Soil organic matter rather than ectomycorrhizal diversity is related to urban tree health

Autoři: Maarten Van Geel aff001;  Kang Yu aff002;  Gerrit Peeters aff001;  Kasper van Acker aff001;  Miguel Ramos aff003;  Cindy Serafim aff003;  Pierre Kastendeuch aff004;  Georges Najjar aff004;  Thierry Ameglio aff005;  Jérôme Ngao aff005;  Marc Saudreau aff005;  Paula Castro aff003;  Ben Somers aff002;  Olivier Honnay aff001
Působiště autorů: Plant Conservation and Population Biology, Department of Biology, KU Leuven, Kasteelpark Arenberg, Heverlee, Belgium aff001;  Division of Forest, Nature & Landscape, Department of Earth & Environmental Sciences, KU Leuven, Celestijnenlaan, Heverlee, Belgium aff002;  Escola Superior de Biotecnologia, Catholic University of Portugal, Rua Arquiteto Lobão Vital, Porto, Portugal aff003;  Laboratoire des Sciences de L'ingénieur, de L'informatique et de L'imagerie, Strasbourg University, Illkirch, France aff004;  Université Clermont Auvergne, INRA, PIAF, Clermont Ferrand, France aff005
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
doi: 10.1371/journal.pone.0225714


Urban trees provide many ecosystem services, including carbon sequestration, air quality improvement, storm water attenuation and energy conservation, to people living in cities. Provisioning of ecosystem services by urban trees, however, may be jeopardized by the typically poor quality of the soils in urban areas. Given their well-known multifunctional role in forest ecosystems, ectomycorrhizal fungi (EcM) may also contribute to urban tree health and thus ecosystem service provisioning. Yet, no studies so far have directly related in situ EcM community composition to urban tree health indicators. Here, two previously collected datasets were combined: i) tree health data of 175 Tilia tomentosa trees from three European cities (Leuven, Strasbourg and Porto) estimated using a range of reflectance, chlorophyll fluorescence and physical leaf indicators, and ii) ectomycorrhizal diversity of these trees as characterized by next-generation sequencing. Tree health indicators were related to soil characteristics and EcM diversity using canonical redundancy analysis. Soil organic matter significantly explained variation in tree health indicators whereas no significant relation between mycorrhizal diversity variables and the tree health indicators was found. We conclude that mainly soil organic matter, through promoting soil aggregate formation and porosity, and thus indirectly tree water availability, positively affects the health of trees in urban areas. Our results suggest that urban planners should not overlook the importance of soil quality and its water holding capacity for the health of urban trees and potentially also for the ecosystem services they deliver. Further research should also study other soil microbiota which may independently, or in interaction with ectomycorrhiza, mediate tree performance in urban settings.

Klíčová slova:

Extracellular matrix – Leaves – Phylogenetic analysis – Phylogenetics – Trees – Urban areas – Urban ecology – Urban ecosystems


1. Seto KC, Guneralp B, Hutyra LR. Global forecasts of urban expansion to 2030 and direct impacts on biodiversity and carbon pools. PNAS. 2012;109:16083–16088. doi: 10.1073/pnas.1211658109 22988086

2. Kumar P, Morawska L, Birmili W, Paasonen P, Hu M, Kulmala M, et al. Ultrafine particles in cities. Environment International. 2014;66:1–10. doi: 10.1016/j.envint.2014.01.013 24503484

3. Kalnay E, Cai M. Impact of urbanization and land-use change on climate. Nature. 2003;423:528–531. doi: 10.1038/nature01675 12774119

4. Fenger J. Urban air quality. Atmospheric Environment. 1999;33:4877–4900.

5. Roy S, Byrne J, Pickering C. A systematic quantitative review of urban tree benefits, costs, and assessment methods across cities in different climatic zones. Urban Forestry & Urban Greening. 2012;11:351–363.

6. Mullaney J, Lucke T, Trueman SJ. A review of benefits and challenges in growing street trees in paved urban environments. Landscape and Urban Planning. 2015;134:157–166.

7. Ng E, Chen L, Wang YN, Yuan C. A study on the cooling effects of greening in a high-density city: An experience from Hong Kong. Building and Environment. 2012;47:256–271.

8. Kuo FE, Sullivan WC. Environment and crime in the inner city—Does vegetation reduce crime? Environment and Behavior. 2001;33:343–367.

9. White MP, Alcock I, Wheeler BW, Depledge MH. Would you be happier living in a greener urban area? A fixed-effects analysis of panel data. Psychological Science. 2013;24:920–928. doi: 10.1177/0956797612464659 23613211

10. Kardan O, Gozdyra P, Misic B, Moola F, Palmer LJ, Paus T, et al. Neighborhood greenspace and health in a large urban center. Scientific Reports. 2015;5: doi: 10.1038/srep11610 26158911

11. Pandit R, Polyakov M, Tapsuwan S, Moran T. The effect of street trees on property value in Perth, Western Australia. Landscape and Urban Planning. 2013;110:134–142.

12. Sanders JR, Grabosky JC. 20 years later: Does reduced soil area change overall tree growth? Urban Forestry & Urban Greening. 2014;13:295–303.

13. Clarck JR, Ljelgren R. Water as a limiting factor in the development of urban trees. Journal of Arboriculture. 1990;16:203–208.

14. Dale AG, Frank SD. Warming and drought combine to increase pest insect fitness on urban trees. Plos One. 2017;12:

15. Roman LA, Scatena FN. Street tree survival rates: Meta-analysis of previous studies and application to a field survey in Philadelphia, PA, USA. Urban Forestry & Urban Greening. 2011;10:269–274.

16. Attiwill PM, Adams MA. Nutrient Cycling in Forests. New Phytologist. 1993;124:561–582.

17. Itoo ZA, Reshi ZA. The multifunctional role of ectomycorrhizal associations in forest ecosystem processes. Botanical Review. 2013;79:371–400.

18. Lehto T, Zwiazek JJ. Ectomycorrhizas and water relations of trees: a review. Mycorrhiza. 2011;21:71–90. doi: 10.1007/s00572-010-0348-9 21140277

19. Chalot M, Brun A. Physiology of organic nitrogen acquisition by ectomycorrhizal fungi and ectomycorrhizas. Fems Microbiology Reviews. 1998;22:21–44. doi: 10.1111/j.1574-6976.1998.tb00359.x 9640645

20. Pozo MJ, Azcon-Aguilar C. Unraveling mycorrhiza-induced resistance. Current Opinion in Plant Biology. 2007;10:393–398. doi: 10.1016/j.pbi.2007.05.004 17658291

21. Sharma T, Watpade S, Thakur J. Role of mycorrhizae: a component of integrated disease management strategies. Journal of Mycology and Plant Pathology. 2014;44:12–20.

22. Jones MD, Twieg BD, Ward V, Barker J, Durall DM, Simard SW. Functional complementarity of Douglas-fir ectomycorrhizas for extracellular enzyme activity after wildfire or clearcut logging. Functional Ecology. 2010;24:1139–1151.

23. Tedersoo L, May TW, Smith ME. Ectomycorrhizal lifestyle in fungi: global diversity, distribution, and evolution of phylogenetic lineages. Mycorrhiza. 2010;20:217–263. doi: 10.1007/s00572-009-0274-x 20191371

24. Van Geel M, Yu K, Ceulemans T, Peeters G, van Acker K, Geerts W, et al. Variation in ectomycorrhizal fungal communities associated with Silver linden (Tilia tomentosa) within and across urban areas. FEMS Microbiol Ecol. 2018;94:

25. Jonsson L, Anders D, Tor-Erik B. Spatiotemporal distribution of an ectomycorrhizal community in an oligotrophic Swedish Picea abies forest subjected to experimental nitrogen addition: above- and below-ground views. Forest Ecology and Management. 2000;132:143–156.

26. Tedersoo L, Bahram M, Polme S, Koljalg U, Yorou NS, Wijesundera R, et al. Global diversity and geography of soil fungi. Science. 2014;346:1078-+.

27. Egli S. Mycorrhizal mushroom diversity and productivity-an indicator of forest health? Annals of Forest Science. 2011;68:81–88.

28. Sapsford SJ, Paap T, Hardy GESJ, Burgess T. The 'chicken or the egg': which comes first, forest tree decline or loss of mycorrhizae? Plant Ecology. 2017;218:1093–1106.

29. Cardinale BJ, Duffy JE, Gonzalez A, Hooper DU, Perrings C, Venail P, et al. Biodiversity loss and its impact on humanity. Nature. 2012;486:59–67. doi: 10.1038/nature11148 22678280

30. Tilman D. The influence of functional diversity and composition on ecosystem processes. Science. 1997;277:1300–1302.

31. Baxter JW, Dighton J. Ectomycorrhizal diversity alters growth and nutrient acquisition of grey birch (Betula populifolia) seedlings in host-symbiont culture conditions. New Phytologist. 2001;152:139–149.

32. Maherali H, Klironomos J. Influence of phylogeny on fungal community assembly and ecosystem functioning. Science. 2007;316:1746–1748. doi: 10.1126/science.1143082 17588930

33. Lekberg Y, Helgason T. In situ mycorrhizal function—knowledge gaps and future directions. New Phytologist. 2018;220:957–962. doi: 10.1111/nph.15064 29436724

34. Van Geel M, De Beenhouwer M, Lievens B, Honnay O. Crop-specific and single-species mycorrhizal inoculation is the best approach to improve crop growth in controlled environments. Agronomy for Sustainable Development. 2016;36:37–47.

35. Yu K, Van Geel M, Ceulemans T, Geerts W, Ramos MM, Sousa N, et al. Foliar optical traits indicate that sealed planting conditions negatively affect urban tree health. Ecological Indicators. 2018;95:895–906.

36. Zadeh ARK, Veroustraete F, Buytaert JAN, Dirckx J, Samson R. Assessing urban habitat quality using spectral characteristics of Tilia leaves. Environmental Pollution. 2013;178:7–14. doi: 10.1016/j.envpol.2013.02.021 23517817

37. Timonen S, Kauppinen P. Mycorrhizal colonisation patterns of Tilia trees in street, nursery and forest habitats in southern Finland. Urban Forestry & Urban Greening. 2008;7:265–276.

38. Sims DA, Gamon JA. Relationships between leaf pigment content and spectral reflectance across a wide range of species, leaf structures and developmental stages. Remote Sensing of Environment. 2002;81:337–354.

39. Eitel JUH, Gessler PE, Smith AMS, Robberecht R. Suitability of existing and novel spectral indices to remotely detect water stress in Populus spp. Forest Ecology and Management. 2006;229:170–182.

40. Gao BC. NDWI—A normalized difference water index for remote sensing of vegetation liquid water from space. Remote Sensing of Environment. 1996;58:257–266.

41. Peñuelas J, Pinol J, Ogaya R, Filella I. Estimation of plant water concentration by the reflectance water index WI (R900/R970). International Journal of Remote Sensing. 1997;18:2869–2875.

42. Seelig HD, Hoehn A, Stodieck LS, Klaus DM, Adams WW, Emery WJ. Relations of remote sensing leaf water indices to leaf water thickness in cowpea, bean, and sugarbeet plants. Remote Sensing of Environment. 2008;112:445–455.

43. Gamon JA, Penuelas J, Field CB. A narrow-waveband spectral index that tracks diurnal changes in photosynthetic efficiency. Remote Sensing of Environment. 1992;41:35–44.

44. Merzlyak MN, Gitelson AA, Chivkunova OB, Rakitin VY. Non-destructive optical detection of pigment changes during leaf senescence and fruit ripening. Physiologia Plantarum. 1999;106:135–141.

45. Peñuelas J, Baret F, Filella I. Semi-empirical indexes to assess carotenoids chlorophyll a ratio from leaf spectral reflectance. Photosynthetica. 1995;31:221–230.

46. Strasser RJ, Srivastava A, Tsimilli-Michael M. The fluorescence transient as a tool to characterize and screen photosynthetic samples. Probing Photosynthesis: Mechanism, Regulation & Adaptation. 2000;445–483.

47. Chen DQ, Wang SW, Xiong BL, Cao BB, Deng XP. Carbon/Nitrogen imbalance associated with drought-induced leaf senescence in Sorghum bicolor. Plos One. 2015;10:e0137026. doi: 10.1371/journal.pone.0137026 26317421

48. Robertson G, Coleman D, Bledsoe C, Sollins P (1999) Standard soil methods for long-term ecological research,. New York, USA: Oxford University Press.

49. Waud M, Busschaert P, Ruyters S, Jacquemyn H, Lievens B. Impact of primer choice on characterization of orchid mycorrhizal communities using 454 pyrosequencing. Molecular Ecology Resources. 2014;14:679–699. doi: 10.1111/1755-0998.12229 24460947

50. Edgar R. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nature methods. 2013;10:996–998. doi: 10.1038/nmeth.2604 23955772

51. Koljalg U, Nilsson RH, Abarenkov K, Tedersoo L, Taylor AFS, Bahram M, et al. Towards a unified paradigm for sequence-based identification of fungi. Molecular Ecology. 2013;22:5271–5277. doi: 10.1111/mec.12481 24112409

52. Edgar RC. SINTAX: a simple non-Bayesian taxonomy classifier for 16S and ITS sequences. bioRxiv 74161. 2016;

53. Nguyen NH, Song ZW, Bates ST, Branco S, Tedersoo L, Menke J, et al. FUNGuild: An open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecology. 2016;20:241–248.

54. Oksanen J, Blanchet G, Kindt R, Legendre P, Minchin P, Simpson G, et al. Vegan: Community Ecology Package. R package version 2.5.4: 2019;

55. Jost L. Entropy and diversity. Oikos. 2006;113:363–375.

56. Faith DP. Conservation evaluation and phylogenetic diversity. Biological Conservation. 1992;61:1–10.

57. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research. 2004;32:1792–1797. doi: 10.1093/nar/gkh340 15034147

58. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution. 2018;35:1547–1549. doi: 10.1093/molbev/msy096 29722887

59. Tsirogiannis C, Sandel B. PhyloMeasures: a package for computing phylogenetic biodiversity measures and their statistical moments. Ecography. 2016;39:709–714.

60. Legendre P. Studying beta diversity: ecological variation partitioning by multiple regression and canonical analysis. Journal of Plant Ecology. 2008;1:3–8.

61. Hudson BD. Soil organic-matter and available water capacity. Journal of Soil and Water Conservation. 1994;49:189–194.

62. Huntington TG (2007) Available water capacity and soil organic matter. Encyclopedia of soil science. New York: Taylor and Francis. pp. 139–143.

63. Lu JWT, Svendsen ES, Campbell LK, Greenfeld J, Braden J, King KL, et al. Biological, social, and urban design factors affecting young street tree mortality in New York city. Cities and the Environment. 2010;3:1–15. doi: 10.15365/cate.3182010

64. Lindahl B, Nilsson R, Tedersoo L, Abarenkov K, Carlsen T, Kjøller R, et al. Fungal community analysis by high-throughput sequencing of amplified markers—a user's guide. New phytologist. 2013;199:288–299. doi: 10.1111/nph.12243 23534863

65. Murphy DV, Cookson WR, Braimbridge M, Marschner P, Jones DL, Stockdale EA, et al. Relationships between soil organic matter and the soil microbial biomass (size, functional diversity, and community structure) in crop and pasture systems in a semi-arid environment. Soil Research. 2011;49:582–594.

66. Vidal-Beaudet L, Galopin G, Grosbellet C. Effect of organic amendment for the construction of favourable urban soils for tree growth. European Journal of Horticultural Science. 2018;83:173–186.

67. Layman RM, Day SD, Mitchell DK, Chen YJ, Harris JR, Daniels WL. Below ground matters: Urban soil rehabilitation increases tree canopy and speeds establishment. Urban Forestry & Urban Greening. 2016;16:25–35.

Článek vyšel v časopise


2019 Číslo 11