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Plant and Soil

, Volume 429, Issue 1–2, pp 159–174 | Cite as

Biocrust tissue traits as potential indicators of global change in the Mediterranean

  • Laura Concostrina-ZubiriEmail author
  • Paula Matos
  • Paolo Giordani
  • Cristina Branquinho
Regular Article

Abstract

Background and aims

Functional traits are promising indicators of global changes and ecosystem processes. Trait responses to environmental conditions have been examined widely in vascular plants. In contrast, few studies have focused on soil lichens and mosses composing biocrusts. We aimed to evaluate the potential of biocrust tissue traits as indicators of changes in climate and soil properties.

Methods

Isotope ratios and nutrient content in biocrust tissue were analyzed in 13 Mediterranean shrublands along an aridity gradient. Differences in tissue traits between biocrust groups (lichens and mosses), and relationships between tissue traits and climatic and soil variables were examined.

Results

Lichens and mosses differed in δ13C, δ15N and N content, indicating distinct physical and physiological attributes. Tissue traits correlated strongly with numerous climatic variables, likely due to a modulator effect on biocrust water relations and metabolism. We found contrasting responses of lichen and moss traits to climate, although they responded similarly to soil properties. Overall, the most responsive trait was δ15N, suggesting this trait is the best to reflect integrated processes occurring in the atmosphere and soil.

Conclusions

Biocrust tissue traits arise as cost-effective, integrative ecological indicators of global change drivers in Mediterranean ecosystems, with potential applications in response-effect trait frameworks.

Keywords

Isotope ratios Tissue nutrient content Biocrusts Climate Soil Mediterranean 

Notes

Acknowledgements

LCZ was supported by a Marie Curie IEF grant from European Commission’s FP7 (BCSES-GA 628406). PM was supported by FCT-MEC through: project PTDC/AAG-GLO/0045/2014. Special thanks to C. Tejada, M. Köbel, A. Nunes, M. Lo Cascio, L. Morillas, and S. Mereu for help in the field, T. Roovers for the assistance in the laboratory and R. Maia for the isotope and elemental analysis. Special thanks also to Professor M. Aleffi (Bryology Laboratory & Herbarium, Camerino University) for his assistance on moss species identification. We also thank P. Pinho who provided valuable comments on the manuscript. M.A. Bowker and other anonymous reviewers provided helpful comments and discussion that improved an earlier version of the manuscript.

Supplementary material

11104_2017_3483_MOESM1_ESM.docx (39 kb)
ESM 1 (DOCX 39 kb)

References

  1. Aerts R, Chapin FS (1999) The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Adv Ecol Res 30:1–67CrossRefGoogle Scholar
  2. Amundson R, Austin AT, Schuur EA et al (2003) Global patterns of the isotopic composition of soil and plant nitrogen. Glob Biogeochem Cycles 17:1031CrossRefGoogle Scholar
  3. Asplund J, Wardle DA (2013) The impact of secondary compounds and functional characteristics on lichen palatability and decomposition. J Ecol 101:689–700CrossRefGoogle Scholar
  4. Asplund J, Wardle DA (2014) Within-species variability is the main driver of community-level responses of traits of epiphytes across a long-term chronosequence. Funct Ecol 28:1513–1522CrossRefGoogle Scholar
  5. Asplund J, Wardle DA (2015) Changes in functional traits of the terricolous lichen Peltigera aphthosa across a retrogressive boreal forest chronosequence. Lichenologist 47:187–195CrossRefGoogle Scholar
  6. Asplund J, Sandling A, Kardol P, Wardle DA (2014) The influence of tree-scale and ecosystem-scale factors on epiphytic lichen communities across a long-term retrogressive chronosequence. J Veg Sci 25:1100–1111CrossRefGoogle Scholar
  7. Ayres E, Van der Wal R, Sommerkorn M, Bardgett RD (2006) Direct uptake of soil nitrogen by mosses. Biol Lett 2:286–288Google Scholar
  8. Bates JW (1992) Mineral nutrient acquisition and retention by bryophytes. J Bryol 17:223–240CrossRefGoogle Scholar
  9. Batts JE, Calder LJ, Batts BD (2004) Utilizing stable isotope abundances of lichens to monitor environmental change. Chem Geol 204:345–368CrossRefGoogle Scholar
  10. Beck A, Mayr C (2012) Nitrogen and carbon isotope variability in the green-algal lichen Xanthoria parietina and their implications on mycobiont-photobiont interactions. Ecol Evol 2:3132–3144CrossRefPubMedPubMedCentralGoogle Scholar
  11. Berg A, Danielsson Å, Svensson BH (2013) Transfer of fixed-N from N2-fixing cyanobacteria associated with the moss Sphagnum Riparium results in enhanced growth of the moss. Plant Soil 362:271–278CrossRefGoogle Scholar
  12. Bohuslavová O, Šmilauer P, Elster J (2012) Usnea Lichen community biomass estimation on volcanic mesas, James Ross Island, Antarctica. Polar Biol 35:1563–1572CrossRefGoogle Scholar
  13. Bowker MA, Belnap J (2008) A simple classification of soil types as habitats of biological soil crusts on the Colorado plateau USA. J Veg Sci 19:831–840CrossRefGoogle Scholar
  14. Bowker MA, Belnap J, Davidson DW, Goldstein H (2006) Correlates of biological soil crust abundance across a continuum of spatial scales: support for a hierarchical conceptual model. J Appl Ecol 43:152–163CrossRefGoogle Scholar
  15. Bowker MA, Belnap J, Chaudhary VB, Johnson NC (2008) Revisiting classic water erosion models in drylands: the strong impact of biological soil crusts. Soil Biol Biochem 40:2309–2316CrossRefGoogle Scholar
  16. Bragazza L, Tahvanainen T, Kutnar L, Rydin H, Limpens J, Hájek M, Iacumin P (2004) Nutritional constraints in ombrotrophic sphagnum plants under increasing atmospheric nitrogen deposition in Europe. New Phytol 163:609–616CrossRefGoogle Scholar
  17. Branquinho C, Matos P, Pinho P (2015) Lichens as ecological indicators to track atmospheric changes: future challenges. In: Lindenmayer D, Barton P, Pierson J (eds) Indicators and surrogates of biodiversity and environmental change. CSIRO Publishing, Melbourne, CRC Press, London, pp 77–87Google Scholar
  18. Bremner JM (1996) Nitrogen-total. In: Sparks DL et al (eds) Methods of soil analysis part 3-chemical methods. Soil science Society of America Inc, Madison, pp 1085–1121Google Scholar
  19. Brown DH, Bates JW (1990) Bryophytes and nutrient cycling. Bot J Linn Soc 104:129–147CrossRefGoogle Scholar
  20. Chamizo S, Cantón Y, Rodríguez-Caballero E, Domingo F (2016) Biocrusts positively affect the soil water balance in semiarid ecosystems. Ecohydrology 9:1208–1221CrossRefGoogle Scholar
  21. Colesie C, Scheu S, Green TA, Weber B, Wirth R, Büdel B (2012) The advantage of growing on moss: facilitative effects on photosynthetic performance and growth in the cyanobacterial lichen Peltigera rufescens. Oecologia 169:599–607CrossRefPubMedGoogle Scholar
  22. Combs SM, Nathan MV (1998) Soil organic matter. In: Brown JR (ed) Recommended Chemical Soil Test Procedures for the North Central Region. NCR Research Publication, Columbia, pp 53–58Google Scholar
  23. Concostrina-Zubiri L, Martínez I, Rabasa SG, Escudero A (2014a) The influence of environmental factors on biological soil crust: from a community perspective to a species level approach. J Veg Sci 25:503–513CrossRefGoogle Scholar
  24. Concostrina-Zubiri L, Pescador DS, Martínez I, Escudero A (2014b) Climate and small scale factors determine functional diversity shifts of biological soil crusts in Iberian drylands. Biodivers Conserv 23:1757–1770.  https://doi.org/10.1007/s10531–014–0683-9 CrossRefGoogle Scholar
  25. Concostrina-Zubiri L, Molla I, Velizarova E, Branquinho C (2016) Grazing or Not Grazing: Implications for Ecosystem Services Provided by Biocrusts in Mediterranean Cork Oak Woodlands. Land Degrad Dev.  https://doi.org/10.1002/ldr2573
  26. Cornelissen JHC, Lavorel S, Garnier E, Diaz S, Buchmann N, Gurvich DE, Pausas JG (2003) A handbook of protocols for 15tandardized and easy measurement of plant functional traits worldwide. Aust J Bot 51:335–380CrossRefGoogle Scholar
  27. Cornelissen JH, Lang SI, Soudzilovskaia NA, During HJ (2007) Comparative cryptogam ecology: a review of bryophyte and lichen traits that drive biogeochemistry. Ann Bot 99:987–1001CrossRefPubMedPubMedCentralGoogle Scholar
  28. Cornwell WK, Ackerly DD (2009) Community assembly and shifts in plant trait distributions across an environmental gradient in coastal California. Ecol Monogr 79:109–126CrossRefGoogle Scholar
  29. Craine JM, Elmore AJ, Aidar MP, Bustamante M, Dawson TE, Hobbie EA, Nardoto GB (2009) Global patterns of foliar nitrogen isotopes and their relationships with climate mycorrhizal fungi foliar nutrient concentrations and nitrogen availability. New Phytol 183:980–992CrossRefPubMedGoogle Scholar
  30. Cruz de Carvalho R, Bernardes da Silva A, Soares R, Almeida AM, Coelho AV, Marques da Silva, Branquinho C (2014) Differential proteomics of dehydration and rehydration in bryophytes: evidence towards a common desiccation tolerance mechanism. Plant Cell Environ 37:1499–1515CrossRefPubMedGoogle Scholar
  31. Cruz de Carvalho R, da Silva AB, Branquinho C, da Silva JM (2015) Influence of dehydration rate on cell sucrose and water relations parameters in an inducible desiccation tolerant aquatic bryophyte. Environ Exp Bot 120:18–22CrossRefGoogle Scholar
  32. Cruz de Carvalho R, Catalá M, Branquinho C, Marques da Silva J, Barreno E (2017) Dehydration rate determines the degree of membrane damage and desiccation tolerance in bryophytes. Physiol Plantarum 159:277–289CrossRefGoogle Scholar
  33. Cuna S, Balas G, Hauer E (2007) Effects of natural environmental factors on δ13C of lichens. Isot Environ Health Stud 43:95–104Google Scholar
  34. Dahlman L, Persson J, Palmqvist K, Näsholm T (2004) Organic and inorganic nitrogen uptake in lichens. Planta 219:459–467CrossRefPubMedGoogle Scholar
  35. Dawson TE, Mambelli S, Plamboeck AH, Templer PH, KP T (2002) Stable isotopes in plant ecology. Annu Rev Ecol Syst 33:507–559CrossRefGoogle Scholar
  36. Deane-Coe KK, Sparks JP (2016) Cyanobacteria associations in temperate forest bryophytes revealed by δ15N analysis. J Torrey Bot Soc 143:50–57CrossRefGoogle Scholar
  37. Deane-Coe KK, Mauritz M, Celis G, Salmon V, Crummer KG, Natali SM, Schuur EA (2015) Experimental warming alters productivity and isotopic signatures of tundra mosses. Ecosystems 18:1070–1082CrossRefGoogle Scholar
  38. Delgado V, Ederra A, Santamaría JM (2013) Nitrogen and carbon contents and δ15N and δ13C signatures in six bryophyte species: assessment of long-term deposition changes (1980–2010) in Spanish beech forests. Glob Chang Biol 19:2221–2228CrossRefPubMedGoogle Scholar
  39. Delgado-Baquerizo M, Gallardo A, Covelo F, Prado-Comesaña A, Ochoa V, Maestre FT (2015) Differences in thallus chemistry are related to species-specific effects of biocrust-forming lichens on soil nutrients and microbial communities. Funct Ecol 29:1087–1098CrossRefGoogle Scholar
  40. Dı́az S, Cabido M (2001) Vive la difference: plant functional diversity matters to ecosystem processes. Trends Ecol Evol 16:646–655CrossRefGoogle Scholar
  41. Elbert W, Weber B, Burrows S, Steinkamp J, Büdel B, Andreae MO, Pöschl U (2012) Contribution of cryptogamic covers to the global cycles of carbon and nitrogen. Nat Geosci 5:459–462CrossRefGoogle Scholar
  42. Eldridge DJ, Rosentreter R (1999) Morphological groups: a framework for monitoring microphytic crusts in arid landscapes. J Arid Environ 41:11–25Google Scholar
  43. Ellis CJ, Coppins BJ (2006) Contrasting functional traits maintain lichen epiphyte diversity in response to climate and autogenic succession. J Biogeogr 33:1643–1656CrossRefGoogle Scholar
  44. Ellis CJ, Coppins BJ (2010) Integrating multiple landscape scale drivers in the lichen epiphyte response: climatic setting pollution regime and woodland spatial-temporal structure. Divers Distrib 16:43–52CrossRefGoogle Scholar
  45. Ellis CJ, Crittenden PD, Scrimgeour CM (2004) Soil as a potential source of nitrogen for mat-forming lichens. Can J Bot 82:145–149CrossRefGoogle Scholar
  46. Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annu Rev Plant Phys 40:503–537CrossRefGoogle Scholar
  47. Furr AK, Schofield CL, Grandolfo MC, Hofstader RA, Gutenmann WH, John LES, Lisk DJ (1979) Element content of mosses as possible indicators of air pollution. Arch Environ Con Tox 8:335–343CrossRefGoogle Scholar
  48. Giordani P, Brunialti G, Bacaro G, Nascimbene J (2012) Functional traits of epiphytic lichens as potential indicators of environmental conditions in forest ecosystems. Ecol Indic 18:413–420CrossRefGoogle Scholar
  49. Giordani P, Incerti G, Rizzi G, Rellini I, Nimis PL, Modenesi P (2014) Functional traits of cryptogams in Mediterranean ecosystems are driven by water light and substrate interactions. J Veg Sci 25:778–792CrossRefGoogle Scholar
  50. Hauck M (2010) Ammonium and nitrate tolerance in lichens. Environ Pollut 158:1127–1133CrossRefPubMedGoogle Scholar
  51. Hevia V, Martín-López B, Palomo S, García-Llorente M, Bello F, González JA (2017) Trait-based approaches to analyze links between the drivers of change and ecosystem services: synthesizing existing evidence and future challenges. Ecol Evol.  https://doi.org/10.1002/ece3.2692
  52. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978CrossRefGoogle Scholar
  53. Hill MO, Preston CD, Bosanquet SDS, Roy DB (2007) Bryoatt: Attributes Of British And Irish Mosses, Liverworts And Hornworts. Centre for Ecology & Hydrology, HuntingdonGoogle Scholar
  54. Huckabee JW, Janzen SA (1975) Mercury in moss: derived from the atmosphere or from the substrate? Chemosphere 4:55–60CrossRefGoogle Scholar
  55. IPCC (2007) Climate Change 2007: Synthesis Report, pp 73Google Scholar
  56. IPCC (2014) Climate Change 2014: Synthesis Report Contribution of Working Groups I II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate ChangeGoogle Scholar
  57. Izquieta-Rojano S, Elustondo D, Ederra A, Lasheras E, Santamaría C, Santamaría JM (2016) Pleurochaete Squarrosa (Brid.) Lindb. As an alternative moss species for biomonitoring surveys of heavy metal, nitrogen deposition and δ15N signatures in a Mediterranean area. Ecol Indic 60:1221–1228CrossRefGoogle Scholar
  58. Kappen L, Valladares F (2007) Opportunistic Growth and Desiccation Tolerance: The Ecological Success of Poikilohydrous Autotrophs. In: Pugnaire F, Valladares F (eds) Functional Plant Ecology, 2nd edn. Taylor and Francis, New York, pp 7–65Google Scholar
  59. Kohn MJ (2010) Carbon isotope compositions of terrestrial C3 plants as indicators of (paleo) ecology and (paleo) climate. Proc Natl Acad Sci 107:19691–19695CrossRefPubMedGoogle Scholar
  60. Lakatos M, Hartard B, Máguas C (2007) The stable isotopes δ13C and δ18O of lichens can be used as tracers of microenvironmental carbon and water sources. Terr Ecol 1:77–92CrossRefGoogle Scholar
  61. Larson DW (1981) Differential wetting in some lichens and mosses: the role of morphology. Bryologist 84:1–15CrossRefGoogle Scholar
  62. Lavorel S, Garnier E (2002) Predicting changes in community composition and ecosystem functioning from plant traits: revisiting the holy grail. Funct Ecol 16:545–556CrossRefGoogle Scholar
  63. Lavorel S, McIntyre S, Landsberg J et al (1997) Plant functional classification: from general groups to specific groups based on response to disturbance. Trends Ecol Evol 12:474–478CrossRefPubMedGoogle Scholar
  64. Lee YI, Lim HS, Yoon HI (2009) Carbon and nitrogen isotope composition of vegetation on king George Island maritime. Antarctic. Polar Biol 32:1607–1615CrossRefGoogle Scholar
  65. Liu YR, Delgado-Baquerizo M, Trivedi P, He JZ, Singh BK (2016) Species identity of biocrust-forming lichens drives the response of soil nitrogen cycle to altered precipitation frequency and nitrogen amendment. Soil Biol Biochem 96:128–136CrossRefGoogle Scholar
  66. Liu YR, Delgado-Baquerizo M, Trivedi P, He JZ, Wang JT, Singh BK (2017) Identity of biocrust species and microbial communities drive the response of soil multifunctionality to simulated global change. Soil Biol Biochem 107:208–217CrossRefGoogle Scholar
  67. Löbel S, Dengler J, Hobohm C (2006) Species richness of vascular plants bryophytes and lichens in dry grasslands: the effects of environment landscape structure and competition. Folia Geobot 41:377–393CrossRefGoogle Scholar
  68. Maestre FT, Bowker MA, Cantón Y, Castillo-Monroy AP, Cortina J, Escolar C, Martínez I (2011) Ecology and functional roles of biological soil crusts in semi-arid ecosystems of Spain. J Arid Environ 75:1282–1291CrossRefPubMedPubMedCentralGoogle Scholar
  69. Mallen-Cooper M, Eldridge DJ (2016) Laboratory-based techniques for assessing the functional traits of biocrusts. Plant Soil 406:131–143CrossRefGoogle Scholar
  70. Máguas M, Griffiths H, Ehleringer J, Serodio J (1993) Characterization of photobiont associations in lichens using carbon isotope discrimination techniques. In: Ehleringer JR, Hall AE, Farquhar GD (eds) Stable Isotopes and Plant Water Relations. Academic Press, San Diego, pp 201–212Google Scholar
  71. Marshall JD, Brooks JR, Lajtha K (2007) Sources of variation in the stable isotopic composition of plants. In: Michener J, Lajtha K (eds) Stable isotopes in ecology and environmentalnnn 2nd edn. Blackwell, Oxford, pp 22–60CrossRefGoogle Scholar
  72. Matos P (2016) Development of ecological indicators of climate change based on lichen functional diversity. Universidade de AveiroGoogle Scholar
  73. Matos P, Pinho P, Aragon G, Martínez I, Nunes A, Soares AM, Branquinho C (2015) Lichen traits responding to aridity. J Ecol 103:451–458CrossRefGoogle Scholar
  74. McCune B, Mefford MJ (2011) PC-ORD multivariate analysis of ecological data version 608. MjM Software, Gleneden BeachGoogle Scholar
  75. McCune B, Grace JB, Urban DL (2002) Analysis of ecological communities. MjM software design, Gleneden BeachGoogle Scholar
  76. Ménot G, Burns SJ (2001) Carbon isotopes in ombrogenic peat bog plants as climatic indicators: calibration from an altitudinal transect in Switzerland. Org Geochem 32:233–245CrossRefGoogle Scholar
  77. Michel P, Payton IJ, Lee WG, During HJ (2013) Impact of disturbance on above-ground water storage capacity of bryophytes in New Zealand indigenous tussock grassland ecosystems. N Z J Ecol 37:114–126Google Scholar
  78. Moore H (1974) Isotopic measurement of atmospheric nitrogen compounds. Tellus 26:169–174CrossRefGoogle Scholar
  79. Nimis PL (2016) The Lichens of Italy. A Second Annotated Catalogue. EUT, Trieste, pp 739Google Scholar
  80. Nimis PL, Scheidegger C, Wolseley PA (2002) Monitoring with lichens – monitoring lichens. Kluwer Academic Publisher, NetherlandsGoogle Scholar
  81. Ochoa-Hueso R, Manrique E (2011) Effects of nitrogen deposition and soil fertility on cover and physiology of Cladonia Foliacea (Huds.) Willd., a lichen of biological soil crusts from Mediterranean Spain. Environ Pollut 159:449–457CrossRefPubMedGoogle Scholar
  82. Palmqvist K (2000) Tansley review no 117. New Phytol 148:11–36CrossRefGoogle Scholar
  83. Pietrasiak N, Regus JU, Johansen JR, Lam D, Sachs JL, Santiago LS (2013) Biological soil crust community types differ in key ecological functions. Soil Biol Biochem 65:68–171CrossRefGoogle Scholar
  84. Pinho P, Branquinho C, Cruz C, Tang YS, Dias T, Rosa AP, Máguas C, Martins-Loução MA, Sutton MA (2009) Assessment of critical levels of atmospheric ammonia for lichen diversity in cork-oak woodland Portugal. In: Sutton MA, Reis S, Baker SMH (eds) Atmosheric ammonia. Springer, Berlin, pp 109–119CrossRefGoogle Scholar
  85. Pinho P, Dias T, Cruz C, Sim Tang Y, Sutton MA, Martins-Loução MA, Máguas C, Branquinho C (2011) Using lichen functional diversity to assess the effects of atmospheric ammonia in Mediterranean woodlands. J Appl Ecol 48:1107–1116CrossRefGoogle Scholar
  86. Pinho P, Bergamini A, Carvalho P, Branquinho C, Stofer S, Scheidegger C, Maguas C (2012) Lichen functional groups as ecological indicators of the effects of land-use in Mediterranean ecosystems. Ecol Indic 15:36–42CrossRefGoogle Scholar
  87. Pinho P, Llop E, Ribeiro M, Cruz C, Soares A, Pereira M, Branquinho C (2014) Tools for determining critical levels of atmospheric ammonia under the influence of multiple disturbances. Environ Pollut 18:88–93CrossRefGoogle Scholar
  88. Pinho P, Barros C, Augusto S, Pereira MJ, Máguas C, Branquinho C (2017) Using nitrogen concentration and isotopic composition in lichens to spatially assess the relative contribution of atmospheric nitrogen sources in complex landscapes. Environ Pollut 230:632–638CrossRefPubMedGoogle Scholar
  89. Porada P, Weber B, Elbert W, Pöschl U, Kleidon A (2013) Estimating global carbon uptake by lichens and bryophytes with a process-based model. Biogeosciences 10:6989–6989CrossRefGoogle Scholar
  90. Potzger JE (1939) Microclimate, evaporation stress, and epiphytic mosses. Bryologist 42:53–61CrossRefGoogle Scholar
  91. Proctor MCF, Raven JA, Rice SK (1992) Stable carbon isotope discrimination measurements in sphagnum and other bryophytes: physiological and ecological implications. J Bryol 17:193–202CrossRefGoogle Scholar
  92. R Core Team (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/
  93. Read CF, Duncan DH, Vesk PA, Elith J (2008) Biological soil crust distribution is related to patterns of fragmentation and land use in a dryland agricultural landscape of southern Australia landscape. Landsc Ecol 23:1093–1105CrossRefGoogle Scholar
  94. Read CF, Duncan DH, Vesk PA, Elith J (2014) Biocrust morphogroups provide an effective and rapid assessment tool for drylands. J Appl Ecol 51:1740–1749CrossRefPubMedPubMedCentralGoogle Scholar
  95. Reed SC, Coe KK, Sparks JP, Housman DC, Zelikova TJ, Belnap J (2012) Changes to dryland rainfall result in rapid moss mortality and altered soil fertility. Nat Clim Chang 2:752–755CrossRefGoogle Scholar
  96. Riera P (2005) δ13C and δ15N comparisons among different co-occurring lichen species from littoral rocky substrata. Lichenologist 37:93–95CrossRefGoogle Scholar
  97. Rosso A, Neitlich P, Smith RJ (2014) Non-destructive lichen biomass estimation in Northwestern Alaska: a comparison of methods. PloS ONE 9:e103739Google Scholar
  98. Royles J, Horwath AB, Griffiths H (2014) Interpreting bryophyte stable carbon isotope composition: plants as temporal and spatial climate recorders. Geochem Geophys Geosyst 15:1462–1475CrossRefGoogle Scholar
  99. Royles J, Amesbury MJ, Roland TP, Jones GD, Convey P, Griffiths H, Charman DJ (2016) Moss stable isotopes (carbon-13 oxygen-18) and testate amoebae reflect environmental inputs and microclimate along a latitudinal gradient on the Antarctic peninsula. Oecologia 181:931–945CrossRefPubMedPubMedCentralGoogle Scholar
  100. Rundel PW, Stichler W, Zander RH, Ziegler H (1979) Carbon and hydrogen isotope ratios of bryophytes from arid and humid regions. Oecologia 44:91–94CrossRefPubMedGoogle Scholar
  101. Shomer-Ilan A, Nissenbaum A, Galun M, Waisel Y (1979) Effect of water regime on carbon isotope composition of lichens. Plant Physiol 63:201–205CrossRefPubMedPubMedCentralGoogle Scholar
  102. Solga A, Burkhardt J, Zechmeister HG, Frahm JP (2005) Nitrogen content 15N natural abundance and biomass of the two pleurocarpous mosses Pleurozium schreberi (Brid) mitt and Scleropodium purum (Hedw) Limpr in relation to atmospheric nitrogen deposition. Environ Pollut 134:465–473CrossRefPubMedGoogle Scholar
  103. Stark LR, Greenwood JL, Brinda JC, Oliver MJ (2013) The desert moss Pterygoneurum lamellatum (Pottiaceae) exhibits an inducible ecological strategy of desiccation tolerance: effects of rate of drying on shoot damage and regeneration. Am J Bot 100:1522–1531CrossRefPubMedGoogle Scholar
  104. Suding KN, Lavorel S, Chapin FS, Cornelissen JH, Diaz S, Garnier E, Navas ML (2008) Scaling environmental change through the community-level: a trait-based response-and-effect framework for plants. Glob Chang Biol 14:1125–1140CrossRefGoogle Scholar
  105. Teeri JA (1981) Stable carbon isotope analysis of mosses and lichens growing in xeric and moist habitats. Bryologist 84:82–84CrossRefGoogle Scholar
  106. Tilman D, Knops J, Wedin D, Reich P, Ritchie M, Siemann E (1997) The influence of functional diversity and composition on ecosystem processes. Science 277:1300–1302CrossRefGoogle Scholar
  107. van den Driessche R (1979) Proceedings. Forest Fertilization Conference, University of Washington, WA, USAGoogle Scholar
  108. Verheyen K, Honnay O, Motzkin G, Hermy M, Foster DR (2003) Response of forest plant species to land-use change: a life-history trait-based approach. J Ecol 91:563–577CrossRefGoogle Scholar
  109. Williams TG, Flanagan LB (1996) Effect of changes in water content on photosynthesis transpiration and discrimination against 13CO2 and C18O16O in Pleurozium and sphagnum. Oecologia 108:38–46CrossRefPubMedGoogle Scholar
  110. Xiao B, Hu K, Ren T, Li B (2016) Moss-dominated biological soil crusts significantly influence soil moisture and temperature regimes in semiarid ecosystems. Geoderma 263:35–46Google Scholar
  111. Zelikova TJ, Housman DC, Grote ED, Neher D, Belnap J (2012) Biological soil crusts show limited response to warming but larger response to increased precipitation frequency: implications for soil processes on the Colorado plateau. Plant Soil 355:265–282CrossRefGoogle Scholar
  112. Zomer RJ, Trabucco A, Bossio DA, van Straaten O, Verchot LV (2008) Climate change mitigation: a spatial analysis of global land suitability for clean development mechanism afforestation and reforestation. Agric Ecosyst Environ 126:67–80CrossRefGoogle Scholar
  113. Zwolicki A, Zmudczyńska-Skarbek K, Richard P, Stempniewicz L (2016) Importance of marine-derived nutrients supplied by planktivorous seabirds to high Arctic tundra plant communities. PLoS ONE 11:e0154950Google Scholar

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© Springer International Publishing AG, part of Springer Nature 2017

Authors and Affiliations

  1. 1.Centre for Ecology, Evolution and Environmental Changes (cE3c)Faculdade de Ciências, Universidade de LisboaLisbonPortugal
  2. 2.Dipartimento di FarmaciaUniversità degli Studi di GenovaGenovaItaly

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