, Volume 16, Issue 7, pp 1248–1261 | Cite as

On the Importance of Shrub Encroachment by Sprouters, Climate, Species Richness and Anthropic Factors for Ecosystem Multifunctionality in Semi-arid Mediterranean Ecosystems

  • José L. Quero
  • Fernando T. Maestre
  • Victoria Ochoa
  • Miguel García-Gómez
  • Manuel Delgado-Baquerizo


One of the most important changes taking place in drylands worldwide is the increase of the cover and dominance of shrubs in areas formerly devoid of them (shrub encroachment). A large body of research has evaluated the causes and consequences of shrub encroachment for both ecosystem structure and functioning. However, there are virtually no studies evaluating how shrub encroachment affects the ability of ecosystems to maintain multiple functions and services simultaneously (multifunctionality). We aimed to do so by gathering data from ten ecosystem functions linked to the maintenance of primary production and nutrient cycling and storage (organic C, activity of β-glucosidase, pentoses, hexoses, total N, total available N, amino acids, proteins, available inorganic P, and phosphatase activity), and summarizing them in a multifunctionality index (M). We assessed how climate, species richness, anthropic factors (distance to the nearest town, sandy and asphalted road, and human population in the nearest town at several historical periods) and encroachment by sprouting shrubs impacted both the functions in isolation and M along a regional (ca. 350 km) gradient in Mediterranean grasslands and shrublands dominated by a non-sprouting shrub. Values of M were higher in those grasslands and shrublands containing sprouting shrubs (43 and 62%, respectively). A similar response was found when analyzing the different functions in isolation, as encroachment by sprouting shrubs increased functions by 2–80% compared to unencroached areas. Encroachment was the main driver of changes in M along the regional gradient evaluated, followed by anthropic factors and species richness. Climate had little effects on M in comparison to the other factors studied. Similar responses were observed when evaluating the functions in isolation. Overall, our results showed that M was higher at sites with higher sprouting shrub cover, longer distance to roads and higher perennial plant species richness. Our study is the first documenting that ecosystem multifunctionality in shrublands is enhanced by encroaching shrubs differing in size and leaf attributes. Our findings reinforce the idea that encroachment effects on ecosystem functioning cannot be generalized, and that are largely dependent on the traits of the encroaching shrub relative to those of the species being replaced.


shrub invasion ecosystem structure ecosystem functioning biodiversity drylands Quercus coccifera Rosmarinus officinalis Stipa tenacissima 

Supplementary material

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Supplementary material 1 (DOC 8041 kb)


  1. Alberti G, Leronni V, Piazzi M. 2011. Impact of woody encroachment on soil organic carbon and nitrogen in abandoned agricultural lands along a rainfall gradient in Italy. Reg Environ Change 11:917–24.CrossRefGoogle Scholar
  2. Archer SR, Schimel DS, Holland EH. 1995. Mechanisms of shrubland expansion: land use, climate or CO2. Clim Chang 29:91–9.CrossRefGoogle Scholar
  3. Azcón-Aguilar C, Palenzuela J, Roldán A, Bautista S, Vallejo R, Barea JM. 2003. Analysis of the mycorrhizal potential in the rhizosphere of representative plant species from desertification-threatened Mediterranean shrublands. Appl Soil Ecol 22:29–37.CrossRefGoogle Scholar
  4. Bastida F, Moreno JL, Hernández T, García C. 2006. Microbiological activity in a soil 15 years after its devegetation. Soil Biol Biochem 38:2503–7.CrossRefGoogle Scholar
  5. Belkhir S, Koubaa A, Khadhri A, Ksontini M, Smiti S. 2012. Variations in the morphological characteristics of Stipa tenacissima fiber: the case of Tunisia. Ind Crop Prod 37:200–6.CrossRefGoogle Scholar
  6. Bessadok A, Marais S, Gouanve F, Colasse L, Zimmerlin I, Roudesli S, Metayer M. 2007. Effect of chemical treatments of Alfa (Stipa tenacissima) fibres on water-sorption properties. Compos Sci Technol 67:685–97.CrossRefGoogle Scholar
  7. Blanca G. 2011. Cabezudo B, Cueto M, Fernandez Lopez C, Morales Torres C. (eds). Flora Vascular de Andalucía oriental. (2a edición corregida y aumentada). Consejería de medio Ambiente, Junta de Andalucía. Sevilla.Google Scholar
  8. Blondel A. 2006. The ‘Design’ of Mediterranean landscapes: a millennial story of humans and ecological systems during the historic period. Hum Ecol 34:713–29.CrossRefGoogle Scholar
  9. Bochet E, Rubio JL, Poesen J. 1998. Relative efficiency of three representative matorral species in reducing water erosion at the microscale in a semi-arid climate (Valencia, Spain). Geomorphology 23:139–50.CrossRefGoogle Scholar
  10. Bochet E, Rubio JL, Poesen J. 1999. Modified topsoil islands within patchy Mediterranean vegetation in SE Spain. Catena 38:23–44.CrossRefGoogle Scholar
  11. Bonfil C. 1998. The effects of seed size, cotyledon reserves and herbivory on seedling survival and growth in Quercus rugosa and Quercus laurina (Fagaceae). Am J Botany 85:79–87.CrossRefGoogle Scholar
  12. Bowker MA, Maestre FT, Mau RL. 2013. Diversity and patch-size distributions of biological soil crusts regulate dryland ecosystem multifunctionality. Ecosystems. doi:10.1007/s10021-013-9644-5.
  13. Burnham KP, Anderson DR. 2002. Model selection and multimodel inference: a practical information-theoretical approach. New York: Springer.Google Scholar
  14. Cable JM, Ogle K, Tyler A. 2009. Woody plant encroachment impacts on soil carbon and microbial processes: results from a hierarchical Bayesian analysis of soil incubation data. Plant Soil 320:153–67.CrossRefGoogle Scholar
  15. Cabral AC, De Miguel JM, Rescia JAJ, Schmitz MF, Pineda FD. 2003. Shrub encroachment in Argentinean savannas. J Veg Sci 14: 145–152. Cambridge: Cambridge University Press.Google Scholar
  16. Calef MP, McGuire AD, Chapin FSIII. 2008. Human influences on wildfire in Alaska from 1988 through 2005: an analysis of the spatial patterns of human impacts. Earth Interact 12:1–17.CrossRefGoogle Scholar
  17. Cañellas I, Miguel AS. 1998. Litter fall and nutrient turnover in Kermes oak (Quercus coccifera L.) shrublands in Valencia (eastern Spain). Ann Sci For 55:589–97.CrossRefGoogle Scholar
  18. Cañellas I, Miguel AS. 2000. Biomass of root and shoot systems of Quercus coccifera shrublands in Eastern Spain. Ann For Sci 57:803–10.CrossRefGoogle Scholar
  19. Cardinale BJ, Matulich KL, Hooper DU, Byrnes JE, Duffy E, Gamfeldt L, Balvanera P, O’Connor MI, Gonzalez A. 2011. The functional role of producer diversity in ecosystems. Am J Bot 98:572–92.PubMedCrossRefGoogle Scholar
  20. Castillo-Monroy AP, Maestre FT, Delgado-Baquerizo M, Gallardo A. 2010. Biological soil crusts modulate nitrogen availability in semi-arid ecosystems: insights from a Mediterranean grassland. Plant Soil 333:21–34.CrossRefGoogle Scholar
  21. Chatterjee S, Price B. 2001. Regression analysis by example. 2nd edn. New York: Wiley.Google Scholar
  22. Daryanto S, Eldridge DJ. 2010. Plant and soil surface responses to a combination of shrub removal and grazing in a shrub-encroached woodland. J Environ Manage 91:2639–2648.Google Scholar
  23. De Schrijver A, Vesterdal L, Hansen K, De Frenne P, Augusto L, Achat DL, Staelens J, Baeten L, De Keersmaeker L, De Neve S, Verheyen K. 2012. Four decades of post-agricultural forest development have caused major redistributions of soil phosphorus fractions. Oecologia 169:221–34.PubMedCrossRefGoogle Scholar
  24. di Castri F. 1981. Mediterranean-type shrublands of the world. In: Di Castri F et al., Eds. Mediterranean-type shrublands. Amsterdam: Elsevier. p 1–52.Google Scholar
  25. Dickie IA, Yeates GW, St. John MG, Stevenson BA, Scott JT, Rillig MC, Peltzer DA, Orwin KH, Kirschbaum M, Hunt JE, Burrows LE, Barbour MM, Aislabie J. 2011. Ecosystem service and biodiversity trade-offs in two woody successions. J Appl Ecol 48: 926–934.Google Scholar
  26. Dupouey JL, Dambrine E, Laffite D, Moares C. 2002. Irreversible impact of past land use on forest soils and biodiversity. Ecology 83:2894–978.CrossRefGoogle Scholar
  27. Eldridge DJ, Bowker MA, Maestre FT, Roger E, Reynolds JF, Whitford WG. 2011. Impacts of shrub encroachment on ecosystem structure and functioning: towards a global síntesis. Ecol Lett 14:709–22.PubMedCrossRefGoogle Scholar
  28. Ferran A, Delitti W, Vallejo VR. 2005. Effects of fire recurrence in Quercus coccifera L. shrublands of the Valencia region (Spain): II plant and soil nutrients. Plant Ecol 177:71–83.CrossRefGoogle Scholar
  29. Freudenberger L, Hobson PR, Schluck M, Ibisch PL. 2012. A global map of the functionality of terrestrial ecosystems. Ecol Complex 12:13–22.CrossRefGoogle Scholar
  30. Gamfeldt L, Hillebrand H, Jonsson PR. 2008. Multiple functions increase the importance of biodiversity for overall ecosystem functioning. Ecology 89:1223–31.PubMedCrossRefGoogle Scholar
  31. Gamfeldt L, Snall T, Bagchi R, Jonsson M, Gustafsson L, Kjellander P, Ruiz-Jaen MC, Fröberg M, Stendahl J, Philipson CD, Mikusinski G, Andersson E, Westerlund B, Andrén H, Moberg F, Moen J, Bengtsson J. 2013. Higher levels of multiple ecosystem services are found in forests with more tree species. Nat Commun 4: 1340.Google Scholar
  32. García C, Roldán A, Hernández T. 2005. Ability of different plant species to promote microbiological processes in semiarid soil. Geoderma 124:193–202.CrossRefGoogle Scholar
  33. García D, Martínez D. 2012. Species richness matters for the quality of ecosystem services: a test using seed dispersal by frugivorous birds. Proc R Soc Lond B 279:3106–13.CrossRefGoogle Scholar
  34. García-Fayos P, Bochet E. 2009. Indication of antagonistic interaction between climate change and erosion on plant species richness and soil properties in semiarid Mediterranean ecosystems. Glob Chang Biol 15:306–18.CrossRefGoogle Scholar
  35. Gómez JM. 2003. Spatial patterns in long-distance dispersal of Quercus ilex acorns by jays in a heterogeneous landscape. Ecography 26:573–84.CrossRefGoogle Scholar
  36. Hector A, Bagchi R. 2007. Biodiversity and ecosystem multifunctionality. Nature 448:188–90.PubMedCrossRefGoogle Scholar
  37. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A. 2005. Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–78.CrossRefGoogle Scholar
  38. Hoeting JA, Davis RA, Merton AA, Thompson SE. 2006. Model selection for geostatistical models. Ecol Appl 16:87–98.PubMedCrossRefGoogle Scholar
  39. Hooper DU, Carol E, Cardinale BJ, Byrnes JEK, Hungate BA, Matulich KL, Gonzalez A, Emmett J, Gamfeldt L, O’Connor M. 2012. A global synthesis reveals biodiversity loss as a major driver of ecosystem change. Nature 486:105–8.PubMedGoogle Scholar
  40. Hooper DU, Chapin III FS, Ewel JJ, Hector A, Inchausti P, Lavorel S, Lawton JH, Lodge DM, Loreau M, Naeem S, Schmid B, Setälä H, Symstad AJ, Vandermeer J, Wardle DA. 2005. Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monogr 75: 3–35.Google Scholar
  41. Hooper DU, Vitousek PM. 1998. Effects of plant composition and diversity on nutrient cycling. Ecol Monogr 68:121–49.CrossRefGoogle Scholar
  42. Huenneke LF, Anderson JP, Remmenga M, Schlesinger WH. 2002. Desertification alters patterns of aboveground net primary production in Chihuahuan ecosystems. Glob Chang Biol 8:247–64.CrossRefGoogle Scholar
  43. Jackson RB, Banner JL, Jobbagy EG, Pockman WT, Wall DH. 2002. Ecosystem carbon loss with woody plant invasion of grasslands. Nature 418:623–6.PubMedCrossRefGoogle Scholar
  44. Johnson JB, Omland KS. 2004. Model selection in ecology and evolution. Trends Ecol Evol 19:101–8.PubMedCrossRefGoogle Scholar
  45. Kacalek D, Dusek D, Novak J, Slodicak M, Bartos J, Cernohous V, Balcar V. 2011. Former agriculture impacts on properties of Norway spruce forest floor and soil. For Syst 20:437–43.Google Scholar
  46. Kier G, Mutke J, Dinerstein E, Ricketts TH, Küper W, Kreft H, Barthlott W. 2005. Global patterns of plant diversity and floristic knowledge. J Biogeogr 32:1–10.CrossRefGoogle Scholar
  47. López G, Rico L, Martin C. 1992. Els vertebrats terrestres de la Comarca d′Alacant. Alicante: Caja de Ahorros Provincial de Alicante.Google Scholar
  48. Maestre FT, Bautista S, Cortina J. 2003. Positive, negative and net effects in grass–shrub interactions in Mediterranean semiarid grasslands. Ecology 84:3186–97.CrossRefGoogle Scholar
  49. Maestre FT, Bowker MA, Puche MD, Hinojosa MB, Martínez I, García-Palacios P, Castillo AP, Soliveres S, Luzuriaga AL, Sánchez AM, Carreira JA, Gallardo A, Escudero A. 2009. Shrub encroachment can reverse desertification in Mediterranean semiarid grasslands. Ecol Lett 12:930–41.PubMedCrossRefGoogle Scholar
  50. Maestre FT, Castillo-Monroy AP, Bowker MA, Ochoa-Hueso R. 2012a. Species richness effects on ecosystem multifunctionality depend on evenness, composition and spatial pattern. J Ecol 100:317–30.CrossRefGoogle Scholar
  51. Maestre FT, Cortina J. 2004. Insights into ecosystem composition and function in a sequence of degraded semiarid steppes. Restor Ecol 12:494–502.CrossRefGoogle Scholar
  52. Maestre FT, Cortina J. 2006. Ecosystem structure and soil-surface conditions drive the variability in the foliar d13C and d15N of Stipa tenacissima in semiarid Mediterranean steppes. Ecol Res 21:44–53.CrossRefGoogle Scholar
  53. Maestre FT, Escudero A. 2009. Is the patch size distribution of vegetation a suitable indicator of desertification processes? Ecology 90:1729–35.PubMedCrossRefGoogle Scholar
  54. Maestre FT, Puche MD, Guerrero C. Escudero A. 2011. Shrub encroachment does not reduce the activity of some soil enzymes in Mediterranean semiarid grasslands. Soil Biol Biochem 43: 1746–1749. Google Scholar
  55. Maestre FT, Quero JL, Gotelli NJ, Escudero A, Ochoa V, Delgado-Baquerizo M, García-Gómez M, Bowker MA, Soliveres S, Escolar C, García-Palacios P, Berdugo M, Valencia E, Gozalo B, Gallardo A, Aguilera L, Arredondo T, Blones J, Boeken B, Bran D, Conceição AA, Cabrera O, Chaieb M, Derak M, Eldridge DJ, Espinosa CI, Florentino A, Gaitán J, Gatica MG, Ghiloufi W, Gómez-González S, Gutiérrez JR, Hernández RM, Huang X, Huber-Sannwald E, Jankju M, Miriti M, Monerris J, Mau RL, Morici E, Naseri K, Ospina A, Polo V, Prina A, Pucheta E, Ramírez-Collantes DA, Romão R, Tighe M, Torres-Díaz C, Val J, Veiga JP, Wang D, Zaady E. 2012b. Plant species richness and ecosystem multifunctionality in global drylands. Science 335:214–18.PubMedCrossRefGoogle Scholar
  56. Maestre FT, Ramírez DA, Cortina J. 2007. Ecología del esparto (Stipa tenacissima L.) y los espartales en la Península Ibérica. Ecosistemas 16:116–35.Google Scholar
  57. Maestre FT. 2004. On the importance of patch attributes, environmental factors and past human impacts as determinants of perennial plant species richness and diversity in Mediterranean semiarid steppes. Divers Distrib 10:21–9.CrossRefGoogle Scholar
  58. McClaran MP, Moore-Kucera J, Martens DA, van Haren J, Marsh SE. 2008. Soil carbon and nitrogen in relation to shrub size and death in a semi-arid grassland. Geoderma 145:60–8.CrossRefGoogle Scholar
  59. Millennium Ecosystem Assessment. 2005. Ecosystems and human well-being: synthesis. Washington, DC: Island Press.Google Scholar
  60. Miranda JD, Padilla FM, Pugnaire FI. 2009. Response of a Mediterranean semiarid community to changing patterns of water supply. Perspect Plant Ecol Evol Syst 11:255–66.CrossRefGoogle Scholar
  61. Mouillot D, Villéger S, Scherer-Lorenzen M, Mason NWH. 2011. Functional structure of biological communities predicts ecosystem multifunctionality. Plos One 6:e17476.PubMedCrossRefGoogle Scholar
  62. Naito AT, Cairns DM. 2011. Relationships between arctic shrub dynamics and topographically-derived hydrologic characteristics. Environ Res Lett 6:045506.CrossRefGoogle Scholar
  63. Noble JC. 1997. The delicate and noxious scrub: CSIRO studies on native tree and shrub proliferation in the semi-arid woodlands of Eastern Australia. Lyneham, ACT: CSIRO.Google Scholar
  64. Paruelo JM, Garbulsky MF, Guerschman JP, Jobbagy EG. 2004. Two decades of normalized difference vegetation index changes in South America: Identufying the imprint of global change. Int J Remote Sens 25:2793–806.CrossRefGoogle Scholar
  65. Pausas JG. 2004. Changes in fire and climate in the eastern Iberian Peninsula (Mediterranean basin). Clim Chang 63:337–50.CrossRefGoogle Scholar
  66. Pearse IS, Hipp AL. 2009. Phylogenetic and trait similarity to a native species predict herbivory on non-native oaks. Proc Natl Acad Sci USA 106:18097–102.PubMedCrossRefGoogle Scholar
  67. Quinn GP, Keough MJ. 2002. Experimental design and data analysis for biologists. Cambridge University Press, Cambridge.Google Scholar
  68. Rangel TF, Diniz-Filho JAF, Bini LM. 2010. SAM: a comprehensive application for spatial analysis in macroecology. Ecography 33:46–50.CrossRefGoogle Scholar
  69. Ratajczak Z, Nippert JB, Collins SL. 2012. Woody encroachment decreases diversity across North American grasslands and savannas. Ecology 93:697–703.PubMedCrossRefGoogle Scholar
  70. Reiss J, Bridle JR, Montoya JM, Woodward G. 2009. Emerging horizons in biodiversity and ecosystem functioning research. Trends Ecol Evol 24:505–14.PubMedCrossRefGoogle Scholar
  71. Rogala JK, Hebblewhite M, Whittington J, White CA, Coleshill J, Musiani M. 2011. Human activity differentially redistributes large mammals in the Canadian Rockies National Parks. Ecol Soc 16:16–36.Google Scholar
  72. Seifan M, Kadmon R. 2006. Indirect effects of casttle grazing on shrub spatial pattern in a mediterranean scrub community. Basic Appl Ecol 7:496–506.CrossRefGoogle Scholar
  73. Selene B, Collin SL. 2008. Shrub invasion decreases diversity and alters community stability in Northern Chihuahuan desert plant communities. PLoS ONE 3:e2332.CrossRefGoogle Scholar
  74. Servicio del Esparto. 1950. El esparto y su economía. Ministerio de Industria, Comercio y Agricultura, Madrid.Google Scholar
  75. Soil Survey Staff. 1994. Keys to soil taxonomy. 6th edn. Blacksburg: Pocahontas Press.Google Scholar
  76. Soliveres S, Eldridge D, Maestre FT, Bowker MA, Tighe M, Escudero A. 2011. Microhabitat amelioration and reduced competition among understorey plants as drivers of facilitation across environmental gradients: towards a unifying framework. Persp Plant Ecol Evol System 13:247–58.CrossRefGoogle Scholar
  77. Throop HL, Archer SR. 2008. Shrub (Prosopis velutina) encroachment in a semidesert grassland: spatial-temporal changes in soil organic carbon and nitrogen pools. Glob Chang Biol 14:2420–31.CrossRefGoogle Scholar
  78. Tongway DJ, Sparrow AD, Friedel MH. 2003. Degradation and recovery processes in arid grazing lands of central Australia. Part 1: soil and land resources. J Arid Environ 55:301–26.CrossRefGoogle Scholar
  79. United Nations Environment Programme. 1992. World Atlas of desertification. London, UK: Edward Arnold.Google Scholar
  80. Waide RB, Willig MR, Steiner CF, Mittelbach G, Gough L, Dodson SI, Juday GP, Parmenter RR. 1999. The relationship between productivity and species richness. Annu Rev Ecol Syst 30:257–300.CrossRefGoogle Scholar
  81. van Auken OW. 2009. Causes and consequences of woody plant encroachment into western North American grasslands. J Environ Manage 90:2931–42.PubMedCrossRefGoogle Scholar
  82. Verdú M, García-Fayos P. 1996. Nucleation processes in a Mediterranean bird-dispersed plant. Funct Ecol 10:275–80.CrossRefGoogle Scholar
  83. Wang G, Li H, An M, Jian N, Shengjun J, Wang J. 2011. A regional-scale consideration of the effects of species richness on above-ground biomass in temperate natural grasslands of China. J Veg Sci 22:414–24.CrossRefGoogle Scholar
  84. Wheeler CW, Archer SR, Asner GP. 2007. Climatic/edaphic controls on soil carbon/nitrogen response to shrub encroachment in desert grassland. Ecol Appl 17:1911–28.PubMedCrossRefGoogle Scholar
  85. White R P, Nackoney J. 2003. Drylands, people, and ecosystem goods and services: a web-based geospatial analysis. Washington, DC: World Resources Institute.
  86. Whitford WG. 2002. Ecology of desert systems. San Diego, CA: Academic Press.Google Scholar
  87. Villar R, Merino J. 2001. Comparison of leaf construction costs in woody species with differing leaf life-spans in contrasting ecosystems. New Phytol 151:213–26.CrossRefGoogle Scholar
  88. Zavaleta ES, Pasari JR, Hulvey KB, Tilman GD. 2010. Sustaining multiple ecosystem functions in grassland communities requires higher biodiversity. Proc Natl Acad Sci USA 107:1443.PubMedCrossRefGoogle Scholar
  89. Zhang D, Hui D, Luo Y, Zhou G. 2008. Rates of litter decomposition in terrestrial ecosystems: global patterns and controlling factors. J Plant Ecol 1:85–93.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • José L. Quero
    • 1
    • 2
  • Fernando T. Maestre
    • 1
  • Victoria Ochoa
    • 1
  • Miguel García-Gómez
    • 1
  • Manuel Delgado-Baquerizo
    • 3
  1. 1.Área de Biodiversidad y Conservación, Departamento de Biología y GeologíaEscuela Superior de Ciencias Experimentales y Tecnología, Universidad Rey Juan CarlosMóstolesSpain
  2. 2.Departamento de Ingeniería ForestalCampus de Rabanales Universidad de CórdobaCórdobaSpain
  3. 3.Departamento de Sistemas Físicos, Químicos y NaturalesUniversidad Pablo de OlavideSevillaSpain

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