Abstract
Ailanthus altissima is one of the worst invasive plants in Europe in several habitat types, including high-biodiversity grasslands. The aim of this work was to evaluate the impact of the invasive A. altissima on high-biodiversity grassland vegetation and the effects of its removal on the recovery of native plant communities. The study area was within the Alta Murgia National Park (SE Italy). Seventeen vegetation quadrats were sampled in invaded grasslands and nine quadrats were sampled in nearby uninvaded areas. A. altissima was removed from six quadrats, which were sampled for two years after plant removal. Cluster analysis and non-metric multidimensional scaling ordination were used to identify and visualize the general vegetation pattern. Generalised Linear Models with different error structures were used to analyse the effects of A. altissima on native grasslands and vegetation recovery after removal. Results showed that the invasion of A. altissima changed drastically the community composition, reduced plant richness and diversity. Invaded stands had a greater presence of ruderal and widely distributed taxa, as opposed to a lesser presence of endemic and Mediterranean ones. The differences in the community composition between invaded and uninvaded quadrats became clearly detectable when A. altissima plants exceeded a threshold of 1 m of height and 50% of coverage. After A. altissima removal, the recovery of the grassland community was not completely achieved after two years.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Availability of data and material
All data generated during this study are included in this published article as Supplementary Material.
Code availability
All scripts and datasets for the analyses are available on GitHub at https://github.com/diegofontaneto/ailanthus.
Change history
23 September 2021
A Correction to this paper has been published: https://doi.org/10.1007/s00267-021-01539-x
References
Badalamenti E, Barone E, La Mantia T (2015) Seasonal effects on mortality rates and resprouting of stems treated with glyphosate in the invasive tree of heaven (Ailanthus altissima (Mill.) Swingle). Arboric J 37:180–195. https://doi.org/10.1080/03071375.2015.1112163
Beckerman AP (2014) What can modern statistical tools do for limnology? J Limnol 73(s1):161–170. https://doi.org/10.4081/jlimnol.2014.808
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
Bianco P (1962) Flora e vegetazione delle murge di nord ovest. Ann Fac Agrar Univ Bari 16:459–640
Botta-Dukat Z (2008) Invasion of alien species to Hungarian (semi-)natural habitats. Acta Bot Hung 50(Suppl):219–227. https://doi.org/10.1556/abot.50.2008.suppl.11
Casella F, Boari A, Zonno MC, Palomba G, Vurro M (2015) Control of Ailanthus altissima in a natural environment. 17th European Weed Research Society Symposium—weed management in changing environments. Montpellier, France, 23–26 June, 2015, p. 218
Casella F, Vurro M, Boari A (2016) Restoration of areas invaded by Ailanthus altissima in the Alta Murgia National Park: experience within a LIFE project. 7th International Weed Science Congress. Prague, Czech Republic, 19–25 June 2016, p. 215
Castro-Díez P, Fierro-Brunnenmeister N, González-Muñoz N, Gallardo A (2012) Effects of exotic and native tree leaf litter on soil properties of two contrasting sites in the Iberian Peninsula. Plant Soil 350:179–191. https://doi.org/10.1007/s11104-011-0893-9
Chytrý M, Otýpková Z (2003) Plot sizes used for phytosociological sampling of European vegetation. J Veg Sci 14:563–570. https://doi.org/10.1111/j.1654-1103.2003.tb02183.x
Constán-Nava S, Bonet A, Pastor E, Lledo MJ (2010) Long-term control of the invasive tree Ailanthus altissima: insights from Mediterranean protected forests. For Ecol Manag 260:1058–1064. https://doi.org/10.1016/j.foreco.2010.06.030
Constán-Nava S, Soliveres S, Torices R, Serra L, Bonet A (2015) Direct and indirect effects of invasion by the alien tree Ailanthus altissima on riparian plant communities and ecosystem multifunctionality. Biol Invas 17:1095–1108. https://doi.org/10.1007/s10530-014-0780-4
Crawley MJ (2012) The R book, 2nd edition. Wiley, Chichester, UK
DiTomaso JM, Kyser GB (2007) Control of Ailanthus altissima using stem herbicide application techniques. Arboric Urban 33:55–63
Dufrêne M, Legendre P (1997) Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol Monogr 67:345–366. https://doi.org/10.1890/0012-9615(1997)067[0345:SAAIST]2.0.CO;2
Eldridge DJ, Bowker MA, Maestre FT, Roger E, Reynolds JF, Whitford WG (2011) Impacts of shrub encroachment on ecosystem structure and functioning: towards a global synthesis. Ecol Lett 14:709–722. https://doi.org/10.1111/j.1461-0248.2011.01630.x
Erdős L, Márkus A, Körmöczi L (2005) Consequences of an extirpation trial of the tree of heaven (Ailanthus altissima (Mill.) Swingle) on rock grasslands and slope steppes. Tiscia 35:3–7
Euro+Med (2006–2020) Euro+Med PlantBase—the information resource for Euro-Mediterranean plant diversity. Published on the Internet http://ww2.bgbm.org/EuroPlusMed/ Accessed 1 Jun 2020
European Commission (2013) Interpretation manual of European Union habitats. EUR 28:1–144
Forte L, Perrino EV, Terzi M (2005) Le praterie a Stipa austroitalica Martinovsky ssp. austroitalica dell’Alta Murgia (Puglia) e della Murgia Materana (Basilicata). Fitosociologia 42:83–103
Fotiadis G, Kyriazopoulos AP, Fraggakis I (2011) The behaviour of Ailanthus altissima weed and its effects on natural ecosystems. J Environ Biol 32:801–806
Fox J, Weisberg S (2019) An R companion to applied regression, Third Edition. Sage, Thousand Oaks CA, https://socialsciences.mcmaster.ca/jfox/Books/Companion/
Foxcroft LC, Pyšek P, Richardson DM, Genovesi P, MacFadyen S (2017) Plant invasion science in protected areas: progress and priorities. Biol Invas 19:1353–1378. https://doi.org/10.1007/s10530-016-1367-z
Fried G, Panetta FD (2016) Comparing an exotic shrub’s impact with that of a native life form analogue: Baccharis halimifolia vs Tamarix gallica in Mediterranean salt marsh communities. J Veg Sci 27:812–823. https://doi.org/10.1111/jvs.12407
Feurdean A, Ruprecht E, Molnár Z, Hutchinson SM, Hickler T (2018) Biodiversity-rich European grasslands: ancient, forgotten ecosystems. Biol Cons 228:224–232. https://doi.org/10.1016/j.biocon.2018.09.022
Gaertner M, Den Breeyen A, Hui C, Richardson DM (2009) Impacts of alien plant invasions on species richness in Mediterranean-type ecosystems: a meta-analysis. Prog Phys Geogr 33:319–338. https://doi.org/10.1177/0309133309341607
Gooden B, French K, Turner PJ, Downey PO (2009) Impact threshold for an alien plant invader, Lantana camara L., on native plant communities. Biol Cons 142:2631–2641. https://doi.org/10.1016/j.biocon.2009
Heisey RM (1990) Allelopathic and herbicidal effects of extracts from tree-of-heaven (Ailanthus altissima). Am J Bot 77:662–670
Hejda M, Pyšek P, Jarošík V (2009) Impact of invasive plants on the species richness, diversity and composition of invaded communities. J Ecol 97:393–403. https://doi.org/10.1111/j.1365-2745.2009.01480.x
Jackson RB, Banner JL, Jobbágy EG, Pockman WT, Wall DH (2002) Ecosystem carbon loss with woody plant invasion of grasslands. Nature 418:623–626. https://doi.org/10.1038/nature00910
Kowarik I, Saümel I (2007) Biological flora of Central Europe: Ailanthus altissima (Mill.) Swingle. Perspect Plant Ecol Evol Syst 8:207–237. https://doi.org/10.1016/j.ppees.2007.03.002
Lamarque LJ, Delzon S, Lortie CJ (2011) Tree invasions: a comparative test of the dominant hypotheses and functional traits. Biol Invas 13:1969–1989. https://doi.org/10.1007/s10530-011-0015-x
Lawrence JG, Colwell A, Sexton OJ (1991) The ecological impact of allelopathy in Ailanthus altissima (Simaroubaceae). Am J Bot 78:948–958
Lenth R (2020) emmeans: estimated marginal means, aka least-squares means. R package version 1.4.7. https://CRAN.R-project.org/package=emmeans
Lepš J, Hadincová V (1992) How reliable are our vegetation analyses? J Veg Sci 3:119–124. https://doi.org/10.2307/3236006
Lüdecke D, Makowski D, Waggoner P, Patil I (2020) Performance: assessment of regression models performance. R package version 0.4.6. https://CRAN.R-project.org/package=performance
Mack RN, Simberloff D, Mark Lonsdale W, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710. https://doi.org/10.1890/1051-0761(2000)010[0689:BICEGC]2.0.CO;2
McCune B, Mefford MJ (2011) PC-ORD. Multivariate analysis of ecological data. Version 6.22. MjM Software, Gleneden Beach, Oregon, US
Medina-Villar S, Rodríguez-Echeverría S, Lorenzo P, Alonso A, Pérez-Corona E, Castro-Díez P (2016) Impacts of the alien trees Ailanthus altissima (Mill.) Swingle and Robinia pseudoacacia L. on soil nutrients and microbial communities. Soil Biol Biochem 96:65–73. https://doi.org/10.1016/j.soilbio.2016.01.015
Meloche C, Murphy SD (2006) Managing tree-of-heaven (Ailanthus altissima) in parks and protected areas: a case study of Rondeau Provincial Park (Ontario, Canada). Environ Manag 37:764–772. https://doi.org/10.1007/s00267-003-0151-x
Ministry for Environment, Land and Sea Protection of Italy (2019). Decreto 28 dicembre 2018. Gazzetta ufficiale della Repubblica Italiana n.19. Accessed 29 Jun 2021.
Montecchiari S, Tesei G, Allegrezza M (2020) Ailanthus altissima forests determine a shift in herbaceous layer richness: a paired comparison with hardwood native forests in sub-Mediterranean Europe. Plants 9:1404. https://doi.org/10.3390/plants9101404
Motard E, Dusz S, Geslin B, Akpa-Vinceslas M, Hignard C, Babiar O, Clair-Maczulajtys D, Michel-Salzat A (2015) How invasion by Ailanthus altissima transforms soil and litter communities in a temperate forest ecosystem. Biol Invas 17:1817–1832. https://doi.org/10.1007/s10530-014-0838-3
Motard E, Muratet A, Clair-Maczulajtys D, Machon N (2011) Does the invasive species Ailanthus altissima threaten floristic diversity of temperate peri-urban forests? Compt Rend Biol 334:872–879. https://doi.org/10.1016/j.crvi.2011.06.003
Mucina L, Bültmann H, Dierßen K, Theurillat J-P, Raus T et al. (2016) Vegetation of Europe: hierarchical floristic classification system of vascular plant, bryophyte, lichen, and algal communities. Appl Veg Sci 19:3–264. https://doi.org/10.1111/avsc.12257
Noss RF (1983) A regional landscape approach to maintain diversity. BioScience 33:700–706. https://doi.org/10.2307/1309350
Panetta FD, Gooden B (2017) Managing for biodiversity: impact and action thresholds for invasive plants in natural ecosystems. NeoBiota 34:53–66. https://doi.org/10.3897/neobiota.34.11821
Peterson BG, Carl P (2020) Performance analytics: econometric tools for performance and risk analysis. R package version 2.0.4. https://CRAN.R-project.org/package=PerformanceAnalytics
Pignatti S, Menegoni P, Pietrosanti S (2005) Biondicazione attraverso le piante vascolari. Valori di indicazione secondo Ellenberg (Zeigerwerte) per le specie della Flora d’Italia. Braun-Blanquetia 39:1–97
Pyšek P, Chytrý M, Pergl J, Sádlo J, Wild J (2012) Plant invasions in the Czech Republic: current state, introduction dynamics, invasive species and invaded habitats. Preslia 84:575–629
Pyšek P, Genovesi P, Pergl J, Monaco A, Wild J (2013) Invasion of protected areas in Europe: an old continent facing new problems. In: Foxcroft LC, Pyšek P, Richardson DM, Genovesi P (eds) Plant invasions in protected areas: patterns, problems and challenges. Springer, Dordrecht, p 209–240
R Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, URL
Richardson D (1998) Forestry trees as invasive aliens. Conserv Biol 12:18–26
Rundel PW, Dickie IA, Richardson DM (2014) Tree invasions into treeless areas: mechanisms and ecosystem processes. Biol Invas 16:663–675. https://doi.org/10.1007/s10530-013-0614-9
Scavo A, Restuccia A, Mauromicale G (2018) Allelopathy: principles and basic aspects for agroecosystem control. In: Gaba S, Smith B, Lichtfouse E (eds.) Sustainable agriculture reviews 28. Sustainable agriculture reviews. Springer, Cham, p 47–101. vol 28
Seebens H, Blackburn TM, Dyer EE, Genovesi P, Hulme PE et al. (2017) No saturation in the accumulation of alien species worldwide. Nat Commun 8:1–9. https://doi.org/10.1038/ncomms14435
Shackleton RT, Foxcroft LC, Pyšek P, Wood LE, Richardson DM (2020) Assessing biological invasions in protected areas after 30 years: revisiting nature reserves targeted by the 1980s SCOPE programme. Biol Conserv 243 https://doi.org/10.1016/j.biocon.2020.108424
Sirbu C, Vîntu V, Samuil C, Stavarache M (2016) Invasive neophytes in natural grasslands of Romania. Rom J Grassl Forage Crops 13:57–72
Sokal RR, Michener CD (1958) A statistical method for evaluating systematic relationships. Univ Kans Sci Bull 38:1409–1438
Strayer DL, Eviner VT, Jeschke JM, Pace ML (2006) Understanding the longterm effects of species invasions. Trends Ecol Evol 21:645–651. https://doi.org/10.1016/j.tree.2006.07.007
Tarantino C, Casella F, Adamo M, Lucas R, Beierkuhnlein C, Blonda P (2019) Ailanthus altissima mapping from multi-temporal very high resolution satellite images. ISPRS J Photogramm Remote Sens 147:90–103. https://doi.org/10.1016/j.isprsjprs.2018.11.013
Terzi M (2007) Conservation of genetic resources in Mediterranean protected areas: the Park of Alta Murgia (South Italy). In: Bullitta S (ed) Plant genetic resources of geographical and “other” Islands (conservation, evaluation and use for plant breeding). CNR-ISPAAM sez. Sassari. Publisher, Sassari (Italy), p 311–319
Terzi M (2015) Numerical analysis of the order Scorzoneretalia villosae. Phytocoenologia 45:11–32. https://doi.org/10.1127/phyto/2015/0009
Terzi M, Di Pietro R, D’Amico FS (2010) Indicator species analysis applied to communities with Stipa austroitalica Martinovsky and relevant syntaxonomic problems. Plant Sociol 47:3–28
Uboni C, Tordoni E, Brandmayr P, Battistella S, Bragato G, Castello M, Colombetta G, Poldini L, Bacaro G (2019) Exploring cross-taxon congruence between carabid beetles (Coleoptera: Carabidae) and vascular plants in sites invaded by Ailanthus altissima versus non-invaded sites: the explicative power of biotic and abiotic factors. Ecol Indic 103:145–155. https://doi.org/10.1016/j.ecolind.2019.03.052
Uzunov Y, Georgiev BB, Varadinoiva E, Ivanova N, Pehlivanov L, Vasilev V (eds) (2012) Ecosystems of the biosphere reserve Srebarna lake. Professor Marin Drinov Academic Publishing House, Sofia, p 218
van der Maarel E (1979) Transformation of cover-abundance values in phytosociology and its effects on community similarity. Vegetatio 39:97–114. https://doi.org/10.1007/BF00052021
Vilà M, Espinar JL, Hejda M, Hulme PE, Jarošik V, Maron JL, Pergl J, Schaffner U, Sun Y, Pyšek P (2011) Ecological impacts of invasive alien plants: a meta-analysis of their effects on species, communities and ecosystems. Ecol Lett 14:702–708. https://doi.org/10.1111/j.1461-0248.2011.01628.x
Vilà M, Tessier M, Suehs CM, Brundu G, Carta L, Galanidis A, Lambdon P, Manca M, Médail F, Moragues E, Traveset A, Troumbis AY, Hulme PH (2006) Local and regional assessments of the impacts of plant invaders on vegetation structure and soil properties of Mediterranean islands. J Biogeogr 33:853–861. https://doi.org/10.1111/j.1365-2699.2005.01430.x
Wang Y, Naumann U, Eddelbuettel D, Wilshire J, Warton D (2020) mvabund: statistical methods for analysing multivariate abundance data. R package version 4.1.3. https://CRAN.R-project.org/package=mvabund
Wang YI, Naumann U, Wright ST, Warton DI (2012) mvabund–an R package for model-based analysis of multivariate abundance data. Methods Ecol Evol 3:471–474
Westhoff V, van der Maarel E (1980) The Braun-Blanquet approach. In: Whittaker RH (ed) Classification of plant communities, 2nd ed. Junk, The Hague (NL), p 287–399
Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer-Verlag, New York, NY
Wilson JB, Peet RK, Dengler J, Pärtel M (2012) Plant species richness: the world records. J Veg Sci 23:796–802. https://doi.org/10.1111/j.1654-1103.2012.01400.x
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
Acknowledgements
This work was supported by the LIFE Programme, a financial instrument for the environment of the European Commission. We thank Maurizio Vurro for his suggestions on the first draft of this paper, Rocco Labadessa for his help during some field surveys, and two anonymous referees for their helpful comments.
Authors’ contributions
MT and FC conceived the study and collected data; FC coordinated the Ailanthus removal interventions; DF and MT performed the analysis; MT led the writing and all authors checked, improved and approved the manuscript.
Funding
This study was partially funded by the European Commission under the Life Biodiversity Programme (Life Alta Murgia project - LIFE12 BIO/IT/000213).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
Rights and permissions
About this article
Cite this article
Terzi, M., Fontaneto, D. & Casella, F. Effects of Ailanthus altissima Invasion and Removal on High-Biodiversity Mediterranean Grasslands. Environmental Management 68, 914–927 (2021). https://doi.org/10.1007/s00267-021-01522-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00267-021-01522-6