PHENOLOGY OF URBAN TREE SPECIES IN THE CITY OF TAUBATÉ, SÃO PAULO STATE, BRAZIL Claudia Helena Vitor dos Santos 1, Simey Thury Vieira Fisch 1 2 3

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1 ISSN ON-LINE PHENOLOGY OF URBAN TREE SPECIES IN THE CITY OF TAUBATÉ, SÃO PAULO STATE, BRAZIL Claudia Helena Vitor dos Santos 1, Simey Thury Vieira Fisch ABSTRACT The objective of this study was to characterize the phenological events of tree species in squares and urban parks in the city of Taubaté, São Paulo State, Brazil. Species of pata-de-vaca (Bauhinia longifolia), pau-brasil (Caesalpinia echinata), sibipiruna (Caesalpinia peltophoroides), paineira rosa (Ceiba speciosa), ipê-roxo (Handroanthus impetiginosus), ipê-amarelo (Handroanthus ochraceus), jasmim-manga (Plumeria rubra), ipê-de-jardim (Tecoma stans), quaresmeira (Tibouchina granulosa) and pau-formiga (Triplaris americana) were studied on a monthly basis, counting 240 individuals. The method used to analyze the observations was based on the index of activity. To rate the relation between the elements of climate and the phenophases, we established the Spearman correlation using the BioEstat 5.0 software. The results obtained showed that leaf fall predominated among individuals during the dry season, and the leaf sprouting during the rainy season. The highest index of activity of flowering prevailed in dry and rainy seasons. The dry season and the beginning of the rainy season presented the highest number of individuals bearing fruits; however, this phenophase occurred throughout the year for the species of Tecoma stans and Tibouchina granulosa. We observed that precipitation and temperature exert great influence on the reproductive and vegetative phenological behavior of tree species. Key-words: urban afforestation; phenological events; environmental data. FENOLOGIA DE ESPÉCIES ARBÓREAS EM REGIÃO URBANA, TAUBATÉ, SP RESUMO O objetivo deste estudo foi caracterizar os eventos fenológicos de espécies arbóreas em praças e parques urbanos da cidade de Taubaté-SP. Foram mensalmente acompanhadas as espécies arbóreas pata-de-vaca (Bauhinia longifolia), paubrasil (Caesalpinia echinata), sibipiruna (Caesalpinia peltophoroides), paineira rosa (Ceiba speciosa), ipê-roxo (Handroanthus impetiginosus), ipê-amarelo (Handroanthus ochraceus), jasmim-manga (Plumeria rubra), ipê-de-jardim (Tecoma stans), quaresmeira (Tibouchina granulosa) e pau-formiga (Triplaris americana), contando com 240 indivíduos. O método aplicado para a análise das observações foi o índice de atividade. Na avaliação da relação entre os elementos climáticos e as fenofases foram estabelecidas as correlações de Spearman, as quais foram realizadas através do programa BioEstat 5.0. Os resultados demonstraram que a queda de folhas entre os indivíduos prevaleceu no período da estação seca e o brotamento foliar na estação chuvosa. A floração apresentou maior índice de atividade no início da estação seca e início da estação chuvosa. A estação seca e início da estação chuvosa foi o período com o maior número de indivíduos com frutos, porém esta fenofase ocorreu ao longo de todo ano entre as espécies Tecoma stans e Tibouchina granulosa. Constatou-se que, a precipitação e a temperatura exercem significativa influência sobre o comportamento fenológico vegetativo e reprodutivo das espécies arbóreas. Palavras-chave: Arborização urbana; eventos fenológicos; dados ambientais. 1 UNITAU - Programa de Pós-Graduação em Ciências Ambientais - PPG-CA. claudiahvs@hotmail.com 2 UNITAU - Universidade de Taubaté, Instituto Básico de Biociências - Campus do Bom Conselho - Praça Marcelino Monteiro, 63. CEP: , Taubaté, SP - Brasil, simey.fisch@gmail.com 3 recebido em e aceito para publicação em

2 INTRODUCTION Vegetation cover in the urban environment improves climatic conditions by decreasing the temperature range, evapotranspiration, interference, speed and direction of winds, providing shading, reduction of air, water, sound and visual pollution (SOUZA; CINTRA, 2007). Urban afforestation, when in harmony with the city architecture, reflects its culture and contributes with elements that compose the urban ecosystem biodiversity (LINDENMAIER; SANTOS, 2008). In addition, it contributes with aesthetic beauty and environment quality. It aids in urban development and physical, psychological and emotional balance of the local population (ROCHA et al., 2004). Cyclical biological events of plants and their relationships with environmental conditions, aka phenology, are widely studied. The monitoring of urban trees phenology is carried out by systematic observations of plant lifecycle, including vegetative, such as sprouting and leaf fall, and reproductive phenophases, which correspond to flowering and fruiting (BENCKE; MORELLATO, 2002; PEREIRA et al., 2008). Phenological studies seek to describe standards for biological cycles and, therefore, their immediate causes (biophysical signals caused by temperature, rainfall and solar radiation, for example) and recent causes such as ecological-evolutionary reasons, biotic interactions and phylogenetic relationships (WILLIAMS-LINERA; MEAVE, 2002). Among the immediate causes, climatic changes can influence and regulate phenological events according to their intensity and frequency (FERRAZ et al., 1999). Temperature changes significantly influence tree flowering and the intensity of these changes provide increased plant stature and precede its flowering (CÂMARA et al., 1997). The knowledge about the biological vegetative and reproductive cycles of plants allows a better understanding ecosystem dynamics (GRUBB, 1977), since it provides important data regarding nutrient cycling, pollination and seed dispersal (MORELLATO, 1992). In tropical urban environments, little is known about the phenological patterns of species used in urban afforestation. This type of information is useful for studies on urban ecology (TOLEDO et al., 2011), to support observations of changes in phenological patterns due to climate change (JOCHNER et al., 2013), besides having important applicability to plan maintenance services of the municipality (sweeping, tree pruning, fruit collections, etc.). The seasonal distribution of climate in the city of Taubaté, São Paulo State, Brazil, is characterized by two distinct and well-defined periods, with rainy summers (44% of annual rain) and dry winters (7% of annual rainfall). The wettest month is January (212 mm) and the driest months are July and August (28-30 mm). There are, on average, days with rainfalls in the summer, decreasing to one day in the winter (FISCH, 1999). Information on the phenological patterns of trees used in urban afforestation of Taubaté and the intensity that climatic seasonality influences these events is still nonexistent. This study aimed to characterize the phenological patterns of tree species of urban squares and parks in the city of Taubaté, with the objective to: a) identify the season of leaf fall and sprouting, flowering and fruiting; and b) relate the phenological events with local climate (monthly average values of temperature and precipitation). Claudia Helena Vitor dos Santos e Simey Thury Vieira Fisch 2

3 MATERIAL AND METHODS Study site The study was carried out in the city of Taubaté, São Paulo State, Brazil. Its population amounts to 273,426 people with a demographic density of inhab./km² (IBGE, 2009). The municipality covers an area of km² with 106 km² in the urbanized area. It is located at 580 m above sea level at S and W, near the Capricorn Tropic ( S), which crosses south of Taubaté (PRADO, 2005). The climate in the region is Cwa with rainy summers and dry winters (Köeppen classification). The hottest months are December-February and June and July are the coldest (FISCH, 1999). The hydrologic year starts in August and ends in July in the following year, with 1,335 mm annual precipitation and 42% occurs between December-February (HORIKOSHI; FISCH, 2007). The dry period, days, occurs in the winter (FISCH, 1999). The monitored trees are situated in the Santa Terezinha Square and Dr. Barbosa de Oliveira Square, in municipal parks Jardim das Nações and Monteiro Lobato and in the Horto Florestal of Taubaté (Figure 1). After a previous survey carried out through aerial photographs and in situ visits, these sites were randomly chosen, taking into account the greater number of species and individuals in one place that facilitate the monthly monitoring. Moreover, in these environments, there is low interference of aerial power grid and the practice of pruning is reduced. Figure 1: Study site: Taubaté City, São Paulo State, Brazil, and the location of arboreal individuals in the urban area: 1. Horto Florestal; 2. Dr. Barbosa de Oliveira Square; 3. Santa Terezinha Square; 4. Municipal Park Jardim das Nações; 5. Municipal Park Monteiro Lobato. Source: Google Earth. PHENOLOGY OF URBAN TREE SPECIES IN THE 3

4 Phenological and climatic study The phenological monitoring (vegetative and reproductive), as well as the collection of environmental data (temperature and precipitation), was conducted on a monthly basis from September 2009 to August We selected adult trees that showed evidence of previous reproductive events. The phenological monitoring was carried out using binoculars (10 x 50) and notes arranged in sheets separated by location. The occurrence of reproductive phenophases was evaluated from the direct observation of treetops, registering only the presence or absence of flowers (flower buds and open flowers) and fruit (green fruits, ripe fruits and senescent fruits) (BENCKE; MORELLATO, 2002). For the vegetative phenophases, we used as pattern of leaf change and classified the species as: evergreen with concomitant leaf fall and budding in low intensity throughout the year; semi-deciduous with drop leaf and partial budding; deciduous with total leaf drop and budding, in high intensity, concentrated in a particular time of year (PARKER et al., 2008). The species were also grouped according to the means of seed dispersal based on types of fruits and observations in specialized literature. The phenophase was considered for all individuals and species, regardless of intensity. For the individuals, the phenophase was determined by the presence of at least one of the stages of phenophase in the tree (ex: to consider the individual flowering, at least one flower bud or an open flower was required). In the phenophase for the species, at least one individual of a given species was required to present a certain phenophase (SANTOS, 2007). The method applied for the analysis of observations was the activity index (or percentage of individuals), in which the presence or absence of phenophase in an individual is observed. This index has the quantitative character in population level and allows to estimate the synchrony between the individuals of a population (BENCKE; MORELLATO, 2002). Environmental data (precipitation and temperature) were collected from the meteorological station of the Department of Agrarian Sciences of the University of Taubaté (UNITAU) (23º 02 S and 45º 30 W) located on Fazenda Piloto (Dr. José Luiz Cembranelli road) in the rural area of Taubaté, 5 km from the city commercial center. In this tudy, we considered that the parks and squares were under the same climate conditions of the meteorological data collected. We used monthly average values, which considers weather conditions characteristic for months of the study. In the assessment of the relationship between climatic elements and phenophases, Spearman correlations were established (r s ), which were performed in the program Bioestat 5.0 (AYRES et al., 2009). These evaluations considered significant correlations with values of p<0.05, and non-significant correlations p>0.05 values. RESULTS From September 2009 to August 2011, we monitored 240 individuals (mature trees) comprising seven families, eight genera and 10 species in two squares and three parks in Taubaté City. Of the 10 species studied, three are evergreen, three semideciduous and four deciduous. Regarding seed dispersal, six are anemochory and four autochory (Table 1). Claudia Helena Vitor dos Santos e Simey Thury Vieira Fisch 4

5 Table 1: Tree species monitored from September 2009 to August 2011 in squares and parks in Taubaté City, São Paulo, Brazil. Scientific name Popular name Ocurrence Seed dispersal Leaf fall No. of individuals Apocynaceae Plumeria rubra L. jasmim-manga PST/PRV Autochory Deciduous 7 Bignoniaceae Handroanthus impetiginosus (Mart. Ex DC.) Mattos ipê-roxo PST/PVR/PJN/PML/HF Anemochory Deciduous 42 Handroanthus ochraceus (Cham.) Mattos ipê-amarelo PST/PRV/PJN/PML/HF Anemochory Deciduous 43 Tecoma stans (l.) Juss. Ex Kunth ipê-de-jardim PJN/PML/HF Anemochory Evergreen 19 Fabaceae Bauhinia forficata (Bong.) Steud pata-de-vaca PJN/HF Autochory Semideciduous 17 Caesalpinia echinata Lam pau-brasil PTS/PJN/PML/HF Autochory Semideciduous 32 Caesalpinia peltophoroides Benth sibipiruna PST/PRV/PML Autochory Semideciduous 30 Malvaceae Ceiba speciosa (A. St.-Hil.) Ravenna paineira rosa PST/PRV/PJN/PML Anemochory Deciduous 12 Melastomaceae Tibouchina granulosa (Desr.) Cogn quaresmeira PST/PRV/PML Anemochory Evergreen 19 Polygonaceae Triplaris brasiliensis L. pau-formiga PST/PJN/PML/HF Anemochory Evergreen 19 Legend: PST Santa Terezinha Square; PRV Rodoviária Velha Square; PJN Jardim das Nações Park; PML Monteiro Lobato Park; HF Horto Florestal. During the two years of observation, the months with the highest rainfall, which characterize the rainy season and summer for the region, were December 2009 (267 mm) and March 2011 (206 mm). The months with the lowest precipitation, which characterize the dry season and winter, were August 2010 (0 mm) and July 2011 (1 mm). The average temperature reached 25 C in January 2010 and 2011 and 15 C in June in both years (Figure 2). Leaf fall The leaf fall was pronounced in autumn, with a peak in the month of May, and greater in autumn and winter among the species in general in the two years monitored. Leaf fall began in March, with temperature drop and precipitation decrease and lasted until August (Figure 2). Leaf fall in Bauhinia longifolia and Caesalpinia echinata was not observed in spring 2009 and summer 2010, predominant in other seasons. Leaf fall C. peltophoroides was little expressive in spring and summer. The species Handroanthus impetiginosus, H. ochraceus, Plumeria rubra and Tecoma stans had higher leaf fall in the autumn, extending until the end of the winter. For Tibouchina granulosa leaf fall occurred from autumn 2010 until winter 2011, but showed low activity in February In the individuals of Triplaris americana, leaf fall was observed in summer (Figure 3). Leaf sprouting The leaf sprouting was more intense in spring, with a peak in October 2010 and in summer, with a peak in January It started in September, with the increase of temperature and precipitation, and extended until March (Figure 3). PHENOLOGY OF URBAN TREE SPECIES IN THE 5

6 The production of new leaves in P. rubra and T. stans was greater in the spring of While for C. echinata and B. longifolia, it was more concentrated in spring and summer and in T. americana in both seasons of In T. granulosa, leaf sprouting was continuous; however, more expressive in autumn of For H. impetiginosus, it was expressive in the winter of 2010 and for H. ochraceus, in the spring of both years. We observed that in Ceiba speciosa, leaf sprouting was low during all seasons. Winter was the season with the smallest number of individuals of this species in foliar activity (Figure 3). Legend: Precipitação = Precipitation; Temperatura = Temperature; No. de indivíduos = No. of individuals; Brotamento foliar = Leaf sprouting; Queda de folha = Leaf fall; Floração = flowering; Frutos maduros = ripe fruits; Meses = months; Set = Sept; Nov = Nov; Jan = Jan; Mar = Mar; Mai = May; Jul = Jul Figure 2: Climate and vegetative and reproductive phenology of tree species in Taubaté City, São Paulo State, Brazil, from September 2009 to August 2011: (A) precipitation (mm) and temperature ( C) monthly average, (B) number of individuals in leaf sprouting and leaf fall X temperature; (C) number of individuals in leaf sprouting and leaf fall X precipitation; (D) number of individuals flowering and fruiting X temperature and (E ) number of individuals flowering and fruiting X precipitation. Claudia Helena Vitor dos Santos e Simey Thury Vieira Fisch 6

7 Figure 3: General characterization of the vegetative phenology of the tree species in Taubaté City, São Paulo State, Brazil ( leaf sprouting leaf fall). Flowering The season with the largest number of individuals with the presence of flower buds and open flowers was autumn due to the occurrence of higher synchronism between individuals of the same species, as observed for P. rubra and T. granulosa. The largest number of species showing flower buds was observed in autumn and in spring, with a peak in September. Flowering was observed throughout the year (Figure 4). The species with flower buds and longer flowering periods were B. longifolia, T. stans, P. rubra and T. granulosa. Flowering was more concentrated in H. impetiginosus and H. ochraceus, starting in the fall for both species. The flowering period extended until the end of winter for H. impetiginosus, with a peak in June and ending in early spring; while for H. ochraceus, the PHENOLOGY OF URBAN TREE SPECIES IN THE 7

8 peak was in September. Plumeria rubra and T. granulosa were the species with most synchrony and the least was the C. echinata, which presented only one individual flowering, of thirty-two individuals evaluated throughout the monitoring period. The species B. longifolia, T. stans and T. granulosa had at least one of their individuals flowering during the two years of study (Figure 4). Fruiting The winter had the greatest number of individuals with green fruit, with a peak in August. On the other hand, the summer had fewer species fruiting. The largest number of individuals with ripe fruits was observed in spring 2009 and the largest number was observed in winter 2010, with a peak in August. In spring 2010, we found the largest number of individuals with senescent fruits, with a peak in October, and the number of species with a peak in November (Figure 4). The species with a longer fruiting period were T. stans and T. granulosa. More concentrated fruiting was observed in H. impetiginosus, starting in winter or spring and ending in spring, and in H. ochraceus, starting and finishing in spring. Bauhinia longifolia, T. stans and T. granulosa were the most synchronic species and C. echinata was the least one with only one individual fruiting throughout the observation period (Figure 4). Correlation between environmental variables and phenophases The phenophase leaf fall did not have significant correlation only with precipitation in species H. impetiginosus, H. ochraceus and P. rubra (Table 2). The temperature showed significant correlation with this phenophase in all species (Table 3). The correlation between precipitation and leaf sprouting was significant only in the species B. longifolia, C. echinata, H. ochraceus and T. stans (Table 2). It was also significant with temperature in these species and in C. peltophoroides (Table 3). The correlation between precipitation and flowering was significant for the species B. longifolia, C. speciosa, H. ochraceus, P.rubra and T. stans (Table 2). Regarding temperature, the correlation was significant for C. speciosa, H. impetiginosus, H. ochraceus, P. rubra and T. stans (Table 3). Only the species T. americana showed significant correlation between open flower and precipitation (Table 2). Regarding temperature and open flower, the correlation was significant for individuals of C. speciosa, H. impetiginosus, H. ochraceus, P. rubra and T. stans (Table 3). The correlation between precipitation and open flower was significant in B. longifolia, C. speciosa, H. impetiginosus, P. rubra and T. granulosa (Table 2). Considering temperature, only in T. stans and T. americana there was no significant correlation (Table 3). The phenophase ripe fruit showed significant correlation with precipitation only for individuals of H. ochraceus and P. rubra; and regarding temperature, only in C. speciosa and P. rubra, the correlation was significant (Tables 2 and 3). Some species, such as C. peltophoroides, C. speciosa, T. granulosa and T. americana, showed significant correlation between senescent fruit and precipitation (Table 2). The correlation with temperature was significant for these species and H. ochraceus (Table 3). We observed that temperature exerted greater influence on fruiting than precipitation. By analyzing, for example, the correlation between temperature and phenophase ripe fruit, we observed that only two species, T. stans and T. Americana, did not show significant correlation. Claudia Helena Vitor dos Santos e Simey Thury Vieira Fisch 8

9 Figure 4: General characterization of the reproductive phenology of tree species in Taubaté City, São Paulo, Brazil ( flowering fruiting). PHENOLOGY OF URBAN TREE SPECIES IN THE 9

10 Table 2: Spearman correlation (r s ) between the average monthly precipitation and the phenophases of tree species sampled in squares and parks in Taubaté City, São Paulo State, Brazil, from September 2009 to August Significant positive correlations (p < 0.05) are in bold. Phenophase Leaf fall Sprouting Flower Open Green Ripe Senescent Species bud flower fruit fruit fruit Bauhinia longifolia Caesalpinia echinata _ Caesalpinia peltophoroides Ceiba speciosa Handroanthus impetiginosus Handroanthus ochraceus Plumeria rubra Tecoma stans Tibouchina granulosa Triplaris americana Table 3: Spearman correlation (r s ) between the average monthly temperature and the phenophases of tree species sampled in squares and parks in Taubaté City, São Paul State, Brazil, from September 2009 to August Significant positive correlations (p < 0.05) are in bold. Phenophase Leaf fall Sprouting Flower bud Open flower Green fruit Ripe fruit Senescent fruit Species Bauhinia longifolia Caesalpinia echinata _ Caesalpinia peltophoroides Ceiba speciosa Handroanthus impetiginosus Handroanthus ochraceus Plumeria rubra Tecoma stans Tibouchina granulosa Triplaris americana Table 4: Spearman correlation (r s ) between the average monthly precipitation and temperature of the previous month to each phenophases of tree species sampled in squares and parks in Taubaté City, São Paulo State, Brazil, from September 2009 to August Significant positive correlations (p < 0.05) are in bold. Climatic Elements Phenophase Leaf fall Sproutin g Flower bud Open flower Green fruit Ripe fruit Senescen t fruit Precipitation (mm) Temperature (ºC) Claudia Helena Vitor dos Santos e Simey Thury Vieira Fisch 10

11 DISCUSSION Foliar change In this study, leaf fall was more intense in autumn, extending until the end of winter. Similar to the results obtained by Pereira et al. (2008), for deciduous and semideciduous species studied here, leaf fall was related mainly with the period with less rainfall and the transitional period to the rainy season. The leaf fall is related to, along with pieces of stems, twigs, fruit, and flower buds, to litterfall production, which accumulates on the soil and integrates nutrient cycling (MORELLATO, 1992). In early spring, the temperature rise and constant precipitation, possibly increased availability of soil nutrients, through litterfall decomposition, even if in small levels, as in the case of the urban environment. Some studies show that the seasonality of environmental variables such as temperature and precipitation, which change water and nutritional characteristics of the soil, influences plant physiology and can determine phenological patterns (COSTA et al., 2007; PEREIRA-SILVA et al., 2007; CARDOSO, 2009). The start of rains is considered favorable for most tree species to show high activity of leaf sprouting (WILLIAMS- LINERA;MEAVE, 2002). In the cities in the region of Vale do Paraíba in the São Paulo State, as in the case of Taubaté, sweeping is commonly practiced in squares and parks. This mechanical process hinders the natural cycling of nutrient return via litterfall in these environments. It is essential that the municipal government, along with its departments, create mechanisms that facilitate maintenance, at least in part, of this natural process. In the case of urban parks, leaving part of the litterfall in the environment can mean financial return in the long run, since there will be a considerable reduction of labor force hired for the sweeping services, increased availability of nutrients and moisture in the soil. It addition, litterfall helps control erosion, which is a worrying factor, especially in areas of slopes and banks of rivers and streams. Local residents disagree with the use of semideciduous and deciduous species in urban afforestation as they clog sewers, gutters and drains. Therefore, the use of adequate of tree species in urban tree planting and a program focused on environmental education could possibly reduce social and environmental conflicts and provide a more harmonious and balanced urban environment. In the current study, the semideciduous species, C. peltophoroides is the most troublesome species for the population in Taubaté City, due to the high deposition of small leaves (MINHOTO et al., 2009). On the other hand, in addition to presenting a more exuberant and showy flowering, the deciduous feature of some tree species can be seen as advantageous, since they reduce the limitations of solar incidence to the urban environment in the winter. Flowering and fruiting It is during the reproductive phase that plant species are more subjected to changes of climatic elements, which can determine the future of the next generations (FISCH et al., 2000). In the current study, flowering showed the highest activity index in the transitional seasons (autumn and spring), seasons when the monthly temperature is cooler, around 20 C and rainfall is moderate, around 45 mm/month. According to Ferraz et al. (1999), climate can distinctly PHENOLOGY OF URBAN TREE SPECIES IN THE 11

12 influence the reproductive phenophases of tree species, as observed for Atlantic Forest trees of Paraná State, Brazil (CARDOSO, 2009), where the highest flowering index was observed in autumn and winter. Fruiting, in this study, as observed by Cardoso (2009), had it highest index of activity during the period of low monthly temperature (~16 C) and little precipitation (~19 mm/month), extending until the spring. Ferraz et al. (1999) studied a fragment of the Atlantic Forest in São Paulo State and found that fruit production in some species was related to precipitation and temperature. However, Santos (2007) studied a fragment of Atlantic Forest in Minas Gerais State and found that fruiting was the phenophase less correlated with the weather. The author suggests that the time of occurrence of this phenophase is more related to the most favorable period to seed dispersal than with the abiotic factors directly. For the tree species monitored in this study, six species have anemochoric seed dispersal, meaning that the dry winter facilitates seed dispersal. Pereira et al. (2008) carried out a study in the Atlantic Forest in Rio de Janeiro State and observed the predominance of fruits in periods that preceded the rainy season. The authors also found that the fruit production varied according to the location of the matrix, with more intense fruiting along the roads, where the trees were exposed to more intense light conditions, when compared to individuals located within the forest. The same behavior was observed in the current study, where the production of fruits, preceded the rainy season and varied according to the location of each individual. The trees located in places with higher light incidence, on the borders of sidewalks and streets and with less competition for physical space had higher fruit production during the two years of monitoring, highlighting in this case the environmental influence on expression of the phenophase. The predominance of fruiting in colder and drier periods of the year, even in little seasonal environments such as tropical, has been proposed as a selective action to decrease predation on fruits and seeds, a time of less activity of pathogens and predators (TALORA; MORELATTO, 2000). Thus, seeds can germinate in spring and early summer, when weather conditions are favorable to the development and growth of seedlings, which guarantee reproductive and vegetative success of the species. The occurrence of flowering throughout the seasons shows the rich relationship between organisms in an urban ecosystem, with the availability of resources (nectar and pollen) that promotes harmony between the species as a whole. Toledo (2007) and Toledo et al. (2011) consider that the urban fauna depends on the local vegetation, which allows the dynamics of vegetation succession and promotes seed dispersal and pollination, fundamental factors in ecological processes. Siqueira et al. (2006) emphasize the importance of well-structured vegetation to obtain a dynamic balance among species and ensure increased biodiversity. Studies conducted by Toledo et. al (2011) in the urban area of Taubaté, São Paulo State, showed that biodiversity of birds in urban environments is defined by abundance and diversity of tree species. Another important factor is that the results obtained in this study show the occurrence of synchronicity between flowering individuals of P. rubra and T. granulosa species and fruits between Claudia Helena Vitor dos Santos e Simey Thury Vieira Fisch 12

13 species of B. longifolia, T. stans and T. granulosa. For Santos (2007), these synchronies are important instruments once they generate a continuous supply of resources to frugivores and pollinators, contributing to the maintenance of the population of these animals that are part of the ecosystem. Precipitation, temperature and phenophases Trees connect urban residents with nature. The constant observation of urban afforestation allows to realize environmental changes, since phenophases of trees reflect climate changes of an ecosystem (MORELLATO, 2008). Several authors have conducted studies to detect the relationship between climatic elements and vegetative and reproductive phenology of tree species (CAMARA et al., 1997; FERRAZ et al., 1999; TALORA; MORELLATO, 2000; FISCH et al., 2000; SANTOS, 2007; MORELLATO, 2008; PEREIRA et al., 2008; CARDOSO, 2009). In this study, we found that the climatic elements evaluated, precipitation and temperature, had significant influence on most reproductive and vegetative phenophases of tree species studied. Although temperature showed greater influence on phenological responses of the trees studied, precipitation also influenced every phenophases; however, with less intensity. The seasonal regime of precipitation and temperature variations are closely related to the reproductive patterns of tropical plants, which in turn, provide resources to the fauna, such as nectar, pollen, fruits and seeds (MORELLATO, 2008). The significant correlation between climate and phenology of tree species is a relevant result when we consider the future conditions of climatic scenarios planned for the city of Taubaté. Horlkoshi and Fisch (2007), using data from scenario B2 of SRS/IPCC (Special Report Emissions Scenarios of IPCC Intergovernmental Panel of Climate-Change) for the time interval , concluded that, based on calculations of the climatological water balance in this region, a water deficit will possibly occur (around 50 to 80 mm) as well as a decrease of the water surplus (close to 200 mm). The authors highlight that although precipitation may increase, the water excess will not be sufficient to maintain the levels of evapotranspiration due to air temperature rise. These changes in the precipitation patterns and air temperature may threaten the sustainability of water resources and compromise the quality of social and environmental life in the region. Climate change may significantly influence the physiological and morphological responses of tree species that compose the urban forest in the city of Taubaté and possibly compromise the entire urban ecosystem. Therefore, the use of phenological monitoring of urban trees can be useful to detect the effect of climate changes on the biota as a whole. CONCLUSION Based on the analysis of the characterization of phenological events of tree species, it was possible to conclude that the seasonality of the climatic elements (precipitation and temperature) exerts significant influence on the phenological behavior, reproductive and vegetative, of trees used in urban afforestation in Taubaté. The results showed that the phenological events vary among species and that some of the frequently observed occurrences were related to PHENOLOGY OF URBAN TREE SPECIES IN THE 13

14 the climate of the region. Leaf fall was the predominant phenophase among individuals in autumn, extending until winter, a period when there is a decrease of rainfall and temperatures drop. Leaf sprouting was more intense in spring, when temperatures rose and rains started. Flowering (flower buds and open flowers) showed the highest activity index in the transitional seasons (autumn and spring), a period when rainfall and temperature are milder. Although fruiting occurred throughout the year for some species, the winter and spring were the seasons with the largest number of fruiting individuals, important information for seed harvesting activity and production of new seedlings. Acknowledgments: The authors wish to thank the biology scholars of the University of Taubaté, Kelly Fernandes, by configuring figures and tables, and Tiago Pereira Ribeiro da Gloria for the revision of the English text. REFERENCES AYRES, M.; AYRES JUNIOR, M.; AYRES, D.; SANTOS, A. BioEstat 5.0: Aplicações estatísticas nas áreas de ciências bio-médicas. Sociedade Civil Mamirauá Belém, PA BENCKE, C. S. C.; MORELLATO, L. P. Comparação de dois métodos de avaliação da fenologia de plantas, sua interpretação e representação. Revista Brasileira de Botânica, São Paulo, v. 25, n. 3, p , CAMARA, G. M. S.; SEDIYAMA, T.; DOURADO-NETO, D.; BERNARDES, M. S. Influence of photoperiod and air temperature on the growth, flowering and maturation. Sci. agric., Piracicaba, v. 54, n. Esp., p , CARDOSO, F. C. G. Variações fenológicas de árvores da Floresta Atlântica, em diferentes condições de solo. Curitiba, f. Dissertação (Mestrado em Ecologia e Conservação) - Universidade Federal do Paraná, Curitiba, COSTA, R. F.; SILVA, V. P. R.; RUIVO, M. L. P.; MEIR, P.; COSTA, A. C. L.; MALHI, Y. S. Transpiração em espécie de grande porte na Floresta Nacional de Caxiuanã, Pará. Revista Brasileira de Engenharia Agrícola e Ambiental, Campina Grande, v. 11, n. 2, p , FERRAZ, D. K.; ARTES, R.; MANTOVANI, W.; MAGALHÃES, L. M. Fenologia de árvores em fragmento de mata em São Paulo, SP. Revista Brasileira de Biologia, São Carlos, v. 59, n. 2, p , FISCH, G. Distribuição da precipitação em Taubaté, Vale do Paraíba (SP). Revista Biociência, Taubaté, v. 5, n. 2, p. 7-11, FISCH, S. T. V.; NOGUEIRA JR, L. R.; MANTOVANI, W. Fenologia reprodutiva de Euterpe edulis Mart. Na Mata Atlântica (Reserva Ecológica do Trabiju, Pindamonhangaba-SP). Revista Biociência, Taubaté, v. 6, n. 2, p , Claudia Helena Vitor dos Santos e Simey Thury Vieira Fisch 14

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