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Changes in biomass allocation in species rich meadow after abandonment: Ecological strategy or allometry?
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Research article
Changes in biomass allocation in species rich meadow after abandonment: Ecological strategy or allometry? ˇ epán Janeˇcek a,c , Vojtˇech Lanta b,d , Jitka Klimeˇsová a Alena Bartuˇsková a,∗ , Jiˇrí Doleˇzal a,b , Stˇ a
Institute of Botany, Czech Academy of Sciences, Dukelská 135, 379 01 Tˇrebon, ˇ Czech Republic ˇ University of South Bohemia, Faculty of Sciences, Department of Botany, Braniˇsovská 31, 370 05 Ceské Budˇejovice, Czech Republic c Department of Ecology, Faculty of Science, Charles University in Prague, Viniˇcná 7, 128 44 Praha 2, Czech Republic d University of Turku, Department of Biology, Section of Ecology, FIN-20014, Turku, Finland b
a r t i c l e
i n f o
Article history: Received 3 October 2014 Received in revised form 29 May 2015 Accepted 9 June 2015 Available online xxx Keywords: Abandonment Allometry Biomass allocation Community Mowing Species-rich meadow
a b s t r a c t Plants respond to changes in biotic and abiotic conditions by altering the allocation of biomass to organs with different functions. The degree to which this response is limited by architectural constraints and follows the rules of the allocation theory has rarely been studied at the community level for several reasons: environmental factors affecting plants in a community are of complex nature with contradictory effects, plants in a community tend to be similar in size, which limits the capability to recognize allometry, and only rarely are plant communities so species rich that robust regression analysis is feasible. We tested whether the often reported effect of meadow abandonment increasing investment into supportive structures due to an increasing competitive milieu is caused by changed allocation strategy of resident species or by an allometric effect. For the study we examined biomass allocation to leaf blades, petioles and stems in 41 plant species in two species rich temperate European meadows differing in water availability (dry versus wet) and subjected to abandonment. Biomass allocation between organs with supportive versus photosynthetic function in meadow species followed a general allocation pattern (allometric exponent 0.75), irrespective of the management. The observed changes in relative investment into supportive structures after abandonment were caused only by the increasing size of the resident species. The effect was restricted to wet meadow, while in dry meadow the reaction of the species was diverse – probably due to low competition after abandonment. © 2015 Geobotanisches Institut ETH, Stiftung Ruebel. Published by Elsevier GmbH. All rights reserved.
Plant nomenclature Kubát et al. (2002). Introduction One of the basic questions in comparative plant ecology is how plants allocate their resources to different functions (Bazzaz and Grace, 1997). The allocation of biomass to plant organs is presumed to be a reflection of actual plant life function demands, but this has its constraints. For example, when biomass is allocated to one organ or function, it is at the expense of other organs or functions; this implies trade-offs (Weiner, 2004). Furthermore, biomass allocation is limited by architectural constraints and these change with plant size. Between individual organs there are, therefore, frequent allo-
∗ Corresponding author. Tel.: +420 384 721 156. E-mail address: [email protected] (A. Bartuˇsková).
metrically scaled relationships (Niklas, 1994a,b; Enquist and Niklas, 2002). Residual variation of these relationships is considered to reflect the ecologically induced variations in biomass allocation within and across species (Zens and Webb, 2002; McCarthy and Enquist, 2007). Understanding the strategy in resource allocation in plants therefore needs to separate the contribution of two components: alteration in allocation might be simply the result of size, which is called ‘apparent’ or ‘passive’ plasticity, or active changes in allocation relationships, called ‘real’ plasticity (McConnaughay and Coleman, 1999; Wright and McConnaughay, 2002). There are many experimental, usually intraspecific studies dealing with the influence of different resource availabilities on changes in biomass investment with mainly light, nutrients, water and CO2 being considered (Poorter et al., 2011 and reference therein); allometric effects are, however, seldom explicitly tested (Janeˇcek et al., 2014). Studies of resource allocation under field conditions are comparatively rare (Niklas, 1994a; Metcalf et al., 2006; Fraterrigo et al., 2006; Niu et al., 2008, 2009; Minden and Kleyer, 2011), and they
http://dx.doi.org/10.1016/j.ppees.2015.06.003 1433-8319/© 2015 Geobotanisches Institut ETH, Stiftung Ruebel. Published by Elsevier GmbH. All rights reserved.
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separate the effect of plant size on the observed allocation of plant biomass and evaluate the response of a whole community even more rarely (Minden and Kleyer, 2011; Niu et al., 2009). The reasons for this are manifold: changes in the allocation strategy of plants under complex environmental effects faced usually by communities bring about contradictory effects of altered competition milieu, nutrient availability, disturbance regime, litter accumulation, etc. (Fortunel et al., 2009; Robson et al., 2009); communities might not be enough species rich to allow robust regression analysis; and species in a community tend to be similar in size. The plants in one community are filtered by certain environmental conditions (Díaz et al., 1998; Westoby and Wright, 2006) and therefore represent only a tiny fraction of the variability in the plant kingdom. In case the similarity concerns plant size, as in herbaceous communities, this could hinder the possibility of recognizing the general allometric pattern described by Enquist and Niklas (2002) for plants across different ecosystems (Robinson, 2004; Tilman et al., 2004; Poorter et al., 2011). Having all those obstacles in mind we aimed to test whether the common observation that with increasing competition plants invest preferably into supporting organs at the expense of assimilation organs is due to active change in allocation strategy or simply due to allometry. As the biomass of leaves scales with the 3/4 power of the stem biomass (Enquist and Niklas, 2002), the whole effect might be due to an increase of plant size with increasing aboveground competition. We selected a species rich temperate meadow subjected to abandonment as a model community. An advantage of meadow communities is that they represent the most species rich communities on a small scale recorded by researchers (Wilson et al., 2012) and therefore allow for examining biomass allocation of a large number of species growing in one community under the same conditions. Although all species in the meadow community are herbaceous and small, there is still some variability in stature (Klimeˇsová et al., 2010), at least in species rich stands. With the changing demands of the human society, the meadows have been exposed to alterations of management and in recent decades, abandonment has become one of the particularly highlighted threats to highly diverse meadow communities (Huhta, 1997; Baur et al., 2006). Abandonment above all other effects is associated with increasing competitive milieu and consequent successional changes resulting in decreasing species richness and ´ changes in species composition towards woody species (Falinska, 1999; Kahmen and Poschlod, 2004; Doleˇzal et al., 2011). In the dense vegetation cover of a meadow, competition for light plays an important role and the coexistence of species differing in size is enabled by the equalizing effect of regular mowing which allows the persistence of small plants regarded as weaker competitors (Zobel, 1992; Klimeˇs and Klimeˇsová, 2001; Klimeˇsová et al., 2010). A first response of resident species to altered competitive milieu, before any species-exclusion happens, is an increase in size and a change in biomass allocation to different organs, resulting in an increased allocation to stems, petioles, i.e. into supportive structures as they are all key components in the competition for light (Kull and Zobel, 1991; Givnish, 1995; Westoby et al., 2002; Poorter et al., 2011; de Bello et al., 2012). Therefore, this study aims to elucidate the role of variation in biomass allocation of plants for two contrasting meadows after a change in management. We expect that the biomass allocation on the community level will be affected by the time since the cessation of mowing. The biomass allocation in response to the cessation of mowing was tested for 41 common species in wet and dry meadows both one and three years after abandonment at the peak of community development in June, just before traditional mowing, and at the end of the season in October. The following questions were considered:
(i) Are the absolute and relative aboveground biomass allocations at community level in the meadows affected by location, management, season and/or year? (ii) Can a deviation from the general allometric relationship (˛ = 0.75) among supportive biomass and biomass of leaf blades for plants in a community be found and is it related to management change? (iii) Is the interspecific response to abandonment comparable to the intraspecific response? Materials and methods Site description These experiments were conducted in two species-rich meadows, differing in water availability, that have already been used to study management impact on community functioning (Lepˇs, 1999, 2004; Klimeˇs et al., 2000). The dry meadow is located in the ˇ Bílé Karpaty Mts., south eastern Czech Republic, in the Certoryje Nature Reserve (48◦ 54 N, 17◦ 25 E) at 440 m a.s.l. The area receives an average of 650 mm precipitation annually and has a mean annual temperature of 8 ◦ C (Tolasz et al., 2007). The dryness is mainly caused by the high permeability of deep soils on a flysch bedrock. The meadow is on calcium-rich soil with scattered Quercus spp. ´ 2007). There are up to trees, classified as Bromion alliance (Chytry, 70 species/m2 (Klimeˇs et al., 2000). The wet meadow is situated in the southern part of the Czech Republic in Ohrazení (48◦ 57 N, 14◦ 36 E), at 500 m a.s.l. The mean annual temperature is 7–8 ◦ C and precipitation is 700 mm (Tolasz et al., 2007). Clay deposits near the soil surface prevent quick rain water infiltration. This meadow is on ´ 2007). There acidic soil and is classified as Molinion alliance (Chytry, are 35–40 species per 0.25 m2 (Lepˇs, 2004). The meadows are mown in June (dry meadow) or July (wet meadow) and have been mown annually for at least 10 years before the experiment started. The wet meadow has a higher productivity of aboveground biomass (dry biomass 320 g m−2 ) than the dry meadow (dry biomass 250 g m−2 ) (de Bello et al., 2012). Experiment The dataset included 12,708 individually measured plant parts (leaves, stems, flowers) from 6129 plant individuals belonging to 41 common meadow species. The data were collected in traditionally mown and recently abandoned plots in both meadows, twice during the growing season: in early June before mowing and in midOctober at the end of the growing period in both 2006 and 2008. The experiment was set up in June 2005, in a randomized block design on regularly mown meadows. Six blocks were selected in the dry meadow and five blocks in the wet meadow. Each block contained nine permanent plots (three rows of three) in which either the fallow treatment (i.e. abandonment) was applied from 2005, or mowing was continued (for further details on experimental set up, see Klimeˇsová et al., 2010). Out of all species only those species occurring in all of the selected plots in a given meadow in June 2006 were selected for data collection, resulting in 22 and 19 target species occurring on the dry and wet meadows respectively (Table 1). A minimum 2–6 randomly selected shoots of each target species were harvested in each block – from two plots differing in management in June 2006 and in two other plots at other collection dates. Sampled shoots were transported in a cooling box to the laboratory where they were partitioned into blades, petioles, stems and reproductive parts. Samples were oven dried at 80 ◦ C for 24 h and then weighed. For later analysis, the petiole biomass with the stem biomass were combined as they are both supportive organs of leaf blades
Please cite this article in press as: Bartuˇsková, A., et al., Changes in biomass allocation in species rich meadow after abandonment: Ecological strategy or allometry? Perspect. Plant Ecol. Evol. Syst. (2015), http://dx.doi.org/10.1016/j.ppees.2015.06.003
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A. Bartuˇsková et al. / Perspectives in Plant Ecology, Evolution and Systematics xxx (2015) xxx–xxx Table 1 List of studied species and abbreviations of their names used in figures. Dry meadow Betonica officinalis L. Bromus erectus HUDS. Carex montana L. Cirsium pannonicum (L. fil.) LINK Clematis recta L. Filipendula vulgaris MOENCH Fragaria vesca L. Geranium sanguineum L. Helianthemum grandiflorum (SCOP.) DC. Inula salicina L. Lathyrus niger (L.) BERNH. Molinia arundinacea SCHRANK Leontodon autumnalis L. Plantago lanceolata L. Potentilla alba L. Primula veris L. Prunella grandiflora (L.) SCHOLLER Ranunculus polyanthemos L. Salvia pratensis L. Serratula tinctoria L. Pyrethrum corymbosum (L.) SCOP. Trifolium montanum L.
Wet meadow BeOf
Angelica sylvestris L.
AnSy
BrEr
Betonica officinalis L.
BeOf
CaMo CiPa
Carex hartmanii CAJANDER Carex pallescens L.
CxHa CxPal
ClRe FiVu
Carex panicea L. Deschampsia cespitosa (L.) PB.
CxPan DeCe
FrVe GeSa
Galium boreale L. Holcus lanatus L.
GaBo HoLa
HeGr
Juncus effusus L.
JuEf
InSa LaNi
Lathyrus pratensis L. Lysimachia vulgaris L.
LaPr LyVu
MoAr
Molinia caerulea (L.) MOENCH
MoCa
LeAu
Potentilla erecta (L.) RÄUSCHEL
PoEr
PlLa
Ranunculus acris L.
RaAc
PoAl PrVe PrGr
Ranunculus auricomus agg. Rumex acetosa L. Sanguisorba officinalis L.
RaAu RuAc SaOf
RaPo
Selinum carvifolia (L.) L.
SeCa
SaPr SeTi PyCo
Viola palustrisL.
ViPa
TrMo
(Niinemets et al., 2007). In the studied species, the photosynthetic function of stems and petioles was considered negligible when compared with the photosynthetic function of the blades. Leaf sheaths in graminoids were regarded as a part of supportive organs.
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(Anon, 1996). Non-overlapping standard error bars were used to describe differences. Principal Component Analysis (PCA) was finally used to assess the overall inter-correlations of biomass values allocated in individual organs and their differences between two localities, within the growing season and between the years in mown and fallow plots. The relation to the main tested variables was assessed by their passive projection to the PCA ordination plane using centroids of four factor level combinations (16 centroids in total). The same method was used to assess the inter-correlations of biomass proportions in individual species and the differences between mown and fallow treatment in June, for both localities separately (44 centroids – the dry meadow, 38 centroids – the wet meadow). The ordination analysis and visualization of the results was carried out using the ˇ CANOCO and CanoDraw programs (ter Braak and Smilauer, 2002). Regressions were used to reveal allometric relationships between biomass allocated to supportive organs and leaf blades and similarity to the relationship observed by Enquist and Niklas (2002) was assessed by comparisons of slopes. Both comparisons were performed with the SMATR program (Falster et al., 2006). In correlation graphs, data were fitted using standardized major axis (SMA) techniques. This minimizes the sum of squares in both x and y dimensions (for details, see Warton et al., 2006). The input data for comparison of the meadows were average values per species. Two species (Carex montana and Juncus effusus) were excluded from this analysis as outliers; the first species is early flowering plant with a rosette shoot having no stems in June or August and second one has no leaves but only photosynthetic stems. For comparison within the meadows, average values per species for either treatment, season or year were used. Data from Betonica officinalis (the only studied species present at both localities) were used to compare intraspecific differences in aboveground biomass allocation between localities. Data available from all harvests were used and for more detailed analysis grouped by either treatment, season or year. Comparison of slopes, common slopes, shift along the common slopes and shift in elevation were performed with the SMATR program (Falster et al., 2006) using a test of heterogeneity in slopes between groups (comparison of slopes) and ANCOVA analogous tests comparing fitted (F) axis scores (shift along axis) or residual (R) axis scores (shifts in elevation); these measure the spread of data along (F) and away from (R) the fitted line. Results
Data analysis Biomass allocation at the community level All the species from both localities were analysed together. In the common test, the effects of locality (dry or wet), management (mowed or abandoned), year (2006 or 2008) and season (June or October) on the biomass allocation, expressed either by the absolute values or proportion of biomass allocated in assimilative (blades), supportive (stems and petioles) and reproductive (flowers and fruits) organs, were analysed. A generalized linear mixed effect model (GLMM) was used because the data represent a hierarchical split-plot design, with both fixed and random effect factors. Each species was considered a “main-plot” and represented a factor with a random effect nested in the locality. Management, location, year and season were the categorical fixed effect factors. The test was based on the restricted maximum likelihood (REML) approach. The statistical significance of the main effects and interactions were assessed by computing Bayesian highest probability (HPD) intervals using Markov chain Monte Carlo simulations, as this is favoured over normal confidence limits for GLMMs. Analyses were done using the lme4 and languageR packages in the R program (R Development Core Team, 2008). Graphs illustrating differences in mean absolute and relative investment in individual organs between sites were plotted in the STATISTICA program
The absolute and relative biomasses of leaf blades, supportive organs and reproductive organs were influenced by all factors including locality, management and season (Table 2). The factor year, however, had no simple effect on the absolute values. The most significant effect had the combination of both the treatment and the season (Fig. 1). The interaction of the treatment and the year had no effect, which together with the significant effect of the locality indicates the importance of different species composition and/or environmental factors in both meadows. The effects of all factors are illustrated in Figs. 1 and 2. Localities differed in the absolute biomass of the aboveground organs under continuing mowing, which served as a control to abandonment. Comparing mown treatments between both meadows, there was higher biomass and also higher absolute investments in supportive organs, blades and also reproductive organs in the dry than in the wet meadow in June. Concerning relative investment in June, there was a larger proportion of leaf blades than supportive organs in the dry meadow (Fig. 2). In October, plants regenerating after mowing in the dry meadow had a higher proportion of leaf blades than plants in the wet meadow (Fig. 2).
Please cite this article in press as: Bartuˇsková, A., et al., Changes in biomass allocation in species rich meadow after abandonment: Ecological strategy or allometry? Perspect. Plant Ecol. Evol. Syst. (2015), http://dx.doi.org/10.1016/j.ppees.2015.06.003
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Table 2 Results of GLMM testing for the effects of locality (dry, wet), management (mowing, fallowing), year (2006, 2008) and season (June, October) and their interactions on the biomass allocation of 41 meadow species (see Table 1) expressed either by the absolute values or proportion of biomass allocated in blades, supportive (stems and petioles) and reproductive (flowers and fruits) organs. Blades Abs Locality (L) Treatment (T) Year (Y) Season (S) L:T L:Y T:Y L:S T:S Y:S L:T:Y L:T:S L:Y:S T:Y:S L:T:Y:S
Supportive organs %
**
11.32 147.18*** n.s. 222.16*** 32.30*** 1.42a n.s. 38.49*** n.s. 4.8* n.s. n.s. 6.82* 9.95** n.s.
Abs *
4.64 127.01*** 13.29*** 96.62*** n.s. 7.26** n.s. n.s. 110.41*** 3.51a n.s. 38.29*** 11.94*** n.s. n.s.
Reproductive organs %
a
2.92 138.52*** n.s. 91.16** 7.57** n.s. n.s. 6.03* 39.51*** 7.48** n.s. 17.81*** n.s. n.s. n.s.
Abs a
4.01 181.52*** 8.90** 21.02*** n.s. 5.52a n.s. 2.48a 114.02*** 10.98*** n.s. 40.94*** 12.10*** n.s. n.s.
% a
3.67 12.98*** n.s. 29.59*** n.s. n.s. n.s. n.s. 36.14*** n.s. 3.23a 10.89** n.s. n.s. n.s.
n.s. n.s. 15.39*** 370.76*** n.s. n.s. n.s. 23.56*** 22.19*** 6.42* n.s. 5.81* 3.90* n.s. n.s.
Each species was considered a “main-plot” and represented a factor with a random effect nested in the locality. Management, location, year and season were the categorical fixed effect factors. The F-statistic values and corresponding type I error estimates for a likelihood-ratio test are shown. a p < 0.1. * p < 0.05. ** p < 0.01. *** p < 0.001.
The response to abandonment was different between the two meadows (Fig. 2). In June, the dry meadow plants under fallow conditions became larger while having the same proportion of blades and supportive organs than those which were mown. The same quantity of biomass was invested in reproductive organs so the lower proportion of reproductive biomass in fallow plots was the effect of the other biomass components. In October, the absolute investment in the leaf blades and supportive organs was higher for the fallow treatment. The highest investment in reproductive organs was observed in fallow treatment in October 2008. As this was higher than in June 2008, this indicates successful sexual reproduction in phenologically late species, which is not usually achieved in a mown meadow. When mown, plants primarily regenerated via leaf blades, whereas the supportive and reproductive organs reached minimal biomass values. In the wet meadow, differences between mown and fallow treatments in absolute investment in blades and supportive organs did not appear until 2008, when the values of biomass of both organs in fallow treatment exceeded those in the mown treatment. They were not in the same range, which led to a decreased proportion in the biomass of blades and an increased proportion
of supportive organs in fallow plots. The biomass of reproductive organs did not differ in either absolute or relative values. In October, the absolute investment in blades in fallow plots was slightly higher in 2006 whereas in 2008 the biomass of the blades was the same in both mown and fallow plots. In both years, the absolute and relative investments in supportive organs were higher in fallow plots. A significant allometric relationship was found between the biomass of leaf blades and supportive organs for the whole set of studied meadow species (Table 3; Fig. 3). The value for the slope was 0.91, and was not statistically different from the Enquist and Niklas (2002) value of 0.75 (F = 2.609, p = 0.115; Table 3; Fig. 3). The dry and wet meadows neither differed in the plant scaling exponent of this relationship nor were the scaling exponents of the dry and the wet meadow significantly different from the scaling exponent in the study by Enquist and Niklas (2002) (Table 3; Fig. 3). The difference between the meadows was in the elevation and their shift along the common slope, reflecting different species composition and thus investment (Table 3; Fig. 3). However, inside the localities there was no effect of the treatment, year or season on the scaling exponent of the relationship. Abandonment does not led to any significant changes in the studied relationship. In the dry meadow, only significant shifts in data along the common slope of the regression line comparing June and October were detected (stat = 4.46, p = 0.035; Table 3). Biomass allocation at the species level
Fig. 1. PCA ordination of biomass allocated to individual organs with passively projected centroids of four factor level combinations. The combinations of the season and the management, influencing most the differences in biomass allocation, are marked with different symbols and fills. The first two principal components explain 53% of the total data variability.
Species in both meadows differed in biomass allocation patterns under the continuing mowing regime, as shown by the mean values in June (Appendix: Fig. A1 and A2). The maximum average biomass of one shoot among individual species was 1.5 g in the dry meadow, compared with 0.9 g in the wet meadow (Appendix: Fig. A1). The investment in supportive organs ranged up to 56% in the dry and 69% in the wet meadow. The maximum investment in reproductive organs was 18% in the dry and 23% in the wet meadow; some species, however, did not flower at the time of mowing (Appendix: Fig. A1). In the dry meadow in June, only three species (Filipendula vulgaris, Helianthemum grandiflorum, Potentilla alba) out of 22 increased their relative investment in supportive organs in fallow
Please cite this article in press as: Bartuˇsková, A., et al., Changes in biomass allocation in species rich meadow after abandonment: Ecological strategy or allometry? Perspect. Plant Ecol. Evol. Syst. (2015), http://dx.doi.org/10.1016/j.ppees.2015.06.003
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Fig. 2. Biomass allocation in individual organs: absolute and relative values. The differences between two localities, within the growing season and between the years in mown and fallow plots are shown (mean, bars denote standard error).
plots. In contrast, four species (Bromus erectus, Cirsium pannonicum, Leontodon autumnalis, Plantago lanceolata) markedly decreased the same investment. Two species (Salvia pratensis, Ranunculus polyanthemos) invested less in reproductive organs in fallow plots and one species (Primula veris) even increased its investment (Fig. 4, Appendix: Fig. A2). In the wet meadow in June, six species (Deschampsia cespitosa, Galium boreale, Lathyrus pratensis, Lysimachia vulgaris, Potentilla
erecta, Selinum carvifolia) increased their relative investment in supportive organs in fallow plots and none of them decreased. An increase in relative investment in reproductive organs was found in one species (Carex pallescens) in fallow plots. The other species showed variable or no reaction to the abandonment (Fig. 4, Appendix: Fig. A2). In October, the plants with late phenology had markedly higher absolute and relative investments in supportive and reproductive
Please cite this article in press as: Bartuˇsková, A., et al., Changes in biomass allocation in species rich meadow after abandonment: Ecological strategy or allometry? Perspect. Plant Ecol. Evol. Syst. (2015), http://dx.doi.org/10.1016/j.ppees.2015.06.003
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Table 3 Allometric scaling coefficients for different groups of plant species and treatment, season or year influence.
Across all species Dry meadow species Wet meadow species Dry meadow Fallow treatment Mown treatment June October Year 2006 Year 2008 Wet meadow Fallow treatment Mown treatment June October Year 2006 Year 2008 Betonica officinalis Dry meadow Wet meadow Dry meadow Fallow treatment Mown treatment June October Year 2006 Year 2008 Wet meadow Fallow treatment Mown treatment June October Year 2006 Year 2008
˛SMA
Log ˇSMA
r2
p
(H0 : ˛ = 0.75) p
(H0 : heterogeneity in slopes) p
(H0 : no shift along slope) p
(H0 : no shift in elevation) p
0.914 0.687 0.926
0.091 0.009 −0.020
0.436 0.422 0.463
*** ** **
n.s. n.s. n.s.
– n.s.
– **
– **
0.492 0.454 0.559 0.381 0.520 0.422
−0.099 −0.195 −0.053 −0.252 −0.105 −0.187
0.517 0.414 0.504 0.217 0.472 0.459
*** ** *** * *** **
* ** n.s. ** * **
n.s.
n.s.
n.s.
n.s.
*
n.s.
n.s.
n.s.
n.s.
0.869 0.940 0.920 0.789 1.020 0.817
−0.091 0.036 −0.027 −0.131 0.021 −0.070
0.559 0.375 0.334 0.436 0.493 0.365
*** ** * ** ** **
n.s. n.s. n.s. n.s. n.s. n.s.
n.s.
n.s.
n.s.
n.s.
n.s.
n.s.
n.s.
n.s.
n.s.
0.761 1.045
0.079 0.107
0.750 0.633
*** ***
n.s. ***
***
–
–
0.925 0.763 0.911 0.657 0.777 0.737
0.096 0.142 0.168 −0.025 0.136 0.018
0.648 0.797 0.904 0.594 0.814 0.689
*** *** *** *** *** ***
** n.s. *** n.s. n.s. n.s.
*
–
–
**
–
–
n.s.
n.s.
n.s.
1.163 0.961 0.949 1.052 1.036 1.101
0.045 0.157 0.105 0.069 0.147 0.079
0.638 0.788 0.724 0.589 0.605 0.668
*** *** *** *** *** ***
*** *** ** *** *** ***
n.s.
n.s.
***
n.s.
*
*
n.s.
n.s.
n.s.
The table shows results of the standard major axis (linear) regression with slope ˛SMA , intercept Log ˇSMA , coefficient of determination r2 and statistical significance p: *, p < 0.05; **, p < 0.01; ***, p < 0.001. Data were calculated from log10 -transformed biomass of supportive organs versus log10 -transformed biomass of blades, with masses expressed in grams. The last part of the table shows statistical significance p of comparison of slopes (presence of common slope), shift along the common slopes and shift in elevation every time between two regression relationships. The top part of the table gives data for interspecific relationships, the bottom part data for intraspecific relationships on a case of Betonica officinalis.
organs in fallow plots than in mown plots. Among them, the allocation in Inula salicina, Serratula tinctoria and the dominant grass species Molinia arundinacea and Molinia caerulea were the most pronounced (Appendix: Fig. A3). The fact that one studied species, Betonica officinalis, occurred on both localities allowed us to compare the relationship between biomass of leaf blades and of supportive organs in relation to the effects of location, management, season and the year on the intraspecific level (Table 3; Appendix: Fig. A4). Localities differed between the slope of the relationship (F = 68.3, p < 0.001; Table 3; Appendix: Fig. A4), which equaled to 0.76 in the dry meadow and 1.04 in the wet meadow. There were also detected effects of the locality, treatment and season on the relationship. In the dry meadow, abandonment led to a higher scaling exponent and in June a higher scaling exponent was found than in October (Table 3; Appendix: Fig. A4). In the wet meadow, a shift in elevation in the case of treatment, and both a shift in elevation and along common slope in the case of season were found (Table 3; Appendix: Fig. A4).
Discussion Meadow plants responded to short term abandonment by producing larger shoots, however, relative investment into supportive structures for the community increased in the wet but not in the dry meadow. This study is the first to show that plants in temperate, European meadows invest more into supportive structures (stems
and petioles) with increasing competitive milieu (wet meadow) and this is not due to changed biomass allocation but to increasing plant size. The changes in the aboveground biomass allocation on the community level were within the frame of an allometric relationship. Allometric theory proved to provide a useful null model to which changes in biomass investment due to alterations of management or environmental conditions can be tested.
Biomass allocation within meadow communities The fact that at the community level meadow species generally follow the allometric relationship described by Enquist and Niklas (2002), suggests that even in one type of community, with species similar in size, the relationship described for all plants from dipterocarp to Arabidopsis could be observed. The results further showed that wet meadow plants invest more stem biomass per unit of leaf biomass than dry meadow plants (the same slope but different intercept of the allometric relationship). This difference between meadows is probably caused by the combined effects of the graminoids to dicot herbs ratio (on dry meadow 2:19, wet meadow 6:12) and a representation of different plant architectures (rosette, semirosette and erosulate shoot; Appendix: Fig. A1 and A2). The broad spectrum of the shoot architectures, in combination with the relatively small range of biomass amount, may lead to different scaling. Although those differences need to be studied in more detail, they indicate differences in allocation for
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Fig. 3. Interspecific log–log relationships between the biomass of supportive organs and the biomass of leaf blades in both the dry and the wet meadows together (a) and separately (b). The SMA regression lines represent the relationship for all the meadow species (a – black solid line), for the dry meadow species (b – black dashed line) and for the wet meadow species (b – black solid line). The grey solid lines represent the model by Enquist and Niklas (2002) with the slope equal to 0.75. The symbols indicate the mean value for each species. The SMA regression scaling coefficients and statistical significance are written in Table 3.
different architectures of herbaceous plants as was similarly found for trees (e.g. angiosperm and conifer leaves [Enquist and Niklas, 2002]). Despite some reservation in the literature for using allocation theory for answering ecologically relevant questions (e.g. Tilman et al., 2004; Metcalf et al., 2006), these results can be
considered as proof that the examination of allocation could contribute to the understanding of meadow plant strategies. An inseparable part of biomass allocation is below-ground biomass. In the meadows, where the below-ground organs are entangled on a small scale, it is not possible to responsibly obtain biomass of this fraction. Although variations in below-ground biomass allocation are known to be affected by environmental conditions or ontogenetic drift, results are, however, inconsistent (e.g. Gedroc et al., 1996; Poorter et al., 2011; Janeˇcek et al., 2014). Community and species level of response to changing management
Fig. 4. PCA ordination of percentage of biomass allocated to individual organs with passively projected centroids of individual species values in mown () and fallow () treatments in June. Species name abbreviations are given in Table 1. In the dry and wet sites, the first two principal components explain 37% and 32% of the total data variability, respectively.
Different species at a site have a mix of strategies (Westoby et al., 2002) that facilitate their occupation of different available niches (Manson et al., 2011; de Bello et al., 2012) and individual species studied here show variable responses. In the wet meadow, several species responded to abandonment by increasing their investment into supportive organs and others did not change the allocation. In the dry meadow, however, the reaction of species was more diverse. Three species increased their relative investment in supportive organs, four other species reduced this investment and the remaining species showed no reaction. A similar mixture of positive and negative effects on growth was observed by Niu et al. (2008) in a Tibetan alpine meadow after fertilization. Additionally, below species level, individual plant shoots experience different competitive pressure from their surrounding and their response is therefore “shoot specific” (Metcalf et al., 2006; Lanta et al., 2011). This effect could be included when scaling biomass allocation on the species level as was done for the Tibetan alpine meadow (Niu et al., 2008): a significant treatment effect on the scaling relationship was found in one quarter of cases and this was in accordance with the trends for the community. In this study, the relationship was tested for only one species which occurred on both sites and its reaction was site-specific, with real plasticity in aboveground biomass allocation. This was therefore not in accordance with the trend for the whole community. This result points
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to the lack of a strong factor affecting all plant individuals in both studied meadows and it also indicates that the response of individual plants in a community context is only partly reflected in the community response; this deserves further study. In Central European meadow communities, all aboveground plant structures are produced during the course of the growing season, which is interrupted by mowing. After mowing, the ability to compensate for the lost biomass is a key factor in determining the biomass allocation late in the season and is affected by plant size and shoot architecture (Klimeˇsová et al., 2010). On the contrary, for fallow plots, the competition for light is a crucial factor. Large plants are usually phenologically late and if they are not subjected to mowing, they may flower and accumulate biomass later in the season (Kahmen and Poschlod, 2004; Sun and Frelich, 2011). The resulting large biomass and tall canopy causes a considerably lower light availability inside a stand (Anten and Hirose, 1999). The increase in the biomass of the tall herbs after abandonment also leads to an increase in their dominance, whereas smaller herbs quickly decrease in abundance (Huhta et al., 2001; Kahmen and Poschlod, 2004; Niu et al., 2008; Lanta et al., 2011; Klimeˇsová et al., 2011). The mowing affects all plants, regardless of their actual phenological phases, at the same time. In this study, biomass allocation was measured as the amount of biomass that meadow plants are able to produce until the mowing time or until the end of the growing season. These two time periods represent rather similar phenological phases in the majority of meadow species (Martínková et al., 2002; Lanta et al., 2011), even when the management itself can change phenology of grassland plants (Niu et al., 2008; Zhang et al., 2014). There were two different effects of the management on biomass partitioning in this study: (i) direct effects of lost versus reserved biomass resulting in large changes in biomass investments during the growing season was dominant on the dry meadow. The mown meadow was more “leafy” in October while the abandoned meadow was less “leafy” and this effect could be attributed to the shoot architecture of meadow plants (Klimeˇsová et al., 2008, 2010); (ii) in the wet meadow, the effect of abandonment, under which plants steadily increased investments into supportive structures, was most pronounced. This indicates a strong effect of species composition and/or environmental factors on the respective meadows. For the wet meadow, the regrowth of plants after mowing is not limited by water availability while the opposite is true for the dry meadow (de Bello et al., 2012). The fact that the wet meadow community has a higher biomass production and was characterized by higher relative investments into supportive structures in most dates and treatments contrasts with the dry meadow and indicates that competitive milieu is higher there. The low-competitive environment of the dry meadow is reflected in the fact that this very meadow is listed as the most species rich community (on the small scale) known to botanists on Earth (Wilson et al., 2012). It is also known that the least productive and the most species-rich parts of this meadow are resistant to short-term changes of management, contrary to the more productive parts (Klimeˇs et al., 2013). Summer drought has strong effect on plant competitive ability and slows down changes in vegetation on abandoned sites. It could therefore be concluded that the lack of uniform changes in biomass allocation on the dry meadow reflect the fact that even three years of abandonment does not result in increasing competitive milieu in the stand.
Acknowledgements This work would not have been possible without cooperation and logistic support from the Bílé Karpaty Protected Landscape
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Changes in biomass allocation in species rich meadow after abandonment: Ecological strategy or allometry? ˇ epán Janeˇcek a,c , Vojtˇech Lanta b,d , Jitka Klimeˇsová a Alena Bartuˇsková a,∗ , Jiˇrí Doleˇzal a,b , Stˇ a
Institute of Botany, Czech Academy of Sciences, Dukelská 135, 379 01 Tˇrebon, ˇ Czech Republic ˇ University of South Bohemia, Faculty of Sciences, Department of Botany, Braniˇsovská 31, 370 05 Ceské Budˇejovice, Czech Republic c Department of Ecology, Faculty of Science, Charles University in Prague, Viniˇcná 7, 128 44 Praha 2, Czech Republic d University of Turku, Department of Biology, Section of Ecology, FIN-20014, Turku, Finland b
a r t i c l e
i n f o
Article history: Received 3 October 2014 Received in revised form 29 May 2015 Accepted 9 June 2015 Available online xxx Keywords: Abandonment Allometry Biomass allocation Community Mowing Species-rich meadow
a b s t r a c t Plants respond to changes in biotic and abiotic conditions by altering the allocation of biomass to organs with different functions. The degree to which this response is limited by architectural constraints and follows the rules of the allocation theory has rarely been studied at the community level for several reasons: environmental factors affecting plants in a community are of complex nature with contradictory effects, plants in a community tend to be similar in size, which limits the capability to recognize allometry, and only rarely are plant communities so species rich that robust regression analysis is feasible. We tested whether the often reported effect of meadow abandonment increasing investment into supportive structures due to an increasing competitive milieu is caused by changed allocation strategy of resident species or by an allometric effect. For the study we examined biomass allocation to leaf blades, petioles and stems in 41 plant species in two species rich temperate European meadows differing in water availability (dry versus wet) and subjected to abandonment. Biomass allocation between organs with supportive versus photosynthetic function in meadow species followed a general allocation pattern (allometric exponent 0.75), irrespective of the management. The observed changes in relative investment into supportive structures after abandonment were caused only by the increasing size of the resident species. The effect was restricted to wet meadow, while in dry meadow the reaction of the species was diverse – probably due to low competition after abandonment. © 2015 Geobotanisches Institut ETH, Stiftung Ruebel. Published by Elsevier GmbH. All rights reserved.
Plant nomenclature Kubát et al. (2002). Introduction One of the basic questions in comparative plant ecology is how plants allocate their resources to different functions (Bazzaz and Grace, 1997). The allocation of biomass to plant organs is presumed to be a reflection of actual plant life function demands, but this has its constraints. For example, when biomass is allocated to one organ or function, it is at the expense of other organs or functions; this implies trade-offs (Weiner, 2004). Furthermore, biomass allocation is limited by architectural constraints and these change with plant size. Between individual organs there are, therefore, frequent allo-
∗ Corresponding author. Tel.: +420 384 721 156. E-mail address: [email protected] (A. Bartuˇsková).
metrically scaled relationships (Niklas, 1994a,b; Enquist and Niklas, 2002). Residual variation of these relationships is considered to reflect the ecologically induced variations in biomass allocation within and across species (Zens and Webb, 2002; McCarthy and Enquist, 2007). Understanding the strategy in resource allocation in plants therefore needs to separate the contribution of two components: alteration in allocation might be simply the result of size, which is called ‘apparent’ or ‘passive’ plasticity, or active changes in allocation relationships, called ‘real’ plasticity (McConnaughay and Coleman, 1999; Wright and McConnaughay, 2002). There are many experimental, usually intraspecific studies dealing with the influence of different resource availabilities on changes in biomass investment with mainly light, nutrients, water and CO2 being considered (Poorter et al., 2011 and reference therein); allometric effects are, however, seldom explicitly tested (Janeˇcek et al., 2014). Studies of resource allocation under field conditions are comparatively rare (Niklas, 1994a; Metcalf et al., 2006; Fraterrigo et al., 2006; Niu et al., 2008, 2009; Minden and Kleyer, 2011), and they
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separate the effect of plant size on the observed allocation of plant biomass and evaluate the response of a whole community even more rarely (Minden and Kleyer, 2011; Niu et al., 2009). The reasons for this are manifold: changes in the allocation strategy of plants under complex environmental effects faced usually by communities bring about contradictory effects of altered competition milieu, nutrient availability, disturbance regime, litter accumulation, etc. (Fortunel et al., 2009; Robson et al., 2009); communities might not be enough species rich to allow robust regression analysis; and species in a community tend to be similar in size. The plants in one community are filtered by certain environmental conditions (Díaz et al., 1998; Westoby and Wright, 2006) and therefore represent only a tiny fraction of the variability in the plant kingdom. In case the similarity concerns plant size, as in herbaceous communities, this could hinder the possibility of recognizing the general allometric pattern described by Enquist and Niklas (2002) for plants across different ecosystems (Robinson, 2004; Tilman et al., 2004; Poorter et al., 2011). Having all those obstacles in mind we aimed to test whether the common observation that with increasing competition plants invest preferably into supporting organs at the expense of assimilation organs is due to active change in allocation strategy or simply due to allometry. As the biomass of leaves scales with the 3/4 power of the stem biomass (Enquist and Niklas, 2002), the whole effect might be due to an increase of plant size with increasing aboveground competition. We selected a species rich temperate meadow subjected to abandonment as a model community. An advantage of meadow communities is that they represent the most species rich communities on a small scale recorded by researchers (Wilson et al., 2012) and therefore allow for examining biomass allocation of a large number of species growing in one community under the same conditions. Although all species in the meadow community are herbaceous and small, there is still some variability in stature (Klimeˇsová et al., 2010), at least in species rich stands. With the changing demands of the human society, the meadows have been exposed to alterations of management and in recent decades, abandonment has become one of the particularly highlighted threats to highly diverse meadow communities (Huhta, 1997; Baur et al., 2006). Abandonment above all other effects is associated with increasing competitive milieu and consequent successional changes resulting in decreasing species richness and ´ changes in species composition towards woody species (Falinska, 1999; Kahmen and Poschlod, 2004; Doleˇzal et al., 2011). In the dense vegetation cover of a meadow, competition for light plays an important role and the coexistence of species differing in size is enabled by the equalizing effect of regular mowing which allows the persistence of small plants regarded as weaker competitors (Zobel, 1992; Klimeˇs and Klimeˇsová, 2001; Klimeˇsová et al., 2010). A first response of resident species to altered competitive milieu, before any species-exclusion happens, is an increase in size and a change in biomass allocation to different organs, resulting in an increased allocation to stems, petioles, i.e. into supportive structures as they are all key components in the competition for light (Kull and Zobel, 1991; Givnish, 1995; Westoby et al., 2002; Poorter et al., 2011; de Bello et al., 2012). Therefore, this study aims to elucidate the role of variation in biomass allocation of plants for two contrasting meadows after a change in management. We expect that the biomass allocation on the community level will be affected by the time since the cessation of mowing. The biomass allocation in response to the cessation of mowing was tested for 41 common species in wet and dry meadows both one and three years after abandonment at the peak of community development in June, just before traditional mowing, and at the end of the season in October. The following questions were considered:
(i) Are the absolute and relative aboveground biomass allocations at community level in the meadows affected by location, management, season and/or year? (ii) Can a deviation from the general allometric relationship (˛ = 0.75) among supportive biomass and biomass of leaf blades for plants in a community be found and is it related to management change? (iii) Is the interspecific response to abandonment comparable to the intraspecific response? Materials and methods Site description These experiments were conducted in two species-rich meadows, differing in water availability, that have already been used to study management impact on community functioning (Lepˇs, 1999, 2004; Klimeˇs et al., 2000). The dry meadow is located in the ˇ Bílé Karpaty Mts., south eastern Czech Republic, in the Certoryje Nature Reserve (48◦ 54 N, 17◦ 25 E) at 440 m a.s.l. The area receives an average of 650 mm precipitation annually and has a mean annual temperature of 8 ◦ C (Tolasz et al., 2007). The dryness is mainly caused by the high permeability of deep soils on a flysch bedrock. The meadow is on calcium-rich soil with scattered Quercus spp. ´ 2007). There are up to trees, classified as Bromion alliance (Chytry, 70 species/m2 (Klimeˇs et al., 2000). The wet meadow is situated in the southern part of the Czech Republic in Ohrazení (48◦ 57 N, 14◦ 36 E), at 500 m a.s.l. The mean annual temperature is 7–8 ◦ C and precipitation is 700 mm (Tolasz et al., 2007). Clay deposits near the soil surface prevent quick rain water infiltration. This meadow is on ´ 2007). There acidic soil and is classified as Molinion alliance (Chytry, are 35–40 species per 0.25 m2 (Lepˇs, 2004). The meadows are mown in June (dry meadow) or July (wet meadow) and have been mown annually for at least 10 years before the experiment started. The wet meadow has a higher productivity of aboveground biomass (dry biomass 320 g m−2 ) than the dry meadow (dry biomass 250 g m−2 ) (de Bello et al., 2012). Experiment The dataset included 12,708 individually measured plant parts (leaves, stems, flowers) from 6129 plant individuals belonging to 41 common meadow species. The data were collected in traditionally mown and recently abandoned plots in both meadows, twice during the growing season: in early June before mowing and in midOctober at the end of the growing period in both 2006 and 2008. The experiment was set up in June 2005, in a randomized block design on regularly mown meadows. Six blocks were selected in the dry meadow and five blocks in the wet meadow. Each block contained nine permanent plots (three rows of three) in which either the fallow treatment (i.e. abandonment) was applied from 2005, or mowing was continued (for further details on experimental set up, see Klimeˇsová et al., 2010). Out of all species only those species occurring in all of the selected plots in a given meadow in June 2006 were selected for data collection, resulting in 22 and 19 target species occurring on the dry and wet meadows respectively (Table 1). A minimum 2–6 randomly selected shoots of each target species were harvested in each block – from two plots differing in management in June 2006 and in two other plots at other collection dates. Sampled shoots were transported in a cooling box to the laboratory where they were partitioned into blades, petioles, stems and reproductive parts. Samples were oven dried at 80 ◦ C for 24 h and then weighed. For later analysis, the petiole biomass with the stem biomass were combined as they are both supportive organs of leaf blades
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A. Bartuˇsková et al. / Perspectives in Plant Ecology, Evolution and Systematics xxx (2015) xxx–xxx Table 1 List of studied species and abbreviations of their names used in figures. Dry meadow Betonica officinalis L. Bromus erectus HUDS. Carex montana L. Cirsium pannonicum (L. fil.) LINK Clematis recta L. Filipendula vulgaris MOENCH Fragaria vesca L. Geranium sanguineum L. Helianthemum grandiflorum (SCOP.) DC. Inula salicina L. Lathyrus niger (L.) BERNH. Molinia arundinacea SCHRANK Leontodon autumnalis L. Plantago lanceolata L. Potentilla alba L. Primula veris L. Prunella grandiflora (L.) SCHOLLER Ranunculus polyanthemos L. Salvia pratensis L. Serratula tinctoria L. Pyrethrum corymbosum (L.) SCOP. Trifolium montanum L.
Wet meadow BeOf
Angelica sylvestris L.
AnSy
BrEr
Betonica officinalis L.
BeOf
CaMo CiPa
Carex hartmanii CAJANDER Carex pallescens L.
CxHa CxPal
ClRe FiVu
Carex panicea L. Deschampsia cespitosa (L.) PB.
CxPan DeCe
FrVe GeSa
Galium boreale L. Holcus lanatus L.
GaBo HoLa
HeGr
Juncus effusus L.
JuEf
InSa LaNi
Lathyrus pratensis L. Lysimachia vulgaris L.
LaPr LyVu
MoAr
Molinia caerulea (L.) MOENCH
MoCa
LeAu
Potentilla erecta (L.) RÄUSCHEL
PoEr
PlLa
Ranunculus acris L.
RaAc
PoAl PrVe PrGr
Ranunculus auricomus agg. Rumex acetosa L. Sanguisorba officinalis L.
RaAu RuAc SaOf
RaPo
Selinum carvifolia (L.) L.
SeCa
SaPr SeTi PyCo
Viola palustrisL.
ViPa
TrMo
(Niinemets et al., 2007). In the studied species, the photosynthetic function of stems and petioles was considered negligible when compared with the photosynthetic function of the blades. Leaf sheaths in graminoids were regarded as a part of supportive organs.
3
(Anon, 1996). Non-overlapping standard error bars were used to describe differences. Principal Component Analysis (PCA) was finally used to assess the overall inter-correlations of biomass values allocated in individual organs and their differences between two localities, within the growing season and between the years in mown and fallow plots. The relation to the main tested variables was assessed by their passive projection to the PCA ordination plane using centroids of four factor level combinations (16 centroids in total). The same method was used to assess the inter-correlations of biomass proportions in individual species and the differences between mown and fallow treatment in June, for both localities separately (44 centroids – the dry meadow, 38 centroids – the wet meadow). The ordination analysis and visualization of the results was carried out using the ˇ CANOCO and CanoDraw programs (ter Braak and Smilauer, 2002). Regressions were used to reveal allometric relationships between biomass allocated to supportive organs and leaf blades and similarity to the relationship observed by Enquist and Niklas (2002) was assessed by comparisons of slopes. Both comparisons were performed with the SMATR program (Falster et al., 2006). In correlation graphs, data were fitted using standardized major axis (SMA) techniques. This minimizes the sum of squares in both x and y dimensions (for details, see Warton et al., 2006). The input data for comparison of the meadows were average values per species. Two species (Carex montana and Juncus effusus) were excluded from this analysis as outliers; the first species is early flowering plant with a rosette shoot having no stems in June or August and second one has no leaves but only photosynthetic stems. For comparison within the meadows, average values per species for either treatment, season or year were used. Data from Betonica officinalis (the only studied species present at both localities) were used to compare intraspecific differences in aboveground biomass allocation between localities. Data available from all harvests were used and for more detailed analysis grouped by either treatment, season or year. Comparison of slopes, common slopes, shift along the common slopes and shift in elevation were performed with the SMATR program (Falster et al., 2006) using a test of heterogeneity in slopes between groups (comparison of slopes) and ANCOVA analogous tests comparing fitted (F) axis scores (shift along axis) or residual (R) axis scores (shifts in elevation); these measure the spread of data along (F) and away from (R) the fitted line. Results
Data analysis Biomass allocation at the community level All the species from both localities were analysed together. In the common test, the effects of locality (dry or wet), management (mowed or abandoned), year (2006 or 2008) and season (June or October) on the biomass allocation, expressed either by the absolute values or proportion of biomass allocated in assimilative (blades), supportive (stems and petioles) and reproductive (flowers and fruits) organs, were analysed. A generalized linear mixed effect model (GLMM) was used because the data represent a hierarchical split-plot design, with both fixed and random effect factors. Each species was considered a “main-plot” and represented a factor with a random effect nested in the locality. Management, location, year and season were the categorical fixed effect factors. The test was based on the restricted maximum likelihood (REML) approach. The statistical significance of the main effects and interactions were assessed by computing Bayesian highest probability (HPD) intervals using Markov chain Monte Carlo simulations, as this is favoured over normal confidence limits for GLMMs. Analyses were done using the lme4 and languageR packages in the R program (R Development Core Team, 2008). Graphs illustrating differences in mean absolute and relative investment in individual organs between sites were plotted in the STATISTICA program
The absolute and relative biomasses of leaf blades, supportive organs and reproductive organs were influenced by all factors including locality, management and season (Table 2). The factor year, however, had no simple effect on the absolute values. The most significant effect had the combination of both the treatment and the season (Fig. 1). The interaction of the treatment and the year had no effect, which together with the significant effect of the locality indicates the importance of different species composition and/or environmental factors in both meadows. The effects of all factors are illustrated in Figs. 1 and 2. Localities differed in the absolute biomass of the aboveground organs under continuing mowing, which served as a control to abandonment. Comparing mown treatments between both meadows, there was higher biomass and also higher absolute investments in supportive organs, blades and also reproductive organs in the dry than in the wet meadow in June. Concerning relative investment in June, there was a larger proportion of leaf blades than supportive organs in the dry meadow (Fig. 2). In October, plants regenerating after mowing in the dry meadow had a higher proportion of leaf blades than plants in the wet meadow (Fig. 2).
Please cite this article in press as: Bartuˇsková, A., et al., Changes in biomass allocation in species rich meadow after abandonment: Ecological strategy or allometry? Perspect. Plant Ecol. Evol. Syst. (2015), http://dx.doi.org/10.1016/j.ppees.2015.06.003
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Table 2 Results of GLMM testing for the effects of locality (dry, wet), management (mowing, fallowing), year (2006, 2008) and season (June, October) and their interactions on the biomass allocation of 41 meadow species (see Table 1) expressed either by the absolute values or proportion of biomass allocated in blades, supportive (stems and petioles) and reproductive (flowers and fruits) organs. Blades Abs Locality (L) Treatment (T) Year (Y) Season (S) L:T L:Y T:Y L:S T:S Y:S L:T:Y L:T:S L:Y:S T:Y:S L:T:Y:S
Supportive organs %
**
11.32 147.18*** n.s. 222.16*** 32.30*** 1.42a n.s. 38.49*** n.s. 4.8* n.s. n.s. 6.82* 9.95** n.s.
Abs *
4.64 127.01*** 13.29*** 96.62*** n.s. 7.26** n.s. n.s. 110.41*** 3.51a n.s. 38.29*** 11.94*** n.s. n.s.
Reproductive organs %
a
2.92 138.52*** n.s. 91.16** 7.57** n.s. n.s. 6.03* 39.51*** 7.48** n.s. 17.81*** n.s. n.s. n.s.
Abs a
4.01 181.52*** 8.90** 21.02*** n.s. 5.52a n.s. 2.48a 114.02*** 10.98*** n.s. 40.94*** 12.10*** n.s. n.s.
% a
3.67 12.98*** n.s. 29.59*** n.s. n.s. n.s. n.s. 36.14*** n.s. 3.23a 10.89** n.s. n.s. n.s.
n.s. n.s. 15.39*** 370.76*** n.s. n.s. n.s. 23.56*** 22.19*** 6.42* n.s. 5.81* 3.90* n.s. n.s.
Each species was considered a “main-plot” and represented a factor with a random effect nested in the locality. Management, location, year and season were the categorical fixed effect factors. The F-statistic values and corresponding type I error estimates for a likelihood-ratio test are shown. a p < 0.1. * p < 0.05. ** p < 0.01. *** p < 0.001.
The response to abandonment was different between the two meadows (Fig. 2). In June, the dry meadow plants under fallow conditions became larger while having the same proportion of blades and supportive organs than those which were mown. The same quantity of biomass was invested in reproductive organs so the lower proportion of reproductive biomass in fallow plots was the effect of the other biomass components. In October, the absolute investment in the leaf blades and supportive organs was higher for the fallow treatment. The highest investment in reproductive organs was observed in fallow treatment in October 2008. As this was higher than in June 2008, this indicates successful sexual reproduction in phenologically late species, which is not usually achieved in a mown meadow. When mown, plants primarily regenerated via leaf blades, whereas the supportive and reproductive organs reached minimal biomass values. In the wet meadow, differences between mown and fallow treatments in absolute investment in blades and supportive organs did not appear until 2008, when the values of biomass of both organs in fallow treatment exceeded those in the mown treatment. They were not in the same range, which led to a decreased proportion in the biomass of blades and an increased proportion
of supportive organs in fallow plots. The biomass of reproductive organs did not differ in either absolute or relative values. In October, the absolute investment in blades in fallow plots was slightly higher in 2006 whereas in 2008 the biomass of the blades was the same in both mown and fallow plots. In both years, the absolute and relative investments in supportive organs were higher in fallow plots. A significant allometric relationship was found between the biomass of leaf blades and supportive organs for the whole set of studied meadow species (Table 3; Fig. 3). The value for the slope was 0.91, and was not statistically different from the Enquist and Niklas (2002) value of 0.75 (F = 2.609, p = 0.115; Table 3; Fig. 3). The dry and wet meadows neither differed in the plant scaling exponent of this relationship nor were the scaling exponents of the dry and the wet meadow significantly different from the scaling exponent in the study by Enquist and Niklas (2002) (Table 3; Fig. 3). The difference between the meadows was in the elevation and their shift along the common slope, reflecting different species composition and thus investment (Table 3; Fig. 3). However, inside the localities there was no effect of the treatment, year or season on the scaling exponent of the relationship. Abandonment does not led to any significant changes in the studied relationship. In the dry meadow, only significant shifts in data along the common slope of the regression line comparing June and October were detected (stat = 4.46, p = 0.035; Table 3). Biomass allocation at the species level
Fig. 1. PCA ordination of biomass allocated to individual organs with passively projected centroids of four factor level combinations. The combinations of the season and the management, influencing most the differences in biomass allocation, are marked with different symbols and fills. The first two principal components explain 53% of the total data variability.
Species in both meadows differed in biomass allocation patterns under the continuing mowing regime, as shown by the mean values in June (Appendix: Fig. A1 and A2). The maximum average biomass of one shoot among individual species was 1.5 g in the dry meadow, compared with 0.9 g in the wet meadow (Appendix: Fig. A1). The investment in supportive organs ranged up to 56% in the dry and 69% in the wet meadow. The maximum investment in reproductive organs was 18% in the dry and 23% in the wet meadow; some species, however, did not flower at the time of mowing (Appendix: Fig. A1). In the dry meadow in June, only three species (Filipendula vulgaris, Helianthemum grandiflorum, Potentilla alba) out of 22 increased their relative investment in supportive organs in fallow
Please cite this article in press as: Bartuˇsková, A., et al., Changes in biomass allocation in species rich meadow after abandonment: Ecological strategy or allometry? Perspect. Plant Ecol. Evol. Syst. (2015), http://dx.doi.org/10.1016/j.ppees.2015.06.003
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Fig. 2. Biomass allocation in individual organs: absolute and relative values. The differences between two localities, within the growing season and between the years in mown and fallow plots are shown (mean, bars denote standard error).
plots. In contrast, four species (Bromus erectus, Cirsium pannonicum, Leontodon autumnalis, Plantago lanceolata) markedly decreased the same investment. Two species (Salvia pratensis, Ranunculus polyanthemos) invested less in reproductive organs in fallow plots and one species (Primula veris) even increased its investment (Fig. 4, Appendix: Fig. A2). In the wet meadow in June, six species (Deschampsia cespitosa, Galium boreale, Lathyrus pratensis, Lysimachia vulgaris, Potentilla
erecta, Selinum carvifolia) increased their relative investment in supportive organs in fallow plots and none of them decreased. An increase in relative investment in reproductive organs was found in one species (Carex pallescens) in fallow plots. The other species showed variable or no reaction to the abandonment (Fig. 4, Appendix: Fig. A2). In October, the plants with late phenology had markedly higher absolute and relative investments in supportive and reproductive
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Table 3 Allometric scaling coefficients for different groups of plant species and treatment, season or year influence.
Across all species Dry meadow species Wet meadow species Dry meadow Fallow treatment Mown treatment June October Year 2006 Year 2008 Wet meadow Fallow treatment Mown treatment June October Year 2006 Year 2008 Betonica officinalis Dry meadow Wet meadow Dry meadow Fallow treatment Mown treatment June October Year 2006 Year 2008 Wet meadow Fallow treatment Mown treatment June October Year 2006 Year 2008
˛SMA
Log ˇSMA
r2
p
(H0 : ˛ = 0.75) p
(H0 : heterogeneity in slopes) p
(H0 : no shift along slope) p
(H0 : no shift in elevation) p
0.914 0.687 0.926
0.091 0.009 −0.020
0.436 0.422 0.463
*** ** **
n.s. n.s. n.s.
– n.s.
– **
– **
0.492 0.454 0.559 0.381 0.520 0.422
−0.099 −0.195 −0.053 −0.252 −0.105 −0.187
0.517 0.414 0.504 0.217 0.472 0.459
*** ** *** * *** **
* ** n.s. ** * **
n.s.
n.s.
n.s.
n.s.
*
n.s.
n.s.
n.s.
n.s.
0.869 0.940 0.920 0.789 1.020 0.817
−0.091 0.036 −0.027 −0.131 0.021 −0.070
0.559 0.375 0.334 0.436 0.493 0.365
*** ** * ** ** **
n.s. n.s. n.s. n.s. n.s. n.s.
n.s.
n.s.
n.s.
n.s.
n.s.
n.s.
n.s.
n.s.
n.s.
0.761 1.045
0.079 0.107
0.750 0.633
*** ***
n.s. ***
***
–
–
0.925 0.763 0.911 0.657 0.777 0.737
0.096 0.142 0.168 −0.025 0.136 0.018
0.648 0.797 0.904 0.594 0.814 0.689
*** *** *** *** *** ***
** n.s. *** n.s. n.s. n.s.
*
–
–
**
–
–
n.s.
n.s.
n.s.
1.163 0.961 0.949 1.052 1.036 1.101
0.045 0.157 0.105 0.069 0.147 0.079
0.638 0.788 0.724 0.589 0.605 0.668
*** *** *** *** *** ***
*** *** ** *** *** ***
n.s.
n.s.
***
n.s.
*
*
n.s.
n.s.
n.s.
The table shows results of the standard major axis (linear) regression with slope ˛SMA , intercept Log ˇSMA , coefficient of determination r2 and statistical significance p: *, p < 0.05; **, p < 0.01; ***, p < 0.001. Data were calculated from log10 -transformed biomass of supportive organs versus log10 -transformed biomass of blades, with masses expressed in grams. The last part of the table shows statistical significance p of comparison of slopes (presence of common slope), shift along the common slopes and shift in elevation every time between two regression relationships. The top part of the table gives data for interspecific relationships, the bottom part data for intraspecific relationships on a case of Betonica officinalis.
organs in fallow plots than in mown plots. Among them, the allocation in Inula salicina, Serratula tinctoria and the dominant grass species Molinia arundinacea and Molinia caerulea were the most pronounced (Appendix: Fig. A3). The fact that one studied species, Betonica officinalis, occurred on both localities allowed us to compare the relationship between biomass of leaf blades and of supportive organs in relation to the effects of location, management, season and the year on the intraspecific level (Table 3; Appendix: Fig. A4). Localities differed between the slope of the relationship (F = 68.3, p < 0.001; Table 3; Appendix: Fig. A4), which equaled to 0.76 in the dry meadow and 1.04 in the wet meadow. There were also detected effects of the locality, treatment and season on the relationship. In the dry meadow, abandonment led to a higher scaling exponent and in June a higher scaling exponent was found than in October (Table 3; Appendix: Fig. A4). In the wet meadow, a shift in elevation in the case of treatment, and both a shift in elevation and along common slope in the case of season were found (Table 3; Appendix: Fig. A4).
Discussion Meadow plants responded to short term abandonment by producing larger shoots, however, relative investment into supportive structures for the community increased in the wet but not in the dry meadow. This study is the first to show that plants in temperate, European meadows invest more into supportive structures (stems
and petioles) with increasing competitive milieu (wet meadow) and this is not due to changed biomass allocation but to increasing plant size. The changes in the aboveground biomass allocation on the community level were within the frame of an allometric relationship. Allometric theory proved to provide a useful null model to which changes in biomass investment due to alterations of management or environmental conditions can be tested.
Biomass allocation within meadow communities The fact that at the community level meadow species generally follow the allometric relationship described by Enquist and Niklas (2002), suggests that even in one type of community, with species similar in size, the relationship described for all plants from dipterocarp to Arabidopsis could be observed. The results further showed that wet meadow plants invest more stem biomass per unit of leaf biomass than dry meadow plants (the same slope but different intercept of the allometric relationship). This difference between meadows is probably caused by the combined effects of the graminoids to dicot herbs ratio (on dry meadow 2:19, wet meadow 6:12) and a representation of different plant architectures (rosette, semirosette and erosulate shoot; Appendix: Fig. A1 and A2). The broad spectrum of the shoot architectures, in combination with the relatively small range of biomass amount, may lead to different scaling. Although those differences need to be studied in more detail, they indicate differences in allocation for
Please cite this article in press as: Bartuˇsková, A., et al., Changes in biomass allocation in species rich meadow after abandonment: Ecological strategy or allometry? Perspect. Plant Ecol. Evol. Syst. (2015), http://dx.doi.org/10.1016/j.ppees.2015.06.003
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Fig. 3. Interspecific log–log relationships between the biomass of supportive organs and the biomass of leaf blades in both the dry and the wet meadows together (a) and separately (b). The SMA regression lines represent the relationship for all the meadow species (a – black solid line), for the dry meadow species (b – black dashed line) and for the wet meadow species (b – black solid line). The grey solid lines represent the model by Enquist and Niklas (2002) with the slope equal to 0.75. The symbols indicate the mean value for each species. The SMA regression scaling coefficients and statistical significance are written in Table 3.
different architectures of herbaceous plants as was similarly found for trees (e.g. angiosperm and conifer leaves [Enquist and Niklas, 2002]). Despite some reservation in the literature for using allocation theory for answering ecologically relevant questions (e.g. Tilman et al., 2004; Metcalf et al., 2006), these results can be
considered as proof that the examination of allocation could contribute to the understanding of meadow plant strategies. An inseparable part of biomass allocation is below-ground biomass. In the meadows, where the below-ground organs are entangled on a small scale, it is not possible to responsibly obtain biomass of this fraction. Although variations in below-ground biomass allocation are known to be affected by environmental conditions or ontogenetic drift, results are, however, inconsistent (e.g. Gedroc et al., 1996; Poorter et al., 2011; Janeˇcek et al., 2014). Community and species level of response to changing management
Fig. 4. PCA ordination of percentage of biomass allocated to individual organs with passively projected centroids of individual species values in mown () and fallow () treatments in June. Species name abbreviations are given in Table 1. In the dry and wet sites, the first two principal components explain 37% and 32% of the total data variability, respectively.
Different species at a site have a mix of strategies (Westoby et al., 2002) that facilitate their occupation of different available niches (Manson et al., 2011; de Bello et al., 2012) and individual species studied here show variable responses. In the wet meadow, several species responded to abandonment by increasing their investment into supportive organs and others did not change the allocation. In the dry meadow, however, the reaction of species was more diverse. Three species increased their relative investment in supportive organs, four other species reduced this investment and the remaining species showed no reaction. A similar mixture of positive and negative effects on growth was observed by Niu et al. (2008) in a Tibetan alpine meadow after fertilization. Additionally, below species level, individual plant shoots experience different competitive pressure from their surrounding and their response is therefore “shoot specific” (Metcalf et al., 2006; Lanta et al., 2011). This effect could be included when scaling biomass allocation on the species level as was done for the Tibetan alpine meadow (Niu et al., 2008): a significant treatment effect on the scaling relationship was found in one quarter of cases and this was in accordance with the trends for the community. In this study, the relationship was tested for only one species which occurred on both sites and its reaction was site-specific, with real plasticity in aboveground biomass allocation. This was therefore not in accordance with the trend for the whole community. This result points
Please cite this article in press as: Bartuˇsková, A., et al., Changes in biomass allocation in species rich meadow after abandonment: Ecological strategy or allometry? Perspect. Plant Ecol. Evol. Syst. (2015), http://dx.doi.org/10.1016/j.ppees.2015.06.003
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to the lack of a strong factor affecting all plant individuals in both studied meadows and it also indicates that the response of individual plants in a community context is only partly reflected in the community response; this deserves further study. In Central European meadow communities, all aboveground plant structures are produced during the course of the growing season, which is interrupted by mowing. After mowing, the ability to compensate for the lost biomass is a key factor in determining the biomass allocation late in the season and is affected by plant size and shoot architecture (Klimeˇsová et al., 2010). On the contrary, for fallow plots, the competition for light is a crucial factor. Large plants are usually phenologically late and if they are not subjected to mowing, they may flower and accumulate biomass later in the season (Kahmen and Poschlod, 2004; Sun and Frelich, 2011). The resulting large biomass and tall canopy causes a considerably lower light availability inside a stand (Anten and Hirose, 1999). The increase in the biomass of the tall herbs after abandonment also leads to an increase in their dominance, whereas smaller herbs quickly decrease in abundance (Huhta et al., 2001; Kahmen and Poschlod, 2004; Niu et al., 2008; Lanta et al., 2011; Klimeˇsová et al., 2011). The mowing affects all plants, regardless of their actual phenological phases, at the same time. In this study, biomass allocation was measured as the amount of biomass that meadow plants are able to produce until the mowing time or until the end of the growing season. These two time periods represent rather similar phenological phases in the majority of meadow species (Martínková et al., 2002; Lanta et al., 2011), even when the management itself can change phenology of grassland plants (Niu et al., 2008; Zhang et al., 2014). There were two different effects of the management on biomass partitioning in this study: (i) direct effects of lost versus reserved biomass resulting in large changes in biomass investments during the growing season was dominant on the dry meadow. The mown meadow was more “leafy” in October while the abandoned meadow was less “leafy” and this effect could be attributed to the shoot architecture of meadow plants (Klimeˇsová et al., 2008, 2010); (ii) in the wet meadow, the effect of abandonment, under which plants steadily increased investments into supportive structures, was most pronounced. This indicates a strong effect of species composition and/or environmental factors on the respective meadows. For the wet meadow, the regrowth of plants after mowing is not limited by water availability while the opposite is true for the dry meadow (de Bello et al., 2012). The fact that the wet meadow community has a higher biomass production and was characterized by higher relative investments into supportive structures in most dates and treatments contrasts with the dry meadow and indicates that competitive milieu is higher there. The low-competitive environment of the dry meadow is reflected in the fact that this very meadow is listed as the most species rich community (on the small scale) known to botanists on Earth (Wilson et al., 2012). It is also known that the least productive and the most species-rich parts of this meadow are resistant to short-term changes of management, contrary to the more productive parts (Klimeˇs et al., 2013). Summer drought has strong effect on plant competitive ability and slows down changes in vegetation on abandoned sites. It could therefore be concluded that the lack of uniform changes in biomass allocation on the dry meadow reflect the fact that even three years of abandonment does not result in increasing competitive milieu in the stand.
Acknowledgements This work would not have been possible without cooperation and logistic support from the Bílé Karpaty Protected Landscape
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Please cite this article in press as: Bartuˇsková, A., et al., Changes in biomass allocation in species rich meadow after abandonment: Ecological strategy or allometry? Perspect. Plant Ecol. Evol. Syst. (2015), http://dx.doi.org/10.1016/j.ppees.2015.06.003