Skip to main content

Advertisement

SpringerLink
Log in

Aspects of soil lichen biodiversity and aggregation interact to influence subsurface microbial function

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Background and aims

Many previous studies have evaluated aboveground–heterotrophic belowground interactions such as plant-soil feedbacks, plant-mycorrhizal fungi associations or plant-actinorhizal symbioses. However, few studies have used biocrusts, which are specialized soil communities of autotrophic cyanobacteria, mosses, lichens and non-photosynthetic fungi and bacteria that are prevalent in drylands worldwide. These communities largely influence ecosystem functioning, and can be used as a model system for studying above-belowground interactions. In this study, we evaluated how biocrusts affect the functional diversity and biomass of microbial diversities beneath biocrusts.

Methods

We performed two microcosm experiments using biocrust-forming lichens where we manipulated their biotic attributes to test independently the effects of species richness (from two to eight species), composition, evenness (maximal and low evenness) and spatial pattern (clumped and random distribution) on the microbial catabolic profile and microbial functional diversity.

Results

Microcosms with a random pattern had a higher microbial catabolic profile than those with a clumped pattern. Significant richness × evenness × pattern and richness × evenness interactions were found when analyzing microbial catabolic profile and biomass, respectively. Microcosms with a random pattern, intermediate number of species, and maximal evenness level had higher microbial catabolic profile. At the maximal evenness level, assemblages had higher microbial catabolic profile and microbial biomass when they contained four species. The richness × evenness × pattern interaction was the most informative predictor of variations in microbial catabolic profile.

Conclusions

Our results indicate that soil microorganisms are influenced by biocrusts, just as they are influenced by plants, and highlight the importance of higher order interactions among species richness, evenness, and spatial pattern as drivers of microbial communities. The results also emphasize the importance of studying several biotic attributes simultaneously when studying biocrust-soil microorganism interactions, as in nature, community properties do not exert their influence in isolation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Aust Ecol 26:32–46

    Google Scholar 

  • Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA + for PRIMER: guide to software and statistical methods. PRIMER-E, PlymouthUK

    Google Scholar 

  • Antarikanonda P (1984) Production of extracellular free amino acids by cyanobacterium Anabaena siamensis. Curr Microbiol 11:191–195

    Article  CAS  Google Scholar 

  • Antoninka A, Wolf JE, Bowker MA, Classen AT, Johnson NC (2009) Linking above- and belowground responses to global change at community and ecosystem scales. Global Change Biol 15:914–929

    Article  Google Scholar 

  • Bardgett R, Wardle D (2010) Aboveground-belowground linkages: biotic interactions, ecosystem processes, and global change. Oxford University Press, Oxford

    Google Scholar 

  • Bates ST, Nash TH, Sweat KG, Garcia-pichel F (2010) Fungal communities of lichen-dominated biological soil crusts: Diversity, relative microbial biomass, and their relationship to disturbance and crust cover. J Arid Environ 74:1192–1199

    Article  Google Scholar 

  • Belnap J (2002) Nitrogen fixation in biological soil crusts from southeast Utah, USA. Biol Fertil Soils 35:128–135

    Article  CAS  Google Scholar 

  • Belnap J, Lange OL (2003) Biological soil crusts: structure function and management. Springer, Berlin

    Book  Google Scholar 

  • Ben Sassi M, Dollinger J, Renault P, Tlili A, Bérard A (2012) The FungiResp method: an application of the MicroResp™ method to assess fungi in microbial communities as soil biological indicators. Ecol Indic 23:482–490

    Article  Google Scholar 

  • Bever JD (2002) Soil community feedback and the coexistence of competitors: conceptual frameworks and empirical tests. New Phytol 157:465–473

    Article  Google Scholar 

  • Billings SA, Schaeffer SM, Evans RD (2003) Nitrogen fixation by biological soil crusts and heterotrophic bacteria in an intact Mojave Desert ecosystem with elevated CO2 and added soil carbon. Soil Biol Biochem 35:643–649

    Article  CAS  Google Scholar 

  • Bowker MA, Maestre FT, Escolar C (2010) Biological crusts as a model system for examining the biodiversity-ecosystem function relationship in soils. Soil Biol Biochem 42:405–417

    Article  CAS  Google Scholar 

  • Bowker MA, Maestre FT, Mau R (2013) Diversity and patch-size distributions of biological soil crusts regulate dryland ecosystem multifunctionality. Ecosystems 16:923–933

    Article  CAS  Google Scholar 

  • Bowker MA, Maestre FT, Eldridge D, Belnap J, Castillo-Monroy A, Escolar C, Soliveres S (2014) Biological soil crusts as a model system in community, landscape and ecosystem ecology. Biodivers Conserv. doi:10.1007/s10531-014-0658-x

    Google Scholar 

  • Bowker MA, Mau RL, Maestre FT, Escolar C, Castillo-Monroy AP (2011) Functional profiles reveal unique ecological roles of various biological soil crust organisms. Funct Ecol 25:787–795

    Article  Google Scholar 

  • Blum U (2011) Plant-plat allelopathic interactions: phenolic acids, cover crops and weed emergence. Springer science, NY

    Book  Google Scholar 

  • Campbell CD, Chapman SJ, Cameron CM, Davidson MS, Potts JM (2003) A rapid microtiter plate method to measure carbon dioxide evolved from carbon substrate amendments so as to determine the physiological profiles of soil microbial communities by using whole soil. Appl Environ Microbiol 69:3593–3599

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cardinale BJ, Matulich KL, Hooper DU, Byrnes JE, Duffy E, Gamfeldt L, Balvanera P, O’Connor MI, González A (2011) The functional role of producer diversity in ecosystems. Am J Bot 98:572–592

    Article  PubMed  Google Scholar 

  • Castillo-Monroy AP, Maestre FT (2014) Data from “Aspects of soil lichen biodiversity and aggregation interact to influence subsurface microbial function”. figshare. doi:10.6084/m9.figshare.1157787

  • Castillo-Monroy AP, Maestre FT, Delgado-Baquerizo M, Gallardo A (2010) Biological soil crust modulate nitrogen availability in semi-arid ecosystem: insights froma Mediterranean grassland. Plant Soil 333:21–34

    Article  CAS  Google Scholar 

  • Castillo-Monroy AP, Maestre FT, Rey A, Soliveres S, García-Palacios P (2011a) Biological soil crust microsites are the main contributor to soil respiration in a semiarid ecosystem. Ecosystems 14:835–847

    Article  CAS  Google Scholar 

  • Castillo-Monroy AP, Bowker MA, Maestre FT, Rodríguez-Echeverría S, Martínez I, Barraza-Zepeda CE, Escolar C (2011b) The relative importance of biological soil crust and soil bacterial diversity and abundance as drivers of ecosystem functioning in a semi-arid environment. J Veg Sci 22:165–174

    Article  Google Scholar 

  • 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 19:110–122

    Article  PubMed  Google Scholar 

  • Donoso DA, Johnston MK, Clay N, Kaspari ME (2013) Trees and seasonality as templates for trophic structure of tropical litter arthropod communities. Soil Biol Biochem 61:45–61

    Article  CAS  Google Scholar 

  • Downing AL (2005) Relative effects of species composition and richness on ecosystem properties in ponds. Ecology 86:701–715

    Article  Google Scholar 

  • De Deyn GB, Van der Putten WH (2005) Linking aboveground and belowground diversity. Trends Ecol Evol 20:625–633

    Article  PubMed  Google Scholar 

  • Doncaster CP, Davey AJH (2007) Analysis of variance and covariance. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Eldridge DJ, Bowker MA, Maestre FT, Alonso P, Mau RL, Papadopolous J, Escudero A (2010) Interactive effects of three ecosystem engineers on infiltration in a semi-arid grassland. Ecosystems 13:499–510

    Article  Google Scholar 

  • García-Palacios P, Bowker MA, Maestre FT, Soliveres S, Valladares F, Papadopoulos J, Escudero A (2011) Ecosystem development in roadside grasslands: biotic control, plant–soil interactions, and dispersal limitations. Ecol Appl 21:2806–2821

    Article  PubMed  Google Scholar 

  • Goldman JC, Caron DA, Dennett MR (1987) Regulation of gross growth efficiency and ammonium regeneration in bacteria by substrate C:N ratio. Limnol Oceanogr 32:1239–1252

    Article  CAS  Google Scholar 

  • Grace JB (2006) Structural equation modeling and natural systems. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Green LE, Porras-Alfaro A, Sinsabaugh RL (2008) Translocation of nitrogen and carbon integrates biotic crust and grass production in desert grassland. J Ecol 96:1076–1085

    Article  CAS  Google Scholar 

  • Gundlapally SR, Garcia-Pichel F (2006) The community and phylogenetic diversity of biological soil crusts in the Colorado Plateau Studied by molecular fingerprinting and intensive cultivation. Microb Ecol 52:345–357

    Article  PubMed  Google Scholar 

  • Huneck S, Yoshimura I (1996) Identification of lichen substances. Springer, Berlin

    Book  Google Scholar 

  • Hooper DU, Chapin FS, Ewel JJ, Hector A, Inchausti P, Lavorel S, Lawton HD, Lodge M, Loreau M, Naeem V, 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

    Article  Google Scholar 

  • Johnson D, Ijdo M, Genney DR, Anderson IC, Alexander IJ (2005) How do plants regulate the function, community structure, and diversity of mycorrhizal fungi? J Exp Bot 56:1751–1760

    Article  CAS  PubMed  Google Scholar 

  • Johnson SL, Kuske CL, Carney TD, Housman DC, Gallegos-Graves L, Belnap J (2012) Increased temperature and altered summer precipitation have differential effects on biological soil crusts in a dryland ecosystem. Global Change Biol 18:2583–2593

    Article  Google Scholar 

  • Kardol P, Bezemer TM, van der Putten WH (2006) Temporal variation in plant–soil feedback controls succession. Ecol Lett 9:1080–1088

    Article  PubMed  Google Scholar 

  • Kefeli VI, Kalevitch MV, Borsari B (2013) Phenolic cycle in plants and environment. J Cell Mol Biol 2:13–18

    Google Scholar 

  • Lange OL, Kidron G, Büdel B, Meyer A, Kilian E, Abeliovich A (1992) Taxonomic composition and photosynthetic characteristics of the “biological soil crusts” covering sand dunes in the western Negev Desert. Funct Ecol 6:519–527

    Article  Google Scholar 

  • Lawrey JD (1995) The chemical ecology of lichen mycoparasites: a review. Can J Bot 73:603–608

    Article  Google Scholar 

  • Loreau M, Naeem S, Inchausti O, Bengtsson J, Grime JP, Hector A, Hooper DU, Huston MA, Raffaelli V, Schmid B, Tilman D, Wardle DA (2001) Biodiversity and ecosystem functioning: current knowledge and future challenges. Science 294:804–808

    Article  CAS  PubMed  Google Scholar 

  • McHugh TA, Gehring CA (2006) Below-ground interactions with arbuscular mycorrhizal shrubs decrease the performance of pinyon pine and the abundance of its ectomycorrhizas. New Phytol 171:171–178

    Article  PubMed  Google Scholar 

  • 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 100:317–330

    Article  CAS  Google Scholar 

  • Maestre FT, Martín N, Díez B, López-Poma R, Santos F, Luque I, Cortina J (2006) Watering, fertilization, and slurry inoculation promote recovery of biological crust function in degraded soils. Microb Ecol 52:365–377

    Article  PubMed  Google Scholar 

  • Maestre FT, Salguero-Gómez R, Quero JL (2012b) It’s getting hotter in here: determining and projecting the impacts of global change on drylands. Philos Trans R Soc B 367:3062–3075

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Maestre FT, Escudero A, Martinez I, Guerrero C, Rubio A (2005) Does spatial pattern matter to ecosystem functioning? Insights from biological soil crusts. Funct Ecol 19:566–573

    Article  Google Scholar 

  • Nash TH (1996) Lichen biology. Cambridge University Press, Cambridge

    Google Scholar 

  • Neher DA, Lewins SA, Weicht TR, Darby BJ (2009) Microarthropod communities associated with biological soil crusts in the Colorado Plateau and Chihuahuan deserts. J Arid Environ 73:672–677

    Article  Google Scholar 

  • Oren A, Steinberger Y (2008a) Catabolic profiles of soil fungal communities along a geographic climatic gradient in Israel. Soil Biol Biochem 40:2578–2587

    Article  CAS  Google Scholar 

  • Oren A, Steinberger Y (2008b) Coping with artifacts induced by CaCO3–CO2–H2O equilibria in substrate utilization profiling of calcareous soils. Soil Biol Biochem 40:2569–2577

    Article  CAS  Google Scholar 

  • Øvreås L (2000) Population and community level approaches for analyzing microbial diversity in natural environments a review. Ecol Lett 3:236–251

    Article  Google Scholar 

  • Petersen U, Wrage N, Köhle L, Leuschner C, Isselstein J (2012) Manipulating the species composition of permanent grasslands - A new approach to biodiversity experiments. Basic Appl Ecol 13:1–9

    Article  Google Scholar 

  • Pringle RM, Doak DF, Brody AK, Jocqué R, Palmer TM (2010) Spatial pattern enhances ecosystem functioning in an African savanna. PLoS Biol 8:e1000377

  • Setälä H, Berg MP, Jones TH (2005) Trophic structure and functional redundancy in soil communities. In: Bardgett RD, Usher MB, Hopkind DW (eds) Biological diversity and function in soil. Cambridge University Press, Cambridge, pp 236–249

    Chapter  Google Scholar 

  • Schwintzer CR, Tjepkema JD (2001) Effect of elevated carbon dioxide in the root atmosphere on nitrogenase activity in three actinorhizal plants. Can J Bot 79:1010–1018

    CAS  Google Scholar 

  • Shipley B (2000) Cause and correlation in Biology. Cambridge University Press, UK

    Book  Google Scholar 

  • Steven B, Gallegos-Graves L, Belnap J, Kuske C (2013) Dryland soil microbial communities display spatial biogeographic patterns associated with soil depth and soil parent material. FEMS Microbiol Ecol 86:101–113

    Article  CAS  PubMed  Google Scholar 

  • Stevenson FJ (1993) Hummus chemistry: genesis, composition reactions. Wiley, New York

    Google Scholar 

  • Tjepkema JD, Schwintzer CR, Burris RH, Johnson GV, Silvester WB (2000) Natural abundance of 15N in actinorhizal plants and nodules. Plant Soil 219:285–289

    Article  CAS  Google Scholar 

  • Van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR (1998) Mycorrhizal fungal diversity determines plant diodiversity, ecosystem variability and productivity. Nature 396:69–72

    Article  Google Scholar 

  • Vivanco L, Austin AT (2008) Tree species identity alters forest litter decomposition through long-term plant and soil interactions in Patagonia, Argentina. J Ecol 96:l727–l736

    Article  Google Scholar 

  • Wardle DA, Bardgett RD, Klironomos JN, Setälä H, van der Putten WH, Wall DH (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633

    Article  CAS  PubMed  Google Scholar 

  • Wilsey BJ, Polley HW (2004) Realistically low species evenness does not alter grassland species-richness-productivity relationship. Ecology 85:2693–2700

    Article  Google Scholar 

  • Wright RT (1984) Dynamic pools of dissolved organic carbon. In: Hobbie JE, Williams PJ (Eds) Heterotrophic activity in the sea. pp. 121–154. Plenum

  • Yeager CM, Kornosky JL, Housman DC, Grote EE, Belnap J, Kuske CR (2004) Diazotrophic community structure and function in two successional stages of biological soil crusts from the Colorado Plateau and Chihuahuan Desert. Appl Environ Microbiol 70:973–983

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yu J, Kidron GJ, Pen-Mouratov S, Wasserstrom H, Barness G (2012) Do development stages of biological soil crusts determine activity and functional diversity in a sand-dune ecosystem? Soil Biol Biochem 51:66–72

    Article  CAS  Google Scholar 

  • Zak JC, Willig MR, Moorhead DL, Wildman HG (1994) Functional diversity of microbial communities: a quantitative approach. Soil Biol Biochem 26:1101–1108

    Article  Google Scholar 

Download references

Acknowledgments

We thank David Elliott and two anonymous reviewers for comments on a previous version of this manuscript. We also thank A. Escudero, I. Martínez, P. Alonso, E. Polaina, S. Soliveres, M. D. Puche, Y. Valiñani, C. Escolar, E. Barahona, S. Beltran de Guevara, C. Iriarte, J. Margalet, C. Díaz, R. Sendra, B. Paredes, L. Giménez-Benavides, Y. Cabrea, I. Conde and I. Pardo for their invaluable help during the development of this work. APCM was supported by a Studentship from the Fundación BBVA (BIOCON06/105 grant). This research was funded by the British Ecological Society (Early Career Project Grant 231/607) and by the European Research Council under the European Community’s Seventh Framework Programme (FP7/2007-2013)/ERC Grant agreement n° 242658 (BIOCOM).

Author information

Authors and Affiliations

  1. Área de Biodiversidad y Conservación, Departamento de Biología y Geología, Escuela Superior de Ciencias Experimentales y Tecnología, Universidad Rey Juan Carlos, Móstoles, 28933, Spain

    Andrea P. Castillo-Monroy & Fernando T. Maestre

  2. Departamento de Ciencias Naturales, Universidad Técnica Particular de Loja, San Cayetano Alto s/n, Loja, Ecuador

    Andrea P. Castillo-Monroy

  3. School of Forestry, Northern Arizona University, 200 E. Pine Knoll, PO Box 15018, Flagstaff, AZ, 86011, USA

    Matthew A. Bowker

  4. Centre d’Ecologie Fonctionnelle & Evolutive, CEFE-CNRS, 1919 route de Mende, Montpellier, 34293, France

    Pablo García-Palacios

Authors
  1. Andrea P. Castillo-Monroy
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Matthew A. Bowker
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Pablo García-Palacios
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Fernando T. Maestre
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Andrea P. Castillo-Monroy.

Additional information

Responsible Editor: Ute Skiba.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOC 574 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Castillo-Monroy, A.P., Bowker, M.A., García-Palacios, P. et al. Aspects of soil lichen biodiversity and aggregation interact to influence subsurface microbial function. Plant Soil 386, 303–316 (2015). https://doi.org/10.1007/s11104-014-2256-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-014-2256-9

Keywords

Search

Navigation