Abstract
Several tree species are found among the most well-know and impacting invasive plants that produce changes in richness, abundance and composition of native plant species as well as in environmental characteristics and ecosystem functioning. Hovenia dulcis Thunb. (Rhamnaceae) is a tree native to East Asia, invasive in southern South America in different forest ecosystems. This study was aimed at assessing the effects of H. dulcis on richness, abundance and composition of regenerating species in seasonal deciduous forest (SDF) by comparing invaded and non-invaded areas. The existence of correlations between abundance and richness of regenerating species with age and density of the invasive species, as well as with characteristics of canopy openness, litter thickness, slope, and soil moisture, was investigated in areas invaded by H. dulcis. Differences observed in canopy openness and litter tickness between areas invaded by H. dulcis and control areas suggest that H. dulcis is able to change environmental conditions on a local scale. Although no difference was observed in species richness between areas with and without H. dulcis, the differences registered in abundance and composition of regenerating species make the impact by H. dulcis on regeneration patterns in SDF fragments evident. The impacts caused by H. dulcis on SDF confirmed by this study highlight the need for its control in legally protected areas and their immediate surroundings, as well as for the adoption of public policies to promote the substitution of H. dulcis for locally native species.
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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
Aragón R, Montti L, Ayup MM, Fernández R (2014) Exotic species as modifiers of ecosystem processes: litter decomposition in native and invaded secondary forests of NW Argentina. Acta Oecol 54:21–28
Bartemucci P, Messier C, Canham CD (2006) Overstory influences on light attenuation patterns and understory plant community diversity and composition in southern boreal forests of Quebec. Can J For Res 36:2065–2079
Barton K (2016) MuMIn: multi-model inference. R package version 1.15.6. https://CRAN.R-project.org/package=MuMIn
Baskin CC, Baskin JM (2014) Seeds: ecology, biogeography, and evolution of dormancy and germination. Elsevier, San Diego
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67(1):1–48
Beard JS (1955) The classification of tropical American vegetation-types. Ecology 36(1):89–100
Bellingham PJ, Tanner EVJ, Martin PH, Healey JR, Burge OR (2018) Endemic trees in a tropical biodiversity hotspot imperilled by an invasive tree. Biol Conserv 217:47–53
Bertin RI, Manner ME, Larrow BF, Cantwell TW, Berstene EM (2005) Norway maple (Acer platanoides) and other non-native trees in urban woodlands of central Massachusetts. J Torrey Bot Soc 132:225–235
Bianchini E, Pimenta JA, Santos FAM (2001) Spatial and temporal variation in a tropical semi-deciduous forest. Braz Arch Biol Technol 4:269–276
Boeni BO (2011) Riqueza, estrutura e composição de espécies em floresta secundária invadida por Hovenia dulcis Thunb., caracterização do seu nicho de regeneração e efeitos alelopáticos. Thesis, Universidade do Vale do Rio dos Sinos, Brazil
Brasil (2008) Instrução Normativa 6, de 23 de setembro de 2008. Reconhece as espécies da flora brasileira ameaçadas de extinção. Diário Oficial da República Federativa do Brasil, Poder Executivo, Brasília, 24 Set 2008
Buono RA, Oliveira AB, Paiva EAS (2008) Anatomy, ultrastructure and chemical composition of food bodies of Hovenia dulcis (Rhamnaceae). Ann Bot 101:1341–1348
Cáceres NC, Monteiro-Filho ELA (2001) Food habits, home range and activity of Didelphis aurita (Mammalia, Marsupialia) in a forest fragment of southern Brazil. Stud Neotrop Fauna Environ 36:85–92
Cadotte MW, Carscadden K, Mirotchnick N (2011) Beyond species: functional diversity and the maintenance of ecological processes and services. J Appl Ecol 48:1079–1087
Capellesso ES, Scrovonski KL, Zanin EM, Hepp LU, Bayer C, Sausen TL (2016) Effects of forest structure on litter production, soil chemical composition and litter–soil interactions. Acta Bot Bras 30(3):329–335
Carvalho PER (1994) Ecologia, silvicultura e usos da uva-do-japão (Hovenia dulcis Thunberg). Circular Técnica EMBRAPA Florestas, Colombo
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
Castro-Díez P, Pauchard A, Traveset A, Vilà M (2016) Linking the impacts of plant invasion on community functional structure and ecosystem properties. J Veg Sci 27(6):1233–1242
Constán-Nava S, Soliveres S, Torices R, Serra L, Bonet A (2014) Direct and indirect effects of invasion by the alien tree Ailanthus altissima on riparian plant communities and ecosystem multifunctionality. Biol Invasions 17:1095–1108
Conway WC, Smith LM, Bergan JF (2002) Potential allelopathic interference by exotic Chinese Tallow Tree (Sapium sebiferum). Am Midl Nat 148:43–53
Davis MA, Grime JP, Thompson K (2000) Fluctuating resources in plant communities: a general theory of invisibility. J Ecol 88:528–534
Dechoum MS, Castellani TT, Zalba SM, Rejmánek M, Peroni N, Tamashiro JY (2015a) Community structure, succession and invasibility in a seasonal deciduous Forest in southern Brazil. Biol Invasions 17(6):1697–1712
Dechoum MS, Zenni RD, Castellani TT, Zalba SM, Rejmánek M (2015b) Invasions across secondary forest successional stages: effects of local plant community, soil, litter, and herbivory on Hovenia dulcis seed germination and seedling establishment. Plant Ecol 216:823–833
Enoki T, Drake DR (2017) Alteration of soil properties by invasive tree Psidium cattleianum along a precipitation gradient on O’ahu Island, Hawai’i. Plant Ecol 218:947–955
Eriksson O (1995) Seedling recruitment in deciduous forest herbs: the effects of litter, soil chemistry and seed bank. Flora 190:65–70
Essl F, Milasowszky N, Dirnbock T (2011) Plant invasions in temperate forests: resistance or ephemeral phenomenon? Basic Appl Ecol 12:1–9
Essl F, Mang T, Moser D (2012) Ancient and recent alien species in temperate forests: steady state and time lags. Biol Invasions 14:1331–1342
Fajardo A, Gundale MJ (2017) Canopy cover type, and not fine-scale resource availability, explains native and exotic species richness in a landscape affected by anthropogenic fires and posterior land-use change. Biol Invasions 20(2):385–398
Gundale MJ, Sutherland S, DeLuca TH (2008) Fire, native species, and soil resource interactions influence the spatiotemporal invasion pattern of Bromus tectorum. Ecography 31:201–210
Hata K, Kato H, Kachi N (2010) Litter of an alien tree, Casuarina equisetifolia, inhibits seed germination and initial growth of a native tree on the Ogasawara Islands (subtropical oceanic islands). J For Res 15(6):384–390
Hejda M, Pysek P, Jarosík V (2009) Impact of invasive plants on the species richness, diversity and composition of invaded communities. J Ecol 97:393–403
Hendges CD, Fortes VB, Dechoum MS (2012) Consumption of the invasive alien species Hovenia dulcis thumb. by Sapajus nigritus Kerr, 1792 in a protected area in southern Brazil. Rev Bras Zoociências 14(1, 2, 3):255–260
Hughes RF, Denslow JS (2005) Invasion by a N-2-fixing tree alters function and structure in wet lowland forests of Hawaii. Ecol Appl 15:1615–1628
Hyun TK, Eom SH, Yu CY, Roitsch T (2010) Hovenia dulcis—an Asian traditional herb. Planta Med 76:943–949
IBGE (2012) Manual técnico da vegetação brasileira, 2a edição. IBGE, Rio de Janeiro
Kazakou E, Vile D, Shipley B, Gallet C, Garnier E (2006) Co-variations in litter decomposition, leaf traits and plant growth in species from a Mediterranean old-field succession. Funct Ecol 20:21–30
Kazakou E, Violle C, Roumet C, Pintor C, Gimenez O, Garnier E (2009) Litter quality and decomposability of species from a Mediterranean succession depend on leaf traits but not on nitrogen supply. Ann Bot 104:1151–1161
Klein RM (1972) Árvores nativas da floresta subtropical do Alto Uruguai. Sellowia 24:6–62
Kumschick S, Gaertner M, Vilà M, Essl F, Jeschke JM, Pyšek P, Ricciardi A, Bacher S, Blackburn TM, Dick JTA, Evans T, Hulme PE, Kühn I, Mrugała A, Pergl J, Rabitsch W, Richardson DM, Sendek A, Winter M (2015) Ecological impacts of alien species: quantification, scope, caveats, and recommendations. Bioscience 65:55–63
Lazzarin LC, Silva AC, Higuchi P, Souza K, Perin JE, Cruz AP (2015) Invasão biológica por Hovenia dulcis Thunb. em fragmentos florestais na região do Alto Uruguai, Brasil. Rev Árvore 39(6):1007–1017
Legendre P, Gallagher ED (2001) Ecologically meaningful transformations for ordination of species data. Oecologia 129:271–280
Lemmon PE (1957) A new instrument for measuring forest overstory density. J For 55(9):667–668
Levine JM, Vilà M, D’Antonio CM, Dukes JS, Grigulis K, Lavorel S (2003) Mechanisms underlying the impacts of exotic plant invasions. Proc R Soc Lond 270:775–781
Lima REM, Dechoum MS, Castellani TT (2015) Native seed dispersers may promote the spread of the invasive Japanese raisin tree (Hovenia dulcis Thunb.) in seasonal deciduous forest in southern Brazil. Trop Conserv Sci 8(3):846–862
Long JA (2019) jtools: analysis and presentation of social scientific data. R package version 2.0.1, https://cran.r-project.org/package=jtools
Lorenzo P, Rodríguez J, González L, Rodríguez-Echeverría S (2016) Changes in microhabitat, but not allelopathy, affect plant establishment after Acacia dealbata invasion. J Plant Ecol 10(4):610–617
Makkonen M, Berg MP, Hättenschwiler S, van Ruijven J, van Bodegom PM, Aerts R (2012) Highly consistent effects of plant litter identity and functional traits on decomposition across a latidudinal gradient. Ecol Lett 15(9):1033–1041
Martin PH, Marks PL (2006) Intact forests provide only weak resistance to a shade-tolerant invasive Norway maple (Acer platanoides L.). J Ecol 94:1070–1079
Martin PH, Canham CD, Kobe RK (2010) Divergence from the growth-survival trade-off and extreme high growth rates drive patterns of exotic tree invasions in closed-canopy forests. J Ecol 98:778–789
Meyer L, Gasper AL, Sevegnani L, Schorn LA, Lingner DV, Vibrans AC, Verdi M, Santos AS, Dreveck S, Korte A (2012) Regeneração natural da Floresta Estacional Decidual em Santa Catarina. In: Vibrans AC, Sevegnani L, de Gasper AL, Lingner DV (eds) Inventário Florístico Florestal de Santa Catarina, Floresta Estacional Decidual, vol 2. Edifurb, Blumenau
Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens, MHH, Wagner H (2013) Vegan: community ecology package. R package version 2.0-7. http://CRAN.Rproject.org/package=vegan
Olden JD, Comte L, Giam X (2018) The Homogocene: a research prospectus for the study of biotic homogenisation. NeoBiota 37:23–36
Padilha DL, Loregian AC, Budke JC (2015) Forest fragmentation does not matter to invasions by Hovenia dulcis. Biodivers Conserv 24:2293–2304
Potgieter LJ, Strasberg D, Wilson JRU, Richardson DM (2014) Casuarina invasion alters primary succession on lava flows in the Mascarene Islands. Biotropica 46:268–275
Pysek P, Krivánek M, Jarosík V (2009) Planting intensity, residence time, and species traits determine invasion success of alien woody species. Ecology 90(10):2734–2744
Reinhart KO, Greene E, Callaway RM (2005) Effects of Acer platanoides invasion on understory plant communities and tree regeneration in the northern Rocky Mountains. Ecography 28:573–582
Reinhart KO, Gurnee J, Tirado R, Callaway RM (2006) Invasion through quantitative effects: intense shade drives native decline and invasive success. Ecol Appl 16(5):1821–1831
Rejmánek M, Richardson DM (2013) Trees and shrubs as invasive species—2013 update on the global database. Divers Distrib 19:1093–1094
Richardson DM, Rejmánek M (2011) Trees and shrubs as invasive alien species—a global review. Divers Distrib 17:788–809
Richardson DM, Hui C, Núñez MA, Pauchard A (2014) Tree invasions: patterns, processes, challenges and opportunities. Biol Invasions 16:473–481
RStudio Team (2017). RStudio: integrated development for R. RStudio, Inc., Boston, MA. http://www.rstudio.com/
Santa Catarina (2014) Plano de Manejo Fase II do Parque Estadual Fritz Plaumann, vol I, Plano Básico. 2014. FATMA, Florianopolis
Scariot A (2000) Seedling mortality by litterfall in Amazonian forest fragments. Biotropica 32:662–669
Schaff LB, Filho AF, Galvão F, Sanquetta CR, Longhi SJ (2006) Modificações florístico-estruturais de um remanescente de Floresta Ombrófila Mista Montana no período de 1979 e 2000. Ci Fl 16(3):271–291
Schuster MJ, Dukes JS (2014) Non-additive effects of invasive tree litter shift seasonal N release: a potential invasion feedback. Oikos 123:1101–1111
Siminski A, Fantini AC, Guries RP, Ruschel AR, Reis MS (2011) Secondary forest succession in the Mata Atlantica, Brazil: floristic and phytosociological trends. ISRN Ecology Article ID 759893
Staska B, Essl F, Samimi C (2014) Density and age of invasive Robinia pseudoacacia modulate its impact on floodplain forests. Basic Appl Ecol 15:551–558
Szefer P, Carmona CP, Chmel K, Konecná M, Libra M, Molem K, Novotný V, Segar ST, Svamberková E, Topliceanu TS, Leps J (2016) Determinants of litter decomposition rates in a tropical forest: functional traits, phylogeny and ecological succession. Oikos 126(8):1101–1111
Vibrans AC, Sevegnani L, Gasper AL, Lingner DV (2012a) Inventário Florístico Florestal de Santa Catarina—Floresta Estacional Decidual, vol 2. Edifurb, Blumenau
Vibrans AC, Sevegnani L, Gasper AL, Lingner DV (2012b) Inventário Florístico Florestal de Santa Catarina—Diversidade e Conservação dos Remanescentes Florestais, vol 1. Edifurb, Blumenau
Vilà M, Espinar JL, Hejda M, Hulme PE, Jarošík 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
Wandscheer ACD, Borella J, Bonatti LC, Pastorini LH (2011) Atividade alelopática de folhas e pseudofrutos de Hovenia dulcis Thunb. (Rhamnaceae) sobre a germinação de Lactuca sativa L. (Asteraceae). Acta Bot Bras 25(1):25–30
Wangen SR, Webster CR (2006) Potential for multiple lag phases during biotic invasions: reconstructing an invasion of the exotic tree Acer platanoides. J Appl Ecol 43:258–268
Wardle DA, Bardgett RD, Callaway RM, Van der Putten WH (2011) Terrestrial ecosystem responses to species gains and losses. Science 332(80):1273–1278
Warren RJ II, Labatore A, Candeias M (2017) Allelopathic invasive tree (Rhamnus cathartica) alters native plant communities. Plant Ecol 218(10):1233–1241
Zanne AE, Oberle B, Dunham KM, Milo AM, Walton ML, Young DF (2015) A deteriorating state of affairs: how endogenous and exogenous factors determine plant decay rates. J Ecol 103:1421–1431
Zenni RD, Ziller SR (2011) An overview of invasive plants in Brazil. Rev Bras Bot 34(3):431–446
Zucaratto R, Pires AS (2014) The exotic palm Roystonea oleracea (Jacq.) O. F. Cook (Arecaceae) on an island within the Atlantic Forest Biome: naturalization and influence on seedling recruitment. Acta Bot Bras 28(3):417–421
Acknowledgements
Financial support was provided by Engie Energia S.A. and the Graduate Program in Ecology of the Federal University of Santa Catarina. We thank the Horus Institute for Environmental Conservation and Development and ECOPEF for logistical and technical support, and IMA SC for authorizing the research. ADS and MSD were supported by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, Brazil). We also thank the two anonymous reviewers and the handling editor who helped to improve the manuscript.
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Schmidt, A.D., Castellani, T.T. & de Sá Dechoum, M. Biotic and abiotic changes in subtropical seasonal deciduous forest associated with invasion by Hovenia dulcis Thunb. (Rhamnaceae). Biol Invasions 22, 293–306 (2020). https://doi.org/10.1007/s10530-019-02089-4
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DOI: https://doi.org/10.1007/s10530-019-02089-4