Abstract
Background and aims
Functional traits are increasingly being used to assess the degree to which ecosystems maintain key processes. The functional traits of vascular plants are well-documented but those of non-vascular plants are poorly known. We describe a comprehensive methodology to measure the functional traits of soil-borne lichens, mosses and liverworts making up biocrust (biological soil crust) communities.
Methods
We collected 40 biocrust taxa from across 10,000 km2 of eastern Australia, and measured eight functional traits using a combination of mensurative studies and laboratory-based experiments. These traits were sediment capture, absorptivity, root (or rhizine) length, height, and the activity of four enzymes involved in key nutrient cycles; β-glucosidase, β-D-cellobiosidase, N-acetyl-β-glucosaminidase and phosphatase.
Results
Taxa were distributed across a broad range of trait values. Sediment capture values ranged from 2 % in the crustose lichen Diploschistes thunbergianus to 83 % in the tall moss Triquetrella papillata. The highest absorptivity value was observed in the moss Bartramia hampeana ssp. hampei, which was able to absorb 12.9 times its dry mass in water, while the lowest value, 0.3, was observed in Diploschistes thunbergianus. Multivariate analyses revealed that biocrust morphological groups differed significantly in their functional profiles.
Conclusions
Our results indicate that biocrust taxa vary greatly in their functional traits and that morphological groups explain, in part, the ability of biocrusts to sequester resources (sediment, moisture) and to undertake key processes associated with the cycling of carbon, nitrogen and phosphorus. This methodology will enhance our understanding of ecosystem functioning in drylands where biocrusts make up a large component of the surface cover and provide a range of ecosystem goods and services.
Similar content being viewed by others
References
Abràmoff MD, Magalhães PJ, Ram SJ (2004) Image processing with ImageJ. Biophoton Int 11:36–42
Adams DJ (2004) Fungal cell wall chitinases and glucanases. Microbiology 150:2029–2035
Anderson MJ (2006) Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62:245–253
Anderson MJ, Walsh DC (2013) PERMANOVA, ANOSIM, and the Mantel test in the face of heterogeneous dispersions: What null hypothesis are you testing? Ecol Monogr 83:557–574
Bailey D, Mazurak AP, Rosowski JR (1973) Aggregation of soil particles by algae. J Phycol 9:99–101
Barger NN, Herrick JE, Van Zee J, Belnap J (2006) Impacts of biological soil crust disturbance and composition on C and N loss from water erosion. Biogeochemistry 77:247–263
Bell CW, Fricks BE, Rocca JD, et al. (2013) High-throughput fluorometric measurement of potential soil extracellular enzyme activities. J Vis Exp:e50961
Belnap J (2003a) Microbes and microfauna associated with biological soil crusts. In: Belnap J, Lange OL (eds) Biological soil crusts: structure, function, and Management. Springer-Verlag, Berlin, pp. 167–174
Belnap J (2003b) The world at your feet: desert biological soil crusts. Front Ecol Environ 1:181–189
Belnap J (2006) The potential roles of biological soil crusts in dryland hydrologic cycles. Hydrol Process 20:3159–3178
Belnap J, Gillette DA (1998) Vulnerability of desert biological soil crusts to wind erosion: the influences of crust development, soil texture, and disturbance. J Arid Environ 39:133–142
Belnap J, Büdel B, Lange OL (2003) Biological soil crusts: characteristics and distribution. In: Belnap J, Lange OL (eds) Biological soil crusts: structure, function, and Management. Springer-Verlag, Berlin, pp. 3–30
Bhattacharya D, Nagpure A, Gupta RK (2007) Bacterial chitinases: properties and potential. Crit Rev Biotechnol 27:21–28
Biswas SR, Mallik AU (2010) Disturbance effects on species diversity and functional diversity in riparian and upland plant communities. Ecology 91:28–35
Bokhorst S, Asplund J, Kardol P, Wardle DA (2015) Lichen physiological traits and growth forms affect communities of associated invertebrates. Ecology 96:2394–2407
Botta-Dukát Z (2005) Rao’s quadratic entropy as a measure of functional diversity based on multiple traits. J Veg Sci 16:533–540
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
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, Maestre FT, Mau RL (2013) Diversity and patch-size distributions of biological soil crusts regulate dryland ecosystem multifunctionality. Ecosystems 16:923–933
Buck WR, Vitt DH (2006) Key to the Genera of Australian Mosses. Flora of Australia Volume 51, Australian Biological Resources Study, Canberra, 2002).
Bureau of Meteorology (2015) Bureau of Meteorology, Australian Government http://www.bom.gov.au/. Accessed 20 Aug 2015.
Cadotte MW, Carscadden K, Mirotchnick N (2011) Beyond species: functional diversity and the maintenance of ecological processes and services. J Appl Ecol 48:1079–1087
Campbell DH (1904) Resistance of drought by liverworts. Torreya 4:81–86
Castillo AP, Maestre FT, Palacios P, et al. (2008) Evaluando el papel funcional de la biodiversidad y el patrón espacial: Una aproximación experimental utilizando la costra biológica como modelo. In: Maestre FT, Escudero A, Bonet A (eds) Introducción al análisis espacial de datos en ecología y ciencias ambientales: métodos y aplicaciones. Universidad Rey Juan Carlos, Móstoles, pp. 617–635
Castillo-Monroy AP, Bowker MA, García-Palacios P, Maestre FT (2015) Aspects of soil lichen biodiversity and aggregation interact to influence subsurface microbial function. Plant Soil 386:303–316
Catcheside DG (1980) Mosses of South Australia. S.A. Govt, Printer, Adelaide
Chown S, Scholtz C (1989) Cryptogam herbivory in Curculionidae (Coleoptera) from the sub-antarctic Prince Edward Islands. The Coleopterists’ Bulletin 43:165–169
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
R Core Team (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/.
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 51:335–380
Cornelissen JH, Lang SI, Soudzilovskaia NA, During HJ (2007) Comparative cryptogam ecology: a review of bryophyte and lichen traits that drive biogeochemistry. Ann Bot 99:987–1001
Cornwell WK, Schwilk LDW, Ackerly DD (2006) A trait-based test for habitat filtering: convex Hull volume. Ecology 87:1465–1471
Daly GT (1970) Bryophyte and lichen indicators of air pollution in Christchurch, New Zealand. Proceedings of the New Zealand Ecological Society 17:70–79
Danin A, Ganor E (1991) Trapping of airborne dust by mosses in the Negev Desert, Israel. Earth Surf Process Landf 16:153–162
De Bello F, Lavorel S, Díaz S, et al. (2010) Towards an assessment of multiple ecosystem processes and services via functional traits. Biodivers Conserv 19:2873–2893
Delgado-Baquerizo M, Gallardo A, Covelo F, et al. (2015) Differences in thallus chemistry are related to species-specific effects of biocrust-forming lichens on soil nutrients and microbial communities. Funct Ecol 29:1087–1098
Díaz S, Cabido M (2001) Vive la difference: plant functional diversity matters to ecosystem processes. Trends Ecol Evol 16:646–655
Díaz S, Lavorel S, de Bello F, et al. (2007) Incorporating plant functional diversity effects in ecosystem service assessments. Proc Natl Acad Sci U S A 104:20684–20689
Duff SM, Sarath G, Plaxton WC (1994) The role of acid phosphatases in plant phosphorus metabolism. Physiol Plant 90:791–800
Eldridge DJ (1996) Distribution and floristics of terricolous lichens in soil crusts in arid and semi-arid new South Wales, Australia. Aust J Bot 44:581–599
Eldridge DJ (1998) Trampling of microphytic crusts on calcareous soils, and its impact on erosion under rain-impacted flow. Catena 33:221–239
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 Research 32:389–415
Eldridge DJ, Koen TB (1998) Cover and floristics of microphytic soil crusts in relation to indices of landscape health. Plant Ecol 137:101–114
Eldridge DJ, Leys JF (1999) Wind dispersal of the vagant lichen Chondropsis semiviridis in semi-arid Eastern Australia. Aust J Bot 47:157–164
Eldridge DJ, Leys JF (2003) Exploring some relationships between biological soil crusts, soil aggregation and wind erosion. J Arid Environ 53:457–466
Eldridge DJ, Rosentreter RR (1999) Morphological groups: a framework for monitoring microphytic crusts in arid landscapes. J Arid Environ 41:11–25
Eldridge DJ, Tozer ME (1996) Distribution and floristics of bryophytes in soil crusts in semi-arid and arid Eastern Australia. Aust J Bot 44:223–247
Ernst R, Linsenmair KE, Rӧdel M-O (2006) Diversity erosion beyond the species level: dramatic loss of functional diversity after selective logging in two tropical amphibian communities. Biol Conserv 133:143–155
Escolar C, Maestre FT, Rey A (2015) Biocrusts modulate warming and rainfall exclusion effects on soil respiration in a semi-arid grassland. Soil Biol Biochem 80:9–17
Filson RB, Rogers RW (1979) Lichens of South Australia. Government Printer, South Australia
Galun M, Braun A, Frensdorff A, Galun E (1976) Hyphal walls of isolated lichen fungi. Arch Microbiol 108:9–16
Gavazov KS, Soudzilovskaia NA, van Logtestijn RS, et al. (2010) Isotopic analysis of cyanobacterial nitrogen fixation associated with subarctic lichen and bryophyte species. Plant Soil 333:507–517
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 18:413–420
Giordani P, Incerti G, Rizzi G, et al. (2013) Functional traits of cryptogams in Mediterranean ecosystems are driven by water, light and substrate interactions. J Veg Sci 25:778–792
Gower JC (1971) A general coefficient of similarity and some of its properties. Biometrics 27:857–871
Huneck S (1999) The significance of lichens and their metabolites. Naturwissenschaften 86:559–570
Kunstler G, Falster D, Coomes DA, et al. (2016) Plant functional traits have globally consistent effects on competition. Nature 529:204–207.
Laliberté E, Legendre P (2010) A distance-based framework for measuring functional diversity from multiple traits. Ecology 91:299–305
Larney FJ, Bullock MS, Janzen HH, et al. (1998) Wind erosion effects on nutrient redistribution and soil productivity. J Soil Water Conserv 53:133–140
Lavorel S (2013) Plant functional effects on ecosystem services. J Ecol 101:4–8
Lavorel S, Garnier E (2002) Predicting changes in community composition and ecosystem functioning from plant traits: revisiting the Holy Grail. Funct Ecol 16:545–556
Leys JF, Eldridge DJ (1998) Influence of cryptogamic crust disturbance to wind erosion on sand and loam rangeland soils. Earth Surf Process Landf 23:963–974
Llop E, Pinho P, Matos P, et al. (2012) The use of lichen functional groups as indicators of air quality in a Mediterranean urban environment. Ecol Indic 13:215–221
Maechler M, Rousseeuw P, Struyf A, et al. (2015) cluster: Cluster Analysis Basics and Extensions. R package version 2.0.3. http://CRAN.R-project.org/package=cluster. Accessed 10 Aug 2015.
Maier S, Schmidt TS, Zheng L, et al. (2014) Analyses of dryland biological soil crusts highlight lichens as an important regulator of microbial communities. Biodivers Conserv 23:1735–1755
Malcolm R (1983) Assessment of phosphatase activity in soils. Soil Biol Biochem 15:403–408
Matos P, Pinho P, Aragón G, et al. (2015) Lichen traits responding to aridity. J Ecol 103:451–458
McCarthy PM (1991) The lichen genus Endocarpon Hedwig in Australia. Lichenologist 23:27–52
McCarthy PM (2006). Checklist of Australian liverworts and Hornworts. Australian Biological Resources Study, Canberra Viewed 06 March 2016. http://www.anbg.gov.au/abrs/liverwortlist/liverworts_intro.html
McCarthy PM (2015) Checklist of Australian Lichenicolous fungi. Australian Biological Resources Study, Canberra Version 10 December 2015. http://www.anbg.gov.au/abrs/lichenlist/Lichenicolous_Fungi.html
McIntyre S, Lavorel S, Landsberg J, Forbes T (1999) Disturbance response in vegetation-towards a global perspective on functional traits. J Veg Sci 10:621–630
Mendoza-Aguilar DO, Cortina J, Pando-Moreno M (2014) Biological soil crust influence on germination and rooting of two key species in a Stipa tenacissima steppe. Plant Soil 375:267–274
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 37:114–126
Mokany K, Raison R, Prokushkin AS (2006) Critical analysis of root: shoot ratios in terrestrial biomes. Glob Chang Biol 12:84–96
Moore C, Scott GAM (1979) The ecology of mosses on a sand dune in Victoria, Australia. J Bryol 10:291–311
Muzzarelli RAA (2011) Chitin nanostructures in living organisms. In: Gupta NS (ed) Chitin: Formation and Diagenesis. Springer, Dordrecht, pp. 1–34
Naeem S, Wright JP (2003) Disentangling biodiversity effects on ecosystem functioning: deriving solutions to a seemingly insurmountable problem. Ecol Lett 6:567–579
Oksanen J, Blanchet FG, Kindt R, et al. (2015) Vegan: community ecology package. R Package Version 2.3. http://CRAN.R-project.org/package=vegan. Accessed 10 Aug 2015.
Pérez-Harguindeguy N, Díaz S, Garnier E, et al. (2013) New handbook for standardised measurement of plant functional traits worldwide. Aust J Bot 61:167–234
Petchey OL, Gaston KJ (2002) Functional diversity (FD), species richness and community composition. Ecol Lett 5:402–411
Pimentel D, Harvey C, Resosudarmo P, et al. (1995) Environmental and economic costs of soil erosion and conservation benefits. Science 267:1117–1122
Pinho P, Dias T, Cruz C, et al. (2011) Using lichen functional diversity to assess the effects of atmospheric ammonia in Mediterranean woodlands. J Appl Ecol 48:1107–1116
Pinho P, Bergamini A, Carvalho P, et al. (2012) Lichen functional groups as ecological indicators of the effects of land-use in Mediterranean ecosystems. Ecol Indic 15:36–42
Read CF, Duncan DH, Vesk PA, Elith J (2014) Biocrust morphogroups provide an effective and rapid assessment tool for drylands. J Appl Ecol 51:1740–1749
Reynolds R, Belnap J, Reheis M, et al. (2001) Aeolian dust in Colorado Plateau soils: nutrient inputs and recent change in source. Proc Natl Acad Sci U S A 98:7123–7127
Rogers R, Lange R (1972) Soil surface lichens in arid and subarid South-Eastern Australia. I Introduction and floristics. Aust J Bot 20:197–213
Sancho LG, Green TA, Pintado A (2007) Slowest to fastest: extreme range in lichen growth rates supports their use as an indicator of climate change in Antarctica. Flora - Morphology, Distribution, Functional Ecology of Plants 202:667–673
Schachtman DP, Reid RJ, Ayling SM (1998) Phosphorus uptake by plants: from soil to cell. Plant Physiol 116:447–453
Scott GAM (1985) Southern Australian liverworts. Australian Government Publishing Service, Canberra
Scott GAM, Stone IG (1976) The mosses of Southern Australia. Australian Government Publishing Service, Canberra
Solow A, Polasky S, Broadus J (1993) On the measurement of biological diversity. J Environ Econ Manag 24:60–68
Soule T, Anderson IJ, Johnson SL, et al. (2009) Archaeal populations in biological soil crusts from arid lands in North America. Soil Biol Biochem 41:2069–2074
Su Y-G, Li X, Zheng J-G, Huang G (2009) The effect of biological soil crusts of different successional stages and conditions on the germination of seeds of three desert plants. J Arid Environ 73:931–936
Villéger S, Mason NWH, Mouillot D (2008) New multidimensional functional diversity indices for a multifaceted framework in functional ecology. Ecology 89:2290–2301
Villéger S, Miranda JR, Hernández DF, Mouillot D (2010) Contrasting changes in taxonomic vs. functional diversity of tropical fish communities after habitat degradation. Ecol Appl 20:1512–1522
Warton DI, Wright ST, Wang Y (2012) Distance-based multivariate analyses confound location and dispersion effects. Methods Ecol Evol 3:89–101
Westoby M, Wright IJ (2006) Land-plant ecology on the basis of functional traits. Trends Ecol Evol 21:261–268
White RP, Nackoney J (2003) Drylands, people, and ecosystem goods and services: a Web-based Geospatial analysis. World Resources Institute. http://pdf.wri.org/drylands. Accessed 30 Jan 2012.
Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer, New York
Acknowledgments
We are grateful to Manuel Delgado-Baquerizo for his assistance in developing the enzyme methods. We also thank Samantha Travers, Henri Dubourdieu, Sarah Barkman and Jason Chan, who helped to prepare samples. We are grateful to Martin Mallen-Cooper for helping to design and construct the portable wind tunnel used in this study.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Jeff R. Powell .
Rights and permissions
About this article
Cite this article
Mallen-Cooper, M., Eldridge, D.J. Laboratory-based techniques for assessing the functional traits of biocrusts. Plant Soil 406, 131–143 (2016). https://doi.org/10.1007/s11104-016-2870-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-016-2870-9