Post-fire phenology in a campo sujo vegetation in the Urucum plateau, Mato Grosso do Sul, Brazil

Studies on the herbaceous and sub-shrub layer of cerrado showed the occurrence of modifications in its composition between different regions, demonstrating sensibility to changes in climate, soil and intensity of fires, among other factors. The aim of this study was to describe the phenological variation in a campo sujo vegetation in the Urucum plateau. We established eight transects of 250 m each, 50 m apart. We sampled all flowering and fruiting species located at least three meters from each side of the transect. Beginning in October 2007, one month after an accidental fire occurred in the study site, we analysed flowering and fruiting plants in the transects’ area. The intensity of the flowering and fruiting phenophases was not uniformly distributed. This study provide us information about the possible fire influence on the reproductive patterns of the community, presenting flowering peaks in October and November, two months after this event. Regression analysis with monthly rainfall also provides us information about the influence of climate data on the flowering and fruiting peaks.


Introduction
The cerrado vegetation, according to the "forestecotone-grassland" concept (Coutinho, 1978), consists of two distinct floras: one of shrubs and trees, predominantly in forest fragments (cerradão), and another of herbs and sub-shrubs, characteristic of grasslands.The savannah physiognomy, the intermediate form (campo sujo and cerrado sensu stricto), is characterised by the occurrence of a mixed flora consisting of forest and grassland elements (Coutinho, 2002).
Studies on the herbaceous layer of cerrado showed the occurrence of modifications in its composition between different regions, demonstrating sensibility to changes in climate, soil, and intensity of fires, among other factors (Batalha and Martins, 2004;Filgueiras, 2002).The strong seasonality of this vegetation type, with rainy summers and dry winters, has been the target of investigations on the phenological pattern of individual species, groups of congeneric species and communities (Mantovani and Martins, 1988;Oliveira, 1998;Miranda, 1995;Gouveia and Felfili, 1998;Munhoz and Felfili, 2005;Silva et al., 2009;Tannus et al., 2006).Mantovani and Martins (1988) demonstrated that an increase in precipitation and temperature correlated positively with the increase in the number of species flowering in the herbaceous and shrub layer.Batalha and Mantovani (2000) reported more autochoric and anemochoric species dispersing in the dry season, while zoochoric species increased during the rainy season when studying differences between dispersal syndromes.
In addition, fire is an important factor causing changes in the floristic composition, physiognomy, structure and phenology reducing the density and height of the vegetation and changing biodiversity (Coutinho, 1977(Coutinho, , 1990;;Sato, 2003).Coutinho (2002) indicated that the occurrence of fires in cerrado dates from 30,000 years ago and the adaptation of the vegetation to fire is related to several factors like the type of fire, the burning regime, frequency, fire intensity and soil temperature (Miranda et al., 2004).
The Urucum plateau, with contrasting vegetation types including semi-deciduous forest to high-altitude campo sujo, has many variables that can influence the phenology of this plant community, such as iron and manganese rich soil, soil humidity and regular fire among others that have not been extensively studied.
The aim of this study was to describe the phenological variations in an area of campo sujo vegetation in the Urucum plateau.We attempted to answer the following questions: 1) What is the phenological pattern of a campo sujo community in the post-fire event period?, 2) Do the observed events correlate with the seasonal rainfall in the area, as proposed in the literature for the herbaceous and sub-shrub layer (Spina et al., 2001;Munhoz and Felfili, 2005)? and 3) Is there phenological variation of the plant species with different dispersal syndromes?

Study site
We conducted this work in the Urucum region, a plateau with about 5,327 ha in Mato Grosso do Sul, which is considered the most prominent plateau of the Pantanal's western edge (Isquierdo, 1997).Among the hills that make up the Urucum plateau, are the Urucum (971 m), the Grande (951 m), the Santa Cruz (1065 m), the São Domingos (800 m), the Tromba dos Macacos (500 m), the Jacadigo (600 m) and the Rabichão with 700 m above sea level (Franco and Pinheiro, 1982).
The region's climate is of the megathermic tropical type (average temperature of 25 °C) with annual rainfall of about 1,120 mm and two distinct seasons, a dry season from April to September (winter) and a rainy season from October to March (summer), classified as Aw in the Köppen system (Soriano, 2000).
The landscape of the region is represented by a mosaic of different types of natural vegetation, according to the variety in the local geology and geomorphology.In the region, there are several vegetation types, such as the cerrado -from campo sujo to cerrado sensu stricto, deciduous forest and semi-deciduous forest (Pott et al., 2000).
The campo sujo vegetation is located covering the top of the hills and characterised by a coverage of grasses, herbs and shrubs with heights ranging between 30 and 40 cm.Species such as Trachypogon spicatus (L.f.) O. Kuntze, Thrasya petrous (Trin.),Aiouea trinervis Meissn.and Qualea cryptantha (Spreng.)Warm.are important for the vegetation coverage (Damasceno Junior et al., 2005).

Phenology
We carried out this study in the Santa Cruz hill (19° 12' S and 57° 35' W), in the city of Corumbá -MS.Sampling began on October 2007, approximately one month after an accidental fire occurred in the study site.
We established eight transects of 250 m, 50 m apart.We sampled all flowering and fruiting species located at least three meters from each side of the transects.Four transects were established on each side of the hill to standardise the data and the whole study area reached 0.6 ha (Figure 1).
We analysed the flowering and fruiting plants within the transect area from October 2007 to September 2008.The criterion for inclusion of species in the phenological analysis was the presence of a flowering or fruiting event during the study period.Mature and immature fruits were considered within the fruiting phenophase.
The vegetation types in this study were divided into herbs, palms, climbers, dwarf plants and sub-shrubs.The dwarf plants are species that, in normal environmental conditions, have the arboreal life-form.However, these species do not develop normally in the campo sujo vegetation within the study area due to the characteristics of the Urucum plateau such as soil (depth, humidity), wind and fire (Lehn et al., 2008).The sub-shrubs form was considered when the plant had secondary growing only at the base, thus not reaching the branches.

Data analysis
We classified the species, with n ≥ 10 individuals, in the categories of the semi-quantitative scale adapted from Fournier (1974) for herbaceous species, which estimates the intensity of each phenological phase using the following scale: 0-absence of characteristic, 1-presence of characteristic in the range from 1-25%, 2-from 26-50%, 3-from 51-75%, 4-from 76-100%.
We executed a regression analysis of monthly rainfall (obtained from the Mineração Corumbaense Reunida S/A company) to the intensity of species in the flowering and fruiting events.We used the Rayleigh test (Zar, 1999) to evaluate whether the species in the study flower and fruit uniformly throughout the year.We also applied the Rayleigh test (Zar, 1999) to assess whether the anemochorous, autochorous and zoochorous species fruit uniformly throughout the year.To test whether the mean of fruiting period for the anemochorous, autochorous and zoochorous species were different, we used the Watson-William test for the three samples (Zar, 1999).
To determine dispersal syndromes, we considered field observations and the scientific literature available for the species (Pott and Pott, 1994;Jardim et al. 2003).Ballistics and barocoric syndromes were grouped into the autochoric category (Van der Pjil, 1972).

Results
Five out of the 53 monitored species had less than 10 individuals in the studied area and therefore were excluded from the calculation of the Fournier intensity.The most representative life-forms of this campo sujo community were dwarf plants with 41.45% individuals, herbs with 32.26% and sub-shrubs with 26.24%.Climbers and palms represented less than 1%.

Flowering
The intensity of the flowering phenophase (Figure 2) was not uniformly distributed (z = 11.87,P < 0.01).The correlation between rainfall and the flowering phenophase was insignificant (r 2 = 0.21, P = 0.49) (Figure 4).The late dry season was the peak period in flowering.

Discussion
Ragusa-Netto and Silva (2007) recorded the flowering peak in August and September while studying a dry forest in the bottom of Santa Cruz hill, near the study site.The flowering peak of campo sujo in the consecutive months can be essential to keep the pollinators in this area.
The fruiting peaks of the dry forest studied by Ragusa-Netto and Silva (2007) were in the middle of the dry season and in the transition between the dry and the rainy season.This last peak was higher and represented by the zoochoric species, such as Protium heptaphyllum March., Guarea guidonia (L.) Sleumer, Pouteria torta Radlk.and Spondias lutea L. Zoochoric species from the high-altitude campo sujo showed the same pattern of nearby forest species (Figure 3) and it happens during the period of greater activity of frugivorous species like small birds.
Janzen (1980) analysed different dispersal syndromes of tropical plants and demonstrated autochoric species flowering in the wet season and fruiting in the dry season.In the campo sujo of the present study, the intensity peak of autochoric species occurred in the late rainy season.This may be due to the fact that 40.29% of the autochoric individuals belonged to the family Fabaceae, which showed flowering peak in the dry season.This pattern must be confirmed with other phenological studies in the Urucum plateau without fire events.
Many herbs and sub-shrubs species in the cerrado have adaptive traits to fire (Coutinho, 1977) such as a soil layer protecting the root system (Coutinho, 1978).These species recover quickly after a fire, synchronising flowering (Sarmiento, 1992).The flowering peaks in October and November, two months after the fire, indicate the adaptation of the studied species.The insignificant difference in the means of the fruiting period was also a consequence of this synchronisation.
Another detectable effect may be the absence of zoochoric species fruiting in the months after the fire since these species are often found fruiting every month of the year (Batalha et al., 1997;Batalha and Mantovani, 2000).Gentry (1982), Morellato and Leitão-Filho (1996) and Talora and Morellato (2000) demonstrated that the proportions of zoochoric species in tropical rainforests were higher than 80%, showing the importance of these species to the maintenance of frugivorous animals.
Grasses in the studied campo sujo did not flower, reducing the percentage of anemochoric individuals in the community.Damasceno-Junior et al. (2005)

Figure 1 .Figure 2 .
Figure 1.Map showing the study site in the Urucum plateau, Corumbá, Mato Grosso do Sul, Brazil and the four transects of 250 m on each side of the hill.Source: Mineração Corumbaense Reunida S/A-2005 IKONOS modified image.

Figure 3 .
Figure 3. Circular histograms of Fournier intensity for the fruiting phenophase in the campo sujo vegetation in the Urucum plateau, Corumbá, Mato Grosso do Sul, and the species classified by dispersal syndromes.Anemochorous (a), Autochorous (b) and Zoochorous (c).

Figure 4 .
Figure 4. Regression between rainfall and the Fournier intensity for the flowering phenophase in the campo sujo vegetation in the Urucum Plateau, Corumbá, Mato Grosso do Sul.

Figure 5 .
Figure 5. Regression between rainfall and the Fournier intensity for the fruiting phenophase in the campo sujo vegetation in the Urucum Plateau, Corumbá, Mato Grosso do Sul.

Table 1 .
Number of individuals from each studied species in the campo sujo vegetation in the Urucum plateau Corumbá, Mato Grosso do Sul, classified according to life-form and dispersal syndrome.

Table 2 .
F values and probability of Watson-Williams test for the dispersal syndromes in a campo sujo vegetation in the Urucum plateau, Mato Grosso do Sul, Brazil.