Biodiversity and Conservation

, Volume 23, Issue 7, pp 1757–1770 | Cite as

Climate and small scale factors determine functional diversity shifts of biological soil crusts in Iberian drylands

  • Laura Concostrina-Zubiri
  • David S. Pescador
  • Isabel Martínez
  • Adrián Escudero
Original Paper


Understanding functional diversity is critical to manage and preserve biodiversity and ecosystem functioning in the face of global change. However, the efforts to characterize this functional component have been mostly directed to vascular vegetation. We sampled lichen-dominated biological soil crusts (BSCs) in semiarid grasslands along an environmental gradient in the Iberian Peninsula. We characterized five effect functional traits for 31 lichens species, and evaluated the influence of large scale (i.e. precipitation) and small scale factors (i.e. substrate type, shrub presence, Stipa tenacissima presence) on dominant trait values; i.e. community weighted means, and functional divergence; i.e. Rao quadratic entropy in 580 sampling quadrats. Across the gradient, we found multiple trait shifts and a general increase of functional divergence with increasing precipitation. We also observed that substrate type and small scale biotic factors determined shifts in all traits studied, while these factors affected less to functional divergence. Comparing functional diversity with taxonomic diversity, we found contrasting responses to both large and small scale factors. These findings suggest that BSC community trait composition is influenced by multi-scale abiotic and biotic factors with environmental filtering dominating at large spatial scales and limiting similarity at specific small scales. Also, our results emphasize the potential differences between taxonomic and functional diversity in response to environmental factors. We concluded that functional diversity of BSCs not only provides novel and critical knowledge of BSC community structure, but also it should be considered as a critical tool in biodiversity conservation strategies, ecosystem services assessment and ecological modelling.


Biological soil crusts Calcareous soils Functional diversity Gypsum soil Lichen Precipitation Semiarid grassland Shrub Stipa tenacissima Traits 



This work was partially supported by the Spanish Ministry of Economy and Competitiveness (Mountains: CGL2012-38427), the Ministry of Science and Innovation (project EPICON: CGL2010-22049/BOS) and the Government of Autonomous Region of Madrid (REMEDINAL2).


  1. Austin AT, Yahdjian L, Stark JM, Belnap J, Porporato A, Norton U, Ravetta D, Schaeffer SM (2003) Water pulses and biogeochemical cycles in arid and semiarid ecosystems. Oecologia 141:221–235Google Scholar
  2. Bates D, Maechler M, Bolker B (2012) lme4: linear mixed-effects models using S4classes.
  3. Belnap J (2006) The potential roles of biological soil crusts in dryland hydrologic cycles. Hydrol Process 20:3159–3178Google Scholar
  4. Belnap J, Lange OL (2003) Biological soil crusts: structure, function, and management. Springer, BerlinCrossRefGoogle Scholar
  5. Botta-Dukát Z (2005) Rao’s quadratic entropy as a measure of functional diversity based on multiple traits. J Veg Sci 16:533–540CrossRefGoogle Scholar
  6. Bowker M, 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
  7. Bowker MA, Maestre FT, Escolar C (2010a) Biological crusts as model system for examining the biodiversity-ecosystem function relationship in soils. Soil Biol Biochem 42:405–417CrossRefGoogle Scholar
  8. Bowker MA, Soliveres S, Maestre FT (2010b) Competition increases with abiotic stress and regulates the diversity of biological soil crusts. J Ecol 98:551–560CrossRefGoogle Scholar
  9. Bowker MA, Maestre FT, Mau RL (2013) Diversity and patch-size distributions of biological soil crusts regulate dryland ecosystem multifunctionality. Ecosystems 16:1–11Google Scholar
  10. Chaudhary VB, Bowker MA, O’Dell TE, Grace JB, Redman AE, Rillig MC, Johnson NC (2009) Untangling the biological contributions to soil stability in semiarid shrublands. Ecol Appl 19:110–122PubMedCrossRefGoogle Scholar
  11. Chave J, Coomes D, Jansen S, Lewis SL, Swenson NG, Zanne AE (2009) Towards a worldwide wood economics spectrum. Ecol Lett 12:351–366PubMedCrossRefGoogle Scholar
  12. Concostrina-Zubiri L, Martínez I, Rabasa SG, Escudero A (2013a) The influence of environmental factors on biological soil crust: from a community perspective to a species level approach. J Veg Sci. doi: 10.1111/jvs.12084 Google Scholar
  13. Concostrina-Zubiri L, Huber-Sannwald E, Martínez I, Flores Flores JL, Escudero A (2013b) Biological soil crusts greatly contribute to small-scale soil heterogeneity along a grazing gradient. Soil Biol Biochem 64:28–36CrossRefGoogle Scholar
  14. Cornelissen J, Lavorel S, Garnier E et al (2003) A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Aust J Bot 51:335–380CrossRefGoogle Scholar
  15. Cornelissen JHC, Lang SI, Soudzilovskaia NA, During HJ (2007) Comparative cryptogam ecology: a review of bryophyte and lichen traits that drive biogeochemistry. Ann Bot 99:987–1001PubMedCentralPubMedCrossRefGoogle Scholar
  16. 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
  17. Cornwell WK, Schwilk DW, Ackerly DD (2006) A trait-based test for habitat filtering: convex hull volume. Ecology 87:1465–1471PubMedCrossRefGoogle Scholar
  18. Darby BJ, Neher DA, Belnap J (2010) Impact of biological soil crusts and desert plants on soil microfaunal community composition. Plant Soil 328:421–431CrossRefGoogle Scholar
  19. de Bello F, Lavorel S, Díaz S, Harrington R, Cornelissen JHC et al (2010a) Towards an assessment of multiple ecosystem processes and services via functional traits. Biodivers Conserv 19:2873–2893CrossRefGoogle Scholar
  20. de Bello F, Lavergne S, Meynard CN, Lepš J, Thuiller W (2010b) The partitioning of diversity: showing Theseus a way out of the labyrinth. J Veg Sci 21:992–1000CrossRefGoogle Scholar
  21. de Bello F, Lavorel S, Lavergne S, Albert CH, Boulangeat I et al (2013) Hierarchical effects of environmental filters on the functional structure of plant communities: a case study in the French Alps. Ecography 36:393–402CrossRefGoogle Scholar
  22. Delgado-Baquerizo M, Maestre FT, Gallardo A (2013) Biological soil crusts increase the resistance of soil nitrogen dynamics to changes in temperatures in a semi-arid ecosystem. Plant Soil 366:35–47CrossRefGoogle Scholar
  23. Dias AT, Berg MP, de Bello F, Oosten AR, Bíla K, Moretti M (2012) An experimental framework to identify community functional components driving ecosystem processes and services delivery. J Ecol 101:29–37CrossRefGoogle Scholar
  24. Díaz S, Lavorel S, de Bello F, Quétier F, Grigulis K, Robson TM (2007) Incorporating plant functional diversity effects in ecosystem service assessments. PNAS 104:20684–20689PubMedCentralPubMedCrossRefGoogle Scholar
  25. Elbert W, Weber B, Burrows S, Steinkamp J, Büdel B et al (2012) Contribution of cryptogamic covers to the global cycles of carbon and nitrogen. Nat Geosci 5:459–462CrossRefGoogle Scholar
  26. Eldridge DJ, Greene RSB (1994) Microbiotic soil crusts: a review of their roles in soil and ecological processes in the rangelands of Australia. Aust J Soil Res 32:389–415Google Scholar
  27. Eldridge DJ, Rosentreter R (1999) Morphological groups: a framework for monitoring microphytic crusts in arid landscapes. J Arid Environ 41:11–25Google Scholar
  28. Eldridge DJ, Tozer ME (1997) Environmental factors relating to the distribution of terricolous bryophytes and lichens in semi-arid eastern Australia. Bryologist 100:28–39Google Scholar
  29. 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
  30. Escolar C, Martinez I, Bowker MA, Maestre FT (2012) Warming reduces the growth and diversity of biological soil crusts in a semi-arid environment: implications for ecosystem structure and functioning. Philos Trans R Soc B 367:3087–3099CrossRefGoogle Scholar
  31. Escudero A, Martínez I, de la Cruz A, Otálora M, Maestre FT (2007) Soil lichens have species-specific effects on the seedling emergence of three gypsophile plant species. J Arid Environ 70:18–28CrossRefGoogle Scholar
  32. Garnier E, Cortez J, Billès G, Navas ML, Roumet C et al (2004) Plant functional markers capture ecosystem properties during secondary succession. Ecology 85:2630–2637CrossRefGoogle Scholar
  33. Garnier E, Lavorel S, Ansquer P, Castro H, Cruz P et al (2007) Assessing the effects of land-use change on plant traits, communities and ecosystem functioning in grasslands: a standardized methodology and lessons from an application to 11 European sites. Ann Bot 99:967–985PubMedCentralPubMedCrossRefGoogle Scholar
  34. Giordani P, Brunialti G, Bacaro G, Nascimben J (2012) Functional traits of epiphytic lichens as potential indicators of environmental conditions in forest ecosystems. Eco Indic 18:413–420CrossRefGoogle Scholar
  35. Giordani P, Incerti G, Rizzi G, Rellini I, Nimis PL, Modenesi P (2013) Functional traits of cryptogams in Mediterranean ecosystems are driven by water, light and substrate interactions. J Veg Sci. doi: 10.1111/jvs.12119 Google Scholar
  36. Harper KT, Belnap J (2001) The influence of biological soil crusts on mineral uptake by associated vascular plants. J Arid Environ 47:347–357CrossRefGoogle Scholar
  37. Hauck M, Jürgens SR, Willenbruch K, Huneck S, Leuschner C (2009) Dissociation and metal-binding characteristics of yellow lichen substances suggest a relationship with site preferences of lichens. Ann Bot 103:13–22 Google Scholar
  38. Jiménez Aguilar A, Huber–Sannwald E, Belnap J, Smart DR, Moreno JTA (2009) Biological soil crusts exhibit a dynamic response to seasonal rain and release from grazing with implications for soil stability. J Arid Environ 73:1158–1169Google Scholar
  39. Karnieli A, Kokaly RF, West NE, Clark RN (2003) Remote sensing of biological soil crusts. In: Belnap J, Lange OL (eds) Biological soil crusts, structure, function, and management, 2nd edn. Springer, Berlin, pp 431–455Google Scholar
  40. Lakatos M, Rascher U, Büdel B (2006) Functional characteristics of corticolous lichens in the understory of a tropical lowland rain forest. New Phytol 172:679–695PubMedCrossRefGoogle Scholar
  41. Laliberté E, Legendre P (2010) A distance-based framework for measuring functional diversity from multiple traits. Ecology 91:299–305PubMedCrossRefGoogle Scholar
  42. Lalley JS, Viles HA (2005) Terricolous lichens in the northern Namib Desert of Namibia: distribution and community composition. Lichenol 37:77–92CrossRefGoogle Scholar
  43. Lavorel S, Grigulis K, McIntyre S et al (2008) Assessing functional diversity in the field-methodology matters! Funct Ecol 22:134–147Google Scholar
  44. Loreau M, Mouquet N, Gonzalez A (2003) Biodiversity as spatial insurance in heterogeneous landscapes. PNAS 100:12765–12770PubMedCentralPubMedCrossRefGoogle Scholar
  45. MA (Millennium Ecosystem Assessment) (2005) Ecosystems and human well-being: desertification synthesis. Island Press, Washington, DCGoogle Scholar
  46. Maestre FT, Escolar C, Martínez I, Escudero A (2008) Are soil lichen communities structured by biotic interactions? A null model analysis. J Veg Sci 19:261–266CrossRefGoogle Scholar
  47. Maestre FT, Bowker MA, Puche MD, Hinojosa MB, Martínez I et al (2009) Shrub encroachment can reverse desertification in semi-arid Mediterranean grasslands. Ecol Lett 12:930–941PubMedCrossRefGoogle Scholar
  48. Malam Issa O, Défarge C, Trichet J, Valentin C, Rajot JL (2009) Microbiotic soil crusts in the Sahel of Western Niger and their influence on soil porosity and water dynamics. Catena 77:48–55CrossRefGoogle Scholar
  49. Martínez I, Escudero A, Maestre FT, de la Cruz A, Guerrero C, Rubio A (2006) Small-scale patterns of abundance of mosses and lichens forming biological soil crusts in two semi-arid gypsum environments. Aust J Bot 54:339–348CrossRefGoogle Scholar
  50. Mason NW, Bello F, Mouillot D, Pavoine S, Dray S (2012) A guide for using functional diversity indices to reveal changes in assembly processes along ecological gradients. J Veg Sci 24:794–806CrossRefGoogle Scholar
  51. Mason NW, Mouillot D, Lee WG, Wilson JB (2005) Functional richness, functional evenness and functional divergence: the primary components of functional diversity. Oikos 111:112–118Google Scholar
  52. McCulloch CE, Searle SR (2001) Generalized linear mixed models (GLMMs). In: McCulloch CE, Searle SR, Neuhaus JM (eds) Generalized, linear, and mixed models, 2nd edn. Wiley, New York, pp 220–246Google Scholar
  53. Miller ME, Belote RT, Bowker MA, Garman S (2011) Alternative states of a semiarid grassland ecosystem: Implications for ecosystem services. Ecosphere 5: art55Google Scholar
  54. Mokany K, Ash J, Roxburgh S (2008) Functional identity is more important than diversity in influencing ecosystem processes in a temperate native grassland. J Ecol 96:884–893CrossRefGoogle Scholar
  55. Molnár K, Farkas E (2010) Current results on biological activities of lichen secondary metabolites: a review. Z Naturforsch C 65:157–173Google Scholar
  56. Mouchet MA, Villéger S, Mason NWH, Mouillot D (2010) Functional diversity measures: an overview of their redundancy and their ability to discriminate community assembly rules. Funct Ecol 24:867–876CrossRefGoogle Scholar
  57. Nash TH (2008) Lichen Biology. Cambridge University Press, CambridgeGoogle Scholar
  58. Nimis PL, Martellos S (2004) Keys to the lichens of Italy I. Terricolous species. Edizioni Goliardiche. Trieste, ItalyGoogle Scholar
  59. Nimis PL, Martellos S (2008) ITALICA. The information system on Italian lichens. Version 4.0. Accessed 24 June 2013
  60. Ochoa–Hueso R, Hernandez RR, Pueyo JJ, 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 Biol Biochem 43:1894–1901Google Scholar
  61. Palmqvist K, Sundberg B (2000) Light use efficiency of dry matter gain in five macro-lichens: relative impact of microclimate conditions and species-specific traits. Plant Cell Environ 23:1–14CrossRefGoogle Scholar
  62. Paoli L, Pisani T, Munzi S, Gaggi C, Loppi S (2010) Influence of sun irradiance and water availability on lichen photosynthetic pigments during a Mediterranean summer. Biologia 65:776–783CrossRefGoogle Scholar
  63. Pérez-Harguindeguy N, Díaz S, Garnier E, Lavorel S, Poorter H et al (2013) New handbook for standardised measurement of plant functional traits worldwide. Aust J Bot 61:167–234Google Scholar
  64. Petchey OL, Gaston KJ (2002) Functional diversity (FD), species richness and community composition. Ecol Lett 5:402–411CrossRefGoogle Scholar
  65. Petchey OL, Gaston KJ (2006) Functional diversity: back to basics and looking forward. Ecol Lett 9:741–758Google Scholar
  66. Pinho P, Bergamini A, Carvalho P, Branquinho C, Stofer S et al (2011a) Lichen functional groups as ecological indicators of the effects of low-intensity land-use in Mediterranean ecosystems. Ecol Indic 15:36–42CrossRefGoogle Scholar
  67. Pinho P, Dias T, Cruz CC, Tang YS, Sutton M et al (2011b) Using lichen functional-diversity to assess the effects of atmospheric ammonia in Mediterranean woodlands. J Appl Ecol 48:1107–1116CrossRefGoogle Scholar
  68. Prieto M, Aragón G, Martínez I (2010a) The genus Catapyrenium s. lat. (Verrucariaceae) in the Iberian Peninsula and the Balearic Islands. Lichenol 42:637–684CrossRefGoogle Scholar
  69. Prieto M, Martínez I, Aragón G (2010b) The genus Placidiopsis in the Iberian Peninsula and the Balearic Islands. Mycotaxon 114:463–472CrossRefGoogle Scholar
  70. R Development Core Team (2010) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  71. Rao CR (1982) Diversity and dissimilarity coefficients: a unified approach. Theor Popul Biol 21:24–43CrossRefGoogle Scholar
  72. Ricotta C, Moretti M (2011) CWM and Rao’s quadratic diversity: a unified framework for functional ecology. Oecologia 167:181–188Google Scholar
  73. Spasojevic MJ, Suding KN (2012) Inferring community assembly mechanisms from functional diversity patterns: the importance of multiple assembly processes. J Ecol 100:652–661CrossRefGoogle Scholar
  74. Stofer S, Bergamini A, Aragón G, Carvalho P, Coppins BJ et al (2006) Species richness of lichen functional groups in relation to land use intensity. Lichenol 38:331–353CrossRefGoogle Scholar
  75. Stubbs WJ, Wilson JB (2004) Evidence for limiting similarity in a sand dune community. J Ecol 92:557–567CrossRefGoogle Scholar
  76. Villéger S, Mason NW, Mouillot D (2008) New multidimensional functional diversity indices for a multifaceted framework in functional ecology. Ecology 89:2290–2301PubMedCrossRefGoogle Scholar
  77. Violle C, Navas ML, Vile D, Kazakou E, Fortunel C et al (2007) Let the concept of trait be functional! Oikos 116:882–892CrossRefGoogle Scholar
  78. Warren SD (2003) Synopsis: influence of biological soil crusts on arid land hydrology and soil stability. In: Belnap J, Lange OL (eds) Biological soil crusts: structure, function, and management. Springer, Berlin, pp 349–360Google Scholar
  79. Weiher E, Keddy P (2001) Ecological assembly rules: perspectives, advances, retreats. Cambridge University Press, CambridgeGoogle Scholar
  80. West NE (1990) Structure and function of microphytic soil crusts in wildland ecosystems of arid to semi-arid regions. In: Begon M (ed) Advances in ecological research. Academic Press, New York, pp 179–223 CrossRefGoogle Scholar
  81. Zedda L, Grongroft A, Schultz M, Petersen A, Mills A, Rambold G (2011) Distribution patterns of soil lichens across the principal biomes of southern Africa. J Arid Environ 75:215–220 Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Laura Concostrina-Zubiri
    • 1
  • David S. Pescador
    • 1
  • Isabel Martínez
    • 1
  • Adrián Escudero
    • 1
  1. 1.Department of Biology and GeologyRey Juan Carlos UniversityMóstolesSpain

Personalised recommendations