Skip to main content
SpringerLink
Log in

An exotic plant species indirectly facilitates a secondary exotic plant through increased soil salinity

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

Indirect facilitation among exotic species may promote their establishment on ecosystems, causing biodiversity losses. However, few experimental studies have identified the mechanisms underlying the indirect facilitation among exotic species. In central-northern Chile, Mesembryanthemum crystallinum (Aizoaceae) is an exotic halophyte that increases soil salinity, while M. nodiflorum is another exotic halophyte –currently less dominant– that often co-occurs with M. crystallinum. In this study, we evaluated the indirect facilitation of M. nodiflorum by M. crystallinum which was mediated by the suppression of salt-susceptible native competitors via increased soil salinity. We further determined the relationship between salt-tolerance traits and the outcome of competitive interactions in saline soil. We included two native Asteraceae plants co-occurring with these Mesembryanthemum species: the –highly probable– salt-susceptible Helenium urmenetae and the salt-tolerant Amblyopappus pusillus. We combined field co-occurrence surveys with greenhouse germination and competition experiments. The Mesembryanthemum species tended to co-occur, which suggests facilitation. Further, the salinity level found under M. crystallinum significantly decreased germination and performance of H. urmenetae, but not of M. nodiflorum and A. pusillus. Accordingly, when in competition, the increased salinity counteracted the negative effect of H. urmenetae on M. nodiflorum biomass, giving M. nodiflorum a competitive advantage. These patterns were associated with decreased specific leaf area and crassulacean acid metabolism expression in M. nodiflorum. In contrast, A. pusillus and M. nodiflorum maintained a neutral interaction regardless of salinity. Overall, our results suggest that M. crystallinum, by increasing soil salinity, may reduce the performance of salt-susceptible competitors, indirectly facilitating the establishment of M. nodiflorum.

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

Similar content being viewed by others

Data Availability

Data will be made available in the Figshare repository upon acceptance.

Ethical approval.

This article does not contain any studies with human participants or animals performed by any of the authors.

References

  • Adams P, Nelson DE, Yamada S, Chmara W, Jensen RG, Bohnert HJ, Griffiths H (1998) Growth and development of Mesembryanthemum crystallinum (Aizoaceae). New Phytol 138:171–190

    Article  CAS  PubMed  Google Scholar 

  • Allen WJ, Wainer R, Tylianakis JM, Barratt BI, Shadbolt MR, Waller LP, Dickie IA (2020) Community-level direct and indirect impacts of an invasive plant favour exotic over native species. J Ecol 108(6):2499–2510

    Article  Google Scholar 

  • Arif Y, Singh P, Siddiqui H, Bajguz A, Hayat S (2020) Salinity induced physiological and biochemical changes in plants: an omic approach towards salt stress tolerance. Plant Physiol Biochem 156:64–77

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Baskin CC, Baskin JM (2014) Seeds: ecology, biogeography, and, evolution of dormancy and germination. Elsevier

  • Benitez L, Kendig AE, Adhikari A, Clay K, Harmon PF, Holt RD et al (2022) Invasive grass litter suppresses a native grass species and promotes disease. Ecosphere 13(1):e3907

    Article  Google Scholar 

  • Bohnert HJ, Cushman JC (2000) The ice plant Cometh: lessons in abiotic stress tolerance. J Plant Growth Regulat 19(3)

  • Braga RR, Gómez-Aparicio L, Heger T, Vitule JRS, Jeschke JM (2018) Structuring evidence for invasional meltdown: broad support but with biases and gaps. Biol Invasions 20(4):923–936

    Article  Google Scholar 

  • Bui EN (2013) Soil salinity: a neglected factor in plant ecology and biogeography. J Arid Environ 92:14–25

    Article  Google Scholar 

  • Butterfield BJ, Callaway RM (2013) A functional comparative approach to facilitation and its context dependence. Funct Ecol 27:907–917

    Article  Google Scholar 

  • Callaway RM (2007) Positive interactions and interdependence in plant communities. Springer, Dordrecht

    Google Scholar 

  • Campoy JG, Acosta AT, Affre L, Barreiro R, Brundu G, Buisson E, González L, Lema M, Novoa A, Retuerto R, Roiloa SR, Fagúndez J (2018) Monographs of invasive plants in Europe: Carpobrotus. Bot Lett 165(3–4):440–475

    Article  Google Scholar 

  • Carboni M, Calderon-Sanou I, Pollock L, Violle C, Thuiller W (2018) Functional traits modulate the response of alien plants along abiotic and biotic gradients. Glob Ecol Biogeogr 27(10):1173–1185

    Article  Google Scholar 

  • Carvajal DE, Loayza AP, Rios RS, Gianoli E, Squeo FA (2017) Population variation in drought-resistance strategies in a desert shrub along an aridity gradient: interplay between phenotypic plasticity and ecotypic differentiation. Perspectives in Plant Ecology. Evol Syst 29:12–19

    Google Scholar 

  • Cavieres LA (2021) Facilitation and the invasibility of plant communities. J Ecol 109:2019–2028

    Article  Google Scholar 

  • Chen D, van Kleunen M (2022) Invasional meltdown mediated by plant-soil feedbacks may depend on community diversity. New Phytol 235:1589–1598

    Article  PubMed  Google Scholar 

  • De Battisti D, Fowler MS, Jenkins SR, Skov MW, Bouma TJ, Neyland PJ, Griffin JN (2020) Multiple trait dimensions mediate stress gradient effects on plant biomass allocation, with implications for coastal ecosystem services. J Ecol 108:1227–1240

    Article  Google Scholar 

  • Dickie IA, St John MG, Yeates GW, Morse CW, Bonner KI, Orwin K, Peltzer DA (2014) Belowground legacies of Pinus contorta invasion and removal result in multiple mechanisms of invasional meltdown. AoB Plants 6:plu056

    Article  PubMed  Google Scholar 

  • Drenovsky RE, Grewell BJ, D’Antonio CM, Funk JL, James JJ, Molinari N, Parker IM, Richards CL (2012) A functional trait perspective on plant invasion. Ann Botany 110(1):141–153

    Article  Google Scholar 

  • El Shayeb FM, El Tantawy H, El Kholi A (2002) Phytosociological studies on the wild Mesembryanthemum species in Egypt: quantitative analysis of the representative communities. J Biol Sci 2:275–279

    Article  Google Scholar 

  • El-Ğhareeb R (1991) Vegetation and soil changes induced by Mesembryanthemum crystallinum L. in a Mediterranean desert ecosystem. J Arid Environ 20:321–330

    Article  Google Scholar 

  • Flory SL, Bauer JT (2014) Experimental evidence for indirect facilitation among invasive plants. J Ecol 1:12–18

    Article  Google Scholar 

  • Freckleton RP, Watkinson AR (2000) Designs for greenhouse studies of interactions between plants: an analytical perspective. J Ecol 88(3):386–391

    Article  Google Scholar 

  • Gotelli NJ (2000) Null model analysis of species co-occurrence patterns. Ecology 81:2606–2621

    Article  Google Scholar 

  • Gutterman Y, Gendler T (2005) Annual rhythm of germination of seeds of Mesembryanthemum nodiflorum 32 years after collection. Seed Sci Res 15(3):249–253

    Article  Google Scholar 

  • Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363

    Article  PubMed  Google Scholar 

  • Jordan NR, Larson DL, Huerd SC (2008) Soil modification by invasive plants: effects on native and invasive species of mixed-grass prairies. Biol Invasions 10:177–190

    Article  Google Scholar 

  • Kuebbing SE, Nuñez MA (2016) Invasive non-native plants have a greater effect on neighbouring natives than other non-natives. Nat Plants 2:1–7

    Article  Google Scholar 

  • Ladenburger CG, Hild AL, Kazmer DJ, Munn LC (2006) Soil salinity patterns in Tamarix invasions in the Bighorn Basin, Wyoming, USA. J Arid Environ 65(1):111–128

    Article  Google Scholar 

  • Levine JM (1999) Indirect facilitation: evidence and predictions from a riparian community. Ecology 80:1762–1769

    Article  Google Scholar 

  • MacDougall AS, Turkington R (2005) Are invasive species the drivers or passengers of change in degraded ecosystems? Ecology 86(1):42–55

    Article  Google Scholar 

  • Madriaza K, Saldaña A, Salgado-Luarte C, Escobedo VM, Gianoli E (2019) Chlorophyll fluorescence may predict tolerance to herbivory. Int J Plant Sci 180(1):81–85

    Article  Google Scholar 

  • Mathakutha R, Steyn C, le Roux PC, Blom IJ, Chown SL, Daru BH et al (2019) Invasive species differ in key functional traits from native and non-invasive alien plant species. J Veg Sci 30(5):994–1006

    Article  Google Scholar 

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence - a practical guide. J Exp Bot 51(345):659–668

    Article  CAS  PubMed  Google Scholar 

  • Molina-Montenegro MA, Palma-Rojas C, Alcayaga-Olivares Y, Oses R, Corcuera LJ, Cavieres LA, Gianoli E (2013) Ecophysiological plasticity and local differentiation help explain the invasion success of Taraxacum officinale (dandelion) in South America. Ecography 36:718–730

    Article  Google Scholar 

  • Morais MC, Panuccio MR, Muscolo A, Freitas H (2012) Salt tolerance traits increase the invasive success of Acacia longifolia in portuguese coastal dunes. Plant Physiol Biochem 55:60–65

    Article  CAS  PubMed  Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681

    Article  CAS  PubMed  Google Scholar 

  • Orrego F, De La Fuente LM, Gómez M, Ginocchio R (2018) Diversidad de halófitas chilenas: distribución, origen y hábito. Gayana Bot 75:555–567

    Article  Google Scholar 

  • Philbrick RN (1972) The plants of Santa Barbara Island, California. Madrono 21:329–393

    Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, Sarkar D (2020) nlme: Linear and Nonlinear Mixed Effects Models. R package version 3.1–148, https://CRAN.R-project.org/package=nlme

  • Prior KM, Adams DC, Klepzig KD, Hulcr J (2018) When does invasive species removal lead to ecological recovery? Implications for management success. Biol Invasions 20(2):267–283

    Article  Google Scholar 

  • Quezada IM, Saldaña A, Gianoli E (2017) Divergent patterns of selection on crassulacean acid metabolism photosynthesis in contrasting environments. Int J Plant Sci 178(5):398–405

    Article  Google Scholar 

  • Rodriguez LF (2006) Can invasive species facilitate native species? Evidence of how, when, and why these impacts occur. Biol Invasions 8(4):927–939

    Article  Google Scholar 

  • Rodríguez R, Marticorena C, Alarcón D, Baeza C, Cavieres L, Finot VL, Fuentes N, Kiessling A, Mihoc M, Pauchard A, Ruiz E, Sanchez P, Marticorena A (2018) Catálogo de las plantas vasculares de Chile. Gayana Bot 75:1–430

    Article  Google Scholar 

  • Roiloa SR, Yu FH, Barreiro R (2020) Plant invasions: mechanisms, impacts and management. Flora 267:151603

    Article  Google Scholar 

  • Saccone P, Pagès JP, Girel J, Brun JJ, Michalet R (2010) Acer negundo invasion along a successional gradient: early direct facilitation by native pioneers and late indirect facilitation by conspecifics. New Phytol 187(3):831–842

    Article  PubMed  Google Scholar 

  • Sayed OH, Hegazy AK (1994) Growth-specific phytomass allocation in Mesembryanthemum nodiflorum as influenced by CAM induction in the field. J Arid Environ 27:325–329

    Article  Google Scholar 

  • Schöb C, Armas C, Guler M, Prieto I, Pugnaire FI (2013) Variability in functional traits mediates plant interactions along stress gradients. J Ecol 101(3):753–762

    Article  Google Scholar 

  • Seebens H, Blackburn TM, Hulme PE, van Kleunen M, Liebhold AM, Orlova-Bienkowskaja M, Pyšek P, Schindler S, Essl F (2021) Around the world in 500 years: Inter‐regional spread of alien species over recent centuries. Glob Ecol Biogeogr 30:1621–1632

    Article  Google Scholar 

  • Simberloff D (2006) Invasional meltdown 6 years later: important phenomenon, unfortunate metaphor, or both? Ecol Lett 9(8):912–919

    Article  PubMed  Google Scholar 

  • Simberloff D, Von Holle B (1999) Positive interactions of nonindigenous species: invasional meltdown? Biol Invasions 1:21–32

    Article  Google Scholar 

  • Stone L, Roberts A (1990) The checkerboard score and species distributions. Oecologia 85:74–79

    Article  PubMed  Google Scholar 

  • Stotz GC, Cahill JF Jr, Bennett JA, Carlyle CN, Bork EW, Askarizadeh D et al (2020) Not a melting pot: plant species aggregate in their non-native range. Glob Ecol Biogeogr 29(3):482–490

    Article  Google Scholar 

  • Ulrich E, Perkins L (2014) Bromus inermis and Elymus canadensis but not Poa pratensis demonstrate strong competitive effects and all benefit from priority. Plant Ecol 215(11):1269–1275

    Article  Google Scholar 

  • Vivrette NJ, Muller CH (1977) Mechanism of invasion and dominance of coastal grassland by Mesembryanthemum crystallinum. Ecol Monogr 47:301–318

    Article  Google Scholar 

  • Von Caemmerer S, Griffiths H (2009) Stomatal responses to CO2 during a diel crassulacean acid metabolism cycle in Kalanchoe daigremontiana and Kalanchoe pinnata. Plant Cell Environ 32:567–576

    Article  Google Scholar 

  • Wang Q, Wang CH, Zhao B, Ma ZJ, Luo YQ, Chen JK, Li B (2006) Effects of growing conditions on the growth of and interactions between salt marsh plants: implications for invasibility of habitats. Biol Invasions 8:1547–1560

    Article  Google Scholar 

  • Welles SR, Funk JL (2021) Patterns of intraspecific trait variation along an aridity gradient suggest both drought escape and drought tolerance strategies in an invasive herb. Ann Botany 127(4):461–471

    Article  Google Scholar 

  • Winter K, Smith JAC (1996) Crassulacean Acid Metabolism: Biochemistry, Ecophysiology and Evolution. Springer 114:119–134

    Google Scholar 

  • Winter K, Ziegler H (1992) Induction of crassulacean acid metabolism in Mesembryanthemum crystallinum increases reproductive success under conditions of drought and salinity stress. Oecologia 92(4):475–479

    Article  PubMed  Google Scholar 

  • Yu K, D’Odorico P, Li W, He Y (2017) Effects of competition on induction of crassulacean acid metabolism in a facultative CAM plant. Oecologia 184:351–361

    Article  PubMed  Google Scholar 

  • Zhang R, Tielbörger K (2019) Facilitation from an intraspecific perspective–stress tolerance determines facilitative effect and response in plants. New Phytol 221:2203–2212

    Article  CAS  PubMed  Google Scholar 

  • Zhang Z, Liu Y, Brunel C, van Kleunen M (2020) Soil-microorganism-mediated invasional meltdown in plants. Nat Ecol Evol 4:1612–1621

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

This work was funded by FONDECYT grant 11181100 to CS-L.

Funding

This work was funded by FONDECYT (Fondo Nacional de Desarrollo Científico y Tecnológico) grant 11181100 to CS-L.

Competing Interests.

The authors declare no conflicts of interest or competing interests.

Author information

Authors and Affiliations

  1. Departamento de Biología, Universidad de La Serena, Casilla 554, La Serena, Chile

    Henry J. De La Cruz, Cristian Salgado-Luarte & Ernesto Gianoli

  2. Instituto de Investigación Multidisciplinario en Ciencia y Tecnología, Universidad de La Serena, Casilla 554, La Serena, Chile

    Cristian Salgado-Luarte

  3. Centro de Investigación para la Sustentabilidad, Facultad de Ciencias de la Vida, Universidad Andrés Bello, Santiago, Chile

    Gisela C. Stotz

Authors
  1. Henry J. De La Cruz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cristian Salgado-Luarte
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gisela C. Stotz
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ernesto Gianoli
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors contributed to the conception and design of the study. Material preparation, data collection and analysis were performed by HJ De La Cruz, C Salgado-Luarte and GC Stotz. The first draft of the manuscript was written by HJ De La Cruz and all authors contributed to the editing of subsequent drafts. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Henry J. De La Cruz.

Additional information

Publisher’s Note

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

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Material 1

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

De La Cruz, H.J., Salgado-Luarte, C., Stotz, G.C. et al. An exotic plant species indirectly facilitates a secondary exotic plant through increased soil salinity. Biol Invasions 25, 2599–2611 (2023). https://doi.org/10.1007/s10530-023-03061-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-023-03061-z

Keywords

Search

Navigation