Seasonal variability of biomass, total leaf area and specific leaf area of forest understory herbs reflects their life strategies

Forest Ecology and Management 374 (2016) 71–81

Contents lists available at ScienceDirect

Forest Ecology and Management journal homepage: www.elsevier.com/locate/foreco

Seasonal variability of biomass, total leaf area and specific leaf area of forest understory herbs reflects their life strategies Andrzej M. Jagodzin´ski a,b,⇑, Marcin K. Dyderski a,b, Katarzyna Rawlik a, Beata Ka˛tna b a b

Polish Academy of Sciences, Institute of Dendrology, Parkowa 5, 62-035 Kórnik, Poland ´ University of Life Sciences, Faculty of Forestry, Department of Game Management and Forest Protection, Wojska Polskiego 71c, 60-625 Poznan ´ , Poland Poznan

a r t i c l e

i n f o

Article history: Received 24 January 2016 Received in revised form 2 April 2016 Accepted 26 April 2016 Available online 8 May 2016 Keywords: Understory vegetation Biomass production Seasonal dynamics Deciduous forest Reproduction effort

a b s t r a c t Seasonal variability of forest understory herbs is not well understood and there are almost no data about seasonal changes of individual plant biomass and specific leaf area (SLA) of this functional group, even though they are a crucial element of forest ecosystem plant biodiversity. The aim of the study was to characterize the seasonal variation of individual aboveground standing biomass, total leaf area and SLA of understory herbaceous species during a growing season. The study was conducted in the Czmon´ Forest (W Poland; 52°150 N, 17°050 E) and covered 12 plant species, i.e. Aegopodium podagraria, Alliaria petiolata, Anemone nemorosa, Anemone ranunculoides, Asarum europaeum, Corydalis cava, Ficaria verna, Galium aparine, Galeobdolon luteum, Hepatica nobilis, Maianthemum bifolium and Paris quadrifolia. Plants were harvested 14 dates, between the 109th and 287th day of year. In all species there were statistically significant differences (p < 0.05) in SLA and total leaf area among harvest dates and in individual plant biomass for all except two species (A. ranunculoides and G. aparine). Changes in SLA and total leaf area were related to changes in light conditions during the growing season. However, responses of the species studied to seasonal changes of light availability were different: those species which persisted through the whole sampling period differed from spring ephemerals, which resulted in different patterns of biomass production and SLA seasonal variation. In most cases, flowering individuals had lower SLA than vegetative plants, which may indicate that light availability is more important than light use efficiency for their generative propagation. Ó 2016 Elsevier B.V. All rights reserved.

1. Introduction Although contribution of the understory to total plant biomass of forest ecosystems is relatively small (c.a. 1–2%), understory plants can have a 20-fold higher share of micro- and macroelement cycling (Yarie, 1980; Gilliam, 2007; Muller, 2014). Species composition and diversity of understory plant communities strongly depends on overstory species composition and canopy closure (Augusto et al., 2003; Barbier et al., 2008; Jagodzin´ski and Oleksyn, 2009; Ampoorter et al., 2015). This impact of tree stands most frequently results from modification of nutrient cycling (Finzi et al., 1998a; Reich et al., 2005; Hobbie et al., 2006, 2007, 2010), pH (Finzi et al., 1998b; Dauer et al., 2007; Mueller et al., 2012), or light availability (Knight et al., 2008; Jagodzin´ski and Oleksyn, 2009;

Abbreviations: DIFN, diffuse non-interceptance; SLA, specific leaf area.

⇑ Corresponding author at: Polish Academy of Sciences, Institute of Dendrology, Parkowa 5, 62-035 Kórnik, Poland. E-mail address: [email protected] (A.M. Jagodzin´ski). http://dx.doi.org/10.1016/j.foreco.2016.04.050 0378-1127/Ó 2016 Elsevier B.V. All rights reserved.

Niinemets, 2010; Mueller et al., 2016). Understory species richness and diversity is positively correlated with overstory species richness and diversity. However, some species of trees, due to high leaf area index, which limits the amount of light available to understory plants, limit the understory species richness and diversity (Mölder et al., 2008; Chmura, 2013). Understory species composition may also influence the density and survival rates of natural regeneration of canopy trees (Gilliam, 2007; Gilliam and Roberts, 2014), which is crucial for further tree stand species composition (Baraloto et al., 2005). Functional diversity of plant species allows their coexistence in the same habitats and results from seasonal dynamics of light availability through the growing season. Some temperate deciduous forest understory plant species are adapted to higher light availability in the spring. The amount of light reaching the forest floor is highest in early spring when foliage of canopy trees has not yet developed. Species typical of early-spring (spring ephemerals) differ from summer-green and semi-evergreen species in relative biomass accumulation patterns (Rothstein and Zak, 2001) and

72

´ ski et al. / Forest Ecology and Management 374 (2016) 71–81 A.M. Jagodzin

in photosynthesis rate (Lapointe, 2001; Neufeld and Young, 2014). These species are geophytes, storing carbohydrates in tubers or bulbs, which allows them to quickly develop foliage and efficiently use the period of increased light availability (Dafni et al., 1981; Rothstein and Zak, 2001; Neufeld and Young, 2014). When canopy foliage cover is at its maximum, the understory is dominated by species with other life strategies, most frequently hemicryptophytes (Ellenberg, 1988; Jagodzin´ski et al., 2013; Gilliam and Roberts, 2014; Neufeld and Young, 2014), usually with summergreen leaves and lower light requirements (Ellenberg, 1988; Rothstein and Zak, 2001; Ellenberg and Leuschner, 2010; Neufeld and Young, 2014). Thus, seasonal dynamics of temperate deciduous forest understory shapes its functional and species diversity (Hunt and Cornelissen, 1997; Small and McCarthy, 2003; Gilliam, 2007; Muller, 2014). Geophytes compose 90% of understory plant community biomass production during their spring emergence, however hemicryptophytes, which are the most frequent life form of woodland herbaceous plant species, compose over 90% of understory plant community biomass during summer (Jagodzin´ski et al., 2013). Seasonal dynamics of understory biomass production is poorly understood. For example, Tremblay and Larocque (2001) found that understory biomass differed statistically significantly among harvest dates only in one of the four types of forests studied. However, Rawlik et al. (2012) and Jagodzin´ski et al. (2013) found that the difference between minimum and maximum understory plant biomass was almost tenfold during the growing season. Opposite to the situation for trees and field or meadow plants, growth patterns and traits of which have been studied in detail, few forest understory species have been included in experimental sets of species (Poorter and Remkes, 1990; Hunt and Cornelissen, 1997; Poorter and De Jong, 1999; Rothstein and Zak, 2001; Curt et al., 2005; Ma et al., 2010; Wang et al., 2010), and most frequently these species were pooled with other herbaceous plants. The exceptions are invasive species of herbaceous plants, for example Impatiens parviflora or I. glandulifera (Perglová et al., 2009; Godefroid and Koedam, 2010; Chmura, 2014), for which detailed assessments of individual traits were done. Only Rothstein and Zak (2001) studied photosynthetic response of three forest herbs to find the differences among their life strategies. In most cases data on herbaceous plant biomass considers the plant community or populations of several species, and given values are expressed as biomass per area unit, not per individual. In our previous studies (Jagodzin´ski et al., 2013; Rawlik et al., 2012) we studied seasonal variation in biomass standing crop of the understory of oakhornbeam forest, and although we provided detailed data about net primary production of the most frequent species, we did not study the individual plant traits in detail. Surprisingly, our literature review also found that there is no information about differences in biomass and specific leaf area (SLA) between flowering and vegetative individuals of forest understory plant species. At this time our knowledge about dynamics of foliage development and SLA during the growing season is scarce. Only Wilson et al. (2000) and Tremblay and Larocque (2001) found that there is variation in SLA of herbaceous understory species within the growing season. However, they did not study this phenomenon for individual species, but for the whole group of understory herbs. Thus, there is a clear lack of data about seasonal dynamics of SLA for forest understory herbaceous plants. The aim of the study was to characterize the seasonal variation of individual aboveground standing biomass, total leaf area and SLA, during a growing season for 12 herbaceous plant species (which compose the understory of a deciduous forest), based on their life histories and ecological requirements. The secondary aim of the study was to assess the differences in parameters studied between flowering and vegetative individuals. We hypothesized that spring ephemerals would show different dynamics of

biomass and SLA than species which persist in the understory during the whole growing season, due to differences in morphology and ecology of these groups (Dafni et al., 1981; Lapointe, 2001; Small and McCarthy, 2003; Neufeld and Young, 2014). We also hypothesized that flowering individuals would have higher SLA than vegetative ones within the same species and time period. We stated this assumption because higher SLA is connected with higher leaf photosynthesis efficiency (Poorter and De Jong, 1999; Cornelissen et al., 2003; Wright et al., 2004). 2. Materials and methods 2.1. Study area The study was conducted in the Czmon´ Forest (Babki Forest District, W Poland; 52°150 N, 17°050 E). According to meteorological data from Babki Forest District, the mean annual temperature in 2004–2008 was 8.5 °C and mean annual precipitation was 507 mm. The study area is located in a deciduous forest complex, where the most abundant plant community is deciduous forest with Quercus robur, Carpinus betulus, which by the phytosociological approach is named Galio sylvatici-Carpinetum (Ellenberg, 1988; Ratyn´ska et al., 2010). Detailed descriptions of this plant community in close vicinity of the study area were given by Wiczyn´ska et al. (2013), Horodecki et al. (2014) and Rawlik et al. (2015). 2.2. Species studied We studied 12 species of vascular plants, which are the most abundant in the understories of deciduous forests in Central Europe (Ellenberg, 1988): Aegopodium podagraria, Alliaria petiolata, Anemone nemorosa, Anemone ranunculoides, Asarum europaeum, Corydalis cava, Ficaria verna, Galium aparine, Galeobdolon luteum, Hepatica nobilis, Maianthemum bifolium, and Paris quadrifolia. These species differed by their ecological requirements and life-history traits (Table A.1). 2.3. Methods In the study area four 50  50 m experimental plots were established. Plant biomass was assessed by the harvest method. Plants were harvested on 14 dates, between the 109th and 287th day of year (19-Apr-2013 to 04-Oct-2013), with two-week intervals, except for the second harvest, which was performed one week after the first. Plants were randomly selected within the experimental plots. A single stem was treated as a single individual, and individuals damaged by herbivores were excluded from the sample. Flowering plants were treated separately to assess the differences between flowering and non-flowering individuals. We planned to harvest 15 (or in sufficient conditions 30) individuals of each species at each harvest date, however due to their seasonal dynamics, the number actually harvested was limited (Table A.2). Moreover, we excluded from statistical analyses two harvests of A. nemorosa and A. ranunculoides, which occurred a month after their emergence. To obtain information about changes of light availability over the spring (during foliage development) we measured canopy openness (diffuse non-interceptance, DIFN) using an LAI-2200 plant canopy analyzer (Li-Cor Inc., Lincoln, NE, USA). We followed methods described by Machado and Reich (1999) and Knight et al. (2008). Results of four to six series of 20 measurements at each date have been shown as means with 95% confidence intervals (Fig. 1). All harvested individuals were packed into envelopes, unfolded and transported to the laboratory, and separated into biomass

´ ski et al. / Forest Ecology and Management 374 (2016) 71–81 A.M. Jagodzin

73

Fig. 1. Mean (±95% CI) canopy openness (diffusive non-interceptance; DIFN) of the study area during the period of canopy foliage development. Differences in DIFN between dates of light measurements were tested by one-way ANOVA and Tukey’s posteriori test – values marked with the same letter do not differ significantly.

components: leaves, stems and flowers. Leaves which were suitable for scanning (according to Cornelissen et al. (2003)), were separated from other plant material. All material was dried in an oven with forced air circulation at 65 °C (ULE 600, Memmert GmbH + Co. KG, Germany), to a constant mass. Then, plant material was weighted using BP 210 S (Sartorius, Göttingen, Germany) and Mettler Toledo PG 1003-S scales, with an accuracy of 0.0001 g. Leaves were scanned and processed using WinFOLIA 2003 software (Regent Instruments Inc., Quebec, Canada) to measure their leaf area. From the area and leaf dry biomass of scanned leaves, specific leaf area (SLA) was calculated. Total leaf area of each individual was calculated from multiplication of SLA and total leaf biomass per plant.

2.4. Data analysis Before statistical analysis, trait data were log transformed. Differences in the parameters studied between harvest terms were assessed using one-way analysis of variance (ANOVA), followed by Tukey’s test. To assess the differences between flowering and vegetative individuals in each harvest, Student’s t-test was applied in harvests of species where at least three replications of each variant were present. This procedure was applied to firstly assess the differences among harvest dates, and secondly to assess differences between flowering and vegetative individuals at the same harvest dates. We did not apply two-way ANOVA due to gaps in observation sequences of flowering individuals, connected with the sampling protocol and uneven flowering periods of the species at the study site. All analyses were conducted in R software (R Core Team, 2015) and JMP 10.0.0 (www.jmp.com).

3. Results Standing biomass differed among herb species and harvest dates. Only five species were present during the whole sampling period: A. podagraria, A. europaeum, G. luteum, H. nobilis and M. bifolium. The lowest number of harvests was of C. cava (four dates), while A. nemorosa, A. ranunculoides, F. verna, G. aparine and P. quadrifolia were harvested on five dates. Light availability (expressed as DIFN) decreased from 0.4–0.45 to less than 0.1 over one month (April; Fig. 1) and then was almost constant.

Table 1 Mean (±SE) traits of the species studied. Values marked with the same letter within columns do not differ significantly at p < 0.001, based on one-way ANOVA and Tukey’s posteriori test. Parameter species

Spring ephemerals Alliaria petiolata Anemone nemorosa Anemone ranunculoides Corydalis cava Ficaria verna Galium aparine Paris quadrifolia

Biomass (g)

SLA (cm2 g1)

Leaf area (cm2)

Mean

SE

Mean

SE

Mean

SE

0.3962a 0.0753de 0.0428e

0.0343 0.0031 0.0018

469.54bc 337.87de 457.19c

18.54 6.82 17.61

75.14a 17.13e 11.49f

5.39 0.74 0.53

0.1076d 0.0891d 0.0651de 0.2090c

0.0078 0.0042 0.0042 0.0192

482.25b 309.00ef 481.76bc 636.61a

14.00 6.51 29.59 15.58

28.43d 18.66e 15.87ef 69.51a

1.52 0.92 1.26 4.61

362.36d

4.92

55.34b

2.59

Species present during the whole season Aegopodium 0.2507bc 0.0146 podagraria Asarum europaeum 0.2429bc 0.0079 Hepatica nobilis 0.2030c 0.0087 Galeobdolon luteum 0.2795b 0.0148 Maianthemum 0.0719de 0.0021 bifolium

g

214.35 225.02g 305.89f 418.07c

3.54 5.94 5.64 4.57

bc

38.86 37.68cd 38.33c 18.06e

1.25 1.71 1.49 0.39

All parameters studied differed among species (p < 0.001; Table 1). The highest mean individual biomass was of A. petiolata (0.3962 ± 0.0343 g), and the lowest – of A. ranunculoides (0.0428 ± 0.0018 g). The highest mean SLA was of P. quadrifolia (636.61 ± 15.58 cm2 g1) and the lowest – of A. europaeum (214.35 ± 3.54 cm2 g1) and H. nobilis (225.02 ± 5.94 cm2 g1). The highest total leaf area per plant was of A. petiolata (75.14 ± 2.59 cm2 ind.1) and P. quadrifolia (69.51 ± 4.61 cm2 ind.1), and the lowest – of A. ranunculoides (11.49 ± 0.53 cm2 ind.1). 3.1. Patterns of seasonal biomass changes Individual standing biomass was statistically significantly different across harvest dates for 10 of 12 species studied (p < 0.01); A. ranunculoides and G. aparine were the two exceptions (Fig. 2). For A. petiolata, A. nemorosa and F. verna individual biomasses increased from the beginning of the sampling period to the end of their emergence. A similar pattern, but with higher individual

74

´ ski et al. / Forest Ecology and Management 374 (2016) 71–81 A.M. Jagodzin

Fig. 2. Mean (±SE) plant (both flowering and vegetative individuals) individual biomass of the species studied at 14 harvest dates. Values with the same letter do not differ significantly at p-levels: ⁄⁄⁄ – p < 0.005, ⁄⁄ – p < 0.01, ⁄ – p < 0.05, ns – not significant (p > 0.05), based on one-way ANOVA and Tukey’s posteriori test. Spring ephemerals are indicated by green panel titles and species present during the whole season, by grey panel titles. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

biomass at the beginning of the growing season, was observed in C. cava and P. quadrifolia. In species which were present throughout the whole sampling period, maximum individual biomass of G. luteum was reached on 04-May-2013, of A. podagraria on 29-Jun2013 and the other species (A. europaeum, H. nobilis and M. bifolium) – at the end of sampling period (in September). There were statistically significant differences between individual plant biomass of flowering and vegetative individuals of several species. In harvest times where comparisons were possible (A. nemorosa, A. ranunculoides, A. europaeum, C. cava, F. verna and P. quadrifolia), generative individuals had statistically significantly (p < 0.05) higher biomass than vegetative shoots (Fig. 3). Other species expressed statistically significant differences only on some harvest dates: A. podagraria, A. petiolata, G. luteum and M. bifolium. Generative and vegetative individuals of H. nobilis did not differ statistically significantly (p > 0.05) in biomass. For G. aparine comparison was impossible due to an insufficient number of plants.

species, SLA had statistically significantly lower values on the third harvest date before the last. In the cases of A. europaeum, G. luteum and H. nobilis, the highest values of SLA were obtained near the beginning of the growing season, in the fourth (A. europaeum and G. luteum) or second (H. nobilis) harvest date. Most species did not have statistically significant differences in SLA between flowering and vegetative individuals (p > 0.05). Only for four species (G. luteum, H. nobilis, M. bifolium and P. quadrifolia) were there statistically significant differences (p < 0.05), but only on some harvest dates (Fig. 5). In most cases, when differences were statistically significant, SLA of vegetative individuals were higher than flowering individuals. When differences were not statistically significant, vegetative individuals also had higher SLA than flowering ones. An exception was H. nobilis, where SLA of flowering plants was always higher than vegetative. Also, on some harvest dates of other species, especially G. luteum, SLA of flowering individuals was higher than vegetative.

3.2. Patterns of specific leaf area seasonal variability

3.3. Patterns of foliage development

Differences in SLA among harvest terms were statistically significant (p < 0.001, except for P. quadrifolia, where p < 0.05, Fig. 4). For A. petiolata, A. nemorosa, A. ranunculoides, C. cava, F. verna, G. aparine and P. quadrifolia, mean SLA was increasing at the beginning of the growing season, however the maximum values were reached not at the last harvest where these species were present, but at the harvest just before the last. Similar tendencies occurred for the cases of A. podagraria and M. bifolium, but for these

The study indicated statistically significant (p < 0.001) differences in individual total leaf area among harvest dates in all species (Fig. 6). For all species, except P. quadrifolia, total leaf area of individuals was lowest at the beginning of the sampling period. In cases of species which were present for only part of the sampling period (A. petiolata, A. nemorosa, A. ranunculoides, C. cava, F. verna, G. aparine and P. quadrifolia), the highest values were obtained in the last or one before last harvest date. Total leaf area

´ ski et al. / Forest Ecology and Management 374 (2016) 71–81 A.M. Jagodzin

75

Fig. 3. Mean (±SE) plant individual biomass of flowering (red) and vegetative (blue) understory species at 14 harvest dates. Asterisks indicate the results of Student t-test (conducted when at least three replications of each variant were present): ⁄⁄⁄ – p < 0.001, ⁄⁄ – p < 0.02, ⁄ – p < 0.05, ns – not significant. Spring ephemerals are indicated by green panel titles and species present during the whole season, by grey panel titles. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

of individuals on the harvest dates with maximum leaf area was 2– 2.5 fold higher than at the beginning of sampling period. Species which were present throughout the whole sampling period (A. podagraria, A. europaeum, G. luteum, H. nobilis and M. bifolium) had their maximum values in the middle of sampling period, and leaf area of G. luteum reached its maximum the earliest – in May, while the other species reached their maximum leaf areas in June or July. There were no statistically significant differences in total leaf area of H. nobilis from 18-May-2013 to 04-Oct-2013, however between these measurements there was high variability among individuals. There were statistically significant differences between total leaf area of flowering and vegetative individuals of several species. On harvest dates where comparisons were possible (A. nemorosa, A. ranunculoides, A. europaeum, C. cava, F. verna, G. luteum and P. quadrifolia), flowering individuals had statistically significantly (p < 0.05) higher leaf area than vegetative ones (Fig. 7), but differences were statistically significant only on some harvest dates; only in the case of A. nemorosa were all differences statistically significant (p < 0.05). However, even when differences were not statistically significant (p > 0.05), flowering individuals of these species in almost all cases had higher leaf area than vegetative ones. For other species this tendency was similar, but not statistically significant, or was impossible to compare due to low number of observations in at least one variant. For M. bifolium total leaf areas between flowering and vegetative individuals were not statistically significantly different (p > 0.05), except on two harvest dates, but in one of them total leaf area of flowering individuals

was higher (p < 0.05) than vegetative, and in the second – total leaf area of vegetative individuals was higher (p < 0.05) than flowering, and values of both variants were similar. For H. nobilis there were no statistically significant differences (p > 0.05), but leaf area of vegetative individuals was higher than that of flowering ones. 4. Discussion The study showed that total individual plant leaf area, aboveground biomass and specific leaf area strongly varied among the species and harvest dates. Therefore, response of the species studied to seasonal changes of light availability was different. Responses of species which persisted through the whole sampling period differed from responses of species which were present only in part of the growing season. Although spring ephemerals differed in absolute values of parameters studied, the pattern of their seasonal dynamics was similar. 4.1. Differences between flowering and vegetative individuals Among species which had statistically significant differences in biomass between flowering and vegetative individuals, all except A. europaeum and P. quadrifolia were spring ephemerals, which occur in early spring, before tree stand foliage development. It is interesting to hypothesize why flowering individuals reached higher biomass than vegetative ones. This phenomenon may reflect intra-specific competition, whereby individuals which acquired more resources, especially by quicker foliage production

76

´ ski et al. / Forest Ecology and Management 374 (2016) 71–81 A.M. Jagodzin

Fig. 4. Mean (±SE) specific leaf area (SLA) of the species studied (both flowering and vegetative individuals) at 14 harvest dates. Values with the same letter do not differ significantly at p-levels: ⁄⁄⁄ – p < 0.005, ⁄⁄ – p < 0.01, ⁄ – p < 0.05, ns – not significant (p > 0.05), based on one-way ANOVA and Tukey’s posteriori test. Spring ephemerals are indicated by green panel titles and species present during the whole season, by grey panel titles. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

(Dafni et al., 1981; Rothstein and Zak, 2001; Neufeld and Young, 2014), were able to afford to spend energy on generative reproduction. Although this pattern is known at the inter-species scale, there is a little known about intra-specific variability of reproductive effort. The fraction of biomass invested in generative reproduction has been measured for only a few species and there was high variation of this value (Whigham, 2004). Our study indicated that sexual reproduction usually is connected with higher biomass of individuals, which is needed to create reproductive organs. Flowering individuals often had higher total leaf area, which may confirm this finding. However, there are no studies which could be compared with our results, especially those which could also compare these patterns between different sites. SLA is considered to be one of the most important parameters in plant ecology (Poorter and Remkes, 1990; Poorter and De Jong, 1999; Rothstein and Zak, 2001; Cornelissen et al., 2003; Wright et al., 2004; Poorter et al., 2012; Wyka et al., 2012). Therefore, higher SLA allows plants to have higher efficiency of light use. One may expect that flowering individuals, those which invested resources into reproduction, should be more efficient in using the most limiting factor, which in this case is light. However, high SLA values are also typical of shaded leaves (Rothstein and Zak, 2001; Wyka et al., 2012; Neufeld and Young, 2014) and may indicate light deficiency. In this study, most cases indicated that vegetative individuals usually had higher SLA than flowering ones. Moreover, Wardle et al. (1998) found that flowering individuals of 20 grassland species competed better with a model plant – Lolium perenne than non-flowering individuals. Thus, it may indi-

cate the second interpretation – that in conditions of light deficiency there is a trade-off between reproduction and persistence (investment in SLA). In the case of clonal species, it may be also connected with resource allocation within the genet, from vegetative stems into generative, which are more important for spread of the whole plant, and are related to the size of the plant and genet density (Schmid et al., 1995; van Kleunen et al., 2001; Bogdanowicz et al., 2011; Neufeld and Young, 2014). 4.2. Specific leaf area seasonal dynamics Dynamics of SLA of each species during the growing season cannot be compared with dynamics of SLA for all herbaceous species provided by Tremblay and Larocque (2001) for two reasons: pooling of species with different SLA values together and differences in species composition described in the cited paper. However, differences between SLA values during the growing season were higher in types of forests where Erythronium americanum – a spring ephemeral – had a high fraction of spring community biomass. In these types of forests, SLA was changing in a pattern similar to that found in our study for spring ephemerals, by the first period of the growing season. In previous studies it was found that SLA is very variable among the samples, regardless of harvest term (Wilson et al., 1999). Our study indicated that there are large differences between SLA values obtained at different times. This is particularly important because SLA values taken from databases are used as predictors in many studies, for example concerning invasiveness (Grotkopp et al.,

´ ski et al. / Forest Ecology and Management 374 (2016) 71–81 A.M. Jagodzin

77

Fig. 5. Mean (±SE) specific leaf area (SLA) of flowering (red) and vegetative (blue) understory species at 14 harvest dates. Asterisks indicate the results of Student t-test (conducted when at least three replications of each variant were present): ⁄⁄⁄ – p < 0.001, ⁄⁄ – p < 0.02, ⁄ – p < 0.05, ns – not significant. Spring ephemerals are indicated by green panel titles and species present during the whole season, by grey panel titles. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

2010; Tecco et al., 2010; te Beest et al., 2015) or relatedness to urban habitats (Knapp et al., 2010; Johnson et al., 2015; Williams et al., 2015). Our data show that this variability may come from seasonal dynamics, thus database administrators should pay attention to these dynamics during data collection and processing. For example, based on traits obtained from the LEDA database (leaf area and leaf mass; Table A.1), computed SLA values may differ two-fold from mean values obtained in this study. However, despite high seasonal variability of SLA, there were statistically significant differences among species studied, which indicates species-specific patterns. SLA is strongly correlated with leaf life-span, photosynthesis efficiency (Wright et al., 2004) and dark respiration rate (Rothstein and Zak, 2001), which could indicate that the increasing trend in SLA for spring ephemerals may be a reaction to lowering light availability. This pattern was also observed for A. petiolata and G. aparine, which are typical in forest edge rather than forest interior habitats, and had the highest light indicator values among the species studied (Table A.1). A. podagraria, which has the same light indicator value as A. petiolata is indicative of a pattern similar to other species which were present throughout the whole sampling period. This may indicate that the pattern of individual species SLA dynamics depends on life-span rather than plant light requirement. For the case of species present throughout the whole sampling period, three species (A. podagraria, A. europaeum and G. luteum) reached their maximum SLA values after a large decrease of light availability during May. This may reflect optimal biomass parti-

tioning theory (Weiner, 2004; McCarthy and Enquist, 2007), which claims that plants allocate more biomass into organs responsible for acquisition of the limiting resources. Because higher SLA is connected with higher leaf photosynthetic efficiency (Wright et al., 2004), this strategy of plants – building thin and efficient leaves in conditions of limited light availability – may be the reason for their ecological success. However, a similar species – H. nobilis – reached two peaks of SLA, at the end of April and in the middle of June. This may be related to the biology of this species – H. nobilis produce leaves after flowering (during the 1st half of May, Fig. 5), and up to the time of flowering, plants use wintergreen leaves from the previous growing season (Inghe and Tamm, 1985). Therefore, the first peak of SLA may be connected with retranslocation of resources from senescing leaves (Chapin, 1980; Del Arco et al., 1991; Cornelissen et al., 1999), and the second, with the reaction of younger leaves. This supposition may be confirmed by the SLA pattern of geophytes (e.g. A. nemorosa, C. cava and F. verna), which produce new, spring-green leaves every year, which have increasing SLA over time. There are no studies about the relationship between SLA and leaf age of understory forest herbaceous plants. In deciduous tree species Reich et al. (1991) and Karavin (2014) found the highest values of SLA at the beginning and end of the growing season. Milla et al. (2008) found that there was a negative relationship between leaf age and SLA, due to storing more carbon-rich compounds in leaves. However, in the case of forest understory species, increasing SLA during the growing season most likely is connected with shading by developing canopy foliage.

78

´ ski et al. / Forest Ecology and Management 374 (2016) 71–81 A.M. Jagodzin

Fig. 6. Mean (±SE) individual leaf area of the species studied at 14 harvest dates. Labels indicate the results of one-way ANOVA between harvest terms. Values with the same letter do not differ significantly at p-levels: ⁄⁄⁄ – p < 0.005, ⁄⁄ – p < 0.01, ⁄ – p < 0.05, ns – not significant (p > 0.05), based on one-way ANOVA and Tukey’s posteriori test. Spring ephemerals are indicated by green panel titles and species present during the whole season, by grey panel titles. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

For most of the spring ephemerals, maximum SLA values were reached at the end of their period of occurrence, possibly due to nutrient retranslocation prior to leaf senescence (Chapin, 1980; Del Arco et al., 1991; Cornelissen et al., 1999). In forbs, resorption efficiency, considered as percentage of retranslocated compounds, was 41% and 42% for nitrogen and phosphorous, respectively (Aerts, 1996). 4.3. Biomass production patterns The forest geophytes studied are characterized by quick biomass production and short period of emergence. Due to belowground storage organs, these species can quickly produce foliage at the beginning of the growing season (Dafni et al., 1981) and effectively use the period with the highest light availability (Neufeld and Young, 2014). After this time, usually ended by generative propagation, their presence above ground is not economically balanced, because optimal photosynthesis temperature of spring ephemerals is lower than that of later occurring species, and higher temperatures lead to higher respiration rates (Lapointe, 2001). Also, the amount of available light decreases about tenfold from the end of March to the end of May (Fig. 1). In a pattern opposite to geophytes, hemicryptophytes maintain their foliage throughout the whole growing season. They reach the highest biomass at the end of their growth period. The exception to this observation is M. bifolium, the geophyte which reached its maximum biomass at the end of the growing season. This may result from a different life strategy (S) than other species, or an

effect of a different type of foliage (summer-green) than other geophytes (spring-green; Table A.1). Species which were present throughout the whole sampling period represented another life strategy. These species were mostly the hemicryptophytes (A. podagraria, A. europaeum and H. nobilis) or chamaephytes – G. luteum, which endure unfavorable periods (winter or drought) with buds, leaves or stems, at the ground level (Raunkiaer, 1934; Klotz et al., 2002). Therefore, to survive, these species must persist through the whole vegetative season under the tree canopy and cannot afford reproduction costs as high as geophytes, which persist through unfavorable conditions as rhizomes or tubers (Dafni et al., 1981). Geophytes also reached lower individual biomass than other species. Because G. aparine, the only therophyte among the species studied, also reached low individual biomass, it may be assumed that higher individual biomass may be connected with lifespan. Although geophytes are also perennial species, the period of their occurrence above ground is shorter than in the case of hemicryptophytes (Dafni et al., 1981). Their biomass patterns were similar – constant increment of biomass, except for A. ranunculoides, which did not show statistically significantly differences in biomass among harvest dates. Although M. bifolium is also a geophyte (Table A.1), it seems to be an exception to this rule. This species was present throughout the whole sampling period, and despite Raunkiaer’s (1934) life form classification as a geophyte, based on morphology, it represents another strategy than ‘spring ephemerals’, commonly identified with understory geophytes. However, probably specimens of M. bifolium recorded in September are the second cohort of seed-

´ ski et al. / Forest Ecology and Management 374 (2016) 71–81 A.M. Jagodzin

79

Fig. 7. Mean (±SE) leaf area of flowering (red) and vegetative (blue) individuals of the understory species at 14 harvest dates. Asterisks indicate the results of Student t-test (conducted when at least three replications of each variant were present): ⁄⁄⁄ – p < 0.001, ⁄⁄ – p < 0.02, ⁄ – p < 0.05, ns – not significant. Spring ephemerals are marked by green panel titles and species present during the whole season, by grey panel titles. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

lings, which emerged in summer, because their biomass and SLA do not indicate senescence, but rather good condition. It may be an effect of favorable climatic conditions in 2013, because in our previous studies (Rawlik et al., 2012; Jagodzin´ski et al., 2013) M. bifolium biomass and proportion of understory biomass was decreasing through the first half of September. M. bifolium had summer-green leaves, which are typical of shade-tolerant species (Neufeld and Young, 2014). This exception and similarity in biomass production patterns of species with different types of leaf persistence, indicates that type of leaf persistence is a better predictor of individual biomass production pattern than life-form, which is more often used in ecological analyses. 4.4. Comparison with community-level approaches Individual biomass increment patterns of different species shape the biomass of the plant community. Jagodzin´ski et al. (2013), discussing their results of biomass standing crop along with the results from other studies, supposed that species composition and individual species growth patterns of the plant community may strongly alter the pattern of seasonal understory production dynamics. Our results confirmed this conjecture, from the individual-based measurements, which indicated differences in standing biomass both among species and harvest terms. In addition, the seasonal variability of biomass production at the plant community level was both confirmed (Rawlik et al., 2012; Jagodzin´ski et al., 2013) and rejected (Tremblay and Larocque, 2001).

Growth pattern of A. nemorosa and G. luteum, obtained by the analysis of species biomass in community sampling (Rawlik et al., 2012; Jagodzin´ski et al., 2013), differed from the pattern obtained here via individual-based sampling. F. verna showed a similar pattern of plant biomass at individual (our study) and community levels in the study of Rawlik et al. (2012), but differed in comparison with the study of Jagodzin´ski et al. (2013). Therefore, differences in biomass patterns between individual-based and community-based approaches are a result of species abundance in the plant community, which is not included in an individuallevel approach. However, due to high variability of individual plant biomass (described in this study) and understory biomass (Rawlik et al., 2012; Jagodzin´ski et al., 2013), estimation of understory primary production and carbon sequestration may be biased by this variability. Our study found that there are statistically significant differences among species and also among harvest times at the single plant level; therefore, this variability should be taken into account during estimation of forest CO2 sequestration ability and ecosystem primary production. 5. Conclusions Our study revealed that understory plant species differed in biomass production, SLA and leaf area among species and harvest dates. Patterns of seasonal variation in biomass production and SLA among the species studied may be divided into two similar groups – spring ephemerals and species present during the whole growing season, and as these two groups differ in the period of

80

´ ski et al. / Forest Ecology and Management 374 (2016) 71–81 A.M. Jagodzin

aboveground persistence, which probably results from differential adaptation to limited light availability, connected with different species traits and seasonal variability of biomass production and SLA. In most cases, flowering individuals had lower SLA than vegetative ones, which may indicate that light availability, rather than light use efficiency, is crucial for generative propagation of forest understory herbs. Moreover, the study presents important new data at the single plant level, for accurate determination of understory primary production and carbon sequestration. Acknowledgements The study was financially supported by the Institute of Dendrology of the Polish Academy of Sciences, Kórnik, Poland, and by General Directorate of State Forests, Warsaw, Poland (research project: ‘Environmental and genetic factors affecting productivity of forest ecosystems on forest and post-industrial habitats’). We kindly thank Dr. Lee E. Frelich (The University of Minnesota Center for Forest Ecology, USA) for valuable comments to the manuscript and linguistic support. We are also thankful to the two anonymous reviewers for their precious comments on the first version of manuscript. We declare that the study complies with the current laws of Poland. Appendix A. Supplementary material Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.foreco.2016.04. 050. References Aerts, R., 1996. Nutrient resorption from senescing leaves of perennials: are there general patterns? J. Ecol. 84, 597–608. Ampoorter, E., Baeten, L., Vanhellemont, M., Bruelheide, H., Scherer-Lorenzen, M., Baasch, A., Erfmeier, A., Hock, M., Verheyen, K., 2015. Disentangling tree species identity and richness effects on the herb layer: first results from a German tree diversity experiment. J. Veg. Sci. 26, 742–755. http://dx.doi.org/10.1111/ jvs.12281. Augusto, L., Dupouey, J.-L., Ranger, J., 2003. Effects of tree species on understory vegetation and environmental conditions in temperate forests. Ann. For. Sci. 60, 823–831. http://dx.doi.org/10.1051/forest:2003077. Baraloto, C., Goldberg, D.E., Bonal, D., 2005. Performance trade-offs among tropical tree seedlings in contrasting microhabitats. Ecology 86, 2461–2472. http://dx. doi.org/10.1890/04-1956. Barbier, S., Gosselin, F., Balandier, P., 2008. Influence of tree species on understory vegetation diversity and mechanisms involved – a critical review for temperate and boreal forests. For. Ecol. Manage. 254, 1–15. http://dx.doi.org/10.1016/ j.foreco.2007.09.038. _ Bogdanowicz, A.M., Olejniczak, P., Lembicz, M., Zukowski, W., 2011. Costs of reproduction in life history of a perennial plant Carex secalina. Cent. Eur. J. Biol. 6, 870–877. http://dx.doi.org/10.2478/s11535-011-0044-6. Chapin, F.S., 1980. The mineral nutrition of wild plants. Annu. Rev. Ecol. Syst. 11, 233–260. Chmura, D., 2014. Biology and Ecology of an Invasion of Impatiens parviflora DC in Natural and Semi-natural Habitats. Wydawnictwo ATH, Bielsko-Biała. Chmura, D., 2013. Impact of alien tree species Quercus rubra L. on understorey environment and flora: a study of the Silesian Upland (southern Poland). Pol. J. Ecol. 61, 431–442. Cornelissen, J.H.C., Lavorel, S., Garnier, E., Diaz, S., Buchmann, N., Gurvich, D.E., Reich, P.B., Ter Steege, H., Morgan, H.D., Van Der Heijden, M.G.A., Pausas, J.G., Poorter, H., 2003. A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Aust. J. Bot. 51, 335–380. http://dx.doi.org/10.1071/BT02124. Cornelissen, J.H.C., Pérez-Harguindeguy, N., Díaz, S., Grime, J.P., Marzano, B., Cabido, M., Vendramini, F., Cerabolini, B., 1999. Leaf structure and defence control litter decomposition rate across species and life forms in regional floras on two continents. New Phytol. 143, 191–200. http://dx.doi.org/10.1046/j.14698137.1999.00430.x. Curt, T., Coll, L., Prévosto, B., Balandier, P., Kunstler, G., 2005. Plasticity in growth, biomass allocation and root morphology in beech seedlings as induced by irradiance and herbaceous competition. Ann. For. Sci. 62, 51–60. http://dx.doi. org/10.1051/forest:2004092. Dafni, A., Cohen, D., Noy-Mier, I., 1981. Life-cycle variation in geophytes. Ann. Mo. Bot. Gard. 68, 652–660.

Dauer, J.M., Chorover, J., Chadwick, O.A., Oleksyn, J., Tjoelker, M.G., Hobbie, S.E., Reich, P.B., Eissenstat, D.M., 2007. Controls over leaf and litter calcium concentrations among temperate trees. Biogeochemistry 86, 175–187. http:// dx.doi.org/10.1007/s10533-007-9153-8. Del Arco, J.M., Escudero, A., Garrido, M.V., 1991. Effects of site characteristics on nitrogen retranslocation from senescing leaves. Ecology 72, 701–708. Ellenberg, H., 1988. Vegetation Ecology of Central Europe. Cambridge University Press, Cambridge. Ellenberg, H., Leuschner, C., 2010. Vegetation Mitteleuropas mit den Alpen in ökologischer, dynamischer und historischer Sicht. UTB, Stuttgard. Finzi, A.C., Van Breemen, N., Canham, C.D., 1998a. Canopy tree–soil interactions within temperate forests: species effects on soil carbon and nitrogen. Ecol. Appl. 8, 440–446. http://dx.doi.org/10.1890/1051-0761(1998)008[0440:CTSIWT]2.0. CO;2. Finzi, A.C., Canham, C.D., Van Breemen, N., 1998b. Canopy tree–soil interactions within temperate forests: species effects on pH and cations. Ecol. Appl. 8, 447– 454. http://dx.doi.org/10.1890/1051-0761(1998)008[0447:CTSIWT]2.0.CO;2. Gilliam, F.S., 2007. The ecological significance of the herbaceous layer in temperate forest ecosystems. Bioscience 57, 845–858. http://dx.doi.org/10.1641/B571007. Gilliam, F.S., Roberts, M.R., 2014. Interactions between the herbaceous layer and overstory canopy of eastern forests. In: Gilliam, F.S. (Ed.), The Herbaceous Layer in Forests of Eastern North America, second ed. Oxford University Press, pp. 233–254. Godefroid, S., Koedam, N., 2010. Comparative ecology and coexistence of introduced and native congeneric forest herbs: Impatiens parviflora and I. noli-tangere. Plant Ecol. Evol. 143, 119–127. http://dx.doi.org/10.5091/plecevo. 2010.397. Grotkopp, E., Erskine-Ogden, J., Rejmánek, M., 2010. Assessing potential invasiveness of woody horticultural plant species using seedling growth rate traits. J. Appl. Ecol. 47, 1320–1328. http://dx.doi.org/10.1111/j.13652664.2010.01878.x. Hobbie, S.E., Ogdahl, M., Chorover, J., Chadwick, O.A., Oleksyn, J., Zytkowiak, R., Reich, P.B., 2007. Tree species effects on soil organic matter dynamics: the role of soil cation composition. Ecosystems 10, 999–1018. http://dx.doi.org/10.1007/ s10021-007-9073-4. Hobbie, S.E., Oleksyn, J., Eissenstat, D.M., Reich, P.B., 2010. Fine root decomposition rates do not mirror those of leaf litter among temperate tree species. Oecologia 162, 505–513. http://dx.doi.org/10.1007/s00442-009-1479-6. Hobbie, S.E., Reich, P.B., Oleksyn, J., Ogdahl, M., Zytkowiak, R., Hale, C., Karolewski, P., 2006. Tree species effects on decomposition and forest floor dynamics in a common garden. Ecology 87, 2288–2297. http://dx.doi.org/10.1890/0012-9658 (2006) 87[2288:TSEODA]2.0.CO;2. Horodecki, P., Wiczyn´ska, K., Jagodzin´ski, A.M., 2014. Natural regeneration in the ‘‘Czmon´” nature reserve (Wielkopolska Region). For. Res. Pap. 75, 61–75. http:// dx.doi.org/10.2478/frp-2014-0007. Hunt, R., Cornelissen, J.H.C., 1997. Components of relative growth rate and their interrelations in 59 temperate plant species. New Phytol., 395–417 Inghe, O., Tamm, C.O., 1985. Survival and flowering of perennial herbs. IV. The behaviour of Hepatica nobilis and Sanicula europaea on permanent plots during 1943–1981. Oikos 45, 400–420. Jagodzin´ski, A.M., Oleksyn, J., 2009. Ecological consequences of silviculture at variable stand densities. III. Stand stability, phytoclimate and biodiversity. Sylwan 153, 219–230. Jagodzin´ski, A.M., Pietrusiak, K., Rawlik, M., Janyszek, S., 2013. Seasonal changes in the understorey biomass of an oak-hornbeam forest Galio sylvatici–Carpinetum betuli. For. Res. Pap. 74, 35–47. http://dx.doi.org/10.2478/frp-2013-0005. Johnson, A.L., Tauzer, E.C., Swan, C.M., 2015. Human legacies differentially organize functional and phylogenetic diversity of urban herbaceous plant communities at multiple spatial scales. Appl. Veg. Sci. 18, 513–527. http://dx.doi.org/ 10.1111/avsc.12155. Karavin, N., 2014. Effects of leaf and plant age on specific leaf area in deciduous tree species Quercus cerris L. var. cerris. Bangladesh J. Bot. 42, 301–306. http://dx.doi. org/10.3329/bjb.v42i2.18034. Klotz, S., Kühn, I., Durka, W., 2002. BIOLFLOR – Eine Datenbank zu biologischökologischen Merkmalen der Gefäßpflanzen in Deutschland. Schriftenreihe für Vegetationskunde, Schriftenreihe für Vegetationskunde. Bundesamt für Naturschutz, Bonn. Knapp, S., Kühn, I., Stolle, J., Klotz, S., 2010. Changes in the functional composition of a Central European urban flora over three centuries. Perspect. Plant Ecol., Evol. Syst. 12, 235–244. http://dx.doi.org/10.1016/j.ppees.2009.11.001. Knight, K.S., Oleksyn, J., Jagodzinski, A.M., Reich, P.B., Kasprowicz, M., 2008. Overstorey tree species regulate colonization by native and exotic plants: a source of positive relationships between understorey diversity and invasibility. Divers. Distrib. 14, 666–675. http://dx.doi.org/10.1111/j.1472-4642.2008. 00468.x. Lapointe, L., 2001. How phenology influences physiology in deciduous forest spring ephemerals. Physiol. Plant. 113, 151–157. http://dx.doi.org/10.1034/j.13993054.2001.1130201.x. Machado, J.-L., Reich, P.B., 1999. Evaluation of several measures of canopy openness as predictors of photosynthetic photon flux density in deeply shaded coniferdominated forest understory. Can. J. For. Res. 29, 1438–1444. http://dx.doi.org/ 10.1139/x99-102. Ma, W., Shi, P., Li, W., He, Y., Zhang, X., Shen, Z., Chai, S., 2010. Changes in individual plant traits and biomass allocation in alpine meadow with elevation variation on the Qinghai-Tibetan Plateau. Sci. China Life Sci. 53, 1142–1151. http://dx.doi. org/10.1007/s11427-010-4054-9.

´ ski et al. / Forest Ecology and Management 374 (2016) 71–81 A.M. Jagodzin McCarthy, M.C., Enquist, B.J., 2007. Consistency between an allometric approach and optimal partitioning theory in global patterns of plant biomass allocation. Funct. Ecol. 21, 713–720. http://dx.doi.org/10.1111/j.1365-2435.2007.01276.x. Milla, R., Reich, P.B., Niinemets, Ü., Castro-Díez, P., 2008. Environmental and developmental controls on specific leaf area are little modified by leaf allometry. Funct. Ecol. 22, 565–576. http://dx.doi.org/10.1111/j.13652435.2008.01406.x. Mölder, A., Bernhardt-Römermann, M., Schmidt, W., 2008. Herb-layer diversity in deciduous forests: raised by tree richness or beaten by beech? For. Ecol. Manage. 256, 272–281. http://dx.doi.org/10.1016/j.foreco.2008.04.012. Mueller, K.E., Eisenhauer, N., Reich, P.B., Hobbie, S.E., Chadwick, O.A., Chorover, J., Dobies, T., Hale, C.M., Jagodzin´ski, A.M., Kałucka, I., Kasprowicz, M., _ Kieliszewska-Rokicka, B., Modrzyn´ski, J., Rozen, A., Skorupski, M., Sobczyk, Ł., Stasin´ska, M., Trocha, L.K., Weiner, J., Wierzbicka, A., Oleksyn, J., 2016. Light, earthworms, and soil resources as predictors of diversity of 10 soil invertebrate groups across monocultures of 14 tree species. Soil Biol. Biochem. 92, 184–198. http://dx.doi.org/10.1016/j.soilbio.2015.10.010. Mueller, K.E., Eissenstat, D.M., Hobbie, S.E., Oleksyn, J., Jagodzinski, A.M., Reich, P.B., Chadwick, O.A., Chorover, J., 2012. Tree species effects on coupled cycles of carbon, nitrogen, and acidity in mineral soils at a common garden experiment. Biogeochemistry 111, 601–614. http://dx.doi.org/10.1007/s10533-011-9695-7. Muller, R.N., 2014. Nutrient relations of the herbaceous layer in deciduous forest ecosystems. In: Gilliam, F. (Ed.), The Herbaceous Layer in Forests of Eastern North America, second ed. Oxford University Press, pp. 12–34. Neufeld, H.S., Young, D.R., 2014. Ecophysiology of the herbaceous layer in temperate deciduous forests. In: Gilliam, F. (Ed.), The Herbaceous Layer in Forests of Eastern North America, second ed. Oxford University Press, pp. 35–95. Niinemets, Ü., 2010. A review of light interception in plant stands from leaf to canopy in different plant functional types and in species with varying shade tolerance. Ecol. Res. 25, 693–714. http://dx.doi.org/10.1007/s11284-010-07124. Perglová, I., Pergl, J., Skálová, H., Moravcová, L., Jarošík, V., Pyšek, P., 2009. Differences in germination and seedling establishment of alien and native Impatiens species. Preslia 81, 357–375. Poorter, H., De Jong, R.O.B., 1999. A comparison of specific leaf area, chemical composition and leaf construction costs of field plants from 15 habitats differing in productivity. New Phytol. 143, 163–176. http://dx.doi.org/10.1046/ j.1469-8137.1999.00428.x. Poorter, H., Niklas, K.J., Reich, P.B., Oleksyn, J., Poot, P., Mommer, L., 2012. Biomass allocation to leaves, stems and roots: meta-analyses of interspecific variation and environmental control. New Phytol. 193, 30–50. http://dx.doi.org/10.1111/ j.1469-8137.2011.03952.x. Poorter, H., Remkes, C., 1990. Leaf area ratio and net assimilation rate of 24 wild species differing in relative growth rate. Oecologia 83, 553–559. http://dx.doi. org/10.1007/BF00317209. Ratyn´ska, H., Wojterska, M., Brzeg, A., Kołacz, M., 2010. Multimedialna encyklopedia zbiorowisk ros´linnych Polski. NFOSiGW, UKW, IETI. Raunkiaer, C., 1934. The Life Forms of Plants and Statistical Plant Geography. Clarendon Press, Oxford. Rawlik, K., Horodecki, P., Jagodzin´ski, A.M., 2015. Odnowienie naturalne drzew i krzewów w płatach dobrze zachowanego oraz spinetyzowanego gra˛du s´rodkowoeuropejskiego Galio sylvatici-Carpinetum (R. Tx. 1937) Oberd. 1957. Studia i Materiały CEPL w Rogowie 17, 112–124. Rawlik, M., Jagodzinski, A.M., Janyszek, S., 2012. Seasonal changes in the understorey biomass of an oak-hornbeam forest Stellario holosteae– Carpinetum betuli. For. Res. Pap. 73, 221–235. http://dx.doi.org/10.2478/ v10111-012-0022-4. R Core Team, 2015. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. Reich, P.B., Oleksyn, J., Modrzynski, J., Mrozinski, P., Hobbie, S.E., Eissenstat, D.M., Chorover, J., Chadwick, O.A., Hale, C.M., Tjoelker, M.G., 2005. Linking litter calcium, earthworms and soil properties: a common garden test with 14 tree species. Ecol. Lett. 8, 811–818. http://dx.doi.org/10.1111/j.14610248.2005.00779.x. Reich, P.B., Walters, M.B., Ellsworth, D.S., 1991. Leaf age and season influence the relationships between leaf nitrogen, leaf mass per area and photosynthesis in

81

maple and oak trees. Plant Cell Environ. 14, 251–259. http://dx.doi.org/10.1046/ j.1365-2435.1998.00208.x. Rothstein, D.E., Zak, D.R., 2001. Photosynthetic adaptation and acclimation to exploit seasonal periods of direct irradiance in three temperate, deciduousforest herbs. Funct. Ecol. 15, 722–731. http://dx.doi.org/10.1046/j.13652435.1998.00208.x. Schmid, B., Bazzaz, F.A., Weiner, J., 1995. Size dependency of sexual reproduction and of clonal growth in two perennial plants. Can. J. Bot. 73, 1831–1837. http:// dx.doi.org/10.1139/b95-194. Small, C.J., McCarthy, B.C., 2003. Spatial and temporal variability of herbaceous vegetation in an eastern deciduous forest. Plant Ecol. 164, 37–48. http://dx.doi. org/10.1023/A:1021209528643. te Beest, M., Esler, K.J., Richardson, D.M., 2015. Linking functional traits to impacts of invasive plant species: a case study. Plant Ecol., 293–305 http://dx.doi.org/ 10.1007/s11258-014-0437-5. Tecco, P.A., Díaz, S., Cabido, M., Urcelay, C., 2010. Functional traits of alien plants across contrasting climatic and land-use regimes: do aliens join the locals or try harder than them? J. Ecol. 98, 17–27. http://dx.doi.org/10.1111/j.13652745.2009.01592.x. Tremblay, N.O., Larocque, G.R., 2001. Seasonal dynamics of understory vegetation in four eastern Canadian forest types. Int. J. Plant Sci. 162, 271–286. van Kleunen, M., Fischer, M., Schmid, B., 2001. Effects of intraspecific competition on size variation and reproductive allocation in a clonal plant. Oikos 94, 515– 524. Wang, L., Niu, K., Yang, Y., Zhou, P., 2010. Patterns of above-and belowground biomass allocation in China’s grasslands: evidence from individual-level observations. Sci. China Life Sci. 53, 851–857. http://dx.doi.org/10.1007/ s11427-010-4027-z. Wardle, D.A., Barker, G.M., Bonner, K.I., Nicholson, K.S., 1998. Can comparative approaches based on plant ecophysiological traits predict the nature of biotic interactions and individual plant species effects in ecosystems? J. Ecol. 86, 405– 420. http://dx.doi.org/10.1046/j.1365-2745.1998.00268.x. Weiner, J., 2004. Allocation, plasticity and allometry in plants. Perspect. Plant Ecol., Evol. Syst. 6, 207–215. http://dx.doi.org/10.1078/1433-8319-00083. Whigham, D.F., 2004. Ecology of woodland herbs in temperate deciduous forests. Annu. Rev. Ecol. Evol. Syst. 35, 583–621. http://dx.doi.org/10.1146/annurev. ecolsys.35.021103.105708. Wiczyn´ska, K., Horodecki, P., Jagodzin´ski, A.M., 2013. Stand structure and species composition in the ‘‘Czmon´” nature reserve. Nauka Przyr. Technol. 7, #69. Williams, N.S.G., Hahs, A.K., Vesk, P.A., 2015. Urbanisation, plant traits and the composition of urban floras. Perspect. Plant Ecol., Evol. Syst. 17, 78–86. http:// dx.doi.org/10.1016/j.ppees.2014.10.002. Wilson, K.B., Baldocchi, D.D., Hanson, P.J., 2000. Spatial and seasonal variability of photosynthetic parameters and their relationship to leaf nitrogen in a deciduous forest. Tree Physiol. 20, 565–578. http://dx.doi.org/10.1093/ treephys/20.9.565. Wilson, P.J., Thompson, K.E.N., Hodgson, J.G., 1999. Specific leaf area and leaf dry matter content as alternative predictors of plant strategies. New Phytol. 143, 155–162. http://dx.doi.org/10.1046/j.1469-8137.1999.00427.x. Wright, I.J., Reich, P.B., Westoby, M., Ackerly, D.D., Baruch, Z., Bongers, F., CavenderBares, J., Chapin, T., Cornelissen, J.H., Diemer, M., Flexas, J., Garnier, E., Gulias, J., Hikosaka, K., Lamont, B.B., Lee, T., Lee, W., Lusk, C., Midgley, J.J., Navas, M.L., Niinemets, Ü., Oleksyn, J., Osada, N., Poorter, H., Poot, P., Prior, L., Pyankov, V.I., Roumet, C., Thomas, S.C., Tjoelker, M.G., Veneklaas, E.J., Villar, R., 2004. The worldwide leaf economics spectrum. Nature 428, 821–827. http://dx.doi.org/ 10.1038/nature02403. _ Wyka, T.P., Oleksyn, J., Zytkowiak, R., Karolewski, P., Jagodzin´ski, A.M., Reich, P.B., 2012. Responses of leaf structure and photosynthetic properties to intra-canopy light gradients: a common garden test with four broadleaf deciduous angiosperm and seven evergreen conifer tree species. Oecologia 170, 11–24. http://dx.doi.org/10.1007/s00442-012-2279-y. Yarie, J., 1980. The role of understory vegetation in the nutrient cycle of forested ecosystems in the mountain hemlock biogeoclimatic zone. Ecology 61, 1498– 1514. http://dx.doi.org/10.2307/1939057.