Vascular flora in dry-shrub and wet grassland Cerrado seven years after a fire

Studies of temporal dynamics for grassland sites report that fire suppression plays a crucial role in floristic changes. The objective of this study was to verify whether after seven years without fire, communities showed variations in terms of composition, life forms, pollination and dispersal syndromes. The first survey (T0) was conducted from September 1999 to October 2000, while the second (T1) took place from August 2006 to August 2007. The floristic results in T1 were compared with the survey in T0 through the Sorensen similarity index and Chi-square tests. Over time, there were differences in the composition, life forms and pollination and dispersion syndromes. The evidence of changes suggests that the frequency of the fire regime can be considered the main agent for change in the flora of these communities.


Introduction
The dynamic process in a community is characterized by patterns, mechanisms and, in many systems, successive disturbances are important sources of changes in the landscape (Glenn-Lewin and van der Maarel 1992).The progression of changes in the composition and structure of a community over time, due to disturbances in the environment, is conceptualized as a succession process or directional change (Buchanan 1982).
Studies of temporal dynamics for grassland sites report that the suppression of disturbances such as fire plays a crucial role in the floristic and structural changes of these communities (San José and Fariñas 1991;Moreira 2000;Behling et al. 2007;Kahmen and Poschlod 2008;Ravi and D'Odorico 2009).Changes over time are related to differences in species abundance and composition, differences in the spectrum of life forms and functional characteristics.The suppression of fire in savannas intervenes in natural ecological processes, and in more open areas like grasslands, a gradual increase in the density of woody and fire-sensitive species can be seen (San José and Fariñas 1983;1991;Silva et al. 2001;Durigan and Ratter 2006;Gardner 2006;Pinheiro and Durigan 2009).
Savannas are considered dynamic ecotones, distributed between grassland formations and more densely vegetated areas (Coutinho 1978, Roitman et al. 2008).In these landscapes grasses and trees coexist, influenced by interactions with the climate, soil and disturbances such as fire, and fluctuations in any of these factors may result in an increase in certain life forms (Roitman et al. 2008).The intensification or suppression of disturbances modifies the composition of species in an area.The landscape is altered by the exclusion of sensitive species in the first case, and by the exclusion of resistant species in the second (Libano and Felfili 2006).
Abstract: Studies of temporal dynamics for grassland sites report that fire suppression plays a crucial role in floristic changes.The objective of this study was to verify whether after seven years without fire, communities showed variations in terms of composition, life forms, pollination and dispersal syndromes.The first survey (T0) was conducted from September 1999 to October 2000, while the second (T1) took place from August 2006 to August 2007.The floristic results in T1 were compared with the survey in T0 through the Sorensen similarity index and Chi-square tests.Over time, there were differences in the composition, life forms and pollination and dispersion syndromes.The evidence of changes suggests that the frequency of the fire regime can be considered the main agent for change in the flora of these communities.
physiognomies of the Cerrado domain and is comprised exclusively by shrubs and herbaceous species, where variations in topography, soil, and humidity allow the establishment of subshrub-herbaceous species and also of some woody species found in adjacent cerrado areas (Ribeiro and Walter 2008).Wet grasslands (Campo limpo úmido) can be found in various topographic positions, with different variations in humidity, depth and soil fertility conditions (Munhoz et al. 2008).This physiognomy rarely occurs in flat areas with deep soils, but is common in Central Brazil, on the slopes of plateaus and alongside "veredas" (palm swampy vegetation) (Ribeiro and Walter 2008).The wet grasslands occur on the edge of gallery forests, seasonally flooded soils in valley bottoms, especially on hydromorphic soils and peaty organic soils (Felfili et al. 2005), with gradations of humidity and segments where the water table is shallow (Munhoz et al. 2008).
This paper reports on an ongoing monitoring project of the flora in an area of wet grassland and dry-shrub grassland, on the Água Limpa Farm, located in the south of the Federal District, Brazil.The study sites had experienced an accidental fire about a month before the first survey (1999)(2000)(2001) (Munhoz and Felfili 2007a), and over a period of seven years there were no disturbances related to the fire regime.The main objectives were to verify whether after seven years without fire, the communities showed variation in their floristic composition, life forms, pollination and dispersal syndromes.

Study site
This study was conducted in adjacent wet grassland and dry-shrub grassland sites (Figure 1), both of approximately 16 ha, located on the Água Limpa Farm (ALF), (15°56' to 15°59' S and 47°55' to 47°58' WGr.), in the south of the Federal District, and owned by the University of Brasilia (UnB), comprising a core area of the Cerrado Biosphere Reserve.
The climate is Aw according to Köppen classification and is characterized by two well defined seasons: one that is hot and rainy (October to April) and the other cold and dry (May-September).In the study site the average annual maximum temperature is 28.5ºC with an average annual minimum of 12ºC.The average annual rainfall from November 1999 to April 2007 was 1,175 mm, measured at the meteorological station of the IBGE Ecological Reserve (RECOR), at a distance of approximately 5 km from the study site.

Data collection
The study sites and the surrounding areas (gallery forest and cerrado sensu stricto) experienced an accidental fire in the first week of August 1999, about a month before the first survey (T0), carried out in the area on a fortnightly basis, from September 1999 to October 2000 (Munhoz and Felfili 2004;2007a), but have never since suffered any disturbances related to the fire regime.
The second floristic survey (T1) was carried out twice a month from August 2006 to August 2007.In both studies, botanical materials in reproductive stage of all specimens with herbaceous, subshrub, shrub and nonwoody liana habits were collected along marked trails running parallel and perpendicular to the edge of the gallery forest stream Taquara, so as to cover the greatest possible extent of the site (Munhoz and Felfili 2004;2007a).
The species collected were classified according to the main groups of plant life forms, following the terminology proposed by Raunkiaer (1934) and adapted by Ellenberg and Mueller-Dombois (1967).The taxonomic identification was performed by reference to the literature, comparison with specimens from the herbarium of the University of Brasilia (UB) and the Ecological Reserve of the Brazilian Institute of Geography and Statistics (IBGE) and subsequent confirmation by specialists in each taxonomic group.The specimens collected were herbalized according to the usual procedures, and stored in the herbaria mentioned above.Exotic species behaving as invasive in the study site were also collected for floristic records.
Species were classified into families based on the Angiosperm Phylogeny Group III system (APG III 2009), and through the Angiosperm Phylogeny Website (Stevens 2001).Author names for all species and synonyms were checked against The Plant List project page (2010) (http:// www.theplantlist.org/).

Data Analysis
Floristic findings in T1 for the ALF wet and dryshrub grasslands were compared with the T0 survey (Munhoz and Felfili 2004;2007a), by means of the Sørensen Similarity Index.The floristic lists produced for both surveys was compiled into a single one, taking into account only Angiosperms.Life forms and the dispersal and pollination syndromes comprised the species matrix, classified for their presence and absence in T1 and T0.In order to classify the species as native and subspontaneous (exotic) we used the information available in the Brazilian Flora Species List (http://floradobrasil.jbrj.gov.br/2012/index) and the recommendations suggested by Moro et al. (2012).The rare species were classified according to the list of rare plants in Brazil (Giulietti et al. 2009).
To verify that the categories of life forms, pollination and dispersal syndromes were significantly different over time and space, Chi-square (c²) tests were applied (Zar 1999).
To assess the similarity between surveys and between communities we used the Sørensen Similarity Index, based on the presence and absence of species (Mueller-Dombois and Ellenberg 1974).This index was calculated by means of the MVSP software, version 3.13 (Kovach Computing Services 2005).

Results and Discussion
After seven years without fire, changes in their floristic composition of the studied communities were verified (Figure 2A).There was an increase in the richness of species, families and genera (Figure 2A).Compared to the first survey, the number of species increased by 7.5% and 6% for the wet (campo limpo úmido) and dry-shrub (campo sujo) grassland, respectively.In both periods, the dry-shrub and wet grasslands had 35 species in common, while in the second survey only 24 such species were found.In the wet grassland, 101 species that were recorded after the 1999 fire were not found in 2006, and 124 settled in the area after seven years, while in the dry-shrub grassland, 101 disappeared and 134 emerged (Table 1).In total (T0 + T1) were listed 317 species for wet grassland and 394 species for the dry-shrub grassland.There was a record of 557 species adding the two areas.
The floristic similarity between the surveys in the dryshrub grassland was 53.5%, while in the wet grassland it was 38.5%.Albeit adjacent, the floristic similarity between the sites is low, 30% in T0 and 33.6% in T1.The low similarity between communities in space and on different observation occasions suggests floristic distinctions between the wet and dry-shrub grasslands, with most species being typical of each area, with low sharing over the seven-year interval between the surveys .
The five families with the greatest number of species in the ALF wet and dry-shrub grassland sites were Asteraceae (91), Poaceae (75), Fabaceae (47), Melastomataceae (25) and Cyperaceae ( 23).The families Poaceae and Cyperaceae showed a reduction in the wealth of species --the former in both sites and the latter only in the wet grassland.In the grassy-woody savanna of the Pantanal an increase in the number and frequency of the Cyperaceae's species and Eudicots was observed after fire (Cardoso et al. 2000), suggesting that its suppression could influence the decline in the richness of these species, as observed in the ALF wet grassland after seven years without the presence of fire.Over time, only Poaceae and Asteraceae were common to the two sites among the five families with the highest number of species.The Asteraceae and Poaceae typically feature greater variety, especially in the savanna and grassland physiognomies of the Cerrado, where they are virtually restricted to the herbaceoussubshrub component (Mantovani and Martins 1993;Batalha and Martins 2002;Munhoz and Felfili 2007a).The high colonization by individuals of these families is due to the fact that most species support direct sunlight and require high light intensity, conditions found in open areas, making these ideal places for their settlement (Tannus and Assis 2004).These two are also among the nine families deemed hyperdiverse in Brazil, since they feature at least a thousand species considered to be native (Rapini et al. 2009).
Significant differences were found in life forms between the wet and dry-shrub grasslands, both in T0 (c² = 41.24,p = 8.39 -08 ) and in T1 (c² = 12.61, p = 0.02).Over time, the dominant life forms in the communities were the hemicryptophytes and chamaephytes, the former predominating in the wet grassland and the latter in the dry-shrub grassland (Figure 2B).As time elapsed since the last fire, the number of phanerophyte species increased in both communities, and that of therophytes and hemicryptophytes dropped in wet grassland (Figure 2B).Over time, only the wet grassland showed significant differences in the number of species by life form (c² = 19.51,p = 0.0015) due to the significant increase in phanerophytes and chamaephytes and reduction in hemicryptophytes and therophytes (Figure 2B).In the open savannas of Africa, the increase in shrubs determined a decline in the number of herbaceous species, after the suppression of fire (Belsky 1994;Duncan and Duncan 2000).The presence of shrubs and small trees in the landscape can change the phenology, composition, spatial distribution, biomass allocation and productivity of the herbaceous component (Scholes and Archer 1997).Shrub establishment, coverage and density cause changes in the soil and shading of herbs, resulting in the declining productivity of the latter (Scholes and Archer 1997).
As for the Cerrado, a gradual increase in tree coverage density has been recorded after years of vegetation protection against fire.In areas of savanna woodland (cerradão), cerrado sensu stricto, "campo cerrado" and shrub savanna (campo sujo), the absence of fires caused a significant increase in the number of woody species, with open areas showing the highest values, that is, the absence of disturbances allowed the settlement and regeneration of the woody component (Moreira 2000).After 44 years of protection from fire, the main change observed with satellite images in vegetation cover at the Assis Ecological Station, an area of Cerrado in southeastern Brazil, was the continuous thickening of vegetation, with open grassland areas being gradually occupied by closed cerrado physiognomies (Pinheiro and Durigan 2009).Protected since 1959, with the suppression of fire since 2004 in that area the wet grassland had its area reduced to one fourth of the initial extent, losing ground to the cerrado sensu stricto and riparian forests (Pinheiro and Durigan 2009).Apparently, in the ALF wet grassland these patterns described by Moreira (2000) and Pinheiro and Durigan (2009) can also be verified, whereby the exclusion of fire for seven years has encouraged the growth and settlement of phanerophytes and chamaephytes (woody component ) and resulted in changes in the landscape due to the density of these shrubs.
The dispersal syndromes, anemochory and autocory remained dominant in the communities studied (Figure 2C).There were significant changes in the dispersal syndromes in the wet grassland over time (c² = 7.93, p = 0.01), with a reduction in autochorous species and an increase in zoochoric ones (Figure 2C).The dispersion syndromes of the wet and dry-shrub grasslands were significantly different in T0 (c² = 8.56, p = 0.01) but not in T1 (c² = 2.03, p = 0.36), suggesting that over time and space a functional strategy of dispersal syndrome convergence occurred between the adjacent areas.
Zoophily was the dominant pollination syndrome in the communities in both surveys (Figure 1d), with increases of 8.6% in the wet grassland and approximately 3% in the dry-shrub grassland.There was a general reduction in the number of anemophilous species: in the wet grassland this decrease was of 8.1% and in the dry-shrub grassland, 2.8% (Figure 2D).Over time, only the wet grassland (c² = 3.40, p = 0.05) showed significant differences in pollination syndromes, due to the increase in the number of zoochoric species between surveys and the decrease in anemophilous species (Figure 2D).
The predominance of anemochoric dispersion over time is associated to the physiognomic types of the sites, which are open grasslands, and the dominance of herbaceous species, a pattern observed in other studies on the Cerrado (Batalha et al. 1997;Batalha and Mantovani 2000;Tannus et al. 2006), and in this dry-shrub grassland seven years ago (Munhoz and Felfili 2007b), but increased zoochory may be another factor to confirm the influence of the absence of fire in the changes found in the landscape over time, especially in the ALF wet grassland, where after years of fire protection a greater density of chamaephytes and phanerophytes was verified.The prevalence of the zoochoric dispersal syndrome in different environments is associated with the dominance of woody species (phanerophytes and chamaephytes), as occurs in the cerrado sensu stricto and forest habitats (Batalha and Mantovani 2000;Kinoshita et al. 2006;Tannus and Assis 2006;Ishara and Maimoni-Rodella 2011).
The conditions of more open vegetation and the dominance of one layer composed of herbs, besides benefiting the presence of wind-dispersed species also favor a high frequency of anemophilous species (Gottsberger and Silberbauer-Gottsberger 2006b;Barbosa and Sazima 2008;Ishara and Maimoni-Rodella 2011), which in the ALF wet and dry-shrub grasslands showed a reduction over time in the studied communities.This anemophily reduction is associated with the exclusion of fire for seven years, since the reproductive behavior of some grasses, a group to which belong most of the species pollinated by wind, is dependent on fire, so few species flourish in the absence of this type of disorder (Sarmiento 1992;Canales et al. 1994;Munhoz and Amaral 2010).The proportions and occurrences of different pollination systems are affected by differences in floristic composition (Ramírez 1989).
Seven species found in the ALF site are on the list of Rare Plants of Brazil (Giulietti et al. 2009 H.loeseneriana e X.diaphanobracteata only settled in the sites after fire suppression, P. juncea was listed after the fire only.This species flowers and fruits from November to May, and flowering is intense especially after fires (Marques 1988).H.tenuifolia e S. irwiniana were recorded in both surveys.H. tenuifolia occurred for a short period in the ALF dry-shrub grassland, and was recorded seven months after the fire, in the month of April during the dry season of 2000 (Munhoz and Felfili 2006).These plants were considered rare, since they have a restricted range of occurrence (<10,000 km²) and therefore meet criteria B1 and D2 of the IUCN (International Union for the Conservation of Nature), that is, in terms of the first criterion they can be classified as threatened depending on the number of locations or fragmentation and if they experience decline and/or extreme fluctuations regarding the boundaries of occurrence, area of occupancy, environmental conditions, number of locations or subpopulations, and/or number of mature individuals; and for the second criterion, these species can be considered endangered in the near future (Rapini et al. 2009).
Three species were classified as subspontaneous to the flora of the Brazil (Brazilian Flora Species List 2012) (Table 1).Clibadium armanii (Balb.)Sch.Bip.ex O.E.Schulz (Asteraceae) e Melinis minutiflora P. Beauv (Poaceae) were recorded only after some distance from fire and only Melinis repens (Willd.)Zizka (Poaceae) appeared in all surveys (Table 1).After seven years of fire the grass Melinis minutiflora P. Beauv.settled in the ALF dry-shrub grassland was listed among the species with the highest percentage of coverage (A.G.Amaral, unpublished data).M. minutiflora is sensitive to fire and is adapted to low soil fertility (Martins et al. 2004), a condition found in the ALF dry-shrub grassland for its settlement and proliferation alongside the absence of fire for seven years.As a consequence of high competitive power, ample plant growth and a vast production of viable seeds, the species M. minutiflora has become a threat to the conservation of the biome's flora (Filgueiras 1991;Martins et al. 2004).
For the herb-shrub layer of the dry-shrub grassland, and particularly in the ALF wet grassland, the evidence found in changes related to composition, life forms and pollination and dispersal syndromes, point to a process of succession in these communities, generated by the exclusion of fire for seven years.For these environments, the frequency of the fire regime can be considered the main agent of change in the composition, life forms and phenology of species.

Figure 1 .
Figure 1.Location of Água Limpa Farm (ALF) in the south of Federal District, Brazil.The study areas are located in northeast at AFL.

Figure 2 .
Figure 2. Floristic composition, life forms, pollination and dispersal syndromes of the species in the dry-shrub and wet grassland in T0 and T1 at Água Limpa Farm, (ALF), Brasília, DF, Brazil.(A) Number of species per family and genera and subspontaneous and rare species; (B) Number of species per life form; (C) Number of species per dispersal syndrome; (D) Number of species per pollination syndrome.