Abstract
Prunus serotina is one of the worst invasive alien plants throughout Europe, able to rapidly replace autochthonous vegetation and form monospecific stands both in open lands and forested areas. Invasion by shrubs and trees due to abandonment of traditional management practices, is one of the major threats to the conservation of “European dry heaths”, a priority habitat included in the Council Directive 92/43/EEC. The aim of this study was to assess the effects of P. serotina invasion on heathland vegetation in terms of species composition and cover, with special regards to the dominant Calluna vulgaris and Molinia arundinacea, in an area of North-Western Italy subjected to massive invasion by this alien species. We collected data on the plant cover along an invasion gradient in 10 linear transects running from P. serotina invaded stands towards non invaded ones. P. serotina differently affected the heathland vegetation. In particular, the cover of C. vulgaris and other typical heathland species such as Cytisus scoparius sharply decreased at P. serotina cover increasing. On the contrary, positive or no effect of P. serotina cover was found on M. arundinacea. Our results showed that shaded conditions created by the alien tree disfavored light demanding C. vulgaris and C. scoparius, enabling fast grower M. arundinacea to outcompete and replace them. This study emphasizes the urgency to develop management strategies to effectively control P. serotina spread in the area and to restore typical heathland species.
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References
AA VV (2013) Relazione tecnica finalizzata alla proposta di riconoscimento del SIC/ZPS “Brughiere di Malpensa e di Lonate” – aggiornamento Novembre 2013. Parco Lombardo della Valle del Ticino, Magenta
Aerts R, Berendse F, de Caluwe H, Schmitz M (1990) Competition in heathland along an experimental gradient of nutrient availability. Oikos 57(3):310–318
Aerts R, Ewald M, Nicolas M, Piat J, Skowronek S, Lenoir J, Hattab T, Garzón-López CX, Feilhauer H, Schmidtlein S, Rocchini D, Decocq G, Somers B, Van De Kerchove R, Denef K, Honnay O (2017) Invasion by the alien tree Prunus serotina alters ecosystem functions in a temperate deciduous forest. Front Plant Sci 8:179. https://doi.org/10.3389/fpls.2017.00179
Ascoli D, Bovio G (2010) Tree encroachment dynamics in heathlands of North-West Italy: the fire regime hypothesis. iForest 3:137–143. https://doi.org/10.3832/ifor0548-003
Banfi E, Galasso G (2010) La flora esotica lombarda. Museo di Storia Naturale di Milano, Milan
Bartolucci F, Peruzzi L, Galasso G, Albano A, Alessandrini A, Ardenghi NMG, Astuti G, Bacchetta G, Ballelli S, Banfi E, Barberis G, Bernardo L, Bouvet D, Bovio M, Cecchi L, Di Pietro R, Domina G, Fascetti S, Fenu G, Festi F, Foggi B, Gallo L, Gottschlich G, Gubellini L, Iamonico D, Iberite M, Jiménez-Mejias P, Lattanzi E, Marchetti D, Martinetto E, Masin RR, Medagli P, Passalacqua NG, Peccenini S, Pennesi R, Pierini B, Poldini L, Prosser F, Raimondo FM, Roma-Marzio F, Rosati L, Santangelo A, Scoppola A, Scortegagna S, Selvaggi A, Selvi F, Soldano A, Stinca A, Wagensommer RP, Wilhalm T, Conti F (2018) An updated checklist of the vascular flora native to Italy. Plant Biosyst 152(2):179–303. https://doi.org/10.1080/11263504.2017.1419996
Biondi E, Blasi C, Burrascano S, Casavecchia S, Copiz R, Del Vico E, Galdenzi D, Gigante D, Lasen C, Spampinato G, Venanzoni R, Zivkovic L (2010) Manuale Italiano di interpretazione degli habitat della (Direttiva 92/43/CEE). Società Botanica Italiana. Ministero dell’Ambiente e della Tutela del Territorio e del Mare, Rome, p 11
Bonanomi G, Legg C, Mazzoleni S (2005) Autoinhibition of germination and seedling establishment by leachate of Calluna vulgaris leaves and litter. Community Ecol 6(2):203–208
Borghesio L (2009) Effects of fire on the vegetation of a lowland heathland in North-Western Italy. Plant Ecol 201:723–731. https://doi.org/10.1007/s11258-008-9459-1
Britton AJ, Marrs RH, Carey PD, Pakeman RJ (2000) Comparison of techniques to increase Calluna vulgaris cover on heathland invaded by grasses in Breckland, south East England. Biol Conserv 95:227–232
Brusa G, Piazza D (2015) La brughiera pedemontana lombarda: aspetti storici, fattori ecologici e indicazioni gestionali per la sua conservazione. Consorzio del Parco Brughiera Briantea, Lonate sul Seveso (Monza Brianza)
Brusa G, Dalle Fratte M, Zanzottera M, Cerabolini BEL (2019) Cambiamenti a lungo termine dell’uso del suolo nell’area di Malpensa e conseguenze sull’attuale presenza della brughiera. Pianura - Scienze e storia dell’ambiente padano 38:72–85
Brys R, Jacquemyn H, De Blust G (2005) Fire increases aboveground biomass, seed production and recruitment success of Molinia caerulea in dry heathland. Acta Oecol 28:299–305. https://doi.org/10.1016/j.actao.2005.05.008
Buffa G, Del Vecchio S, Acosta ATR (2016) Il metodo del transetto di vegetazione. In: Angelini P, Casella L, Grignetti A, Genovesi P (ed) Manuali per il monitoraggio di specie e habitat di interesse comunitario (Direttiva 92/43/CEE) in Italia: habitat. Istituto Superiore per la Protezione e la Ricerca Ambientale, p 21
Caronni F (1988) Il prugnolo tardivo (Prunus serotina Ehrh.) in Italia. Dissertation, University of Padova
Carvalheiro LG, Buckley YM, Memmott J (2010) Diet breadth influences how the impact of invasive plants is propagated through food webs. Ecol 91(4):1063–1074
Cerabolini BEL, Brusa G, Ceriani RM, Armiraglio S, De Molli C, Pierce S (2017) Ecology and floristic composition of heathlands in the Po basin and the Southern Alps (NW Italy). Bot Lett. https://doi.org/10.1080/23818107.2017.1387077
Closset-Kopp D, Chabrerie O, Valentin B, Delachapelle H, Decocq G (2007) When Oskar meets Alice: does a lack of trade-off in r/K-strategies make Prunus serotina a successful invader of European forests? For Ecol Manag 247:120–130
Csiszàr A, Korda M, Schmidt D, Sporcic D, Teleki B, Tiborcz V, Zagyvai G, Bartha D (2012) Study on allelopathic potential of some invasive and potentially invasive neophytes. Proceedings of the International Scientific Conference on Sustainable Development & Ecological Footprint. Sopron, Hungary, 26-27 March 2012, University of West Hungary, 1-6
Dostálek J, Frantík T (2015) Dry heathland restoration in the Zlatnice nature reserve (Czech Republic): an assessment of the effectiveness of grazing and sod-cutting. Hacquetia 14(1):113–122. https://doi.org/10.1515/hacq-2015-0006
Dyderski MK, Jagodziński AM (2018) Drivers of invasive tree and shrub natural regeneration in temperate forests. Biol Invasions 20:2363–2379. https://doi.org/10.1007/s10530-018-1706-3
Early R, Bradley BA, Dukes JS, Lawler JJ, Olden JD, Blumenthal DM, Gonzalez P, Grosholz ED, Ibañez I, Miller LP, Sorte CJB, Tatem AJ (2016) Global threats from invasive alien species in the twenty-first century and national response capacities. Nat Commun 7. https://doi.org/10.1038/ncomms12485
Ehrenfeld JG (2003) Effect of exotic invasion on soil nutrient cycling processes. Ecosyst 6(6):503–523
Ellenberg H, Weber HE, Düll R, Wirth V, Werner W (2001) Indicator values of plants in Central Europe. Scr geobot 18, 3rd edn. Goltze Publishing, Göttingen, (DE)
European Environmental Agency (EEA) (2015) Habitat: 4030 European dry heaths - report under the article 17 of the habitat directive, period 2007–2012. Copenhagen
Fagúdez J (2013) Heathlands confronting global change: drivers of biodiversity loss from past to future scenarios. Ann Bot 111:151–172. https://doi.org/10.1093/aob/mcs257
Galasso G, Conti F, Peruzzi L, Ardenghi NMG, Banfi E, Celesti-Grapow L, Albano A, Alessandrini A, Bacchetta G, Ballelli S, Bandini Mazzanti M, Barberis G, Bernardo L, Blasi C, Bouvet D, Bovio M, Cecchi L, Del Guacchio E, Domina G, Fascetti S, Gallo L, Gubellini L, Guiggi A, Iamonico D, Iberite M, Jiménez-Mejías P, Lattanzi E, Marchetti D, Martinetto E, Masin RR, Medagli P, Passalacqua NG, Peccenini S, Pennesi R, Pierini B, Podda L, Poldini L, Prosser F, Raimondo FM, Roma-Marzio F, Rosati L, Santangelo A, Scoppola A, Scortegagna S, Selvaggi A, Selvi F, Soldano A, Stinca A, Wagensommer RP, Wilhalm T, Bartolucci F (2018) An updated checklist of the vascular flora alien to Italy. Plant Biosyst 152(3):556–592. https://doi.org/10.1080/11263504.2018.1441197
Gentili R, Ferrè C, Cardarelli E, Montagnani C, Bogliani G, Citterio S, Comolli R (2019) Comparing negative impacts of Prunus serotina, Quercus rubra and Robinia pseudoacacia on native forest ecosystems. Forests 10:842. https://doi.org/10.3390/f10100842
Giacomini V (1958) Sulla vegetazione della Brughiera di Gallarate. In: Wikus E, Pignatti S (ed) Relazione sulla terza escursione fitosociologica internazionale. Arch Bot Biogeogr Ital 34(2):63–68
Godefroid S, Phartyal SS, Weyembergh G, Koedam N (2005) Ecological factors controlling the abundance of non-native black cherry (Prunus serotina) in deciduous forest understory in Belgium. For Ecol Manag 210:91–105. https://doi.org/10.1016/j.foreco.2005.02.024
Guzzetti L, Galimberti A, Bruni I, Magoni C, Ferri M, Tassoni A, Sangiovanni E, Dell’Agli M, Labra M (2017) Bioprospecting on invasive plant species to prevent seed dispersal. Sci Rep 7:13799. https://doi.org/10.1038/s41598-017-14183-5
Halarewicz A, Zolnierz L (2014) Changes in the understorey of mixed coniferous forest plant communities dominated by the American black cherry (Prunus serotina Ehrh.). For Ecol Manag 313:91–97
Henning K, Lorenza A, von Oheimb G, Härdtle W, Tischew S (2017a) Year-round cattle and horse grazing supports the restoration of abandoned, dry sandy grassland and heathland communities by supressing Calamagrostis epigejos and enhancing species richness. J Nat Conserv 40:120–130. https://doi.org/10.1016/j.jnc.2017.10.009
Henning K, von Oheimb G, Härdtle W, Fichtner A, Tischew S (2017b) The reproductive potential and importance of key management aspects for successful Calluna vulgaris rejuvenation on abandoned continental heaths. Ecol Evol 7:2091–2100. https://doi.org/10.1002/ece3.2816
Hester AJ, Miles J, Gimingham CH (1991) Succession from heather moorland to birch woodland. I Experimental alteration of specific environmental conditions in the field J Ecol 79(2):303–315
Jacini F, Moser L, Allegri E, Cartiera Vita Mayer & C, Perego E, Pepe G (1957) Le brughiere lombarde. Assoc For Lomb - Cassa di Risparmio delle Province Lombarde, Milan
Kawaletz H, Mölder I, Zerbe S, Annighöfer P, Terwei A, Ammer C (2013) Exotic tree seedlings are much more competitive than natives but show underyielding when growing together. J Plant Ecol 6:305–315. https://doi.org/10.1093/jpe/rts044
Lazzaro L, Giuliani C, Fabiani A, Agnelli AE, Pastorelli R, Lagomarsino A, Benesperi R, Calamassi R, Foggi B (2014) Soil and plant changing after invasion: the case of Acacia dealbata in a Mediterranean ecosystem. Sci Total Environ 1:491–498
Lazzaro L, Mazza G, d'Errico G, Fabiani A, Giuliani C, Inghilesi AF, Lagomarsino A, Landi S, Lastrucci L, Pastorelli R, Roversi PF, Torrini G, Tricarico E, Foggi B (2018) How ecosystems change following invasion by Robinia pseudoacacia: insights from soil chemical properties and soil microbial, nematode, microarthropod and plant communities. Sci Total Environ 622-623:1509–1518. https://doi.org/10.1016/j.scitotenv.2017.10.017
Litt AR, Cord EE, Fulbright TE, Schuster GL (2014) Effects of invasive plants on arthropods. Conserv Biol 28:1532–1549. https://doi.org/10.1111/cobi.12350
Lonati M, Gorlier A, Ascoli D, Marzano R, Lombardi G (2009) Response of the alien species Panicum acuminatum to disturbance in an Italian lowland heathland. Bot Helv 119:105–111. https://doi.org/10.1007/s00035-009-0063-3
Luzzatto F, Artini E, Brizi U, Fenaroli L, Pratolongo U, Parisi P, Alpe V, Favari A (1927) Le brughiere. Fed Ital dei Consorzi Agrar, Piacenza
Manning P, Putwain PD, Webb NR (2004) Identifying and modelling the determinants of woody plant invasion of lowland heath. J Ecol 92:868–881
Mazza G, Tricarico E, Genovesi P, Gherardi F (2014) Biological invaders are threats to human health: an overview. Ethol Ecol Evol 26:112–129. https://doi.org/10.1080/03949370.2013.863225
Mitchell RJ, Marrs RH, Le Duc MG, Auld MHD (1997) A study of succession on lowland heaths in Dorset, southern England: changes in vegetation and soil chemical properties. J Appl Ecol 34(6):1426–1444
Nentwig W, Bacher S, Kumschick S, Petr Pyšek P, Vilá M (2018) More than “100 worst” alien species in Europe. Biol Invasions 20:1611. https://doi.org/10.1007/s10530-017-1651-6
Pavari A, De Philippis A (1941) La sperimentazione di specie forestali esotiche in Italia. Risultati del primo ventennio. Ann Sper Agrar 38:9–96
Pignatti S, Menegoni P, Pietrosanti S (2005) Bioindicator values of vascular plants of the flora of Italy. Braun-Blanquetia 39:3–62
Pimentel D, Zuniga R, Morrison D (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol Econ 52:273–288. https://doi.org/10.1016/j.ecolecon.2004.10.002
Quin SLO, Artz RRE, Coupar AM, Littlewood NA, Woodin SJ (2014) Restoration of upland heath from a graminoid- to a Calluna vulgaris-dominated community provides a carbon benefit. Agric, Ecosyst Env 185:133–143. https://doi.org/10.1016/j.agee.2013.12.022
Ramil Rego P, Rodriguez Guitián MA, López Castro H, Ferreiro da Costa J, Muñoz Sobrino C (2013) Loss of european dry heaths in NW Spain: a case study. Divers 5(3):557–580. https://doi.org/10.3390/d5030557
Sartori F (1988) Prunus serotina Ehrh. En Italie. Colloq Phytosociol 14:185–217
Società per Azioni Esercizi Aeroportuali (SEA S.p.A.) (2010) Studio di Impatto Ambientale - Nuovo Master Plan Aeroportuale dell’Aeroporto di Malpensa. Segrate (Milano)
Starfinger U (1990) Die Einbürgerung der Spӓtblühenden Traubenkirsche (Prunus serotina Ehrh.) in Mitteleuropa. Landschaftsentwicklung und Umweltforschung 69:118
Starfinger U (1997) Introduction and naturalization of Prunus serotina in Central Europe. In: Starfinger U, Edwards K, Kowarik I, Williamson M (1998) Plant invasions: ecological mechanisms and human responses. Backhuys Publ, Leiden, The Netherlands, pp 161–171
Starfinger U (2010) Prunus serotina Ehrh. Online Database of the European Network on Invasive Alien Species. www.nobanis.org. Accessed 4 November 2018
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
Ter Braak CJF, Šmilauer P (2012) Canoco reference manual and User's guide: software for ordination, version 5.0. Microcomputer power, USA
Terwei A, Zerbe S, Zeileis A, Annighofer P, Kawaletz H, Molder I, Ammer C (2013) Which are the factors controlling tree seedling establishment in North Italian floodplain forests invaded by non-native tree species? For Ecol Manag 304:192–203. https://doi.org/10.1016/j.foreco.2013.05.003
Vanhellemont M, Wauters L, Baeten L, Bijlsma RJ, De Frenne P, Hermy M, Verheyen K (2010a) Prunus serotina unleashed: invader dominance after 70 years of forest development. Biol Invasions 12:1113–1124
Vanhellemont M, Verheyen K, Staelens J, Hermy M (2010b) Factors affecting radial growth of the invasive Prunus serotina in pine plantations in Flanders. Eur J For Res 129:367–375
Verheyen K, Vanhellemont M, Stock T, Hermy M (2007) Predicting patterns of invasion by black cherry (Prunus serotina Ehrh.) in Flanders (Belgium) and its impact on the forest understorey community. Divers Distrib 13:487–497
Viciani D, Cerabolini BEL (2016) 4030 Lande secche europee. In: Angelini P, Casella L, Grignetti A, Genovesi P (ed) Manuali per il monitoraggio di specie e habitat di interesse comunitario (Direttiva 92/43/CEE) in Italia: habitat. Istituto Superiore per la Protezione e la Ricerca Ambientale, pp 100-101
Vilà M, Espinar JL, Hejda M, Hulme PE, Jarošìk 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
Acknowledgments
We wish to thank Nicola MG Ardenghi (Univerity of Pavia), Gabriele Galasso and Enrico Banfi (Natural History Museum of Milano) for their valuable help in plant species identification; Italian Ministry of Defence for access to the area where the study took place; the Ticino Regionol Park administration for useful information about the study area; Società per Azioni Aeroportuali SEA and Bird Control Italy S.r.l. for funding this research.
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Vegini, E., Lastrucci, L., Lazzaro, L. et al. Impact of Prunus serotina Ehrh. invasion on heathland vegetation: a case of study in North-Western Italy. Biologia 75, 327–336 (2020). https://doi.org/10.2478/s11756-019-00408-7
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DOI: https://doi.org/10.2478/s11756-019-00408-7