Exotic woody plants in Pelotas , Rio Grande do Sul , southernmost Brazil

Exotic species are spreading in various parts of the planet and sometimes becoming biological invaders. A floristic survey was carried out to find exotic trees, shrubs, and climbers in different communities in Pelotas, Rio Grande do Sul, southern Brazil. The traversal method was used at 26 sites. The richness totaled 26 species in 22 genera and 17 families. There are 19 trees, 5 arborescents, 1 shrub, and 1 climber. Most of the exotic species are already naturalized in the study area. Between 1 and 10 individuals sporadically occur at each site. For species of characteristically invasive exotic plants were observed, including 3 trees (Pinus elliottii Engel, Pinus taeda L. Engelm., and Pittosporum undulatum Vent.) and 1 shrub (Ulex europaeus L.). A continuous monitoring of exotic flora is needed to eliminate or control invasive plant species and to avoid economic and ecological damage to ecosystems.


Introduction
Most species have their geographical extent limited by climatic and/or environmental barriers (Ricklefs 2009).Mountain chains and oceans form natural barriers to the dispersal of species and ecosystems remain relatively isolated (Lowe et al. 2000).However, natural biogeographical barriers have lost their effectiveness due to the increase in economic globalization (Borokini 2010).The flow of species associated with the disturbance of habitat and destruction and fragmentation of ecosystems accelerates the accidental or intentional introduction of many species of plants into ecosystems where they are not native (Cronk and Fuller 1995, Richardson et al. 2000, Delnatte and Meyer 2011).
Biological invasion is a process of introduction and consequent adaptation of species that are not naturally part of an ecosystem (Ziller 2001).The capacity for reproduction of invasive exotic species permits these invasives to colonize areas far from the parent plant and with the potential to spread in a considerable area of the environment (Richardson et al. 2000).Biological invasion has been causing economic damage and undermining the provision of services and the functioning of ecosystems (Gisp 2005).In addition, invasive exotic species are considered the second greatest threat and cause of global biodiversity loss (Wilson 1997, Lowe et al. 2000, Ziller 2001).
In the state of Rio Grande do Sul, in southernmost Brazil, floristic and phytosociological surveys were conducted that included exotic plants (Silveira 1992, Carneiro and Irgang 2005, Mondin 2006, Medeiros and Focht 2007, Schneider 2007, Venzke et al. 2008, Guadagnin et al. 2009, Soligo et al. 2009, Cordazzo and Rosa 2010, Karam and Cardoso 2010, Burgueño et al. 2013, Rio Grande do Sul 2013, Rio Grande do Sul 2014, Rolim et al. 2015, Cordero et al. 2016).In these studies, exotic species in the process of biological invasion were found sporadically.Guadagnin et al. (2009) collected data from alien species in the Biome of Pampa, the grassland physiognomy in Uruguay, Argentina, and Brazil in Southernmost, where 365 species were found with spontaneous populations.The floristic of alien species of Silveira (1992) researches more than 1500 exotic plants.Schneider (2007) listed 270 vegetables exotics herbaceous and subspontaneous.In forests of state of Rio Grande do Sul, Mondin (2006) found 59 exotic species.Carneiro and Irgang (2005) studied the geographical origin of the vascular flora of the municipality of General Câmara, and found that 32% were non-native species from around the world, and several pantropical and pansubtropicals.Medeiros and Focht (2007) wrote about the invasive Eragrostis plana Nees, an aggressive Poaceae invasive in grassland of Rio Grande do Sul.
In Brazil of Southernmost, in the urban areas of maritime dunes of Cassino's Beach, Cordazzo and Rosa (2010) found half (35 spp.) of the plant species exotic, originating as ornamentals.Cordero et al (2016) studied the phytossociology of the shrub Ulex europaeus in a forest-grassland mosaic and found that this shrub it cover 10.1% of the total area studied.In a literature survey of alien herbaceous plants and shrubs, Rolim et al. (2015) found that most species have geographical origin in Central Europe and predominantly reproduce by small seeds or fruits.The authors also observed a lack of data on natural ecosystems in several regions of the state.
The ecological problem of the biological invasion is governed by Brazilian law through the National Biodiversity Policy (Brasil 2002) and in Rio Grande do Sul, by state law (Rio Grande do Sul 2013).The federal decree points out the need for inventory and mapping of invasive exotic species to guide studies evaluate of the generated environmental impacts and control actions (Brasil 2002).State law prohibits the cultivation of and establishes control rules for 99 species of plants, algae, fish, invertebrates, and terrestrial vertebrates.Thus, we contribute to the knowledge of non-native species by surveying of trees, arborescents and woody shrubs into forest and grassland physiognomies in the municipality of Pelotas, southernmost Brazil.

Methods
Study area.The study area was vegetation in the municipality of Pelotas, in southernmost Brazil.(Fig. 1).The native vegetation is classified into 2 phytogeographical regions: (1) areas of Pioneer Formations with fluvial influence and distributed in the Coastal Plain geological unit (This region of the landscape matrix is formed by grassland vegetation, wetland vegetation, lagoon and clumps of tree); and (2) Semideciduous Seasonal Forest, on the eastern slope of the Shield of Rio Grande do Sul geological unit (IBGE 1986).
Data collection.This survey of the exotic species with tree, arborescents and woody shrub was part of a larger study including native vegetation in Pelotas.At moment, the richness of native plants in Pelotas is 148 species tree, arborescents and woody shrub (Venzke 2012).The list of species was estimated by the method of walking in different transects and others phytossociological data at 26 sites with forest and grassland vegetation.(Fig. 1, Table 1).The transversal method is performed by walking through the same physiognomy of vegetation, noting species (Filgueiras et al 1994).
The survey of the exotic species in fragmented habitats consisted of 28 transects in the phytogeographic unit of the Semideciduous Seasonal Forest unit and 9 transects in Areas of Pioneer Formations.Sampling time was 596 h.In the Semideciduous Seasonal Forest, sites were in riparian forest and slope forests, as well as abandoned mines and plantations of Pinus and Eucalyptus.In areas of Pioneer Formations, sites were in sandy and swamp forest, in mosaic of grassland-forest, alongside roads, and in urban areas.
These fragmented habitats were at different successional stages or were anthropic areas around abandoned houses, in orchards, in abandoned plantation forests, along roads, and in abandoned rock and sand quarries.We included in the sample species of trees, arborescents, shrubs, and climbers.We classified trees as having a minimum height of 6 m and diameter at breast height (DBH) of at least 5 cm, and arborescents having heights between 3 m and 6 m.
The plants were identified using popular knowledge and by consultating the herbarium of the Federal University of Pelotas (PEL).We classified exotic species in the field following Richardson et al. (2000) and Zenni and Ziller (2011), and reserch in database about the theme (Gisp 2005, Mondin 2006, Zenni and Ziller 2011, Rio Grande do Sul 2013, Australian Invasive Species Program 2015, Hear 2014, Instituto Horus 2015, Issg 2015).Two categories were used.Naturalized exotic plants are those with scattered individuals, usually near adult plants.However, invasive exotic plants are those having many seedlings, often at a considerable distance from the parent plant, reproducing and spreading in the environment and advanced over natural and/or anthropic habitats (Richardson et al. 2000).We classified exotic species by their anthropic use.Ornamental, wood, food and hedges.Ornamental: planted for shade or to beautify parks, gardens, streets and avenues.Wood: planted for use as firewood or lumber.Food: planted for consumption of edible fruits and seeds.Hedges: planted to divide areas, such as farms, as living fences.(2006).Numbers refer to collection sites in Table 1.

Results
The survey resulted in 26 exotic species, 22 genera and 17 families (Table 2).There are 19 trees, 5 arborescents, 1 shrub, and 1 climber.The richest family was the Fabaceae, with 4 species, followed by Rutaceae with 3 species, and Rosaceae and Pinaceae with 2 each.We found 2 native species from other phytogeographic regions of Rio Grande do Sul state, Ceiba speciosa (A.St.-Hil., A.Juss.& Cambess) Ravenna and Araucaria angustifolia (Bertol.)Kuntze, from the Deciduous Seasonal Forest and Mixed Ombrophilous Forest, respectively.Anthropic usages are listed in the Table 1 (see also Fig. 2).The ornamental usage was the most common.For 84% of the species shown there was no focal point of biological invasion, and we consider these to be naturalized exotic species.
However, currently, invasive exotic species at an advanced stage of infestation has been observed for species Pinus elliottii Engelm., Pinus taeda L., Pittosporum undulatum Vent.and Ulex europaeus L. Pinus species have a preference for grasslands (Fig. 3a, 3c).The largest foci area of infestation was observed in open grasslands of  the Coastal Plain, near forest plantations and windbreaks of pine (Fig. 3).Pinus elliottii and P. taeda occurred on cropland and/or pastures within the Semideciduous Seasonal Forest and in abandoned stone and sand quarries.
Ulex europaeus occurred on roadsides, and in grasslands used as pastures (Fig. 4a).We observed Pittosporum undulatum in open areas in the early stages of forest succession of Semidecidu-ous Seasonal Forest fragments and in shaded understory (Figs 3d,4c,4d).

Discussion
Thus as ornamentals is the primary means worldwide by which exotic plants become invasive.This is pattern was seen in other studies (Mondin 2006, Cordazzo and Rosa

2010)
. Guadagnin et al. (2009) noted that there are no records of exotic woody plants introduced accidentally to the Pampas biome.All woody plants were introduced intentionally for some anthropic use, and that half of the species introduced for ornamental purposes became invasive over time should be considered dangerous (Ziller 2001).Mondin (2006) comments that more research about the greater use of native flora for ornamental, fruits, and wood is necessary Pittosporum undulatum and Pinus spp.are frequent in urban and rural afforestation in the region of our study, and this tradition of using exotic plants in the afforestation does not value native biodiversity, favoring the development of a culture distanced from the surrounding natural environment (Leão et al. 2011).Furthermore, forestation with exotic trees can work as a source of propagules for biological invasions (Dehnen-Schmutz et al. 2007, Blum et al. 2008).Reforestation with native species should be encouraged to improving the natural environment and to avoid possible future biological invasions.The state law of Rio Grande do Sul (2013) established procedures and standards to prevent and control biological invasions.Under this law, cultivation of some species such as Acacia longifola, Hovenia dulcis, Lonicera japonica, Pittosporum undulatum, and Ulex europaeus are prohibited in farming.Another category of law is that alien species may be used under controlled conditions such as Pinus spp., Acacia mearnsii, Leucaena leucocephala, Morus nigra and Syzygium cumini.
Although some naturalized species do not show characteristics of invasive plants, which spreads throughout the environment, they are cited in other regions of Brazil and in the world, behaving as biological invasive (Australian Invasive Species Program 2015, Hear 2014, Instituto Horus 2015, Issg 2015, Rio Grande do Sul 2013, Zenni and Ziller 2011).Sometimes, the naturalized species present a long-term pattern of pre-infestation, before the explosive invasion (Odum 2001).This principle shows the necessity to accompany exotic species for preliminary detection of the biological invasion process.These species are not currently spreading in the studied sites, citing Acacia longifolia, Leucaena leucocephala, Melia azedarach, Ligustrum japonicum and Eriobotrya japonica.For this group of plants, monitoring is necessary, for the possibility of biological invasion in the future.
Biological invasion of Pinus in grassland environments is an expected pattern.Its regeneration is not being sampled in the understory of native forests and planta-tions of the species (Lombardi and Motta-Junior 1992, Oberhauser 1997, Soligo et al. 2009, Venzke et al. 2012).This reinforces such genus Pinus as an invader of grasslands (Ziller and Galvão 2002, Gisp 2005, Soligo et al. 2009, Falleiros et al. 2011, Leão et al. 2011, Zenni and Ziller 2011).
The infestation of Pittosporum undulatum in the understory of native forests was observed in Australia, Portugal and Brazil (Gleadow and Ashton 1981, Alves et al. 2003, Karam and Cardoso 2010, Zenni and Ziller 2011, Mielke et al. 2015).The specie in the Semideciduous Seasonal Forest in the municipality of Pelotas had the highest importance values in three forest fragments (Karam and Cardoso 2010).The invasion of P. undulatum in native ecosystems is conditioned by allelopathy, rapid dispersal, early seed production and rapid growth, forming high densities in the canopy that reduce the intensity of luminosity, suppressing the survival and growth of native species that are tolerant to shade (Goodland and Healey 1996).
In the studied region, the use of shallow cutting and burning for pasture renovation is very common for farmers.This practice benefits the gorse Ulex europaeus, since it accelerates the process of invasion.This is explained once the species sprouts with multiple stems, maximizing the occupation of the area and forming dense bushes (Zielke et al. 1992).As illustrated in Figure 4b, U. europaeus has numerous spines and forms dense clumps, which decreases natural pasture and become insurmountable by animals and humans (Rees andHill 2001, Gisp 2005).Furthermore, seeds of the species germinate best if subjected to fire at high temperatures and for prolonged time (Zielke et al. 1992, Mcalpine andTimmins 2002).The seed bank of the soil may continue to germinate after 30 years, being extremely difficult to eradicate it from pastures (Lee et al. 1986).The fire, besides benefiting germination, provides open sites for establishment of U. europaeus.As Johnson (2001) highlights, the expansion of established gorse bushes scrub into the areas of natural grasslands after fire.Cordero et al (2016), in the study of the structure of mosaics community of forests and fields in the region, observed that Ulex did not invade native forests.However, the species invaded planted forests and highly grazed fields.The authors found out in the understory of Ulex few species and more homogeneous populations than outside the understory of Ulex.The woody species were more abundant in the Ulex canopy, but it was a group of pioneers and ruderal species.It must be emphasized that economic costs of controlling exotics invaders are growing with the passage of time.In this way, precaution is the most efficient strategy to face and prevent biological invasions (Hobbs andHumphries 1995, Ziller et al. 2007).The precaution generates lower economic costs and the chances of solving the problems are greater when compared to control strategies after biological invasion is already established (Leão et al. 2011).
Currently, it is necessary to seek strategies for management of invasive species on ecosystems to eradicate or even reduce the infestation and control the geographic expansion of these species.Moreover, the use of inva-sive exotic species in urban and rural afforestation and degraded areas recovery projects is not recommended.Other studies are necessary to evaluate the exotic species of herbaceous stratum to identify possible biological invaders.Some invasive exotic herbaceous species around the world have been identified inhabiting the ecosystems in the region (Asparagus setaceus Kunth (Jessop), Impatiens walleriana Hook.f., Cyperus esculentus L. and Cynodon dactylon L. (Pers.).

Figure 1 .
Figure 1.Location map fragments in the Municipality of Pelotas, Rio Grande do Sul State, Brazil.• = collection points.Adapted from relief map of the Prefeitura Municipal de Pelotas(2006).Numbers refer to collection sites in Table1.

Figure 2 .
Figure 2. Anthropic uses for exotic species observed in fragments of native vegetation in the municipality city of Pelotas, Rio Grande do Sul state, Brazil.

Figure 3 .
Figure 3. Exotic invasive species in the municipality of Pelotas, RS, Brazil.a. Seedlings in annual crops abandoned and trees in the background matrices of a windbreaker.b.Natural regeneration in heavily thickened area after harvest of pine trees.c.Understory in areas of fossil dunes on the Coastal Plain.d.Canopy of mature individuals of Pinus with Pittosporum undulatum on the edge of the fragment.

Figure 4 .
Figure 4. Exotic invasive species in the municipality of Pelotas, RS, Brazil.a. Grazing field invaded by Ulex europaeus in the Coastal Plain.b.Ulex europaeus branch full of thorns.c.Seedling Pittosporum undulatum inhabiting the understory of Semideciduous Seasonal Forest.d.Fragment infested of Pittosporum undulatum (arrows).
Resuming, the invasion of U. europaeus changes the successional vegetables, affecting the cover and diversity of native plants community.The species nowadays have focus on invaders in the municipality of Pelotas, Pinus spp., Ulex europaeus and Pittosporum undulatum, already cited as invasive for the studied region (Mondin 2006, Zenni and Ziller 2011, Rio Grande do Sul 2013).The state law for Pinus (Rio Grande do Sul 2014) prohibits the use as windbreak, shading and thermal comfort, ornamentation of urban areas and roads, environmental recuperation and other purposes that are not specific to forest production.Still, for forest production, for Pinus plantations, environmental licensing and permanent control methods of dispersion into the environment are required.Ulex europaeus and Pittosporum undulatum cultivation is prohibited in any situation (Rio Grande do Sul 2013).

Table 1 .
Characteristics of collection points of study the exotic species in the municipality of Pelotas, Rio Grande do Sul, Brazil.Estimated area = estimated area of the fragment; s = Semideciduous Seasonal Forest; r = areas of pioneer formations (Restinga Forest).