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Management priorities for exotic plants in an urban Atlantic Forest reserve

ABSTRACT

Biological diversity is directly affected by alien species, even though the diagnosed impacts vary with scale. Early identification of the invasion of natural patches is essential for effective conservation actions. We aimed to determine the exotic plant species present inside Fontes do Ipiranga State Park (PEFI), an urban protected area located in the city of São Paulo, Brazil, and their relative proportions of occurrence in the native forest. Our goal was to use these data to assess their invasion status according to specific literature and to define management priorities for them. Therefore, we surveyed the presence of exotic plants within the canopy layer and understory of three native forest areas with different levels of disturbance. We found ten exotic plant species. The species found in both strata (60 %) were considered non-dominant ruderal. We assessed the density:coverage ratio to try to distinguish groups of priority, and found Livistona chinensis, Archontophoenix cunninghamiana, and Syzygium jambos to be classified as high priority for management. The early stage of the invasion process at PEFI indicates it is an area of high conservation value, and so we provide recommendations for management priorities prior to severe changes in the composition of the natural plant community.

Keywords:
botanical garden; disturbance; invasion biology; invasion status; protected area; species population ecology

Introduction

Exotic species differ from native species in that they colonize regions where they originally would not have existed without intentional or accidental human transport (Richardson et al. 2000Richardson DM, Pyšek P, Rejmánek M, Barbour MG, Panetta FD, West CJ. 2000. Naturalization and invasion of alien plants: concepts and definitions. Diversity and Distributions 6: 93-107.). The degree of establishment and success of an alien species, and thus their naturalization, in a new environment encompasses a gradient of the invasion process (Richardson et al. 2000Richardson DM, Pyšek P, Rejmánek M, Barbour MG, Panetta FD, West CJ. 2000. Naturalization and invasion of alien plants: concepts and definitions. Diversity and Distributions 6: 93-107.). Invasive alien species are capable of constant propagation, viable population maintenance and efficient dispersion, which all favor the expansion of the area where they occur beyond the source of introduction, thus allowing them to enter new environments (Richardson et al. 2000Richardson DM, Pyšek P, Rejmánek M, Barbour MG, Panetta FD, West CJ. 2000. Naturalization and invasion of alien plants: concepts and definitions. Diversity and Distributions 6: 93-107.). Due to these characteristics, invasive alien species are considered a serious environmental issue (Moro et al. 2012Moro MF, Souza VC, Oliveira-Filho AT, et al. 2012. Aliens in the room: what to do with exotic species in taxonomic, floristic and phytosociological studies? Acta Botanica Brasilica 26: 991-999.).

Indicators created to measure the rate of biodiversity loss have converged upon growing trends of pressure asserted by alien species on biological diversity (Butchart et al. 2010Butchart SHM, Walpole M, Collen B, et al. 2010. Global biodiversity: indicators of recent declines. Science 328: 1164-1168. ). The impact of exotic plant species on natural plant communities can increase biomass and primary production, although other variables, such as growth, abundance, diversity, and fitness of native plants, are harmed in the invasion process (Vilà et al. 2011Vilà M, Espinar JL, Hejda M, et al. 2011. Ecological impacts of invasive alien plants: a meta-analysis of their effects on species, communities and ecosystems. Ecology Letters 14: 702-708.). It is estimated that between 0.5 and 0.7 % of trees and shrubs are currently described by the literature as invasive (Pyšek et al. 2004Pyšek P, Richardson DM, Rejmánek M, Webster GL, Williamson M, Kirschner J. 2004. Alien plants in checklists and floras: towards better communication between taxonomists and ecologists. Taxon 53: 131-143.). Since exotic species are not equally harmful, local scale assessments are needed despite their economic and environmental impacts (Rejmánek 2014Rejmánek M. 2014. Invasive trees and shrubs: where do they come from and what we should expect in the future? Biological Invasions 16: 483-498.). The most traditional definitions of the different paths in the invasion process differ by incorporating (Davis et al. 2000Davis MA, Grime JP, Thompson K. 2000. Fluctuating resources in plant communities: a general theory of invasibility. Journal of Ecology 88: 528-534.; Lockwood et al. 2007Lockwood JL, Hoopes MF, Marchetti MP. 2007. Invasion ecology. 1st. edn. Oxford, Wiley-Blackwell.; Blackburn et al. 2014Blackburn TM, Essl F, Evans T, et al. 2014. A unified classification of alien species based on the magnitude of their environmental impacts. PLOS Biology 12(5): e1001850. doi:10.1371/journal.pbio.1001850
https://doi.org/10.1371/journal.pbio.100...
) or not (Richardson et al. 2000Richardson DM, Pyšek P, Rejmánek M, Barbour MG, Panetta FD, West CJ. 2000. Naturalization and invasion of alien plants: concepts and definitions. Diversity and Distributions 6: 93-107.; Pyšek et al. 2004Pyšek P, Richardson DM, Rejmánek M, Webster GL, Williamson M, Kirschner J. 2004. Alien plants in checklists and floras: towards better communication between taxonomists and ecologists. Taxon 53: 131-143.) the impacts alien species have on the native community for categorizing them as invaders.

Worldwide, cataloged species richness is 1.2 million species, however, considering just terrestrial species it is estimated that 86 % have not yet been discovered and described (Mora et al. 2011Mora C, Tittensor DP, Adl S, Simpson AGB, Worm B. 2011. How Many Species Are There on Earth and in the Ocean? PLOS Biology 9(8): e1001127. doi: 10.1371/journal.pbio.1001127
https://doi.org/10.1371/journal.pbio.100...
). South America has the greatest biological diversity in the world, housing around 20 % of all its flora and fauna (GISP 2005GISP - Global Invasive Species Programme. 2005. A América do Sul invadida: a crescente ameaça das espécies exóticas invasoras. Curitiba, GISP. ). Brazil is considered to have the richest flora of any country in the world, even though only approximately one-third of its species expected richness is known (Forzza et al. 2012Forzza RC, Baumgratz JFA, Bicudo CEM, et al. 2012. New Brazilian floristic list highlights conservation challenges. Bioscience 62: 39-45.). Biological invasion by exotic species has been one of the main factors for the loss of biodiversity globally (Kowarik 2011Kowarik I. 2011. Novel urban ecosystems, biodiversity, and conservation. Environmental Pollution 159: 1974-1983. ).

Given the characteristics of globally invasive alien species, comparative studies of floras can elucidate general patterns of plant invasions, thereby promoting a link between taxonomists and ecologists (Pyšek et al. 2004Pyšek P, Richardson DM, Rejmánek M, Webster GL, Williamson M, Kirschner J. 2004. Alien plants in checklists and floras: towards better communication between taxonomists and ecologists. Taxon 53: 131-143.). Among researchers, whether to include exotic species data, or even highlight them as such, has been debatable, as Moro et al. (2012Moro MF, Souza VC, Oliveira-Filho AT, et al. 2012. Aliens in the room: what to do with exotic species in taxonomic, floristic and phytosociological studies? Acta Botanica Brasilica 26: 991-999.) explain when analyzing the scenario nationally. According to these authors, useful information is lost when naturalized and invasive species are excluded from published plant lists (Moro et al. 2012Moro MF, Souza VC, Oliveira-Filho AT, et al. 2012. Aliens in the room: what to do with exotic species in taxonomic, floristic and phytosociological studies? Acta Botanica Brasilica 26: 991-999.). Reviewing the Brazilian flora (BFG 2015BFG. 2015. Growing knowledge: an overview of Seed Plant diversity in Brazil. Rodriguésia 66: 1085-1113.), Zenni (2015Zenni RD. 2015. The naturalized flora of Brazil: a step towards identifying future invasive non-native species. Rodriguésia 66: 1137-1144. ) diagnosed the presence of non-native species in all biomes, but especially the Atlantic Forest where the largest number of naturalized species was found. Human actions and activities were directly correlated with the observed patterns of naturalization (Zenni (2015Zenni RD. 2015. The naturalized flora of Brazil: a step towards identifying future invasive non-native species. Rodriguésia 66: 1137-1144. ).

In Brazil, protected areas, whether federal, state or municipal, are also affected by exotic species (Ziller & Dechoum 2014Ziller SR, Dechoum MS. 2014. Plantas e vertebrados exóticos invasores em unidades de conservação no Brasil. Biodiversidade Brasileira 2: 4-31.). Early diagnosis of the establishment of exotic species in protected areas is a major factor and a starting point for accomplishing conservation purposes (Ziller 2009Ziller SR. 2009. Como estabelecer prioridades para ações de controle de espécies exóticas invasoras em escala estadual. In: Cadernos da Mata Ciliar: Espécies exóticas invasoras. Coordenadoria de Biodiversidade e Recursos Naturais. São Paulo, Secretaria de Estado do Meio Ambiente. p. 12-16.). An initial overview of biological invasion on a nation-wide scale has demonstrated the need for monitoring and management (Sampaio & Schmidt 2014Sampaio AB, Schmidt IB. 2014. Espécies exóticas invasoras em unidades de conservação federais do Brasil. Biodiversidade Brasileira 2: 32-49.), especially to avoid the introduction of invasive species into protected areas (Ziller 2009Ziller SR. 2009. Como estabelecer prioridades para ações de controle de espécies exóticas invasoras em escala estadual. In: Cadernos da Mata Ciliar: Espécies exóticas invasoras. Coordenadoria de Biodiversidade e Recursos Naturais. São Paulo, Secretaria de Estado do Meio Ambiente. p. 12-16.). For example, Fontes do Ipiranga State Park (PEFI) is a protected area within the Atlantic Forest biome that is surrounded by an urban matrix. PEFI was officially created in 1969, and the first study on vegetation structure within its boundaries was that of Vuono (1985Vuono Y. 1985. Fitossociologia do estrato arbóreo da floresta da reserva biológica do Instituto de Botânica (São Paulo, SP). MSc Thesis, Instituto de Biociências, Universidade de São Paulo, São Paulo.), who indicated the presence of exotic tree species in the native forest. Eleven other studies involving floristics, phytosociology and population dynamics (Costa & Mantovani 1992Costa M, Mantovani W. 1992. Composição e estrutura de clareiras em mata mesófica na Bacia de São Paulo, SP. Revista do Instituto Florestal 4: 178-183.; Nastri et al. 1992Nastri V, Catharino ELM, Rossi L, et al. 1992. Estudos fitossociológicos em uma área do Instituto de Botânica de São Paulo utilizados em programas de educação ambiental. Revista do Instituto Florestal 4: 219-225.; Knobel 1995Knobel MG. 1995. Aspectos da regeneração natural do componente arbóreo-arbustivo de trecho da floresta da Reserva Biológica do Instituto de Botânica em São Paulo, SP. MSc Thesis, Universidade de São Paulo, São Paulo.; Gomes & Mantovani 2001Gomes EPC, Mantovani W. 2001. Size structure in a warm temperate forest tree populations in São Paulo, SP, Southeastern Brazil. Naturalia (São José do Rio Preto) 26: 131-158.; Pivello & Peccinini 2002Pivello V, Peccinini AA. 2002. A vegetação do PEFI. In: Bicudo DC, Forti MC, Bicudo CEM. (orgs.) Parque Estadual das Fontes do Ipiranga: unidade de conservação que resiste à urbanização de São Paulo . São Paulo, Secretaria do Meio Ambiente de São Paulo . p. 75-92.; Gomes et al. 2003Gomes EPC, Mantovani W, Kageyama PY. 2003. Mortality and recruitment of trees in a secondary montane rain forest in Southeastern Brazil. Brazilian Journal of Biology 63: 47-60.; Davison 2006Davison CP. 2006. Estrutura e composição da vegetação de sub-bosque em dois trechos de floresta do Parque Estadual das Fontes do Ipiranga, São Paulo-SP. Monograph, Universidade Presbiteriana Mackenzie, São Paulo.; 2009; Hirata et al. 2010Hirata J, Melo MMRF, Eisenlohr P. 2010. Padrões florísticos do componente arbóreo sob interferência de trilhas em um trecho de Floresta Ombrófila Densa de Transição em São Paulo, SP, Brasil. Hoehnea 37: 555-570.; Tanus et al. 2012Tanus MR, Pastore M, Bianchini RS, Gomes EPC. 2012. Estrutura e composição de um trecho de Mata Atlântica no Parque Estadual das Fontes do Ipiranga, São Paulo, SP, Brasil. Hoehnea 39: 157-168.; Kondrat 2014Kondrat H. 2014. Dinâmica da Comunidade Vegetal de Remanescente de Mata Atlântica na Região Metropolitana de São Paulo. MSc Thesis, Instituto de Botânica, São Paulo.) have since been carried out in different areas of PEFI (more than 10,000 individual plants sampled), all of which discriminated exotic species.

Considering this conceptual framework, and the current situation of the natural vegetation of PEFI, we aimed to determine the exotic plant species presently existing among the natural vegetation near the Botanical Garden of PEFI. The literature cites some exotic plant species as more frequently invasive than others. Thus, we also aimed to determine which of the exotic species found occurring in PEFI are found elsewhere around the world. Exotic plant species that occur only in the canopy layer are likely to have already been established, having become so only when the canopy was sufficiently open. Such a situation is compatible with a more disturbed environment and, considering the progression of restoration, exotic plant species are likely not to be able to change the status of the invasiveness. On the other hand, the presence of exotic plants in both strata (canopy layer and understory) of the forest, or only in the understory, may indicate a more continuous/recent disturbance. Therefore, we expect increasing similarity in the exotic plant species that occur in the canopy layer and the understory with increasing disturbance level. So, are the same exotic species present in the canopy layer and the understory? The investigation of exotic species in the understory strata can be indicative of either the regeneration of canopy layer individuals or the dispersal of species from other sites. In order to assess the characteristics of the populations of these species, we aimed to determine if the proportion of exotic species is the same between the canopy layer and the understory. Furthermore, we aimed to determine which exotic species should be key priorities for the allocation of resources for management in order to prevent the spread of invasion based on population ecology (Fig. 1).

Figure 1
Conceptual model of a proposed framework for defining exotic plant management priorities in order to identify the potential for invasions to spread. In Situation 1, the exotic species is in both the canopy layer and the understory, suggesting that it has the capacity for maintaining a viable population, at least with surviving juveniles, and that it should be a priority species for management. In Situation 2, the exotic species is present only in the canopy layer, and without juveniles in understory. It is impossible to predict if such a species is incapable of leaving descendants or if they fail to survive, so monitoring is recommended. Situation 3 portrays a situation where only juveniles are detected. It is impossible to predict if this species will or will not turn into an environmental problem for the community, but its low density facilitates management at low cost. We also suggest that management of this exotic species follow the precaution principle.

Materials and methods

Study site

The study was conducted in the natural vegetation of Fontes do Ipiranga State Park (PEFI), a protected area located between 23°38'08''S-23°40'18''S 46°36'48''W-46°38'00''W in the city of São Paulo, Brazil, with elevations ranging between 759 and 837 m (Barbosa et al. 2002Barbosa LM, Potomati A, Peccinini AA. 2002. O PEFI: histórico e legislação. In: Bicudo DC, Forti MC, Bicudo CEM. (orgs.) Parque Estadual das Fontes do Ipiranga: unidade de conservação que resiste à urbanização de São Paulo. São Paulo, Secretaria do Meio Ambiente de São Paulo. p. 15-28.; São Paulo 2006São Paulo. 2006. Os elementos naturais e as interferências urbanas. In: Santos RF. (coord.). Estudos sócio-econômico-ecológico e legislativo para caracterização, zoneamento e implantação do Plano de Manejo do Parque Estadual das Fontes do Ipiranga e do seu programa de eco-desenvolvimento: diagnóstico. Campinas, Laboratório de Planejamento Ambiental - LAPLA/Planejamento Engenharia Agrícola - PLANTEC.). Currently, the total area of PEFI is around 490 ha, with the uncertainty being due to conflicting sources of information about the limits of the park. According to Köppen's climatic classification, the region of the park is characterized as temperate climate Cwb, with an annual average temperature of 19.1 °C and an average annual rainfall of 1,540 mm (Santos & Funari 2002Santos P, Funari F. 2002. Clima local. In: Bicudo DC, Forti MC, Bicudo CEM. (orgs.) Parque Estadual das Fontes do Ipiranga: unidade de conservação que resiste à urbanização de São Paulo . São Paulo, Secretaria do Meio Ambiente de São Paulo . p. 27-46.). Over eight decades of climate monitoring conducted by the Institute of Astronomy, Geophysics and Atmospheric Sciences of the University of São Paulo, which has a meteorological station inside PEFI, has recorded considerable climate change. The average annual and minimum temperatures for 2015 were, respectively, 20.4 ˚C and 16.3 ˚C, both the highest recorded since 1933, while the average annual maximum temperature of 26.8 ˚C was the second highest historical record (Camargo 2015Camargo R (coord.). 2015. Boletim Climatológico Anual da Estação Meteorológica do IAG-USP - Seção Técnica do Serviço Meteorológico, Instituto de Astronomia, Geofísica e Ciências Atmosféricas da Universidade de São Paulo 18: 1-76.). Rainfall exhibited a 30 % increase compared to the historical average (Camargo 2015Camargo R (coord.). 2015. Boletim Climatológico Anual da Estação Meteorológica do IAG-USP - Seção Técnica do Serviço Meteorológico, Instituto de Astronomia, Geofísica e Ciências Atmosféricas da Universidade de São Paulo 18: 1-76.). The predominant soil type in PEFI is Red Oxisol with considerable acidity - pH between 3.5 and 4.5 (Fernandes et al. 2002Fernandes AJ, Reis LAM, Carvalho A. 2002. Caracterização do meio físico. In: Bicudo DC, Forti MC, Bicudo CEM. (orgs.) Parque Estadual das Fontes do Ipiranga: unidade de conservação que resiste à urbanização de São Paulo . São Paulo, Secretaria do Meio Ambiente de São Paulo . p. 49-62.); the management plan indicates the presence of argisols and cambisols as well (São Paulo 2006São Paulo. 2006. Os elementos naturais e as interferências urbanas. In: Santos RF. (coord.). Estudos sócio-econômico-ecológico e legislativo para caracterização, zoneamento e implantação do Plano de Manejo do Parque Estadual das Fontes do Ipiranga e do seu programa de eco-desenvolvimento: diagnóstico. Campinas, Laboratório de Planejamento Ambiental - LAPLA/Planejamento Engenharia Agrícola - PLANTEC.). PEFI partially occupies the scarps of the Serra do Mar and the Serra da Mantiqueira, within the Planalto Atlântico (Atlantic Plateau; Almeida 1958 apud São Paulo 2006São Paulo. 2006. Os elementos naturais e as interferências urbanas. In: Santos RF. (coord.). Estudos sócio-econômico-ecológico e legislativo para caracterização, zoneamento e implantação do Plano de Manejo do Parque Estadual das Fontes do Ipiranga e do seu programa de eco-desenvolvimento: diagnóstico. Campinas, Laboratório de Planejamento Ambiental - LAPLA/Planejamento Engenharia Agrícola - PLANTEC.), comprising the Alto Rio Tietê basin and incorporating the headwaters of Riacho do Ipiranga (São Paulo 2006São Paulo. 2006. Os elementos naturais e as interferências urbanas. In: Santos RF. (coord.). Estudos sócio-econômico-ecológico e legislativo para caracterização, zoneamento e implantação do Plano de Manejo do Parque Estadual das Fontes do Ipiranga e do seu programa de eco-desenvolvimento: diagnóstico. Campinas, Laboratório de Planejamento Ambiental - LAPLA/Planejamento Engenharia Agrícola - PLANTEC.). The presence of headwaters in the area was the main justification for the creation of PEFI (São Paulo 2006São Paulo. 2006. Os elementos naturais e as interferências urbanas. In: Santos RF. (coord.). Estudos sócio-econômico-ecológico e legislativo para caracterização, zoneamento e implantação do Plano de Manejo do Parque Estadual das Fontes do Ipiranga e do seu programa de eco-desenvolvimento: diagnóstico. Campinas, Laboratório de Planejamento Ambiental - LAPLA/Planejamento Engenharia Agrícola - PLANTEC.).

PEFI is located in an Atlantic Forest patch, which suffered a reduction of 27 % between 1953 and 1994 due to urbanization both in the surroundings and within the park itself (Pivello & Peccinini 2002Pivello V, Peccinini AA. 2002. A vegetação do PEFI. In: Bicudo DC, Forti MC, Bicudo CEM. (orgs.) Parque Estadual das Fontes do Ipiranga: unidade de conservação que resiste à urbanização de São Paulo . São Paulo, Secretaria do Meio Ambiente de São Paulo . p. 75-92.). It constitutes a vegetation island within an urban matrix, and so is affected by a variety of impacts. Most of the plant species present in PEFI are representatives of rainforest vegetation, with some elements of tropical semideciduous forest (Nastri et al. 1992Nastri V, Catharino ELM, Rossi L, et al. 1992. Estudos fitossociológicos em uma área do Instituto de Botânica de São Paulo utilizados em programas de educação ambiental. Revista do Instituto Florestal 4: 219-225.; Barros et al. 2002Barros F, Mamede MCH, Melo MMRF, et al. 2002. A flora fanerogâmica do PEFI: composição, afinidades e conservação. In: Bicudo DC, Forti MC, Bicudo CEM. (orgs.) Parque Estadual das Fontes do Ipiranga: unidade de conservação que resiste à urbanização de São Paulo . São Paulo, Secretaria do Meio Ambiente de São Paulo . p. 93-110.). PEFI features over 1,500 native species of phanerogams (Barros et al. 2002Barros F, Mamede MCH, Melo MMRF, et al. 2002. A flora fanerogâmica do PEFI: composição, afinidades e conservação. In: Bicudo DC, Forti MC, Bicudo CEM. (orgs.) Parque Estadual das Fontes do Ipiranga: unidade de conservação que resiste à urbanização de São Paulo . São Paulo, Secretaria do Meio Ambiente de São Paulo . p. 93-110.), bryophytes (Visnadi 2015Visnadi SR. 2015. Parque Estadual das Fontes do Ipiranga: unidade de conservação importante para a proteção da brioflora da Mata Atlântica na cidade de São Paulo, Brasil. Boletim Museu Paraense Emílio Goeldi Ciências Naturais 10: 437-469.), and ferns and lycophytes (Hirai et al. 2016Hirai RY, Gissi DS, Prado J. 2016. Criptógamos do Parque Estadual das Fontes do Ipiranga, São Paulo, SP, Brasil. Pteridophyta: 22. Thelypteridaceae e lista atualizada dos táxons. Hoehnea 43: 39-56.).

Field procedures

Considering that more than ten studies have sampled the vegetation of PEFI over the last 30 years, and that all of them indicated exotic species, their previous records were compiled to form a guide list (Tab. 1) for our sampling. Any additional exotic species found during our field procedures and taxonomic identifications were added to the list. We sampled the natural vegetation from September 2015 to October 2016 in 90 10 m x 10 m (100 m²) plots for a total sampled area of 9,000 m². The plots were equally distributed among three different native forest areas (i.e., 3,000 m² in each area) (Fig. 2). Historical land-use mapping from 1953 to 1994 (Peccinini & Pivello 2002Peccinini AA, Pivello V. 2002. Histórico do uso das terras e condição da vegetação no PEFI. In: Bicudo DC, Forti MC, Bicudo CEM. (orgs.) Parque Estadual das Fontes do Ipiranga: unidade de conservação que resiste à urbanização de São Paulo . São Paulo, Secretaria do Meio Ambiente de São Paulo . p. 253-258.), revealed that the vegetation patch that contains Area 1 remained categorized as "heterogeneous canopy forest", with only the height of vegetation changing over time. Area 1 has not suffered any direct disturbance such as fire, logging, or understory clear-cutting from 1994 to the present. Consequently, Area 1 has been without severe anthropic disturbances for at least 64 years, although it is just 150 m from the park perimeter (east boundary with Cursino Avenue). This low level of perturbation has been corroborated by recent studies on nutrient cycling (Moraes 2002Moraes RM. 2002. Ciclagem de nutrientes na floresta do PEFI: Produção e decomposição da serapilheira. In: Bicudo DC, Forti MC, Bicudo CEM. (orgs.) Parque Estadual das Fontes do Ipiranga: unidade de conservação que resiste à urbanização de São Paulo . São Paulo, Secretaria do Meio Ambiente de São Paulo . p. 133-142.; Santos 2014Santos AR. 2014. Produção, estoque e nutrientes da serapilheira em Floresta Ombrófila Densa do Parque Estadual das Fontes do Ipiranga, São Paulo, Brasil. MSc Thesis, Instituto de Botânica, São Paulo.; Bazi & Gomes 2015Bazi CA, Gomes EPC. 2015. Produção de serapilheira no Parque Estadual das Fontes do Ipiranga - PEFI (2014-2015). In: 22 Reunião Anual do Instituto de Botânica, São Paulo. Secretaria do Meio Ambiente de São Paulo . p. 17.; 2016Bazi CA, Gomes EPC. 2016. Produção de serapilheira no Parque Estadual das Fontes do Ipiranga - PEFI - (2015-2016). In: 23 Reunião Anual do Instituto de Botânica, São Paulo. Secretaria do Meio Ambiente de São Paulo. p. 125.; Vieira 2015Vieira MO. 2015. Decomposição da serapilheira em dois trechos de Floresta Atlântica no Parque Estadual das Fontes do Ipiranga, São Paulo, um deles sob influência do bambu Aulonemia aristulata (Döll) -MacClure. MSc Thesis, Instituto de Botânica, São Paulo.) and plant community dynamics (Davison 2006Davison CP. 2006. Estrutura e composição da vegetação de sub-bosque em dois trechos de floresta do Parque Estadual das Fontes do Ipiranga, São Paulo-SP. Monograph, Universidade Presbiteriana Mackenzie, São Paulo.; 2009Davison CP. 2009. Estrutura de clareiras e a presença de bambus em um fragmento de Floresta Atlântica, SP, Brasil. MSc Thesis, Instituto de Botânica, São Paulo.; Carvalho et al. 2011Carvalho PG, Mellis J, Ascenção BM, Cestari FM, Alves LF, Grombone-Guaratini MT. 2011. Abundância e biomassa de lianas em um fragmento de floresta Atlântica. Hoehnea 38: 307-314.; Kondrat 2014Kondrat H. 2014. Dinâmica da Comunidade Vegetal de Remanescente de Mata Atlântica na Região Metropolitana de São Paulo. MSc Thesis, Instituto de Botânica, São Paulo.).

Table 1
Exotic plant species with specific previous records of occurrence in Fontes do Ipiranga State Park, São Paulo, SP. The compilation served as a guide list for field searches during sampling.

Figure 2
Map of the studied protected area. Location of distributed plots in the three sampled areas (Area 1 = lowest disturbance level, Area 2 = intermediate disturbance level, Area 3 = highest disturbance level) of natural vegetation inside Fontes do Ipiranga State Park, São Paulo-SP. JBSP = Botanical Garden of São Paulo.

The road Alameda Von Martius, which belongs to the Botanical Garden (JBSP), an administrative unit inside PEFI, borders Area 2. The area is considered to have intermediate disturbance, with its floral composition and plant structure being consistent with that of disturbed environments (when studied from the edge to the forest inner by Tanus et al. 2012Tanus MR, Pastore M, Bianchini RS, Gomes EPC. 2012. Estrutura e composição de um trecho de Mata Atlântica no Parque Estadual das Fontes do Ipiranga, São Paulo, SP, Brasil. Hoehnea 39: 157-168.). Finally, Area 3 has a higher level of disturbance than the other two areas. It is located in the forest of JBSP, and is adjacent to Terra Batida Trail, which is used daily by visitors and for environmental education. The floristic patterns of Area 3 were partially investigated by Hirata et al. (2010Hirata J, Melo MMRF, Eisenlohr P. 2010. Padrões florísticos do componente arbóreo sob interferência de trilhas em um trecho de Floresta Ombrófila Densa de Transição em São Paulo, SP, Brasil. Hoehnea 37: 555-570.), who indicated that the use this trail for public purposes influences plant species establishment. Therefore, these three areas represent the entire disturbance gradient of the natural area of PEFI.

Sampling of exotic individuals comprised two size classes reflecting occurrence in the understory or the canopy layer. In the understory, all individuals with height > 1 m, and diameter at breast height (dbh) < 4.8 cm were counted but only the exotic species were identified, making it possible to calculate the percentage of exotics in the regenerating layer of each plot. For the canopy layer (dbh > 4.8 cm), all individuals (except climbers, and epiphytes) were sampled. For all species (native or exotic) in canopy layer dbh was measured and plant material collected for species identification. All the botanical material collected was identified to the species level, whenever possible, with support from Núcleo de Pesquisas e Curadoria do Herbário SP of the Instituto de Botanica. We incorporated one-dried voucher of each species into the collection of SP Herbarium. The coverage of each exotic species was estimated by calculating the canopy area of each individual by approximating it into an ellipse shape, i.e. the product of the semi-major axis and the semi-minor axis of canopy, multiplied by pi.

Data analysis

Differences in species richness among sampling units (Areas 1, 2 and 3) were compared using individual rarefaction (1,000 permutations), with the respective 95 % confidence interval, to control for differences in sampling individual's effort (Krebs 1989Krebs CJ. 1989. Ecological methodology. New York, Harper & Row.). We evaluated diversity among the three areas using the diversity profile, which allows simultaneous analysis of species richness and relative abundance of each species (Tothmeresz 1995Tothmeresz, B. 1995. Comparison of different methods for diversity ordering. Journal of Vegetation Science 6:283-290.).

For the canopy layer, the usual quantitative descriptors (absolute and relative abundances, relative frequency and dominance, and importance and cover values) of vegetation structure were performed, including the entire community, using Fitopac 2.1.2.85 (Shepherd 2010Shepherd G. 2010. Fitopac 2.1. 2.85. Manual do usuário. Departamento de Biologia Vegetal, Universidade Estadual de Campinas, Campinas.). The definition considered for a rare species was that of Martins (1991Martins FR. 1991. Estrutura de uma floresta mesófila. Campinas, Universidade Estadual de Campinas.), who defined a rare species as having a unique individual in the sample. For the understory, we calculated the proportion of exotic individuals relative to native plants. In order to test for significant differences in the densities of exotic species among the three areas, the non-parametric Kruskal-Wallis test was used, and when there was a significant difference (p < 0.05) the Mann-Whitney pairwise (non-parametric) post-hoc test was applied. With the purpose of identifying significant differences in the density of each exotic species between the canopy layer and the understory in all areas surveyed, the Mann-Whitney pairwise (non-parametric) test was applied. The usual tests for normality (Shapiro-Wilk) and homogeneity of variance (Levene) were performed a priori, but even with transforming the data it was not possible to use parametric tests. We performed all analyses in R (R Core Team 2016R Core Team. 2016. R: A language and environment for statistical computing. Vienna, R Foundation for Statistical Computing. https://www.r-project.org/. 31 Dec. 2016.
https://www.r-project.org/...
), mainly using the packages “iNEXT”, “entropart”, “car” and “ggplot2”. The script is available in Text S1 in supplementary material.

The definition of invasion status for the exotic species followed the key proposed by Durigan et al. (2013Durigan G, Ivanauskas NM, Zakia MJB, Abreu RCR. 2013. Control of invasive plants: ecological and socioeconomic criteria for the decision making process. Brazilian Journal of Nature Conservation 11:23-30.). However, in order to avoid conflicts in the classification of management priorities between the proposed population ecology conceptual framework (Fig. 1), and the invasion status from the criteria defined by Durigan et al. (2013Durigan G, Ivanauskas NM, Zakia MJB, Abreu RCR. 2013. Control of invasive plants: ecological and socioeconomic criteria for the decision making process. Brazilian Journal of Nature Conservation 11:23-30.), we performed a regression analysis to investigate the effect of exotic individuals’ density on exotic coverage. We expected that species with both higher density and coverage would be indicated as a priority for management, especially in cases when an exotic species was present both in the canopy layer and in the understory but was classified as non-dominant ruderal, which is typical of early invasion. The geographical regions of origin of the alien species were determined using the national database of invasive alien species I3N Brazil (Instituto Hórus 2017Instituto Hórus. 2017. Base de dados nacional de espécies exóticas invasoras I3N Brasil. Florianópolis, Instituto Hórus. http://i3n.institutohorus.org.br/www. 05 Jan. 2017.
http://i3n.institutohorus.org.br/www...
).

Results

With the number of individuals fixed, the rarefaction curves for the presence of exotic species in the community (Fig. 3A) showed no differences in species richness among the areas due to overlapping confidence intervals. However, Area 2 (intermediate level of disturbance) had higher richness with a sampling effort of 400 specimens, indicating a point at which sampling effort could reveal significant differences in observed richness from the other areas. In the diversity profile (Fig. 3B), the omission of the evenness component showed that Area 2 was always richer. The presence of alien species afforded a higher richness to Area 3 (higher level of disturbance) when compared to Area 1 (lowest level of disturbance) (alpha = 0). When evenness is included, that is by including the relative abundance of species by using indexes equivalent to Shannon’s (alpha = 1) and Simpson’s (alpha = 2) indexes, the diversity profile curves intersect and Area 1 has the greatest diversity.

Figure 3
Analysis comparing the three sampled areas (Area 1 = lowest disturbance level, Area 2 = intermediate disturbance level, Area 3 = highest disturbance level) considering the entire community (i.e., native and exotic species). A. Individual rarefaction curves with 1,000 simulations. B. Diversity profiles comparing the sampled areas.

In terms of the complete community (native and exotic species) in the canopy layer, Area 1 had 476 individuals of 103 species from 39 families (Tab. S2 in supplementary material); Area 2 had 587 individuals of 130 species from 41 families (Tab. S3 in supplementary material); and Area 3 had 521 individuals of 105 species from 40 families (Tab. S4 in supplementary material). There were no significant differences in basal area (One-way ANOVA, F = 0.08213, p > 0.05), and density of canopy individuals (One-way ANOVA, F = 2.48, p > 0.05) among sites. Considering all areas together as a unit, Myrtaceae was the family with the greatest number of individuals (194) and species (35) and, together with Lauraceae, Rubiaceae, Fabaceae, Melastomataceae, and Euphorbiaceae, comprised 50.4 % of all species identified. A total of 32.2 % of all the species were considered rare. None of the exotic species were among the plants with the highest importance values (IV).

A total of 10 exotic species were sampled, and the density of exotic individuals per hectare in the understory was four times higher than that of the canopy layer (Tab. 2). The loquat (Eriobotrya japonica) and Pinus sp. were exclusively found in the canopy layer. In contrast, Dracaena fragrans and Livistona chinensis were found only in the understory. Three of the exotic species found were not on the guide list (Tab.1), and thus recorded in PEFI for the first time: Caryota urens, Persea americana and Syzygium jambos. The rose apple (S. jambos) was the species with the greatest density of individuals per hectare, with 94.6 % of them being in the understory. Area 1 had a lower density of exotic individuals per hectare (43.4 indiv. ha-1) (Kruskal-Wallis H = 9.447 p <0.05) than Area 2 and Area 3 (Tab. 2); only the exotic species Coffea arabica and L. chinensis occurred in Area 1, where they were exclusive to the understory. These species were also found in Area 2 and Area 3. Area 3 had the highest richness of exotic species (seven species). The rose apple (S. jambos) was present exclusively in disturbed areas in both Area 2 and Area 3, but with greater abundance in the former. Comparing the densities of each exotic species distributed in both strata, there was a significant difference in densities between the canopy layer and the understory for C. arabica (Mann-Whitney U = 3528.5 p < 0.05), L. chinensis (Mann-Whitney U = 3580.5 p < 0.05), and S. jambos (Mann-Whitney U = 3516 p < 0.05).

Table 2
Density (individuals.hectare-1) of exotic species in the canopy (dbh > 4.8 cm) layer and understory (height > 1 m and dbh < 4.8 cm) for each area (Area 1 = lowest disturbance level, Area 2 = intermediate disturbance level, Area 3 = highest disturbance level) in Fontes do Ipiranga State Park, São Paulo, SP. Invasion status (Durigan et al., 2013Durigan G, Ivanauskas NM, Zakia MJB, Abreu RCR. 2013. Control of invasive plants: ecological and socioeconomic criteria for the decision making process. Brazilian Journal of Nature Conservation 11:23-30.): casual alien species (CaAl), non-dominant ruderal (NDoRu), non-dominant invader (NDoIn), dominant invader (DoIn). Origin of exotic species: I3N Brazil database of invasive alien species. Mann-Whitney pairwise (non-parametric) test.

Considering the invasion status of the exotic species, E. japonica and Pinus sp. were categorized as casual alien species since they were not leaving persistent descendants. Archontophoenix cunninghamiana, C. urens, D. fragans, P. americana, Pittosporum undulatum, and S. jambos were classified as non-dominant ruderal species since they were only present in one or both of the areas (Area 2 and Area 3) considered to have some level of disturbance and do not dominate the community there. The species C. arabica was classified as a non-dominant invader since it is present in Area 1, but has no detectable direct effect on the native community. The species L. chinensis was classified as a dominant invader, and also occurred in the least disturbed area (Area 1), as did C. arabica. In addition, less regeneration of native species was diagnosed under de L. chinensis individuals, possibly due to shading in Area 3. Applying the conceptual framework proposed in Fig. 1, the management indications for these species would be: E. japonica, and Pinus sp. as low priority and L. chinensis as high priority. The other species considered as low (the remaining) or intermediate (C. arabica) priority by their invasion status, we would consider as high priority for management following the conceptual framework proposed in Fig. 1. Even though the adjusted linear regression had a low coefficient (R² = 0.18), two distinct groups could be highlighted: A. cunninghamiana, and L. chinensis (the latter as expected) with higher coverage values, and C. arabica, and S. jambos with higher values for density:coverage ratio (Fig. 4).

Figure 4
Visual representation of the ratio between coverage and density of exotic species. Estimated exotic species coverage as a function of individuals per unit area revealing important species in need of priority management among others diagnosed as non-dominant ruderal (Archontophoenix cunninghamiana and Syzygium jambos).

The geographic origins of the studied exotic species included Asia, with four species, followed by the Australia and Africa, with two species each, and then Central and North America, with one species each.

Discussion

The most frequent geographic regions for the origin of the exotic species encountered in the present study are compatible with the literature. Asia can be considered the main source region for exotic tree species in the world, followed by Australia. Africa and North and Central America are also characterized as important sources of non-native species (Rejmánek 2014Rejmánek M. 2014. Invasive trees and shrubs: where do they come from and what we should expect in the future? Biological Invasions 16: 483-498.). North America and Europe are the continents that provide more species of Pinaceae (Rejmánek 2014Rejmánek M. 2014. Invasive trees and shrubs: where do they come from and what we should expect in the future? Biological Invasions 16: 483-498.), which includes the genus Pinus. A global review of invasive trees and shrubs found that the genus Pinus is invasive in 11 of the different geographic regions defined by Richardson & Rejmánek (2011Richardson DM, Rejmánek M. 2011. Trees and shrubs as invasive alien species - a global review. Diversity and Distributions 17: 788-809.), among which South America is included. The Asian continent, the source region for C. urens and L. chinensis, is the greatest source of Arecaceae in the present study (Rejmánek 2014Rejmánek M. 2014. Invasive trees and shrubs: where do they come from and what we should expect in the future? Biological Invasions 16: 483-498.). Among the most widespread invasive alien plant species in the world, P. undulatum and S. jambos are in at least six of the geographic regions studied by Richardson & Rejmánek (2011Richardson DM, Rejmánek M. 2011. Trees and shrubs as invasive alien species - a global review. Diversity and Distributions 17: 788-809.), and both have invaded South America.

The sweet pittosporum, P. undulatum, is an Australian species, where it occurs along the coastline and in mainland mountains (Souza et al. 2016Souza SCPMD, Silva AG, Franco GADC, Ivanauskas NM. 2016. A vegetação secundária em um fragmento florestal urbano: influência de exóticas invasoras na comunidade vegetal. Revista do Instituto Florestal 28: 7-35.). The species is considered invasive worldwide. In Brazil, the species is invasive in forests of the state of Paraná (Blum et al. 2005Blum CT, Posonski M, Hoffmann PM, Borgo M. 2005. Espécies vegetais invasoras em comunidades florestais nativas nas margens da Represa do Vossoroca, APA de Guaratuba, Paraná, Brasil. Brasília, Sociedade Chauá.; Mielke et al. 2015Mielke EC, Negrelle RRB, Cuquel FL, Lima WP. 2015. Espécies exóticas invasoras arbóreas no Parque da Barreirinha em Curitiba: registro e implicações. Ciência Florestal 25: 327-336.), while in São Paulo it is considered as subspontaneous (Garcia & Pirani 2001Garcia RJF, Pirani JR. 2001. Estudo florístico dos componentes arbóreo e arbustivo da mata do Parque Santo Dias, São Paulo, SP, Brasil. Boletim de Botânica da Universidade de São Paulo 19: 15-42.), as exotic (Almeida et al. 2010Almeida RS, Cielo-Filho R, Souza SCPM, et al. 2010. Campo sujo úmido: fisionomia de Cerrado ameaçada pela contaminação de Pinus elliottii Engelm. na Estação Ecológica de Itapeva, Estado de São Paulo. Revista do Instituto Florestal 22: 71-91.), as with invasive potential (Nascimento et al. 2011aNascimento FDS, Aragaki S, Silva FHD. 2011a. Ameaça ao Patrimônio florestal do "Parque Municipal Alfredo Volpi" (São Paulo, SP): avaliação rápida de três espécies exóticas e invasoras. In: I Congresso de Áreas Verdes: Florestas Urbanas. São Paulo, Secretaria Municipal do Verde e do Meio Ambiente e Universidade Aberta do Meio Ambiente e Cultura de Paz. p. 167-169.), and as a dominant invader (Souza et al. 2016Souza SCPMD, Silva AG, Franco GADC, Ivanauskas NM. 2016. A vegetação secundária em um fragmento florestal urbano: influência de exóticas invasoras na comunidade vegetal. Revista do Instituto Florestal 28: 7-35.), with documented dispersion by frugivorous birds (Campagnoli et al. 2016Campagnoli ML, Santos SRG, Silva SDSR, Antunes AZ. 2016. O papel das aves na dispersão e germinação de sementes do pau-incenso (Pittosporum undulatum Vent.) em um remanescente de Mata Atlântica. Revista do Instituto Florestal 28: 59-67.). This species was categorized as a non-dominant ruderal species in our study, however, according to the literature, it is considered invasive in several places. In PEFI, large numbers of individuals of the species are known to occur in other non-sampled vegetation areas (e.g., in the vegetation north of the JBSP visitation area), making population monitoring extremely important.

The rose apple, S. jambos, is considered a dominant invader of 27 of 30 groups of oceanic islands studied by Kueffer et al. (2010Kueffer C, Daehler CC, Torres-Santana CW, et al. 2010. A global comparison of plant invasions on oceanic islands. Perspectives in Plant Ecology Evolution and Systematics 12: 145-161.), appearing on massifs. These include, for example, the Galapagos Archipelago (Watson et al. 2010Watson J, Trueman M, Tufet M, Henderson S, Atkinson R. 2010. Mapping terrestrial anthropogenic degradation on the inhabited islands of the Galapagos Archipelago. Oryx 44: 79-82.) and the Pitcarin Islands, British Territory in Polynesia, where it was introduced two centuries ago and has already replaced altitudinal and lowland forests (Kingston & Waldren 2003Kingston N, Waldren S. 2003. The plant communities and environmental gradients of Pitcairn Island: The significance of invasive species and the need for conservation management. Annals of Botany 92: 31-40.). In Brazil, S. jambos was found to have a high importance value both in the understory (Santiago et al. 2014Santiago DS, Fonseca C, Carvalho FA. 2014. Fitossociologia da regeneração natural de um fragmento urbano de Floresta Estacional Semidecidual (Juiz de Fora, MG). Revista Brasileira de Ciências Agrárias 9: 117-123.) and in the canopy layer of an urban forest in the state of Minas Gerais (Fonseca & Carvalho 2012Fonseca CR, Carvalho FA. 2012. Floristic and phytosociological aspects of the tree community in an urban atlantic forest fragment (Juiz de Fora, state of Minas Gerais, Brazil). Bioscience Journal 28: 820-832.). In São Paulo the species is considered as an exotic (Almeida et al. 2010Almeida RS, Cielo-Filho R, Souza SCPM, et al. 2010. Campo sujo úmido: fisionomia de Cerrado ameaçada pela contaminação de Pinus elliottii Engelm. na Estação Ecológica de Itapeva, Estado de São Paulo. Revista do Instituto Florestal 22: 71-91.), and as a non-dominant invader in Alberto Löfgren State Park (Souza et al. 2016Souza SCPMD, Silva AG, Franco GADC, Ivanauskas NM. 2016. A vegetação secundária em um fragmento florestal urbano: influência de exóticas invasoras na comunidade vegetal. Revista do Instituto Florestal 28: 7-35.). Its characteristics confirm the recent invasive diagnosis, as this species was the most abundant exotic found in PEFI, and so we consider it a priority for management.

Also in Brazil, the invasion and dominance by the Australian palm, Archontophoenix cunninghamiana are well documented in the forest of Cidade Universitária "Armando Salles de Oliveira" - CUASO - (Dislich et al. 2002Dislich R, Kisser N, Pivello VR. 2002. The invasion of a forest fragment in São Paulo (SP) by the Australian palm Archontophoenix cunninghamiana H. Wendl. & Drude. Brazilian Journal of Botany 25: 55-64.; Christianini 2006Christianini AV. 2006. Fecundidade, dispersão e predação de sementes de Archontophoenix cunninghamiana H. Wendl. & Drude, uma palmeira invasora da Mata Atlântica. Brazilian Journal of Botany 29: 587-594.; Mengardo et al. 2012Mengardo ALT, Figueiredo CL, Tambosi LR, Pivello VR. 2012. Comparing the establishment of an invasive and an endemic palm species in the Atlantic rainforest. Plant Ecology & Diversity 5: 345-354.; Mengardo & Pivello 2014Mengardo ALT, Pivello VR. 2014. The effects of an exotic palm on a native palm during the first demographic stages: contributions to ecological management. Acta Botanica Brasilica 28: 552-558.), and has been recorded by other population studies (Nascimento et al. 2011bNascimento FDS, Aragaki S, Silva FHD. 2011b. Avaliação populacional de Archontophoenix cunninghamiana H. Wendl. & Drud no “P.M. Alfredo Volpi” (São Paulo, SP). In: 18 Reunião Anual do Instituto de Botânica. São Paulo, Secretaria do Meio Ambiente de São Paulo . p. 1-4.; Garcia & Pirani 2001Garcia RJF, Pirani JR. 2001. Estudo florístico dos componentes arbóreo e arbustivo da mata do Parque Santo Dias, São Paulo, SP, Brasil. Boletim de Botânica da Universidade de São Paulo 19: 15-42.; Souza et al. 2016Souza SCPMD, Silva AG, Franco GADC, Ivanauskas NM. 2016. A vegetação secundária em um fragmento florestal urbano: influência de exóticas invasoras na comunidade vegetal. Revista do Instituto Florestal 28: 7-35.). Another palm tree identified in the present study, Caryota urens, was classified as invasive in Manipur, India (Singh et al. 2015Singh TB, Das AK, Singh P. 2015. Study of alien and invasive flora of Valley District of Manipur and their control. International Journal for Innovative Research in Science & Technology 1: 616-626.). Finally, the Chinese fan palm (L. chinensis) is considered to be one of the most documented invasive palms (Meyer et al. 2008Meyer JY, Lavergne C, Hodel DR. 2008. Time bombs in gardens: invasive ornamental palms in tropical islands, with emphasis on French Polynesia (Pacific Ocean) and the Mascarenes (Indian Ocean). Palms, Lawrence 52: 71-83.). Of the three invasive palm trees found in PEFI, L. chinensis was the most abundant in the understory and exhibited invasive attributes, while A. cunninghamiana had a high density:coverage ratio.

The coffee, Coffea arabica, can be considered invasive in the Pacific Islands (Meyer 2000Meyer JY. 2000. Preliminary review of the invasive plants in the Pacific islands (SPREP Member Countries). In: Sherley G. (ed.) Invasive species in the Pacific: A technical review and draft regional strategy. Apia, Samoa. p. 85-115.) and Hawaii (Mascaro et al. 2008Mascaro J, Becklund KK, Hughes RF, Schnitzer SA. 2008. Limited native plant regeneration in novel, exotic-dominated forests on Hawai’i. Forest Ecology and Management 256: 593-606.), and an exotic ornamental without indications of naturalization in South Africa (Foxcroft et al. 2008Foxcroft LC, Richardson DM, Wilson JRU. 2008. Ornamental plants as invasive aliens: problems and solutions in Kruger National Park, South Africa. Environmental Management 41: 32-51.). In Brazil, this species was found to occur in low density in the regenerating layer of a tropical semideciduous forest in Juiz de Fora, Minas Gerais (Santiago et al. 2014Santiago DS, Fonseca C, Carvalho FA. 2014. Fitossociologia da regeneração natural de um fragmento urbano de Floresta Estacional Semidecidual (Juiz de Fora, MG). Revista Brasileira de Ciências Agrárias 9: 117-123.), and in São Paulo, where it has been characterized as having invasive potential (Nascimento et al. 2011aNascimento FDS, Aragaki S, Silva FHD. 2011a. Ameaça ao Patrimônio florestal do "Parque Municipal Alfredo Volpi" (São Paulo, SP): avaliação rápida de três espécies exóticas e invasoras. In: I Congresso de Áreas Verdes: Florestas Urbanas. São Paulo, Secretaria Municipal do Verde e do Meio Ambiente e Universidade Aberta do Meio Ambiente e Cultura de Paz. p. 167-169.) and as the dominant invader (Souza et al. 2016Souza SCPMD, Silva AG, Franco GADC, Ivanauskas NM. 2016. A vegetação secundária em um fragmento florestal urbano: influência de exóticas invasoras na comunidade vegetal. Revista do Instituto Florestal 28: 7-35.). The species has also been recorded in the state of Rio de Janeiro, the location for the introduction of coffee to the country in the middle of the 18th century (Silva 2006Silva AFCD. 2006. Ciência nos cafezais: a campanha contra a broca do café em São Paulo (1924-1929). MSc Thesis, Fundação Oswaldo Cruz, Rio de Janeiro.). Coffee cultivation spread by planting in farms and backyards in São Paulo (Silva 2006Silva AFCD. 2006. Ciência nos cafezais: a campanha contra a broca do café em São Paulo (1924-1929). MSc Thesis, Fundação Oswaldo Cruz, Rio de Janeiro.), and often remains present in the most remote regions of small urban centers. This information was confirmed by Article 3rd, Law No. 2020 (Brasil 1924 apud Silva 2006Silva AFCD. 2006. Ciência nos cafezais: a campanha contra a broca do café em São Paulo (1924-1929). MSc Thesis, Fundação Oswaldo Cruz, Rio de Janeiro.), enacted with the aim of rapidly diagnosing it as a major pest coffee, and emphasizing the presence of isolated or monoculture plantations in farms, ranches, sites, gardens or orchards (Silva 2006Silva AFCD. 2006. Ciência nos cafezais: a campanha contra a broca do café em São Paulo (1924-1929). MSc Thesis, Fundação Oswaldo Cruz, Rio de Janeiro.). Thus, we believe that C. arabica was present in PEFI before the park was even created, given the history of its foundation from the expropriation of land. Thus, this species is not considered an immediate issue for the natural vegetation of PEFI.

The dispersion and presence of avocado, P. americana, can be associated with anthropogenic activities (Souza et al. 2016Souza SCPMD, Silva AG, Franco GADC, Ivanauskas NM. 2016. A vegetação secundária em um fragmento florestal urbano: influência de exóticas invasoras na comunidade vegetal. Revista do Instituto Florestal 28: 7-35.) and structures (Alston & Richardson 2006Alston KP, Richardson DM. 2006. The roles of habitat features, disturbance, and distance from putative source populations in structuring alien plant invasions at the urban/wildland interface on the Cape Peninsula, South Africa. Biological Conservation 132: 183-198. ). This species was considered invasive in Hawaii (Mascaro et al. 2008Mascaro J, Becklund KK, Hughes RF, Schnitzer SA. 2008. Limited native plant regeneration in novel, exotic-dominated forests on Hawai’i. Forest Ecology and Management 256: 593-606.) and possibly naturalized in South Africa (Alston & Richardson 2006Alston KP, Richardson DM. 2006. The roles of habitat features, disturbance, and distance from putative source populations in structuring alien plant invasions at the urban/wildland interface on the Cape Peninsula, South Africa. Biological Conservation 132: 183-198. ; Foxcroft et al. 2008Foxcroft LC, Richardson DM, Wilson JRU. 2008. Ornamental plants as invasive aliens: problems and solutions in Kruger National Park, South Africa. Environmental Management 41: 32-51.). In São Paulo, P. americana is known to occur in a number of different parks (Garcia & Pirani 2001Garcia RJF, Pirani JR. 2001. Estudo florístico dos componentes arbóreo e arbustivo da mata do Parque Santo Dias, São Paulo, SP, Brasil. Boletim de Botânica da Universidade de São Paulo 19: 15-42.; Almeida et al. 2010Almeida RS, Cielo-Filho R, Souza SCPM, et al. 2010. Campo sujo úmido: fisionomia de Cerrado ameaçada pela contaminação de Pinus elliottii Engelm. na Estação Ecológica de Itapeva, Estado de São Paulo. Revista do Instituto Florestal 22: 71-91.; Souza et al. 2016Souza SCPMD, Silva AG, Franco GADC, Ivanauskas NM. 2016. A vegetação secundária em um fragmento florestal urbano: influência de exóticas invasoras na comunidade vegetal. Revista do Instituto Florestal 28: 7-35.). Similarly, the dispersion of E. japonica is human mediated (Souza et al. 2016Souza SCPMD, Silva AG, Franco GADC, Ivanauskas NM. 2016. A vegetação secundária em um fragmento florestal urbano: influência de exóticas invasoras na comunidade vegetal. Revista do Instituto Florestal 28: 7-35.), and in South Africa it is considered the invasive species most frequently used for medical purposes (Maema et al. 2016Maema LP, Potgieter M, Mahlo SM. 2016. Invasive alien plant species used for the treatment of various diseases in Limpopo province, South Africa. African Journal of Traditional Complementary and Alternative Medicines 13: 223-231.). In Brazil, this species has been recorded as invasive in Paraná (Blum et al. 2005Blum CT, Posonski M, Hoffmann PM, Borgo M. 2005. Espécies vegetais invasoras em comunidades florestais nativas nas margens da Represa do Vossoroca, APA de Guaratuba, Paraná, Brasil. Brasília, Sociedade Chauá.), while in São Paulo it has already been sampled among natural vegetation (Garcia & Pirani 2001Garcia RJF, Pirani JR. 2001. Estudo florístico dos componentes arbóreo e arbustivo da mata do Parque Santo Dias, São Paulo, SP, Brasil. Boletim de Botânica da Universidade de São Paulo 19: 15-42.; Catharino et al. 2006Catharino ELM, Bernacci LC, Franco GADC, Durigan G, Metzger JP. 2006. Aspectos da composição e diversidade do componente arbóreo das florestas da Reserva Florestal do Morro Grande, Cotia, SP. Biota Neotropica 6: 1-28.; Almeida et al. 2010Almeida RS, Cielo-Filho R, Souza SCPM, et al. 2010. Campo sujo úmido: fisionomia de Cerrado ameaçada pela contaminação de Pinus elliottii Engelm. na Estação Ecológica de Itapeva, Estado de São Paulo. Revista do Instituto Florestal 22: 71-91.; Souza et al. 2016Souza SCPMD, Silva AG, Franco GADC, Ivanauskas NM. 2016. A vegetação secundária em um fragmento florestal urbano: influência de exóticas invasoras na comunidade vegetal. Revista do Instituto Florestal 28: 7-35.). Considering that PEFI is a protected area and among the categories of greater restriction, the administrative management of the park through preventive actions connected to public use indirectly controls human-associated dispersion of these species. This situation corroborates the low management priority for both P. americana and E. japonica.

The corn plant, Dracaena fragrans, is considered invasive in Costa Rica (Morales 2015Morales CO. 2015. Floristic and structural characterization of three secondary forest fragments in Costa Rica. Revista de Biología Tropical 57: 69-82.) and occurs along trails in Mount Halimun-Salak National Park in Indonesia (Kudo et al. 2014Kudo Y, Mutaqien Z, Simbolon H, Suzuki E. 2014. Spread of invasive plants along trails in two national parks in West Java, Indonesia. Tropics 23: 99-110.). In Brazil, the only invasion record found for the species is in Tijuca National Park, Rio de Janeiro, where it was diagnosed as a competitive and aggressive invader (Ribeiro 2006Ribeiro MDO. 2006. Levantamento populacional e manejo da espécie exótica invasora Dracaena fragrans Ker-Gawl (Angiospermae-Liliaceae), em um trecho de Floresta Atlântica sob efeitos de borda no Parque Nacional da Tijuca, Rio de Janeiro, Brasil. Monograph, Universidade Federal Rural do Rio de Janeiro, Rio de Janeiro.). Considering the punctual nature of the invasion records for this species throughout the world and in Brazil, non-dominant ruderal invasion status with low priority of management seems consistent with PEFI’s reality.

A single individual of the genus Pinus was found in the present work, however, this genus is commonly found in protected areas in South and Southeast Brazil. In those places, its invasion is generally enhanced by the presence of adjacent reforestation plots or typically open native vegetation areas such as Itapeva Ecological Station (Almeida et al. 2010Almeida RS, Cielo-Filho R, Souza SCPM, et al. 2010. Campo sujo úmido: fisionomia de Cerrado ameaçada pela contaminação de Pinus elliottii Engelm. na Estação Ecológica de Itapeva, Estado de São Paulo. Revista do Instituto Florestal 22: 71-91.), Angatuba Ecological Station (Monteiro et al. 2009Monteiro C, Prado B, Dias A. 2009. Plano de Manejo da Estação Ecológica de Angatuba. Instituto Florestal. São Paulo, Secretaria do Meio Ambiente.), and Itirapina Ecological Station (Zanchetta & Diniz 2006Zanchetta D, Diniz FV. 2006. Estudo da contaminação biológica por Pinus spp. em três diferentes áreas na Estação Ecológica de Itirapina (SP, Brasil). Revista do Instituto Florestal 18: 1-14.). Likewise, the probable propagule source of this genus in PEFI is an arboretum adjacent to Area 2. Since no juvenile plants were found in the understory, even though the adult tree sampled inside the forest was reproductive, low priority in management with periodic monitoring should be a sufficiently careful strategy for PEFI. It should be noted that the literature search for evidence of occurrence and/or invasion throughout the world and in Brazil has not been exhaustively discussed here and that the records presented are simply exemplary.

The exotic species diagnosed in PEFI vegetation did not have high important values (IVs) in any of studied areas. Consequently, the exotic species are not a dominant component of the community structure. In contrast, in a secondary succession semideciduos forest, Moreira & Carvalho (2013Moreira B, Carvalho FA. 2013. A comunidade arbórea de um fragmento urbano de Floresta Atlântica após 40 anos de sucessão secundária (Juiz de Fora, Minas Gerais). Biotemas 26: 59-70.) diagnosed Pinus elliottii Engelm. as being among the five species with highest IVs, where its presence is due to propagule pressure, and S. jambos as opportunistic in places with anthropic disturbance. Both of these species were identified in our study (for Pinaceae taxonomic identification stopped at the level of genus). In a study at Alberto Löfgren State Park, a protected area in São Paulo that began as a botanical garden, all the exotic species found, with the exception of C. urens, were also found in PEFI (Souza et al. 2016Souza SCPMD, Silva AG, Franco GADC, Ivanauskas NM. 2016. A vegetação secundária em um fragmento florestal urbano: influência de exóticas invasoras na comunidade vegetal. Revista do Instituto Florestal 28: 7-35.). About 29 % of the richness found at Alberto Löfgren State Park was exotic, and of these P. undulatum, the genus Pinus and the Australian palm Archontophoenix spp. were among the 12 plants with the highest IVs (Souza et al. 2016Souza SCPMD, Silva AG, Franco GADC, Ivanauskas NM. 2016. A vegetação secundária em um fragmento florestal urbano: influência de exóticas invasoras na comunidade vegetal. Revista do Instituto Florestal 28: 7-35.). When combined with previous studies of vegetation structure in PEFI, A. cunninghamiana is the most abundant, with a total of 45 individuals (Hirata et al. 2010Hirata J, Melo MMRF, Eisenlohr P. 2010. Padrões florísticos do componente arbóreo sob interferência de trilhas em um trecho de Floresta Ombrófila Densa de Transição em São Paulo, SP, Brasil. Hoehnea 37: 555-570.; Tanus et al. 2012Tanus MR, Pastore M, Bianchini RS, Gomes EPC. 2012. Estrutura e composição de um trecho de Mata Atlântica no Parque Estadual das Fontes do Ipiranga, São Paulo, SP, Brasil. Hoehnea 39: 157-168.), followed by P. undulatum with eight (Vuono 1985Vuono Y. 1985. Fitossociologia do estrato arbóreo da floresta da reserva biológica do Instituto de Botânica (São Paulo, SP). MSc Thesis, Instituto de Biociências, Universidade de São Paulo, São Paulo.; Nastri et al. 1992Nastri V, Catharino ELM, Rossi L, et al. 1992. Estudos fitossociológicos em uma área do Instituto de Botânica de São Paulo utilizados em programas de educação ambiental. Revista do Instituto Florestal 4: 219-225.), Dracaena sp. with five (Davison 2009Davison CP. 2009. Estrutura de clareiras e a presença de bambus em um fragmento de Floresta Atlântica, SP, Brasil. MSc Thesis, Instituto de Botânica, São Paulo.), C. arabica with three (Kondrat 2014Kondrat H. 2014. Dinâmica da Comunidade Vegetal de Remanescente de Mata Atlântica na Região Metropolitana de São Paulo. MSc Thesis, Instituto de Botânica, São Paulo.), and E. japonica with one (Tanus et al. 2012Tanus MR, Pastore M, Bianchini RS, Gomes EPC. 2012. Estrutura e composição de um trecho de Mata Atlântica no Parque Estadual das Fontes do Ipiranga, São Paulo, SP, Brasil. Hoehnea 39: 157-168.) (the same individual counted by us).

Disturbance has a strong influence on the process of invasion by exotic species (Lake & Leishman 2004Lake JC, Leishman MR. 2004. Invasion success of exotic in natural ecosystems: the role of disturbance, plant attributes and freedom from herbivores. Biological Conservation 117: 215-226.). If the typical vegetation regime of disturbance an area is maintained, it can serve to decrease the propensity for invasion (Alpert et al. 2000Alpert P, Bone E, Holzapfel C. 2000. Invasiveness, invasibility and the role of environmental stress in the spread of non-native plants. Perspectives in Plant Ecology Evolution and Systematics 3: 52-66.), but if it is atypical, it can become decisive in the successful invasion of non-native species and their impact on the native plant community (Lake & Leishman 2004Lake JC, Leishman MR. 2004. Invasion success of exotic in natural ecosystems: the role of disturbance, plant attributes and freedom from herbivores. Biological Conservation 117: 215-226.; Hansen & Clevenger 2005Hansen MJ, Clevenger AP. 2005. The influence of disturbance and habitat on the presence of non-native plant species along transport corridors. Biological Conservation 125: 249-259.; Jauni et al. 2015Jauni M, Gripenberg S, Ramula S. 2015. Non-native plant species benefit from disturbance: a meta-analysis. Oikos 124: 122-129.). The differentiation and categorization of exotic species invaders as those that invade undisturbed natural ecosystems and those that survive in disturbed areas as ruderals by Durigan et al. (2013Durigan G, Ivanauskas NM, Zakia MJB, Abreu RCR. 2013. Control of invasive plants: ecological and socioeconomic criteria for the decision making process. Brazilian Journal of Nature Conservation 11:23-30.), is consistent with our purposed framework based on population ecology. This distinction seems to facilitate a process of initial filtering of all exotic species resident in a specific region. From this confluence of interpretations of the presence of exotic species in the native plant community, specifically in PEFI, L. chinensis is considered to be of high priority for management, while E. japonica and Pinus sp. as low priority.

As highlighted by Durigan et al. (2013Durigan G, Ivanauskas NM, Zakia MJB, Abreu RCR. 2013. Control of invasive plants: ecological and socioeconomic criteria for the decision making process. Brazilian Journal of Nature Conservation 11:23-30.), their dichotomous key is effective in cases where the establishment of exotic species has already occurred. We noticed that the low proportions of exotics in the community concentrate most species in a unique category, as does our population interpretation model, though its objective was to define and refine priorities. Consequently, we suggest that the density:coverage ratio for exotic species is both an easy and fast measurement to make during field data collection. Furthermore, it seems to visually separate groups and serves as an elucidative alternative for distinguishing the priorities of exotic species in such cases. Considering this new approach, A. cunninghamiana, C. arabica, and S. jambos were added as high priority species for management actions. As discussed above, the presence of coffee is probably due to the historical land use of the areas that were decreed as PEFI. This species has been present in PEFI for at least 48 years and, until now, in low densities compared to the native community. Hence, we suggest C. arabica to be monitored instead of managed at the present moment. We indicate periodic monitoring for all other exotic species not classified as high priority.

The invasion process detected at PEFI is in its early stages allows for more opportunities with regard to making decisions about management based on the actual scenario (Crooks 2005Crooks JA. 2005. Lag times and exotic species: The ecology and management of biological invasions in slow-motion. Ecoscience 12:316-329.). However, the low abundance of exotic species should not be ignored. The initial stage of the invasion of PEFI forests must be addressed with responsibility and in a timely manner in order to maintain the integrity of this important Atlantic Forest patch immersed in an urban matrix. Thus, the presented invasion panorama makes it possible to identify some invasive exotic species as priorities for management, and assist decision-making and allocation of financial resources.

Acknowledgements

The authors thank Instituto de Botânica for institutional and technical support (process SMA 00235/08). L.P. thanks CAPES for the granting of a Master thesis scholarship. E.P.C.G. thanks Conselho Nacional de Desenvolvimento Científico e Tecnológico - CNPq, as this work was partially supported through a research grant (475831/2012-08). The authors thank the anonymous reviewer and the Associate Editor for their helpful comments and suggestions on an earlier version of this manuscript.

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Publication Dates

  • Publication in this collection
    Oct-Dec 2018

History

  • Received
    09 Sept 2017
  • Accepted
    23 May 2018
Sociedade Botânica do Brasil SCLN 307 - Bloco B - Sala 218 - Ed. Constrol Center Asa Norte CEP: 70746-520 Brasília/DF. - Alta Floresta - MT - Brazil
E-mail: acta@botanica.org.br