Biological Soil Crusts as a Model System in Ecology

  1. Maestre, Fernando T.
  2. Bowker, Matthew A.
  3. Eldridge, David J.
  4. Cortina, Jordi
  5. Lázaro, Roberto
  6. Gallardo, Antonio
  7. Delgado-Baquerizo, Manuel
  8. Berdugo, Miguel
  9. Castillo-Monroy, Andrea P.
  10. Valencia, Enrique
Libro:
Biological Soil Crusts: An Organizing Principle in Drylands

Editorial: Springer

ISSN: 0070-8356 2196-971X

ISBN: 9783319302126 9783319302140

Año de publicación: 2016

Páginas: 407-425

Tipo: Capítulo de Libro

DOI: 10.1007/978-3-319-30214-0_20 GOOGLE SCHOLAR lock_openAcceso abierto editor

Objetivos de desarrollo sostenible

Resumen

We explore in this chapter how biological soil crusts (biocrusts) may serve as a useful model system for studying multiple questions of interest in ecology, including biodiversity–ecosystem function relationships, positive and negative species interactions along environmental gradients, the source–sink hydrological dynamics in drylands, and ecosystem resistance and resilience. To illustrate our views, we synthesize recent and ongoing studies that are employing biocrusts as model systems to tackle these and other related questions, emphasizing the main features of biocrusts that make them special and well suited to advance ecological theory and our understanding of many important topics in community and ecosystem ecology. We complete the synthesis of the studies conducted so far with recommendations aiming to promote the use of biocrusts by community and ecosystem ecologists.

Información de financiación

Financiadores

Referencias bibliográficas

  • Aguiar MR, Sala OE (1999) Patch structure, dynamics and implications for the functioning of arid ecosystems. Trends Ecol Evol 14:273–277
  • Armstrong RA, Welch AR (2007) Competition in lichen communities. Symbiosis 43:1–12
  • Baggs EM, Philippot L (2011) Nitrous oxide production in the terrestrial environment. In: Moir JWB (ed) Nitrogen cycling in bacteria – molecular analysis. Caister Academic Press, Norfolk, pp 211–232
  • Barger NN, Belnap J, Ojima DS, Mosier A (2005) NO gas loss from biologically crusted soils in Canyonlands National Park, Utah. Biogeochemistry 75:373–391
  • Belnap J (2002) Nitrogen fixation in biological soil crusts from southeast Utah, USA. Biol Fert Soils 35:128–135
  • Belnap J (2006) The potential roles of biological soil crusts in dryland hydrologic cycles. Hydrol Process 20:3159–3178
  • Belnap J, Phillips SL, Troxler T (2006) Soil lichen and moss cover and species richness can be highly dynamic: the effects of invasion by the annual exotic grass Bromus tectorum, precipitation, and temperature on biological soil crusts in SE Utah. Appl Soil Ecol 32:3–76
  • Berdugo M, Soliveres S, Maestre FT (2014) Vascular plants and biocrust modulate how abiotic factors affect wetting and drying events in drylands. Ecosystems 17:1242–1256
  • Bhark EW, Small EE (2003) Association between plant canopies and the spatial patterns of infiltration in shrubland and grassland of the Chihuahuan Desert, New Mexico. Ecosystems 6:0185–0196
  • Bowker MA (2007) Biological soil crust rehabilitation in theory and practice: an underexploited opportunity. Restor Ecol 15:13–23
  • Bowker MA, Reed SC, Belnap J, Phillips SL (2002) Temporal variation in community composition, pigmentation, and Fv/Fm of desert cyanobacterial soil crusts. Microb Ecol 43:13–25
  • Bowker MA, Soliveres S, Maestre FT (2010a) Competition increases with abiotic stress and regulates the diversity of biological soil crusts. J Ecol 98:551–560
  • Bowker MA, Maestre FT, Escolar C (2010b) Biological crusts as a model system for examining the biodiversity-function relationship in soils. Soil Biol Biochem 42:405–417
  • Bowker MA, Mau RL, Maestre FT et al (2011) Functional profiles reveal unique ecological roles of various biological soil crust organisms. Funct Ecol 25:787–795
  • Bowker MA, Eldridge DJ, Val J, Soliveres S (2013a) Hydrology in a patterned landscape is co-engineered by soil-disturbing animals and biological crusts. Soil Biol Biochem 61:14–22
  • Bowker MA, Maestre FT, Mau RL (2013b) Diversity and patch-size distributions of biological soil crusts regulate dryland ecosystem multifunctionality. Ecosystems 16:923–933
  • Bowker MA, Maestre FT, Eldridge DJ et al (2014) Biological soil crusts as a model system in community, landscape and ecosystem ecology. Biodivers Conserv 23:1619–1637
  • Brooker RW, Maestre FT, Callaway MR et al (2008) Facilitation in plant communities: the past, the present and the future. J Ecol 96:18–34
  • Büdel B, Colesie C, Green TGA et al (2014) Improved appreciation of the functioning and importance of biological soil crusts in Europe: the Soil Crust International Project (SCIN). Biodivers Conserv 23:1639–1658
  • Cardinale BJ, Matulich KL, Hooper DU et al (2011) The functional role of producer diversity in ecosystems. Am J Bot 98:572–592
  • Cardinale BJ, Duffy JE, Gonzalez A et al (2012) Biodiversity loss and its impact on humanity. Nature 486:59–67
  • Castillo-Monroy AP, Bowker MA, Maestre FT et al (2011) Relationships between biological soil crusts, bacterial diversity and abundance, and ecosystem functioning: insights from a semi-arid Mediterranean environment. J Veg Sci 22:165–174
  • Castillo-Monroy AP, Bowker MA, García-Palacios P et al (2015) Aspects of soil lichen biodiversity and aggregation interact to influence subsurface microbial function. Plant Soil 386:303–316
  • Colesie C, Scheu S, Green TGA et al (2012) The advantage of growing on moss: facilitative effects on photosynthetic performance and growth in the cyanobacterial lichen Peltigera rufescens. Oecologia 169:599–607
  • Concostrina-Zubiri L, Pescador DS, Martínez I, Escudero A (2014) Climate and small scale factors determine functional diversity shifts of biological soil crusts in Iberian drylands. Biodivers Conserv 23:1757–1770
  • Contreras S, Cantón Y, Solé-Benet A (2008) Sieving crusts and macrofaunal activity control soil water repellency in semiarid environments: evidences from SE Spain. Geoderma 145:225–258
  • Cortina J, Maestre FT (2005) Plant effects on soils in drylands: implications on community dynamics and ecosystem restoration. In: Binkley D, Menyailo O (eds) Proceedings of the NATO on tree species effects on soils: implications for global change. Springer, Berlin, pp 85–118
  • Cortina J, Maestre FT, Vallejo R et al (2006) Ecosystem structure, function, and restoration success: are they related? J Nat Conserv 14:152–160
  • Delgado-Baquerizo M, Covelo F, Maestre FT, Gallardo A (2013a) Biological soil crusts affect small-scale spatial patterns of inorganic N in a semiarid Mediterranean steppe. J Arid Environ 91:147–150
  • Delgado-Baquerizo M, Gallardo A, Wallenstein MD, Maestre FT (2013b) Vascular plants mediate the effects of aridity and soil properties on ammonia-oxidizing bacteria and archaea. FEMS Microbiol Ecol 85:273–282
  • Delgado-Baquerizo M, Maestre FT, Rodríguez JGP, Gallardo A (2013c) Biological soil crusts promote N accumulation in response to dew events in dryland soils. Soil Biol Biochem 62:22–27
  • Delgado-Baquerizo M, Morillas M, Maestre FT, Gallardo A (2013d) Biocrusts control the nitrogen dynamics and microbial functional diversity of semi-arid soils in response to nutrient additions. Plant Soil 372:643–654
  • Delgado-Baquerizo M, Gallardo A, Covelo F et al (2015) Differences in the chemistry of thalli determine species-specific effects of biocrust-forming lichens on soil nutrients and microbial communities. Funct Ecol 29:1087–1098
  • Delgado-Baquerizo M, Maestre FT, Eldridge DJ et al (2016) Biocrusts mitigate the negative impacts of increasing aridity on ecosystem multifunctionality in drylands. New Phytol 209:1540–1552
  • Eldridge DJ (1999) Distribution and floristics of moss- and lichen-dominated soil crusts in a patterned Callitris glaucophylla woodland in eastern Australia. Acta Oecol 20:159–170
  • Eldridge DJ, Rosentreter RR (1999) Morphological groups: a framework for monitoring microphytic crusts in arid landscapes. J Arid Environ 41:11–25
  • Eldridge DJ, Bowker MA, Maestre FT et al (2010) Interactive effects of three ecosystem engineers on infiltration in a semi–arid Mediterranean grassland. Ecosystems 13:499–510
  • Escolar C, Martínez 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 367:3087–3099
  • Fogg GE (1966) The extracellular products of algae. Oceanogr Mar Biol 4:195–212
  • Fraser LH, Henry MA, Carlyle CN et al (2013) Coordinated distributed experiments: an emerging tool for testing global hypotheses in ecology and environmental science. Front Ecol Environ 11:147–155
  • García-Palacios P, Bowker MA, Maestre F et al (2011) Ecosystem development in roadside grasslands: biotic control, plant–soil interactions, and dispersal limitations. Ecol Appl 21:2806–2821
  • Green TGA, Sancho LG, Pintado A (2011) Ecophysiology of desiccation/rehydration cycles in mosses and lichens. In: Lüttge U, Beck E, Bartels D (eds) Plant desiccation tolerance. Springer, Berlin, pp 89–120
  • Hauck M (2008) Metal homeostasis in Hypogymnia physodes is controlled by lichen substances. Environ Pollut 153:304–308
  • Hauck M, Jürgens S-R, Willenbruch K et al (2009) Dissociation and metal-binding characteristics of yellow lichen substances suggest a relationship with site preferences of lichens. Ann Bot 103:13–22
  • Hawksworth DL (1982) Secondary fungi in the lichen symbioses: parasites, saprophytes and parasymbionts. J Hattori Bot Lab 52:357–366
  • Hector A, Philipson C, Saner P et al (2011) The Sabah biodiversity experiment: a long term test of the role of tree diversity in restoring tropical forest structure and functioning. Philos Trans R Soc B 366:3303–3315
  • Hobbs RJ, Higgs E, Harris JA (2009) Novel ecosystems: implications for conservation and restoration. Trends Ecol Evol 24:599–605
  • Hu C, Liu Y, Song L, Zhang D (2002) Effect of desert soil algae on the stabilization of fine sands. J Appl Phycol 14:281–292
  • Kowalski M, Hausner G, Piercey-Normore MD (2011) Bioactivity of secondary metabolites and thallus extracts from lichen fungi. Mycoscience 52:413–418
  • Kuske CR, Yeager CM, Johnson S et al (2012) Response and resilience of soil biocrust bacterial communities to chronic physical disturbance in arid shrublands. ISME J 6:886–897
  • Lange OL (1974) Chelating agents and blue-green algae. Can J Microbiol 20:1311–1321
  • Lawrey JD (1986) Biological role of lichen substances. Bryologist 89:111–122
  • Lázaro R, Cantón Y, Solé-Benet A et al (2008) The influence of competition between lichen colonization and erosion on the evolution of soil surfaces in the badlands (SE Spain) and its landscape effects. Geomorphology 102:252–266
  • Li H, Colica G, Wu P-P et al (2013) Shifting species interaction in soil microbial community and its influence on ecosystem functions modulating. Microb Ecol 65:700–708
  • Maestre FT (2003a) Small-scale spatial patterns of two soil lichens in semi-arid Mediterranean steppe. Lichenologist 35:71–81
  • Maestre FT (2003b) Variaciones en el patrón espacial a pequeña escala de los componentes de la costra biológica en un ecosistema mediterráneo semiárido. Rev Chil Hist Nat 76:35–46
  • Maestre FT, Cortina J (2002) Spatial patterns of surface soil properties and vegetation in a Mediterranean semi-arid steppe. Plant Soil 241:279–291
  • Maestre FT, Huesca MT, Zaady E, Bautista S, Cortina J (2002) Infiltration, penetration resistance and microphytic crust composition in contrasted microsites within a Mediterranean semi-arid steppe. Soil Biol Biochem 34:895–898
  • Maestre FT, Escudero A, Martinez I et al (2005) Does spatial pattern matter to ecosystem functioning? Insights from biological soil crusts. Funct Ecol 19:566–573
  • Maestre FT, Escolar C, Martínez I, Escudero A (2008) Are soil lichen communities structured by biotic interactions? A null model analysis. J Veg Sci 19:261–266
  • Maestre FT, Martínez I, Escolar C, Escudero A (2009) On the relationship between abiotic stress and co-occurrence patterns: an assessment at the community level using soil lichen communities and multiple stress gradients. Oikos 118:1015–1022
  • Maestre FT, Bowker MA, Cantón Y et al (2011) Ecology and functional roles of biological soil crusts in semi-arid ecosystems of Spain. J Arid Environ 75:1282–1291
  • Maestre FT, Castillo-Monroy AP, Bowker MA, Ochoa-Hueso R (2012) Species richness effects on ecosystem multifunctionality depend on evenness, composition, and spatial pattern. J Ecol 100:317–330
  • Maestre FT, Escolar C, Ladrón de Guevara M et al (2013) Changes in biocrust cover drive carbon cycle responses to climate change in drylands. Glob Change Biol 19:3835–3847
  • Maestre FT, Escolar C, Bardgett R et al (2015) Warming reduces the cover and diversity of biocrust-forming mosses and lichens, and increases the physiological stress of soil microbial communities in a semi-arid Pinus halepensis plantation. Front Microbiol 6:865
  • Mager DM, Thomas AD (2011) Extracellular polysaccharides from cyanobacterial soil crusts: a review of their role in dryland soil processes. J Arid Environ 75:91–97
  • McKay JK, Christian CE, Harrison S et al (2005) How local is local? A review of practical and conceptual issues in the genetics of restoration. Restor Ecol 13:432–440
  • Miller ME, Belote RT, Bowker MA et al (2011) Alternative states of a semiarid grassland ecosystem: implications for ecosystem services. Ecosphere 2:art55
  • Miralles I, Domingo F, García-Campos E et al (2012a) Biological and microbial activity in biological soil crusts from the Tabernas Desert, a sub-arid zone in SE Spain. Soil Biol Biochem 55:113–121
  • Miralles I, van Wesemael B, Cantón Y et al (2012b) Surrogate descriptors of C-storage processes on crusted semiarid ecosystems. Geoderma 189–190:227–235
  • Naeem S, Duffy JE, Zavaleta E (2012) The functions of biological diversity in an age of extinction. Science 336:1401–1406
  • Orlando J, Alfaro M, Bravo L et al (2010) Bacterial diversity and occurrence of ammonia-oxidizing bacteria in the Atacama Desert soil during a “desert bloom” event. Soil Biol Biochem 42:1183–1188
  • Palmquist K, Dahlman L, Valladares F et al (2002) CO2 exchange and thallus nitrogen across 75 contrasting lichens associations from different climate zones. Oecologia 13:295–306
  • Pasari JR, Levi T, Zavaleta ES et al (2013) Several scales of biodiversity affect ecosystem multifunctionality. Proc Natl Acad Sci USA 110:10219–10222
  • Pointing SB, Belnap J (2012) Microbial colonization and controls in dryland systems. Nat Rev Microbiol 10:551–562
  • Puigdefábregas J, Solé A, Gutierrez L et al (1999) Scales and processes of water and sediment redistribution in drylands: results from the Rambla Honda field site in Southeast Spain. Earth Sci Rev 48:39–70
  • Rajeev L, Nunes da Rocha U, Klitgord N et al (2013) Dynamic cyanobacterial response to hydration and dehydration in a desert biological soil crust. ISME J 7:2178–2191
  • Reed SC, Coe KK, Sparks JP et al (2012) Changes to dryland rainfall result in rapid moss mortality and altered soil fertility. Nat Clim Change 2:752–755
  • Rodríguez-Caballero E, Cantón Y, Chamizo S et al (2013) Soil loss and runoff in semiarid ecosystems: a complex interaction between biological soil crusts, micro-topography and hydrological drivers. Ecosystems 16:529–546
  • Rodríguez-Caballero E, Cantón Y, Lázaro R, Solé-Benet A (2014) Cross-scale interactions and nonlinearities in the hydrological and erosive behavior of semiarid catchments: the role of biological soil crusts. J Hydrol 517:815–825
  • Roscher C, Schumacher J, Baade J et al (2004) The role of biodiversity for element cycling and trophic interactions: an experimental approach in a grassland community. Basic Appl Ecol 5:107–121
  • Seybold CA, Herrick JE, Brejda JJ (1999) Soil resilience: a fundamental component of soil quality. Soil Sci 164:224–234
  • Soliveres S, Eldridge DJ, 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. Perspect Plant Ecol Evol Syst 13:247–258
  • Soliveres S, Smit C, Maestre FT (2015) Moving forward on facilitation research: response to changing environments and effects on the diversity, functioning and evolution of plant communities. Biol Rev 90:297–313
  • Spitale D (2009) Switch between competition and facilitation within a seasonal scale at colony level in bryophytes. Oecologia 160:471–482
  • Tilman D, Isbell F, Cowles JM (2014) Biodiversity and ecosystem functioning. Annu Rev Ecol Evol Syst 45:471–493
  • Turnbull L, Wilcox BP, Belnap J et al (2012) Understanding the role of ecohydrological feedbacks in ecosystem state change in drylands. Ecohydrology 5:174–183
  • Ulrich W, Soliveres S, Kryszewski W, Maestre FT, Gotelli NJ (2014) Matrix models for quantifying competitive intransitivity from species abundance data. Oikos 123:1057–1070
  • Vitousek P (2002) Oceanic islands as model systems for ecological studies. J Biogeogr 29:573–582
  • Wang WB, Liu YD, Li DH, Hu CX, Rao BQ (2008) Feasibility of cyanobacterial inoculation for biological soil crusts formation in desert area. Soil Biol Biochem 41:926–929
  • Wedin M, Maier S, Fernandez-Brime S, Cronholm B et al (2015) Microbiome change by symbiotic invasion in lichens. Environ Microbiol. doi: 10.1111/1462-2920.13032
  • Whitford WG (2002) Ecology of desert systems. Academic Press, London, 343 pp.
  • Whitton BA, Al-Shehri AM, Ellwood NTW et al (2005) Ecological aspects of phosphatase activity in cyanobacteria, eukaryotic algae and bryophytes. In: Turner BL, Frossard E, Baldwin DS (eds) Organic phosphorus in the environment. CABI, Wallingford, pp 205–241
  • Xu S, Yin C, He M et al (2008) A technology for rapid reconstruction of moss-dominated soil crusts. Environ Eng Sci 25:1129–1138