Assessing the impact of land abandonment, nitrogen enrichment and fairy-ring fungi on plant diversity of Mediterranean grasslands

Biodiversity and Conservation

Volumn 22, Issue 10, 2013, Pages 2285-2304

  Bonanomi, Giuliano ^a   Incerti, Guido ^a   Allegrezza, Marina ^b  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

Author keywords

Biodiversity conservation; Semi natural grassland; Soil borne pathogen; Species coexistence; Species diversity; Vegetation pattern

Indexed keywords

ABANDONED LAND; BIODIVERSITY; COEXISTENCE; CONSERVATION MANAGEMENT; DATA SET; EUTROPHICATION; GRASSLAND; GRAZING; HUMAN ACTIVITY; IMPACT; LITTER; MOWING; NITROGEN; PATHOGEN; PLANT COMMUNITY; RARE SPECIES; SPECIES DIVERSITY; SPECIES RICHNESS; VEGETATION;

CENTRAL EUROPE; ITALY; MEDITERRANEAN SEA;

EID: 84883271605     PISSN: 09603115     EISSN: 15729710     Source Type: Journal    
DOI: 10.1007/s10531-013-0502-8     Document Type: Article

References (108)

1. Abesha E, Caetano-Anollés G, Høiland K (2003) Population genetics and spatial structure of the fairy ring fungus Marasmius oreades in a Norwegian sand dune ecosystem. Mycologia 95: 1021-1031.
2. Amatangelo KL, Dukes JS, Field CB (2009) Responses of a California annual grassland to litter manipulation. J Veg Sci 19: 605-612.
3. Antonsen H, Olsson PA (2005) Relative importance of burning, mowing and species translocation in the restoration of a former boreal hayfield: responses of plant diversity and the microbial community. J Appl Ecol 42: 337-347.
4. Basso F, Santilocchi R, Postiglione L, Cavallero A, Grignani C, Reyneri A, Costa G, Pasca U, Ziliotto M, Scotton A, Pardini G, Pazzi S, Piemontese P, Talamucci C, Zagni AA, Bianchi M, Bencivenga F, Carone E, De Falco A, Corleto E, Cazzato S, Caredda P, Bullitta G, Longo S, Cassaniti PG, Litrico S, Cosentino S (1992) Gestione e miglioramento di pascoli italiani. Riv Agron 26: 344-359.
5. Bayliss-Elliott JS (1926) Concerning fairy rings in pastures. Ann Appl Biol 33: 227-288.
6. Berendse F (1990) Organic matter accumulation and nitrogen mineralization during secondary succession in heathland ecosystems. J Ecol 78: 413-427.
7. Biondi E, Allegrezza M, Zuccarello V (2005) Syntaxonomic revision of the Apennine grasslands belonging to Brometalia erecti and an analysis of their relationships with the xerophilous vegetation of Rosmarinetea officinalis (Italy). Phytocoenologia 35: 129-163.
8. Blenis PV, Chow PS, Duncan I, Knowles NR (2004) Cyanide levels near fairy rings affect the growth of grasses and fungi. Can J Bot 82: 1324-1329.
9. Bobbink R (2004) Plant species richness and empirical nitrogen critical loads: an inventory. Report Landscape Ecology. Utrecht University/RIVM, Bilthoven.
10. Bobbink R, Willems JH (1987) Increasing dominance of Brachypodium pinnatum (L.) Beauv. in chalk grasslands: a threat to a species-rich ecosystem. Biol Conserv 40: 301-314.
11. Bobbink R, Willems JH (1991) Impact of different cutting regimes on the performance of Brachypodium pinnatum in Dutch chalk grassland. Biol Conserv 56: 1-21.
12. Bobbink R, Hick K, Galloway J, Spranger T, Alkemade R, Ashmore M, Bustamante M, Cinderby S, Davidson E, Dentener F, Emmett B, Erisman J-W, Fenn M, Gilliam F, Nordin A, Pardo L, WallisDeVries M (2010) Global assessment of nitrogen deposition effects on terrestrial plant diversity: a synthesis. Ecol Appl 20: 30-59.
13. Bonanomi G, Caporaso S, Allegrezza M (2006) Short-term effect of nitrogen enrichment, litter removal and cutting on a Mediterranean grassland. Acta Oecol 30: 419-425.
14. Bonanomi G, Caporaso S, Allegrezza M (2009) Effects of nitrogen enrichment, plant litter removal and cutting on a species-rich Mediterranean calcareous grassland. Plant Biosyst 143: 443-455.
15. Bonanomi G, Incerti G, Barile E, Capodilupo M, Antignani V, Mingo A, Lanzotti V, Scala F, Mazzoleni S (2011) Phytotoxicity, not nitrogen immobilization, explains plant litter inhibitory effects: evidence from solid-state 13C NMR spectroscopy. New Phytol 191: 1018-1030.
16. Bonanomi G, Mingo A, Incerti G, Mazzoleni S, Allegrezza M (2012) Fairy rings caused by a killer fungus foster plant diversity in species-rich grassland. J Veg Sci 23: 236-248.
17. Bugalho MN, Caldeira MC, Pereira JS, Aronson J, Pausas JG (2011) Mediterranean cork oak savannas require human use to sustain biodiversity and ecosystem services. Front Ecol Environ 9: 278-286.
18. Carson WP, Peterson CJ (1990) The role of litter in an old-field community: impact of litter quantity in different seasons on plant species richness and abundance. Oecologia 85: 8-13.
19. Cartenì F, Marasco A, Bonanomi G, Mazzoleni S, Rietkerk M, Giannino F (2012) Negative plant soil feedback and ring formation in clonal plants. J Theor Biol 313: 153-161.
20. Catorci A, Cesaretti S, Gatti R, Ottaviani G (2011) Abiotic and biotic changes due to spread of Brachypodium genuense (DC.) Roem. and Schult. in sub-Mediterranean meadows. Comm Ecol 12: 117-125.
21. Chesson P (2000) Mechanisms of maintenance of species diversity. Ann Rev Ecol Syst 31: 343-366.
22. Clements FE (1916) Plant succession. Carnegie Institution, Washington.
23. Connell JH (1978) Diversity in tropical rain forest and coral reefs. Science 199: 1302-1310.
24. Cramer VA, Hobbs RJ, Standish RJ (2007) What's new about old fields? Land abandonment and eco system assembly. Trends Ecol Evol 23: 112-194.
25. WallisDeVries MF, Poschlod P, Willems JH (2002) Challenges for the conservation of calcareous grasslands in northwestern Europe: integrating the requirements of flora and fauna. Biol Conserv 104: 265-273.
26. Deák B, Valkó O, Kelemen A, Török P, Miglécz T, Ölvedi T, Lengyel S, Tóthmérész B (2011) Litter and graminoid biomass accumulation suppresses weedy forbs in grassland restoration. Plant Biosyst 145: 730-737.
27. Dekker LW, Ritsema CJ (1996) Uneven moisture patterns in water repellent soils. Geoderma 70: 87-89.
28. Djajakirana G, Joergensen RG (1996) Changes in soil organic matter, microbial biomass C and ergosterol under a fairy ring of Marasmius oreades. Pedobiologia 40: 498-504.
29. Donath TW, Hölzel N, Otte A (2006) Influence of competition by sown grass, disturbance and litter on recruitment of rare flood-meadow species. Biol Conserv 130: 315-323.
30. Dowson CG, Rayner ADM, Boddy L (1989) Spatial dynamics and interactions of the woodland fairy ring fungus, Clitocybe nebularis. New Phytol 111: 699-705.
31. Eckstein RL, Ruch D, Otte A, Donath TW (2012) Invasibility of a nutrient-poor pasture through resident and non-resident herbs is controlled by litter, gap size and propagule pressure. PLoS ONE 7: e41887.
32. Edwards PJ (1984) The growth of fairy rings of Agaricus arvensis and their effect upon grassland vegetation and soil. J Ecol 72: 505-513.
33. Edwards PJ (1988) Effects of the fairy ring fungus Agaricus arvensis on nutrient availability in grassland. New Phytol 110: 377-381.
34. Enyedi ZM, Ruprecht E, Deák M (2008) Long-term effects of the abandonment of grazing on steppe-like grasslands. Appl Veg Sci 11: 55-62.
35. Facelli JM, Pickett STA (1991) Plant litter: its dynamics and its role in plant community structure. Bot Rev 57: 1-32.
36. FAOSTAT (2012) FAOSTAT Population module. http://faostat. fao. org/site/550/default. aspx. Accessed 30 April 2012.
37. Farris E, Filigheddu R, Deiana P, Farris GA, Garau G (2010) Short-term effects on sheep pastureland due to grazing abandonment in a Western Mediterranean island ecosystem: a multidisciplinary approach. J Nat Conserv 18: 258-267.
38. Fidanza MA, Cisar JL, Kostka SJ, Gregos JS, Schlossberg MJ, Franklin M (2007) Preliminary investigation of soil chemical and physical properties associated with type-I fairy ring symptoms in turfgrass. Hydrol Process 21: 2285-2290.
39. Filer TH Jr (1965) Parasitic aspects of a fairy ring fungus, Marasmius oreades. Phytopathology 55: 1132-1134.
40. Fisher RF (1977) Nitrogen and phosphorus mobilization by the fairy ring fungus, Marasmiums oreades (Bolt) Fr. Soil Biol Biochem 9: 239-241.
41. Foster BL, Gross KL (1998) Species richness in a successional grassland: effects of nitrogen enrichment and plant litter. Ecology 79: 2593-2602.
42. Fox RTV (2006) Fungal foes in your garden: fairy ring mushrooms. Mycologist 20: 36-37.
43. Fridley JD, Grime JP, Huston MA, Pierce S, Smart SM, Thompson K, Börger L, Brooker RW, Cerabolini BEL, Gross N, Liancourt P, Michalet R, Le Bagousse-Pinguet Y (2012) Comment on "Productivity Is a Poor Predictor of Plant Species Richness". Science 335: 1441.
44. Galvánek D, Lepš J (2012) The effect of management on productivity, litter accumulation and seedling recruitment in a Carpathian mountain grassland. Plant Ecol 213: 523-533.
45. Gilliam FS (2006) Response of the herbaceous layer of forest ecosystems to excess nitrogen deposition. J Ecol 94: 1176-1191.
46. Goldberg DE, Werner PA (1983) The effects of size of opening in vegetation and litter cover on seedling establishment of goldenrods (Solidago spp.). Oecologia 60: 149-155.
47. Gramss G, Voigt K, Bergmann H (2005) Factors influencing water solubility and plant availability of mineral compounds in the tripartite fairy rings of Marasmius oreades (Bolt.: fr.) Fr. J Basic Microbiol 45: 41-54.
48. Grime JP, Fridley JD, Askew AP, Thompson K, Hodgson JG, Bennett CR (2008) Long-term resistance to simulated climate change in an infertile grassland. Proc Natl Acad Sci USA 105: 10028-10032.
49. Harrison S, Inouye BD, Safford HD (2003) Ecological heterogeneity in the effects of grazing and fire on grassland diversity. Conserv Biol 17: 837-845.
50. Heady HF (1956) Changes in a California annual plant community induced by manipulation of natural mulch. Ecology 37: 798-812.
51. Henry HA, Chiariello NR, Vitousek PM, Mooney HA, Field CB (2006) Interactive effects of fire, elevated carbon dioxide, nitrogen deposition, and precipitation on a California annual grassland. Ecosystems 9: 1066-1075.
52. Huenneke LF, Hamburg SP, Koide R, Mooney HA, Vitousek PM (1990) Effects of soil resources on plant invasion and community structure in Californian serpentine grassland. Ecology 71: 478-491.
53. Huston MA (1994) Biological diversity: the coexistence of species on changing landscape. Cambridge University, Cambridge.
54. Juergens N (2013) The biological underpinnings of Namib Desert fairy circles. Science 339: 1618-1621.
55. Klironomos JN (2002) Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417: 67-70.
56. Koide RT, Huenneke LF, Hamburg SP, Mooney HA (1988) Effects of applications of fungicide, phosphorus and nitrogen on the structure and productivity of an annual serpentine plant community. Funct Ecol 2: 335-344.
57. Kull K, Zobel M (1991) High species richness in a Estonian wooded meadow. J Veg Sci 2: 711-714.
58. Körner C (2003) Alpine plant life. Springer, Berlin.
59. Kulmatisky A, Beard KH, Stevens JR, Cobbold SM (2008) Plant-soil feedbacks: a meta-analytical review. Ecol Lett 11: 980-992.
60. Lebeau JB, Hawn EJ (1963) Formation of hydrogen cyanide by the mycelial stage of a fairy ring fungus. Phytopathology 53: 1395-1396.
61. Lian C, Narimatsu M, Nara K, Hogetsu T (2006) Tricholoma matsutake in a natural Pinus densiflora forest: correspondence between above- and below-ground genets, association with multiple host trees and alteration of existing ectomycorrhizal communities. New Phytol 171: 825-836.
62. Loydi A, Eckstein RL, Otte A, Donath TW (2013) Effects of litter on seedling establishment in natural and semi-natural grasslands: a meta-analysis. J Ecol 101: 454-464.
63. Mathur SP (1970) Degradation of soil humus by the fairy ring mushroom. Plant Soil 33: 717-720.
64. Mazzoleni S, di Pasquale G, Mulligan M, di Martino P, Rego F (2004) Recent dynamics of the Mediterranean vegetation and landscape. Wiley, Chichester.
65. Muller S (2002) Appropriate agricultural management practices required to ensure conservation and biodiversity of environmentally sensitive grassland sites designated under Natura 2000. Agric Ecosyst Environ 89: 261-266.
66. Nordin A, Strengbom J, Ericson L (2006) Responses to ammonium and nitrate additions by boreal plants and their natural enemies. Environ Pollut 141: 167-174.
67. Norstadt FA, Frey CR, Sigg H (1973) Soil urease: paucity in the presence of the fairy ring fungus Marasmius oreades (Bolt.) Fr. Soil Sci Am J 37: 880-885.
68. Ochoa-Hueso R, Allen EB, Branquinho C, Cruz C, Dias T, Fenn ME, Manrique E, Pérez-Corona ME, Sheppard LJ, Stock WD (2011) Nitrogen deposition effects on Mediterranean-type ecosystems: an ecological assessment. Environ Pollut 159: 2265-2279.
69. Ogawa M (1985) Ecological characters of ectomycorrhizal fungi and their mycorrhizae. Jpn Agric Res Q 18: 305-314.
70. Ohara H, Hamada M (1967) Disappearance of bacteria from the zone of active mycorrhizas in Tricholoma matsutake (S. Ito et Imai) Singer. Nature 213: 528-529.
71. Palmer MW (1994) Variation in species richness: towards a unification of hypotheses. Folia Geobot 29: 511-530.
72. Peter M (2006) Ectomycorrhizal fungi-fairy rings and the wood-wide web. New Phytol 171: 685-687.
73. Poschlod P, WallisDeVries MF (2002) The historical and socioeconomic perspective of calcareous grassland-lesson from the distant and recent past. Biol Conserv 104: 361-376.
74. Rasran L, Vogt K, Jensen K (2007) Effects of litter removal and mowing on germination and establishment of two fen-grassland species along a productivity gradient. Folia Geobot 42: 271-288.
75. Rivas-Martínez S (2004) Global Bioclimatics. Clasificación bioclimática de la tierra. http://www. globalbioclimatics. org. Accessed 30 April 2012.
76. Rodwell JS, Schaminée JHJ, Mucina L, Pignatti S, Dring J, Moss D (2002) The diversity of European vegetation-an overview of phytosociological alliances and their relationships to EUNIS habitats. National Reference Centre for Agriculture Nature and Fisheries, Wageningen.
77. Ruprecht E, Enyedi MZ, Eckstein RL, Donath TW (2010) Restorative removal of plant litter and vegetation 40 years after abandonment enhances re-emergence of steppe grassland vegetation. Biol Conserv 143: 449-456.
78. Seabloom EW, Harpole WS, Reichman OJ, Tilman D (2003) Invasion, competitive dominance, and resource use by exotic and native California grassland species. Proc Natl Acad Sci USA 100: 13384-13389.
79. Shantz HL, Piemeisel RL (1917) Fungus fairy rings in Eastern Colorado and their effect on vegetation. J Agric Res 11: 191-245.
80. Smith JD (1980) Is biologic control of Marasmius oreades fairy rings possible? Plant Dis 64: 348-354.
81. Smith JD, Rupps R (1978) Antagonism and Marasmius oreades fairy rings. J Sports Turf Res Inst 54: 97-105.
82. Smith HL, Jackson N, Woolhouse AR (1989) Fungal diseases of amenity turfgrasses, 3rd edn. Spon, London, pp 341-353.
83. Špačková I, Lepš J (2004) Variability of seedling recruitment under dominant, moss, and litter removal over four years. Folia Geobot 39: 41-55.
84. Stevens CJ, Dise NB, Mountford JO, Gowing DJ (2004) Impact of nitrogen deposition on the species richness of grasslands. Science 303: 1876-1879.
85. Suding KN, Goldberg DE (1999) Variation in the effects of vegetation and litter on recruitment across productivity gradients. J Ecol 87: 436-449.
86. Tanner EVJ, Vitousek PM, Cuevas E (1998) Experimental investigation of nutrient limitation of forest growth on wet tropical mountains. Ecology 79: 10-22.
87. Terashima Y, Fukiharu T, Fujiie A (2004) Morphology and comparative ecology of the fairy ring fungi, Vascellum curtisii and Bovista dermoxantha, on turf of bentgrass, bluegrass, and Zoysiagrass. Mycoscience 45: 251-260.
88. Tilman D (1988) Plant strategies and the dynamics and structure of plant communities. Princeton University Press, Princeton.
89. Tilman D (1994) Competition and biodiversity in spatially structured habitats. Ecology 75: 2-16.
90. Turitzen SN (1982) Nutrient limitations to plant growth in a California serpentine grassland. Am Midl Nat 107: 95-99.
91. Uys RG, Bond WJ, Everson TM (2004) The effect of different fire regimes on plant diversity in southern African grasslands. Biol Conserv 118: 489-499.
92. Vaario LM, Fritze H, Spetz P, Heinonsalo J, Hanajík P, Pennanen T (2011) Tricholoma matsutake dominates diverse microbial communities in different forest soils. Appl Environ Microb 77: 8523-8531.
93. van der Maarel E, Sykes MT (1993) Small-scale plant species turnover in a limestone grassland: the carousel model and some comments on the niche concept. J Veg Sci 4: 179-188.
94. van der Putten WH, Bardgett RD, Bever JD, Bezemer TM, Casper BB, Fukami T, Kardol P, Klironomos JN, Kulmatiski A, Schweitzer JA, Suding KN, van de Voorde1 TFJ, Wardle DA (2013) Plant-soil feedback: the past, the present and the future challenges. J Ecol 101: 265-276.
95. Vassilev K, Pedashenko H, Nikolov SC, Apostolova I, Dengler J (2011) Effect of land abandonment on the vegetation of upland semi-natural grasslands in the Western Balkan Mts Bulgaria. Plant Biosyst 145: 654-665.
96. Wang J, Zhao M, Willms WD, Han G, Wang Z, Bai Y (2011) Can plant litter affect net primary production of a typical steppe in Inner Mongolia? J Veg Sci 22: 367-376.
97. Watt AS (1947) Pattern and process in the plant community. J Ecol 35: 1-22.
98. Weaver JE, Rowland NW (1952) Effects of excessive natural mulch on development, yield, and structure of native grassland. Bot Gaz 107: 1-19.
99. Wedin DA, Tilman D (1993) Competition among grasses along a nitrogen gradient: initial conditions and mechanisms of competition. Ecol Monogr 63: 199-229.
100. Weiss SB (1999) Cars, cows, and checkerspot butterflies: nitrogen deposition and management of nutrient-poor grasslands for a threatened species. Conserv Biol 13: 1476-1486.
101. Willems JH (2001) Problems, approaches, and results in restoration of Dutch calcareous grassland during the last 30 years. Restor Ecol 9: 147-154.
102. Willms WD, Smoliak S, Bailey AW (1986) Herbage production following litter removal on Alberta native grasslands. J Range Manage 39: 536-540.
103. Wilson EJ, Wells TCE, Sparks TH (1995) Are calcareous grasslands in the UK under threat from nitrogen deposition?-an experimental determination of a critical load. J Ecol 83: 823-832.
104. Wilson JB, Peet RK, Dengler J, Pärtel M (2012) Plant species richness: the world records. J Veg Sci 23: 796-802.
105. Xiong S, Nilsson C (1999) The effect of plant litter on vegetation: a meta-analysis. J Ecol 27: 984-994.
106. York CA, Canaway PM (2000) Water repellent soils as they occur on UK golf greens. J Hydrol 231-232: 126-133.
107. 2, precipitation, and N deposition. Ecol Monogr 73: 585-604.
108. Zhao J, Shao Y, Bao Q (2003) Soil-vegetation system surround the fairy ring in steppe. Chin J Ecol 5: 36-43.