Abstract
Alien invasive trees may expand and form monospecific forests by enhancing mutualism with arbuscular mycorrhizal fungi (AMF) and/or preventing the establishment of other plants through accumulation of antagonists for native plants. The success of invasive plants also has been associated with their higher phenotypic plasticity. Here we tested these mechanisms by studying the global invasive tree Ligustrum lucidum (hereafter Ligustrum) and the dominant native tree of the Chaquean montane forest (central Argentina) Lithraea molleoides (hereafter Lithraea). We experimentally addressed the effects of soil biota from Ligustrum monospecific forest stands and native montane forests on growth, biomass allocation, and nutrition of alien Ligustrum and native Lithraea. Soil biota was recovered from the rooting zone of adult trees of both species in each forest type. We found that arbuscule colonization in Ligustrum roots was significantly higher in seedlings grown with AMF communities from monospecific invaded forests in comparison to native soils. Mycorrhizal colonization in Lithraea roots did not differed between forest types. Soil biota from the rooting zone of the native Lithraea had no major effects on both itself and the invasive Ligustrum. Instead, AMF from Ligustrum rooting zone almost tripled and doubled P nutrition of the alien and the native compared with non-AMF treatments, respectively. Besides, antagonistic effects of soil biota were not observed. Lithraea root mass fraction (root mass/total plant mass, RMF) was not affected by forest type nor by soil treatment but Ligustrum RMF was affected by both factors. In particular, RMF decreased when seedlings grew with AMF from its rooting zone. The observed positive plant–soil feedback and the phenotypic plasticity of Ligustrum could explain, at least in part, the high invasiveness and the formation of monospecific forest stands by this global invader.
Similar content being viewed by others
References
Aldorfová A, Knobová P, Münzbergová Z (2020) Plant-soil feedback contributes to predicting plant invasiveness of 68 alien plant species differing in invasive status. Oikos. https://doi.org/10.1111/oik.07186
Aragón R, Groom M (2003) Invasion by Ligustrum lucidum (Oleaceae) in NW Argentina: early stage characteristics in different habitat types. Rev Biol Trop 51:59–70
Aragón R, Sardans J, Peñuelas J (2014) Soil enzymes associated with carbon and nitrogen cycling in invaded and native secondary forests of northwestern Argentina. Plant Soil 384:169–183. https://doi.org/10.1007/s11104-014-2192-8
Bellard C, Cassey P, Blackburn TM (2016) Alien species as a driver of recent extinctions. Biol Lett 12:20150623. https://doi.org/10.1098/rsbl.2015.0623
Bennett JA, Klironomos J (2019) Mechanisms of plant–soil feedback: interactions among biotic and abiotic drivers. New Phytol 222:91–96. https://doi.org/10.1111/nph.15603
Bennett JA, Maherali H, Reinhart KO, Lekberg Y, Hart MM, Klironomos J (2017) Plant-soil feedbacks and mycorrhizal type influence temperate forest population dynamics. Science 355:181–184. https://doi.org/10.1126/science.aai8212
Bever JD, Dickie IA, Facelli E, Facelli JM, Klironomos J, Moora M, Rillig MC, Stock WD, Tibbett M, Zobel M (2010) Rooting theories of plant community ecology in microbial interactions. Trends Ecol Evol 25:468–478. https://doi.org/10.1016/j.tree.2010.05.004
Blackburn TM, Pyšek P, Bacher S, Carlton J, Duncan RP, Jarošík V, Wilson JRU, Richardson DM (2011) A proposed unified framework for biological invasions. Trends Ecol Evol 26:333–339. https://doi.org/10.1016/j.tree.2011.03.023
Borda V, Cofré MN, Longo S, Grilli G, Urcelay C (2020) El “siempreverde” (Ligustrum lucidum), ¿Altera la composición de las comunidades de hongos micorrícicos arbusculares en el Chaco Serrano? Ecol Aust 30:282–294. https://doi.org/10.25260/EA.20.30.2.0.1017
Brixner-Dreyer JB, Higuchi P, Silva AC (2019) Ligustrum lucidum WT Aiton (broad-leaf privet) demonstrates climatic niche shifts during global-scale invasion. Sci Rep 9:1–6. https://doi.org/10.1038/s41598-019-40531-8
Brundrett M, Bougher N, Dell B, Grove T (1996) Working Ylith Mycorrhizas in Forestry and Agriculture. ACIAR Monograph 32, Australian Centre for International Agricultural Research, Canberra.
Bunn RA, Ramsey PW, Lekberg Y (2015) Do native and invasive plants differ in their interactions with arbuscular mycorrhizal fungi? A meta-analysis. J Ecol 103:1547–1556. https://doi.org/10.1111/1365-2745.12456
Castro-Díez P, Vaz AS, Silva JS, Van Loo M, Alonso Á, Aponte C, Bayón A, Bellingham PJ, Chiuffo MC, DiManno N, Kahua J, Kandert S, La Porta N, Marchante H, Maule HG, Mayfield MM, Metcalfe DM, Monteverdi C, Núñez MA, Ostertag R, Parker IM, Peltzer DA, Potgieter LJ, Raymundo M, Rayome D, Reisman-Berman O, Richardson DM, Roos RE, Saldaña A, Shackleton RT, Torres A, Trudgen M, Urban J, Vicente JR, Vilà M, Ylioja Y, Zenni RD, Godoy O (2019) Global effects of non-native tree species on multiple ecosystem services. Biol Rev 94:1477–1501. https://doi.org/10.1111/brv.12511
Davidson AM, Jennions M, Nicotra AB (2011) Do invasive species show higher phenotypic plasticity than native species and if so, is it adaptive? A meta-analysis. Ecol Lett 14:419–431. https://doi.org/10.1111/j.1461-0248.2011.01596.x
Del Fabbro C, Prati D (2015) Invasive plant species do not create more negative soil conditions for other plants than natives. Perspect Plant Ecol Evol Syst 17:87–95. https://doi.org/10.1016/j.ppees.2015.02.002
Di Rienzo JA, Casanoves F, Balzarini MG, Gonzalez L, Tablada M, Robledo CW (2013) InfoStat Versión 2013. Grupo InfoStat, FCA, Universidad Nacional de Córdoba, Córdoba
Dickie IA, Bufford JL, Cobb RC, Desprez-Loustau ML, Grelet G, Hulme PE, Klironomos J, Makiola A, Nuñez MA, Pringle A, Thrall PH, Tourtellot SG, Waller L, Williams NM (2017) The emerging science of linked plant–fungal invasions. New Phytol 215:1314–1332. https://doi.org/10.1111/nph.14657
Diez JM, Dickie I, Edwards G, Hulme PE, Sullivan JJ, Duncan RP (2010) Negative soil feedbacks accumulate over time for non-native plant species. Ecol Lett 13:803–809. https://doi.org/10.1111/j.1461-0248.2010.01474.x
Eppinga MB, Rietkerk M, Dekker SC, De Ruiter PC, Van der Putten WH, Van der Putten WH (2006) Accumulation of local pathogens: a new hypothesis to explain alien plant invasions. Oikos 114:168–176. https://doi.org/10.1111/j.2006.0030-1299.14625.x
Fernandez RD, Ceballos SJ, Aragón R, Malizia A, Montti L, Whitworth-Hulse JI, Castro-Díez P, Grau RH (2020) A global review of Ligustrum lucidum (OLEACEAE) invasion. Bot Rev. https://doi.org/10.1007/s12229-020-09228-w
Ferreras AE, Giorgis MA, Tecco PA, Cabido MR, Funes G (2015) Impact of Ligustrum lucidum on the soil seed bank in invaded subtropical seasonally dry woodlands (Córdoba, Argentina). Biol Invasions 17:3547–3561. https://doi.org/10.1007/s10530-015-0977-1
Foxcroft LC, Pickett ST, Cadenasso ML (2011) Expanding the conceptual frameworks of plant invasion ecology. Perspect Plant Ecol Evol Syst 13:89–100. https://doi.org/10.1016/j.ppees.2011.03.004
Fracchia S, Aranda A, Gopar A, Silvani V, Fernandez L, Godeas A (2009) Mycorrhizal status of plant species in the Chaco Serrano Woodland from central Argentina. Mycorrhiza 19:205–214. https://doi.org/10.1007/s00572-009-0231-8
Funk JL (2008) Differences in plasticity between invasive and native plants from a low resource environment. J Ecol 96:1162–1173. https://doi.org/10.1111/j.1365-2745.2008.01435.x
Gavier-Pizarro GI, Bucher EH (2004) Deforestación de las Sierras Chicas de Córdoba (Argentina) en el período 1970–1997. Academia Nacional de Ciencias, Córdoba
Gavier-Pizarro GI, Kuemmerle T, Hoyos LE, Stewart SI, Huebner CD, Keuler NS, Radeloff VC (2012) Monitoring the invasion of an alien tree (Ligustrum lucidum) from 1983 to 2006 with Landsat TM/ETM+ satellite data and Support Vector Machines in Córdoba, Argentina. Remote Sens Environ 122:134–145. https://doi.org/10.1016/j.rse.2011.09.023
Giorgis MA, Cingolani AM, Gurvich DE, Tecco PA, Chiapella J, Chiarini F, Cabido M (2017) Changes in floristic composition and physiognomy are decoupled along elevation gradients in central Argentina. Appl Veg Sci 20:558–571. https://doi.org/10.1111/avsc.12324
Grove S, Haubensak KA, Gehring C, Parker IM (2017) Mycorrhizae, invasions, and the temporal dynamics of mutualism disruption. J Ecol 105:1496–1508. https://doi.org/10.1111/1365-2745.12853
Hoyos LE, Gavier-Pizarro GI, Kuemmerle T, Bucher EH, Radeloff VC, Tecco PA (2010) Invasion of glossy privet (Ligustrum lucidum) and native forest loss in the Sierras Chicas of Córdoba, Argentina. Biol Invasions 12:3261–3275. https://doi.org/10.1007/s10530-010-9720-0
Jones JB, Wolf B, Mills HA (1991) Plant analysis handbook. A practical sampling, preparation, analysis, and interpretation guide. Micro-Macro Publishing Inc., Athens
Kardol P, Wardle DA (2010) How understanding aboveground–belowground linkages can assist restoration ecology. Trends Ecol Evol 25:670–679. https://doi.org/10.1016/j.tree.2010.09.001
Lendenmann M, Thonar C, Barnard RL, Salmon Y, Werner RA, Frossard E, Jansa J (2011) Symbiont identity matters: carbon and phosphorus fluxes between Medicago truncatula and different arbuscular mycorrhizal fungi. Mycorrhiza 21:689–702. https://doi.org/10.1007/s00572-011-0371-5
Lichstein JW, Grau HR, Aragón R (2004) Recruitment limitation in secondary forests dominated by an exotic tree. J Veg Sci 15:721–728. https://doi.org/10.1111/j.1654-1103.2004.tb02314.x
Longo S, Nouhra E, Tecco PA, Urcelay C (2020) Functional stability of mycorrhizal interactions in woody natives and aliens facing fire disturbance. Plant Ecol. https://doi.org/10.1007/s11258-020-01014-3
Luti R (1979) Vegetation. In: Vázquez JB, Miatello RA, Roque ME (eds) Geografía Física de la provincia de Córdoba. Boldt, Buenos Aires, pp 297–368
Mangla S, Callaway RM (2008) Alien invasive plant accumulates native soil pathogens which inhibit native plants. J Ecol 96:58–67. https://doi.org/10.1111/j.1365-2745.2007.01312.x
McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA (1990) A new method which gives an objective measure of colonization of roots by vesicular–arbuscular mycorrhizal fungi. New Phytol 115:495–501. https://doi.org/10.1111/j.1469-8137.1990.tb00476.x
Meisner A, Hol WG, de Boer W, Krumins JA, Wardle DA, van der Putten WH (2014) Plant–soil feedbacks of alien plant species across life forms: a meta-analysis. Biol Invasions 16:2551–2561. https://doi.org/10.1007/s10530-014-0685-2
Morello J, Matteuci S, Rodriguez A, Silva M (2012) Ecorregiones y complejos ecosistémicos argentinos. Orientación Gráfica Editora, Buenos Aires
Nijjer S, Rogers WE, Siemann E (2007) Negative plant–soil feedbacks may limit persistence of an invasive tree due to rapid accumulation of soil pathogens. Proc R Soc B Biol Sci 274:2621–2627. https://doi.org/10.1098/rspb.2007.0804
Osunkoya OO, Perrett C (2011) Lantana camara L. (Verbenaceae) invasion effects on soil physicochemical properties. Biol Fertil Soils 47:349–355. https://doi.org/10.1007/s00374-010-0513-5
Oyarzabal M, Clavijo J, Oakley L, Biganzoli F, Tognetti P, Barberis I, Maturo HM, Aragón R, Campanello PI, Prado D, Oesterheld M, León RJC (2018) Unidades de vegetación de la Argentina. Ecol Aust 28:40–63. https://doi.org/10.25260/EA.18.28.1.0.399
Palacio-López K, Gianoli E (2011) Invasive plants do not display greater phenotypic plasticity than their native or non-invasive counterparts: a meta-analysis. Oikos 120:1393–1401. https://doi.org/10.1111/j.1600-0706.2010.19114.x
Qiu YJ, Zhang NL, Zhang LL, Zhang XL, Wu AP, Huang JY, Yu SQ, Wang YH (2020) Mediation of arbuscular mycorrhizal fungi on growth and biochemical parameters of Ligustrum vicaryi in response to salinity. Physiol Mol Plant Pathol 112:101522. https://doi.org/10.1016/j.pmpp.2020.101522
R Development Core Team (2009) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Austria
Reinhart KO, Callaway RM (2006) Soil biota and invasive plants. New Phytol 170:445–457. https://doi.org/10.1111/j.1469-8137.2006.01715.x
Rejmánek M, Richardson DM (2013) Trees and shrubs as invasive alien species—2013 update of the global database. Divers Distrib 19:1093–1094. https://doi.org/10.1111/ddi.12075
Richards CL, Bossdorf O, Muth NZ, Gurevitch J, Pigliucci M (2006) Jack of all trades, master of some? On the role of phenotypic plasticity in plant invasions. Ecol Lett 9:981–993. https://doi.org/10.1111/j.1461-0248.2006.00950.x
Richardson DM, Allsopp N, D’antonio CM, Milton SJ, Rejmánek M (2000) Plant invasions—the role of mutualisms. Biol Rev 75:65–93. https://doi.org/10.1111/j.1469-185X.1999.tb00041.x
Richardson DM, Hui C, Nuñez MA, Pauchard A (2014) Tree invasions: patterns, processes, challenges and opportunities. Biol Invasions 16:473–481. https://doi.org/10.1007/s10530-013-0606-9
Río ME, Achával L (1904) Geografía de la Provincia de Córdoba. Gobierno de Córdoba, Compañía Sudamericana de Billetes, Buenos Aires
Rubio G, Lavado RS, Pereyra FX (2019) The soils of Argentina. Springer, Cham
Sala OE, Chapin FS, Armesto JJ, Berlow E, Bloomfield J, Dirzo R, Huber-Sanwald E, Huenneke LF, Jackson RB, Kinzig A, Leemans R, Lodge DM, Mooney HA, Oesterheld M, LeRoy-Poff N, Sykes MT, Walker BH, Walker M, Wall DH, (2000) Global biodiversity scenarios for the year 2100. Science 287:1770–1774. https://doi.org/10.1126/science.287.5459.1770
Simberloff D, Martin JL, Genovesi P, Maris V, Wardle DA, Aronson J, Curchamp F, Galil B, García-Bertou E, Pascal M, Pysek P, Sousa R, Tabacchi E, Vilà M (2013) Impacts of biological invasions: what’s what and the way forward. Trends Ecol Evol 28:58–66. https://doi.org/10.1016/j.tree.2012.07.013
Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, New York
Smith SE, Smith FA, Jakobsen I (2003) Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiol 133:16–20. https://doi.org/10.1104/pp.103.024380
Stinson KA, Campbell SA, Powell JR, Wolfe BE, Callaway RM, Thelen GC, Hallett SG, Prati D, Klironomos JN (2006) Invasive plant suppresses the growth of native tree seedlings by disrupting belowground mutualisms. PLoS Biol. https://doi.org/10.1371/journal.pbio.0040140
Suding KN, Stanley Harpole W, Fukami T, Kulmatiski A, MacDougall AS, Stein C, van der Putten WH (2013) Consequences of plant–soil feedbacks in invasion. J Ecol 101:298–308. https://doi.org/10.1111/1365-2745.12057
Te Beest M, Stevens N, Olff H, Van Der Putten WH (2009) Plant–soil feedback induces shifts in biomass allocation in the invasive plant Chromolaena odorata. J Ecol 97:1281–1290. https://doi.org/10.1111/j.1365-2745.2009.01574.x
Tecco PA, Gurvich DE, Diaz S, Pérez-Harguindeguy N, Cabido M (2006) Positive interaction between invasive plants: the influence of Pyracantha angustifolia on the recruitment of native and alienwoody species. Austral Ecol 31:293–300. https://doi.org/10.1111/j.1442-9993.2006.01557.x
Tecco PA, Diaz S, Gurvich DE, Perez-Harguindeguy N, Cabido M, Bertone GA (2007) Facilitation and interference underlying the association between the woody invaders Pyracantha angustifolia and Ligustrum lucidum. Appl Veg Sci 10:211–218. https://doi.org/10.1111/j.1654-109X.2007.tb00519.x
Tecco PA, Urcelay C, Diaz S, Cabido M, Pérez-Harguindeguy N (2013) Contrasting functional trait syndromes underlay woody alien success in the same ecosystem. Austral Ecol 38:443–451. https://doi.org/10.1111/j.1442-9993.2012.02428.x
Tecco PA, Pais-Bosch AI, Funes G, Marcora PI, Zeballos SR, Cabido M, Urcelay C (2016) Mountain invasions on the way: are there climatic constraints for the expansion of alien woody species along an elevation gradient in Argentina? J Plant Ecol 9(4):380–392. https://doi.org/10.1093/jpe/rtv064
Teste FP, Kardol P, Turner BL, Wardle DA, Zemunik G, Renton M, Laliberté E (2017) Plant-soil feedback and the maintenance of diversity in Mediterranean-climate shrublands. Science 355:173–176. https://doi.org/10.1126/science.aai8291
Urcelay C, Longo S, Geml J, Tecco PA (2019a) Can arbuscular mycorrhizal fungi from non-invaded montane ecosystems facilitate the growth of alien trees? Mycorrhiza. https://doi.org/10.1007/s00572-018-0874-4
Urcelay C, Tecco P, Borda V, Longo S (2019b) Latitudinal distribution of mycorrhizal types in native and alien trees in Montane ecosystems from Southern South America. In: Pagano M, Lugo M (eds) Mycorrhizal fungi in South America. Springer, Cham, pp 29–48
Van Grunsven RH, Van Der Putten WH, Bzemer TM, Tamis WL, Berendse F, Veenendaal EM (2007) Reduced plant-soil feedback of plant species expanding their range as compared to natives. J Ecol. https://doi.org/10.1111/j.1365-2745.2007.01282.x
van Kleunen M, Bossdorf O, Dawson W (2018) The ecology and evolution of alien plants. Annu Rev Ecol Evol Syst 49:25–47. https://doi.org/10.1146/annurev-ecolsys-110617-062654
Verbeek JD, Kotanen PM (2019) Soil-mediated impacts of an invasive thistle inhibit the recruitment of certain native plants. Oecologia. https://doi.org/10.1007/s00442-019-04435-8
Veresoglou SD, Menexes G, Rillig MC (2012) Do arbuscular mycorrhizal fungi affect the allometric partition of host plant biomass to shoots and roots? A meta-analysis of studies from 1990 to 2010. Mycorrhiza 22:227–235. https://doi.org/10.1007/s00572-011-0398-7
Vilà M, Bacher S, Hulme P, Kenis M, Kobelt M, Nentwig W, Sol D, Solarz W (2006) Impactos ecológicos de las invasiones de plantas y vertebrados terrestres en Europa. Ecosistemas 2:1–12
Waller LP, Allen WJ, Barratt BIP, Condron LM, França FM, Hunt JE, Koele N, Orwin KH, Steel GS, Tylianakis JM, Wakelin SA, Dickie IA (2020) Biotic interactions drive ecosystem responses to alien plant invaders. Science 368:967–972. https://doi.org/10.1126/science.aba2225
Whitworth-Hulse JI, Magliano PN, Zeballos SR, Gurvich DE, Spalazzi F, Kowaljow E (2020) Advantages of rainfall partitioning by the global invader Ligustrum lucidum over the dominant native Lithraea molleoides in a dry forest. Agric For Meteorol. https://doi.org/10.1016/j.agrformet.2020.108013
Yang Q, Carrillo J, Jin H, Shang L, Hovick SM, Nijjer S, Siemann E (2013) Plant–soil biota interactions of an invasive species in its native and introduced ranges: Implications for invasion success. Soil Biol Biochem 65:78–85. https://doi.org/10.1016/j.soilbio.2013.05.004
Zeballos SR, Giorgis MA, Cingolani AM, Cabido M, Whitworth-Hulse JI, Gurvich DE (2014) Do alien and native tree species from Central Argentina differ in their water transport strategy. Austral Ecol 39:984–991. https://doi.org/10.1111/aec.12171
Zhang P, Li B, Wu J, Hu S (2019) Invasive plants differentially affect soil biota through litter and rhizosphere pathways: a meta-analysis. Ecol Lett 22:200–210. https://doi.org/10.1111/ele.13181
Acknowledgements
The authors wish to acknowledge the assistance of the Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) and the Universidad Nacional de Córdoba (U.N.C), both of which have provided facilities used for this study. This research program is funded by Secretaría de Ciencia y Tecnología: Universidad Nacional de Córdoba (Secyt) (Universidad Nacional de Córdoba) and Ministerio de Ciencia de la Provincia de Córdoba. The authors also thank Ana Elisa Ferreras and Juan Ignacio Whitworth-Hulse for providing the seeds utilized in this study. We also thank the Organic Chemistry department of the Instituto Multidisciplinario de Biología Vegetal, especially Damian Maestri, for making possible the foliar phosphorus analysis as well as the technical staff who collaborated in those analyses: Norma Gallardo, Marcela Alejandra Palacio, Luis Damián Barrionuevo, and Pablo Ramiro Cortina. Finally, we thank the contribution of two anonymous reviewers.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflicts of interest.
Additional information
Communicated by Martin Nunez.
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.
Rights and permissions
About this article
Cite this article
Borda, V., Longo, S., Marro, N. et al. The global invader Ligustrum lucidum accumulates beneficial arbuscular mycorrhizal fungi in a novel range. Plant Ecol 222, 397–408 (2021). https://doi.org/10.1007/s11258-021-01114-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11258-021-01114-8