Skip to main content

Advertisement

SpringerLink
Log in

The influence of cushion plants on soil fertility islands under their canopies with ontogenesis in an extreme alpine ecosystem

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

Abstract

Purpose

Alpine cushion plants are known as “nurse plants” in alpine ecosystems. Soil fertility islands underneath the cushion canopies are responsible for their nursing potential. However, little is known about how cushion plants affect fertility islands under their canopies with ontogenesis.

Methods

To assess the influence of cushion plants on soil fertility islands under their canopies with ontogenesis. Three sizes (substitution ontogenesis) of Thylacospermum caespitosum were studied. Soil samples beneath the T. caespitosum canopy (generated soils and base soil were respectively collected) and in its’ surrounding area (the bare ground) were sampled. Then, the litter content, soil nutrient, and soil microbial biomass were measured.

Results

The litter content, most nutrient availability, and soil microbial biomass carbon and nitrogen were higher in generated soils than in the bare ground soil and base soil (P < 0.05), and this tendency increased with size. In the generated soils, levels of litter, soil organic carbon, and ammonium nitrogen were 2.4, 4.9, 4.8 and (small-sized), 8.3, 6.9, and 8.1 (medium-sized), 8.5, 9.9, and 9.8 (large-sized) times higher than in the bare ground soil. Soil microbial biomass carbon and nitrogen were 4.6 and 2.1 (medium-sized) and 5.8 and 2.5 (large-sized) times higher than bare ground soil.

Conclusion

Generated soils were the core of fertility islands built by T. caespitosum in extreme alpine ecosystems. The fertility islands beneath cushions were built with generated soils and associated with ontogenesis.

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
Fig. 6
Fig. 7

Similar content being viewed by others

Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Allegrezza M, Corti G, Cocco S, Pesaresi S, Chirico GB, Saracino A, Bonanomi G (2016) Microclimate buffering and fertility island formation during Juniperus communis ontogenesis modulate competition–facilitation balance. J Veg Sci 27:616–627

    Article  Google Scholar 

  • Armas C, Kim JH, Bleby TM, Jackson RB (2012) The effect of hydraulic lift on organic matter decomposition, soil nitrogen cycling, and nitrogen acquisition by a grass species. Oecologia 168:11–22

    Article  PubMed  Google Scholar 

  • Arroyo MTK, Cavieres LA, Peñaloza A, Arroyo-Kalin MA (2003) Positive associations between the cushion plant Azorella monantha (Apiaceae) and alpine plant species in the Chilean Patagonian Andes. Plant Ecol 169:121–129

    Article  Google Scholar 

  • Aubert S, Boucher F, Lavergne S, Renaud J, Choler P (2014) 1914–2014: A revised worldwide catalogue of cushion plants 100 years after Hauri and Schröter. Alp Bot 124:59–70

    Article  Google Scholar 

  • Behie SW, Bidochka MJ (2014) Nutrient transfer in plant–fungal symbioses. Trends Plant Sci 19:734–740

    Article  CAS  PubMed  Google Scholar 

  • Berendse F (1994) Litter decomposability–a neglected component of plant fitness. J Ecol 82:187–190

    Article  Google Scholar 

  • Bonanomi G, Stinca A, Chirico GB, Ciaschetti G, Saracino A, Incerti G (2016) Cushion plant morphology controls biogenic capability and facilitation effects of Silene acaulis along an elevation gradient. Funct Ecol 30:1216–1226

    Article  Google Scholar 

  • Butterfield BJ, Cavieres LA, Callaway RM, Cook BJ, Kikvidze Z, Lortie CJ, ... Brooker RW (2013) Alpine cushion plants inhibit the loss of phylogenetic diversity in severe environments. Ecol Lett 16:478–486

  • Byers JE, Cuddington K, Jones CG, Talley TS, Hastings A, Lambrinos JG, Crooks JA, Wilson WG (2006) Using ecosystem engineers to restore ecological systems. Trends Ecol Evol 21:493–500

    Article  PubMed  Google Scholar 

  • Cavieres LA, Badano EI, Sierra-Almeida A, Molina-Montenegro MA (2007) Microclimatic modifications of cushion plants and their consequences for seedling survival of native and non-native herbaceous species in the high Andes of central Chile. Arct Antarct Alp Res 39:229–236

    Article  Google Scholar 

  • Cavieres LA, Brooker RW, Butterfield BJ, Cook BJ, Kikvidze Z, Lortie CJ, ... Callaway RM (2014) Facilitative plant interactions and climate simultaneously drive alpine plant diversity. Ecol Lett 17:193–202

  • Cavieres LA, Badano EI, Sierra-Almeida A, Gomez-Gonzalez S, Molina-Montenegro MA (2006) Positive interactions between alpine plant species and the nurse cushion plant Laretia acaulis do not increase with elevation in the Andes of central Chile. New Phytol 169:59–69

    Article  PubMed  Google Scholar 

  • Chang S, Chen J, Su J, Yang Y, Sun H (2018) Seasonal comparison of bacterial communities in rhizosphere of alpine cushion plants in the Himalayan Hengduan Mountains. Plant Divers 40:209–216

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen J, Yang Y, Stöcklin J, Cavieres LA, Peng D, LiZ SH (2015) Soil nutrient availability determines the facilitative effects of cushion plants on other plant species at high elevations in the south-eastern Himalayas. Plant Ecol Divers 8:199–210

    Article  Google Scholar 

  • Chen J, Zhang Y, Zhang H, Schöb C, Wang S, Chang S, Sun H (2021) The positive effects of the alpine cushion plant Arenaria polytrichoides on insect dynamics are determined by both physical and biotic factors. Sci Total Environ 762:143091

    Article  CAS  PubMed  Google Scholar 

  • Combrinck ML, Harms TM, McGeoch MA, Schoombie J, Le Roux PC (2020) Wind and seed: a conceptual model of shape-formation in the cushion plant Azorella Selago. Plant Soil 455:339–366

    Article  CAS  Google Scholar 

  • Dolezal J, Dvorsky M, Kopecky M, Altman J, Mudrak O, Capkova K, ...Liancourt P (2019) Functionally distinct assembly of vascular plants colonizing alpine cushions suggests their vulnerability to climate change. Ann Bot-London 123:569–578

  • Dvorský M, Doležal J, Kopecký M, Chlumská Z, Janatková K, Altman J, ... Řeháková K (2013) Testing the stress-gradient hypothesis at the roof of the world: effects of the cushion plant Thylacospermum caespitosum on species assemblages. PLoS One 8:e53514

  • Edwards KA, Jefferies RL (2013) Inter-annual and seasonal dynamics of soil microbial biomass and nutrients in wet and dry low-Arctic sedge meadows. Soil Biol Biochem 57:83–90

    Article  CAS  Google Scholar 

  • Escudero A, Giménez-Benavides L, Iriondo JM, Rubio A (2004) Patch dynamics and islands of fertility in a high mountain Mediterranean community. Arct Antarct Alp Res 36:518–527

    Article  Google Scholar 

  • Fernandez-Marin B, Saenz-Ceniceros A, Solanki T, Robson TM, Garcia-Plazaola JI (2021) Alpine forbs rely on different photoprotective strategies during spring snowmelt. Physiol Plantarum 172:1506–1517

    Article  CAS  Google Scholar 

  • Flora of China Editorial Committee (1999) Flora of China. Science Press, Beijing

    Google Scholar 

  • Frenot Y, Gloaguen J, Cannavacciuolo M, Bellido A (1998) Primary succession on glacier forelands in the subantarctic Kerguelen Islands. J Veg Sci 9:75–84

    Article  Google Scholar 

  • Gavazov KS (2010) Dynamics of alpine plant litter decomposition in a changing climate. Plant Soil 337:19–32

    Article  CAS  Google Scholar 

  • He Y, Xu X, Kueffer C, Zhang X, Shi P (2014) Leaf litter of a dominant cushion plant shifts nitrogen mineralization to immobilization at high but not low temperature in an alpine meadow. Plant Soil 383:415–426

    Article  CAS  Google Scholar 

  • He YT, Wang F, Niu B, Wang ZP, Li M, Shi PL, Zhang XZ (2022) The Facilitation of Restoration by Cushion Plant Androsace tapete in a Degraded Alpine Grassland. JRE 13:107–112

    Google Scholar 

  • Jonasson S, Michelsen A, Schmidt IK (1999) Coupling of nutrient cycling and carbon dynamics in the Arctic, integration of soil microbial and plant processes. Appl Soil Ecol 11:135–146

    Article  Google Scholar 

  • Kleier C, Rundel PW (2004) Microsite requirements, population structure and growth of the cushion plant Azorella compacta in the tropical Chilean Andes. Austral Ecol 29:461–470

    Article  Google Scholar 

  • Koch O, Tscherko D, Kandeler E (2007) Temperature sensitivity of microbial respiration, nitrogen mineralization, and potential soil enzyme activities in organic alpine soils. Glob Biogeochem Cycles 21:017

    Article  Google Scholar 

  • Körner C (2003) Alpine plant life. Springer, Berlin, p 344

    Book  Google Scholar 

  • Le Roux PC, McGeoch MA (2004) The use of size as an estimator of age in the subantarctic cushion plant, Azorella selago (Apiaceae). Arct Antarct Alp Res 36:509–517

    Article  Google Scholar 

  • Li F, Liu M, Li Z, Jiang C, Han F, Che Y (2013) Changes in soil microbial biomass and functional diversity with a nitrogen gradient in soil columns. Appl Soil Ecol 64:1–6

    Article  Google Scholar 

  • Li Y, Shi X, Wang N, Pu J, Yao T (2011) Concentration of trace elements and their sources in a snow pit from Yuzhu Peak, north–east Qinghai-Tibetan Plateau. Sci Cold Arid Reg 3:216–222

    Google Scholar 

  • Liczner AR, Lortie CJ (2014) A global meta-analytic contrast of cushion-plant effects on plants and on arthropods. PeerJ 2:e265

    Article  PubMed  PubMed Central  Google Scholar 

  • Lin Y, Han G, Zhao M, Chang SX (2010) Spatial vegetation patterns as early signs of desertification: A case study of a desert steppe in Inner Mongolia, China. Landscape Ecol 25:1519–1527

    Article  Google Scholar 

  • Lipson DA, Schmidt SK (2002) Kinetics of microbial processes and population growth in soil. The encyclopedia of environmental microbiology. Wiley and Sons, New York, pp 1748–1757

    Google Scholar 

  • Lipson DA, Schmidt SK (2004) Seasonal changes in an alpine soil bacterial community in the Colorado Rocky Mountains. Appl Environ Microb 70:2867–2879

    Article  CAS  Google Scholar 

  • Liu L, Gundersen P, Zhang W, Zhang T, Chen H, Mo JM (2015) Effects of nitrogen and phosphorus additions on soil microbial biomass and community structure in two reforested tropical forests. Sci Rep 5:14378

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • López-Angulo J, Pescador DS, Sánchez AM, Luzuriaga AL, Cavieres LA, Escudero A (2020) Impacts of climate, soil and biotic interactions on the interplay of the different facets of alpine plant diversity. Sci Total Environ 698:133960

    Article  PubMed  Google Scholar 

  • Lozano YM, Armas C, Hortal S, Casanoves F, Pugnaire FI (2017) Disentangling above-and below-ground facilitation drivers in arid environments: the role of soil microorganisms, soil properties and microhabitat New Phytol 216:1236–1246

  • Lu Q, Yang X, Dong C, Zhang Z, Zhang X, Zhu X (2011) Influence of pyrolysis temperature and time on the cellulose fast pyrolysis products: Analytical Py-GC/MS study. J Anal Appl Pyrol 92:430–438

    Article  CAS  Google Scholar 

  • Mainetti A, D’Amico M, Probo M, Quaglia E, RavettoEnri S, Celi L, Lonati M (2021) Successional herbaceous species affect soil processes in a high-elevation alpine proglacial chronosequence. Front Environ Sci 8:615499

    Article  Google Scholar 

  • Meier CL, Bowman WD (2008) Links between plant litter chemistry, species diversity, and below–ground ecosystem function. Proc Natl Acad Sci USA 105:19780–19785

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mihoč MAK, Giménez-Benavides L, Pescador DS, Sánchez AM, Cavieres LA, Escudero A (2016) Soil under nurse plants is always better than outside: a survey on soil amelioration by a complete guild of nurse plants across a long environmental gradient. Plant Soil 408:31–41

    Article  Google Scholar 

  • Minor MA, Babenko AB, Ermilov SG, Khaustov AA, Makarova OL (2016) Effects of cushion plants on high-altitude soil microarthropod communities: cushions increase abundance and diversity of mites (Acari), but not springtails (Collembola). Arct Antarct Alp Res 48:485–500

    Article  Google Scholar 

  • Molenda O, Reid A, Lortie CJ (2012) The alpine cushion plant Silene acaulis as foundation species: a bug’s-eye view to facilitation and microclimate. PLoS One 7:e37223

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Molina-Montenegro MA, Badano EI, Cavieres LA (2006) Cushion plants as microclimatic shelters for two ladybird beetles species in alpine zone of central Chile. Arct Antarct Alp Res 38:224–227

    Article  Google Scholar 

  • Nagy L, Grabherr G (2009) The biology of alpine habitats. Oxford University Press, Oxford

    Google Scholar 

  • Navarro-Cano JA, Goberna M, Valiente-Banuet A, Montesinos-Navarro A, García C, Verdú M (2014) Plant phylodiversity enhances soil microbial productivity in facilitation-driven communities. Oecologia 174:909–920

    Article  PubMed  Google Scholar 

  • Nelson DW, Sommers LE (1982) Organic matter. Methods of Soil Analysis Part2. Chemical and Microbiological Properties Second Edition. Agronamy (9 Part 2):574–579

  • Nuñez CI, Aizen MA, Ezcurra C (1999) Species associations and nurse plant effects in patches of high-Andean vegetation. J Veg Sci 10:357–364

    Article  Google Scholar 

  • Ochoa-Hueso R, Munzi S, Alonso R, Arróniz-Crespo M, Avila A, Bermejo V, ... Theobald M. R (2017) Ecological impacts of atmospheric pollution and interactions with climate change in terrestrial ecosystems of the Mediterranean Basin: Current research and future directions. Environ Pollut 227:194–206

  • Olsen SR, Sommers LE, Page AL (1982) Methods of soil analysis. Part, 2, 403–430

  • Pérez-Valera E, Verdú M, Navarro-Cano JA, Goberna M (2018) Resilience to fire of phylogenetic diversity across biological domains. Mol Ecol 27:2896–2908

    Article  PubMed  Google Scholar 

  • Pugnaire FI, Haase P, Puigdefábregas J, Cueto M, Clark SC, Incoll LD, Puigdefabregas J (1996) Facilitation and succession under the canopy of a leguminous shrub, Retama sphaerocarpa, in a semi-arid environment in south-east Spain. Oikos 76(3):455–464. https://doi.org/10.2307/3546339

  • Pugnaire FI, Pistón N, Macek P, Schöb C, Estruch C, Armas C (2020) Warming enhances growth but does not affect plant interactions in an alpine cushion species. Perspect Plant Ecol 44:125530

    Article  Google Scholar 

  • Reid AM, Lamarque LJ, Lortie CJ (2010) A systematic review of the recent ecological literature on cushion plants: champions of plant facilitation. Web Ecol 10:44–49

    Article  Google Scholar 

  • Rodríguez-Echeverría S, Delgado-Baquerizo M, Morillo JA, Gaxiola A, Manzano M, Marquet PA, ... Armas C (2021) Azorella cushion plants and aridity are important drivers of soil microbial communities in Andean ecosystems. Ecosystems 24:1576–1590

  • Rodríguez-Echeverría S, Pérez-Fernández MA (2003) Soil fertility and herb facilitation mediated by Retama sphaerocarpa. J Veg Sci 14:807–814

    Article  Google Scholar 

  • Roy J, Albert CH, Choler P, Clément JC, Ibanez S, Lavergne S, ... Geremia RA (2013) Microbes on the cliff: alpine cushion plants structure bacterial and fungal communities. Front Microbiol 4:64

  • Roy J, Bonneville JM, Saccone P, Ibanez S, Albert CH, Boleda M, ... Geremia RA (2018) Differences in the fungal communities nursed by two genetic groups of the alpine cushion plant, Silene acaulis. Ecol Evol 8:11568–11581

  • Schinner F (1982) Soil microbial activities and litter decomposition related to altitude. Plant Soil 65:87–94

    Article  Google Scholar 

  • Schlesinger WH, Reynolds JF, Cunningham GL, Huenneke LF, Jarrell WM, Virginia RA, Whitford WG (1990) Biological feedbacks in global desertification. Science 247:1043–1048

    Article  CAS  PubMed  Google Scholar 

  • Sklenár P (2007) Temperature environment of Xenophyllum humile (Kunth) VA Funk, a high Andean cushion plant. Arnaldoa 14:97–104

    Google Scholar 

  • Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19:703–707

    Article  CAS  Google Scholar 

  • Vogel B, Rostagno CM, Antilef M, La Manna L (2021) Cushion shrubs encroach subhumid rangelands: fertility islands in fragile soils along a grazing gradient in patagonia. Res Square. https://doi.org/10.21203/rs.3.rs-730754/v1

  • Volkov IV, Volkova II (2015) More than just a plant: cushion plants as biodiversity protectors in high mountains of Siberia. Int J Environ Anal Chem 72:474–489

    Google Scholar 

  • Wang C, Michalet R, Liu Z, Jiang X, Wang X, Zhang G, ... Xiao S (2020) Disentangling large-and small-scale abiotic and biotic factors shaping soil microbial communities in an alpine cushion plant system. Front Microbiol 11:925

  • Wang Y, Sun J, Liu B, Wang J, Zeng T (2021) Cushion plants as critical pioneers and engineers in alpine ecosystems across the Tibetan Plateau. Authorea. https://doi.org/10.22541/au.162098021.11170496/v1

  • Wu X, Dong S, Liu S, Liu SL, Su XK, Han YH, Shi JB, Zhang Y, Zhao ZZ, Sha W, Zhang X, Gao F, Xu DH (2017) Predicting the shift of threatened ungulates’ habitats with climate change in Altun Mountain National Nature Reserve of the Northwestern Qinghai-Tibetan Plateau. Clim Change 142:331–344

    Article  Google Scholar 

  • Xing TT, Liu YQ, Wang NL, Shen L, Gu ZQ, Guo BX (2016) The physiological characteristics of culturable bacteria in Muztag、Yuzhufeng and Zadang glaciers on Tibetan Plateau, China. J Glaciol Geocryol 38:528–538

    Google Scholar 

  • Xue Z, An S, Cheng M, Wang W (2014) Plant functional traits and soil microbial biomass in different vegetation zones on the Loess Plateau. J Plant Interact 9:889–900

    Article  CAS  Google Scholar 

  • Yang Y, Chen JG, Schöb C, Sun H (2017) Size-mediated interaction between a cushion species and other non-cushion species at high elevations of the Hengduan Mountains. SW China Front Plant Sci 8:465

    PubMed  Google Scholar 

  • Yang Z, Gao J, Zhao L, Xu X, Ouyang H (2012) Linking thaw depth with soil moisture and plant community composition: effects of permafrost degradation on alpine ecosystems on the Qinghai-Tibet Plateau. Plant Soil 367:687–700

    Article  Google Scholar 

  • Yang Y, Niu Y, Cavieres LA, Sun H (2010) Positive associations between the cushion plant Arenaria polytrichoides (Caryophyllaceae) and other alpine plant species increase with altitude in the Sino-Himalayas. J Veg Sci 21:1048–1057

    Article  Google Scholar 

  • Zak DR, Holmes WE, White DC, Peacock AD, Tilman D (2003) Plant diversity, soil microbial communities, and ecosystem function: are there any links? Ecology 84:2042–2050

    Article  Google Scholar 

  • Zhao RM, Zhang H, An LZ (2018) Thylacospermum caespitosum population structure and cushion species community diversity along an altitudinal gradient. Environ Sci Pollut R 25:28998–29005

    Article  Google Scholar 

  • Zhao R, An L (2021) Plant size of the alpine cushion Thylacospermum caespitosum affects soil amelioration at different elevations. Plant Ecol 222:323–335

    Article  Google Scholar 

Download references

Funding

This work was supported by Scientific Research Startup Funds for Openly-recruited Doctors of Gansu Agricultural University (GAU-KYQD-2019–02).

Author information

Authors and Affiliations

  1. College of Agronomy, Gansu Agricultural University, No. 1 Yingmen Village, Anning District, 730070 Lanzhou, Gansu, China

    Ruiming Zhao

Authors
  1. Ruiming Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Investigation, sample collection and measurement, data collection and analysis, and the manuscript writing were performed by Ruiming Zhao. Author read and approved the final manuscript.

Corresponding author

Correspondence to Ruiming Zhao.

Ethics declarations

Competing interests

The authors have no relevant financial or non-financial interests to disclose.

Additional information

Responsible Editor: Mian Gu.

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhao, R. The influence of cushion plants on soil fertility islands under their canopies with ontogenesis in an extreme alpine ecosystem. Plant Soil 484, 379–392 (2023). https://doi.org/10.1007/s11104-022-05798-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-022-05798-3

Keywords

Search

Navigation