94
|
Appl Veg Sci. 2020;23:94–106.Applied Vegetation Science
wileyonlinelibrary.com/journal/avsc
Received: 2 July 2019
|
Revised: 9 September 2019|
Accepted: 28 October 2019 DOI: 10.1111/avsc.12471R E S E A R C H A R T I C L E
Barriers to restoration: Soil acidity and phosphorus limitation
constrain recovery of heathland plant communities after sod
cutting
Joost J. Vogels
1,2| Maaike J. Weijters
3| Roland Bobbink
3| Rienk-Jan Bijlsma
4|
Leon P. M. Lamers
5| Wilco C. E. P. Verberk
2| Henk Siepel
2This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
© 2019 The Authors. Applied Vegetation Science published by John Wiley & Sons Ltd on behalf of International Association for Vegetation Science 1Bargerveen Foundation, Nijmegen, The
Netherlands
2Department of Animal Ecology and Physiology, Radboud University Nijmegen, Nijmegen, The Netherlands
3B-WARE Research Centre, Radboud University Nijmegen, Nijmegen, The Netherlands
4Department of Vegetation, Forest and Landscape Ecology, Wageningen Environmental Research, Wageningen, The Netherlands
5Department of Aquatic Ecology and Environmental Biology, Radboud University Nijmegen, Nijmegen, The Netherlands Correspondence
Joost J. Vogels, Bargerveen Foundation, Toernooiveld 1 6525 ED Nijmegen, The Netherlands.
Email: j.vogels@science.ru.nl Funding information
This research was funded by the O + BN programme, financed by the Dutch Ministry of Agriculture, Nature and Food Quality and BIJ12 (Grant No. OBN207-DZ).
Co-ordinating Editor: Rob Marrs
Abstract
Questions: Sod cutting has been used extensively as an effective measure in re-moving excess N and restoring dwarf shrub dominance in heathlands affected by increased nitrogen deposition. However, recovery of other plant species is often very limited. One barrier is high soil acidity following sod cutting, which results in soil
alu-minium (Al3+) and ammonium (NH
4+) reaching toxic concentrations. Sod-cutting
man-agement also removes most of the major nutrients from the system, so intensified nutrient limitation could be an additional barrier to the recovery of species-rich com-munities. Soil phosphorus (P) is of special interest as research indicates sod-cutting management can shift the system to P limitation.
Location: Hoge Veluwe National Park, The Netherlands.
Methods: We set up a full-factorial experiment in sod-cut heathland formerly en-croached by Molinia caerulea, adding phosphate (P+) and lime (Ca+) and over the next three growing seasons, we recorded soil chemistry and plant responses.
Results: Soil inorganic N, especially soil NH4+, strongly declined after liming compared
to the control situation, confirming that liming alleviates NH4+ toxicity. Addition of P
resulted in a similar decline, also suggesting a role for soil phosphate availability in this process. Acid-sensitive plant species richness increased significantly in both Ca+ and P+ treatment, whereas acid-insensitive plant species richness only increased sig-nificantly as a result of P+ treatment. Mean vegetation relative growth rate increased significantly in both Ca+ and P+ treatments.
Conclusions: Excessive P removal due to sod cutting constitutes a second barrier to restoration in addition to soil acidity. We discourage the large-scale use of sod cut-ting to reduce soil N availability in heathlands and propose to use interventions that leave the soil nutrient balance intact, such as burning and grazing, mowing or litter removal, in combination with measures that restore the soil buffer capacity.
Applied Vegetation Science
1 | INTRODUCTION
Human activities have dramatically increased the emissions of ni-trogen oxides (NOx), ammonia (NH3) and sulphur dioxide (SO2) into the atmosphere during the last century, affecting ecosystem func-tioning on a global scale (Likens, Bormann, & Johnson, 1972; Elser, 2011). Increased atmospheric deposition of eutrophying and acidify-ing compounds is considered a major threat to the conservation of Western-European lowland dry heathlands (Roelofs, 1986; Bobbink & Heil, 1993; Heil & Bobbink, 1993; Power, Ashmore, Cousins, & Ainsworth, 1995; Bobbink, Hornung, & Roelofs, 1998; Dorland et al., 2013; Friedrich et al., 2011). Annual nitrogen (N) deposition, mostly as reduced N (NHx, i.e. NH3 and NH4+), is high in this region due to the high level of industrialization and agricultural intensification. While the deposition of acidifying sulphuric acids has strongly de-clined in the last decades due to strong regulation, the empirical crit-ical load for N compounds for dry heathlands (10–20 kg ha−1 year−1, Bobbink & Hettelingh, 2011) has been exceeded in the Netherlands for 4–5 decades and deposition continues to exceed critical loads (Velders et al., 2015). Concomitantly, dry heathlands have been in-creasingly dominated by grasses (Heil & Diemont, 1983; Bobbink et al., 1998). Shifts towards grass dominance have largely been attributed to increased competitive strength of graminoids under conditions of higher N availability (Heil & Bruggink, 1987; Kirkham, 2001; Falk et al., 2010). In addition, increased levels of soil am-monium (NH4+) and soil aluminium (Al
3+) and resulting higher soil NH4:NO3 and/or Al:Ca ratios have repeatedly been found to neg-atively impact vascular plants, in particular forb species (Houdijk, Verbeek, Vandijk, & Roelofs, 1993; De Graaf, Bobbink, Verbeek, & Roelofs, 1997; De Graaf, Bobbink, Roelofs, & Verbeek, 1998a; Roem & Berendse, 2000; Roem, Klees, & Berendse, 2002; Stevens et al., 2011). Concurrently, a general decrease in plant species richness has occurred. Plant communities that have been strongly affected by at-mospheric deposition of N and S are relatively species-rich Violion caninae communities and formerly more species-rich heaths, such as Genisto-Callunetum danthonietosum (Stevens et al., 2010; Southon, Field, Caporn, Britton, & Power, 2013).
In order to mitigate the effects of increased N deposition, res-toration management efforts have focused largely on maximizing N removal, usually by organic matter removal. Consequently, rigorous measures such as sod cutting (shallow topsoil removal) have been implemented in lowland heathlands subject to increased N depo-sition (Diemont, 1996; Webb, 1998; Härdtle, Niemeyer, Niemeyer, Assmann, & Fottner, 2006).
Although proven highly effective in removing excess N from the system and in restoring dominance of the dwarf shrub Calluna
vulgaris (Aerts & Heil, 1993; Diemont, 1996; Britton, Marrs, Carey, & Pakeman, 2000), recovery of a species-rich heathland vegetation after sod cutting is often very limited (Dorland et al., 2004). The re-moval of organic matter, which serves as the major component of the soil cation exchange capacity (van den Berg, Vergeer, & Roelofs, 2003), and in which the majority of viable seeds is stored (Bruggink, 1993; Jansen, de Graaf, & Roelofs, 1996) is implicated in the poor recovery. However, removal of soil organic matter also results in the indiscriminate removal of soil nutrients. Soils in dry heathland ecosystems are characterized by a high degree of nutrient stratifi-cation, with the majority of nutrients being stored and recycled in the humus-rich O, Ah and B horizons (Nielsen, Hansen, Ladekarl, & Nørnberg, 2000). Removal of the top soil is therefore not only highly effective in removing excess N from the system; other nutrients, in particular phosphorus (P), are also removed in substantial quantities (De Graaf, Verbeek, Bobbink, & Roelofs, 1998b; Härdtle et al., 2006, 2009). Thus, sod-cutting management contributes further to the shift from N to P limitation in dry heathlands, something which can be further exacerbated by increased soil acidity, which fixes P in the soil by the formation of Fe and Al-complexes with decreasing pH (Kooijman, Dopheide, Sevink, Takken, & Verstraten, 1998; Blume et al., 2016) and impacts ecosystem functioning across trophic levels through increased plant N:P stoichiometry (Vogels, Verberk, Lamers, & Siepel, 2017).
A decline in heathland plants sensitive to acidification has been mechanistically explained by the relatively high sensitivity these plants have to high Al:Ca and/or NH4:NO3 ratios in the soil (De Graaf et al., 1997; De Graaf, Bobbink, et al., 1998a;van den Berg et al., 2005; van den Berg, Peters, Ashmore, & Roelofs, 2008), which can lead to root damage, Al and/or NH4 toxicity (Rengel, 1992; Ryan, Kinraide, & Kochian, 1994; Gerendas, Zhu, Bendixen, Ratcliffe, & Sattelmacher, 1997), ultimately resulting in lowered germination rates and reduced settlement success of these plant species (De Graaf et al., 1997; van den Berg et al., 2005; Stevens et al., 2011). Liming has been proven to reduce NH4 and Al toxicity (i.e. lowered NH4:NO3 and Al:Ca ra-tios) and shown to increase germination and settlement rates of ac-id-sensitive plant species (De Graaf, Verbeek, et al., 1998b; Dorland, Bobbink, Messelink, & Verhoeven, 2003; Dorland et al., 2004). Alleviation of P limitation is also known to be able to decrease the ratio of NH4 to NO3 uptake in plants (Schjørring, 1986). This may be particularly relevant for this study since sod cutting also strongly reduces nitrification rates (Dorland et al., 2004, 2003) and thus in-creases soil NH4:NO3- ratios. NH4 typically increases strongly in heathland soils 1–2 years after sod-cutting management (De Graaf, Verbeek, et al., 1998b; Dorland et al., 2003).
Acidification can also hamper P uptake by plants, as a high soil Al concentration has been found to negatively affect plant P K E Y W O R D S
acidification, aluminium toxicity, eutrophication, heathlands, nitrogen availability, nutrient balance, phosphorus availability, restoration management, sod cutting, species richness, turf cutting
uptake performance (Gessa, Mimmo, Deiana, & Marzadori, 2005). We therefore hypothesize that heathland plants that have relative high P requirements are more sensitive to acidification than species with low P requirements. Under circumstances of already reduced P availability through sod-cutting management, this may as well ex-plain poor vegetation recovery. Thus, recovery could be constrained by acidity-induced toxicity, or by increased P limitation due to re-duced P uptake efficiency. These two hypotheses are not mutually exclusive and may act in tandem.
In order to test both hypotheses, we set up a full-factorial ex-periment in Molinia caerulea-encroached dry lowland heathland that underwent sod-cutting management. We experimentally added P to levels resembling total P before sod-cutting management took place, experimentally mitigated soil acidity by adding dolomite (CaCO3/ MgCO3) in half of the experimental plots and assessed vegetation response in the settlement phase. Next, we attempted to unravel the underlying mechanisms governing vegetation responses by drawing on ecological information from the recorded species available from national and international data sources, and compared these with changes in all relevant soil chemistry parameters.
2 | METHODS
2.1 | Site description
Experimental plots were established in Hoge Veluwe National Park, in the centre of the Netherlands (52°.2′.30″ N; 5°.49′.50″ E) at a site that underwent sod-cutting management in the first quarter of 2012. Before sod cutting the vegetation was highly dominated by M. caerulea. At the start of the experiment in autumn 2012, the soil was still bare, no vegetation had yet established. For more detailed infor-mation on the experimental site and setup see Figure 1 and Siepel et al. (2018).
2.2 | Experimental setup
Experimental plots measured 15 m × 15 m in size and were placed in a randomized block design each consisting of four plots. In total five blocks were installed (n = 5). On the plots, the treatment to re-duce soil acidity (further referred to as Ca+, but note that Mg was also added in this treatment) was achieved by the addition of do-lomite (200 g/m2 granular Dolokal; 80% CaCO
3 and 20% MgCO3). P-replenishment treatment (further P+) was achieved by adding 5 g P/m2 by spraying an aqueous solution of NaH
2PO4·2H2O, add-ing in total 5.67 kg NaH2PO4·2H2O per plot. P+ treatment (early April 2013) was carried out substantially later than Ca+ treatment (December 2012), in order to avoid high PO43- sorption resulting from liming acid soils, as reported by Haynes (1982). Each plot re-ceived either P+ or no addition (P−) and Ca+ or no addition (Ca−), resulting in four treatment combinations: P+Ca+, P+Ca−, P−Ca+ and P−Ca−. Vegetation was allowed to develop naturally.
2.3 | Soil chemical sampling and analysis
Soils were sampled on 9.07.2012 (t = 0; immediately after sod cut-ting), after addition of P and Ca on 24.09.2013 (t = 1; one growing season after application of treatments) and on 23.09.2014 (t = 2; two growing seasons after application of treatments). From each plot, a pooled soil sample was obtained by random sampling of three soil cores (0–10 cm depth; 3 cm diameter) using an auger (Eijkelkamp Soil & Water). Samples were immediately packed in airtight containers and stored at 4°C until extraction.
Soil pH, NO3−, NH
4+ and exchangeable ion concentration were determined by mixing fresh soil (17.5 g) with 50 ml 0.2 M NaCl solution. pH of the solution was measured immediately using a combined pH electrode (radiometer and a TIM840 pH meter, Hach Lange GmbH). Soil extract was collected under vacuum conditions with Teflon pore water samplers (SMS10, Rhizosphere Research products). For later analysis of dissolved ions, 10 ml soil extract was transferred to a tube and HNO3 was added until a 1% concentration was reached and then stored at 4°C. For later analysis of NO3− and NH4+, 20 ml of extract was transferred to a 20-ml flask and stored at −20°C. Plant-available P (POlsen) was determined by incubating 3 g dried soil in 60 ml 0.5 M sodium carbonate (NaHCO3) for 30 min at 105 rpm (Olsen, Cole, Watanabe, & Dean, 1954).
Concentrations of cations and POlsen in the soil extracts were measured with inductive coupled plasma spectrophotometry (ICP: IRIS Intrepid II XDL, Thermo Electron Corporation). The concen-trations of NO3− and NH
4+ were determined with an Auto Analyser III (Bran & Luebbe), using hydrazine sulphate (Kamphake, Hannah, & Cohen, 1967) and salicylate (Grasshoff & Johannsen, 1972) respectively.
2.4 | Vegetation relevés
Vegetation composition was quantified in all plots, two (09.2014) and three (07.2015) growing seasons after treatment applica-tion, using the full surface of each experimental 15 m × 15 m plot. Percentage cover was estimated for the total herb and moss layer and for individual vascular plant species with cover >1%. All other species (with cover <1%) were estimated in abundance classes (rare, uncommon, common, abundant) using the adapted Braun-Blanquet scale proposed by Barkman, Doing and Segal (1964).
2.5 | Data gathering and analysis
We quantified the response of acid-sensitive plants by contrasting the patterns in species richness (SR) of plant species typical of the Violion caninae (acid-sensitive) with those of the Calluno-Genistion pilosae (insensitive). Nominal vegetation relevé data were first trans-formed from occurrence code to cover percentage classes (rare: 1%, uncommon: 2%, common: 3%, abundant: 4%) before analysis. Total vegetation cover was calculated as the sum of all recorded plant
Applied Vegetation Science
cover percentage classes in each plot. Plant species were assigned to one or more of the phytosociological unions Violion caninae and Calluno-Genistion pilosae according to Schaminée, Stortelder and Weeda (1996), or to "other plants" when not typical for any of these communities (Appendix S1). For each plot, the SR of these groups was calculated. We used relative growth rate (RGR) as proxy for the relative P need of a plant species, as species with a high RGR tend to have higher relative P needs reflected by lower N:P ratios (Sterner & Elser, 2002). We used the median species RGR values of available species data from the TRY database (Kattge et al., 2011) in order to calculate occurrence-based mean species RGR for each plot (Appendix S1: 47.1% of species data available). Plot SR, total veg-etation cover, plant community SR and TRY-derived mean species RGR were then used to evaluate the response of the vegetation to experimental treatments.
Statistical analyses were performed using R version 3.4.1 (R Core Team, 2017). As normality and variance assumptions for
linear methods were not met, effects of treatments on soil chem-ical parameters, SR and percent cover data were tested by fitting a General Linear Mixed-Effect Model (GLMM) with block as ran-dom factor. We initially constructed a full model formulation for both soil chemistry and vegetation response variables with all pos-sible interactions: response ~ P × Ca × Growing season. Models were then simplified to the minimum adequate model by dropping non-significant interactions from the model and by AIC compari-son. In order to retain model balance, when a treatment × growing season interaction was significant, all other interaction terms of the same level with growing season were kept in the model regard-less of their significance. Soil chemistry data were fitted using a gamma distribution with log link, except for pH and plant-available phosphorus, where identity link usage was more appropriate. SR and percent cover data were fitted using a Poisson distribution with log link. As normality and variance assumptions for RGR were appropriate for linear prediction models, we used LMMs using the
F I G U R E 1 Aerial false-colour photo taken in 2016, showing the lay-out of the experimental plots in De Hoge Veluwe National Park. Dark
red surfaces are old, light-red surfaces are recent sod-cut sites in Molinia-dominated vegetation (grey surfaces). Numbered replicates (PM) represent treatment blocks, treatment plots of 15 m × 15 m are represented by white (P−Ca−), yellow (P−Ca+), blue (P+Ca−) and red (P+Ca+) circles. P−: no P added, P+: P added, Ca−: no lime added, Ca+: lime added. Distance between numbers along the margin is 100 m
same model structure and procedures as for the GLMMs for signif-icance testing of treatment effects. GLMMs were fitted using the package lme4 (Bates, Maechler, Bolker, & Walker, 2015), LMMs using the package nlme (Pinheiro, Bates, DebRoy, Sarkar & R Core Team, 2017).
3 | RESULTS
3.1 | Soil chemistry
At the start of the experiment in 2012, soil pH and concentrations of exchangeable Ca and Mg were similar to those for other Dutch dry heathland soils (De Graaf, Bobbink, Smits, Van Diggelen, & Roelofs, 2009; Table 1; see Appendix S2 for treatment means of all measured soil chemistry parameters). Soil NH4+ concentrations were very high in all plots with concentrations above 1,500 µmol/kg soil (Figure 2). Concentrations of NO3− were also higher (60–86 µmol NO
3−/kg
soil; Figure 2) compared to species-rich heathland soils (0–33 µmol/ kg soil; De Graaf et al., 2009). Plant-available P (POlsen) ranged be-tween 499 and 596 µmol/kg soil (Figure 2). Not surprisingly, Ca+ treatment led to a substantial increase in soil exchangeable Ca (by a
factor of 8.2 and 6.2 in the years following application; Appendix S2) and Mg (by a factor of 19.5 and 14.7; Appendix S2).
Soil chemistry status was homogenous for all tested soil chem-ical parameters in pretreatment conditions; no significant P or Ca effect was found in pretreatment conditions (Table 1). Soil pHNaCl increased significantly in Ca+ treatment plots in both subsequent growing seasons (Table 1). Ca+ treatment resulted in a significant decrease (Table 1) in exchangeable Al (by a factor of 6.7 and 7.4). P+ treatment had no significant effect on soil pH nor soil exchange-able Al (Texchange-able 1). No significant post-treatment interaction effects of P+ with Ca+ on soil chemistry parameters were found (Table 1), so effects were either additive or resulting from one single treatment only.
Plant-available PO43- decreased over time in treatments without P addition (i.e. both the control and Ca+ treatment) (Figure 2) result-ing in significantly lowered plant-available P in the second growresult-ing season (Table 1, Figure 2). P+ treatment initially led to a strong and significant increase in plant-available PO43- concentration (by a fac-tor of 1.42 in the first growing season; Table 1). In the second grow-ing season, plant-available PO43- in the P+ treatment had dropped to pretreatment levels, but was still higher compared to the treatments without P addition (Figure 2).
TA B L E 1 GLMM summaries for soil chemistry data
pH(NaCl)a Al3+
(NaCl)b NH4+ (NaCl)b NO3− (NaCl)b PO43− (Olsen)a
Estimate
(SE) t
Estimate
(SE) t Estimate (SE) t
Estimate
(SE) t Estimate (SE) t
Intercept 3.52 (0.07) 51.35*** 8.03 (0.22) 37.27*** 7.44 (0.22) 34.15*** 4.29 (0.23) 18.38*** 526.8 (38.1) 13.81*** P −0.03 (0.07) −0.46NS 0.003 (0.25) 0.01NS 0.06 (0.23) 0.28NS 0.10 (0.27) 0.36NS 21.5 (45.8) 0.47NS Ca −0.07 (0.07) −1.01NS −0.02 (0.25) −0.08NS −0.07 (0.23) −0.32NS −0.08 (0.27) −0.29NS 6.86 (47.8) 0.14NS Growing season 1 0.09 (0.09) 1.00NS −0.26 (0.30) −0.88NS −0.65 (0.28) −2.33* −0.03 (0.32) −0.09NS −47.4 (50.1) −0.95NS Growing season 2 0.09 (0.09) 1.03 NS −0.34 (0.30) −1.15NS −2.15 (0.28) −7.58*** −0.34 (0.31) −1.08NS −142.7 (44.3) −3.22** P × Growing season 1 −0.02 (0.10) −0.22NS 0.13 (0.35) 0.37NS −0.23 (0.33) −0.71NS −0.44 (0.38) −1.14NS 321.4 (68.9) 4.67*** P × Growing season 2 −0.05 (0.10) −0.50NS 0.22 (0.36) 0.62NS −1.61 (0.34) −4.79*** −2.17 (0.39) −5.53*** 208.8 (60.5) 3.45*** Ca × Growing season 1 0.61 (0.10) 6.02*** −1.71 (0.35) −4.82*** −0.70 (0.33) −2.16* 0.70 (0.38) 1.84NS −82.3 (68.4) −1.20NS Ca × Growing season 2 0.46 (0.10) 4.67*** −1.79 (0.36) −5.04*** −0.52 (0.33) −1.60NS −1.57 (0.39) −4.04*** −97.1 (59.6) −1.63NS P × Ca – – – – – – – – – – P × Ca × Growing season 1 – – – – – – – – – – P × Ca × Growing season 2 – – – – – – – – – –
Model parameters and t-scores are estimates from the simplified model formulation: response ~ P × Growing season + Ca × Growing season. No significant P × Ca × Growing season effects were found in the initial model formulation. –, Term removed from model formulation during model simplification steps. NS, no significant effect. *, **, ***, Significance p levels of 0.05; 0.01 and 0.001, respectively.
aGamma GLMM, identity link.
Applied Vegetation Science
NH4+ concentrations decreased significantly in the first andsec-ond growing season regardless of the treatment (Table 1; Figure 2). Additionally, both Ca+ (first growing season) and P+ (second growing season) treatment resulted in a significant further decrease of soil NH4+ compared to control (Table 1; Figure 2). Soil NO
3− concentra-tion decreased significantly in the second growing season in both P+ and Ca+ treatments (Table 1; Figure 2), with P+ treatment having a stronger effect than Ca+ treatment. NO3− concentrations in the P− Ca+, P+Ca− and P+Ca+ treatments after two years were well within the range measured in species-rich dry heathlands (De Graaf et al., 2009).
3.2 | Vegetation response
Total SR and typical plant SR increased considerably between the second and third growing season as the overall mean SR in-creased from 10 to 21 species (Figure 3; Table 2). Both P+ and Ca+ treatment significantly increased SR (Figure 3; Table 2). Mean SR increased by a factor of 1.39/1.64 (P+), 1.35/2.52 (Ca+) and 2.71/3.58 (P+Ca+) compared to control in the second and third growing season respectively (Figure 2). SR of plants typical for Violion caninae increased significantly between both growing sea-sons, from 8.25 to 14.9. Both P+ and Ca+ treatments significantly increased SR by a factor of 1.40/1.59 (P+), 1.17/1.82 (Ca+) and 1.93/2.06 (P+Ca+) in the second and third growing season. SR of plants typical for Calluno-Genistion pilosae increased significantly between both growing seasons (from 7.2 and 10.8 species) and as an effect of P+ treatment, by a magnitude of 1.28/1.48 in the second and third growing season, but Ca+ treatment did not lead to a significant increase. Non-typical plant species increased be-tween growing seasons (overall from 1.75 to 5.75) but were almost exclusively found in P+ and/or Ca+ treatments. Hence, both P+ (average of 0.2/3.8 species in second/third growing season), Ca+ treatment (1.4/7.2 species) and P+Ca+ treatment (5.2/11.8 species) led to a significant increase in non-typical plant SR. No significant interaction effects between P+ and Ca+ treatments nor treatment by season interactions were found in either of the SR estimates, indicating that treatment responses were additive and that SR had increased to the same degree in all treatments in the third grow-ing season. Overall mean vegetation cover increased significantly (Table 3) between the second and third growing season from 43.1% to 64.1%. P+ and Ca+ treatments significantly increased vegeta-tion cover compared to control, by a magnitude of 1.65/1.77 for P+, 1.34/1.75 for Ca+ and 2.34/2.43 for P+ Ca+ in the second and third growing season respectively (Figure 3, Table 2). Vegetation cover increased significantly faster with Ca+ treatment in the third growing season compared to the second growing season (Table 2). Mean occurrence-based vegetation RGR values increased signifi-cantly between growing seasons and for P+ as well as Ca+ treat-ments (Figure 3; Table 2), with Ca+ treatment having a stronger effect than P+ treatment.
4 | DISCUSSION
The results of the experimental treatments on soil chemistry largely confirm our hypotheses: both addition of Ca (suggesting recovery to be constrained by acidity-induced toxicity) and addition of P (suggesting recovery to be constrained by P limitation) enhanced vegetation recovery, including better recovery of target species characteristic for either communities of Violion caninae (effects of both P and Ca) and of Calluno-Genistion pilosae (effects of P). Soil pH increased and exchangeable Al decreased in both seasons a result of Ca+ treatment only. Phosphate addition increased plant-available P in the first season and kept plant-available P concentrations at pretreatment levels, whereas in controls plant-available P remained constant in the first season and significantly declined in the second season. This reduction of soil P concentration below pretreatment conditions could have resulted from uptake by resettling plants and microorganisms, suggesting that plant-available P in the soil becomes increasingly limiting as vegetation development progresses. As re-ported in earlier studies (Dorland et al., 2003; 2004), soil inorganic N significantly decreased in Ca+ treatments compared to control, probably through stimulation of soil microbial activity and net nitri-fication. Soil inorganic N also decreased stronger in P+ treatments compared to control and the magnitude of the decrease was largely similar between Ca+ and P+ treatment. The mechanism driving the decrease in soil inorganic N could be increased uptake by vascular plants and/or soil microbes or enhanced nitrification rates by higher microbial activity. While both mechanism are possible, it is clear that increasing bioavailable phosphate stimulates N uptake and/or turno-ver, thus supporting the increased P limitation hypothesis.
Species typical for Violion caninae communities strongly in-creased in response to the experimental amelioration of P limita-tion (P+) as well as soil acidity (Ca+), especially in the first growing season. These communities generally occur on soils with higher soil buffer capacity within the heathland landscape (De Graaf et al., 2009), explaining the positive effect of liming. Strikingly, our results indicate that higher P availability also promotes the estab-lishment of species from this community. Furthermore, species only typical for Calluno-Genistion pilosae (dry heathland) commu-nities increased only in response to P addition, but liming did not significantly increase species settlement. The lack of a response to liming probably reflects the greater tolerance of these species to high soil acidity. The effects of P addition on vegetation re-covery indicate that establishment of species of Calluna heathland may be hampered as a result of excessive P removal resulting from sod-cutting management (Härdtle et al., 2006; Vogels et al., 2017). We also observed an increase in species that were not typical for heathlands in our P+ and Ca+ treatments. These species are likely driven by the presence of bare soil with a temporal increase in soil nutrients, as most of these species are typical ruderal or pioneer species of dry sandy soils, temporarily settling on disturbed sites such as clear-cuts in forests and after burning. With decreasing plant-available N and P due to plant uptake and a gradual reduction
of N mineralization, these non-typical species are therefore not expected to persist in the longer term.
As hypothesized, mean vegetation RGR increased in P+ and Ca+ treatments and was highest when both treatments were combined. This further supports our hypotheses that: (i) root up-take efficiency for P is partly affected by soil acid status; (ii) plant species with higher RGR have higher relative P needs; and sub-sequently (iii) acid sensitivity of plant species characteristic for heathland is partly due to higher P needs driven by higher RGR. Examining the mean RGR of these groups in our study supported this: Calluno-genistion mean RGR [±1 SE] was 0.12 [0.017] day−1,
while for Violion caninae this was 0.14 [0.014] day−1 and for the species unique to Violion caninae, 0.15 [0.019] day−1. In general, herbaceous species have higher relative growth rates than woody species (Hunt & Cornelissen, 1997), and the species under scru-tiny in this study followed this general rule (mean RGR of herbs vs. woody [±1 SE] = 0.15 [0.012] vs. 0.11 [0.019] day−1). The RGR of Ericaceae is especially low, with a median of 0.05 for Calluna vulgaris (derived from the TRY database: Kattge et al., 2011). Graminoids have relatively high P resorption rates (Aerts, 1996), enabling them to sustain a relatively high RGR under P-limited conditions. As species adapted to P-limited conditions tend to
F I G U R E 2 Soil exchangeable NH4+, NO
3−, pH(NaCl), soil-exchangeable Al3+ and plant-available (Olsen) PO43− concentration (µmol/kg soil)
at pretreatment (2012), and after one (2013) and two growing seasons (2014) in all different treatment combinations. P−: no P added, P+: P added, Ca−: no lime added, Ca+: lime added
Applied Vegetation Science
resorb more P from senescent leaves (Wright & Westoby, 2003), this explains why in the naturally N- and P-poor heathland envi-ronment, grass species adapted to low P availability (i.e. M. caeru-lea; Kirkham, 2001) are becoming dominant when N deposition is increased. Ericoid mycorrhizal symbiosis enables the host plant, Ericaceae, to also utilize organic sources of N (Stribley & Read, 1980) and P (Pearson & Read, 1973) even at high concentrations of Fe and Al that are associated with high acidity (Shaw & Read, 1989) and have an important function in avoiding metal toxic-ity in the plant by binding these ions to the intercellular hyphal
complexes (Bradley, Burt, & Read, 1982). This enables ericaceous species to become dominant on highly acidic soils that are char-acterized by low concentrations of inorganic N and P. Sod-cutting management creates these conditions, explaining why this man-agement practice results in recovery of Calluna dominance. At the same time, it also explains the high failure rate of this prac-tice in restoring species-rich dry heathland plant communities, as sod-cutting management does not alleviate soil acidity-re-lated toxicity and results in shifting the system to an increased P-limited state.
F I G U R E 3 Box-plots of total species richness, vegetation cover, amount of typical species of Violion caninae and Calluno-Genistion pilosae
plant communities, other (non-typical) plant species and mean Relative Growth Rate in all treatments, after two (2014) and three (2015) growing seasons. Y-axes depict number of species, except for vegetation cover (%cover) and mean Relative Growth Rate (day−1). P−: no P added, P+: P added, Ca−: no lime added, Ca+: lime added
T A B LE 2 G LM M /L M M s um m ar ie s f or v as cu la r p la nt s pe ci es r ic hn es s ( SR ), t ot al v eg et at io n c ov er , p la nt c om m un ity t yp ic al p la nt S R a nd o cc ur en ce b as ed m ea n v eg et at io n R G R ba se d o n ve ge ta tio n r el ev é d at a Spec ie s r ich ne ss Ve ge ta tio n co ve r V io lio n ca ni na e SR a Call un o-G en is tio n p ilo sa e SR a O th er p la nt s S R b RG R c Es tim at e ( SE ) Z Es tim at e ( SE ) Z Es tim at e ( SE ) Z Es tim at e ( SE ) Z Es tim at e ( SE ) Z Es tim at e ( SE ) t Inte rc ep t 1. 62 ( 0. 11 ) 14 .5 5*** 3. 28 ( 0. 08 ) 42 .6 3*** 1. 74 ( 0. 12 ) 15 .1 6*** 1. 77 ( 0. 12 ) 15 .1 2*** −1 .5 3 ( 0. 40 ) -3 .8 2*** 0.0 98 (0.0 07 ) 13 .7 1*** P 0. 45 (0.0 8) 5. 42 *** 0. 53 (0.0 7) 10 .5 1*** 0. 32 (0.0 9) 3. 38 *** 0. 22 ( 0. 11 ) 2.1 0* 1. 05 ( 0. 27 ) 3. 94 *** 0.0 13 (0.0 05 ) 2.7 7* * Ca 0. 73 (0.0 8) 8. 57 *** 0. 33 (0.0 7) 10 .6 0*** 0. 35 (0.0 9) 3. 75 *** 0.1 7 (0 .1 1) 1. 58 N S 1. 93 ( 0. 30 ) 6. 47 *** 0.0 22 (0.0 05 ) 4. 69 *** G ro w in g s ea so n 3 0. 74 (0.0 8) 8. 64 *** 0. 32 (0.0 9) 9. 99 *** 0. 59 (0.0 9) 6. 09 *** 0. 41 ( 0. 11 ) 3.7 8* * 1. 34 ( 0. 27 ) 4. 91 *** 0.0 23 (0.0 05 ) 5. 04 *** P × G ro w in g se aso n 3 – – −0. 11 (0.0 9) −1 .2 0 NS – – – – – – – – C a × G ro w in g se aso n 3 – – 0. 23 (0.0 9) 2. 59 ** – – – – – – – – P × C a – – – – – – – – – – – – P × C a × G ro w in g se aso n 3 – – – – – – – – – – – – M od el pa ra m et er s, Z -s co re s ( Po is so n, l og l in k G LM M ) a nd t-sc or es ( LM M ) p re se nt ed a re e st im at es f ro m t he s im pl ifi ed m od el f or m ul at io n r es po ns e ~ P × G ro w in g s ea so n + C a × G ro w in g s ea so n o r re sp on se ~ P +C a+ G ro w in g s ea so n. N o s ig ni fic an t P × C a × G ro w in g s ea so n e ff ec ts w er e f ou nd i n t he i ni tia l m od el f or m ul at io n. – , T er m r em ov ed f ro m m od el f or m ul at io n d ur in g m od el s im pl ifi ca tio n st ep s. N S, n o s ig ni fic an t e ff ec t. * , * *, * ** , S ig ni fic an ce p l ev el s o f 0 .0 5; 0 .0 1 a nd 0 .0 01 r es pe ct iv el y. aSp ec ie s r ic hn es s b as ed o n t ot al n um be r o f s pe ci es f ou nd i n p lo ts , t yp ic al f or t he n am ed p la nt c om m un ity a cc or di ng t o S ch am in ée e t a l. ( 19 96 ). bSp ec ie s r ic hn es s b as ed o n t ot al n um be r o f s pe ci es f ou nd i n p lo ts , n ot t yp ic al f or t he p la nt c om m un iti es c on si de re d. cSp ec ie s o cc ur re nc e-ba se d m ea n r el at iv e g ro w th r at e ( RG R) b as ed o n m ed ia n s pe ci es R G R v al ue s d er iv ed f ro m t he T RY d at ab as e ( K at tg e, V ile , S hi pl ey , G al le t, & G ar ni er , 2 00 6) , u si ng d at a c on tr ib ut io ns fr om F itt er a nd P ea t ( 19 94 ), F ry , P ow er a nd M an ni ng ( 20 14 ), K az ak ou e t a l. ( 20 06 ), S hi pl ey ( 19 89 ), ( 20 02 ), S hi pl ey a nd P ar en t ( 19 91 ) a nd V ile ( 20 05 ).
Applied Vegetation Science
5 | CONCLUSIONS
In combining the effects and interrelationships between P availability, soil acidity and plant characteristics, we were able to better explain the general observations that: (i) forb species are most negatively affected by acidification in poorly buffered habitats in the heath-land heath-landscape; (ii) some well-adapted graminoid species are able to increase competitive strength under increased N load; and (iii) sod cutting mainly has positive effects on germination and dominance of ericaceous species (i.e. species with low RGR), but much less on graminoids and forbs. We conclude that both increased P limitation and root stress due to high soil acidity contribute to poor recovery of species-rich dry heathland following sod-cutting management. P limitation has likely been further exacerbated in European lowland heathland ecosystems due to increased N (Mohren, Van Den Burg, & Burger, 1986) and acidic deposition (Asp, Bengtsson, & Jensén, 1991; Rout, Samantaray, & Das, 2001; Vogels et al., 2017), irrespec-tive of management.
We discourage the use of sod-cutting management as a large-scale solution to counterbalance increased soil N availability from chronically increased atmospheric N deposition, and advise to save sod cutting as a method of last resort, to be implemented in special cases only (e.g. when there is a risk of extinction of threatened species). Such small-scaled implementation of sod cutting should be accompanied by measures aimed at restoring the natural gradi-ents in soil buffer capacity (i.e. liming) and at alleviating increased P limitation (phosphate addition) as these represent important barriers to the restoration of characteristic plant communities. These accompanying actions render this method an increasingly complicated and cost-ineffective measure. Large-scaled manage-ment options should therefore aim at reducing the concentration of inorganic forms of N in the soil while keeping the soil profile intact. Sheep grazing (Fottner et al., 2007), preferably combined by prescribed burning (Niemeyer, Niemeyer, Mohamed, Fottner, & Härdtle, 2005) and regular mowing (Barker, Power, Bell, & Orme, 2004) have been proven successful in reducing nitrogen avail-ability and in promoting Calluna dominance in nitrogen-stressed lowland heathlands. Under conditions of N deposition well above critical loads, however, these have to be repeated at a high fre-quency (every five years) in order to prevent buildup of N (Fottner et al., 2007; Härdtle et al., 2006), and as a result have also been found to shift the system towards P limitation due to excessive removal of P from the aboveground biomass (Härdtle et al., 2009). Therefore, we strongly advocate renewed priority on further re-ducing atmospheric N deposition below critical levels, since evi-dence is mounting that restoring N-poor soil conditions without inadvertently affecting the nutrient balance of the ecosystem is highly complicated.
ACKNOWLEDGEMENTS
We declare no conflict of interest. We thank Wanda-Floor Zwart, Jan Kuper, Rein de Waal and Evi Verbaarschot for assistance with field work, and the National Park De Hoge Veluwe for providing
access to the park and allowing us to perform experimental research. The study has been supported by the TRY initiative on plant traits (http://www.try-db.org). The TRY initiative and database is hosted, developed and maintained by J. Kattge and G. Bönisch (Max Planck Institute for Biogeochemistry, Jena, Germany). TRY is currently sup-ported by DIVERSITAS/Future Earth and the German Centre for Integrative Biodiversity Research (iDiv) Halle–Jena-–Leipzig.
AUTHOR CONTRIBUTIONS
JJV, MJW, RB and HS conceived the ideas and designed methodol-ogy; JJV, MJW and RJB collected the data; JJV and MJW analysed the data and drafted the manuscript. All authors contributed to the drafts and gave final approval for publication.
DATA AVAIL ABILIT Y STATEMENT
Data files used in this study are stored in the DANS EASY data re-pository, accessible via http://doi.org/10.17026/ dans-xhf-jz9t.
ORCID
Joost J. Vogels https://orcid.org/0000-0003-4599-4320
Maaike J. Weijters https://orcid.org/0000-0002-7124-9861
Leon P. M. Lamers https://orcid.org/0000-0003-3769-2154
Wilco C. E. P. Verberk https://orcid.org/0000-0002-0691-583X
Henk Siepel https://orcid.org/0000-0003-4503-4485 REFERENCES
Aerts, R. (1996). Nutrient resorption from senescing leaves of perennials: Are there general patterns? Journal of Ecology, 84, 597–608. https :// doi.org/10.2307/2261481
Aerts, R., & Heil, G. W. (1993). Heathlands: Patterns and processes in a
changing environment. Dordrecht, The Netherlands: Kluwer Academic
Publishers.
Asp, H., Bengtsson, B., & Jensén, P. (1991). Influence of alumin-ium on phosphorus and calcalumin-ium localization in roots of beech (Fagus sylvatica). Physiologia Plantarum, 83, 41–46. https ://doi. org/10.1111/j.1399-3054.1991.tb012 79.x
Barker, C. G., Power, S. A., Bell, J. N. B., & Orme, C. D. L. (2004). Effects of habitat management on heathland response to atmospheric ni-trogen deposition. Biological Conservation, 120, 41–52. https ://doi. org/10.1016/j.biocon.2004.01.024
Barkman, J. J., Doing, H., & Segal, S. (1964). Kritische bemerkungen und vorschläge zur quantitativen vegetationsanalyse. Acta Botanica
Neerlandica, 13, 394–419. https ://doi.org/10.1111/j.1438-8677.1964.
tb001 64.x
Bates, D., Mächler, M., Bolker, B., & Walker, S. (2015). lme4: Fitting Linear Mixed-Effects Models Using Eigen and S4. Journal of
Statistical Software, 67(1), 1–48. https ://doi.org/10.18637/ jss.
v067.i01
Blume, H. P., Brümmer, G. W., Fleige, H., Horn, R., Kandeler, E., Kögel-Knabner, I., … Wilke, B. M. (2016). Scheffer/Schachtschabel Soil
Science, 1st ed. Berlin, Heidelberg: Springer-Verlag.
Bobbink, R., & Heil, G. W. (1993). Atmospheric deposition of sulphur and nitrogen in heathland ecosystems. In R. Aerts, & G. W. Heil (Eds.),
Heathlands: Patterns and processes in a changing environment (pp.
25–50). Dordrecht, The Netherlands: Kluwer Academic Publishers. Bobbink, R., & Hettelingh, J. P. (2011). Review and revision of empirical
critical loads and dose-response relationships. Coordination Centre for
Effects, National Institute for Public Health and the Environment (RIVM). www.rivm.nl/cce
Bobbink, R., Hornung, M., & Roelofs, J. G. M. (1998). The effects of air-borne nitrogen pollutants on species diversity in natural and semi-natural European vegetation. Journal of Ecology, 86, 717–738. https ://doi.org/10.1046/j.1365-2745.1998.86507 17.x
Bradley, R., Burt, A. J., & Read, D. J. (1982). The biology of mycorrhiza in the Ericaceae. 8. The role of mycorrhizal infection in heavy-metal resistance. New Phytologist, 91, 197–209.
Britton, A. J., Marrs, R. H., Carey, P. D., & Pakeman, R. J. (2000). Comparison of techniques to increase Calluna vulgaris cover on heathland invaded by grasses in Breckland, south east England.
Biological Conservation, 95, 227–232. https ://doi.org/10.1016/
S0006-3207(00)00047-1
Bruggink, M. (1993). Seed bank, germination, and establishment of erica-ceous and gramineous species in heathlands. In R. Aerts, & G. W. Heil (Eds.), Heathlands: Patterns and processes in a changing environment (pp. 153–180). Dordrecht, The Netherlands: Kluwer Academic Press. De Graaf, M. C. C., Bobbink, R., Roelofs, J. G. M., & Verbeek, P. J. M.
(1998a). Differential effects of ammonium and nitrate on three heathland species. Plant Ecology, 135, 185–196.
De Graaf, M. C. C., Bobbink, R., Smits, N. A. C., Van Diggelen, R., & Roelofs, J. G. M. (2009). Biodiversity, vegetation gradients and key biogeochemical processes in the heathland landscape.
Biological Conservation, 142, 2191–2201. https ://doi.org/10.1016/j.
biocon.2009.04.020
De Graaf, M. C. C., Bobbink, R., Verbeek, P. J. M., & Roelofs, J. G. M. (1997). Aluminium toxicity and tolerance in three heathland species.
Water Air and Soil Pollution, 98, 229–239. https ://doi.org/10.1007/
BF020 47036
De Graaf, M. C. C., Verbeek, P. J. M., Bobbink, R., & Roelofs, J. G. M. (1998b). Restoration of species-rich dry heaths: The importance of appropriate soil conditions. Acta Botanica Neerlandica, 47, 89–111. Diemont, W. H. (1996). Survival of Dutch heathlands. "IBN Scientific
Contributions 1". Wageningen, The Netherlands: DLO Institute for
Forestry and Nature Research (IBN-DLO).
Dorland, E., Bobbink, R., Messelink, J. H., & Verhoeven, J. T. A. (2003). Soil ammonium accumulation after sod cutting hampers the resto-ration of degraded wet heathlands. Journal of Applied Ecology, 40, 804–814. https ://doi.org/10.1046/j.1365-2664.2003.00845.x Dorland, E., Stevens, C. J., Gaudnik, C., Corcket, E., Rotthier, S.,
Wotherspoon, K., … Bobbink, R. (2013). Differential effects of oxi-dised and reduced nitrogen on vegetation and soil chemistry of spe-cies-rich acidic grasslands. Water Air and Soil Pollution, 224, 13. Dorland, E., van den Berg, L. J. L., van de Berg, A. J., Vermeer, M. L.,
Roelofs, J. G. M., & Bobbink, R. (2004). The effects of sod cutting and additional liming on potential net nitrification in heathland soils. Plant
and Soil, 265, 267–277. https ://doi.org/10.1007/s11104-005-0363-3
Elser, J. J. (2011). A World awash with nitrogen. Science, 334, 1504–1505. https ://doi.org/10.1126/scien ce.1215567
Falk, K., Friedrich, U., von Oheimb, G., Mischke, K., Merkle, K., Meyer, H., & Härdtle, W. (2010). Molinia caerulea responses to N and P fertilisa-tion in a dry heathland ecosystem (NW-Germany). Plant Ecology, 209, 47–56. https ://doi.org/10.1007/s11258-010-9720-2
Fitter, A. H., & Peat, H. J. (1994). The ecological flora database. Journal of
Ecology, 82, 415–425. https ://doi.org/10.2307/2261309
Fottner, S., Härdtle, W., Niemeyer, M., Niemeyer, T., von Oheimb, G., Meyer, H., & Mockenhaupt, M. (2007). Impact of sheep grazing on nutrient budgets of dry heathlands. Applied Vegetation Science, 10, 391–398. https ://doi.org/10.1111/j.1654-109X.2007.tb004 38.x Friedrich, U., von Oheimb, G., Dziedek, C., Kriebitzsch, W. U., Selbmann,
K., & Härdtle, W. (2011). Mechanisms of purple moor-grass (Molinia
caerulea) encroachment in dry heathland ecosystems with chronic
nitrogen inputs. Environmental Pollution, 159, 3553–3559. https ://doi. org/10.1016/j.envpol.2011.08.010
Fry, E. L., Power, S. A., & Manning, P. (2014). Trait-based classification and manipulation of plant functional groups for biodiversity-ecosystem
function experiments. Journal of Vegetation Science, 25, 248–261. https ://doi.org/10.1111/jvs.12068
Gerendas, J., Zhu, Z. J., Bendixen, R., Ratcliffe, R. G., & Sattelmacher, B. (1997). Physiological and biochemical processes related to am-monium toxicity in higher plants. Zeitschrift Fur Pflanzenernahrung
Und Bodenkunde, 160, 239–251. https ://doi.org/10.1002/jpln.19971
600218
Gessa, C. E., Mimmo, T., Deiana, S., & Marzadori, C. (2005). Effect of al-uminium and pH on the mobility of phosphate through a soil-root in-terface model. Plant and Soil, 272, 301–311. https ://doi.org/10.1007/ s11104-004-5693-z
Grasshoff, K., & Johannsen, H. (1972). A new sensitive and direct method for the automatic determination of ammonia in sea Water. ICES
Journal of Marine Science, 34, 516–521. https ://doi.org/10.1093/icesj
ms/34.3.516
Härdtle, W., Niemeyer, M., Niemeyer, T., Assmann, T., & Fottner, S. (2006). Can management compensate for atmospheric nutrient deposition in heathland ecosystems? Journal of Applied Ecology, 43, 759–769. https ://doi.org/10.1111/j.1365-2664.2006.01195.x
Härdtle, W., von Oheimb, G., Gerke, A.-K., Niemeyer, M., Niemeyer, T., Assmann, T., … Meyer, H. (2009). Shifts in N and P budgets of heathland ecosystems: Effects of management and atmo-spheric inputs. Ecosystems, 12, 298–310. https ://doi.org/10.1007/ s10021-008-9223-3
Haynes, R. (1982). Effects of liming on phosphate availability in acid soils.
Plant and Soil, 68, 289–308. https ://doi.org/10.1007/BF021 97935
Heil, G. W., & Bobbink, R. (1993). Impact of atmospheric nitrogen depo-sition on dry heathlands - A stochastic model simulating competition between Calluna vulgaris and two grass species. In R. Aerts, & G. W. Heil (Eds.), Heathlands: Patterns and processes in a changing
environ-ment (pp. 181–200). Dordrecht, The Netherlands: Kluwer Academic
Press.
Heil, G. W., & Bruggink, M. (1987). Competition for nutrients between
Calluna vulgaris (L.) Hull and Molinia caerulea (L.) Moench. Oecologia, 73, 105–107. https ://doi.org/10.1007/BF003 76984
Heil, G. W., & Diemont, W. H. (1983). Raised nutrient levels change heath-land into grassheath-land. Vegetatio, 53, 113–120. https ://doi.org/10.1007/ BF000 43031
Houdijk, A. L. F. M., Verbeek, P. J. M., Vandijk, H. F. G., & Roelofs, J. G. M. (1993). Distribution and decline of endangered herbaceous heath-land species in relation to the chemical-composition of the soil. Plant
and Soil, 148, 137–143. https ://doi.org/10.1007/BF021 85393
Hunt, R., & Cornelissen, J. H. C. (1997). Components of relative growth rate and their interrelations in 59 temperate plant species. New Phytologist,
135, 395–417. https ://doi.org/10.1046/j.1469-8137.1997.00671.x
Jansen, A. J. M., de Graaf, M. C. C., & Roelofs, J. G. M. (1996). The res-toration of species-rich heathland communities in the Netherlands.
Vegetatio, 126, 73–88.
Kamphake, L. J., Hannah, S. A., & Cohen, J. M. (1967). Automated analysis for nitrate by hydrazine reduction. Water Research, 1, 205–216. https ://doi.org/10.1016/0043-1354(67)90011-5
Kattge, J., Díaz, S., Lavorel, S., Prentice, I. C., Leadley, P., Bönisch, G., … Wirth, C. (2011). TRY – a global database of plant traits. Global Change Biology, 17, 2905–2935. https ://doi. org/10.1111/j.1365-2486.2011.02451.x
Kazakou, E., Vile, D., Shipley, B., Gallet, C., & Garnier, E. (2006). Co-variations in litter decomposition, leaf traits and plant growth in spe-cies from a Mediterranean old-field succession. Functional Ecology,
20, 21–30. https ://doi.org/10.1111/j.1365-2435.2006.01080.x
Kirkham, F. W. (2001). Nitrogen uptake and nutrient limitation in six hill moorland species in relation to atmospheric nitrogen deposition in England and Wales. Journal of Ecology, 89, 1041–1053. https ://doi. org/10.1111/j.1365-2745.2001.00626.x
Kooijman, A. M., Dopheide, J. C. R., Sevink, J., Takken, I., & Verstraten, J. M. (1998). Nutrient limitations and their implications on the effects
Applied Vegetation Science
of atmospheric deposition in coastal dunes; lime-poor and lime-richsites in the Netherlands. Journal of Ecology, 86, 511–526. https ://doi. org/10.1046/j.1365-2745.1998.00273.x
Likens, G. E., Bormann, F. H., & Johnson, N. M. (1972). Acid rain.
Environment: Science and Policy for Sustainable Development, 14,
33–40.
Mohren, G. M. J., Van Den Burg, J., & Burger, F. W. (1986). Phosphorus deficiency induced by nitrogen input in Douglas fir in the Netherlands. Plant and Soil, 95, 191–200. https ://doi.org/10.1007/ BF023 75071
Nielsen, K. E., Hansen, B., Ladekarl, U. L., & Nørnberg, P. (2000). Effects of N-deposition on ion trapping by B-horizons of Danish heathlands.
Plant and Soil, 223, 267–278.
Niemeyer, T., Niemeyer, M., Mohamed, A., Fottner, S., & Härdtle, W. (2005). Impact of prescribed burning on the nutrient balance of heathlands with particular reference to nitrogen and phosphorus.
Applied Vegetation Science, 8, 183–192. https ://doi.org/10.1111/
j.1654-109X.2005.tb006 44.x
Olsen, S. R., Cole, C. V., Watanabe, F. S., & Dean, L. A. (1954). Estimation of available phosphorus in soils by extraction with sodium bicarbon-ate (No. 939). US Dept. of Agriculture.
Pearson, V., & Read, D. J. (1973). Biology of mycorrhiza in Ericaceae. 2. Transport of carbon and phosphorus by endophyte and mycorrhiza.
New Phytologist, 72, 1325–1331.
Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D., & R Core Team (2017). nlme: Linear and Nonlinear Mixed Effects Models. R package version 3, 1–131.
Power, S. A., Ashmore, M. R., Cousins, D. A., & Ainsworth, N. (1995). Long term effects of enhanced nitrogen deposition on a lowland dry heath in southern Britain. Water Air and Soil Pollution, 85, 1701–1706. https ://doi.org/10.1007/BF004 77225
R Core Team. (2017). R: A language and environment for statistical
comput-ing. Vienna, Austria: R Foundation for Statistical Computcomput-ing.
Rengel, Z. (1992). Role of calcium in aluminum toxicity. New Phytologist,
121, 499–513.
Roelofs, J. G. M. (1986). The effect of airborne sulfur and nitrogen depo-sition on aquatic and terrestrial heathland vegetation. Experientia, 42, 372–377.
Roem, W. J., & Berendse, F. (2000). Soil acidity and nutrient supply ratio as possible factors determining changes in plant species diversity in grassland and heathland communities. Biological Conservation, 92, 151–161. https ://doi.org/10.1016/S0006-3207(99)00049-X Roem, W. J., Klees, H., & Berendse, F. (2002). Effects of nutrient
addi-tion and acidificaaddi-tion on plant species diversity and seed germina-tion in heathland. Journal of Applied Ecology, 39, 937–948. https ://doi. org/10.1046/j.1365-2664.2002.00768.x
Rout, G., Samantaray, S., & Das, P. (2001). Aluminium toxicity in plants: A review. Agronomie, 21, 3–21. https ://doi.org/10.1051/agro:2001105
Ryan, P. R., Kinraide, T. B., & Kochian, L. V. (1994). Al3+-Ca2+ interactions
in aluminum rhizotoxicity. 1. inhibition of root-growth is not caused by reduction of calcium-uptake. Planta, 192, 98–103.
Schaminée, J. H. J., Stortelder, A. H. F., & Weeda, E. J. (1996). De Vegetatie
van Nederland. Deel 3: Plantengemeenschappen van graslanden, zomen en droge heiden. Uppsala, Sweden: Opulus.
Schjørring, J. K. (1986). Nitrate and ammonium absorption by plants growing at a sufficient or insufficient level of phosphorus in nutri-ent solutions. Plant and Soil, 91, 313–318. https ://doi.org/10.1007/ BF021 98114
Shaw, G., & Read, D. J. (1989). The biology of mycorrhiza in the Ericaceae. 14. Effects of iron and aluminum on the activity of acid-phosphatase in the ericoid endophyte Hymenoscyphus ericae (Read) Korf and Kernan. New Phytologist, 113, 529–533.
Shipley, B. (1989). The use of above-ground maximum relative growth-rate as an accurate predictor of whole-plant maximum
relative growth-rate. Functional Ecology, 3, 771–775. https ://doi. org/10.2307/2389510
Shipley, B. (2002). Trade-offs between net assimilation rate and spe-cific leaf area in determining relative growth rate: Relationship with daily irradiance. Functional Ecology, 16, 682–689. https ://doi. org/10.1046/j.1365-2435.2002.00672.x
Shipley, B., & Parent, M. (1991). Germination responses of 64 wetland species in relation to seed size, minimum time to reproduction and seedling relative growth-rate. Functional Ecology, 5, 111–118. https :// doi.org/10.2307/2389561
Siepel, H., Vogels, J., Bobbink, R., Bijlsma, R.-J., Jongejans, E., de Waal, R., & Weijters, M. (2018). Continuous and cumulative acidification and N deposition induce P limitation of the micro-arthropod soil fauna of mineral-poor dry heathlands. Soil Biology and Biochemistry, 119, 128–134. https ://doi.org/10.1016/j.soilb io.2018.01.025
Southon, G. E., Field, C., Caporn, S. J. M., Britton, A. J., & Power, S. A. (2013). Nitrogen deposition reduces plant diversity and alters eco-system functioning: Field-scale evidence from a nationwide sur-vey of UK Heathlands. PLoS ONE, 8. https ://doi.org/10.1371/journ al.pone.0059031
Sterner, R. W., & Elser, J. J. (2002). Ecological stoichiometry: The biology
of elements from molecules to the biosphere. Princeton, NJ: Princeton
University Press.
Stevens, C. J., Duprè, C., Dorland, E., Gaudnik, C., Gowing, D. J. G., Bleeker, A., … Dise, N. B. (2010). Nitrogen deposition threatens spe-cies richness of grasslands across Europe. Environmental Pollution,
158, 2940–2945. https ://doi.org/10.1016/j.envpol.2010.06.006
Stevens, C. J., Manning, P., van den Berg, L. J. L., de Graaf, M. C. C., Wamelink, G. W. W., Boxman, A. W., … Dorland, E. (2011). Ecosystem responses to reduced and oxidised nitrogen inputs in European ter-restrial habitats. Environmental Pollution, 159, 665–676. https ://doi. org/10.1016/j.envpol.2010.12.008
Stribley, D. P., & Read, D. J. (1980). The biology of mycorrhiza in the Ericaceae. 7. The relationship between mycorrhizal infection and the capacity to utilize simple and complex organic nitrogen-sources. New
Phytologist, 86, 365–371.
van den Berg, L. J. L., Dorland, E., Vergeer, P., Hart, M. A. C., Bobbink, R., & Roelofs, J. G. M. (2005). Decline of acid-sensitive plant spe-cies in heathland can be attributed to ammonium toxicity in com-bination with low pH. New Phytologist, 166, 551–564. https ://doi. org/10.1111/j.1469-8137.2005.01338.x
van den Berg, L. J. L., Peters, C. J. H., Ashmore, M. R., & Roelofs, J. G. M. (2008). Reduced nitrogen has a greater effect than oxidised nitrogen on dry heathland vegetation. Environmental Pollution, 154, 359–369. https ://doi.org/10.1016/j.envpol.2007.11.027
van den Berg, L. J. L., Vergeer, P., & Roelofs, J. G. M. (2003). Heathland restoration in The Netherlands: Effects of turf cutting depth on ger-mination of Arnica montana. Applied Vegetation Science, 6, 117–124. https ://doi.org/10.1111/j.1654-109X.2003.tb005 71.x
Velders, G. J. M., Aben, J. M. M., Geilenkirchen, G. P., den Hollander, H. A., van der Swaluw, E., de Vries, W. J., & Van Zanten, M. C. (2015). Grootschalige concentratie- en depositiekaarten Nederland -
Rapportage 2015. Bilthoven, The Netherlands: Rijksinstituut voor
Volksgezondheid en Milieu (RIVM).
Vile, D. (2005). Significations fonctionnelle et ecologique des traits des
es-peces vegetales: exemple dans une succession post-cultural mediterra-neenne et generalisations. PhD thesis.
Vogels, J. J., Verberk, W. C. E. P., Lamers, L. P. M., & Siepel, H. (2017). Can changes in soil biochemistry and plant stoichiometry explain loss of animal diversity of heathlands? Biological Conservation, 212, 432–447. https ://doi.org/10.1016/j.biocon.2016.08.039
Webb, N. R. (1998). The traditional management of European heath-lands. Journal of Applied Ecology, 35, 987–990. https ://doi. org/10.1111/j.1365-2664.1998.tb000 20.x
Wright, I. J., & Westoby, M. (2003). Nutrient concentration, resorption and lifespan: Leaf traits of Australian sclerophyll species. Functional Ecology,
17, 10–19. https ://doi.org/10.1046/j.1365-2435.2003.00694.x
SUPPORTING INFORMATION
Additional supporting information may be found online in the Supporting Information section.
Appendix S1. Associated community assignment and relative growth
rate (RGR) values of recorded species in the experimental plots
Appendix S2. Overview of mean soil chemistry values per treatment
per year
How to cite this article: Vogels JJ, Weijters MJ, Bobbink R,
et al. Barriers to restoration: Soil acidity and phosphorus limitation constrain recovery of heathland plant communities after sod cutting. Appl Veg Sci. 2020;23:94–106. https ://doi. org/10.1111/avsc.12471
