0.1) (0.3)

(0.3) (0.1) (0.1) (0.3)

5.0b 5.6b 4.6c 4.9a

(0.3) (0.2) (0.1) (0.3)

Vegetative propagation* Leaf persistence** Leaf anatomy***

Flowering phenology*** Seed weight* ***

P  0.001;

vs. vs. vs. vs. vs. vs. vs. vs. vs. vs. vs. vs. vs.

2 3 2 3 3 2 3 2 3 3 2 3 3

**

P  0.01; *P < 0.05.

namely, therophytes, biennial and creeping hemicryptophytes; tufts, pleiocorms and primary storage roots as storage organs; summer and overwintering green leaves; mesomorphic leaves; absence of vegetative propagation (only sexual reproduction); flowering from late spring to late summer and in early autumn; seed weight ranging from 0.01 to 0.20 mg and from 0.21 to 0.50 mg. The majority of these shifts occurred also between the first two regenerative phases (Table 4). Most of indicator trait states of intermediate-aged stands (rhizomatous geophytes; early flowering species; and plants with scleromorphic/mesomorphic leaves and with spring green leaves) increased significantly their abundance from young stands, but did not show significant differences if compared to mature stands. The relative mean cover percent values of species sharing each trait state with respect to the total mean cover of all trait states in each regeneration stage are reported in Table 5. The total explained variance for trait data set, constrained by light intensity, air temperature, soil moisture and nutrients, was 14.2% (adjusted R-squares). As indicated in the RDA ordination graph (Fig. 1) biennial hemicryptophytes, species with pleiocorms, primary storage roots or lacking storage organs, with summer green and mesomorphic leaves, and flowering from late spring to late summer were strictly related to high light intensity and low soil moisture; therophytes, overwintering green leaves, and species without vegetative propagation modes were linked both to high light intensity and to high temperatures. Conversely, species with rhizomes as storage organs and vegetative propagation modes and with mesomorphic/ hygromorphic leaves are closely related to high soil moisture and nutrients and to low light intensity. Bulbous geophytes, spring green leaves, hypocotyl bulbs, scapose and rosulate hemicryptophytes were favoured under high soil nutrients and relatively high soil moisture and air temperature; rhizomatous geophytes, persistent green leaves and early flowering species, instead, are less moisture, shadow and nutrient-demanding, and are linked to lower temperatures. Species with runners (in some cases also with rhizomes), flowering from mid-summer to late summer, caespitose hemicryptophytes, and species with sclero/mesomorphic leaves, are related to arid nutrient-poor soils and low temperatures. The independent explained variance extracted from the trait data set (Table 6) showed that light had the greatest effect (adj.-

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Table 3 List of indicator trait states of the age classes for each trait, as determined by indicator species analysis. Only trait states with P < 0.05 and indicator value >40 are reported (Max age class - age class with maximum observed indicator value; P - proportion of randomized trials with an indicator value equal to or exceeding the observed indicator value; 1 young stands; 2 - intermediate-aged stands; 3 - mature stands). Trait

Trait state

Max age class

Observed indicator value

P

Life form

Therophytes Biennial hemicryptophytes Creeping hemicryptophytes Bulbous geophytes Rhizomatous geophytes Absent Runner/pleiocorm Primary storage root Tuft Pleiocorm Runner/rhizome Hypocotyl bulb Rhizome Absent (only sexual reproduction) Summer green leaves Overwintering green leaves Spring green leaves Mesomorphic leaves Scleromorphic/mesomorphic leaves Mesomorphic/hygromorphic leaves Late spring-late summer Early autumn Early spring 0.01e0.20 0.21e0.50

1 1 1 2 2 1 1 1 1 1 2 2 3 1 1 1 2 1 2 3 1 1 2 1 1

71.2 68.1 52.2 61.0 47.2 71.2 40.5 67.0 58.8 73.4 54.7 51.3 48.9 60.7 50.0 75.9 62.0 56.6 47.2 47.4 84.6 50.3 53.4 43.2 58.2

0.0002 0.0006 0.0164 0.0022 0.0442 0.0004 0.0018 0.0002 0.0004 0.0002 0.0354 0.0146 0.0396 0.0004 0.0070 0.0002 0.0014 0.0008 0.0022 0.0278 0.0002 0.0028 0.0002 0.0268 0.0376

Storage organs

Vegetative propagation Leaf persistence

Leaf anatomy

Flowering phenology

Seed weight (mg)

R2 ¼ 0.0646, P ¼ 0.001), accounting for about the 46% of the variability explained by the environmental variables, followed by soil nutrients (adj.-R2 ¼ 0.0161, P ¼ 0.034), while no significant effect was shown by air temperature (adj.-R2 ¼ 0.0139, P ¼ 0.058) and soil moisture (adj.-R2 ¼ 0.0019, P ¼ 0.556). Further analyses on the two partial data sets revealed that significant effect on trait states variation was shown by light (adj.-R2 ¼ 0.1044, P ¼ 0.001) when the first and second age classes were considered. Temperature was the only factor to determine significant variation (adj.-R2 ¼ 0.0249, P ¼ 0.049) when relevés from the second and third age classes were processed, while the 3.4% of variance was accounted by the joint effect of light, soil moisture and nutrients. 4. Discussion The results indicated that the temporal pattern of herb layer functional composition of submediterranean O. carpinifolia coppiced forests is characterized by variation in the relative weighted abundance of trait states (Table 5). Indeed, very few trait states disappear, and no new trait state appears after the first regenerative step (Table 4). Furthermore, two dominant trait states, namely caespitose hemicryptophytes and species flowering for mid-spring to late spring, do not show significant variations both in absolute and in relative weighted abundance along the chronosequence (Tables 4 and 5) and seem not to be influenced by the changing in environmental conditions, during the regeneration process (Fig. 1). Caespitose hemicryptophytes are mostly graminoid competitive species (e.g., Luzula sylvatica) or stress tolerantcompetitive species (e.g., Brachypodium rupestre, Sesleria nitida) that may spread throughout the forest undergrowth by runners and/or rhizomes, and are related to arid, nutrient-poor conditions. It can be hypothesized that persistence of this kind of species in the understory indicates that the coppicing rotation cycle is too short to lower the abundance of these species, mostly typical of pastures, forest edges or thermophilous woods (Catorci et al., 2011a). Instead, the dominance of species flowering from mid-spring to late spring throughout the regenerative cycle is probably due to the lack, in

this period, of high intensity stresses (cold, drought, etc.) which determine the most favourable conditions for the flowering phenological phases in each type of submediterranean plant community (Gatti et al., 2007) and forest successional stage. With regard to the other traits, it is possible to state that the differentiation of their abundance along the chronosequence was mainly driven by the change in environmental conditions, especially the light availability at the undergrowth level, as shown by the results of RDA ordination and variance partitioning (Fig. 1, Table 6). It is also possible to argue that change in light intensity, due to the tree canopy cover modification along the chronosequence, is the main factor driving the traits shift between plots of young and intermediate-aged stands. Instead, changes in understory microclimatic conditions drove the traits shift between the two last regenerative phases (temperature bioindicator value showed a significant difference between intermediate-aged and mature stands, and was the only factor to determine significant trait variation when relevés from the second and third age classes were processed). As regards soil features, soil moisture bioindicator values showed a significant difference between plots of young and mature stands, while no trend was detected in soil nutrient bioindicator values, even though nutrients account significantly for a part of variance of trait states abundance of the whole trait data set (Table 6). As nutrients bioindicator values did not account singly for significant variations between age classes, it may be hypothesized that variation explained for the whole trait data set was due to small-scale heterogeneity of nutrients distribution among relevés sites of the same age class. Indeed, Catorci et al. (2011b) demonstrated that in long-term coppiced woods, the high nutrient-demanding species are restricted to shelter niches associated with land forms that preserve soil from erosion (e.g., not steep drainage lines, hollows, soil depressions, flat or semi-flat lands). Indicator trait states of young stands (Table 3) were related to high light intensity and temperatures (Fig. 1) due to the lack of light interception by the tree canopy. Moreover, herb species had a lot of space available for spreading, as highlighted by the mean herb and

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Table 4 Mean weighted absolute abundance values of trait states in the three age classes since the last coppicing event. Standard deviation is reported in parentheses (1- young stands; 2 - intermediate-aged stands; 3 - mature stands). Equal letters indicate no statistical difference as determined by ManneWhitney U-test, after Holm correction. Trait

Trait state

Mean abundance (%) Age class 1

Life form

Storage organs

Vegetative propagation

Leaf persistence

Leaf anatomy

Flowering phenology

Seed weight (mg)

Bulbous geophytes Rhizomatous geophytes Scapose hemicryptophytes Rosulate hemicryptophytes Biennial hemicryptophytes Caespitose hemicryptophytes Creeping hemicryptophytes Chamaephytes Therophytes Absent Runner Runner-like rhizome Rhizome-like pleiocorm Rhizome Runner/rhizome Runner/tuft Runner/tuft/rhizome Pleiocorm Pleiocorm/primary storage root Runner/pleiocorm Tuft Tuft/rhizome Primary storage root/rhizome-like pleiocorm Bulb Bulbil/bulb Hypocotyl bulb Root tuber Primary storage root Succulence Absent (only sexual reproduction) Runner Runner-like rhizome Rhizome-like pleiocorm Root shoot Rhizome-like pleiocorm/root shoot Rhizome Runner/rhizome Runner/root shoot Fragmentation/rhizome Rhizome/root shoot Bulb Bulbil/bulb Innovation bud with root tuber Overwintering green leaves Spring green leaves Summer green leaves Persistent green leaves Mesomorphic leaves Scleromorphic leaves Scleromorphic/mesomorphic leaves Mesomorphic/hygromorphic leaves Hygromorphic and hygromorphic/helomorphic leaves Succulent leaves Early spring Mid-spring-late spring Late spring-late summer Mid-summer-late summer Mid-summer-early autumn Early autumn 0.01e0.20 0.21e0.50 0.51e1.00 1.01e2.00 2.01e4.00 4.01e10.00 10.01e50.00

1.31a 3.94a 10.33a 2.38a 5.69a 30.51a 2.81a 0.38a 9.31a 7.31a 19.56a 1.19a 0.25a 6.19a 3.70a 0.19a 4.25a 2.06a 0.44a 0.56a 4.63a 4.64a 0.25a 0.06a 0.44a 2.25a 0.06a 7.94a 0.69a 25.44a 20.31a 1.19a 0.38a 0.75a 0.13a 8.20a 7.45a 0.50a 1.06a 0.69a 0.06a 0.44a 0.06a 7.44a 0.75a 24.89ab 33.58a 40.65a 1.38a 13.06a 9.81a 1.06a 0.69a 4.58a 32.76a 11.75a 8.94a 1.31a 6.44a 5.38a 10.31a 10.00a 14.94a 14.94a 4.56a 2.45a

2 (1.06) (3.31) (7.88) (1.76) (9.69) (15.62) (3.03) (0.34) (13.09) (8.91) (13.89) (2.68) (0.32) (3.16) (3.27) (0.36) (8.14) (2.82) (0.66) (0.98) (4.10) (4.85) (0.37) (0.17) (0.31) (3.26) (0.17) (14.57) (1.69) (27.97) (13.65) (2.68) (0.50) (0.95) (0.22) (5.32) (8.24) (1.00) (1.42) (1.03) (0.17) (0.31) (0.17) (11.30) (1.03) (18.21) (15.88) (31.54) (1.32) (7.43) (9.34) (0.85) (1.69) (2.84) (16.31) (16.40) (9.76) (1.97) (9.70) (6.20) (10.26) (10.05) (13.01) (10.55) (4.87) (3.40)

7.29a 9.82b 4.13b 3.79a 0.32b 35.63a 1.95a 0.32a 0.47b 1.11b 23.11a 0.00b 0.11a 10.03b 7.55a 0.05a 7.29a 0.18b 0.05a 0.08ab 1.87b 4.53a 0.21a 0.24a 0.68a 6.37a 0.16a 0.11b 0.00a 10.29ab 24.66a 0.00b 0.26a 0.11a 0.05a 9.03a 13.39a 0.05ab 3.89a 0.89a 0.24a 0.68a 0.16a 0.21b 6.87b 16.05bc 40.58a 20.21b 1.26a 29.84b 10.95a 1.45a 0.00a 18.58b 30.63a 0.53b 9.29a 0.66a 3.05b 1.32b 2.89b 17.71a 13.79a 13.39a 6.97a 1.18a

3 (8.07) (9.26) (1.94) (3.61) (0.42) (24.54) (1.85) (0.51) (0.82) (0.91) (16.91) (0.00) (0.21) (4.62) (10.25) (0.16) (10.63) (0.38) (0.16) (0.19) (1.34) (6.84) (0.25) (0.92) (1.30) (7.92) (0.29) (0.21) (0.00) (7.05) (17.16) (0.00) (0.26) (0.27) (0.16) (4.40) (14.24) (0.16) (6.92) (0.99) (0.92) (1.30) (0.29) (0.42) (8.45) (13.06) (23.04) (16.89) (0.79) (11.93) (11.15) (1.48) (0.00) (10.27) (23.43) (0.66) (10.70) (0.55) (12.60) (0.90) (1.90) (14.26) (14.71) (15.12) (7.66) (0.82)

3.34a 7.05ab 9.95ab 2.66a 0.26b 27.42a 0.63b 0.21a 0.84b 1.21b 15.45a 0.00b 0.03a 15.50b 2.55a 0.21a 8.50a 0.21b 0.08a 0.05b 1.37b 3.05a 0.32a 0.11a 0.32a 3.13a 0.18a 0.11b 0.00a 6.42bc 16.32a 0.00b 0.32a 0.16a 0.03a 14.61a 10.45a 0.00bc 2.05a 1.42a 0.11a 0.32a 0.18a 0.32b 2.87ab 8.87c 40.32a 10.95b 0.76a 20.29ab 18.68b 1.68a 0.00a 11.63b 26.18a 0.74b 12.63a 0.53a 0.11b 1.29b 1.87b 14.50a 13.53a 10.53a 3.11a 1.58a

(4.12) (4.77) (14.48) (1.70) (0.48) (21.75) (0.50) (0.38) (1.68) (1.79) (15.81) (0.00) (0.11) (16.62) (3.94) (0.30) (9.71) (0.30) (0.19) (0.16) (0.90) (4.13) (0.25) (0.21) (0.25) (3.87) (0.30) (0.21) (0.00) (4.74) (15.74) (0.00) (0.25) (0.29) (0.11) (15.28) (9.48) (0.00) (3.71) (2.42) (0.21) (0.25) (0.30) (0.56) (4.01) (4.21) (21.15) (5.83) (0.51) (17.08) (14.93) (1.56) (0.00) (7.02) (15.49) (1.61) (14.49) (0.61) (0.21) (0.93) (1.22) (10.02) (14.77) (14.25) (4.01) (1.26)

A. Catorci et al. / Acta Oecologica 43 (2012) 29e41

35

Table 5 Mean relative abundance of trait states in each age class. Standard deviation is reported in parentheses (1- young stands; 2 - intermediate-aged stands; 3 - mature stands). Equal letters indicate no statistical difference as determined by ManneWhitney U-test, after Holm correction. Trait

Trait state

Mean abundance (%) Age class 1

Life form

Storage organs

Vegetative propagation

Leaf persistence

Leaf anatomy

Flowering phenology

Seed weight (mg)

Bulbous geophytes Rhizomatous geophytes Scapose hemicryptophytes Rosulate hemicryptophytes Biennial hemicryptophytes Caespitose hemicryptophytes Creeping hemicryptophytes Chamaephytes Therophytes Absent Runner Runner-like rhizome Rhizome-like pleiocorm Rhizome Runner/rhizome Runner/tuft Runner/tuft/rhizome Pleiocorm Pleiocorm/primary storage root Runner/pleiocorm Tuft Tuft/rhizome Primary storage root/rhizome-like pleiocorm Bulb Bulbil/bulb Hypocotyl bulb Root tuber Primary storage root Succulence Absent (only sexual reproduction) Runner Runner-like rhizome Rhizome-like pleiocorm Root shoot Rhizome-like pleiocorm/root shoot Rhizome Runner/rhizome Runner/root shoot Fragmentation/rhizome Rhizome/root shoot Bulb Bulbil/bulb Innovation bud with root tuber Overwintering green leaves Spring green leaves Summer green leaves Persistent green leaves Mesomorphic leaves Scleromorphic leaves Scleromorphic/mesomorphic leaves Mesomorphic/hygromorphic leaves Hygromorphic and hygromorphic/helomorphic leaves Succulent leaves Early spring Mid-spring-late spring Late spring-late summer Mid-summer-late summer Mid-summer-early autumn Early autumn 0.01e0.20 0.21e0.50 0.51e1.00 1.01e2.00 2.01e4.00 4.01e10.00 10.01e50.00

2.71a 5.99a 14.77a 4.47a 6.89a 49.78a 4.90a 0.55a 9.93a 8.65a 32.69a 1.36a 0.35a 11.18a 6.26a 0.33a 7.16a 2.62a 0.48a 0.71a 6.70a 6.98a 0.60a 0.14a 0.77a 3.30a 0.10a 8.87a 0.74a 31.59a 34.09a 1.35a 0.77a 0.94a 0.17a 13.47a 12.52a 0.57a 2.02a 1.38a 0.14a 0.77a 0.10a 7.84a 1.72a 37.07a 53.37a 57.11a 2.57a 22.03a 15.74a 1.80a 0.74a 8.94a 53.75a 13.36a 12.32a 1.82a 9.81a 7.56ab 14.38a 17.31ab 24.50a 25.18a 7.63a 3.44a

2 (2.82) (4.01) (6.82) (4.29) (10.08) (18.10) (6.02) (0.52) (10.61) (8.10) (20.64) (3.40) (0.51) (6.71) (6.40) (0.65) (13.13) (3.01) (0.73) (1.10) (4.29) (6.58) (0.94) (0.38) (0.77) (3.79) (0.28) (12,55) (1.94) (17.22) (20.28) (3.35) (1.10) (1.10) (0.33) (8.16) (13.89) (1.11) (2.56) (1.91) (0.39) (0.78) (0.27) (10.04) (2.67) (13.64) (14.97) (20.51) (3.23) (13.93) (13.80) (1.43) (1.94) (7.39) (15.39) (12.30) (10.72) (2.47) (14.82) (6.85) (9.28) (17.81) (18.17) (11.33) (7.82) (3.67)

15.93a 15.52b 7.12b 6.44a 0.54b 50.22a 2.85a 0.56a 0.83b 1.87b 33.29a 0.00b 0.16ab 17.93b 10.43a 0.12a 9.21a 0.28b 0.05a 0.08b 3.07b 6.58a 0.38a 0.81a 1.05a 14.24a 0.22a 0.21b 0.01a 20.58ab 35.72a 0.00b 0.44a 0.06b 0.10a 16.40a 17.43a 0.05ab 5.40a 1.43a 0.81a 1.05a 0.22a 0.37b 15.65a 24.04b 59.94ab 29.21b 2.27a 49.55bc 16.50a 2.47a 0.00a 34.10b 44.69a 0.83b 15.44a 1.18a 3.77b 2.32c 5.05b 27.84bc 23.95a 21.25a 16.95a 2.64a

3 (18.70) (12.21) (3.40) (6.43) (0.84) (21.78) (2.12) (0.91) (1.38) (1.55) (16.14) (0.00) (0.35) (10.11) (12.95) (0.41) (11.95) (0.57) (0.16) (0.20) (2.09) (8.47) (0.49) (3.22) (1.58) (17.64) (0.42) (0.46) (0.01) (17.31) (15.51) (0.00) (0.48) (0.20) (0.33) (9.95) (15.39) (0.17) (8.74) (1.36) (3.22) (1.58) (0.42) (0.68) (19.88) (13.07) (21.68) (16.64) (1.72) (15.95) (12.62) (2.51) (0.00) (20.55) (17.93) (1.11) (16.66) (1.10) (14.68) (1.38) (2.50) (15.00) (20.96) (17.42) (19.07) (2.19)

5.87a 15.93b 18.30ab 5.21a 0.59b 50.98a 1.45b 0.45a 1.23b 1.92b 27.14a 0.00b 0.10b 31.75b 4.64a 0.49a 15.38a 0.52b 0.13a 0.07b 3.23b 7.06a 0.92a 0.14a 0.64a 5.38a 0.32a 0.18b 0.00a 11.84b 28.79a 0.00b 0.91a 1.04a 0.10a 30.03a 18.72a 0.00b 4.74a 2.48a 0.14a 0.63a 0.32a 0.52b 5.03a 20.82b 73.63b 24.15b 1.67a 36.50ab 34.59b 3.08a 0.00a 25.03b 52.18a 1.05b 20.20a 1.19a 0.35b 3.48ac 5.01b 31.82c 24.62a 23.79a 6.59a 4.70a

(7.66) (11.25) (21.55) (2.95) (1.17) (26.76) (1.32) (0.89) (2.14) (2.43) (22.54) (0.00) (0.44) (26.47) (6.25) (0.76) (17.16) (0.91) (0.34) (0.21) (2.79) (8.32) (1.02) (0.28) (0.62) (7.30) (0.52) (0.38) (0.00) (7.90) (21.87) (0.00) (1.01) (1.18) (0.42) (24.77) (16.25) (0.00) (6.79) (3.73) (0.28) (0.61) (0.51) (0.89) (7.57) (15.61) (16.34) (15.68) (1.14) (19.40) (21.77) (2.26) (0.00) (16.22) (21.68) (1.99) (18.45) (1.92) (0.81) (3.31) (3.81) (17.22) (19.86) (26.66) (9.25) (5.23)

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A. Catorci et al. / Acta Oecologica 43 (2012) 29e41

Fig. 1. Redundancy analysis ordination graph for plant trait data set, using average Ellenberg indicator values as constraining variables (L - light intensity; T - air temperature; M soil moisture; N - soil nutrients content); ar - runner-like rhizome; b - bulbil; Ch - chamaephyte; fl - flowering phenology (1 - early spring; 2 - mid-spring-late spring; 3 - midsummer-late summer; 23 - late spring-late summer; 4 - early autumn); fr - fragmentation; Gbul - bulbous geophyte; Grh - rhizomatous geophyte; h - tuft; Hbien - biennial hemicryptophyte; Hcaes - caespitose hemicryptophyte; hh - hygromorphic and hygromorphic/helomorphic leaves; hk - hypocotyl bulb; Hrep - creeping hemicryptophyte; Hros rosulate hemicryptophyte; Hscap - scapose hemicryptophyte; i - persistent green leaves; iw - innovation bud with root tuber; m - mesomorphic leaves; mh - mesomorphic/ hygromorphic leaves; n - absence of the trait; p - pleiocorm; r - primary storage root; rh - rhizome; rp - rhizome-like pleiocorm; run - runner; s - summer green leaves; sc scleromorphic leaves; sm - scleromorphic/mesomorphic leaves; so - storage organ; su - succulence; sw - seed weight (1 - 0.01e0.20 mg; 2 - 0.21e0.50 mg; 3 - 0.51e1.00 mg; 4 1.01e2.00 mg; 5 - 2.01e4.00 mg; 6 - 4.01e10.00 mg; 7 - 10.01e50.00 mg); Th - therophytes; v - spring green leaves; vp - vegetative propagation mode; w - overwintering green leaves; wk - root tuber; ws - root shoot; z - bulb).

shrub layers cover that lower to their minimum value in plots of mature stands, before coppicing. High light availability determines the establishment of short life-cycle species (i.e., ruderal species), which are adapted for efficient resource acquisition, with traits devoted to high resource investment in fast growth and sexual reproduction. More specifically, therophytes (e.g., Geranium columbinum, Myosotis arvensis, Torilis arvensis, and Trifolium campestre), which reproduce exclusively by seeds, and biennial hemicryptophytes (e.g., Campanula rapunculus, Cirsium vulgare, Daucus carota, and Verbascum thapsus), which have primary storage roots and sexual reproduction, were identified. These observations are in agreement with Decocq et al. (2004), Díaz et al. (1998), Graae and Heskyær (1997), Meier et al. (1995), and Schmidt et al. (1991). Such species may be considered as being transient sensu Grime (2001); they spread rapidly throughout forest undergrowth by means of the local seed-bank or the seed-rain from the surrounding landscape. Species with overwintering green leaves (mostly therophytes) gain a competitive advantage by photosynthesizing throughout winter, which is characterized, in the submediterranean climatic context, by having low cold stress. The occurrence of this trait as indicator of post-logged stands is consistent with the results of Kenderes and Standovár (2003) for managed stands. Moreover, this life-history trait limits competition with species that have summer green leaves (Regehr and Bazzaz, 1976), which are also indicator of the first regeneration stage.

The identification by ISA of two trait states for flowering phenology (flowering from late spring to late summer and in early autumn) is in agreement with the observation of Graae and Sunde (2000) that the proportion of species with later and longer flowering periods are higher in young forests than in the old ones. Regarding seed weight, classes ranging from 0.01 to 0.20 mg and from 0.21 to 0.50 mg emerged from ISA. Plants with these trait states showed a decreasing trend of relative abundance along the chronosequence, so that it can be argued, in accordance with Kenderes and Standovár (2003), that species with small seeds are advantaged in disturbed conditions of managed forests because small and light seeds have a better colonization capacity than larger ones (Verheyen et al., 2003; Willson and Traveset, 2000). Also the occurrence of creeping hemicryptophytes (e.g., Fragaria vesca and Ajuga reptans) among the indicator trait states of postlogged stands is likely connected to disturbance. It has been proposed that disturbance may enhance shoot mobility (van der Maarel, 1996), because overstory canopy openings offer more opportunities for rooting in conditions of light availability (Grime, 2001; Sammul et al., 2004), getting to efficient space occupation. To sum up, non-forest species, favoured by high light intensity and space availability, spread in the forest herb layer after felling. These species showed strategies addressed to a quick space occupation and sexual reproduction. Significant shifts in most traits occurred from young to intermediate-aged plots, and in all traits from young to mature

A. Catorci et al. / Acta Oecologica 43 (2012) 29e41 Table 6 Results of partial redundancy analyses (adjusted R2) performed using absolute abundance data of trait states (Hellinger-transformed), constrained by light intensity (L), air temperature (T), soil moisture (M), and soil nutrients content (N). The analyses were run on the whole data set, and on data sets composed of age classes 1 and 2, and age classes 2 and 3. Adjusted R2 (R2adj ¼ 1  [(n  1)/(n  m  1)](1  R2), where n is the number of objects and m is the number of explanatory variables) were calculated to produce unbiased estimates of the contributions of the independent variables to the explanation of the response variables. Importance of both single and joint effects of environmental variables are shown. Significance of the adjusted R2 was tested with 1,000 permutations (*P < 0.05; ***P ¼ 0.001; n.s.: not significant). The joint fractions and residuals could not be tested for significance. Negative values can be considered as null. Effect of variables

L T M N Joint effect of variables L and T L and M T and M L and N T and N M and N L, T, and N L, M, and N T, M, and N L, T, and M L, T, M, and N Residuals

Adjusted R2 Whole trait data set

Age classes 1 and 2

Age classes 2 and 3

0.0646*** 0.0139 (n.s.) 0.0019 (n.s.) 0.0161*

0.1044*** 0.0005 (n.s.) 0.0093 (n.s.) 0.0205 (n.s.)

0.0185 (n.s.) 0.0249* 0.0074 (n.s.) 0.0091 (n.s.)

0.0039 0.0034 0.0077 0.0042 0.0126 0.0106 0.0029 0.0129 0.0105 0.0158 0.0006 0.8585

0.0043 0.0012 0.0043 0.0163 0.0074 0.0008 0.0032 0.0009 0.0073 0.0098 0.0014 0.8849

0.0002 0.0002 0.0091 0.0263 0.0122 0.0106 0.0016 0.0338 0.0106 0.0021 0.0057 0.8938

plots (Table 2). After the first regenerative phase, species with traits associated with high persistence in time and preferential resource allocation to storage prevailed. These findings are consistent with those of Bazzaz (1996), Garnier et al. (2004), Huston and Smith (1987), and Newell and Tramer (1978), who found that changes in plant traits in a forest succession point to the replacement of fastgrowing species, acquiring external resources rapidly, which dominate the early stages, by slower growing species, which tend to conserve more efficiently internal resources. As stated by Grime et al. (1997), this pattern appears to reflect a trade-off between attributes conferring an ability for high rates of resource acquisition in productive habitats (acquisitive traits), such as in the high light conditions of young stands, and those responsible for retention of resource capital in unproductive conditions (retentive traits), such as in the shaded understory of mature stands. In intermediate-aged plots, a group of indicator traits and strategies that increase significantly their abundance from young plots, including early flowering rhizomatous geophytes and spring green leaves, has been identified (Tables 3 and 4). This set of trait states, related to intermediate light conditions (Fig. 1), is mostly associated with small vernal geophytes. A similar trend for vernal geophytes was observed by Decocq et al. (2004) in coppices with standards of Northern France. Such species exhibit early leaf and flower production, which allows them to differentiate their temporal niche from tree and shrub species. They can exploit the early spring peak of photosynthetically active radiation before leaves of trees emerge (Anderson, 1964; Graves, 1990; Mitchell, 1992; Pons, 1976); thereby reducing interspecific competition (Newell and Tramer, 1978), and, probably, avoiding summer drought stress. Vegetative spread by runners, which get to its maximum value in this phase, enables species to maximize the competitive ability by exploiting neighbouring niches (Friedman and Alpert, 1991). In this regeneration stage, this could be a winning strategy, because available photosynthetically active

37

radiation is not homogeneous, owing to the incomplete tree canopy closure. Our findings seem to highlight that in plots of intermediateaged stands the environmental conditions are similar to those of the forest edge, in which the available light at the ground level is lowered by the forest canopy. Nevertheless the other environmental conditions (temperature first of all) are not so far from those of open or semi-open environments. Indicator trait states of the last age class include the presence of rhizomes as storage organs and mesomorphic/hygromorphic leaves (Table 3), that are linked to nutrient-rich and moist soils and to low light intensity (Fig. 1). Species that have such traits are Aremonia agrimonoides, Epipactis helleborine, Euphorbia dulcis, Hieracium racemosum, Lathyrus venetus, L. vernus, Sanicula europaea, and Viola reichenbachiana. Underground structures improve the water and nutrients uptake of plants, hence increasing the likelihood to establish in the forest undergrowth (Newell and Tramer, 1978). Furthermore, the importance of rhizomes (indicator trait of old stage) and of runners (the most abundant trait state in this phase) can be attributed to the advantage of fast vegetative spread and growth below ground (Kenderes and Standovár, 2003). The observed decreasing trend of abundance of species not endowed with vegetative propagation modes (i.e., species that propagate exclusively by sexual reproduction) along the regeneration stages, is consistent with the results of other studies (e.g., Newell and Tramer, 1978; Silvertown, 2008; van Groenendael et al., 1996; Vandepitte et al., 2009). Such scenario suggests that sexual reproduction is reduced under closed canopies of older succession stages, while clonal growth is generally less abundant in disturbed habitats and more abundant in shaded ones. The increase in the abundance of mesomorphic/hygromorphic leaves and of hygromorphic and hygromorphic/helomorphic leaves (Table 4) along the chronosequence is probably filtered by the occurrence of microclimatic conditions that are typical of dense forests, as indicated by the temperature bioindicator value showing significant differences between plots of intermediate-aged and mature stands. The litter deposition due to the seasonal leaf fall, and the related soil humification could play an important role in the characterization of the trait set of the last regeneration stage. The decreasing abundance of small vernal geophytes from intermediate-aged to mature plots (Tables 4 and 5) could be due to litter accumulation on the forest floor, which could decrease the chance of resource uptake (Decocq and Hermy, 2003). Indeed, litter has been found to be an important limiting factor of vernal herbs (Al-Mufti et al., 1977; Sydes and Grime, 1981). Hence, in mature plots both environmental features and trait composition seem to indicate that the regenerative processes get to a new stage. Indeed, not only the light available at the ground level is lowered by the forest canopy (as it happens in intermediate-aged plots), but also the other environmental conditions differ from those of open environments. In the last phase of the regenerative cycle, the environmental conditions and the indicator traits seem to fit with the characteristics of the late-successional species (Huston and Smith, 1987), which may be considered as “ancient forest species” (Hermy et al., 1999; Peterken, 1974; Putman, 1994; Rackham, 1980; Whitney and Foster, 1988). They are more shade-tolerant, prefer moist soils, and have a lower competitive ability than the generalist forest species. Their poor ability to colonize new forest sites may be attributed to their limited dispersal abilities, low diaspore production and recruitment problems (Hermy et al., 1999). Nevertheless, the not significant change in soil nutrients bioindicator value from intermediateaged to mature plots could mean that the soil properties and the related trait set would have the potential for further variation if coppice turnover was longer, allowing the optimal mineralization of the organic matter and release of available nutrients for plants.

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A. Catorci et al. / Acta Oecologica 43 (2012) 29e41

Finally, persistent green leaves gain a higher relative weight as the forest regeneration proceeds (Table 5). It is known that persistent green leaves offer an advantage under stressing environmental conditions (in which resource uptake is limited) because evergreen plants can photosynthesize throughout the year without seasonal photosynthetic tissue regrowth (Al-Mufti et al., 1977; Grime, 1977, 2001). Moreover, shade-tolerant plants tend to remain green throughout the year (Hughes, 1975; Kubicek and Brechtl, 1970), probably due to the presence of a large number of basal leaves during the winter, which promotes spring flowering and sexual reproduction, as also observed by van Calster et al. (2008).

5. Conclusions Our findings indicate that changes in environmental conditions that happen during forest recovery after felling, filter different groups of plant traits in the herb layer of the O. carpinifolia coppiced forests. However, very few functional traits disappear along the chronosequence. This seems to indicate a certain stability of the forest understory, probably due to the short coppicing rotation cycle that allows most plants to persist even during the less favourable phases of the regenerative chronosequence. Only short life-cycle species with acquisitive strategies, disappeared in the intermediate and late successional phases. In the intermediate-aged plots, the shadow cast by O. carpinifolia suckers acts as a filter for species of the understory. Resource uptake and sexual reproduction are placed in a short temporal niche between the end of winter cold stress and tree canopy closure. The abundance of species which have only sexual reproduction decreases, conversely cover percentage of species endowed with vegetative propagation modes increases. Species with traits that confer adaptation for the environmental conditions of old forests are less abundant than in the last regenerative phase. In plots of mature stands species show retentive strategies aimed at resource storage in below-ground organs (rhizomes) and have leaves that are well adapted to the microclimatic conditions of an ancient forest. Indeed, as argued by Grime (2001), in shaded habitats, the ability to compete is likely to be of secondary importance to the capacity to tolerate shade conditions.

The research outputs suggest that in submediterranean region the 25-years long traditional coppicing cycle could be optimal to preserve non-specialist forest species, getting to a higher value of species richness. Nevertheless, it seems to be not very adequate for the late successional species. Indeed, they are prone to restrict to shelter niches and, as indicated by Catorci et al. (2011b), these species have a low ability to colonise the forest understory. In fact, their absolute weighted abundance does not change dramatically along the regenerative chronosequence (Table 4). Instead, the trait states indicators of the first successional stage strongly decrease both in absolute and in relative weighted abundance within the intermediate-aged and mature stands. Hence, some different or integrated types of management could be useful (e.g., a longer coppicing turnover, a patchy distribution of forest management types, leaving some stands unmanaged or releasing a high density of standards). Such approach should allow the maintenance of the traits composition of O. carpinifolia forests, therefore their ecosystem functionality (Díaz et al., 2004; Hooper et al., 2005; Lavorel et al., 2011). Role of the funding source The funding sources had no involvement in study design, in the collection, analysis, interpretation of data, in the writing of the report, and in the decision to submit the article for publication. Role of authors Andrea Catorci - coordination of research and text processing. Alessandra Vitanzi, Federico Maria Tardella - data collection. Vladimir Hrsak, Federico Maria Tardella - statistical elaboration Acknowledgements This research was supported by University of Camerino Research Funds assigned to Prof. Catorci Andrea and a grant of the School of Advanced Studies, PhD Course in Environmental Sciences and Public Health, University of Camerino (Italy), assigned to Dr. Alessandra Vitanzi. We would to thank Sheila Beatty for the linguistic revision of the manuscript.

Appendix List of the traits considered in the study and of their states; trait description, and data sources. Trait

Trait states

Storage organs Absent; bulb; bulbil; hypocotyl bulb; pleiocorm; primary storage root; rhizome-like pleiocorm; rhizome; root tuber; runner; runner-like rhizome; succulence; tuft Vegetative Absent (only sexual propagation reproduction); bulb; bulbil; fragmentation; innovation bud with root tuber; rhizome; rhizome-like pleiocorm; root shoot; runner; runner-like rhizome Life form Biennial hemicryptophytes; bulbous geophytes; caespitose hemicryptophytes; chamaephytes; creeping hemicryptophytes; rhizomatous geophytes; rosulate hemicryptophytes; scapose hemicryptophytes; therophytes

Description

Data source

Type of storage organ identified following Krumbiegel (2002). The presence of storage organs is in most cases closely related to the capacity for vegetative reproduction and spread. For this reason storage organs include almost all the forms of vegetative propagation. Species may have more than one type of storage organ (e.g., tuft/rhizome; pleiocorm/primary storage root). Each combination of storage organs was considered in statistical elaborations. Type of vegetative propagation, identified following Krumbiegel (2002). Species may have more than one vegetative propagation mode (e.g., runner/rhizome; runner/root shoot; rhizome/root shoot). Each combination of vegetative propagation modes was considered in statistical elaborations.

Klotz et al. (2002), checked and supplemented by field observations

Location of perennating organs as an adaptation used by plants to overcome the adverse seasons, according to Raunkiaer (1934) classification

Klotz et al. (2002), checked and supplemented by field observations

Pignatti (1982); checked by field observations

A. Catorci et al. / Acta Oecologica 43 (2012) 29e41

39

(continued ) Trait

Trait states

Leaf anatomy

Helomorphic; hygromorphic; mesomorphic; scleromorphic; succulent

Description

Data source

Main structures within the leaves to fulfil specific tasks (e.g., aeration, supporting tissues, water storage), identified following Klotz and Kühn (2002) and Küster et al. (2010). Species may have more than one type of leaf anatomy (e.g., scleromorphic/ mesomorphic; mesomorphic/hygromorphic). Each combination of leaf anatomy types was considered in statistical elaborations. Leaf persistence Overwintering green; persistent Classification of how long a leaf persist on green; spring green; summer green a plant from emergence until cast, according the categories indicated in Klotz and Kühn (2002) Flowering Early spring; mid-spring-late Flowering period of each species, classified in six phenology spring; late spring-late summer; categories (early spring; from mid-spring to late early autumn; midsummer- early spring; from late spring to late summer; from autumn; mid-summer-late summer mid-summer to late summer; from mid-summer to early autumn; early autumn) Seed weight 0.01e0.20 mg; 0.21e0.50 mg; Seed weight categorized in classes (Hodgson et al., 1995; modified) 0.51e1.00 mg; 1.01e2.00 mg; 2.01e4.00 mg; 4.01e10.00 mg; 10.01e50.00 mg

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