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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

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Abstract

Aims

Soil under nurse plants is more fertile than in the harsh surroundings. This is a primary mechanism involved in plant to plant facilitation and it is critical in structuring plant communities under stressful conditions. However we do not know how this soil enrichment process varies along complex environmental gradients and among coexisting nurse plants.

Methods

Soil properties related to structure, resource stocks and microbial activity, were compared among up to ten nurse plant species and adjacent barren soil areas, along a 1600 m elevation gradient above the treeline in central Chilean Andes. Shifts in Relative Interaction Index (RII) sensu Armas (Ecology 85: 2682–2686, 2004) and in coefficient of variation on soil properties were also modelled.

Results

Soil under nurse plants was always richer than on barren areas irrespective of altitude, except in the case of texture with more small particles in the intermediate altitude. β-glucosidase activity was higher under cushion plants than under nurse plants with other growth habit. Besides β-glucosidase and phosphatase activities were more variable at higher altitudes. Nitrogen was more variable under nurse plants than in barren areas and its RII values were lower at intermediate altitudes.

Conclusions

Soil amelioration by nurse plants occurred all along the studied environmental gradient promoting islands of fertility and a general increase on soil niches heterogeneity.

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Abbreviations

RII:

Relative Interaction Index

PSD:

Particle Size Distribution

EC:

Electric Conductivity

References

  • Aguiar MR, Sala OE (1999) Patch structure, dynamics and implications for the functioning of arid ecosystems. Trends Ecol Evol 14:273–277

    Article  PubMed  Google Scholar 

  • Anthelme F, Dangles O (2012) Plant–plant interactions in tropical alpine environments. Perspect Plant Ecol Evol Syst 14:363–372

    Article  Google Scholar 

  • Anthelme F, Buendia B, Mazoyer C, Dangles O (2012) Unexpected mechanisms sustain the stress gradient hypothesis in a tropical alpine environment. J Veg Sci 23:62–72

    Article  Google Scholar 

  • Antonsson H, Björk RG, Molau U (2009) Nurse plant effect of the cushion plant Silene acaulis (L.) Jacq. in an alpine environment in the subarctic Scandes, Sweden. Plant Ecol Divers 2:17–25

    Article  Google Scholar 

  • Armas C, Ordiales R, Pugnaire FI (2004) Measuring plant interactions: a new comparative index. Ecology 85:2682–2686

    Article  Google Scholar 

  • Arroyo MTK, Cavieres LA, Peñaloza A, Arroyo-Kalin M (2003) Positive association between the cushion plant Azorella monantha (Apiaceae) and alpine plant species in the Chilean Patagonian Andes. Plant Ecol 161:121–129

    Article  Google Scholar 

  • Badano EI, Cavieres LA (2006) Impacts of ecosystem engineers on community attributes: effects of cushion plants at different elevations of the Chilean Andes. Divers Distrib 12:388–396

    Article  Google Scholar 

  • Badano EI, Marquetb PA, Cavieres LA (2010) Predicting effects of ecosystem engineering on species richness along primary productivity gradients. Acta Oecol 36(1):46–54

    Article  Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S (2014). lme4: Linear mixed-effects models using Eigen and S4. R package version 1.1–6. http://CRAN.R-project.org/package=lme4

  • Bertness MD, Hacker SS (1994) Physical stress and positive association among marsh plants. Am Nat 144(3):363–372

    Article  Google Scholar 

  • Bonanomi G, Incerti G, Mazzoleni S (2011) Assessing occurrence, specificity, and mechanisms of plant facilitation in terrestrial ecosystems. Plant Ecol 212:1777–1790

  • Bremner JM (1965) Inorganic forms of nitrogen. In Black CA et al. (eds.) Methods of soil analysis. Part 2. Agronomy Monograph. 9. ASA, Madison pp 1179–1237

  • Callaway RM, Howard TG (2007). Competitive networks, indirect interactions, and allelopathy: a microbial viewpoint on plant communities. In Progress in Botany. Springer, Berlin, pp 317–335

  • Callaway RM, Brooker RW, Choler P, Kikvidze Z, Lortie CJ, Michalet R (2002) Positive interactions among alpine plants increase with stress. Nature 417:844–848

    Article  CAS  PubMed  Google Scholar 

  • Casanova-Katny MA, Torres-Mellado GA, Palfner G, Cavieres LA (2011) The best for the guest: high Andean nurse cushions of Azorella madreporica enhance arbuscular mycorrhizal status in associated plant species. Mycorrhiza 21:613–622

    Article  PubMed  Google Scholar 

  • Cavieres LA, Badano EI (2009) Do facilitative interactions increase species richness at the entire community level? J Ecol 97:1181–1191

    Article  Google Scholar 

  • Cavieres LA, Peñaloza A, Arroyo MTK (2000) Altitudinal vegetation belts in the high-Andes of central Chile. Rev Chil Hist Nat 73:331–344

    Article  Google Scholar 

  • Cavieres LA, Mary TK, Peñaloza AA, Molina-Montenegro MA (2002) Nurse effect of Bolax gummifera cushion plants in the alpine vegetation of the Chilean Patagonian Andes. J Veg Sci 13(4):547–554

    Google Scholar 

  • Cavieres LA, Badano EI, Sierra-Almeida A, Gómez-González A, 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 

  • 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, Quiroz CL, Molina-Montenegro MA (2008) Facilitation of the non-native Taraxacum officinale by native nurse cushion species in the high Andes of central Chile: are there differences between nurses? Funct Ecol 22:148–156

    Article  Google Scholar 

  • Cavieres LA, Brooker RW, Butterfield BJ, Cook BJ, Kikvidze Z, Lortie CJ, Michalet R, Pugnaire FI, Schöb C, Xiao S, Anthelme F, Björk RG, Dickinson KJM, Cranston BH, Gavilán R, Gutiérrez-Girón A, Kanka R, Maalouf J-P, Mark AF, Noroozi J, Parajuli R, Phoenix GK, Reid AM, Ridenour WM, Rixen C, Wipf S, Zhao L, Escudero A, Zaitchik BF, Lingua E, Aschehoug ET, Callaway RM (2014) Facilitative plant interactions and climate simultaneously drive alpine plant diversity. Ecol Lett 17:193–202

  • Charley JL, West NE (1975) Plant-induced soil chemical patterns in some shrub-dominated semi-desert ecosystems of Utah. J Ecol 63:945–963

    Article  CAS  Google Scholar 

  • Chen J, Yang Y, Stöcklin J, Cavieres L, Peng D, Lif Z, Sun H (2014) 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 

  • Crain CM, Bertness MD (2005) Community impacts of a tussock sedge: is ecosystem engineering important in benign habitats? Ecology 86:2695–2704

    Article  Google Scholar 

  • Crain CM, Bertness MD (2006) Ecosystem engineering across environmental gradients: implications for conservation and management. Bioscience 56:211–218

    Article  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 

  • Escudero A, Palacio S, Maestre FT, Luzuriaga AL (2015) Plant life on gypsum: a review of its multiple facets. Biol Rev 90:1–18

    Article  PubMed  Google Scholar 

  • Flores J, Jurado E (2003) Are nurse-protege interactions more common among plants from arid environments? J Veg Sci 14:911–916

    Article  Google Scholar 

  • Eskelinen A, Stark S, Mannisto M (2009) Links between plant community composition, soil organic matter quality and microbial communities in contrasting tundra habitats. Oecologia 161(1):113–123

  • Fox J, Weisberg S (2011) An R Companion to Applied Regression, 2nd edn http://z.umn.edu/carbook. Sage, Thousand Oaks CA

    Google Scholar 

  • Ghazoul J (2006) Floral diversity and the facilitation of pollination. J Ecol 94:295–304

    Article  Google Scholar 

  • Giménez-Benavides L, Escudero A, Iriondo JM (2007) Reproductive limits of a late-flowering high mountain Mediterranean plant along an elevational climate gradient. New Phytol 173:367–382

    Article  PubMed  Google Scholar 

  • Gómez-Aparicio L, Zamora R, Gómez JM (2005) Regeneration status of the endangered Acer opalus subsp. granatense throughout its geographical distribution in the Iberian peninsula. Biol Conserv 121:195–206

    Article  Google Scholar 

  • Holmgren M, Scheffer M, Huston MA (1997) The interplay of facilitation and competition in plant community. Ecology 78:1966–1975

    Article  Google Scholar 

  • Körner C (2003) Alpine plant life: functional plant ecology of high mountain ecosystems. Springer, Germany

    Book  Google Scholar 

  • Kuznetsova A, Brockhoff PB, Christensen RHB (2014). lmerTest: Tests in Linear Mixed Effects Models. R package version 2.0–20. http://CRAN.R-project.org/package=lmerTest

  • Michalet R, Xiao S, Touzard B, Smith DS, Cavieres LA, Callaway RM, Whitham O (2011) Phenotypic variation in nurse traits and community feedbacks define an alpine community. Ecol Lett 14(5):433–443

    Article  PubMed  Google Scholar 

  • Moora M, Zobel M (2010) Arbuscular mycorrhizae and plant-plant interactions. In: Pugnaire FI (ed) Positive Plant Interactions and Community Dynamics. CRC Press, Boca Ratón, FL, USA, pp. 79–98

  • Nuñez CI, Aizen MA, Ezcurra C (1999) Species associations and nurse plant effects in patches of high-Andean vegetation. J Veg Sci 10(3):357–364

    Article  Google Scholar 

  • R Core Team (2015) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna

  • Rebollo S, Milchunas DG, Noy-Meir I, Chapman PL (2002) The role of a spiny plant refuge in structuring grazed shortgrass steppe plant communities. Oikos 98:53–64

    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 

  • Reynolds JF, Stafford-Smith MD, Lambin EF, Turner BLII, Mortimore M, Batterbury J, et al. (2007) Global desertification: building a science for dryland development. Science 316:847–851

    Article  CAS  PubMed  Google Scholar 

  • Rietkerk M, Dekker M, Ruiter K, van de Koppel J (2004) Self-organized patchiness and catastrophic shifts in ecosystems. Science 305:1926–1932

    Article  CAS  PubMed  Google Scholar 

  • Roy J, Albert CH, Ibanez S, et al. (2013) Microbes on the cliff: alpine cushion plants structure bacterial and fungal communities. Front Microbiol 4:64

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schlesinger WH, Pilmanis AM (1998) Plant-soil interactions in deserts. Biogeochemistry 42:168–187

    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 

  • Seastedt TR, Vaccaro L (2001) Plant species richness, productivity, and nitrogen and phosphorous limitations across a snowpack gradient in alpine tundra, Colorado, USA. Arct Antarct Alp Res 33(1):100–106

    Article  Google Scholar 

  • Tabatabai MA (1982) Soil enzymes. In: Page AL, Miller RH, Keeney DR (Eds.), Methods of Soil Analysis. Part 2. Agronomical Monograph No. 9. 2nd ed. American Society of Agronomy and Soil Science of America, Madison, pp 501–538

  • Tabatabai MA, Bremner JM (1969) Use of p-nitrophenyl phosphate in assay of soil phosphatase activity. Soil Biol Biochem 1:301–307

    Article  CAS  Google Scholar 

  • Wentworth CK (1922) A scale of grade and class terms for clastic sediments. J Geol 30(5):377–392

    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 

  • Yeaton RI (1978) A cyclical relationship between Larrea tridentata and Opuntia leptocaulis in the northern Chihuahuan Desert. J Ecol 66:651–656

    Article  Google Scholar 

  • Zinger L, Lejon DPH, Baptist F, et al. (2011) Contrasting diversity patterns of crenarchaeal, bacterial and fungal soil communities in an alpine landscape. PLoS One 6:e19950. doi:10.1371/journal.pone.0019950

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This work was supported by the projects REMEDINAL-3CM (S2013/MAE-2719), ROOTS (CGL2015-66809-P), and we also thank F.T. Maestre for his support through the BIOCON06 ⁄ 105 project.

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Correspondence to A. M. Sánchez.

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Responsible Editor: Jeffrey Walck.

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Mihoč, M.A.K., Giménez-Benavides, L., Pescador, D.S. et al. 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 (2016). https://doi.org/10.1007/s11104-016-2908-z

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