Biocrust tissue traits as potential indicators of global change in the Mediterranean
- 425 Downloads
Background and aims
Functional traits are promising indicators of global changes and ecosystem processes. Trait responses to environmental conditions have been examined widely in vascular plants. In contrast, few studies have focused on soil lichens and mosses composing biocrusts. We aimed to evaluate the potential of biocrust tissue traits as indicators of changes in climate and soil properties.
Isotope ratios and nutrient content in biocrust tissue were analyzed in 13 Mediterranean shrublands along an aridity gradient. Differences in tissue traits between biocrust groups (lichens and mosses), and relationships between tissue traits and climatic and soil variables were examined.
Lichens and mosses differed in δ13C, δ15N and N content, indicating distinct physical and physiological attributes. Tissue traits correlated strongly with numerous climatic variables, likely due to a modulator effect on biocrust water relations and metabolism. We found contrasting responses of lichen and moss traits to climate, although they responded similarly to soil properties. Overall, the most responsive trait was δ15N, suggesting this trait is the best to reflect integrated processes occurring in the atmosphere and soil.
Biocrust tissue traits arise as cost-effective, integrative ecological indicators of global change drivers in Mediterranean ecosystems, with potential applications in response-effect trait frameworks.
KeywordsIsotope ratios Tissue nutrient content Biocrusts Climate Soil Mediterranean
LCZ was supported by a Marie Curie IEF grant from European Commission’s FP7 (BCSES-GA 628406). PM was supported by FCT-MEC through: project PTDC/AAG-GLO/0045/2014. Special thanks to C. Tejada, M. Köbel, A. Nunes, M. Lo Cascio, L. Morillas, and S. Mereu for help in the field, T. Roovers for the assistance in the laboratory and R. Maia for the isotope and elemental analysis. Special thanks also to Professor M. Aleffi (Bryology Laboratory & Herbarium, Camerino University) for his assistance on moss species identification. We also thank P. Pinho who provided valuable comments on the manuscript. M.A. Bowker and other anonymous reviewers provided helpful comments and discussion that improved an earlier version of the manuscript.
- Ayres E, Van der Wal R, Sommerkorn M, Bardgett RD (2006) Direct uptake of soil nitrogen by mosses. Biol Lett 2:286–288Google Scholar
- Branquinho C, Matos P, Pinho P (2015) Lichens as ecological indicators to track atmospheric changes: future challenges. In: Lindenmayer D, Barton P, Pierson J (eds) Indicators and surrogates of biodiversity and environmental change. CSIRO Publishing, Melbourne, CRC Press, London, pp 77–87Google Scholar
- Bremner JM (1996) Nitrogen-total. In: Sparks DL et al (eds) Methods of soil analysis part 3-chemical methods. Soil science Society of America Inc, Madison, pp 1085–1121Google Scholar
- Combs SM, Nathan MV (1998) Soil organic matter. In: Brown JR (ed) Recommended Chemical Soil Test Procedures for the North Central Region. NCR Research Publication, Columbia, pp 53–58Google Scholar
- Concostrina-Zubiri L, Molla I, Velizarova E, Branquinho C (2016) Grazing or Not Grazing: Implications for Ecosystem Services Provided by Biocrusts in Mediterranean Cork Oak Woodlands. Land Degrad Dev. https://doi.org/10.1002/ldr2573
- Cruz de Carvalho R, Bernardes da Silva A, Soares R, Almeida AM, Coelho AV, Marques da Silva, Branquinho C (2014) Differential proteomics of dehydration and rehydration in bryophytes: evidence towards a common desiccation tolerance mechanism. Plant Cell Environ 37:1499–1515CrossRefPubMedGoogle Scholar
- Cuna S, Balas G, Hauer E (2007) Effects of natural environmental factors on δ13C of lichens. Isot Environ Health Stud 43:95–104Google Scholar
- Eldridge DJ, Rosentreter R (1999) Morphological groups: a framework for monitoring microphytic crusts in arid landscapes. J Arid Environ 41:11–25Google Scholar
- Hevia V, Martín-López B, Palomo S, García-Llorente M, Bello F, González JA (2017) Trait-based approaches to analyze links between the drivers of change and ecosystem services: synthesizing existing evidence and future challenges. Ecol Evol. https://doi.org/10.1002/ece3.2692
- Hill MO, Preston CD, Bosanquet SDS, Roy DB (2007) Bryoatt: Attributes Of British And Irish Mosses, Liverworts And Hornworts. Centre for Ecology & Hydrology, HuntingdonGoogle Scholar
- IPCC (2007) Climate Change 2007: Synthesis Report, pp 73Google Scholar
- IPCC (2014) Climate Change 2014: Synthesis Report Contribution of Working Groups I II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate ChangeGoogle Scholar
- Izquieta-Rojano S, Elustondo D, Ederra A, Lasheras E, Santamaría C, Santamaría JM (2016) Pleurochaete Squarrosa (Brid.) Lindb. As an alternative moss species for biomonitoring surveys of heavy metal, nitrogen deposition and δ15N signatures in a Mediterranean area. Ecol Indic 60:1221–1228CrossRefGoogle Scholar
- Kappen L, Valladares F (2007) Opportunistic Growth and Desiccation Tolerance: The Ecological Success of Poikilohydrous Autotrophs. In: Pugnaire F, Valladares F (eds) Functional Plant Ecology, 2nd edn. Taylor and Francis, New York, pp 7–65Google Scholar
- Máguas M, Griffiths H, Ehleringer J, Serodio J (1993) Characterization of photobiont associations in lichens using carbon isotope discrimination techniques. In: Ehleringer JR, Hall AE, Farquhar GD (eds) Stable Isotopes and Plant Water Relations. Academic Press, San Diego, pp 201–212Google Scholar
- Matos P (2016) Development of ecological indicators of climate change based on lichen functional diversity. Universidade de AveiroGoogle Scholar
- McCune B, Mefford MJ (2011) PC-ORD multivariate analysis of ecological data version 608. MjM Software, Gleneden BeachGoogle Scholar
- McCune B, Grace JB, Urban DL (2002) Analysis of ecological communities. MjM software design, Gleneden BeachGoogle Scholar
- 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 37:114–126Google Scholar
- Nimis PL (2016) The Lichens of Italy. A Second Annotated Catalogue. EUT, Trieste, pp 739Google Scholar
- Nimis PL, Scheidegger C, Wolseley PA (2002) Monitoring with lichens – monitoring lichens. Kluwer Academic Publisher, NetherlandsGoogle Scholar
- Pinho P, Branquinho C, Cruz C, Tang YS, Dias T, Rosa AP, Máguas C, Martins-Loução MA, Sutton MA (2009) Assessment of critical levels of atmospheric ammonia for lichen diversity in cork-oak woodland Portugal. In: Sutton MA, Reis S, Baker SMH (eds) Atmosheric ammonia. Springer, Berlin, pp 109–119CrossRefGoogle Scholar
- R Core Team (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/
- Rosso A, Neitlich P, Smith RJ (2014) Non-destructive lichen biomass estimation in Northwestern Alaska: a comparison of methods. PloS ONE 9:e103739Google Scholar
- Royles J, Amesbury MJ, Roland TP, Jones GD, Convey P, Griffiths H, Charman DJ (2016) Moss stable isotopes (carbon-13 oxygen-18) and testate amoebae reflect environmental inputs and microclimate along a latitudinal gradient on the Antarctic peninsula. Oecologia 181:931–945CrossRefPubMedPubMedCentralGoogle Scholar
- Solga A, Burkhardt J, Zechmeister HG, Frahm JP (2005) Nitrogen content 15N natural abundance and biomass of the two pleurocarpous mosses Pleurozium schreberi (Brid) mitt and Scleropodium purum (Hedw) Limpr in relation to atmospheric nitrogen deposition. Environ Pollut 134:465–473CrossRefPubMedGoogle Scholar
- van den Driessche R (1979) Proceedings. Forest Fertilization Conference, University of Washington, WA, USAGoogle Scholar
- Xiao B, Hu K, Ren T, Li B (2016) Moss-dominated biological soil crusts significantly influence soil moisture and temperature regimes in semiarid ecosystems. Geoderma 263:35–46Google Scholar
- Zwolicki A, Zmudczyńska-Skarbek K, Richard P, Stempniewicz L (2016) Importance of marine-derived nutrients supplied by planktivorous seabirds to high Arctic tundra plant communities. PLoS ONE 11:e0154950Google Scholar