Floristic composition and dispersal syndromes in Araucaria Forest remnants in the municipality of Colombo , Paraná state , Brazil

This study was conducted in Araucaria Forest remnants in the municipality of Colombo, eastern Paraná state, Brazil. Data on species occurrence, life forms and dispersal syndromes were collected once a week along a 9 km transect, revealing the presence of 512 species among trees (n = 135), shrubs (n = 121), herbs (n = 157), climbers (n = 70), epiphytes (n = 24) and hemiparasites (n = 5). Of 469 species classified according to dispersal syndromes, 42.4% were zoochoric, 33.6% autochoric and 23.8% anemochoric. The high richness observed, the highest among similar studies previously conducted in the Araucaria Forest, along with the occurrence of endangered species of trees (and mammals), indicates that the study area is an important remnant for biodiversity conservation.


INTRODUCTION
Mixed Ombrophyllous Forest ("Floresta Ombrófila Mista", FOM according to the Brazilian classification system), also known as Araucaria Forest, is an Atlantic Forest formation.It occurs in the southern area of the states of Paraná, Santa Catarina, Rio Grande do Sul and in the southern region of São Paulo state and also in disjoint areas in the Serra da Mantiqueira mountain range, between São Paulo and south Minas Gerais states (IBGE 1992).For Hueck (1953), the limits of FOM expand to remote areas of the state of Rio de Janeiro to the north and to Argentina towards the south.In Paraná, this formation is present from 500 m altitude, starting in the western slopes of Serra do Mar, towards the First, Second and Third ("Primeiro", "Segundo" and "Terceiro") Paraná plateaus (Maack 1980).In its original distribution, the FOM covered approximately 200,000 km 2 of Paraná, covering 40% of the surface of this state (Klein 1960).However, today the Paraná FOM is reduced to less than 1% of preserved native forests, distributed in small remnants surrounded by a modified matrix (Castella and Britez 2004), such as those occurring in the metropolitan region of Curitiba (Kozera et al. 2006), where property speculation is one of the main degradation agents.
Among the various floristic surveys in the FOM (Carvalho 1980;Oliveira and Rotta 1982;Galvão et al. 1989;Negrelle and Silva 1992;Koehler et al. 1998;Sanquetta et al. 2001), few have collected all life forms (Britez et al. 1995;Kozera et al. 2006;Liebsch et al. 2009), as pointed out by Liebsch et al. (2009).It is notable that most studies give preference to tree species at the expense of other life forms, even if in some cases the trees represent less than half the local plant diversity (Kozera et al. 2006;Liebsch et al. 2009).
Regarding seed dispersal, plant species can be classified into three groups, depending on the presence of appropriate structures to facilitate dispersal: zoochoric (animals), anemochoric (wind) and autochoric (explosive devices) (van der Pijl 1972).In tropical forests, zoochory is the most common dispersal syndrome among tree species (Tabarelli et al. 1999;Talora and Morellato 2000;Mikich and Silva 2001;Almeida-Neto et al. 2008;Liebsch et al. 2008).The same pattern has contains forest plantations of native and exotic species, areas devoid of trees and scrubs and marsh land.The area is also traversed by water courses, including the Palmital River, which originates in the city of Colombo (Figure 1).The best preserved parts of the FOM remnants have a canopy formed by trees of up to 30 m tall, with a predominance of Araucaria angustifolia (Bertol.)Kuntze and under-canopy of up to 20 m, while the less conserved parts are characterized by a 15 m canopy and the presence of Ilex paraguariensis A. St. Hil.

Data collection
For the collection of reprodutive material (flowers and fruits) weekly surveys were conducted along 9 km of roads and trails that crossed and bordered the forest remnants of the study area (Figure 1).Samples were collected in two periods, from April 2003to March 2004and April 2005to March 2006.All environments (except the experimental plantations of native and exotic species) and life forms (trees, shrubs, climbers, herbs, epiphytes, hemiparasites) found in the study area were sampled.
The collected material was identified based on literature, reference collections and experts.Later the vouchers were deposited in the Herbarium Fernando Cardoso da Silva (HFC) of Embrapa Forestry, with duplicates sent also been found for FOM trees (Rondon Neto et al. 2001;Liebsch and Acra 2007;Liebsch et al. 2009).
The present study presents the floristic composition of FOM remnants located in the city of Colombo, Paraná state, including diverse life forms and dispersal syndromes.As the study area borders a large urban center, it is expected that the results may assist in its protection and conservation, besides contributing to increase the knowledge regarding the FOM as a whole.

Study area
The study was conducted in a 301 ha area that belongs to the Brazilian Agricultural Research Corporation -Embrapa Forestry (25°26′52″ S, 049°13′50″ W), located in the municipality of Colombo, 30 km from the state capital Curitiba.The average elevation of the study area is 928 m above sea level and the climate is type Cfb, according to the Koeppen classification system (Koeppen 1948).Historical rainfall data (1984 and 2001) collected in the area showed that the average annual rainfall is 1,403.5 mm, the rainiest month is January with an average of 198 mm, and the least rainy is August, averaging 64.77 mm.
In total, 124 ha of the area are FOM remnants in various successional stages (Rotta 1981).The area also
Taking into account the classification of species in different habits, the greatest richness was observed for herbs (n = 157), followed by trees (n = 135) (Table 2).If we separate all species in only two groups, trees and nontrees, most species would be "non-trees" (74%).
The dispersal characteristics and syndromes were described for 469 taxa, which corresponds to 91% of all recorded species.Zoochorous fruits were the most common (n = 199), followed by autochorous (n = 158) and anemochorous (n = 112).When life forms were taken into account, zoochory was more common among trees, encompassing 73% of species (n = 98), followed by autocory (n = 18) and anemochory (n = 17) (Table 3).Zoochory was also the most common syndrome among shrubs, but with a lower percentage of species (47%).In herbaceous species, there was a predominance of autochory with 78 species (60%), followed by anemochory with 37 species (28%), and zoochory with 16 species (12%).Epiphytes and hemiparasites also presented zoochory as the most common syndrome, accounting for 68% and 60% of species, respectively.Of the 459 species classified according to fruit type, 172 were dry dehiscent, followed by fleshy indehiscent with 171 species, dry indehiscent with 107 and fleshy dehiscent with only nine species (Table 03).Considering the 380 species classified according to the color of their fruits, there was a clear predominance of brown fruits (n = 198), followed by black (n = 76) and red (n = 38); the other 68 species were distributed in ten different colors.With respect to the dispersal mode within these 380 species, zoochorous fruits encompassed eight colors, with predominance of black fruits (n = 75), followed by red (n = 38), purple (n = 18), green (n =19), yellow (n = 15), orange (n = 12), brown (n = 10) and wine (n = 1).Most anemochorous fruits were brown (n = 33), with only one green species.Autochorous fruits were nearly always brown (n = 155), although one green species were recorded.

DISCUSSION
To date, this is the study encompassing various life forms that have recorded the greatest number of species in the FOM of Paraná state.In fact, in this Brazilian state, Kozera et al. (2006) have found 390 species in Curitiba, Britez et al. (1995) 307 species in São Mateus do Sul, and Liebsch et al. (2009) 210 species in Bituruna.It is interesting to observe that although several inventories ignore non-trees, this group might represent the majority of the species found in a particular area as in the present study.In fact, previous studies have shown that trees can represent only about half of terrestrial plant diversity (Ishara et al. 2008;Gasper et al. 2013), including FOM areas (Kozera et al. 2006;Liebsch et al. 2009).
The presence of endangered species, coupled with the location of the studied remnants in the vicinity of an important urban center, highlight the importance of the study area for the conservation of genetic resources.Such role, however, might be threatened by the presence of several exotic species, as Ligustrum japonicum, Hovenia dulcis and Eriobotrya japonica, which provide a large supply of zoochorous fruits and can compete for dispersers with native species (Lorenzi et al. 2003;Rose et al. 2008).
In tropical forest ecosystems, zoochory is often the most common dispersal syndrome among trees and shrubs, as well as overall (Howe and Smallwood 1982;Motta-Junior and Lombardi 2002;Almeida-Neto et al. 2008).In fact, such predominance has already been observed in the Dense Ombrophyllous Forest (Tabarelli et al. 1999;Liebsch et al. 2008), the Semideciduous Seasonal Forest (Mikich and Silva 2001;Santos et al. 2003;Yamamoto et al. 2007) and for the FOM (Rondon Neto et al. 2001;Liebsch and Acra 2007;Liebsch et al. 2009;present study).Anemochoric dispersal, usually with several representatives among trees and vines, in the present study was only well represented by the latter.Additionally, anemochorous fruits were less common than autochorous ones, which are usually rare (Vieira et al. 2002;Yamamoto et al. 2007) but in the study area were represented by several species of Fabaceae, Euphorbiaceae and Plantaginaceae.
The fact that most trees and shrubs had fleshy fruits (dehiscent or indehiscent) is probably related to their dispersal syndrome as fleshy fruits are usually zoochorous, while dry fruits are usually anemochorous or autochorous (van der Pijl 1972;Spina et al. 2001).In the present study, dry fruits were more common among herbs and vines.
In a FOM remnant located in Rio Grande do Sul state, Paise and Vieira (2005) analyzed 27 zoochorous species and also found eight different colors of fruit, but in this case, red or orange were the most frequent.In a Semideciduous Seasonal Forest, Mikich and Silva (2001) observed that zoochorous fruits were predominantly green, black or red.Colored fruits are meant to attract dispersers and different groups of dispersers are drawn preferably by some colors, such that birds tend to prefer black, red, wine or blue fruits, whereas primates prefer orange, yellow or green ones (Howe 1986;Wilson et al. 1990).For autochorous and wind dispersed species, which do not depend on the attraction of biotic agents for dispersing their seeds, Mikich and Silva (2001) found basically red-brownish fruits, here classified as brown.
The high diversity of plant species, the presence of several endangered species (plants, this study; mammals, Dias and Mikich 2006), and the large proportion of species dispersed by animals, emphasize the importance of the study area for the conservation of the Atlantic Forest and the FOM biodiversity.The threats imposed by the proximity of a large urban center are ameliorated by the fact that the area is possessed by a forestry research institution that maintains its native forest remnants as reserves.

Figure 1 .
Figure 1.Detail of the study area and the transect (narrow line) used to collect the data within Embrapa Forestry field station limits (thick line), Colombo, Paraná state (left map), Brazil.
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Table 2 .
Number of species, genera and families collected per life form in Araucaria Forest remnants, Colombo, Paraná, Brazil.

Table 3 .
Type of fruit and dispersal syndromes of plant species collected in Araucaria Forest remnants, Colombo, Piraná, Brazil.Possette et al. | Floristics and dispersal syndromes in Araucaria Forest