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Factors at multiple scales influence the composition of terricolous lichen communities in temperate semi-arid sandy grasslands

Published online by Cambridge University Press:  08 December 2021

Katalin Veres*
Affiliation:
Institute of Ecology and Botany, Centre for Ecological Research, H-2163 Vácrátót, Alkotmány u. 2–4, Hungary
Zsolt Csintalan
Affiliation:
Department of Plant Physiology and Ecology, Institute of Biological Sciences, Hungarian University of Agriculture and Life Sciences, H-2100 Gödöllő, Páter K. u. 1, Hungary
Bence Kovács
Affiliation:
Institute of Ecology and Botany, Centre for Ecological Research, H-2163 Vácrátót, Alkotmány u. 2–4, Hungary
Edit Farkas
Affiliation:
Institute of Ecology and Botany, Centre for Ecological Research, H-2163 Vácrátót, Alkotmány u. 2–4, Hungary
*
Author for correspondence: Katalin Veres. E-mail: [email protected]

Abstract

Inland dune ecosystems are rich in terricolous lichen species. However, these communities are sensitive to human activities, both locally and globally. Since terricolous lichens have a dominant role in semi-arid sandy grasslands, it is important to explore the composition of their communities and the environmental factors affecting them. We studied the structure of the terricolous lichen assemblages of calcareous grassland in an inland duneland ecosystem by comparing the lichen communities of arid and humid dune sides on two sites with different disturbance histories. Microcoenological data were collected according to the Braun-Blanquet method. Environmental variables include the cover of bare soil, moss, litter, herb cover and height of herbs. We investigated the relationship of these variables and the presence and absence data of terricolous lichen species to sites and dune side. We found that the site had a significant effect on species richness that might reflect the different types and severity of previous disturbance events at the studied sites. On a smaller, ‘dune’ scale, in general lower herb cover and height and a higher moss cover were characteristic of arid dune sides. Most of the frequent species were negatively affected by higher moss cover. Some lichen species were more abundant (e.g. Cladonia furcata) or found only (e.g. Xanthoparmelia subdiffluens, Gyalolechia fulgens) on arid dune sides, while others preferred (e.g. C. pyxidata) or occurred only on (e.g. Peltigera species, C. rei) humid sides. It was observed that the impact of the dune side on several variables differed between sites. The diverse microhabitat types, microclimate and landscape structure, results in species-rich and valuable terricolous lichen communities forming in inland dune ecosystems.

Type
Standard Paper
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press on behalf of the British Lichen Society

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References

Adamska, E (2010) Biota of lichens on the Zadroże Dune and its immediate surroundings. Ecological Questions 12, 5158.CrossRefGoogle Scholar
Adamska, E and Adamski, A (2014) Materials to the lichen biota of the hill in Folusz near Szubin (NW Poland). Ecological Questions 20, 3944.CrossRefGoogle Scholar
Anderson, MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecology 26, 3246.Google Scholar
Arup, U, Ekman, S, Lindblom, L and Mattsson, JE (1993) High performance thin layer chromatography (HPTLC), an improved technique for screening lichen substances. Lichenologist 25, 6171.CrossRefGoogle Scholar
Balogh, R, Farkas, E, Lőkös, L, Papp, B, Budai, J, Antal, K, Novák, T and Matus, G (2017) Mosses and lichens in dynamics of acidic sandy grasslands: specific response to grazing exclosure. Acta Biologica Plantarum Agriensis 5(1), 30.CrossRefGoogle Scholar
Bartholy, J, Pongrácz, R, Torma, Cs, Pieczka, I, Kardos, P and Hunyady, A (2009) Analysis of regional climate change modelling experiments for the Carpathian Basin. International Journal of Global Warming 1, 238252.CrossRefGoogle Scholar
Bates, D, Maechler, M, Bolker, B and Walker, S (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 148.CrossRefGoogle Scholar
Belnap, J and Eldridge, D (2001) Disturbance and recovery of biological soil crusts. In Belnap, J and Lange, O (eds), Biological Soil Crusts: Structure, Function, and Management. Berlin, Heidelberg: Springer-Verlag, pp. 363383.CrossRefGoogle Scholar
Belnap, J and Lange, OL (2003) Biological Soil Crusts: Structure, Function, and Management. Berlin, Heidelberg: Springer-Verlag.CrossRefGoogle Scholar
Biró, M and Molnár, Z (1998) A Duna-Tisza köze homokbuckásainak tájtípusai, azok kiterjedése, növényzete és tájtörténete a 18. századtól [Vegetation and land-use history in the sand dunes of the Duna-Tisza köze from the 18th century and the mapping of landscape types of the late 18th century] Történeti Földrajzi Füzetek 5, 134. (Hungarian article with an extended English summary pp. 30–34)Google Scholar
Biró, M, Szitár, K, Horváth, F, Bagi, I and Molnár, Z (2013) Detection of long-term landscape changes and trajectories in a Pannonian sand region: comparing land-cover and habitat-based approaches at two spatial scales. Community Ecology 14, 219230.CrossRefGoogle Scholar
Biró, M, Iványosi Szabó, A and Molnár, Z (2015) Táj és történelem-ez a mi kis hazánk: a Duna-Tisza köze tájtörténete. In Szabó A, Iványosi (ed.), A Kiskunsági Nemzeti Park Igazgatóság negyven éve. Kecskemét: Kiskunsági Nemzeti Park Igazgatóság, pp. 4158.Google Scholar
Blum, O (1973) Water relations. In Ahmajian, V and Hale, ME (eds), The Lichens. New York: Academic Press, pp. 381400.CrossRefGoogle Scholar
Boch, S, Prati, D, Schöning, I and Fischer, M (2016) Lichen species richness is highest in non-intensively used grasslands promoting suitable microhabitats and low vascular plant competition. Biodiversity and Conservation 25, 225238.CrossRefGoogle Scholar
Bolker, BM, Brooks, ME, Clark, CJ, Geange, SW, Poulsen, JR, Stevens, MHH and White, JSS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends in Ecology and Evolution 24, 127135.CrossRefGoogle ScholarPubMed
Borcard, D, Gillet, F and Legendre, P (2018) Numerical ecology with R. New York: Springer.CrossRefGoogle Scholar
Borhidi, A, Kevey, B and Lendvai, G (2012) Plant Communities of Hungary. Budapest: Akadémiai Kiadó.Google Scholar
Braun-Blanquet, J (1964) Pflanzensoziologie, Grundzüge der Vegetationskunde, 3rd Edn. Vienna, New York: Springer.Google Scholar
Brooks, ME, Kristensen, K, van Benthem, KJ, Magnusson, A, Berg, CW, Nielsen, A, Skaug, HJ, Maechler, M and Bolker, BM (2017) glmmTMB: balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. The R Journal 9, 378400.CrossRefGoogle Scholar
Büdel, B (2001) Biological soil crusts in European temperate and Mediterranean regions. In Belnap, J and Lange, O (eds), Biological Soil Crusts: Structure, Function, and Management. Berlin, Heidelberg: Springer-Verlag, pp. 7586.CrossRefGoogle Scholar
Büdel, B and Scheidegger, C (2008) Thallus morphology and anatomy. In Nash, TH III (ed.), Lichen Biology, 2nd Edn. Cambridge: Cambridge University Press, pp. 40–68.Google Scholar
Büdel, B, Colesie, C, Green, TGA, Grube, M, Lázaro Suau, R, Loewen-Schneider, K, Maier, S, Peer, T, Pintado, A, Raggio, J, et al. (2014) Improved appreciation of the functioning and importance of biological soil crusts in Europe: the Soil Crust International Project (SCIN). Biodiversity and Conservation 23, 16391658.CrossRefGoogle Scholar
CABI (2020) Index Fungorum. [WWW resource] URL http://www.indexfungorum.org. [Accessed 15 January 2020].Google Scholar
Colesie, C, Scheu, S, Green, TGA, Weber, B and Büdel, B (2012) The advantage of growing on moss: facilitative effects on photosynthetic performance and growth in the cyanobacterial lichen Peltigera rufescens. Oecologia 169, 599607.CrossRefGoogle ScholarPubMed
Concostrina-Zubiri, L, Pescador, DS, Martínez, I and Escudero, A (2014) Climate and small scale factors determine functional diversity shifts of biological soil crusts in Iberian drylands. Biodiversity and Conservation 23, 17571770.CrossRefGoogle Scholar
Condon, LA and Pyke, DA (2018) Resiliency of biological soil crusts and vascular plants varies among morphogroups with disturbance intensity. Plant and Soil 433, 271287.CrossRefGoogle Scholar
Dunn, PK (2017) tweedie: evaluation of tweedie exponential family models. R package version 2.3.3. [WWW resource] URL https://CRAN.R-project.org/package=tweedie.Google Scholar
Dunn, PK and Smyth, GK (2018) Generalised Linear Models with Examples in R. New York: Springer.Google Scholar
Escolar, C, Martínez, I, Bowker, MA and Maestre, FT (2012) Warming reduces the growth and diversity of biological soil crusts in a semi-arid environment: implications for ecosystem structure and functioning. Philosophical Transactions of the Royal Society B: Biological Sciences 367, 30873099.CrossRefGoogle Scholar
European Commission (2013) Interpretation Manual of European Union Habitats. EUR 28 Nature ENV B.3. European Commission, DG Environment, Brussels, Belgium. [WWW resource] URL https://ec.europa.eu/environment/nature/legislation/habitatsdirective/docs/Int_Manual_EU28.pdfGoogle Scholar
Farkas, EE and Lőkös, LS (1994) Distribution of the lichens Cladonia magyarica Vain., and Solorinella asteriscus Anzi in Europe. Acta Botanica Fennica 150, 2130.Google Scholar
Farkas, E and Lőkös, L (2006) Védett zuzmófajok Magyarországon. [Protected lichen species in Hungary]. Mikológiai közlemények, Clusiana 45, 159171.Google Scholar
Farkas, E, Lőkös, L and Molnár, K (2012) Legally protected species of lichen-forming fungi in Hungary. In Lipnicki, L (ed.), Lichen Protection – Protected Lichen Species. Gorzów Wielkopolski: Sonar Literacki, pp. 3542.Google Scholar
Fekete, G (1997) Évelő nyílt homokpusztagyepek. In Fekete, G, Molnár, Zs and Horváth, F (eds), A magyarországi élőhelyek leírása és határozókönyve. Budapest: A Nemzeti Élőhely-osztályozási Rendszer, Magyar Természettudományi Múzeum, pp. 100102.Google Scholar
Ferrenberg, S, Reed, SC and Belnap, J (2015) Climate change and physical disturbance cause similar community shifts in biological soil crusts. Proceedings of the National Academy of Sciences of the United States of America 112, 1211612121.CrossRefGoogle ScholarPubMed
Gallé, L (1973) Flechtenvegetation der Sandgebiete der Tiefebene Sundungarns. Móra Ferenc Múzeum Évkönyve 1972/73, 259278.Google Scholar
Gams, H (1938) Über einige Flechtenreiche Trockenrasen Mitteldeutschlands. Hercynia 1, 279284.Google Scholar
Gheza, G, Assini, S and Valcuvia-Passadore, M (2015) Contribution to the knowledge of lichen flora of inland sand dunes in the western Po Plain (N Italy). Plant Biosystems 149, 307314.CrossRefGoogle Scholar
Gheza, G, Assini, S and Valcuvia, Passadore M (2016) Terricolous lichen communities of Corynephorus canescens grasslands of Northern Italy. Tuexenia 36, 121142.Google Scholar
Gheza, G, Assini, S, Lelli, C, Marini, L, Mayrhofer, H and Nascimbene, J (2020) Biodiversity and conservation of terricolous lichens and bryophytes in continental lowlands of northern Italy: the role of different dry habitat types. Biodiversity and Conservation 29, 35333550.CrossRefGoogle Scholar
[Hungarian] Ministry of Rural Development (2013) Numbers 61–77 of Annex 5 of Ministry of Rural Development Decree No. 83/2013.(IX.25) VM. Magyar Közlöny 156, 67503.Google Scholar
Janssen, JAM, Rodwell, JS, García Criado, M, Gubbay, S, Haynes, T, Nieto, A, Sanders, N, Landucci, F, Loidi, J, Ssymank, A, et al. (2016) European Red List of Habitats. Part 2. Terrestrial and Freshwater Habitats. Luxembourg: Publications Office of the European Union.Google Scholar
Johansen, JR (2001) Impacts of fire on biological soil crusts. In Belnap, J and Lange, O (eds), Biological Soil Crusts: Structure, Function, and Management. Berlin, Heidelberg: Springer-Verlag, pp. 385397.CrossRefGoogle Scholar
Jun, R and Rozé, F (2005) Monitoring bryophytes and lichens dynamics in sand dunes: example on the French Atlantic coast. In Herrier, J-L, Mees, J, Salman, A, Seys, J, Van Nieuwenhuyse, H and Dobbelaere, I (eds), Proceedings Dunes and Estuaries 2005’. International Conference on Nature Restoration Practices in European Coastal Habitats. Koksijde: Flanders Marine Institute, pp. 291313.Google Scholar
Jüriado, I, Kämärä, ML and Oja, E (2016) Environmental factors and ground disturbance affecting the composition of species and functional traits of ground layer lichens on grey dunes and dune heaths of Estonia. Nordic Journal of Botany 34, 244255.CrossRefGoogle Scholar
Ketner-Oostra, R and Sýkora, KV (2000) Vegetation succession and lichen diversity on dry coastal calcium-poor dunes and the impact of management experiments. Journal of Coastal Conservation 6, 191.CrossRefGoogle Scholar
Ketner-Oostra, R and Sýkora, V (2009) Vegetation change in a lichen-rich inland drift sand area in the Netherlands. Phytocoenologia 38, 267286.CrossRefGoogle Scholar
Ketner-Oostra, R, Aptroot, A, Jungerius, PD and Sýkora, KV (2012) Vegetation succession and habitat restoration in Dutch lichen-rich inland drift sands. Tuexenia 32, 245268.Google Scholar
Koster, EA (2009) The ‘European Aeolian Sand Belt’: geoconservation of drift sand landscapes. Geoheritage 1, 93110.CrossRefGoogle Scholar
Gy, Kröel-Dulay, Ónodi, G, Szitár, K, Lhotsky, B, Mojzes, A and Kertész, M (2018) Combining extreme drought experiments with chronic precipitation manipulations: altered species composition prevents fast recovery of ecosystem functioning. In European Geosciences Union General Assembly 2018, 813 April 2018, Vienna, Austria, paper EGU2018-8800.Google Scholar
Kuznetsova, A, Brockhoff, PB and Christensen, RHB (2017) lmerTest package: tests in linear mixed effects models. Journal of Statistical Software 82, 126.CrossRefGoogle Scholar
Legendre, P and Legendre, L (2012) Numerical Ecology. Amsterdam: Elsevier.Google Scholar
Lellei-Kovács, E, Kovács-Láng, E, Botta-Dukát, Z, Kalapos, T, Emmett, B and Beier, C (2011) Thresholds and interactive effects of soil moisture on the temperature response of soil respiration. European Journal of Soil Biology 47, 247255.CrossRefGoogle Scholar
Lenth, RV (2021) emmeans: estimated marginal means, aka least-squares means. R package version 1.5.4. [WWW resource] URL https://CRAN.R-project.org/package=emmeansGoogle Scholar
Leppik, E, Jüriado, I, Suija, A and Liira, J (2013) The conservation of ground layer lichen communities in alvar grasslands and the relevance of substitution habitats. Biodiversity and Conservation 22, 591614.CrossRefGoogle Scholar
Lőkös, L and Tóth, E (1997) Red list of lichens of Hungary (a proposal). In Tóth, E and Horváth, R (eds), Proceedings of the ‘Research, Conservation, Management’ Conference: Aggtelek, Hungary, 1–5 May 1996, Volume I. Aggtelek: Aggtelek National Park Directorate, pp. 337343.Google Scholar
Lőkös, L and Verseghy, K (2001) The lichen flora of the Kiskunság National Park and southern part of the Danube-Tisza interfluves. In Lőkös, L and Rajczy, M (eds), The Flora of the Kiskunság National Park: Vol. 2, Cryptogams. Budapest: Magyar Termeszettudomanyi Muzeum, pp. 299362.Google Scholar
Molnár, Z (2003) A Kiskunság Száraz Homoki Növényzete. (Dry Sand Vegetation of the Kiskunság). Budapest: Természetbúvár Alapítvány Kiadó.Google Scholar
Molnár, Z (2008) A Duna-Tisza köze és a Tiszántúl fontosabb vegetáció típusainak holocén kori története: irodalmi értékelés egy vegetációkutató szemszögéből. Kanitzia 16, 93118.Google Scholar
Molnár, Z, Bartha, S, Seregélyes, T, Illyés, E, Tímár, G, Horváth, F, Révész, A, Kun, A, Botta-Dukát, Z, Bölöni, J, et al. (2007) A grid-based, satellite-image supported, multi-attributed vegetation mapping method (MÉTA). Folia Geobotanica 42, 225247.CrossRefGoogle Scholar
Molnár, Z, Biró, M, Bartha, S, Fekete, G (2012) Past trends, present state and future prospects of Hungarian forest-steppes. In Werger, MJA and van Staalduinen, MA (eds), Eurasian Steppes. Ecological Problems and Livelihoods in a Changing World. Dordrecht: Springer, pp. 209252.CrossRefGoogle Scholar
Ochoa-Hueso, R, Hernandez, RR, Pueyo, JJ and Manrique, E (2011) Spatial distribution and physiology of biological soil crusts from semi-arid central Spain are related to soil chemistry and shrub cover. Soil Biology and Biochemistry 43, 18941901.CrossRefGoogle Scholar
Oksanen, J, Blanchet, FG, Friendly, M, Kindt, R, Legendre, P, McGlinn, D, Minchin, PR, O'Hara, RB, Simpson, GL, Solymos, P, et al. (2019) vegan: community ecology package. R package version 2.5-6. [WWW resource] URL https://CRAN.R-project.org/package=vegan.Google Scholar
Ónodi, G, Kertész, M and Botta-Dukát, Z (2006) Effects of simulated grazing on open perennial sand grassland. Community Ecology 7, 133141.CrossRefGoogle Scholar
Pécsi, M (1967) A felszín kialakulása és mai képe (Duna-Tisza közi Hátság). In Pécsi, M (ed.), Magyarország Tájföldrajza. 1. A dunai Alföd. Budapest: Akadémiai Kiadó, pp. 214222.Google Scholar
Péczely, G (1967) Éghajlat. In Pécsi, M (ed), Magyarország Tájföldrajza. 1. A dunai Alföd. Budapest: Akadémiai Kiadó, pp. 222225.Google Scholar
Pino-Bodas, R, Burgaz, AR, Ahti, T and Stenroos, S (2018) Taxonomy of Cladonia angustiloba and related species. Lichenologist 50, 267282.CrossRefGoogle Scholar
Pintado, A, Sancho, LG, Green, TGA, Blanquer, JM and Lazaro, R (2005) Functional ecology of the biological soil crust in semi-arid SE Spain: sun and shade populations of Diploschistes diacapsis (Ach.) Lumbsch. Lichenologist 37, 425432.CrossRefGoogle Scholar
R Core Team (2020) R: a Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. [WWW resource] URL https://www.R-project.org/. [Accessed 15 January 2020].Google Scholar
Scheidegger, C, Groner, U, Keller, C and Stofer, S (2002) Biodiversity assessment tools – lichens. In Nimis, PL, Scheidegger, C and Wolseley, PA (eds), Monitoring with Lichens – Monitoring Lichens. Dordrecht: Kluwer Academic Publishers, pp. 359365.CrossRefGoogle Scholar
Schmidt, B (1986) Lichens from two inland dune areas in Western Jutland. Graphis Scripta 1, 3342.Google Scholar
Sinigla, M, Lőkös, L, Varga, N and Farkas, E (2014) Distribution of the lichen species Cetraria aculeata in Hungary. Studia Botanica Hungarica 45, 515.CrossRefGoogle Scholar
Sinigla, M, Lőkös, L, Varga, N and Farkas, E (2015) Distribution of the legally protected lichen species Cetraria islandica in Hungary. Studia Botanica Hungarica 46, 91100.CrossRefGoogle Scholar
Smith, CW, Aptroot, A, Coppins, BJ, Fletcher, A, Gilbert, OL, James, PW and Wolseley, PA (eds) (2009) The Lichens of Great Britain and Ireland. London: British Lichen Society.Google Scholar
Sparrius, LB (2011) Inland dunes in the Netherlands: soil, vegetation, nitrogen deposition and invasive species. Ph.D. thesis, University of Amsterdam.Google Scholar
Szatmári, J, Tobak, Z and Novák, Z (2016) Environmental monitoring supported by aerial photography – a case study of the burnt down Bugac juniper forest, Hungary. Journal of Environmental Geography 9, 3138.CrossRefGoogle Scholar
Tilk, M, Ots, K and Tullus, T (2018) Effect of environmental factors on the composition of terrestrial bryophyte and lichen species in Scots pine forests on fixed sand dune. Forest Systems 27, e015.CrossRefGoogle Scholar
Ullmann, I and Büdel, B (2001) Ecological determinants of species composition of biological crusts on a landscape scale. In Belnap, J and Lange, O (eds), Biological Soil Crusts: Structure, Function, and Management. Berlin, Heidelberg: Springer-Verlag, pp. 203213.CrossRefGoogle Scholar
Veres, K, Farkas, E and Csintalan, Z (2020) The bright and shaded side of duneland life: the photosynthetic response of lichens to seasonal changes is species-specific. Mycological Progress 19, 629641.CrossRefGoogle Scholar
Verseghy, K (1958) Die endemischen Flechten der Karpaten und des Karpatenbeckens. Annales Historico-Naturales Musei Nationalis Hungarici 50(ser. nov. 9), 6573.Google Scholar
Verseghy, K (1994) Magyarország Zuzmóflórájának Kézikönyve. Budapest: Magyar Természettudományi Múzeum.Google Scholar
Walter, H and Breckle, SW (1984) Ökologie der Erde. Stuttgart: Gustav Fischer Verlag.Google Scholar
Warren, SD and Eldridge, DJ (2001) Biological soil crusts and livestock in arid ecosystems: are they compatible? In Belnap, J and Lange, O (eds), Biological Soil Crusts: Structure, Function, and Management. Berlin, Heidelberg: Springer-Verlag, pp. 401415.CrossRefGoogle Scholar
Wirth, V, Hauck, M and Schultz, M (2013) Die Flechten Deutschlands. Stuttgart: Ulmer.Google Scholar
Zielinska, J (1967) Porosty Puszczy Kampinoskiej [Lichenes of the Kampinos Forest]. Monographiae Botanicae [Warszawa] 24, 1129.Google Scholar
Zuur, A, Ieno, EN, Walker, N, Saveliev, AA and Smith, GM (2009) Mixed Effects Models and Extensions in Ecology with R. New York: Springer-Verlag.CrossRefGoogle Scholar