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Resilience in Coastal Dune Grasslands: Ph and Soil Organic Matter Effects

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Resilience in Coastal Dune Grasslands: Ph and Soil Organic Matter Effects UvA-DARE (Digital Academic Repository) Resilience in coastal dune grasslands: pH and soil organic mattereffects on P nutriti on, plant strategies, and soil communities Kooijman, A.M.; Morriën, E.; Jagers op Akkerhuis, G.; Missong, A.; Bol, R.; Klumpp, E.; van Hall, R.; van Til, M.; Kalbitz, K.; Bloem, J. DOI 10.1002/ecs2.3112 Publication date 2020 Document Version Final published version Published in Ecosphere License CC BY Link to publication Citation for published version (APA): Kooijman, A. M., Morriën, E., Jagers op Akkerhuis, G., Missong, A., Bol, R., Klumpp, E., van Hall, R., van Til, M., Kalbitz, K., & Bloem, J. (2020). Resilience in coastal dune grasslands: pH and soil organic mattereffects on P nutriti on, plant strategies, and soil communities. Ecosphere, 11(5), [e03112]. https://doi.org/10.1002/ecs2.3112 General rights It is not permitted to download or to forward/distribute the text or part of it without the consent of the author(s) and/or copyright holder(s), other than for strictly personal, individual use, unless the work is under an open content license (like Creative Commons). Disclaimer/Complaints regulations If you believe that digital publication of certain material infringes any of your rights or (privacy) interests, please let the Library know, stating your reasons. In case of a legitimate complaint, the Library will make the material inaccessible and/or remove it from the website. Please Ask the Library: https://uba.uva.nl/en/contact, or a letter to: Library of the University of Amsterdam, Secretariat, Singel 425, 1012 WP Amsterdam, The Netherlands. You will be contacted as soon as possible. UvA-DARE is a service provided by the library of the University of Amsterdam (https://dare.uva.nl) Download date:05 Oct 2021 Resilience in coastal dune grasslands: pH and soil organic matter effects on P nutrition, plant strategies, and soil communities 1, € 1,2 3 4 1,3 ANNEMIEKE KOOIJMAN, ELLY MORRIEN, GERARD JAGERS OP AKKERHUIS, ANNA MISSONG, ROLAND BOL, 3 1 5 1,6 3 ERWIN KLUMPP, RUTGER VAN HALL, MARK VAN TIL, KARSTEN KALBITZ, AND JAAP BLOEM 1Department of Ecosystem and Landscape Dynamics, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Science Park, P.O. Box 94062, Amsterdam 1090 GB The Netherlands 2Terrestrial Ecology, NIOO-KNAW, P.O. Box 50, Wageningen 6700 AB The Netherlands 3Wageningen University and Research Centre, P.O. Box 47, Wageningen 6700 AA The Netherlands 4Institute of Bio- and Geosciences (IBG-3) Agrosphere, Forschungszentrum Julich,€ Wilhelm-Johnen-Straße, Julich 52425 Germany 5Waternet, P.O. Box 94370, Amsterdam 1090 GJ The Netherlands 6Soil Resources and Land Use, Technische Universit€at Dresden, Pienner Straße 19, Tharandt 01737 Germany Citation: Kooijman, A., E. Morri€en, G. Jagers op Akkerhuis, A. Missong, R. Bol, E. Klumpp, R. van Hall, M. van Til, K. Kalbitz and J. Bloem. 2020. Resilience in coastal dune grasslands: pH and soil organic matter effects on P nutrition, plant strategies, and soil communities. Ecosphere 11(5):e03112. 10.1002/ecs2.3112 Abstract. Soil organic matter (SOM) and pH are key ecosystem drivers, influencing resilience to environ- mental change. We tested the separate effects of pH and SOM on nutrient availability, plant strategies, and soil community composition in calcareous and acidic Grey dunes (H2130) with low, intermediate, and/or high SOM, which differ in sensitivity to high atmospheric N deposition. Soil organic matter was mainly important for biomass parameters of plants, microbes, and soil animals, and for microarthropod diversity and network complexity. However, differences in pH led to fundamental differences in P availability and plant strategies, which overruled the normal soil community patterns, and influenced resilience to N depo- sition. In calcareous dunes with low grass-encroachment, P availability was low despite high amounts of inorganic P, due to low solubility of calcium phosphates and strong P sorption to Fe oxides at high pH. Cal- careous dunes were dominated by low-competitive arbuscular mycorrhizal (AM) plants, which profit from mycorrhiza especially at low P. In acidic dunes with high grass-encroachment, P availability increased as calcium phosphates dissolved and P sorption weakened with the shift from Fe oxides to Fe-OM complexes. Weakly sorbed and colloidal P increased, and at least part of the sorbed P was organic. Acidic dunes were dominated by nonmycorrhizal (NM) plants, which increase P uptake through exudation of carboxylates and phosphatase enzymes, which release weakly sorbed P, and disintegrate labile organic P. The shifts in P availability and plant strategies also changed the soil community. Contrary to expectations, the bacterial pathway was more important in acidic than in calcareous dunes, possibly due to exudation of carboxylates and phosphatases by NM plants, which serve as bacterial food resource. Also, the fungal AM pathway was enhanced in calcareous dunes, and fungal feeders more abundant, due to the presence of AM fungi. The changes in soil communities in turn reduced expected differences in N cycling between calcareous and acidic dunes. Our results show that SOM and pH are important, but separate ecosystem drivers in Grey dunes. Differences in resilience to N deposition are mainly due to pH effects on P availability and plant strategies, which in turn overruled soil community patterns. Key words: arbuscular mycorrhizal (AM) plants; atmospheric N deposition; bacteria; fungi; Grey dunes H2130; iron; nonmycorrhizal (NM) plants; soil community network. Received 30 December 2019; revised 17 January 2020; accepted 22 January 2020; final version received 11 March 2020. Corresponding Editor: Uffe N. Nielsen. Copyright: © 2020 The Authors. This 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. E-mail: [email protected] ❖ www.esajournals.org 1 May 2020 ❖ Volume 11(5) ❖ Article e03112 KOOIJMAN ET AL. INTRODUCTION and biological activity than acidic, fungi-domi- nated soils (Aerts and Chapin 2000, Schimel and Soil organic matter (SOM) and pH are major Bennett 2004, De Vries et al. 2011, Kooijman et al. ecosystem drivers that influence soil communi- 2016). However, because N immobilization is ties, plant-available nutrients, and vegetation in higher for bacteria than for fungi, net N mineral- many ways (Ellenberg et al. 1974, Swift et al. ization, which is a proxy for N availability to the 1979). In coastal dune grasslands, which belong vegetation, may actually show the opposite pat- to the priority habitat Grey dunes (H2130) of the tern (Zottle€ 1960, Davy and Taylor 1974, Verho- EU habitat directive (European Union 1992), pH even et al. 1990, Kooijman et al. 2008, 2016). and SOM may be especially important. In many Bacteria have higher N demand and lower C:N ecosystems, pH and SOM change together dur- ratios than fungi (Moore et al. 2005), due to their ing succession, but in Grey dune areas, these fac- faster life cycles and use of amino acids for tors may be clearly separated. Older dunes with osmoregulation rather than carbohydrates (Mea- acidic topsoils alternate with younger calcareous sures 1975, Kuehn et al. 1998). This may imply dunes, both consisting of mosaics of low and that availability of N to the vegetation is lower in high SOM, due to differences in eolian activity calcareous than in acidic Grey dunes, which may (Aggenbach et al. 2017). Also, in the dunes all explain why grass-encroachment is higher in the soils are sandy, which precludes differences in P latter. sorption (Shen et al. 2011) and microbial commu- Soil pH and SOM may also influence resilience nity composition (Hassink 1994) due to texture. to high N deposition through their effects on P In industrialized countries, pH and SOM are also nutrition (Kooijman et al. 1998, 2017). Phospho- important to Grey dunes because different dune rus is an essential nutrient for plant growth, zones respond in a different way to high atmo- which may reduce effects of high N deposition spheric N deposition (Bobbink et al. 2010, Kooij- when this is a limiting factor. However, different man et al. 2017). Grass-encroachment, that is, the forms of P, such as inorganic P in primary and dominance of tall graminoid species and associ- secondary minerals, sorbed P, organic P, and col- ated loss of plant diversity, is generally higher in loidal P systematically change during succession acidic than in calcareous Grey dunes, and more and soil development (Walker and Syers 1976, pronounced on soils with high than with low Hinsinger 2001, Shen et al. 2011). This means that SOM (Fig. 1; Remke et al. 2009a, b, Kooijman P availability to the vegetation may change with et al. 2017). pH and/or SOM. In calcareous dunes, primary Soil organic matter and pH may influence resi- and secondary calcium phosphates may be abun- lience to high N deposition in Grey dunes dant (Walker and Syers 1976, Kooijman et al. through differences in soil community composi- 1998), but P availability to the vegetation may tion, which in turn affect microbial respiration still be low due to their low solubility at high pH and N cycling (Swift et al. 1979). Soil organic (Lindsay and Moreno 1966). During bedrock matter is a food resource for bacteria and fungi, weathering and pedogenetic development, P is which are in turn eaten by protists and released from primary and secondary minerals microarthropods, and soil communities usually (Walker and Syers 1976). In calcareous dunes, increase during succession in microbial biomass, this process is especially important around pH microarthropod diversity, and network interac- 6.5, when calcium phosphates dissolve together tion strength (Kaufmann 2001, Frouz et al. 2008, with calcium carbonates (Lindsay and Moreno Morri€en et al. 2017). Soil pH is probably more 1966) and become available to the vegetation important in shaping microbial communities (Kooijman and Besse 2002, Kooijman et al.
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