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Biocrust moss populations differ in growth rates, stress response, and microbial associates

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Abstract

Aims

A growing body of research supports the feasibility of biocrust rehabilitation. Identifying populations of key species that are amenable to cultivation and that are resilient in rehabilitation contexts would advance the efficacy of these technologies. Here we investigate the growth and stress response of the cosmopolitan biocrust moss, Syntrichia ruralis.

Methods

We sampled populations of S. ruralis along a precipitation seasonality gradient from the Colorado Plateau ecoregion of the western United States. We cultivated these populations in an experiment manipulating duration of hydration periods on a weekly cycle. We then treated greenhouse grown materials with brief, stressful watering events, measuring how many events they could survive.

Results

All populations grew at an accelerated rate compared to growth in a natural setting, at least doubling biomass in five months. Increasing duration of hydration periods led to more growth in all but one population. Volunteer biocrust algae and cyanobacteria developed during cultivation, and differed among populations. Greenhouse grown mosses differed in their response to stressful watering, with the most susceptible populations dying at half the number events compared to the most tolerant.

Conclusions

These findings argue for informed selection and deployment of Syntrichia ruralis populations for soil rehabilitation.

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References

  • Anderson MJ (2001) Permutation tests for univariate or multivariate analysis of variance and regression. Can J Fish Aquat Sci 58:626–639

    Article  Google Scholar 

  • Antoninka AJ, Bowker MA, Reed SC, Doherty KD (2015) Production of greenhouse-grown biocrust mosses and associated cyanobacteria to rehabilitate dryland soil function. Restor Ecol 24:324–335

    Article  Google Scholar 

  • Barker DH, Stark LR, Zimpfer JF, Mcletchie ND, Smith SD (2005) Evidence of drought-induced stress on biotic crust moss in the Mojave Desert. Plant Cell Environ 28:939–947

    Article  Google Scholar 

  • Belnap J, Gardner JS (1993) Soil microstructure in soils of the Colorado plateau: the role of the cyanobacterium Microcoleus vaginatus. West North Am Naturalist 53:40–47

    Google Scholar 

  • Belnap J, Lange OL (2003) Structure and functioning of biological soil crusts: a synthesis. In: Belnap J, Lange OL (eds) Biological soil crusts: structure, function, and management. Springer, Berlin, Heidelberg, pp  471-479

  • Belnap J, Reynolds RL, Reheis MC, Phillips SL, Urban FE, Goldstein HL (2009) Sediment losses and gains across a gradient of livestock grazing and plant invasion in a cool, semi-arid grassland, Colorado Plateau, USA. Aeol Res 1:27-43

  • Bowker MA, Stark LR, McLetchie DN, Mishler BD (2000) Sex expression, skewed sex ratios, and microhabitat distribution in the dioecious desert moss Syntrichia caninervis (Pottiaceae). Am J Bot 87:517–526

    Article  PubMed  CAS  Google Scholar 

  • Bowker MA (2007) Biological soil crust rehabilitation in theory and practice: an underexploited opportunity. Restor Ecol 15:13–23

    Article  Google Scholar 

  • Bowker MA, Antoninka AJ (2016) Rapid ex situ culture of N-fixing soil lichens and biocrusts is enhanced by complementarity. Plant Soil 408:415–428

    Article  CAS  Google Scholar 

  • Bowker MA, Belnap J, Büdel B, Sannier C, Pietrasiak N, Eldridge DJ, Rivera-Aguilar V (2016) Controls on distribution patterns of biological soil crusts at micro- to global scales. In: Weber B, Büdel B, Belnap J (eds) Biological soil crusts: an organizing principle in drylands. Springer-Verlag, Berlin, pp 173–197

  • Bowker MA, Antoninka A, Durham A (2017) Applying community ecological theory to maximize productivity of cultivated biocrusts. Ecol Appl. https://doi.org/10.1002/eap.1582

  • Brinda JC, Stark LR, Clark TA, Greenwood JL (2015) Embryos of a moss can be hardened to desiccation tolerance: effects of rate of drying on the timeline of recovery and dehardening in Aloina ambigua (Pottiaceae). Ann Bot 117:153–163

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bu C, Wang C, Yang Y, Zhang L, Bowker MA (2017) Physiological protective responses of artificial moss biocrusts to dehydration-rehydration cycles and heat stress on the loess plateau. Journal of Arid Land 9:419–431

    Article  Google Scholar 

  • Chen L, Xie Z, Hu C, Li D, Wang G, Liu Y (2006) Man-made desert algal crusts as affected by environmental factors in Inner Mongolia, China. J Arid Environ 67:521–527

    Article  Google Scholar 

  • Coe K, Belnap J, Sparks J (2012) Precipitation-driven carbon balance controls survivorship of desert biocrust mosses. Ecology 93:1626–1636

    Article  PubMed  Google Scholar 

  • Condon LA, Pyke DA (2016) Filling the interspace—restoring arid land mosses: source populations, organic matter, and overwintering govern success. Ecol Evol 6:7623–7632

    Article  PubMed  PubMed Central  Google Scholar 

  • Cook BI, Miller RL, Seager R (2009) Amplification of the north American “dust bowl” drought through human-induced land degradation. Proc Natl Acad Sci USA 106:4997–5001

    Article  PubMed  Google Scholar 

  • Doherty KD, Antoninka AJ, Bowker MA, Ayuso SV,  Johnson NC (2015) A novel approach to cultivate biocrusts for restoration and experimentation. Ecol Restor 33:13-16

  • Garcia-Pichel F, Sherry ND, Castenholz RW (1993) Evidence for an ultraviolet sunscreen role of the extracellular pigment scytonemin in the terrestrial cyanobacterium Chlorogloeopsis sp. Photochem Photobiol 56:17–23

    Article  Google Scholar 

  • Green TA, Sancho LG, Pintado A (2011) Ecophysiology of desiccation/rehydration cycles in mosses and lichens. In: Jenks MA, Wood AJ (eds) Plant desiccation tolerance. Springer, Berlin, Heidelberg, pp 89–120

  • Griffin DW, Kellogg CA (2004) Dust storms and their impact on ocean and human health: dust in Earth’s atmosphere. EcoHealth 1:284–295

    Article  Google Scholar 

  • Hereford J (2009) A quantitative survey of local adaptation and fitness trade-offs. Am Nat 173:579–588

    Article  PubMed  Google Scholar 

  • Johnson GR, Sorensen FC, St. Clair JB, Cronn RC (2004) Pacific northwest Forest tree seed zones a template for native plants? Native Plants J 5:131–140

    Article  Google Scholar 

  • Johnson R, Stritch L, Olwell P, Lambert S, Horning ME, Cronn R (2010) What are the best seed sources for ecosystem restoration on BLM and USFS lands? Native Plants Journal 11:117–131

    Article  Google Scholar 

  • Langlet O (1971) Revising some terms of intra-specific differentiation. Hereditas 68:277–280

    Article  Google Scholar 

  • Langsrud Ø (2003) ANOVA for unbalanced data: use type II instead of type III sums of squares. Stat Comput 13:163–167

    Article  Google Scholar 

  • Leimu R, Fischer M (2008) A meta-analysis of local adaptation in plants. PLoS One 3:e4010

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Linhart YB, Grant MC (1996) Evolutionary significance of local genetic difference in plants. Annu Rev Ecol Syst 27:237–277

    Article  Google Scholar 

  • Mazor G, Kidron GJ, Vonshak A, Abeliovich A (1996) The role of cyanobacterial exopolysaccharides in structuring desert microbial crusts. FEMS Microbiol Ecol 21:121–130

    Article  CAS  Google Scholar 

  • Nath V, Asthana AK (2001) Reproductive biology of bryophytes. In: Johri BM, Srivastava PS (eds) Reproductive Biology of Plants. Springer, Berlin, Heidelberg, pp 148–174

  • Okin GS, Gillette DA (2001) Distribution of vegetation in wind-dominated landscapes: implications for wind erosion modeling and landscape processes. J Geophys Res-Atmos 106:9673–9683

    Article  Google Scholar 

  • Painter TH, Deems JS, Belnap J, Hamlet AF, Landry CC, Udall B (2010) Response of Colorado River runoff to dust radiative forcing in snow. Proc Natl Acad Sci 107:17125–17130

    Article  PubMed  Google Scholar 

  • Paasch AE, Mishler BD, Nosratinia S, Stark LR, Fisher KM (2015) Decoupling of sexual reproduction and genetic diversity in the female-biased Mojave Desert moss Syntrichia caninervis (Pottiaceae). Int J Plant Sci 176:751–761

    Article  Google Scholar 

  • Peppin DL, Fulé PZ, Lynn JC, Mottek-Lucas AL, Hull Sieg C (2010) Market perceptions and opportunities for native plant production on the southern Colorado plateau. Restor Ecol 18:113–124

    Article  Google Scholar 

  • Pointing SB, Belnap J (2012) Microbial colonization and controls in dryland systems. Nat Rev Microbiol 10:551–562

    Article  PubMed  CAS  Google Scholar 

  • R Core Team (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/

  • Reed SC, Coe KK, Sparks JP, Housman DC, Zelikova TJ, Belnap J (2012) Changes to dryland rainfall result in rapid moss mortality and altered soil fertility. Nat Clim Chang 2:752–755

    Article  CAS  Google Scholar 

  • Reski R, Abel WO (1985) Induction of budding on chloronemata and caulonemata of the moss, Physcomitrella patens, using isopentenyladenine. Planta 165:354–358

    Article  PubMed  CAS  Google Scholar 

  • Rosentreter R, Bowker M, Belnap J (2007) Syntrichia ruralis. In: Rosentreter R, Bowker M, Belnap J (eds) A field guide to biological soil crusts of western US drylands: common lichens and bryophytes. U.S. Government Printing Office, Denver, Colorado, pp 23

  • Seager R, Ting M, Held I, Kushnir Y, Lu J, Vecchi G et al (2007) Model projections of an imminent transition to a more arid climate in southwestern North America. Science 316:1181–1184

    Article  PubMed  CAS  Google Scholar 

  • Shaw N, Pellant M, Fisk M, Denney E (2012) A collaborative program to provide native plant materials for the Great Basin. Rangelands 34:11–16

    Article  Google Scholar 

  • Stark LR, Brinda JC, McLetchie DN, Oliver MJ (2012) Extended periods of hydration do not elicit dehardening to desiccation tolerance in regeneration trials of the moss Syntrichia caninervis. Int J Plant Sci 173:333–343

    Article  CAS  Google Scholar 

  • Stark LR, Mishler BD, McLetchie DN (2000) The cost of realized sexual reproduction: assessing patterns of reproductive allocation and sporophyte abortion in a desert moss. Am J Bot 87:1599–1608

    Article  PubMed  CAS  Google Scholar 

  • Stark LR, Nichols L, McLetchie DN, Smith SD, Zundel C (2004) Age and sex-specific rates of leaf regeneration in the Mojave Desert moss Syntrichia caninervis. Am J Bot 91:1–9

    Article  PubMed  Google Scholar 

  • Xu S, Yin C, He M, Wang Y (2008) A technology for rapid reconstruction of moss-dominated soil crusts. Environ Eng Sci 25:1129–1138

    Article  CAS  Google Scholar 

  • Xu SJ, Jiang PA, Wang ZW, Wang Y (2009a) Crystal structures and chemical composition of leaf surface wax depositions on the desert moss Syntrichia caninervis. Biochem Syst Ecol 37:723–730

    Article  CAS  Google Scholar 

  • Xu SJ, Liu CJ, Jiang PA, Cai WM, Wang Y (2009b) The effects of drying following heat shock exposure of the desert moss Syntrichia caninervis. Sci Total Environ 407:2411–2419

    Article  PubMed  CAS  Google Scholar 

  • Weber W, Wittman RC (2007) Syntrichia. In: Weber W, Wittman RC (eds) Bryophytes of Colorado. Pilgrims Process, United States, pp 127-130

  • Weber B, Bowker M, Zhang Y, Belnap J (2016) Natural Recovery of Biological Soil Crusts After Disturbance. In: Weber B, Büdel B, Belnap J (eds) Biological Soil Crusts: An Organizing Principle in Drylands, 1 edn. Springer, Switzerland, pp 479-498

  • Yeager CM, Kuske CR, Carney TD, Johnson SL, Ticknor LO, Belnap J (2012) Response of biological soil crust diazotrophs to season, altered summer precipitation, and year-round increased temperature in an arid grassland of the Colorado plateau, USA. Front Microbiol 3:358

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang B, Zhang Y, Zhao J, Wu N, Chen R, Zhang J (2009) Microalgal species variation at different successional stages in biological soil crusts of the Gurbantunggut Desert, northwestern China. Biol Fertil Soils 45:539–547

    Article  Google Scholar 

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Acknowledgements

We would like to thank the United States Bureau of Land Management and Colorado Plateau Native Plant Program for funding this research. We would also like to thank Ana Giraldo Silva for assistance with identification of algae and cyanobacteria. Finally, we would like to thank Jeffrey Wright for his help with the stress experiment.

Author information

Authors and Affiliations

  1. School of Forestry, Northern Arizona University, 200 East Pine Knoll Dr., PO Box 15018, Flagstaff, AZ, 86011, USA

    Kyle D. Doherty, Matthew A. Bowker & Anita J. Antoninka

  2. School of Earth Sciences and Environmental Sustainability, Northern Arizona University, Flagstaff, AZ, 86011, USA

    Nancy C. Johnson

  3. Department of Biological Sciences and Merriam-Powell Center for Environmental Research, Northern Arizona University, Flagstaff, AZ, 86011, USA

    Troy E. Wood

Authors
  1. Kyle D. Doherty
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  2. Matthew A. Bowker
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  5. Troy E. Wood
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Corresponding author

Correspondence to Kyle D. Doherty.

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Responsible Editor: David John Eldridge

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Appendix S1

Patterns of mean percent cover (y-axis) of dominant taxa (color fill) differed over time (x-axis) across five Syntrichia ruralis populations (individual facets). (PNG 440 kb)

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Doherty, K.D., Bowker, M.A., Antoninka, A.J. et al. Biocrust moss populations differ in growth rates, stress response, and microbial associates. Plant Soil 429, 187–198 (2018). https://doi.org/10.1007/s11104-017-3389-4

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