FLORISTIC AND ECOLOGY OF ORCHIDACEAE IN SEMIDECIDUOUS SEASONAL FOREST FRAGMENT IN ARARAS, SÃO PAULO, BRAZIL

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1 Revista em Agronegócio e Meio Ambiente, Maringá (PR) DOI: FLORISTIC AND ECOLOGY OF ORCHIDACEAE IN SEMIDECIDUOUS SEASONAL FOREST FRAGMENT IN ARARAS, SÃO PAULO, BRAZIL Cristiano Pedroso de Moraes * Thiago Souza-Leal ** Marcela Marques da Silva Favetta *** Janiere Regina Sommer **** Ligia Eleonor Prezzi ***** Thiago Fernandes Canonici ****** Olavo Raymundo Junior ******* ABSTRACT: The neotropical riparian forests are widely studied, but there are little informations about orchids in phytophisiognomies. The aim of this study was to characterize the floristic composition, and ecological relationship and categories related to habitat of Orchidaceae family representatives in riparian forest in Semideciduous Seasonal Forest fragment in Araras, SP. By the demarcation of 20 plots of 20 X 10 m (400 m 2 ) parallel to the local water body, it was sampled 10 genera and 12 species: Baptistonia cornigera, Campylocentrum grisebachii, Campylocentrum robustum, Capanemia micromera, Catasetum fimbriatum, Cattleya loddigesii, Oeceoclades maculata, Pleurothallis miniato-lineolata, Polystachya estrellensis, Sacoila lanceolata and Lophiaris pumila. The existing populations of orchids in the study area decreased due to anthropogenic disturbance, resulting in the current low diversity. High densities presented by some species, chiefly L. pumila, make it clear the processes of recolonization related to adaptative mechanisms and to the current conservation status of the fragment. KEY WORDS: Orchids, Phytogeography, Taxonomy. * Docente Doutor em Biologia Vegetal; Docente no Centro Universitário Hermínio Ometto (UNIARARAS), Araras (SP), Brasil; pedroso@uniararas.br ** Mestrando do Departamento de Botânica, IB (Unesp), Rio Claro (SP), Brasil. *** Mestranda em Agroecologia e Desenvolvimento Rural pela Universidade Federal de São Carlos (UFSCAR), Brasil. **** Discente de Iniciação Científica do Centro Universitário Hermínio Ometto UNIARARAS), Araras (SP), Brasil ***** Mestranda em Engenharia de Alimentos. ****** Discente de Iniciação Científica do Centro Universitário Hermínio Ometto UNIARARAS), Araras (SP), Brasil. ******* Pró-Reitor de Graduação do Centro Universitário Hermínio Ometto UNIARARAS), Araras (SP), Brasil.

2 666 Floristic and ecology of orchidaceae in semideciduous seasonal forest fragment in Araras... FLORÍSTICA E ECOLOGIA DE ORCHIDACEAE EM FRAGMENTO FLORESTAL ESTACIONAL SEMIDECIDUAL DE ARARAS, SÃO PAULO, BRASIL RESUMO: Os bosques ribeirinhos neotropicais são amplamente estudados, entretanto, existem poucas informações a respeito de orquídeas nestas fitofisionomias. O objetivo deste trabalho foi caracterizar a composição florística, a relação ecológica e categorias relacionadas com o habitat dos representantes da família Orchidaceae em fragmento Florestal Estacional Semidecidual ribeirinho em Araras (SP). Pela demarcação de 20 parcelas de 20 x 10 m (400 m 2 ) paralelas ao corpo d água local, foram amostrados 10 gêneros e 12 espécies: Baptistonia cornigera, Campylocentrum grisebachii, Campylocentrum robustum, Capanemia micromera, Catasetum fimbriatum, Cattleya loddigesii, Oeceoclades maculata, Pleurothallis miniato-lineolata, Polystachya estrellensis, Sacoila lanceolata e Lophiaris pumila. As populações de orquídeas existentes na área de estudo se reduziram devido à perturbação antropogênica, que resultou na baixa diversidade atual. As altas densidades apresentadas por algumas espécies, principalmente L. pumila, demonstram processos de recolonização relacionados com os mecanismos adaptativos e o estado de conservação atual do fragmento. PALAVRAS-CHAVE: Fitogeografia; Orquídeas; Taxonomia. INTRODUCTION The forest fragmentation modifies the structure of the fragments and the processes of interaction with other elements of the landscape and is due mainly to anthropogenic action, especially for agriculture and urbanization. The evolution of land occupation in tropical region bequeathed a fragmented forest landscape, and, in the case of South and Southeast of Brazil, this chart is even more worrying (VIANA et al., 1992; 1997). The municipality of Araras, São Paulo State, currently occupies a conspicuous position in the production of sugar cane, and this monoculture is the main agricultural activity in the region. However, throughout the deployment and growth of this activity, it became necessary the expansion of agricultural borders, in

3 Moraes, Souza-Leal, Favetta, Sommer, Prezzi, Canonici e Raymundo Junior 667 order to increase the production to meet the growing demand. Thus, changes made in the natural landscape resulted in its fragmentation (RAYMUNDO JUNIOR et al., 2008). Data collected in 1962 and 2000 show a considerable reduction in the fragments of the city, either in quantity or in occupied area, worrying factor for the conservation of the diversity of wildlife, local flora and for the maintenance of important environmental resources such as water (FADEL et al., 2008). Nowadays, the city counts on few remaining forest areas in terms of space, which represent only 4.8% of its territory (SÃO PAULO, 2006). The main factors affecting the dynamics of forest fragments are: size, shape, insulation, type of neighborhood and disturbance history (VIANA et al., 1992). These factors have relation with the biological phenomena that affect the birth rate and mortality of plants (VIANA; PINHEIRO, 1998), especially those that provide more complex ecological relationships, among which, there are the orchids. These plants take in primary forests, specialized niches, which gives the excellent condition of environmental bioindicators, because they are sensitive to anthropogenic interference (ZOTZ; ANDRADE, 2002), unable, in most cases, to settle in areas that suffered disturbance (BAWA, 1992). Such a fact is verified in the natural reminiscent state of Sao Paulo, where the abundance and diversity of this family have low rates (DISLICH; MANTOVANI, 1998; PEDROSO-DE-MORAES et al., 2010, SCHUSTER et al., 2010). It is noteworthy that the abundance and diversity of orchids are strongly influenced by changes in the ecological conditions along altitudinal, latitudinal and continental gradients, and the distribution of rainfall throughout the year, combined with changes in temperatures, important phenomena to the success of these plants (GENTRY; DODSON, 1987a, b). The Orchidaceae family is composed of approximately 780 genera and 20,000 species of epiphytic plants, lithophytes or terrestrial, constituting one of the largest and most derived families of angiosperms (SOLTIS et al., 2005; PRIDGEON et al., 2009), being studied in various regions of the world (BUDOWSKI, 1965; BENZING, 1990, 1993; ZIMMERMAN; OLMESTD, 1992; PINTO et al., 1995; BARTHLOT et al., 2001, SOLTIS et al., 2005; KUMAR et al., 2007; JALAL et al., 2008; PRIDGEON

4 668 Floristic and ecology of orchidaceae in semideciduous seasonal forest fragment in Araras... et al., 2009). In Brazil, were described about 200 genera and 2,500 species, with predominance of small, inconspicuous flowers (COGNIAUX, 1896; 1902; 1906; BARROS, 1990; DRESSLER, 2005; SOUZA; LORENZI, 2005; CAMPOS, 2008). For Brazil, the various studies are reported about this family, which are directed to the knowledge of the floristic composition and community structure (DISLICH; MANTOVANI, 1998; KERSTEN; SILVA, 2001; ROGALSKI; ZANIN, 2003; MENINI NETO et al., 2004a, b; BUZZATO et al., 2007; CERVI; BORGO, 2007; BRUSTULIN; SCHMITT, 2008; DETTKE et al., 2008; BATAGHIN et al., 2010). However, despite the vast literature aforesaid, work in different regions become necessary, given the current high level of endemism observed, the result of fragmentation, which leads to isolation and gradual reduction of species diversity combined with floristic and climatic differences in each area (RIZZINI, 1997). The present work had as an aim to determine the floristic composition and ecology of the Orchidaceae family in riparian forest which includes the largest fragment of Semideciduous Seasonal Forest in the municipality of Araras, São Paulo, thus contributing to the floristic and phytogeographic knowledge of regional forest formation. 2 MATERIAL AND METHODS 2.1 STUDY AREA The study was conducted from March 2010 to March 2011 in the largest municipal forest fragment, belonging to the Nova Santa Cruz farm, Araras, SP, located at coordinates S, O. The property has 388 hectares, with 97 of these, covered with a remnant of Semideciduous Seasonal Forest (Figure 1). The remaining area is occupied by pastures and crops of Citrus and sugar cane. The climate of the area corresponds, according to the classification of Köeppen, to the Cwa; that is, mesothermal with a dry winter in which the average temperature of the coldest month is below 18ºC and the warmest month of 22 C. The total rainfall in the driest month does not exceed 30 mm. The temperature of the warmest month varies between 22ºC and 14 C, with the annual average temperature around 21ºC (MAGINI; CHAGAS, 2003).

5 Moraes, Souza-Leal, Favetta, Sommer, Prezzi, Canonici e Raymundo Junior PROCEDURE For the floristic and ecological survey of Orchidaceae family, was used the methodology described by Clements (1929) and adapted by Dislich and Mantovani (1998), being demarcated 20 plots of 20 X 10 m, totalizing 4000 m 2 (0.4 ha) (Figure 1). The orchid species found were recorded and the material was herborized, as usual procedures (MORI et al., 1989). Plants that had a single individual had their last pseudobulbs and inflorescences collected for herborization. Figure 1. Thematic map and location of plots in the fragment of Semideciduous Seasonal Forest from Nova Santa Cruz farm, Araras, SP.

6 670 Floristic and ecology of orchidaceae in semideciduous seasonal forest fragment in Araras... The vouchers were tumbled in the collection of the Herbarium Rio Clarense (HRCB), from Institute of Biosciences, Universidade Estadual Paulista - UNESP, Rio Claro. The identification was by consulting the works of Rodrigues (1877; 1882), Cogniaux (1896; 1902; 1906), Hoehne (1940; 1942; 1945; 1949; 1953), Pabst and Dungs (1975; 1977), Sprunger et al. (1996) and the species names were checked on Kewensis Index on line (2013) and the site of the Missouri Botanical Garden W3Trópicos - MOBOT (2013) using the abbreviations for the authors suggested in Brummitt and Powell (1992). The species were classified into ecological categories, in relation to the substrate: terrestrial (TER), holoepiphytes (HOL) and hemi-epiphytes (HEM). It was also recorded for each species its position in the phorophyte, in the following adapted categories of Tersteege and Cornelissen (1989): the lower half of the stem (LHS), the upper half of the stem (UHS), primary branches (PRB), intermediate branches (INB) and external branches (EXB). From the count of individuals ecological parameters were calculated: absolute and relative density, absolute and relative frequency (MATTEUCCI; COLMA, 1982), importance value index (IVI) for epiphytic species (WAECHTER, 1998) and terrestrial. 3 RESULTS AND DISCUSSION This study identified 11 species of orchids, distributed in 10 genera (Table 1). Nine representatives of the family presented themselves as holoepiphytes while two were ecologically classified as terrestrial (Table 2).

7 Moraes, Souza-Leal, Favetta, Sommer, Prezzi, Canonici e Raymundo Junior 671 Table 1. Ecological parameters to orchids of the riparian forest from the forest fragment from Nova Santa Cruz Farm. Species, absolute densities (D), absolute frequency (AF - being adopted the following criteria: very abundant > 50% abundant 50-30%, not so abundant 30-10% and rare < 10%), importance value index (IVI). Registration number in Herbarium (N o. HRCB) Species D AF IVI N o. (%) (%) HRCB Baptistonia cornigera (Lindl). Chiron & V.P. Castro Campylocentrum grisebachii Cogn Campylocentrum robustum Cogn Capanemia micromera Barb. Rodr Catasetum fimbriatum (Morren) Lindl Cattleya loddigesii Lindl Oeceoclades maculata Lindl Pleurothallis miniatolineolata Hoehne Polystachya estrellensis Rchb.f Sacoila lanceolata (Aubl.) Garay Lophiaris pumila (Lindl.) Braem Table 2. Species and position of epiphytic orchids in the phorophyte in the riparian forest of the forest fragment of the Nova Santa Cruz Farm. Lower half of the stem (LHS), the upper half of the stem (UHS), primary branches (PRB), intermediate branches (INB) external branches (EXB) Species Vertical Distribution (holoepiphytes) LHS UHS PRB INB Baptistonia cornigera (Lindl.) Chiron & V.P. Castro X X X Campylocentrum grisebachii Cogn. X Campylocentrum robustum Cogn. X X X Capanemia micromera Barb. Rodr. X Catasetum fimbriatum (Morren) Lindl. X X Cattleya loddigesii Lindl. X Pleurothallis miniato-lineolata Hoehne X Polystachya estrellensis Rchb.f. X X Lophiaris pumila (Lindl.) Braem X X X

8 672 Floristic and ecology of orchidaceae in semideciduous seasonal forest fragment in Araras... The epiphytic species with the highest number of individuals were respectively: Baptistonia cornigera (Lindl). Chiron & V.P. Castro, Campylocentrum robustum Cogn., Pleurothallis miniatolineolata Hoehne and TLophiaris pumila (Lindl.) Braem (Table 1). The low number of species obtained is related to the history of occupation, once the study area is in the middle of the crop of Citrus sp., generating a high degree of impaction, which causes a reduction in the number and abundance of orchids (BUDOWSKI, 1965; PINTO et al., 1995; BARTHLOT et al., 2001; PEDROSO-DE- MORAES et al., 2010), corroborating with data found in other studies conducted in areas of Semideciduous Seasonal Forest, likes Dislich and Mantovani (1998), where six species were identified, Brustulin and Schmitt (2008), with seven, Dettke et al. (2008), with three and Bataghin et al. (2008), with two. However, when compared to studies in the best preserved areas, such as those carried out by Rogalski and Zanin (2003), Menini Neto et al. (2004a), Buzzato et al. (2007) and Cervi and Borgo (2007), who found 38, 44, 50 and 21 species, respectively, the diversity found was low, even with constant local humidity, due to the nearby riparian area, a feature that provides a greater abundance of orchids (GENTRY; DODSON, 1987b). Among the plants recorded Cattleya loddigesii Lindl. (Table 1) is in the list of endangered species (BAPTISTA; LONGHI-WAGNER, 1998), this fact is due to the species be highly targeted by predators because of their ornamental appeal, justifying, possibly, the presence of only one individual in the fragment. With respect to vertical distribution, the largest number of species is found in the lower halves (LHS), upper stem (UHS) and primary branches (PRB) (Table 2), a factor attributed to better quality and availability of substrate (horizontal branches and accumulation of organic matter) for the establishment of epiphytic species (SCHUTZ-GATTI, 2000). Species that grow in the lower half of the stem (LHS) are those that require more moist and shady environments because they require environmental conditions similar to those found in the soil (ROGALSKI; ZANIN, 2003). Epiphytes that occur in the upper half of the stem (UHS), as Catlleya loddigesii (Table 2) and that have adaptations to withstand drought (presence of pseudobulbs and coriaceous leaves), tolerate higher light intensities (MORAES; ALMEIDA, 2004). There were no species occurring in external branches (EXB), which was also found

9 Moraes, Souza-Leal, Favetta, Sommer, Prezzi, Canonici e Raymundo Junior 673 in the studies of Rogalski and Zanin (2003), which can be attributed to the difficulty of establishment of epiphytic species due to mechanical and spatial issues, arising from the recent development of the branches, since the time when the substrate is available influences the colonization of epiphytic ( YEATON; GOLDSTONE, 1982). Most of the species is not restricted to a single vertical position (Table 2). This fact is due to the density and moisture of the photon flux (BENZING, 1995) occurring due to the variation in height of phorophyte and forest stratification (RO- GALSKI; ZANIN, 2003). Among the species, those which varied their vertical positions were Baptistonia cornigera, Campylocentrum robustum and Lophiaris pumila, demonstrating to be adapted to the area for presenting bigger populations (Table 1). Polystachya estrellensis, stands out to appear more frequently in secondary forest and on isolated trees, with more suberose and dry cortex (HOEHNE, 1949). According to Barros (1993) Polystachya estrellensis and Trichocentrum pumilum are the first species of orchids to recolonize anthropically disturbed environments by being able to settle quickly into secondary forests. The wide dispersion of terrestrial specie Oeceoclades maculata (Table 1), Can be attributed to their highly developed mechanism of autogamy, in which the flowers give rise to fruit with anemochoric seeds, which, in turn, are easily dispersed (GONZALEZ-DIAZ; ACKERMAN, 1988; PEDROSO-DE-MORAES et al., 2010). Such species has the potential to be used as a bioindicator, it is possessed of enormous capacity for colonization of habitats, especially, the anthropogenic (COHEN; AC- KERMAN, 2009). Regarding Sacoila lanceolata, anthropogenic disturbances occurred in the past of the study area, possibly, resulted in the lowest occurrence in the area (Table 1), since their populations tend to be eugenic due to the large amount of apomictic monoembryonic seeds developed by the species during its breeding (BROWN, 2008). The low populations found to Campylocentrum grisebach, Capanemia micromera, Catasetum fimbriatum, Cattleya loddigesii, Polystachya estrellensis and Sacoila lanceolata (Table 1), indicate a high susceptibility to local extinction in the fragment in case of death or indiscriminate collection of individuals.

10 674 Floristic and ecology of orchidaceae in semideciduous seasonal forest fragment in Araras... 4 CONCLUSION The populations of orchids existent in the study area suffered declination due to anthropogenic disturbance, resulting in low diversity nowadays. High densities presented by some species, especially Lophiaris pumila, evidence of recolonization processes related to adaptation mechanisms and the current condition of conservation of the fragment. 5 ACKNOWLEDGEMENTS The authors thank the owners of Nova Santa Cruz farm, who kindly allowed this work on their property and Herminio Ometto Foundation UNIARARAS (NU- CIA-UNIARARAS) by fomentation. REFERENCES BAPTISTA, L.R.M.; LONGHI-WAGNER, H. M. Lista preliminar de espécies ameaçadas da flora do Rio Grande do Sul. Porto Alegre: Sociedade Botânica do Brasil BARROS, F. Diversidade taxonômica e distribuição geográfica das Orchidaceae brasileiras. Acta Botanica Brasilica, v. 4, p , BARROS, F. Flora Fanerogâmica da Reserva do Parque Estadual das Fontes do Ipiranga (São Paulo, Brasil): 198 Orchidaceae. Hoehnea, v. 10, p , BARTHLOT, W.; SCHMIT-NEUERBURG, V.; NIEDER, J.; ENGWALD, S. Diversity and abundance of vascular epiphytes: a composition of secondary vegetation and primary montane rain forest in the Venezuelan Andes. Plant Ecolog y, v. 152, p , 2001.

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17 Moraes, Souza-Leal, Favetta, Sommer, Prezzi, Canonici e Raymundo Junior 681 bash Trees (Crescentia alata HBK) in Guanascate Province, Costa Rica, Biotropica, v. 14, p , ZIMMERMAN, J. K.; OLMESTD, I. C. Host tree utilization by vascular epiphytes in a seasonally inundated forest (Tintal) in Mexico. Biotropica, p. 24, p , ZOTZ, G.; ANDRADE, J. L. La ecología y la fisiología de las epifitas y las hemiepífitas. In: GUARIGUATA, M.; CATAN, G. (Ed.) Ecología y conservación de bosques neotropicales. San José: Libro Universitario Regional, p Recebido em: 05 de setembro de 2013 Aceito em: 21 de fevereiro de 2014