Abstract
Background and aims
Biocrusts are communities of cyanobacteria, mosses, and/or lichens found in drylands worldwide. Biocrusts are proposed to enhance soil fertility and productivity, but simultaneously act as a barrier to the invasive grass, Bromus tectorum, in western North America. Both biocrusts and B. tectorum are sensitive to climate change drivers, yet how their responses might interact to affect dryland ecosystems is unclear.
Methods
Using mesocosms with bare soil versus biocrust cover, we germinated B. tectorum seeds collected from warmed, warmed + watered, and ambient temperature plots within a long-term climate change experiment on the Colorado Plateau, USA. We characterized biocrust influences on soil fertility and grass germination, morphology, and chemistry.
Results
Biocrusts increased soil fertility and B. tectorum biomass, specific leaf area (SLA), and root:shoot ratios. Germination rates were unaffected by mesocosm cover-type. Biocrusts delayed germination timing while also interacting with the warmed treatment to advance, and with the warmed + watered treatment to delay germination.
Conclusions
Biocrusts promoted B. tectorum growth, likely through positive influence on soil fertility which was elevated in biocrust mesocosms, and interacted with seed treatment-provenance to affect germination. Understanding how anticipated losses of biocrusts will affect invasion dynamics will require further investigation of how plant plasticity/adaptation to specific climate drivers interact with soil and biocrust properties.
This is a preview of subscription content, access via your institution.





References
Ågren GI, Franklin O (2003) Root: shoot ratios, optimization and nitrogen productivity. Ann Bot 92(6):795–800
Arianoutsou M, Delipetrou P, Vilà M, Dimitrakopoulos PG, Celesti-Grapow L, Wardell-Johnson G et al (2013) Comparative patterns of plant invasions in the Mediterranean biome. PLoS One 8(11):e79174
Baran R, Brodie EL, Mayberry-Lewis J, Hummel E, Da Rocha UN, Chakraborty R, Bowen BP, Karaoz U, Cadillo-Quiroz H, Garcia-Pichel F, Northen TR (2015) Exometabolite niche partitioning among sympatric soil bacteria. Nat Commun 6:8289
Barger NN, Weber B, Garcia-Pichel F, Zaady E, Belnap J (2016) Patterns and controls on nitrogen cycling of biological soil crusts. In: Weber B, Büdel B, Belnap J (eds) Biological soil crusts: an organizing principle in drylands (pp. 257–285). Springer International Publishing, New York
Belnap J, Phillips SL (2001) Soil biota in an ungrazed grassland: response to annual grass (Bromus tectorum) invasion. Ecol Appl 11(5):1261–1275
Belnap J, Warren SD (2002) Patton's tracks in the Mojave Desert, USA: an ecological legacy. Arid Land Res Manag 16:245–258
Belnap J, Prasse R, Harper KT (2001) Influence of biological soil crusts on soil environments and vascular plants. In: Belnap J, Lange OL (eds) Biological soil crusts: structure, function, and management (pp. 281–300). Springer, Berlin
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(1):63–76
Bestelmeyer BT, Okin GS, Duniway MC, Archer SR, Sayre NF, Williamson JC, Herrick JE (2015) Desertification, land use, and the transformation of global drylands. Front Ecol Environ 13(1):28–36
Bradford JB, Lauenroth WK (2006) Controls over invasion of Bromus tectorum: the importance of climate, soil, disturbance and seed availability. J Veg Sci 17(6):693–704
Bradley BA, Mustard JF (2005) Identifying land cover variability distinct from land cover change: cheatgrass in the Great Basin. Remote Sens Environ 94(2):204–213
Bradley BA, Curtis CA, Chambers JC (2016) Bromus response to climate and projected changes with climate change. In: Germino MJ, Chambers JC, Brown CS (eds) Exotic brome-grasses in arid and semi-arid ecosystems of the Western US: causes, consequences and management implications (pp. 257–274). Springer, New York
Chambers JC, Bradley BA, Brown CS, D’Antonio C, Germino MJ, Grace JB, Hardegree SP, Miller RF, Pyke DA (2014) Resilience to stress and disturbance, and resistance to Bromus tectorum L. invasion in cold desert shrublands of western North America. Ecosystems 17(2):360–375
Chambers JC, Germino MJ, Belnap J, Brown CS, Schupp EW, Clair SBS (2016) Plant community resistance to invasion by Bromus species: the roles of community attributes, Bromus interactions with plant communities, and Bromus traits. In: Germino MJ, Chambers JC, Brown CS (eds) Exotic brome-grasses in arid and semi-arid ecosystems of the Western US: causes, consequences and management implications (pp. 275–304). Springer, New York
Cheng L, Zhang N, Yuan M, Xiao J, Qin Y, Deng Y, Tu Q, Xue K, Van Nostrand JD, Wu L, He Z (2017) Warming enhances old organic carbon decomposition through altering functional microbial communities. ISME J 11:1825–1835
Chytrý M, Jarošík V, Pyšek P, Hájek O, Knollová I, Tichý L, Danihelka J (2008) Separating habitat invasibility by alien plants from the actual level of invasion. Ecology 89(6):1541–1553
Compagnoni A (2014) Warming, soil moisture, and loss of snow increase Bromus tectorum’s population growth rate. Elem Sci Anth 2:1–10
Compagnoni A, Adler PB (2014) Warming, competition, and Bromus tectorum population growth across an elevation gradient. Ecosphere 5(9):1–34
D’Antonio C, Vitousek P (1992) Biological invasions by exotic grasses, the grass/fire cycle, and global change. Annu Rev Ecol Syst 23:63–87
Deines L, Rosentreter R, Eldridge DJ, Serpe MD (2007) Germination and seedling establishment of two annual grasses on lichen-dominated biological soil crusts. Plant Soil 295(1–2):23–35
Didham RK, Tylianakis JM, Gemmell NJ, Rand TA, Ewers RM (2007) Interactive effects of habitat modification and species invasion on native species decline. Trends Ecol Evol 22(9):489–496
Donohue K (2002) Germination timing influences natural selection on life-history characters in Arabidopsis Thaliana. Ecology 83(4):1006–1016
Faist AM, Herrick JE, Belnap J, Van Zee JW, Barger NN (2017) Biological soil crust and disturbance controls on surface hydrology in a semi‐arid ecosystem. Ecosphere 8(3):e01691
Fenesi A, Rédei T, Botta-Dukát Z (2011) Hard traits of three Bromus species in their source area explain their current invasive success. Acta Oecol 37(5):441–448
Ferrenberg S, Reed SC (2017) Biocrust ecology: unifying micro-and macro-scales to confront global change. New Phytol 216(3):643–646
Ferrenberg S, Reed SC, Belnap J (2015) Climate change and physical disturbance cause similar community shifts in biological soil crusts. PNAS 112:12116–12121
Ferrenberg S, Tucker CL, Reed SC (2017) Biological soil crusts: diminutive communities of potential global importance. Front Ecol Environ 15(3):160–167
Germino MJ, Belnap J, Stark JM, Allen EB, Rau BM (2016) Ecosystem impacts of exotic annual invaders in the genus Bromus. In: Germino MJ, Chambers JC, Brown CS (Eds) Exotic brome-grasses in arid and semiarid ecosystems of the Western US: causes, consequences and management implications. Springer, New York
Godínez-Alvarez H, Morín C, Rivera-Aguilar V (2012) Germination, survival and growth of three vascular plants on biological soil crusts from a Mexican tropical desert. Plant Biol 14(1):157–162
Griffith AB, Andonian K, Weiss CP, Loik ME (2014) Variation in phenotypic plasticity for native and invasive populations of Bromus tectorum. Biol Invasions 16(12):2627–2638
Hufft RA, Zelikova TJ (2016) Ecological genetics, local adaptation, and phenotypic plasticity in Bromus tectorum in the context of a changing climate. In: Germino MJ, Chambers JC, Brown CS (eds) Exotic brome-grasses in arid and semi-arid ecosystems of the Western US: causes, consequences and management implications. Springer, New York
JMP Pro Version 13.0.0 (2016) SAS Institute Inc., Carry
Kanarek AR, Kao RH (2011) The relationships among plant cover, density, seed rain, and dispersal of Bromus tectorum in high-elevation populations. Western north. Am Nat 71(1):131–136
Kuo S (1996) Methods of soil analysis. Part 3: Chemical methods. In: Sparks DL (ed) Phosphorus. Soil Society of America, Madison, pp 869–919
Lavergne S, Molofsky J (2007) Increased genetic variation and evolutionary potential drive the success of an invasive grass. Proc Natl Acad Sci 104(10):3883–3888
Leger EA, Espeland EK, Merrill KR, Meyer SE (2009) Genetic variation and local adaptation at a cheatgrass (Bromus tectorum) invasion edge in western Nevada. Mol Ecol 18(21):4366–4379
Li J, Okin GS, Epstein HE (2009) Effects of enhanced wind erosion on surface soil texture and characteristics of windblown sediments. J Geophys Res 114:G02003
Lu JJ, Tan DY, Baskin JM, Baskin CC (2014) Germination season and watering regime, but not seed morph, affect life history traits in a cold desert diaspore-heteromorphic annual. PLoS One 9(7):e102018
Lu JJ, Tan DY, Baskin CC, Baskin JM (2016) Effects of germination season on life history traits and on transgenerational plasticity in seed dormancy in a cold desert annual. Sci Rep 6:25076
Lyles L, Tatarko J (1986) Wind erosion effects on soil texture and organic matter. J Soil Water Conserv 41(3):191–193
Mack RN (1981) Invasion of Bromus tectorum L. into western North America: an ecological chronicle. Agro-Ecosystems 7:145–165
Maestre FT, Eldridge DJ, Soliveres S, Kéfi S, Delgado-Baquerizo M, Bowker MA, García-Palacios P, Gaitán J, Gallardo A, Lázaro R, Berdugo M (2016) Structure and functioning of dryland ecosystems in a changing world. Annu Rev Ecol Evol Syst 47:215–237
Mitton JB, Ferrenberg SM (2012) Mountain pine beetle develops an unprecedented summer generation in response to climate warming. Am Nat 179(5):E163–E171
Monk C (1966) Ecological importance of root/shoot ratios. Bulletin of the Torrey Botanical Club 93(6):402–406
Olsen SR, Sommers LE (1982) Phosphorus. In: Page AL et al (eds) Methods of soil analysis, part 2, 2nd edn, Agron Monogr 9. ASA and ASSA, Madison, pp 403–430
Peltzer DA, Kurokawa H, Wardle DA (2016) Soil fertility and disturbance interact to drive contrasting responses of co-occurring native and nonnative species. Ecology 97(2):515–529
Pendleton RL, Pendleton BK, Howard GL, Warren SD (2003) Growth and nutrient content of herbaceous seedlings associated with biological soil crusts. Arid Land Res Manag 17(3):271–281
Peterjohn WT, Schlesinger WH (1990) Nitrogen loss from deserts in the southwestern United States. Biogeochemistry 10(1):67–79
Peterson EB (2013) Regional-scale relationship among biological soil crusts, invasive annual grasses, and disturbance. Ecol Process 2(1):2
Prevéy JS, Seastedt TR (2014) Seasonality of precipitation interacts with exotic species to alter composition and phenology of a semi-arid grassland. J Ecol 102(6):1549–1561
Prevéy JS, Seastedt TR (2015) Effects of precipitation change and neighboring plants on population dynamics of Bromus tectorum. Oecologia 179(3):765–775
PRISM Climate Group, Oregon State University (2017) http://prism.oregonstate.edu, created 1 June 2017
Pyke DA, Chambers JC, Beck JL, Brooks ML, Mealor BA (2016) Land uses, fire, and invasion: exotic annual Bromus and human dimensions. In: Germino MJ, Chambers JC, Brown CS (Eds) Exotic bromegrasses in arid and semi-arid ecosystems of the Western US: causes, consequences and management implications (pp. 307-337). Springer, New York
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(10):752–755
Reed SC, Maestre FT, Ochoa-Hueso R, Kuske CR, Darrouzet-Nardi A, Oliver M, Darby B, Sancho LG, Sinsabaugh RL, Belnap J (2016) Biocrusts in the context of global change. In: Weber B, Büdel B, Belnap J (eds) Biological soil crusts: an organizing principle in drylands (pp. 451-476). Springer International Publishing, New York
Reynolds JF, Smith DMS, Lambin EF, Turner BL, Mortimore M, Batterbury SP, Downing TE, Dowlatabadi H, Fernández RJ, Herrick JE, Huber-Sannwald E (2007) Global desertification: building a science for dryland development. Science 316:847–851
Rice KJ, Dyer AR (2001) Seed aging, delayed germination and reduced competitive ability in Bromus tectorum. Plant Ecol 155(2):237–243
Rimer RL, Evans RD (2006) Invasion of downy brome (Bromus tectorum L.) causes rapid changes in the nitrogen cycle. Am Midl Nat 156:252–258
Rutherford WA, Painter TH, Ferrenberg S, Belnap J, Okin GS, Flagg C, Reed SC (2017) Albedo feedbacks to future climate via climate change impacts on dryland biocrusts. Sci Rep 7:44188
Seastedt TR, Pyšek P (2011) Mechanisms of plant invasions of north American and European grasslands. Annu Rev Ecol Evol Syst 42:133–153
Serpe MD, Orm JM, Barkes T, Rosentreter R (2006) Germination and seed water status of four grasses on moss-dominated biological soil crusts from arid lands. Plant Ecol 185(1):163–178
Sokol NW, Kuebbing SE, Bradford MA (2017) Impacts of an invasive plant are fundamentally altered by a co-occurring forest disturbance. Ecology 98(8):2133–2144
Suding KN, Ashton IW, Bechtold H, Bowman WD, Mobley ML, Winkleman R (2008) Plant and microbe contribution to community resilience in a directionally changing environment. Ecol Monogr 78(3):313–329
Vasquez E, Sheley R, Svejcar T (2009) Nitrogen enhances the competitive ability of cheatgrass (Bromus tectorum) relative to native grasses. Invasive Plant Science and Management 1(3):287–295
West AM, Kumar S, Wakie T, Brown CS, Stohlgren TJ, Laituri M, Bromberg J (2015) Using high-resolution future climate scenarios to forecast Bromus tectorum invasion in Rocky Mountain National Park. PLoS One 10(2):e0117893
Yan Y, Xin X, Xu X, Wang X, Yang G, Yan R, Chen B (2013) Quantitative effects of wind erosion on the soil texture and soil nutrients under different vegetation coverage in a semiarid steppe of northern China. Plant Soil 369(1–2):585–598
Zelikova TJ, Hufbauer RA, Reed SC, Wertin T, Fettig C, Belnap J (2013) Eco‐evolutionary responses of Bromus tectorum to climate change: implications for biological invasions. Ecol Evol 3(5):1374–1387
Zhang Y, Aradottir AL, Serpe M, Boeken B (2016) Interactions of biological soil crusts with vascular plants. In: Weber B, Büdel B, Belnap J (eds) Biological soil crusts: an organizing principle in drylands (pp. 385-406). Springer International Publishing, New York
Acknowledgements
Our manuscript was improved by comments from two anonymous reviewers, R. Mann, and the editors. We thank Ed Grote and Robin Reibold for logistical support throughout this experiment. This work was supported by the Terrestrial Ecosystem Science Program of the U.S. Department of Energy’s Office of Biological and Environmental Research (award DESC-0008168) and by the U.S. Geological Survey Ecosystems Mission Area. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Matthew A. Bowker
Electronic supplementary material
Table S1
(XLSX 10 kb)
Rights and permissions
About this article
Cite this article
Ferrenberg, S., Faist, A.M., Howell, A. et al. Biocrusts enhance soil fertility and Bromus tectorum growth, and interact with warming to influence germination. Plant Soil 429, 77–90 (2018). https://doi.org/10.1007/s11104-017-3525-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-017-3525-1
Keywords
- Biocrusts
- Bromus tectorum
- Cheatgrass
- Drylands
- Nitrogen
- Phenotypic plasticity
- Provenance
- Soil fertility