Brazilian Journal of Ecology ISSN 1516-5868 BRAZILIAN JOURNAL OF ECOLOGY REVISTA BRASILEIRA DE ECOLOGIA Publication of the Ecology Society of Brazil Editores: Dra Edisa F. I. Nascimento Dra Carla Soraia Soares de Castro ASSESSOR BOARD Antonio Domingos Brescovit Bruno Pastrelli Kamada Cássia Beatriz R. Munhoz Claudio de Moura Cristiane Elizabeth Macedo Elaine Folly Evelise Márcia Locatelli Fabrício Carvalho Flávia Souza Rocha Francisco Eduardo Silva Pinto Vilela Frederico Alexandre Roccia Dal Pozzo Arzolla Geraldo Ceni Coelho Gláucia Cortez Ramos de Paula Helena França Ingo Isernhagen Jairo José Zocche Josué Raizer Marcelo Dutra da Silva Márcio Seiji Suganuma Maria Iracema Bezerra Loiola Maria Santina de Castro Morini Marina Janzantti Lapenta Milton Cezar Ribeiro Natalia Ghilardi Lopes Ricardo Augusto Lombello Vladimir Stolzenberg Torres Yumi Oki Zelma Glebya Maciel Quirino Mailing Adress Departamento de Ecologia Rua do Matão, Travessa 14 no. 321. CEP.: 05508-900. Cidade Universitária – São Paulo, SP. Phone: (11) 3091 7600 e-mail: contato@seb-ecologia.org.br site: www.seb-ecologia.org.br 1 Revista SEB Ano 14 Final.indd 1 09/10/2012 13:43:51 Brazilian Journal of Ecology ISSN 1516-5868 FICHA CATOLOGRÁFICA Brazilian Journal of Ecology Revista Brasileira de Ecologia Vol. 01 Ano 14 – 2012 São Paulo, SP. Ecology Society of Brazil (Sociedade de Ecologia do Brasil). V/:il; 27cm Anual 2010 – 2012, 1 II. Ecologia I. Sociedade de Ecologia do Brasil 2 Revista SEB Ano 14 Final.indd 2 09/10/2012 13:43:51 Brazilian Journal of Ecology ISSN 1516-5868 BRAZILIAN JOURNAL OF ECOLOGY A publication on the ECOLOGY SOCIETY OF BRAZIL SOCIEDADE DE ECOLOGIA DO BRASIL BOARD PRESIDENT Dra Edisa Ferreira Inocêncio Nascimento - IB/USP, VICE PRESIDENT Dr. Welington Braz Carvalho Delitti - IB/USP 1st SECRETARY Dr.Wladimir Stolzenberg Torres - SMPA 2st SECRETARY Dr. Júlio Cesar Voltolini – UNITAU 1ST TREASURER Dra. Tatiana Pavão -CUSC 2ST TREASURER Dra. Karla Conceição Pereira - APTA/SP 3 Revista SEB Ano 14 Final.indd 3 09/10/2012 13:43:51 Brazilian Journal of Ecology ISSN 1516-5868 CONSELHO FISCAL Dra. Marisa Domingos, Brasileira IBt/SP Dr. Marcelo Dutra da Silva – FURG Dr. Demétrio Luis Guadagini - FSM Dra. Ana Tereza Araujo Rodarte – UFS Dra. Regina Celi Costa Luizão - INPA CONSELHO CONSULTIVO Dra. Carla Soraia Soares de Castro – UFPB Dr. Frederico de Siqueira Neves – UFMG Dr. José Luiz Campana Camargo – INPA Dra. Marisa Dantas Bittencourt IB/USP Dr. Geraldo Ceni Coelho – UFFS Dr. Philip Martin Fearnside - INPA Sociedade de Ecologia do Brasil Departamento de Ecologia - Instituto de Biociências Universidade de São Paulo Rua do Matão Travessa 14 no. 321. CEP 05508-900 Phone: (11) 3091-7600 – Cidade Universitária e-mail: contato@seb-ecologia.org.br site: www.seb-ecologia.org.br 4 Revista SEB Ano 14 Final.indd 4 09/10/2012 13:43:51 Brazilian Journal of Ecology ISSN 1516-5868 RAZILIAN JOURNAL OF ECOLOGY REVISTA BRASILEIRA DE ECOLOGIA Volune 1 – Ano 14 - 2012 5 Revista SEB Ano 14 Final.indd 5 09/10/2012 13:43:51 Brazilian Journal of Ecology ISSN 1516-5868 6 Revista SEB Ano 14 Final.indd 6 09/10/2012 13:43:52 Brazilian Journal of Ecology ISSN 1516-5868 Evaluation of aboveground growth and biomass in Glicine max plants exposed to various concentrations of copper *Karina Gonçalves – Undergraduate student of the Faculty of Biology, Directorate of Health, University Nove de Julho (email: kazinhavgt@yahoo.com.br) Marli Sá Torres- Undergaduate student of the Faculty of Biology, Directorate of Health, University Nove de Julho (email: satorpp@ig.com.br ) Patrícia Marinho – Undergaduate student of the Faculty of Biology, Directorate of Health, University Nove de Julho (email: patinalda@hotmail.com) Juliana de Mello Botelho – Undergraduate student of the Faculty of Biology, Directorate of Health, University Nove de Julho (email: ju_melbo@hotmail.com) Armando Reis Tavares – Researcher of the Nucleus of Research on Ornamental Plants of the Botanical Institute of São Paulo (email: atavares2005@yahoo.com.br) Shoey Kanashiro – Researcher of the Nucleus of Research on Ornamental Plants of the Botanical Institute of São Paulo (email: skanashi@uol.com.br) Ana Paula N. Lamano Ferreira – Professor Doctor in Ecology of the Faculty of Biology, Directorate of Health, University ‘Nove de Julho’ (email: apbnasci@yahoo.com.br) Luis Alberto Valotta - Professor Doctor of the Faculty of Biology, Directorate of Health, University ‘Nove de Julho’ (email: lavalotta@yahoo.com) Cleber da Silva Costa – Full Professor of the Faculty of Biology, Directorate of Health, University ‘Nove de Julho’ (email: costacs@uninove.br) Rafael Souza Queiroz – Full Professor of the Faculty of Biology, Directorate of Health, University ‘Nove de Julho’ (email: rs.queiroz@gmail.com) Hilton Lourenço Ozório Filho - Full Professor of the Faculty of Biology, Directorate of Health, University ‘Nove de Julho’ (email: ozoriofi@uninove.br) Maurício Lamano Ferreira – Doctorate student in Ecology in the Center of Nuclear Energy in Agriculture of the Unversity of São Paulo (CENA/USP) and Professor of the Faculty of Biology, Directorate of Health, University ‘Nove de Julho’ (email: mauecologia@yahoo.com.br) ABSTRACT Soybean (Glycine max) represents a plant-species of considerable economical importance for Brazil, considered one of the main producers worldwide. The aim here was to analyze the influence of copper on the development of the plant’s aboveground growth and biomass. With this in mind, an experiment was developed under natural conditions of humidity and temperature using 112 plants cultivated in vases with sand. The randomized block design was adopted, with each containing four blocks, seven treatments and four repetitions, all irrigated for 30 days with a solution of Hoagland & Arnon, enriched with various concentrations of CuCl2. Subsequent variance analysis and Tukey testing showed that plants undergoing treatment with 0,9 g CuCl2 L-1 (T6) 7 Revista SEB Ano 14 Final.indd 7 09/10/2012 13:43:52 Brazilian Journal of Ecology ISSN 1516-5868 were those that presented the least growth in relation to both control plants and those under lower-grade treatments. The values of stem-dry-mass were equivalent to the tendencies encountered in biometrics, whereby the conclusion that copper at high concentrations can exert an influence on growth in Glycine max plants. Keywords: Soybean, plant biometrics, aerial organs, copper INTRODUCTION In general, micronutrients, even though required in reduced amounts, are essential for completion of the plant vegetative cycle. Their deficiency, besides inducing reduced productivity and alterations in the defense system, may even interfere in phenology (7). Among such nutrients, copper is outstanding by being an important cofactor in anti-oxidizing enzymes, as, for example, the activator of some of the enzymes involved in oxidation and reduction, besides participating in the opening and closing of stomata and lignification in some cells (3). Through its involvement in several physiological and structural aspects in plant development, copper, in certain concentrations, can serve as manure, the lack thereof possibly giving rise to damage to the plant in various forms. Some of the main symptoms of copper deficiency can be observed in young leaves, which, besides very often presenting necrotic patches, become dark green in color, rolled up and deformed. Worthy of note, copper deficient plants can manifest lower protein synthesis and diminished photosynthetic activity, through this nutrient being an activator of those enzymes which participate in terminal electronic transport in respiration and photosynthesis. These symptoms of deficiency occur in newer tissues, due to their lower mobility in the plant (18). A good example is a study by Zampieri (2010), comprising an analysis of the effects of copper and zinc on Aechmea blanchetiana (Baker) L.B. Smith, whereby it was demonstrated that seedlings cultivated under high concentrations of Cu++ were those that presented the highest structural variation in morphometric and anatomic parameters. In studies by Silva et al. (2010) on the tolerance of certain Cassia species (Peltophorum dubium) seedlings in soils with an excess of copper, it was observed that, inversely to the increase in dose, there was a decrease in plant biometric parameters, such as height and diameter. Only required in small amounts in cultures, copper is one of the ultimate nutrients whereby symptoms of deficiency develop, when supply does not attend to plant requirements. Generally occurring at very low rates in the soil, its dynamics is very much affected by soil characteristics. Thus, besides pH and humidity, and apart from the plant itself, the degree of organic material and mineral and biological fractions in the soil, are factors that condition its availability and utilization by the plant, insofar as they interfere in the reactions, thereby giving rise to the formation of products of greater or lesser solubility (3).The normal concentration of this metal in the soil is 20mg kg-1, with variations to the rate of 6 to 80mg kg-1 (20,11). Another decisive factor in the activity of copper is the inner of a soil for the capacity cationic change (CTC). CTC is intimately linked to both the concentrations of changeable ions present in the solution of the soil, and the sites of changes on the colloidal intersurfaces of the system. High CTC facilitates greater retention of the metal. Organic material, even though representing only around 5% of soil components, is responsible for about 30% to 65% of the CTC in mineral soils, and for more than 50% in sandy and organic ones (10, 20). Besides its natural distribution in the soil, copper can be further obtained in several other ways, such as by means of defensive chemicals, agricultural fertilizers, and more recently, through the widespread use of domestic and industrial residues. Emphasis must be given to the use of sewage sludge obtained in treatment stations, a mode which nowadays has been extensively adopted in several monocultures. Nevertheless, caution should be taken, for when in large concentrations, copper can induce toxic effects to plant tissue 8 Revista SEB Ano 14 Final.indd 8 09/10/2012 13:43:52 Brazilian Journal of Ecology ISSN 1516-5868 and cause a deficiency in other essential nutrients through adverse interactions (8). Urban residues, for example, through normally presenting high rates of heavy metals, when compared to those present in the soil, are liable to inducing toxicity or altering availability in certain agroecosystems (13). Furthermore, through possible absorption by plants, there is the possibility of their entering the food chains (14). When in excess, the accumulation of copper in different parts of the plant can always be associated to cellular alteration in various forms, thereby interfering in physiological processes, to the point that, the toxicity so caused can eventually lead to oxidative stress, chlorophyll derangement and effects on Fe translocation, among others (9). According to Sfredo (2008), over the latter years, leaf analysis has been applied to evaluating the availability of limitative nutrients for plants, thereby furnishing a new tool for improving recommendations as regards manure application, as a further means for increasing productivity. The agricultural use of organic residues is only plausible, when there are no high inner concentrations of Cd, Pb, Cu, Cr, Ni and Zn, since these metals are prone to absorption by plant roots, with the subsequent transference to various organs (3), and consequently, into foodstuff for human consumption. For the satisfactory development of a culture of the soybean Glycine max (L.), a grain of extreme importance in the Brazilian economy, it is essential that macro- and micronutrients be present in the appropriate concentrations. OBJECTIVES The aim of this study was to analyze the aboveground growth and biomass of Glycine max (L.), under different copper treatments and natural conditions of temperature and humidity. METHODOLOGY Study area The experiment took place in an open area for experiments of the University ‘Nove de Julho’, located in metropolitan São Paulo. São Paulo, in southeast Brazil, is located at around 770 meters above sea level, within the coordinates 23º30’S and 46º40’W. Characteristically, winters (from June to August) are dry, and summers (from December to March) humid. Plant exposure During the experiment, the plants were individually irrigated weekly with 50 ml of a Hoagland & Arnon solution contaminated with 0,0 (T0); 0,000009 (T1); 0,00009 (T2); 0,0009 (T3); 0,009 (T4) , 0,09 (T5) and 0,9 (T6) g, with CuCl2 L-1 as element source. Approximately two weeks after germination, and before exposure to the contaminant, the plants were initially measured, both for height, starting from an average height of 10 cm from soil level in the vase up to the apical bud, as well as for stem diameter. The lot was homogeneous, especially as regards the required coloring of cotyledonal leaves. The experiments took place from November 6th to December 3rd, 2009. The plants were measured once again at the end of the experiment, whereat the diameter of the stem was measured with a common pachymeter, and height and leaf measurements with a meter tape. Subsequent to exposure and the collection of stem and leaf biometric data, the leaf area index (LAI) were calculated for leaves 1-7 through multiplication of the width by the length, i.e.,. LAI = WIDTH X LENGTH After the experimental period, the plants were collected from the vases and split up by organ, which were then separately weighed on a digital balance, to so obtain the weights of fresh-mattermass of the aerial parts and stems. These were then placed in identified paper bags, and subsequently dried at 80ºC for 48 hours (12), thereby obtaining dry-matter-mass values. Statistical analysis The process adopted was the statistical analysis of randomized blocks containing one Glycine max plant per vase with sand, cultivated from the seedling to the fruit stages. The procedure consisted of seven treatments and four repetitions, with four plants per treatment, thus 112 plants all told. The Tukey test was applied to the averages of the results obtained for all the variables in the CuCl2 concentration, using P ≤ 0.05 in the SISVAR program. 9 Revista SEB Ano 14 Final.indd 9 09/10/2012 13:43:52 After the experimental period, the plants were collected from the vases and split up by organ, which were then separately weighed on a digital balance, to so obtain the weights of fresh-matter-mass of the aerial parts and stems. These were then placed in identified paper bags, and subsequently dried at 80̊-ºC for 48 hours (NAKAZONO et al., 2001), thereby obtaining dry-matter-mass values. Brazilian Journal of Ecology statistical analysis ISSN 1516-5868 The process adopted was the statistical analysis of randomized blocks containing one Glycine max plant per RESULTS main branch), the lowest LAI values were observed in T3, and the highest in T1, whereas for the intermedirepetitions, with four plants per treatment, thus 112 plants all told. The Tukey test was applied to the averages of the ate ones (3, 4 and 5), the tendency for development reRainfall was theCuCl experiment, results obtained forhigh all thethroughout variables in the 2 concentration, using P ≤ 0.05 in the SISVAR program. even more so than that registered in the preceding mained the same until T4. Once again, T6 proved to be that which presented the lowest development (Table 2). years. According RESULTS to data furnished by the Astronomy, the newest in years. this experiGeophysics and Atmospheric Sciences Institute (IAG), Rainfall was high throughout the experiment, even more so Amongst than that registered in theleaves preceding it wasSciences observed that, throughout the treatfrom University São Paulo by (USP), the average dur- andment, According toofdata furnished the Astronomy, Geophysics Atmospheric Institute (IAG), from University ment, and25% in the case leaf 6, the doses were insufing theofmonths of(USP), studythe was around 25% São Paulo average during thehigher months than of study was around higher thanofthat registered for the years ficient to induce statistical differences, whereas for 1993 to 2002 1). 1993 to 2002 (Table 1). that registered for (Table the years vase with sand, cultivated from the seedling to the fruit stages. The procedure consisted of seven treatments and four Table 1. Average values of temperature (°C) and relative humidity (%) of the air, rainfall (mm), number of days with rain, irradiation (MJ/m².dia), and wind velocity (m/s) in the city of São Paulo during the period of culture Month October November December Temperature (ºC) 19 (24-15) 23 (29-19) 22 (27-18) Relative humidity (%) 86 (95-67) 80 (95-56) 84 (95-62) 138.0 234.4 208.5 Rainfall (mm) Number of days with rain (days) 19 21 22 Irradiation (w/m-2) 13.3 17.6 16.4 wind velocity (m/s) 5.9 6.5 5.8 As regards leaf biometrics, over time there was greater differentiation between treatments. Thus, in the case of leafLAI 7, the tendency was similar that leaves 1 and 2 (the oldest leaves on the branch), the lowest values were observed in T3,to and thenoted highestfor in the T1, Although there were no main statistic differAlthough there were no statistic differences between treatments, there was an enhanced tendency for growth in remainder. In other words, T6 was theT4. treatment in ences stem between treatments, enhanced whereas for diameter the intermediate 4was andan 5),The thegreatest tendency development remained theofsame until Once again, at the endones ofthere the(3, experiment. stemfor heights encountered at the end the experiment were which theT6plants presented the lowest growth, and tendency intostem diameter at the endthose of related T6 proved tofor begrowth that which presented theand lowest development (Table 2). those corresponding treatments T0 T1, whereas to high doses were the lowest (Table 2). and T4 the highest (Table 2). the experiment. Thenewest greatest stem heights encoun-it wasT3 Amongst the leaves in this experiment, observed that, throughout the treatment, and in the case Equivalence was observed, as regards valtered at the end of the experiment were those corof leaf 6, the doses were insufficient to induce statistical differences, whereas for leaf 7, the tendency was similar to that responding to treatments T0 and T1, whereas those ues for leaf dry-biomass. Moreover, the same tennoted for the remainder. In other words, T6 was the treatment in which the plants presented the lowest growth, and T3 dency encountered for leaves was also observed for related to high T6 doses were the lowest (Table 2). and T4 the highest (Table 2). As regards leaf biometrics, over time there stem-dry-mass, in that treatments with higher conwas greater differentiation between treatments. Thus, centrations of Cu (T5 and T6) were those in which in the case of leaves 1 and 2 (the oldest leaves on the plants accumulated less dry mass. Table 2. Results for mean values and standard deviation of biometric variables in stem height (SH), stem diameter (SD) and leaf area index (LAI), obtained at the end of plant exposure to the different concentrations of copper. T0 T1 T2 T3 T4 T5 T6 SH 26.6 ±5.6a 27.1 ±3.8a 23.8 ±2.8a 23.4 ±2.3a 24.5 ±2.7a 23.9 ±1.8a 22.4 ±2.8a SD 0.4 0.03ab 0.4 ±0.04b 0.4 ±0.04a 0.4 0.02ab 0.4 0.02ab 0.4 0.02ab 0.4 ±0.07a LAI1 14.1±0.7ab 15.6±1.1b 13.8±2.1ab 13.5±0.2a 15.4±2.2b 15.2±1.5ab 13.3±0.2a LAI2 14.9±2.6ab 15.2±1.5b 12.9±2.7ab 20.2±13.1a 13.5±0.9ab 13.9±1.1b LAI3 14.3±1.9b 12.2±1.4a 13.1±2.7ab 12.8±1.9ab 12.4±2.0ab 13.2±1.6ab 12.8±2.4ab 10.9±0.8a LAI4 14.0±1.4b 13.4±0.7ab 12.9±1.6ab 12.6±1.4ab 12.2±1.6ab 13.2±2.3ab 11.2±1.3a LAI5 16.6±2.1b 16.3 2.2ab 15.1±1.5ab 16.8±3.1b LAI6 19.2±1.4a 20.3±4.4a 18.6±1.6a LAI7 20.2±4.6ab 21.8±0.6ab 18.8±2.7ab 22.0±1.4b 19.7±2.6a 17.6±2.8b 16.3±1.4b 14.7±3.2a 18.5±1.8a 17.6±2.6a 16.5±3.4a 19.5±1.04b 19.4±2.03b 12.6±1.8a Equivalence was observed, as regards values for leaf dry-biomass. Moreover, the same tendency encountered for 10leaves was also observed for stem-dry-mass, in that treatments with higher concentrations of Cu (T5 and T6) were those in which plants accumulated less dry mass. Revista SEB Ano 14 Final.indd 10 09/10/2012 13:43:52 hich plants accumulated less dry mass. Brazilian Journal of Ecology ISSN 1516-5868 Table 3. Mean values in grams and standard deviation es of soils, obtained different results from those Mean values in gramsofand deviation of leaf and end stemofdry at the end of the experiment. leafstandard and stem dry mass at the themass experiment. observed with soybean, since stem-heights did not Treatment Dry Mass (leaf) Dry Mass (stem) T0 0.96 ±0.08 1.37 ±0.31 T1 1.10 ±0.59 1.30 ±0.26 T2 1.06 ±0.09 1.07 ±0.18 T3 1.00 ±0.20 1.07 ±0.22 T4 1.23 ±0.17 1.17 ±0.30 T5 1.02 ±0.13 1.02 ±0.19 T6 1.11 ±0.24 1.06 ±0.19 DISCUSSION Heavy rainfall occurred in São Paulo during the period of plant exposure. As was observed by Bertoni et al. (1999), since the element Cu++ is extremely prone to edaphic conditions, mainly humidity, this may have influenced the results, as regards percolation, the availability of the element and its interaction with the plant. Variations in chemical attributes in the soil may have induced changes in the micronutrient content, consequently leading to its deficiency or toxicity (3). Hence, results which did not present significant differences, such as the diameter of the stem, the LAI values for newer leaves, and biomass variables, could be explained by this momentarily excessive rainfall, with the consequential washing out of the soil. This was observed by Viera et al. (2005), who, on studying the availability of nutrients in the soil, the quality of soybean grains and their productivity in soil manured with sewage sludge, and when evaluating the rates of N in the soil in the first cultivation of the plant, demonstrated that, in the treatment I + L3, the amount of biosolids applied may have induced the loss of N by lixiviation. Thus, seeing that the plants were not exposed under controlled conditions of climatic variables, high percolation of the element in the soil may have interfered in the rates of Cu root absorption. On analyzing stem heights, it was noted that in the first, lower-concentration treatments, the low doses of Cu++ probably functioned as manure, hence with a greater tendency to induce growth. Santos et al. (2009), when analyzing the effects of Cu++ and Zn++ on sorghum cultivated in three class- present significant differences between treatments, whereas diameters did, both as regards treatments and the soils in which they were cultivated, thus contrary to our results, whence stem heights were significantly greater in treatments 0 and 1. With the exception of new leaves, leaf measurements followed the same pattern. It was noted that growth was less in the more concentrated treatments, a possible indication of toxicity, with the consequential prejudice to the development of organs. Copper is a prerequisite for the satisfactory development of the plant, seeing that there is a reduction in leaf area in those with a deficiency or excess of this nutrient (13). According to Anjos and Mattiazzo (2000), in studies with corn in soils enriched with a biosolid (sewage sludge), it was noted that the highest rates of this metal were concentrated in the leaves, even though in this method of fertilization, independent of either the treatment or the soil, this element presented no toxic effects for the plants. According to Rangel et al. (2006), when studying the rates of heavy metals in the leaves and grains of corn on applying sewage sludge, it was noted that of the heavy metals assayed, copper was that which presented rates in the leaf within the range considered to be phytotoxic, although, until the third culture, notably not above the upper range of toxicity. Significant effects of the application of doses of sewage sludge were only observed in leafcopper-rates in the first LB-culture and the third LF, an indication of the absence of response in leafrates with the application of increased doses of the sludge. Another factor which came under consideration, not only by Rangel (2006), but also by several other authors (6, 16), is that Cu+ tends to accumulate more in roots than in leaves, thereby indicating that the lower response to the addition of sewer sludge, in terms of leaf-copper-rates, could also be related to the low translocation of this nutrient in the plant. Dry biomass variables presented no statistic differences between treatments. In a study by Araujo et al. (2005) of the effects of a textile sludge compound on seedlings of soybean and wheat, it was observed that the increase in concentrations of the compound above 19 g L-1 caused a significant 11 Revista SEB Ano 14 Final.indd 11 09/10/2012 13:43:52 Brazilian Journal of Ecology ISSN 1516-5868 decrease in total dry-matter-mass, height of the aerial part and root length in those of both plant-species. In the case of soybean, there was a reduction, in relation to the control, of 29% to 34% in total drymatter-mass, 15% to 36% in the height of the aerial part, and 28% to 67% in root length with the application of 38, 76 and 152 g L-1, respectively. The author emphasized that, although the amount of heavy metals present in textile sludge was in accordance with the values stipulated by CETESB, the decrease in total dry matter could be an indication of the effect of toxicity in the plants induced by heavy metals, especially copper and zinc. Moreover, Araujo et al. (2005) also noted that in soybean and wheat seedlings, there was a significant decrease in chlorophyll content, simultaneous with a corresponding decrease in liquid photosynthesis, from the 76 g L-1 concentration one. In a study of the growth and mineral nutrition of Eucalyptus maculata and Eucalyptus urophylla in concentrations of Cu++ (19), it was noted that symptoms of phytotoxicity already appeared in the first five days of the experiment, even at the lowest concentrations, such as 32 and 64 μM of Cu++ supplied as CuSO4. As to the aerial part and leaf area, there was a decrease in dry matter at concentrations above 32 μM of Cu++. In studies with sorghum (15), it was noted that doses of 1,07, 1,24 and 1,26 mg/Kg of copper applied induced an increase in dry matter. In certain studies of toxicity with chlorine, no direct relationship linking the element with effects on growth was observed. In neither of two studies, one involving chemical sterilization with chlorine dioxide in an in vitro culture of Anthurium (4), and the other (21), the in vitro culture of Eucalyptus pellita in a medium sterilized by NaOCl, were toxic effects arising from these solutions observed in plant development. On the other hand, there was a considerable increase, distribution and accumulation of copper and zinc in conifers (Jatropha curcas), where copper and zinc chlorates were used as sources of contamination (5). The authors only noted toxicological effects on increasing the doses of both elements, which seems to imply that chlorine itself did not interfere in these effects in the cultivars analyzed, thereby facilitating transposition to the present work with specimens of G. max, and thus making it possible to attribute tendencies for growth in plants cultivated in more concentrated solutions, only to copper. CONCLUSION With these results, it was noted that Glycine max plants can present a tendency for aboveground growth inversely proportional to Cu rates, thereby inferring their sensitivity to high doses of this element. The plants presented no evident toxicological effects under the parameters analyzed in this study, which can be justified by the possible percolation of the element, as a result of the high rainfall which occurred during the experimental period. It is therefore proposed that new experiments be undertaken with G. max and copper under controlled conditions, in order to determine the relationship of toxicity between the element and the development of this plant species. RESUMO A soja (Glycine max) apresenta-se como sendo uma espécie de grande importância econômica para o Brasil, que é considerado um dos grandes produtores desta cultura. O trabalho objetivou analisar a influência do cobre sobre o desenvolvimento de órgãos aéreos da espécie. Para tanto foi desenvolvido experimento em condições naturais de umidade e temperatura utilizando 112 plantas cultivadas em vasos com areia. Foi adotado um delineamento de blocos casualisados contendo, quatro blocos, sete tratamentos e quatro repetições, que foram irrigadas com solução de Hoagland & Arnon enriquecida com diferentes concentrações de CuCL2 por 30 dias. Após este período foram realizadas análises de variância e teste Tukey, onde se observou que as plantas submetidas ao tratamento 0,9 g CuCl2 L-1 (T6) foram as que apresentaram menor crescimento em relação as plantas controles ou aos menores tratamentos. Os valores de massa seca do caule apresentaram equivalência às tendências encontradas na biometria. Conclui-se assim que o cobre em altas concentrações pode influenciar no crescimento de plantas de Glycine max. Palavras chave: soja, biometria vegetal, órgãos aéreos, cobre. 12 Revista SEB Ano 14 Final.indd 12 09/10/2012 13:43:52 Brazilian Journal of Ecology ISSN 1516-5868 REFERENCES 1. -Anjos, A. R. M.; MATTIAZZO, M. E. Metais pesados em plantas de milho cultivadas em latossolos repetidamente tratados com biossólido. Scientia Agricola, Piracicaba, V.57, n.4, p.769-776, 2000. 2.­ -Araújo, A. S. F.; Monteiro, R. T. R.; Cardoso, P. F. Composto de lodo têxtil em plântulas de soja e trigo. Pesquisa Agropecuária Brasileira, Brasília, V.40, n.6, p.549-554, 2005. 3. -BERTONI, J. C.; HOLANDA, F. S. R.; CARVALHO, J. G.; PAULA, M. B.; ASSIS, M. P. Efeito do cobre na nutrição do arroz irrigado por inundação- Teores e acumulo de nutrientes. Ciência e Agrotecnologia, Lavras, V.23, n.3, p.547-559, 1999. 4. -Cardoso, J. C. Notas Científicas Esterilização química de meio de cultura no cultivo in vitro de antúrio. Pesquisa Agropecuaria Brasileira, Brasília, V.44, n.7, p.785-788, 2009. 5. CHAVES, L. H. G.; MESQUITA, E. F.; ARAUJO, D. L.;FRANÇA, C.P. Crescimento, distribuição e acúmulo de cobre e zinco em plantas de pinhão-manso. Revista Ciência Agronômica, Fortaleza, V. 41, n. 2, p. 167-176, 2010. 6. JUNIOR, C. H. A.; BOARETTO, A. E.; MURAOKA, T.; KIEL, J. C. Uso agrícola de resíduos orgânicos potencialmente poluentes: propriedades químicas do solo e produção vegetal. Tópicos em Ciência do Solo, Viçosa, V.4, n. 10, p. 371-470, 2005. 7. Luchese, A. V.; JUNIOR, A. C. G; LUCHESE, E. B; BRACCINI, M. C. L. Emergência e absorção de cobre por plantas de milho (Zea mays) em resposta ao tratamento de sementes com cobre. Ciência Rural, Santa Maria, V.34, n.6. p. 19491952, 2004. 8. Lui, J. J.; GALBIATI, J. A.; MELHEIROS, E. B. Efeito da irrigação e utilização de lixo orgânico na formação de mudas de Eucalipto. Holos Emvironmen, Rio Claro,V.8, n. 2, p. 179-194, 2008. 9. MANTOVANI, A. Composição química de solos contaminados por cobre ; formas, sorção e efeito no desenvolvimento de espécies vegetais. 2009. 105 f. Tese (Doutorado em Ciência do solo) - Faculdade de Agronomia, Universidade Federal do Rio Grande do Sul , Porto Alegre. 2009. 10. MATOS, A. T.; FONTES, M. P. F.; JORDÃO, C. P.; COSTA, L. M. Heavy metals mobility and retention forms in a brazilian oxisol. Revista Brasileira Ciência do Solo, Campinas, V. 20, n.3, p.379 – 386, 1996. 11. MCBRIDE, M.; SAUVE, S.; HENDERSHOT, W. Solubility control of Cu, Zn, Cd and Pb in contaminated soils. European Journal Soil Science,Oxford, V. 48, n. 2, p. 337 – 346, 1997. 12. NAKAZONO, E. M.; COSTA, M. C. D.; FUTATSUGI, K.; PAULILO, M. T. S. Crescimento inicial de Euterpe edulis Mart. em diferentes regimes de luz. Revista Brasileira de Botânica, São Paulo, V. 2, p. 173-179, 2001. 13. PEGORINI, E. S.; ANDREOLK, C. V.; SOUZA, M .L.; FERREIRA, A. 2003. Qualidade do lodo de esgoto utilizado na reciclagem agrícola na região metropolitana de Curitiba - PR. In: SIMPÓSIO LATINO AMERICANO DE BIOSSÓLIDOS, 1., São Paulo. 14. RangeL, O. J. P.; Silva, C. A.; Bettiol, W.; Dynia, J. F. Efeito de aplicação de lodos de esgoto sobre os teores de metais pesados em folha e grão de milho. Revista Brasileira de Ciência do Solo, Campinas, V.30 ,p.583-594, 2006. 15. SANTOS, H. C.; Fraga, V. S.; RaposO, R. W. C.; PereirA, W. E. Cu e Zn na cultura do sorgo cultivado em três classes de solos. I. Crescimento vegetativo e produção. Revista Brasileira de Engenharia Agrícola e Ambiental, Campina Grande, V.13, n.2, p.125–130, 2009. 16. Silva, e. b.; TANURE, L. P. P.; SANTOS, S. R.; JUNIOR, P. S. R. Sintomas visuais de deficiências nutricionais em pinhão-manso. Pesquisa Agropecuária Brasileira, Brasília, V.44, n.4, p.392-397, 2009. 17. SILVA, R. F.; ANTONIOLLI, Z. I.; LUPATIMI, M.; TRINDADE, L. L.; SILVA, A. S. Tolerância de mudas de Canafístula Peltophorum dubium (SPRENG.) TAUB.) inoculadas com Pisolithus microcarpus a solo com excesso de cobre. Ciência Florestal, Santa Maria, V. 20, n. 1,p. 147-156, 2010. 18. SFREDO, G. J. Soja no Brasil; Calagem, adubação e nutrição mineral. Londrina – PR . Embrapa Soja. 2008. P. 48; 81-82 19. SOARES, C. R. F. S.; SIQUEIRA, J. O.; CARVALHO, J. G.; MOREIRA, F. M. S.; GRAZZIOTTI, P. H. Crescimento e nutrição mineral de 13 Revista SEB Ano 14 Final.indd 13 09/10/2012 13:43:52 Brazilian Journal of Ecology ISSN 1516-5868 Eucalyptus maculata e Eucalyptus urophylla em solução nutritiva com concentração crescente de cobre. Revista Brasileira de Fisiologia Vegetal, Campinas, V.12, n.3, P. 213-225, 2000. 20. SODRE, F. F.; LENZI, E. Utilização de modelos físico-químicos de adsorção no estudo do comportamento do cobre em solos argilosos. Química Nova, São Paulo, V. 24, n.3, p. 324-330, 2001. 21. TEIXEIRA, S. L.; RIBEIRO, J. M.; TEIXEIRA, M. T. Utilização de hipoclorito de sódio na esterilização de meio de cultura para multiplicação in vitro de Eucalyptus pellita L. Ciência Florestal, Santa Maria, V.18, n.2, p.185‑191, 2008. 22. VIEIRA, R. F.; Tanaka, R. T.; Tsai, S. M.; Pérez, P. Disponibilidade de nutrientes no solo, qualidade de grãos e produtividade da soja em solo adubado com lodo de esgoto. Pesquisa Agropecuária Brasileira, Brasília, V.40, n.9, p.919-926, 2005. 23. ZAMPIERI, M. C. T. Estudo sobre os efeitos do cobre e zinco no crescimento da plântula de Aechmea blanchetiana (Baker)L. B. Smith cultivadas em vitro. Aplicação da analise por ativação com nêutrons. 160 f. Tese (Mestrado em Ciência na área de Tecnologia Nuclear- Aplicações) - Instituto de Pesquisas energéticas e nucleares. Autarquia associada à Universidade de São Paulo. São Paulo. 2010. 14 Revista SEB Ano 14 Final.indd 14 09/10/2012 13:43:52 Brazilian Journal of Ecology ISSN 1516-5868 Environmental characterization of the Lajeado Tunas watershed, RS, Brazil Lisiane Zanella* – Universidade Regional Integrada do Alto Uruguai e das Missões – Campus de Frederico Westphalen - RS, Laboratório de Geoprocessamento (lisianezanella@gmail.com) Eloir Missio – Universidade Regional Integrada do Alto Uruguai e das Missões – Campus de Frederico Westphalen - RS, Laboratório de Geoprocessamento (eloirmissio@unipampa.edu.br) Rosângela Alves Tristão Borém, Universidade Federal de Lavras – UFLA, Setor de Ecologia/Departamento de Biologia (tristao@dbi.ufla.br) Maurício Castro dos Santos – Universidade Regional Integrada do Alto Uruguai e das Missões Campus de Frederico Westphalen - RS, Laboratório de geoprocessamento (castro86@hotmail.com) Marcos Antônio Ritterbuch – Universidade Regional Integrada do Alto Uruguai e das Missões – URI, Laboratório de Geoprocessamento (ritterbuch@fw.uri.br) ABSTRACT Geographic Information System (GIS), Remote Sensing Imagery and Global Positioning System (GPS) coordinates were employed to characterize landscape structure and land use features of the Lajeado Tunas watershed, Frederico Westphalen, Rio Grande do Sul State, Brazil. Based on data so obtained, two land-cover maps were compiled. These were after compared in order to evaluate the methodology employed. The watershed, spread over approximately 650 ha, is apparently on a mild, east-to-west slope (6.95%). Due to this relative flatness, local conditions are favorable for farming. Notwithstanding, preservation is a prerequisite for controlling erosion and protecting water resources. The land uses mapping has shown how the predominant occupation for anthropogenic usage has exerted negative effects on the quality of the environment and the conservation of biodiversity. Even though only a simple set of GIS tools were used for analyzing the focal landscape, these have helped to arrive at an adequate understanding of the structurally important characteristics of the landscape in a regional context. The results obtained have proved to be of interest for understanding which conservation action is more appropriate for improving the maintenance of local and regional biodiversity, to so guarantee the long-term maintenance of agricultural ecosystems, and, in future analyses, for generating knowledge on how local fauna and flora respond to regional landscape characteristics, the key-points for guaranteeing the maintenance of biodiversity. Key-words: Environmental Planning, Landscape Structure, Sustainable Management, Geographic Information Systems (GIS) INTRODUCTION Increased anthropic action has given rise to important alterations in the environment, with consequential impacts. Among the main aspects of these modifications we can cite the loss of habitat, and the fragmentation and decrease in quality in the remaining areas (4). Environmental planning has acquired pre-eminence over the latter decades, due to the interest in redirecting for consideration, not 15 Revista SEB Ano 14 Final.indd 15 09/10/2012 13:43:52 Brazilian Journal of Ecology ISSN 1516-5868 only the environments so created and modified by human-kind, but also the remaining, surrounding natural environments. The growing need to present solutions and strategies, with a mind to interrupting and reverting the effects of environmental degradation and the impoverishment of natural resources, has led to intense questioning, mainly as to (a) how to face the agglomeration of environmental problems detected in large urban centers, (b) how to elaborate and develop efficient strategies for their solution, and (c) how to guarantee the application of such strategies. In order to respond to such questions, the environmental issue should be analyzed within a perspective that surpasses urban limits. We must take into consideration that cities and human-kind do not exist apart from the natural elements (water, air, soil, among others), but all together compile a natural global system – the planet Earth - on which we have been acting and intervening without concern for the eventual accumulative effects, thus compromise not only the present, but especially, the very future of their own existence. We need to recognize that human-kind subsist as part of this controversy. Thus, on contemplating the principles of landscape ecology, anthropic action should come under consideration throughout all the phases of planning, inasmuch as, if well conducted, better equilibrated alternatives may be arrived at, as means of inducing the sustainable usage of the environment. 16 Even though each study may present distinct forms of partitioning the space to be analyzed or planned (14), several authors give preference to water basins, in special watersheds, since these constitute minimum units in the environment planning approach, due to the agglomeration of important pertinent components aggregated to their structuring, such as characteristic fauna and flora, besides the drainage itself (3.12). The management of watersheds involves a process that permits formulating an integrated assemblage of actions on the environment (social, economic, institutional and legal structures of a watershed), in order to promote the conservation and sustainable utilization of prevalent natural resources, whereby the prerequisite of acquiring knowledge on the structure, composition and dynamics of the catchment itself and surroundings. The Geographic Information System (GIS), within the context of the integrated planning of and systemic approach to watersheds, has been the way of applying the methodology and philosophy of analysis and synthesis of organizational problems and questions related to the environment, with world-wide application in terms of relationships and integration (15). Due to its characteristics of data integration, GIS, together with remote sensing products, functions as probably one of the most adequate tools in support of decision making for systemicfocusing, in the management of natural resources. Figure 1 – Localization of the Lajeado Tunas watershed, Frederico Westphalen – RS, Brazil. Revista SEB Ano 14 Final.indd 16 09/10/2012 13:43:53 Brazilian Journal of Ecology ISSN 1516-5868 Thus, the aim of this study was to apply two methodologies to the analysis and comparison of the land use geographic distribution, as well as to elaborate thematic maps of the study area, with an eye to the environmental characterization of a watershed in the south of Brazil, thereby supplying subsistence for the elaboration of a plan for its territorial management. METODOLOGY Localization of the Study Area The Lajeado Tunas watershed (Fig. 1) is located in Frederico Westphalen County, Rio Grande do Sul, Brazil, between the parallels 27°22’ and 27°33’ south and the meridians 53°24’ and 53º27’ west. It discharges into the Rio Pardo, pertaining to the Rio Uruguay Basin, at around 200 m from the dam of the Companhia Riograndense de Saneamento – CORSAN, thereby contributing to the water supply of the urban area (7). Frederico Westphalen presents a humid subtropical climate (Cfa), according to the Köppen classification, with average minimum and maximum temperatures of 13°C and 31°C, respectively (8). Annual rainfall, of between 1.800 and 2.100 mm, is well distributed throughout the year (8). The pattern of drainage in the watershed is dendrite-like, with wide-spreading branches and tributaries at various angles (Howard, 1967). Aluminum-ferric red latosoil predominates in the highest and flattest parts, and neosoils closer to the river mouth (17). The region of the Upper Uruguay, where Frederico Westphalen county is located, was originally totally covered by Atlantic Forest latu senso, composed of deciduous seasonal and mixed ombrophylous forests (17). Based on the biogeographic region delimitation proposed by Silva & Casteletti (2003), the study area corresponds to a transition region between interior and araucaria forests (14). With the introduction of farming, the original native vegetation experienced profound modifications. The present scenario is composed by forest fragments, vegetal cover characterized by the predominance of early secondary forest in various successive stages, diversified farming and other agricultural activities (10). Methodological procedures The first step involved the construction of a cartographic base of the study area, using the softwares Idrisi Kilimanjaro (1) and MapInfo (7.8 9), together with information contained in the topographic chart Folha SG.22-Y-C-II-3 MI 2885/3, of Frederico Westphalen, scale 1:50.000, elaborated by the Diretoria de Serviços Geográficos of the Brazilian Army – DSG (IBGE, 1979), and in the LandSat TM 5 satellite image, orbit 223/079, of 8/3/2004 at 13h 12’ and 59”. We obtained the watershed delimitation starting from the identification of the corresponding drainage area, or rather that referring to the area drained by the entire fluvial system confined within topographic limits, all projected onto a horizontal plane (21). The perimeter of the watershed consisted of the length of an imaginary line drawn along the water divisors, which in turn coincide with geomorphometric aspects of the region under analysis. Water bodies and road network were digitized from DSG charts, and complemented with field data obtained with a Garmin 12 GPS. This process allowed us to include roads and other forms of access to rural properties, as well as streams and springs, which do not appear in the official charts. The ordering of water courses and drainage density were both used to characterize regional drainage. This arrangement, which represents the degree of branching of the system of watershed drainage (23), was defined according to the classification proposed by Strahler (1952), by which, watercourses with no tributaries are considered of the first order, those of the second order only receive tributaries of the first order, independent of the number of tributaries, those of the third order receive two or more tributaries of the second order, although they are also capable of receiving tributaries of the first order, and so on. Drainage density refers to the efficiency with which rainwater quits the watershed. It is calculated as the relationship between the total combined length of all the water courses present, and the entire area occupied by the system (4). Hypsometry was elaborated from the interpolation of vectorial maps of the level curves, which gave rise to the generation of a digital elevation model (DEM). Hypsometry was divided into four 17 Revista SEB Ano 14 Final.indd 17 09/10/2012 13:43:53 Brazilian Journal of Ecology ISSN 1516-5868 different altimetrical classes (400 – 450 m; 450 – 500 m; 500 – 550 m; 550 – 600 m). A clinographic map, elaborated with the aid of models available in Idrisi and using DEM as a base, was applied to classifying the area into five different patterns of declivity (13). Land use mapping was based on the application of two methodologies: (i) the supervised classification of satellite images and (ii) data obtained in the field with GPS geographic coordinates. We used methods of image processing, as recommended by Easteman (1998) for the supervised classification of the LandSat TM5 satelite image (bands 3, 4 and 5), thereby simplifying the elaboration of one of the land use maps with Idrisi software. In this study, the following land use for mapping were defined: (a) natural vegetation; all the vegetal forms, as fragment forest, riverine forest and early secondary forest; (b) agriculture – areas allocated to annual culture and those with exposed soil in the phase of preparation or implantation of annual cultures; (c) pasture - areas with pasture and those allotted to cattle raising; (d) waterbodies – water bodies, either naturally formed or reservoirs and ponds; (e) urban area – urban lots and rural buildings. The edition of refinement classification was done with Mapinfo 7.8 software. On completion, the results were introduced into PhotoImpact 4.0 software for the manipulation of images and elaboration of the figures corresponding to consolidated thematic charts. Geographic coordinates obtained in the field with GPS were used in the second methodology. For mapping the outlines of land use classes in the watershed, area marking was based on the limits of rural properties, urban areas and the main land uses within each rural property. Within the limits that were being investigated and duly registered, each point corresponded to an extremity of the polygon or line that was being mapped. Simultaneous with the collection of points, a manual outline of the mapped properties was drawn up, this contributing as a source of orientation for elaborating the layers corresponding to differences in land use and occupation, as recognized and identified in the field. Field work lasted for around two months (January and February, 2006), running up to approximately 400 work-hours carried into effect by a team of 2. The points collected were transferred from GPS to the software GPS Track Maker, and stored in a geographic database. These were introduced into MapInfo 7.8. for the manipulation and development of layers corresponding to the following land use classes: (i) forest – those with primary or secondary vegetation in an advanced stage of succession; (ii) secondary forest – areas covered by vegetation in the initial to mid stages of regeneration; (iii) groves - areas with few trees which do not constitute a forest; (iv) swamp - flooded areas, generally located near to springs and reservoirs; (v) annual agriculture – annual cultures and areas with exposed soil; (vi) eucalyptus – areas for planting eucalyptus; (vii) perennial agriculture - areas for the plantation of Paraguay tea; (viii) citrus – areas specifically allotted to producing grapes and oranges; (ix) pasture – grassland, ultimately used for cattle raising; (x) waterbodies – bodies of water and artificial lakes (reservoirs); (xi) farms – small properties, not for farming and without rural installations; (xii) builtup areas – an area comprising elaborated properties and their respective rural surroundings; (xiii) urban area – an assemblage of lots with buildings of low standard; (xv) Roads/access routes – comprising areas for public use (roads, streets, etc.). RESULTS The area occupied by the Lajeado Tunas watershed (around 650 ha), with a perimeter of 10.6 km, represented only 2.5% of the total area of Frederico Westphalen county. It was mostly situated in a region occupied by small rural properties characterized as family concerns, which, as such, were strongly exploited as regards natural resources. Orientation was east-to-west, and the main watercourse was around 5 km in extent. The calculated drainage density was 22.3 m/ha. The watershed itself, comprising an extension of 14.5 km, was drained by a main perennial watercourse composed of 14 springs, three located in the urban perimeter, and the remainder in the rural zone. The greater part of the watershed was located in the rural zone. The smaller part, which was in 18 Revista SEB Ano 14 Final.indd 18 09/10/2012 13:43:53 Brazilian Journal of Ecology ISSN 1516-5868 the urban zone, presented a paved federal highway, (545.69 ha), distributed among 54 small rural fambut only 238 m of which encroached upon water- ily properties, entirely or partially inserted into shed limits. Unpaved roads, 22.67 km all told, and the watershed. Annual cultures consist of planting characterized as earth roads, also included routes corn and soybean, and to a lesser extent, beans and of access to rural properties. We took the drain- tobacco. Other activities, such as olericulture and age density as a base to obtain the density of roads, fruit culture are also undertaken in some properties, which was also high (35 m/ha) in the watershed. but only for family consumption. Animal breeding The surface of the watershed presented a is basically restricted to dairy cattle and pigs. variation of 200 m in height, between the quotas The extension of agriculture diagnosed by 400 to 600 m above sea level, the greater part of GPS mapping methodology occupied 57.63 % of which (more than 80%) being situated between 450 the area and corresponded to annual cultures, includand 550 m. The two extremes referred to the highest ing areas of perennial cultures and horticulture, as and lowest altitudes, corresponding to 13.3% and can be seen in Figure 2. According to field mapping 4.1%, respectively, of the whole area. (GPS approach) of this class, this percentage was reThe biggest part of watershed relief duced to 31.56%. (92.77%) consisted of low declivity areas (0 – 13%), Although eucalyptus, citrus and perennial classified as flat, and slightly or moderately wavy. agriculture were distinguished from annual culWavy relief (13 to 20%) occurred in less than 5% tures, their areas were little representative, and ocof the whole. On the other hand slopes between 20 cupy only 4.19 ha, 1.87 ha and 2.71 ha, respectively. and 45% were found in 15.57 ha of the whole area, Other classes lacking in the satellite image mapwhereas those above 45%, considered mountainous to cliff-like, were not registered. The average de- ping, were identified through GPS approach (Figure 3): (i) roads/access routes (1.07%); (ii) built-up clivity was estimated at 6.95%. Although satellite images interpretation areas (2.97%); and, (iii) farms (2.17%). Urban area allowed us to classify the study area in five main occupied only 16% of the watershed. According to GPS mapping approach, pasland use classes, a larger number of classes were tures occupied 105.2 ha, and natural vegetation diagnosed only through the GPS mapping methodFigure 1 – Localization of the Lajeado Tunas watershed, Frederico Westphalen – RS, Brazil.according to image around 86 ha. On the other hand, ology (Table 1). Land use classes Natural cover Anthropic cover Forest Secondary forest Groves Swamp Annual agriculture Eucalyptus Perennial agriculture Citrus Pasture Waterbodies Farms Built-up areas Urban areas Roads/access routes Total The area of the watershed situated in the rural zone corresponded to 84% of the landscape LandSat Area (ha) Area (%) 86.31 13.29 374.41 57.63 82.53 0.09 12.70 0.01 106.29 16.36 649.63 100.00 GPS Area (ha) Area (%) 156.20 24.04 14.11 2.17 5.61 0.86 0.20 0.03 205.00 31.56 4.19 0.64 1.87 0.29 2.71 0.42 105.20 16.19 5.41 0.83 14.10 2.17 19.28 2.97 108.80 16.75 6.95 1.07 649.63 100.00 classification approach, pastures occupied 81.89 ha, and natural vegetation was divided in four classes: 19 Revista SEB Ano 14 Final.indd 19 09/10/2012 13:43:53 Brazilian Journal of Ecology ISSN 1516-5868 forest (24.04%), secondary forest (2.17%), groves (0.86%) and swamps (0.03%). classification, this class was not identified due to the waterbodies being smaller in size than the pixel Figure 2 – Chart of land use mapping using LandSat TM5 image classification approach of the Lajeado Tunas watershed, Frederico Westphalen – RS. Figure 2 – Chart of land use mapping using LandSat TM5 image classification approach of the Lajeado Tunas watershed, Frederico Westphalen – RS. Figure 3 – Chart of land use mapping using GPS field mapping approach of the Lajeado Tunas watershed, Frederico Westphalen RS. of land use mapping using GPS field mapping approach of the Lajeado Tunas watershed, Frederico Figure 3 ––Chart Westphalen RS. ‘waterbodies’ corresponded to an The– class area of 5.41 ha in field mapping approach. In image of the LandSat image employed in the study (pixel = 30 x 30 m). 20 Revista SEB Ano 14 Final.indd 20 09/10/2012 13:43:53 Brazilian Journal of Ecology ISSN 1516-5868 DISCUSSION The Lajeado Tunas watershed, classified as of the third order, can be considered a small unit, with high drainage density (4) and thus, with favorable conditions for constraining local intervening factors. This high drainage density means that infiltration is more difficult, with higher surface drainage, and consequently, greater hewing out of permanent channels, due to the hydrological deportment of rocks (2). The quantification of roads, in relation to the entire area occupied by the watershed, facilitates diagnosing their density. Roads, on one hand, present a positive contribution when considering accessibility among properties. But, on the other hand, they expose natural areas to human presence through easy access, thereby compromising their preservation, both through favoring the entrance of toxic substances, as from the facility in collecting plants and the capture or running over of wild animals (10). The watershed also presents low average altitude and hypsometric amplitude, factors which influence the amount of radiation received and, consequently, evapotranspiration, temperature and rainfall. According to Tonello et al. (2009), the greater the altitude, the less the amount of solar energy that the environment receives, thus resulting in less energy availability. In this sense, the amount of available energy in the watershed can be considered high. Most of the watershed is considered as appropriate for agriculture, provided that simple steps for controlling erosion are taken. We considered those areas with an accentuated slope as apt for developing annual cultures. However, due to the considerably high susceptibility to erosion in this type of relief, the implantation of this type of culture is conditioned to the implementation of intensive soil conservation techniques. The few areas that present restriction to agriculture due to this high susceptibility, offer adequate conditions for the establishment of permanent cultures such as perennial agriculture and citrus. Since declivity is intimately related to the distribution of water in a watershed (20), the average slope presented by the watershed plays a sig- nificant role in the distribution of water between surface and subterranean drainage, thereby functioning positively in the natural conservation of the drainage system as a whole. Nevertheless, in the present case, signs of erosion in the watershed were observed. This was characterized by ravines in farming areas and gullies along the roads, mainly where there is higher declivity. As regards land use classification in the study area, image classification was limited, due to low spatial resolution, thereby precluding identification with the same precision as that of some classes mapped with GPS approach. Nonetheless, the classification of this type of image can be an excellent tool when used for larger study areas. The results obtained from the land use classification permit inferring that the matrix of land use is agriculture, represented by the corn, soybean and tobacco cultivation. These cultures are undertaken with no heed to conservation procedures, thus possibly giving rise to a high loss of soil by erosion. The divergence among the percentages obtained for the class ‘agriculture’ in the different methodologies adopted, is possibly related to the period in which the LandSat image classification was obtained, viz., October, as this coincides with a critical period, in which the lowest indices of vegetal cover occur, and when there is a similarity between the coloration of agropastoral cultures and natural vegetation, whereby the spectral response makes identification difficult, especially the case of small forest fragments and secondary forests, which end up being incorporated into the local farming matrix. Besides this, in the GPS approach we could separate annual plantations from the perennial agriculture, eucalyptus and citrus classes. We believe that roads/access routes, builtup areas, farms, secondary forest, groves, eucalyptus, and swamps, as identified through GPS mapping approach, as well as small forest fragments, were incorporated as agricultural areas in the interpretation of the satellite image. Thus, the difference between the two methodologies of land use classification was significantly increased regarding to the differentiation among distinct land use classes. It is important to point out that high resolution images are more indicated for small study areas, since they permit the correct differentiation 21 Revista SEB Ano 14 Final.indd 21 09/10/2012 13:43:54 Brazilian Journal of Ecology ISSN 1516-5868 of various land use classes. However, as the acquisition of this type of image is very costly (1 ha costs around R$10.00 for Quickbird satellite images: spatial resolution = 0.60 m), this can compromise the feasibility of the projects with the required characteristics. Selection of the most adequate image is a preponderant factor in a research project, since there are images available in internet free of charge, as is the case of LandSat images. GPS mapping approach makes a precise and correct diagnosis, and is also indicated in the study of small areas, due to the intense field work involved. For larger study areas, satellite images are once again recommended, in view of the costbenefit factor and the rapid task execution, since the difference in results is more significant, regarding to the number of categories in the same class, than in relation to the differentiation between natural and anthropic areas. Pastures occupy the third largest area, possibly due to the economic importance of dairy-cattle breeding for the region. It is importante to note that pastures, when well-managed, is a form of maintaining the surface of the soil covered throughout the year. This practice reduces the speed of surface drainage, contrary to agricultural activities, which leave the soil exposed during its preparation prior to planting (10). As a rule, animal breeding in the region is developed extensively, with pasture of low productivity. According to field observations, we visualize badly-managed compacted areas, having all the available forage used. The results of these actions let the soil exposed and without protection against the erosive action of rain and wind, and significantly diminishing infiltration and directly affecting the drainage of springs and watercourses. The difference between the values observed in satellite-image classification and GPS mapping approach is explained by the presence of small areas with pasture, as well as pastures close to or inserted into agricultural areas that possess a similar spectral response, and thus, are not differentiated in satellite-image classification. Field mapping differentiated vegetation in forest, secondary forest and groves. Forest, that originally occupied all the study area, are mainly located next to springs, accompanying river courses and in areas of high declivity. We considered forest as of fundamental importance in the erosion control and to replenish phreatic water. Accelerated erosive processes prejudice both the environment and society through diminishing the fertility of the soil, and affecting plant growth. They also diminish the capacity of soil water retention, as in near and remote areas, through the drainage of water and sediments, local damage, negative changes in the environment related to floods, the fill-in of rivers, lakes and reservoirs, the contamination of bodies of water, etc.. In such cases, natural vegetation is a potential aid in minimizing these processes (6). Nevertheless, the area of native forest shows that the watershed represents the conservation status equivalent to the region where it is located. Based on LandSat image classification, Tonial et al., (2005) encountered approximately 16% of forest areas in the five water basins located in the northeastern region of the state of Rio Grande do Sul, where the present study area is located. On the other hand, Cemin et al. (2009) found a higher coverage (51.96%) of natural vegetation, in a water basin located close to the same study area. APPs present a large degree of deforestation, as a result of the urban expansion. Thereabouts, the execution of environmental projects should be intensified, as a way of preserving areas where springs occur. We believe this class needs special attention due to the negative impact which can be associated with areas covered by solid material, thereby hindering various physical and biological processes, such as the absorption of rainwater, which normally occur between the soil and the atmosphere. Furthermore, the production of residues and the conversion of areas with natural vegetation into lots constitute two serious recurring problems arising from urbanization (11). Urban expansion should be redirected to locations with more favorable physical conditions, avoiding negative environmental impacts, and so maintain the quality of hydric resources. We do not identify small watercourses in the image classification due to its scale of 1:50.000, and the pixels size. CONCLUSIONS The watershed is considered appropriate for agro-pastural activities, through being on 22 Revista SEB Ano 14 Final.indd 22 09/10/2012 13:43:54 Brazilian Journal of Ecology ISSN 1516-5868 a plain, and possesses high drainage efficiency, thereby favoring surface drainage and minimizing the aftermath of erosive processes. Agriculture is the landscape matrix, and thus constitutes the main threat to the environmental quality of the watershed. Farming areas present a lack of adequate management, and require urgent conservation actions, as a means of mitigating the impacts arising from the intense exploitation of natural resources. Forest recomposition in the study area is imperative, mainly in areas of permanent protection, with the aim of maintaining the ecological functions associated with natural ecosystems, especially the control of erosion and aid in replenishing phreatic water. The methodologies used for diagnosing the distribution of land use mapping differed, mainly as regards the identification of the different land use classes. Although GPS mapping approach identified a larger number of categories of land use, more time was dedicated to undertaking the task, thereby conditioning the application of this method to small areas. Satellite images of mid-spatial resolution proved to be most indicated in the study of larger areas, due to the adequate relationship cost-benefits. ACKNOWLEDGMENT We thank the Universidade Regional Integrada do Alto Uruguai e das Missões – URI – Campus de Frederico Westphalen, and the Laboratory of Geoprocessing for undertaking this work. RESUMO Este trabalho analisa o uso da terra e da estrutura da paisagem da sub-bacia hidrográfica do Lajeado Tunas, Frederico Westphalen, RS, Brasil. Sistemas de Informação Geográfica (SIG), imagens de Sensoriamento Remoto e Coordenadas de Global Positioning System (GPS) foram usadas para caracterizar a paisagem e para gerar dois mapas cobertura da terra, que foram posteriormente comparados para avaliar as metodologias utilizadas. A sub-bacia do Lajeado possui cerca de 650 ha, e os resultados sugerem que o relevo possui declive suave (6,95%), estando orientado de leste a oeste. Devido ao ter- reno ser ligeiramente plano, a sub-bacia possui condições favoráveis para atividades agropastoris, no entanto, práticas conservacionistas são necessárias a fim de controlar a erosão e proteger os recursos hídricos. O mapeamento dos usos da terra mostrou que a região é predominantemente ocupada por usos antrópicos, que desempenham efeitos negativos para a qualidade ambiental e a conservação da biodiversidade. Embora tenha sido usado um conjunto simples de ferramentas de SIG para analisar a paisagem focal, esses métodos auxiliaram o entendimento de características da paisagem estruturalmente importantes no contexto regional, e os resultados obtidos mostraram-se interessantes para entender quais ações de conservação devem ser usadas para melhorar a manutenção da biodiversidade local ou regional, para garantir a longo prazo a manutenção dos ecossistemas agrícolas, e que, em futuras análises, a compreensão de como fauna e flora locais respondem às características da paisagem regional são os pontos-chave para garantir a manutenção da biodiversidade. Palavras-chave: Planejamento Ambiental, Estrutura da Paisagem, Manejo Sustentável, Sistemas de Informação Geográfica (SIG) REFERENCES 1 - CLARK LABS. IDRISI kilimanjaro software student user’s guide. Worcester: Clark University. 2003. 2 - CEMIN, G.; PERICO, E.; REMPEL, C. Composição e configuração da paisagem da sub-bacia do arroio jacaré, Vale do Taquari, RS, com ênfase nas áreas de florestas. Rev. Árvore, Viçosa, v. 33, n. 4, p. 705-711. 2009. 3 - CHRISTOFOLETTI, A. Morfologia de bacias de drenagem. Not. Geomorfol. v. 18, p.130-132, 1978. 4 - DEPARTAMENTO NACIONAL DE ÁGUAS E ENERGIA ELÉTRICA – ESTAÇÃO ECOLÓGICA DE SÃO CARLOS. Bacia experimental rio Jacaré-Guaçu. São Carlos: EESCUSP, 1980. 114 p. 3 - EASTMANN, J. R. Idrisi for Windows: introdução e exercícios tutoriais. (Trad.) HASENACK, H.; WEBER, E. Porto Alegre: UFRGS – Centro de Recursos Idrisi. 1998. 240p. 4 - FAHRIG, L. Effects of habitat fragmentation on 23 Revista SEB Ano 14 Final.indd 23 09/10/2012 13:43:54 Brazilian Journal of Ecology ISSN 1516-5868 biodiversity. Annu. Rev. Ecol. Evol. Syst, Palo Alto, v. 34, p. 487-515. 2003. 6 - GUERRA; A. J. T.; MENDONÇA, J. K. S. Erosão dos solos e a questão ambiental. In: VITTE, A. C.; GUERRA, A. J. T. (Orgs). Reflexões sobre a geografia física no Brasil. Rio de Janeiro: Bertrand Brasil, 2004. 280p. 7 - INSTITUTO BRASILEIRO DE GEOGRAFIA E ESTATÍSTICA. Diretoria de Serviço Geográfico do Exército Brasileiro. Folha SG.22-Y-C-II3MI-2885/3 – Frederico Westphalen. 1979. 8 - INSTITUTO NACIONAL DE METEOROLOGIA. Normais Climatológicas do Brasil 19611990. Versão revista e ampliada. Org.: RAMOS, A. M.; SANTOS, L. A. R.; FORTES, L. T. G. Brasília, DF: INMET, 2009. 465p. 9 - MAPINFO PROFESSIONAL. Guia do Usuário. Troy: MapInfo Corporation. 1998. 591p. 10 - MISSIO, E.; SANTOS, J.E; PIRES, J.S.R.; MARKOSKI, P.R.; TONIAL, T.M.. Caracterização, diagnóstico e zoneamento ambiental da paisagem do município de Frederico Westphalen, RS. In: : SANTOS J.E.; CAVALHEIRO, F.; PIRES, J.S.R.; HENKE-OLIVEIRA, C.; PIRES, A.M.Z.C.R. (Org.). Faces da polissemia da paisagem: ecologia, planejamento e percepção. São Carlos: RIMA, 2004. v. 1, p. 383-404. 11 - NUNES, J. O. R.; SANTANA-NETO, J. L. A produção do espaço urbano e o destino dos resíduos sólidos. Caderno Prudentino de Geografia, Presidente Prudente, v. 1, n. 24, p. 60-73, 2002. 12 - PISSARRA, T. C. T., POLITANO, W., FERRAUDO, A. S. Avaliação de características morfométricas na relação solo-superfície da Bacia Hidrográfica do Córrego Rico, Jaboticabal (SP). Rev. Bras. Ciênc. Solo, Viçosa, v. 28, n. 2, p. 297-305. 2004. 13 - RAMALHO-FILHO, A.; BEEK, K.J. Sistema de avaliação da aptidão agrícola das terras. 3. ed. rev. Rio de Janeiro: EMBRAPA/CNPS. 1995. 65p. 14 - RIBEIRO, M. C.; MARTENSEN, A. C.; METZGER, J. P.; TABARELLI, M.; SCARANO, F.; FORTIN, M. J. The Brazilian Atlantic Forest: a shrinking biodiversity hotspot. In: ZACHOS, F. E.; HABEL, J. C (Org.). Biodiver- sity hotspots. Berlin and Heidelberg: SpringerVerlag. 2011. 15 - ROCHA, J. V.; Sistema de informações geográficas no contexto do planejamento integrado de bacias hidrográficas. In: ORTEGA, E. (Org.). Engenharia ecológica e agricultura sustentável. Campinas: [s.n.], 2003. cap. 20, p. 1-13. 16 - SILVA, J.M.C., CASTELETI, C.H.M. Status of the biodiversity of the Atlantic Forest of Brazil. In: GALINDO-LEAL, C., CÂMARA, I.G. (Orgs.). The Atlantic Forest of South America: biodiversity status, threats, and outlook. Washington: CABS and Island Press, p. 43–59. 2003. 17 - SOS MATA ATLÂNTICA, INSTITUTO NACIONAL DE PESQUISAS ESPACIAIS. Atlas dos remanescentes florestais e ecossistemas associados no domínio da Mata Atlântica. São Paulo. 2000. 156p. 18 - STRAHLER, A. N. Dynamic basis of geomorphology. Bull. Geol. Soc. Am, v. 63, p. 923-938. 1952. 19 - STRECK, E. V.; KAMPF, N.; DALMOLIN, R. S. D.; KLAMT, E.; NASCIMENTO, P. C.; SCHNEIDER, P. Solos do Rio Grande do Sul. Porto Alegre: EMATER/RS, UFRGS, 2002. 107p. 20 - TEODORO, V. L. I.; TEIXEIRA, D.; COSTA, D. J. L.; FULLER, B. B. O conceito de bacia hidrográfica e a importância da caracterização morfométrica para o entendimento da dinâmica ambiental local. Ver. Uniara, Araraquara, n. 20, 2007. 21 - TONELLO, K.C.; DIAS, H. C. T.; SOUZA, A. L.; RIBEIRO, C. A. A. S.; FIRME, D. J.; LEITE, F. P. Diagnóstico hidroambiental da bacia hidrográfica da Cachoeira das Pombas, município de Guanhães, MG. Brasil. Ambi-Agua, Taubaté, v. 4, n. 1, p. 156-168. 2009. 22 - TONIAL, T. M.; MISSIO, E.; SANTOS, J. E. dos; HENKE-OLIVEIRA, C.; HOLZSCHUH, M. L.; ZANG, N. Diagnóstico ambiental de unidades da paisagem da região Noroeste do Estado do Rio Grande do Sul no período de 1984 a 1999. Rev. Bras. Cartografia, Presidente Prudente, v. 57, n. 3, p. 213-225, 2005. 23 - TUCCI, C.E.M. Hidrologia: ciência e aplicação. Porto Alegre, RS. Porto Alegre: UFRGS/ Edusp/ABRH, 2001. 943p. 24 Revista SEB Ano 14 Final.indd 24 09/10/2012 13:43:54 Brazilian Journal of Ecology ISSN 1516-5868 Structure of avian guilds in a bird fragment-corridor community in Lavras county, Minas Gerais, Brazil Bruno Senna Corrêa - CEFET-MG - Campus IX Nepomuceno - Av. Monsenhor - Luiz de Gonzaga, 103 - Centro, Nepomuceno, MG, CEP: 37250-000. (bruno.senna@gmail.com) Júlio Neil Cassa Louzada - UFLA – Caixa Postal 37 CEP 37200-000, Lavras, MG Campus Universitário, DBio Setor Ecologia. (jlouzada@dbi.ufla.br) Aloysio Souza Moura - Centro Universitário de Lavras “UNILAVRAS”, Caixa Postal 197, CEP 37200-000, Lavras, MG. (thraupidaelo@yahoo.com.br) ABSTRACT Analysis was centered on avian guild structure of a community of birds in a forest fragment|corridor|farming matrix complex in the Cerrado, in Lavras county, Minas Gerais, Brazil (21o14’45’’S/44o59’51’’W). Samples were collected from eight semidecidual forest fragments of 1,0 to 12,1 ha, connected by 5 hedgerow corridors bordered by an adjacent agricultural matrix. The hypothesis to be tested was whether the distribution of frequency, diversity and composition of the guilds was similar among the fragments, ecological corridors and matrix. 176 bird species belonging to 44 families were recorded. The main guilds recorded were insectivore, omnivore and granivore. The environments sampled proved to be statistically dissimilar as to guild distribution and composition. Composition can be altered by the various landscape components. As a whole, insectivore (68 species) and omnivore (53 species) guilds were predominant. Nevertheless, the average number of species in both was higher in the matrix and corridors, than in forest fragments. The latter, through functioning more as an efficient way of facilitating the movement of generalist species can mask the reduction in regional species richness. Key words: birds, forest fragments, avian guilds. INTRODUCTION Forest fragmentation, a historical process in the Cerrado biome, increased in the 20th century due to agricultural expansion in the Brazilian center-west. Among the outcomes of the consequential reduction in habitat, a decline in fauna and flora diversity could be observed. Even though there still are natural forest fragments in the Cerrado, it is not known whether the influence of ecological processes is similar to those observed in forest environments of the Atlantic Rain Forest and the Amazon Forest. The impact on tropical ecosystems originating from the fragmentation process has led to alterations in various parameters which, in turn, have given rise to the disappearance of insectivore guilds.(13). Notably, the decline in these guilds in small forest fragments is more strongly related to the capacity for dispersion by way of anthropic matrices than to the low availability of food resources (29). Research related to forest fragmentation involves the theory of isle biogeography and metapopulation dynamics (19). The former defines a diminishing in isle surface or fragments as being associated to an exponential decrease in the number of species, and the reduction in interspecies relationships (17). The formation of metapopulations is favored by habitat fragmentation, with each species occurring in a fragment, even though these populations can also occur in continuous habitats. The theory of metapopulations has supplanted that of isle biogeography through its potential to explain the dynamics of populations in fragmented areas. 25 Revista SEB Ano 14 Final.indd 25 09/10/2012 13:43:54 Brazilian Journal of Ecology ISSN 1516-5868 Forest mosaics or fragmentation can cause profound impacts on species that require large areas for survival. These, known as interior species, tend to quickly disappear in deforested or impacted areas. Meanwhile, under these circumstances, other species adapted to margin or ECOTONE conditions become dominant. Interior species can be maintained through adequate management, to so guarantee immigration from larger contiguous areas (17). From studies dealing with fragmented environments, it can be inferred that parameters, such as area (3), format and isolation, exert an influence on the distribution of the flora and the movement of wild fauna (28). Other ecological aspects of vegetal structures, such as succession stage, vertical stratification and heterogeneity, comprise important parameters in the determination of environmental avian guild OBJECTIVE In the present work, the response of the different avian guilds to the elements of a fragmented agricultural landscape was evaluated. The hypothesis to be tested was that the distribution of avian guild frequency, diversity and composition between forest fragments, ecological corridors and matrix remains unchanged. METHODOLOGY Study site The corridor-fragment studied is located in Lavras county, the Alto Rio Grande region, in the south of Minas Gerais State (21º17’15.1”S/44°58’59.3”W) (Figure 1). M2 M1 M3 M5 M4 Environments Áreas (ha) Physiognomy Successional stage Fragment diversity (21). Piratelli & Pereira (2002) emphasized Florest F1 7,19 Semid seas for Secondary F2 11,84 avian Semidguilds, seas for the importance of studying asSecondary a source F3 1,03 Semid seas for Secondary 7,36 Semid seas for Secondary of relevantF4F5 data on community trophic as 7,80 Semid seas for structures, Secondary F6 12,40 Semid seas for Secondary F7 2,25 Semid seas for Secondary well as abiotic parameters. AsSemidregards small F8 1,25 seas for SecondaryfragCorridors C1 0,2 Semidthe seas for quality Secondary ments, even though connected, of the C2 0,28 Semid seas for Secondary C3 0,44 Semid seas for Secondary habitat may be poor, and, the association C4 0,12 with Semid seas for Secondary of a C5 0,72 Semid seas for Secondary Matrix reduced area with anthropic disturbance in the surM1 71,0 Anthropized field Secondary M2 27,0 Agríc cultivation Secondary 24,0 Cerrado Secondary roundings,M3 viz., fire, agricultural defensives, invadM4 28,0 Cerrado Secondary M5 93,0 Anthropized field Secondary ing vegetal species, etc., the occurrence of popula51,16 Total fragments 1,76 Total corridors 243,0 Total matrix tions could become unfeasible, or there might even 295,92 Total be the exclusion of certain ecological groups (18). Points shown Sampling area (m2) Altitude Coordinates The study site is located around 6 km from 965 m 21 17’28’’S/44 59’13’’W 8 2513 m Lavras, onm the slopes of the21 Serra do Carrapato. In 971 m 17’43’’S/44 59’40’’W 8 2513 977 m 21 17’51’’S/44 59’13’’W 8 2513 m 973 m 21 18’08’’S/44 59’48’’W 8 2513 m all, there eight (F), 59’16’’W interlinked by a 977 mfragments 21 18’13’’S/44 8 2513are m 996 m 21 19’01’’S/44 59’47’’W 8 2513 m 990 m 21 19’01’’S/44 59’47’’W 8 2513 m vegetal corridor 1044 (C)m composed of a main axis and 21 19’13’’S/44 59’32’’W 8 2513 m four branches (Figure), in which seven 960 m 21 17’39’’S/44 59’10’’W of the frag8 628 m 985 m 21 17’38’’S/44 59’24’’W 8 628 m 996 m 21 17’58’’S/44 59’41’’W 8 628 m ments present an interior river course, within an ag991 m 21 18’17’’S/44 59’29’’W 8 628 m 1002 m 21 18’43’’S/44 59’35’’W 8 628 m ricultural matrix (old regional farming properties). 985 m 21 17’46’’S/44 59’23’’W 8 10053 m 980 m 21 17’33’’S/44 59’28’’W 8 10053 m The total of 997 them properties is 51,1624 ha, vary21 17’50’’S/44 59’43’’W 8 10053area m 934 m 21 18’33’’S/44 59’53’’W 8 10053 m 1022 m 8 10053 m O 21 18’49’’S/44 59’19’’W O ing from 1,0302 ha (21 17’51’’S/44 59’13’’W) to 64 20104 m 40 3140 m O O 40 50265 m 12,40 ha (21 19’01’’S/44 59’47’’W). The corridors 144 73509 m dealt with in the present study are defined as lin2 O O 2 O O 2 O O 2 O O 2 O O 2 O O 2 O O 2 O O 2 O O 2 O O 2 O O 2 O O 2 O O 2 O O 2 O O 2 O O 2 O O 2 O O 2 2 2 2 26 R= Revista SEB Ano 14 Final.indd 26 rb– rw___ N(N – 1)/4 09/10/2012 13:43:54 Brazilian Journal of Ecology ISSN 1516-5868 eal vegetal structures of various origins, of reduced width (between 3 and 6 meters), which can be connected to various-sized fragments (6). In the area studied, it was possible to identify: a) a farming matrix (M), comprising annual cultures, i.e., corn, soybean and beans, among others, planted pasture (Brachiaria spp.) for raising cattle, and M2 natural farmland. Through dealing with a fragmented area, the matrix was defined as any farming area, without any form of forest formation, such as forest fragments or vegetal corridors, since, M1 from the beginning of M3 th the 20 century, these phytophysiognomies have been gradually substituted by open areas, due to the regional expansion of agriculture; b) corridors of regenerating (30 years) arboreal vegetation occurring in hollows; c) portions of mosaic type M5 habitat, consisting of secondary stage cerrado M4 vegetation in the broad sense, secondary stage man-formed galleries and patches of secondary stage semideciduous forest (6). The climate of the region can be defined as of the Köppen Cwa type, with an average annual rainfall of 1.529,7 mm, and an average annual temperature of 19,4°C (5). The minimum altitude is 920 meters and the maximum 1.180 meters. Environments Fragment Florest F1 F2 F3 F4 F5 F6 F7 F8 Corridors C1 C2 C3 C4 C5 Matrix M1 M2 M3 M4 M5 Total fragments Total corridors Total matrix Total to a total of 132 days (924 hours) of field work. Work began at 5:30 a.m. and finished around 9:30 a.m. The visits took place twice a week, at twilight (4:00 p.m. to 7:00 p.m.). One and the same point was visited only once a day. The identification of species and the nomenclature used was according to basic references on the birds encountered in the Comitê Brasileiro de Registros Ornitológicos (2011). One of the parameters used for studying bird communities in closed environments is the composition of avian guilds (24). Trophic category analysis was applied to understanding bird community composition patterns within the system fragme nt|corridor|matrix. For guild characterization, information on the foraging form was used, whence, according to Pimm (1991), guilds could be defined as: Carnivores, Frugivores, Granivores, Insectivores, Nectarivores, Omnivores and Piscivores. In order to discern the differences in interenvironment guild composition, data was submitted to NMDS (nonmetric multi-dimensional scaling) analysis. Accordingly, the program is applied to calculating similarity among samples, by cartesian grouping of the more similar points, as to Áreas (ha) Physiognomy Successional stage Points shown Sampling area (m2) Altitude Coordinates 7,19 11,84 1,03 7,36 7,80 12,40 2,25 1,25 Semid seas for Semid seas for Semid seas for Semid seas for Semid seas for Semid seas for Semid seas for Semid seas for Secondary Secondary Secondary Secondary Secondary Secondary Secondary Secondary 8 8 8 8 8 8 8 8 2513 m2 2513 m2 2513 m2 2513 m2 2513 m2 2513 m2 2513 m2 2513 m2 965 m 971 m 977 m 973 m 977 m 996 m 990 m 1044 m 21O17’28’’S/44O59’13’’W 21O17’43’’S/44O59’40’’W 21O17’51’’S/44O59’13’’W 21O18’08’’S/44O59’48’’W 21O18’13’’S/44O59’16’’W 21O19’01’’S/44O59’47’’W 21O19’01’’S/44O59’47’’W 21O19’13’’S/44O59’32’’W 0,2 0,28 0,44 0,12 0,72 Semid seas for Semid seas for Semid seas for Semid seas for Semid seas for Secondary Secondary Secondary Secondary Secondary 8 8 8 8 8 628 m2 628 m2 628 m2 628 m2 628 m2 960 m 985 m 996 m 991 m 1002 m 21O17’39’’S/44O59’10’’W 21O17’38’’S/44O59’24’’W 21O17’58’’S/44O59’41’’W 21O18’17’’S/44O59’29’’W 21O18’43’’S/44O59’35’’W 71,0 27,0 24,0 28,0 93,0 51,16 1,76 243,0 295,92 Anthropized field Agríc cultivation Cerrado Cerrado Anthropized field Secondary Secondary Secondary Secondary Secondary 8 8 8 8 8 64 40 40 144 10053 m2 10053 m2 10053 m2 10053 m2 10053 m2 20104 m2 3140 m2 50265 m2 73509 m2 985 m 980 m 997 m 934 m 1022 m 21O17’46’’S/44O59’23’’W 21O17’33’’S/44O59’28’’W 21O17’50’’S/44O59’43’’W 21O18’33’’S/44O59’53’’W 21O18’49’’S/44O59’19’’W guild composition and abundance (7). This method Sampling Planning The Point (32) Sampling Method, with was basically used to represent differences in guild 10 minutes per point, was used for qualitative and composition in fragment, corridor and matrix environments. The Bray-Cutis similarity index was R = rb– rw___ quantitative surveying. used for analysis. N(N – 1)/4 Observations were carried out three times One-way ANOSIM testing was used to a week, between February and December, 2005, 27 Revista SEB Ano 14 Final.indd 27 09/10/2012 13:43:54 Secondary Secondary Secondary Secondary Secondary 8 8 8 8 8 628 m2 628 m2 628 m2 628 m2 628 m2 71,0 27,0 24,0 28,0 93,0 1,16 1,76 43,0 95,92 Anthropized field Agríc cultivation Cerrado Cerrado Anthropized field Secondary 8 10053 m2 960 m 985 m 996 m 991 m 1002 m 21O17’39’’S/44O59’10’’W 21O17’38’’S/44O59’24’’W 21O17’58’’S/44O59’41’’W 21O18’17’’S/44O59’29’’W 21O18’43’’S/44O59’35’’W 985 m 21O17’46’’S/44O59’23’’W 21O17’33’’S/44O59’28’’W 21O17’50’’S/44O59’43’’W 21O18’33’’S/44O59’53’’W 21O18’49’’S/44O59’19’’W Secondary 8 10053 m 980 m BrazilianSecondary Journal of Ecology ISSN 1516-5868 997 m 8 10053 m 2 2 Secondary Secondary 8 8 64 40 40 144 10053 m2 10053 m2 20104 m2 3140 m2 50265 m2 73509 m2 934 m 1022 m statistically verify the differences among groups formed by NMDS. This is a nonparametric test which, based on Bray-Curtis similarity (7), furnishes a way of testing whether there is a significant difference between two or more groups, according to the formula: R= rb– rw___ N(N – 1)/4 0.12 omnivores. -0.24 0.06 -0.16 -0.08 0.12 -0.06 Coordinate 2 Semid seas for Semid seas for Semid seas for Semid seas for Semid seas for 0.08 0.16 0.24 0.32 0.4 0.06 -0.12 -0.24 -0.16 -0.08 -0.18 Coordinate 2 0,2 0,28 0,44 0,12 0,72 0.08 0.16 0.24 0.32 0.4 -0.06 -0.24 -0.12 -0.3 -0.18 -0.36 rb average of all the distances among the groups r w average of all the distances within the groups N: samples -0.24 -0.3 Coordinate 1 -0.36 Figure 2. NMDS testing of inter-environment guilds (species diversity) (Symbols: + = fragment; o = The SIMPER (Analysis of similarity of percentages) test was used for examining the inter-environment contribution of each group, according to Bray-Curtis dissimilarity, and to determine the contribution of each to intra- environment similarity (7). Coordinate 1 corridor; ▲ = matrix). Figure 2. NMDS testing of inter-environment guilds (species diversity) (Symbols: + = fragment; o = corridor; ▲ = matrix). 0.36 RESULTS 0.24 Coordinate 2 0.36 0.18 0.3 0.12 0.24 0.06 0.18 Coordinate 2 176 bird species belonging to 44 families were registered. The main guilds were comprised of insectivores, omnivores and granivores . The insectivore guild presented the highest species richness with 68 species (38,0%) in fragment environments. Insectivore species richness was similar to that of omnivores in corridor environments (18 species each {10%}). As to the matrix environment, there was a reduction in insectivore species richness (21 species) in relation to omnivore (23 species). Behavior of the omnivore guild was the contrary to that of insectivores. There was a gradual rise in omnivore species richness matrixwise. In general, granivore species richness was inferior (22 species), followed by nectarivores (12 species), carnivores (11 species), frugivores (10 species) and piscivores (3 species). Distribution in the matrix was different from that of the other environments. In fragments and corridors distribution was more grouped (Figures 2 and 3). In axis 1, the omnivore guild contributed to the overall appearance of the fragment-corridor-matrix grid. In axis 2, there were differences in distribution among fragments, corridors and matrix. Once again, the greater contribution towards these differences came from the 0.3 -0.5 -0.4 -0.3 -0.2 -0.1 0.12 -0.06 0.1 0.2 0.3 0.4 0.06 -0.12 -0.5 -0.4 -0.3 -0.2 -0.18 -0.1 0.1 0.2 0.3 0.4 -0.06 Coordinat e 1 -0.12 Figure 3. NMDS testing of inter-environment guilds (number of -0.18 individuals) (Symbols: + = fragment; o = corridor; ▲ = matrix). Coordinat e 1 Analysis of similarity (ANOSIM) detected significant differences among the inter-environment individuals) (Symbols: + = fragment; o = corridor; ▲ = guilds studied, both by species (r = 0.67, P=0.0001, average matrix). dissimilarity =27.4), and individuals (r = 0.53; P<0.0001, average dissimilarity =34.2). Significant differences of guilds among the components of the system were obvious: Fragment and Corridor by species (r = 0.46, P<0.012, average dissimilarity=23.84); by individuals (r = 0.26, P<0.05, average dissimilarity=26.02); Fragment and Matrix by species (r = 0.70, P<0.001, average dissimilarity =29.83); by individuals (r = 0.76, P<0.008, average Figure 3. NMDS testing of inter-environment guilds (number of 28 Revista SEB Ano 14 Final.indd 28 09/10/2012 13:43:54 Brazilian Journal of Ecology ISSN 1516-5868 dissimilarity=42.13); Corridor and Matrix by species (r = 0.91, P<0.007, average dissimilarity=29.81); by individuals (r = 0.66, P<0.008, average dissimilarity = 35.81). The aim was to evaluate the importance of the guilds (Table 2). among the three cited environments, with higher average abundance in corridors (106) than in matrices (93.6) and fragments (76.3) (Table 4). Species Interactions Fragment x Corridor Fragment x Matrix Corridor x Matrix R 0.46 P 0.011 Average dissimilarity 22.84 0.70 0.001 29.83 0.91 0.007 29.81 R P 0.26 0.0448 0.76 0.0008 0.66 0.0079 Individuals Average dissimilarity 26.02 42.13 35.81 On separating the 3 environments DISCUSSION evaluated, viz., fragments, corridors and matrices, SIMPER species analysis showed that the Among the environments studied, the maAverage Average Average insectivore guild presented the most expressive trix abundance was clearly dissimilar to fragments and corabundance abundance in in result, 10.98 (40.44% accumulated). The average as regards aviancorridors guild structure, frequency in matrices fragments Guilds Contribution % Accumulated ridors, abundance of insectivore 10.98 species was greater Species Individuals Insectivores 40.44 in 27.8 The guilds 14 greatest relative 13.6 imand diversity. with Average Average dissimilarity fragments (27.8) than in corridors (14) and matrices Omnivores 4.13 55.67 13.2 portance15.4 in the matrix were the insectivore19.2 and omInteractions R secondP most abundant dissimilarity R P (13.6). Omnivores, Frugivores as the 3.91 70.09 2.25 0.6 nivore, thus corroborating studies on avian 7.8 guilds in 0.46 0.011 22.84 26.02 Fragment x Corridor 0.26 0.0448 guild, contributed (15.23% accumulated). Granivores with 4.1363.01 81.18 7.63 7.8The greater part 12.8of the tropical environments (23,9). 0.70 0.001 29.83 42.13 Fragment x Matrix 0.76 0.0008 Average omnivore abundance higher insectivores Carnivores 2.68 was a little 91.06 2.25 registered 1.4 6.4for the presented preference 0.91 0.007 29.81 35.81 Corridor x Matrix 0.66 0.0079 in the matrix (19.2) than in2.02 fragments (15.4) Nectarivores 98.5and 6 matrix. 6.25 In tropical forests,8.2 the high percentage of 100 0 0 0.8 corridorsPiscivores (13.2) (Table 3). 0.40 insectivore bird species is common (9;26). Guilds Guilds Insectivores Omnivores Granivores Frugivores Nectarivores Granivores Insetivores Carnivores Carnivores Nectarivores Frugivores Piscivores Piscivores Omnivores Average Average Average Average Average Average abundance abundance in abundance in % abundance abundance in matrices abundance corridors fragments Contribution % Accumulated Contribution Accumulated in27.8 fragments in 14 corridors in13.6 matrices 10.98 40.44 13.19 9.83 3.91 3.31 3.01 3.29 2.68 2.09 2.02 1.69 0.40 0.09 4.13 39.35 68.68 70.09 78.57 81.18 88.40 91.06 94.66 98.5 99.72 100 100 55.67 SIMPER analysis by individuals presented different results from those by species. The omnivore guild contributed with 13.19 (39.3% accumulated) towards distinction the 3 environments (fragments, % corridors and matrices) evaluated. Average omnivore Guilds Contribution Accumulated abundance was higher in matrices (191) than in Omnivores 13.19 39.35 corridors (107) and fragments (73.8). Granivores Granivores 9.83 68.68 contributed with 9.83 (29.33%) towards distinction Nectarivores Insetivores Carnivores Frugivores Revista SEB Ano 14 Final.indd Piscivores 29 3.31 3.29 2.09 1.69 0.09 78.57 88.40 94.66 99.72 100 73.8 76.3 2.25 21 7.63 40.5 2.25 12.1 6.25 6.88 0 0 15.4 107 106 0.6 43.4 7.8 50.2 1.4 4.2 8.2 5 0 0 13.2 191 93.6 7.8 21 12.8 23 6.4 22.6 6 16 0.8 1 19.2 Among insectivore guilds, most were Passeriformes (72,4%), with a predominance of species from the families Tyrannidae (21,7%) and FurnariAverage Average idaeAverage (18,8%). With the exception of insectivores abundance abundance abundance and omnivores, the matrix environment is normally in fragments corridors in matrices associated to places in which offer little attraction to 73.8 107 birds in fragmented landscapes (12). There 191 was a 76.3in the relative importance 106 93.6 reduction of insectivore 21 40.5 12.1 6.88 0 43.4 50.2 4.2 5 0 21 2329 22.6 16 09/10/2012 1 13:43:55 Granivores 3.01 81.18 Carnivores 2.68 91.06 Nectarivores 2.02 98.5 Piscivores 0.40 100 0 Brazilian Journal of Ecology ISSN 1516-5868 Guilds Omnivores Granivores Nectarivores Insetivores Carnivores Frugivores Piscivores Contribution 13.19 9.83 3.31 3.29 2.09 1.69 0.09 % Accumulated 39.35 68.68 78.57 88.40 94.66 99.72 100 and omnivore guilds, in corridor environments. Corridors, besides contributing towards reducing the isolation of these and other guilds, makes the conservation of diversity in farming areas possible (1). The use of corridors, by way of perches, shelters and food resources (33), facilitates the slightly more efficient distribution of forest bird guilds (11, 14, 16) Generally speaking, forest fragments presented low insectivore diversity, possibly related to variations in their structure (4). According to Ribon et al. (2003) and Develey & Metzger (2005), as habitat-specialist bird guilds are more sensitive to alterations in landscape elements, such as fragmentation, this could possibly account for local extinction. These aspects are thus relevant for enlightenment on the use of the most appropriate landscape elements for each guild. . As regards matrix environments, normally, omnivore guilds are the most relatively important, followed by granivores. In the present case, omnivore guilds were the most abundant (15.23%). This guild was mainly formed by Passeriformes (75,4%), predominantly by species of the family Thraupidae (24,5%). The greater omnivore density in relation to granivores presumes that alterations in a landscape are capable of inducing structural changes in the environment, which would reflect on local bird-guild abundance. Corroborating Willis (1976), the increase in omnivores is expected in small environments, since omnivorousness would have a buffer effect against fluctuations in the available food supply thereabouts. Habitat structure is a relevant factor in the composition of bird-guild communities in tropical environments (30). MacArthur & Whitmore (1979) noted that, depending on its size, guild 7.63 7.8 12.8 2.25 1.4 6.4 6.25 8.2 6 0 0.8 Average abundance in fragments 73.8 76.3 21 40.5 12.1 6.88 0 Average abundance in corridors 107 106 43.4 50.2 4.2 5 0 Average abundance in matrices 191 93.6 21 23 22.6 16 1 diversity in a forest fragment can endure distance from a source and the prevailing habitat structure. As regards the fragment environment, granivore guilds were relatively the most important, followed by the omnivores. Marini (2001) also registered the highest diversity of granivores in small forest patches of the cerrado. On the contrary, in the corridor environment, the omnivore guild presented the highest relative importance, followed by the granivores. In the highly man-formed environments, omnivore guilds were on the increase (23). In the matrix environments, granivore guilds presented the highest relative importance, followed by the omnivores. A guild distribution pattern in relation to the three environments sampled became apparent. This pattern indicated that guilds that are the most adaptable to an environment, and to establishing therein, are those capable of movement among landscape elements (31) (Figure 4). All the environments sampled appeared to undergo direct influence from the matrix. Through being reduced environments (1 to 12 ha), fragments functioned as islands, with the available resources limited to some, less sensitive, groups. Apparently, certain factors, such as original habitat loss and a reduction in remnants (2), are limiting factors to the presence of certain groups. . Guild distribution in the environments under study seemed to be linked to bird community composition and the physical structure of the vegetal mosaic. As to individuals, omnivore and granivore guilds were apparently predominant in corridors and matrices. The low frugivore density could be related to seasonal variation in the offer of fruits, and the dependency on fruits and insects (15). Semi-dependent insectivore guilds were observed in several frag- 30 Revista SEB Ano 14 Final.indd 30 09/10/2012 13:43:55 vores vores vores 2.09 94.66 12.1 4.2 22.6 1.69 99.72 6.88 5 Average 16 Average Average 0.09 100 0% 0 abundance 1 abundance abundance Guilds Contribution Accumulated in fragments in corridors in matrices Omnivores 13.19 39.35 73.8 107 191 Granivores 9.83 68.68 76.3 106 93.6 Journal of Ecology ISSN 1516-5868 Brazilian Nectarivores 3.31 78.57 21 43.4 21 Insetivores 3.29 88.40 40.5 50.2 23 granívoros. Os ambientes amostrados são ments and corridors. The 94.66 capacity of dispersion of 4.2 onívoros, 22.6 Carnivores 2.09 12.1 Frugivores 1.69 favored by 99.72 6.88and avail- 5 estatisticamente 16 dissimilares para a distribuição e these groups was the structure Piscivores 0.09 100 0 0 1 ability of landscape elements. . composição das guildas. A composição das guildas é alterada pelos diferentes componentes da paisagem. Houve predomínio das guildas de insetívoros (68 espécies) e de onívoros (53 espécies), de maneira geral. Contudo, a média de espécies da guilda de onívoros e granívoros foi maior na matriz e nos corredores que nos fragmentos. Os corredores ecológicos funcionam de maneira eficiente para o deslocamento de espécies generalistas, fato que pode mascarar a redução da riqueza de espécies na área. Palavras chave: aves, fragmentos florestais, guildas alimentares. REFERENCES Figure 4. Relative abundance of bird guilds in the three environments. CONCLUSION The response of the various avian guilds to the elements of a fragmented agricultural landscape showed the importance of insectivores in the separation of the three environments evaluated, viz., fragments, corridors and matrices. On considering species and individual analysis, it was noted that the distribution of frequency was not the same, the distribution of diversity remained the same, and avian guild composition was not maintained among the three. RESUMO Foi analisada a estrutura de guildas alimentares na comunidade de aves num sistema fragmento-corredor-matriz em ambiente de Cerrado, no município de Lavras, Minas Gerais (21o14’45’’S/44o59’51’’W). Foram amostrados oito (8) fragmentos de floresta estacional semidecidual de 1,0 a 12,1 ha, conectados por 5 corredores ecológicos delimitados por uma matriz agrícola adjacente. A hipótese a ser testada é se a distribuição da freqüência, diversidade e composição das guildas alimentares é similar entre os fragmentos, corredores ecológicos e matriz. Foram registradas 176 espécies de aves, pertencentes a 44 famílias. As principais guildas registradas foram insetívoros, 1- ARAÚJO GABRIEL, V de. Uso de cercas vivas por aves em uma paisagem fragmentada de mata atlântica semidecídua. 2005. 77 f. Dissertação (Mestrado em Ciências Biológicas) - Universidade Estadual Paulista “Júlio de Mesquita Filho”, Campus de Rio Claro. 2005. 2- BENNET, A. Habitat fragmentation. In: ATTIWILL, P.; WILSON, B. (Org.). Ecology an Australian perspective. Oxford: Oxford University, 2003. p. 440-456. 3- BIERREGAARD JUNIOR, R.O.; STOUFFER, P.C. Understory birds and dynamic habitat mosaics in Amazonian rainforest. In: LAURANCE, W. F.; BIERREGAARD JUNIOR, R. O. (Org.). Tropical forest remnants: ecology, management, and consevation of fragmented communities. Chicago: University of Chicago, 1997. p 138-155. 4- BLAKE, J. G.; LOISELLE, B. A.. Variation in resource abundance affects capture rates of birds in 3 lowland habitats in Costa Rica. Auk, Albuquerque, v. 108, n. 1, p. 114-130, 1991. 5- BRASIL. Ministério da agricultura e reforma agrária. Departamento Nacional de Meteorologia. Normas climatológicas: 1961-1990. Brasília: Editora da Universidade de Brasília, 1992. 132 p. 6- CASTRO, G. C. Análise da estrutura, diversidade florística e variações espaciais do componente arbóreo de corredores de vegetação na região do Alto Rio Grande, MG. 2004. 83 f. Dissertação (Mestrado em Engenharia Florestal) – Universi- 31 Revista SEB Ano 14 Final.indd 31 09/10/2012 13:43:57 Brazilian Journal of Ecology ISSN 1516-5868 dade Federal de Lavras, Brasil. 2004. 7- CLARKE, K. R. Non-parametric multivariate analysis of changes in community structure. Australian Journal of Ecology, Canberra, v. 18, n. 1, p. 117-143, 1993. 8- COMITÊ BRASILEIRO DE REGISTROS ORNITOLÓGICOS. Listas das aves do Brasil. 2011. Versão 24/02/2005. Disponível em: <http:// www.cbro.org.br>. Acesso em: [02 abril. 2011]. 9- DARIO, F. R. Influência de corredor florestal entre fragmentos da mata atlântica utilizando-se a avifauna como indicador ecológico. 1999. 172 f. Dissertação (Mestrado em Ciências) – Escola Superior de Agricultura “Luiz de Queiroz”, Universidade de São Paulo. Brasil. 1999. 10-DEVELEY, P. F.; METZGER, J. P. Birds in Atlantic forest landscapes: effects of forest cover and configuration. In: LAURANCE, W; PERES, C. A. (Org.). Emerging threats to tropical forests. Chicago: University of Chicago, 2005. p. 269-289. 11-ESTRADA, A.; COATES-ESTRADA, R.; MERITT JUNIOR, D. A. Anthropogenic landscape changes and avian diversity at Los Tuxtlas, Mexico. Biodiversity and Conservation, London, v. 6, n. 1, p. 19-43, 1997. 12-ESTRADA, A.; CAMMARANO, P.; COATESESTRADA, R. Bird species richness in vegetation fences and in strips residual rain forest vegetation at Los Tuxtlas, Mexico. Biodiversity and Conservation, London, v. 9, n. 10, p. 1399-1416, 2000. 13-FORD, H. A.; BARRET, G.; SAUNDERS, D.; RECHER, H. Why have birds in the woodlands of Southern Australia declined? Biological Conservation, Cambridge, v. 97, n. 1, p. 71-88, 2001. 14-GIMENES, M. R.; ANJOS, L. Efeitos da fragmentação florestal sobre as comunidades de aves. Acta Scientiarum Biological Sciences, Maringá, v. 25, n. 2, p. 391-402, 2003. 15-GOMES, V. S. M.; SILVA, W. R. Spatial variation in understory frugivorous birds in an Atlantic Forest fragment of southeastern Brazil. Revista Brasileira de Ornitologia, Ararajuba, Rio de Janeiro, v. 10, n. 2, p. 219-225, 2002. 16-HADDAD, N.; BOWNE, D. R.; CUNNINGHAM, A.; DANIELSON, B. J.; LEVEY, D. J.; SARGENT, S.; SPIRA, T. Corridor use by diverse taxa. Ecology, Amsterdam, v. 84, n. 3, p. 609-615, 2003. 17-HANSKI, I.; GILPIN, M.E. Metapopulation dynamics: brief history and conceptual domain. In: HANSKI, I.; GILPIN, M.E. (Org.). Metapopulation dynamics: empirical and theoretical investigations. London: Academic, 1991. p. 3-16. 18-JANSEN, D.H. The eternal external threat. In: SOULÉ, M.E (Org.). Conservation biology: the science of scarcity and diversity. Dordrecht: Sinauer Associates, 1986. p. 286-303. 19-KORMAN, V. Proposta de integração das glebas do Parque Estadual de Vassununga, Santa Rita do Passa Quatro, SP. 2003. 131 f. Dissertação (Mestrado em Ecologia de Agroecossistemas) – Escola Superior de Agricultura “Luiz de Queiroz”, Universidade de São Paulo, Piracicaba. Brasil. 2003. 20-MAC ARTHUR, R. H.; WHITMORE, R. C. Passerine community composition and diversity in man-altered environments. Morgantown, West Virginia, n. 7, v. 1, p. 1-12, 1979. 21-MARINI, M. A. Efeitos da fragmentação florestal sobre as aves de Minas Gerais. In: SANTOSALVES, M. A.; SILVA, J. M. C.; SLUYS, M.; BERGALLO, H. G.; ROCHA, C. F. D. (Org.). A ornitologia no Brasil: pesquisa atual e perspectivas. Rio de Janeiro: UERJ, 2000. p. 41-54. 22-MARINI, M. A. Effects of forest fragmentation on birds of the cerrado region, Brazil. Bird Conservation International, Cambridge, n. 1, v. 11, p. 11-23, 2001. 23-MOTTA JÚNIOR, J.C. Estrutura trófica e composição das avifaunas de três habitats terrestres na região central do Estado de São Paulo. Revista Brasileira de Ornitologia, Ararajuba, Rio de Janeiro, v. 1, n. 6, p. 65-71, 1990. 24-PIMM, S.L. The balance of nature?: ecological issues in the conservation of species and communities. Chicago: University of Chicago, 1991. 448 p. 25-PIRATELLI, A.; PEREIRA, M.R. Dieta de aves na região leste de Mato Grosso do Sul, Brasil. Revista Brasileira de Ornitologia, Ararajuba, Rio de Janeiro, v. 10, n. 2, p. 131-139, 2002. 26-POZZA, D.D. Composição da avifauna da Estação Ecológica de São Carlos (Brotas-SP) e reserva ambiental da fazenda Santa Cecília (Patrocínio Paulista-SP), São Carlos-SP. 2002. 89 f. Dissertação (Mestrado em Ecologia e Recursos Naturais) - Universidade Federal de São Carlos, São Carlos. 2002. 32 Revista SEB Ano 14 Final.indd 32 09/10/2012 13:43:57 Brazilian Journal of Ecology ISSN 1516-5868 27-RIBON, R.; SIMON, J. E.; MATTOS, G. T. Bird extinctions in Atlantic Forest Fragments of Viçosa Region, Southeastern Brazil. Conservation Biology, Malden, v. 17, n. 6, p. 1827-1839, 2003. 28-SAUNDERS, D. A.; HOBBS, R. J. Nature conservation 2: the role of corridors. Chipping Norton: Surrey Beatty & Sons Pty, 1991. 442 p. 29-SEKERCIOGLU, C. H.; EHRLICH, P.; DAILY, G. C.; AYGEN, D.; GOEHRING, D.; SANDI, R. F. Disappearance of insectivorous birds from tropical forest fragments. PNAS, Oklahoma City, v. 99, n. 1, p. 263-267, 2002. 30 -TERBORGH, J. Habitat selection in Amazonian birds. In: CODY, M.L. (Org.). Habitat selection in birds. New York: Academic, 1985. p. 311-338. 31-UEZU, A.; METZGER, J. P.; VIELLIARD, J. M. E. Effects on structural and functional connec- tivity and patch size on the abundance of seven Atlantic Forest bird species. Biological Conservation, Cambridge, v. 123, n. 4, p. 507-519, 2005. 32-VIELLIARD, J; SILVA, W. R. Nova metodologia de levantamento quantitativo e primeiros resultados no interior do Estado de São Paulo. In: ENCONTRO NACIONAL DE ANILHADORES DE AVES, 4, 1989, Recife. Anais... Recife: UFRPe, 1989. p. 117-151. 33-WEGNER, J. F.; MERRIAM, G. Movements by birds and small mammals between a wood and adjoining farmland habitats. Journal of Applied Ecology, Oxford, v. 16, n. 1, p. 349-357, 1979. 34-WILLIS, E. O. Effects of a cold wave on an Amazonia avifauna in the upper Paraguay Drainage, western Mato Grosso, and suggestions on oscine-suboscine relationships. Acta Amazonia, Manaus, v. 6, n. 3, p. 379-394, 1976. 33 Revista SEB Ano 14 Final.indd 33 09/10/2012 13:43:57 Brazilian Journal of Ecology ISSN 1516-5868 34 Revista SEB Ano 14 Final.indd 34 09/10/2012 13:43:57 Brazilian Journal of Ecology ISSN 1516-5868 Emergence and growth of Ateleia glazioveana Baill. seedlings in direct sowing in an early secondary succession stage Ana Claudia Escaio - Universidade Regional do Noroeste do Estado do Rio Grande do Sul, Depto. de Biologia e Química, bolsista PET/SESu/MEC (acescaio@gmail.com) Geodeli Adelita Penz Corrêa - Universidade Regional do Noroeste do Estado do Rio Grande do Sul, bolsista PET/SESu/MEC, Depto. de Biologia e Química (geodelli@yahoo.com.br) Jonas Darci Noronha de Lima - Universidade Regional do Noroeste do Estado do Rio Grande do Sul, Depto. de Biologia e Química (jonasnoronha@yahoo.com.br) * Geraldo Ceni Coelho – Universidade Federal da Fronteira Sul (cenicoelho@gmail.com) ABSTRACT Ateleia glazioveana Baill. (Fabaceae), a pioneer tree species from south and southeastern Brazil, reaches a high population density in Seasonal Forests. The aim was to analyze the emergence, growth and survival of A. glazioveana seedlings under natural conditions. The experiment was installed in an eleven-year-old post-agricultural site, with herbaceous vegetation in an early stage of secondary succession. The plots measured 2 x 3 m, with four random replications in four blocks. The experimental design was factorial 2 x 2 x 2, in two different conditions of vegetation management (with and without the removal of herbaceous and shrubby plants), two levels of fertilizer (with and without the addition of 33 g/m 2 of NPK 4:20:12), and with and without seed sowing. Each plot received 200 seeds, i.e., 33 seeds/m2. Dates of emergence and survival were recorded at the second, fifth and twelfth months. Growth data (height and diameter) were obtained after 12 months. Spontaneous emergence was nil. Emergence from direct sowing reached a total of 48 (1.5%) seedlings after two months, and 77 (2.4%) after 12 months, from which 56 survived ,viz. 5,833 per hectare. Although the removal of vegetation had no effect on seedling height and survival, diameters were increased. Moreover, differences with the addition of fertilizer were insignificant. The average height was 11.96 cm (± 4.08). Direct sowing was viable. Even so, frost damage after the winter of 2010 was general, thus indicating the possibility of microclimate limitations to recruitment. Key words: secondary succession, Forest restoration, Semideciduous Seasonal Forest. INTRODUCTION Although pre-colonial cover by Subtropical Semideciduous Forest was 1,000,000 km2, including Brazil, Argentina and Paraguay, nowadays this has been reduced to only 6% of the original area (4). The remnants present high reduction and fragmentation, with an expressive degree of isolation (23). Forest fragmentation leads to significant modifications in the composition, structure and dy- namics of local communities and populations, with a corresponding reduction in species habitat and ecological niche (19). Forest restoration could be helpful in reducing wild ecosystem fragmentation, promoting the improvement of degraded areas, and recovering environmental services. Seedling planting with a combination of tree species from different successional groups, is a frequently used method for restoring forest cover (16,15, 24). Notwithstanding, direct sowing and spontaneous regeneration are 35 Revista SEB Ano 14 Final.indd 35 09/10/2012 13:43:57 Brazilian Journal of Ecology ISSN 1516-5868 promising alternatives for minimizing costs, and making restoration feasible from a socioeconomic point of view (10). Direct sowing is particularly recommended for both pioneer and early secondary species, and for sites without vegetal cover. It is also recommended for late successional species in secondary forest enrichment (15). Secondary succession is the transformation, over time, of the community structure, following a local disturbance (13). The first species to colonize a given site are denominated pioneers. Pioneers are capable of facilitating, hindering, or simply playing a neutral role, in the settlement and growth of other species (9). Plant population renewal or recruitment presents a series of limitations. These limiting factors can be divided into three groups, namely source and fecundity, dispersion and establishment. The source and fecundity refers to limitations in seed production by adult plants. Such limitations could be related to climate variation (lack or excess of rain, late frosts, etc.) or biotic factors (lack of pollinators and flowers, or fruit predation). Moreover, seed availability, besides being variable year to year, is also affected by landscape structure and the size of neighboring, wild remnant vegetation. Dispersion efficiency depends on the available dispersion agents and propagule quality (8). A. glazioveana is wind-dispersed, so that the force, amount and direction of the winds are all determinant for dispersion efficiency. Establishment factors refer to seedling survival and development. Losses throughout the process could be due to predation, competition or the inadaptability of seedlings to local ecological conditions. In the case of early succession stages in abandoned cropland (old-field succession), competition with herbs and climbing plants could be the most limiting factor for woody species (5). Herbaceous vegetation withdrawal or topsoil removal could improve the germination rates and early growth of woody species (25,12). Ateleia glazioveana Baill. (Fabaceae), a pioneer tree species in Seasonal Subtropical Forest and secondary forest formations in south and southeastern Brazil, Argentina (Misiones) and Paraguay, is outstanding by its high-capacity to occupy sites with adverse conditions. The fruit is an orbicular, sa- maroid, indehiscent legume with only one seed that reaches maturity between May and August. Dispersion is anemochoric (6). The species, through association with nitrogen fixative bacteria, provides an excellent green manure. The foliage in dry matter can reach 3.5 to 4.9 % of nitrogen (1). This species, dominant in the first stages of forest succession, remains as a canopy component in the late succession stages and frequently forms spontaneous monospecific stands denominated ‘timbozais’ in the vernacular (2). Thus, the presence and regeneration of A. glazioveana can play a key role in nutrient cycling processes and the recruitment of other species. The aim was to evaluate spontaneous and induced recruitment through the direct sowing of A. glazioveana seeds under various management conditions. The experiment was carried out in an 11-year-old post-agricultural site with herbaceous vegetation in an early stage of secondary succession. The spontaneous emergence of other tree species was also quantified. METHODOLOGY Study site The experiment was carried out in a forest remnant named ‘Mato do Silva’, in Chiapetta, State of Rio Grande do Sul, Brazil (27° 55’ 02” S and 53° 53’ 18” W). The climate is SL PU perhumid subtropical, with an average annual temperature of 19 ºC, and annual rainfall of 1,800 mm (17). The altitude ranges between 400 and 472 m above mean sea level. The forest remnant comprises 240 ha of late successional semi-deciduous seasonal forest, and around 50 ha of areas of secondary herbaceous or secondary forest vegetation (2). The area of the experiment was an abandoned cropland, which after 11 years has become dominated by Poaceae such as Saccharum villosum Steud. (dominant), Schizachyrium microstachyum (Ham.) Roseng. et al., Leersia hexandra Sw., and Calamagrostis viridiflavescens Steud. Sparse individuals of various woody species also occur, especially Schinus terebinthifolius Raddi and Aegiphila brachiata Vell. The topographic level ranges between 402 and 403 m above mean sea level (Figure 1). The late successional Semi-deciduous Seasonal Forest begins 100 meters from the 408 m quota. 36 Revista SEB Ano 14 Final.indd 36 09/10/2012 13:43:57 The experiment was carried out in a forest remnant named ‘Mato do Silva’, in Chiapetta county, State of Rio Grande do Sul, Brazil (27° 55' 02” S and 53° 53' 18" W). The climate is SL PU perhumid subtropical, with an average annual temperature of 19 ºC, and annual rainfall of 1,800 mm (17). The altitude ranges between 400 and 472 m above mean sea level. The forest remnant comprises 240 ha of late successional semi-deciduous seasonal forest, and around 50 ha of areas of secondary herbaceous or secondary forest vegetation (2). The area of the experiment was an abandoned cropland, which after 11 years has become dominated by Poaceae such as Saccharum villosum Steud. (dominant), Schizachyrium microstachyum (Ham.) Roseng. et al., Leersia Brazilian Journal of Ecology ISSN 1516-5868 hexandra Sw., and Calamagrostis viridiflavescens Steud. Sparse individuals of various woody species also occur, Seed germination capacity, determined in a greenhouse in the IRDeR- Instituto Regional de Desenvolvimento Rural (UNIJUÍ), at ambient temperature and in a PLANTMAX ® substrate (a mixture of vermiculite and Pinus residues), was 55%. Statistical Analysis Figure 1. Topographic diagram in a northeast-southwest direction between the Inhacorá River, on the left, and the Considering as experimental factors vegbeginning of secondary forest dominated by A. glazioveana, on the right. The arrow indicates the location of the experiment, the quotas 402 and 403 m above sea level.in a northeast-southwest Figurebetween 1. Topographic diagram etation removal and the addition of fertilizer, analydirection between the Inhacorá3 River, on the left, and the sis of seedling emergence with direct sowing was beginning of secondary forest dominated by A. glazioby one-factor ANOVA, whereas comparative analyveana, on the right. The arrow indicates the location of sis of maximum height and diameter was by twothe experiment, between the quotas 402 and 403 m above factor ANOVA. Seeing that emergence without seed sea level. sowing under the prescribed conditions was zero, Table 1. Soil physiochemical profile in an old-field with these experiments were excluded from the analysis. Physicochemical soil data were provided by UNIJUÍ Soil Laboratory (Table 1). especially Schinus terebinthifolius Raddi and Aegiphila brachiata Vell. The topographic level ranges between 402 and 403 m above mean sea level (Figure 1). The late successional Semi-deciduous Seasonal Forest begins 100 meters from the 408 m quota. Physicochemical soil data were provided by UNIJUÍ Soil Laboratory (Table 1). secondary vegetation, Mato do Silva, Chiapetta-RS, Brazil, 2009. Table 1. Soil physiochemical profile in an old-field with secondary vegetation, Mato do Silva, Chiapetta-RS, Brazil, 2009. pH P K S Cu Zn Mn Ca Mg Al CEC H + Al (pH = 7.0) V% M% O.M. (%) 71.0 0.0 4.0 RESULTS Emergence only occurred in treatments with sowing (Table 2), thus spontaneous emergence was nil. After one year, there was no significant difexperimental protocol ference among treatments as regards emergence or Experimental protocol Seeds of A. glazioveana, gathered between July and September, 2009, were first cleaned and then stored at room the number of remnant seedlings. The highest emertemperature in sealed recipients.of It was by casting was in October, 2009, in plots measuring 2 x 3 m. Data on Seeds A.Ssowing glazioveana, gathered between gence rate occurred in the first 60 days, reaching 48 emergence, survival and growth were obtained between December, 2009 and October, 2010. The experimental design July and 2009, were firstmanagement, cleaned was factorial 2 x 2 xSeptember, 2, under two adverse different conditions of vegetation viz., withand and without the seedlings. After one year, 77 seedlings had emerged removal of herbaceous and shrubby plants, with and without the addition of fertilizer, and with and without seed then stored at room temperature in sealed recipisowing. (Figure 2), corresponding to a density of 8,021 seedThe fertilizer used was 33 g/m of NPK 200Two hundred corresponding to 33 per m , were sowed ents. It was sowing by4:20:12. casting was seeds, in October, 2009, in each plot. lings per ha. in plots measuring 2replications x 3 m.distributed Dataat random, on emergence, surEach treatment consisted of four one per block. The blocks were located in Table 2. Survivor seedlings (% of seeds) of transverse strips in relation to the slope of the site. The northward-sloping inclination of the site was 2%. vivalEmergence and growth were obtained between December, and survival were recorded after 60 days (December, 2009), 150 days (March, 2010) and one year Ateleia glazioveana obtained through direct sowing, (October, 2010). After one year, the maximum height and the diameter of the basal portion of the stem were measured 2009 and October, 2010. The experimental design with ruler and pachymeter. Mato do Silva, Chiapetta-RS, 2009-2010. There was Table 2. Survivor seedlings (% of seeds) of Ateleia glazioveana obtained through direct sowing, Mato do Silva, germination capacity, IRDeR-different Instituto Regional de Desenvolvimento was Seed factorial 2 xdetermined 2 x in2,a greenhouse underin thetwo conno difference atwasany timeatamong Rural (UNIJUÍ), at ambient temperature and in a PLANTMAX ® substrate (a mixture of vermiculite and Pinus Chiapetta-RS, 2009-2010. There no difference any time amongtreatments treatments (P > 0,05).(P > 0,05). ditions of vegetation management, viz., with and residues), was 55%. R RF NR NRF Total without the removal of herbaceous and shrubby December, 2009 2.1 1.4 0.9 1.6 1.5 statistical Analysis plants, with and without the addition of fertilizer, March, 2010 0.9 1.4 4.6 0.4 1.8 Considering as experimental factors vegetation removal and the addition of fertilizer, analysis of seedling and with and without seed sowing. October, 2010 0.5 1.4 4.9 0.3 1.8 emergence with direct sowing was by one-factor ANOVA, whereas comparative analysis of maximum height and diameter was by two-factor ANOVA. Seeing that emergence without seed sowing under2the prescribed conditions was of vegetation without fertilizer, RF = removal of vegetation with fertilizer, NR = without both vegetation The fertilizer used was 33 g/m of NPK RR= removal zero, these experiments were excluded from the analysis. = removal of vegetation without fertilizer, RF = reremoval and fertilizer, NRF = without vegetation removal, but with the addition of fertilizer 4:20:12. Two hundred seeds, corresponding to 33 moval of vegetation with fertilizer, NR = without both RESULTS 2 per m , were sowed in each plot. vegetation removal and fertilizer, NRF = without vegetaBetween 150 days and one year, 21 seedlings (36% of the total emergence) had disappeared, the remaining 56 As eEmergence only occurred in treatments with sowing (Table 2), thus spontaneous emergence was nil. removal, but with the addition of fertilizer Each treatment consisted of four replica- thustion After one year, there was no significant difference among treatments as regards emergence or the number of corresponding to a density of 5,833 seedlings per hectare. remnant seedlings. The highest emergence rate occurred in the first 60 days, reaching 48 seedlings. After one year, 77 tions distributed at random, one per block. The As to average height, no difference was observed among treatments, the overall average height reaching11.96 seedlings had emerged (Figure 2), corresponding to a density of 8,021 seedlings per ha. Between 150 days and one year, 21 seedblocks were located in transverse strips in relation cm ( ± 4.08). 4 of the totalin treatments emergence) disappeared, to the slope of the site. The northward-sloping incli- lings The (36% average diameter of seedlings with vegetationhad removal was higher than those without the remaining 56 thus corresponding to a density of removal. There was no significant difference with the addition of fertilizer (Table 3 and Figure 3). nation of the site was 2%. th On the 60 day, three seedlings of other species were observed, two of Eugenia uniflora L. and one of Emergence and survival were recorded 5,833 seedlings per hectare. Allophylus edulis (A. St.-Hil.) Niederl. One E. uniflora seedling disappeared between 150 days and one year. As to average height, no difference was obafter 60 days (December, 2009), 150 days (March, In October, 2010, all the seedlings presented signs of frost damage, which caused loss of the shoot apex and among treatments, the overall average height 2010) and one year (October, 2010). After one year, theserved absence of lateral bud expansion. reaching11.96 cm (± 4.08). the maximum height and the diameter of the basal The average diameter of seedlings in treatportion of the stem were measured with ruler and ments with vegetation removal was higher than those pachymeter. mg/dm³ 5.9 4.2 73.0 4.3 8.3 cmolc/dm³ 4.9 2 54.1 7.0 2.9 0.0 4.2 14.6 2 37 Revista SEB Ano 14 Final.indd 37 09/10/2012 13:43:57 Table 2. Survivor seedlings (% of seeds) of Ateleia glazioveana obtained through direct sowing, Mato do Silva, Chiapetta-RS, 2009-2010. There was no difference at any time among treatments (P > 0,05). R RF NR NRF Total December, 2009 2.1 1.4 0.9 1.6 1.5 October, 2010 0.5 1.4 4.9 0.3 Brazilian Journal ISSN 1516-5868 March, 2010 0.9 of Ecology 1.4 4.6 0.4 1.8 1.8 without removal. There was no significant difference DISCUSSION removal and fertilizer, NRF = without vegetation removal, but with the addition of fertilizer with the addition of fertilizer (Table 3 and Figure 3). Between 150 days and one year, 21 seedlings (36% of the total emergence) had disappeared, the remaining 56 On the 60th day, three seedlings of other Seedling emergence only occurred in treatthus corresponding to a density of 5,833 seedlings per hectare. As to average no difference wastwo observed treatments, theuniflora overall average height species wereheight, observed, ofamong Eugenia L. reaching11.96 ments that received seeds. The absence of spontanecm (± 4.08). and The one of Allophylus edulis (A. St.-Hil.) Niederl. ous emergence could be explained by insufficient average diameter of seedlings in treatments with vegetation removal was higher than those without removal. no significantseedling difference with thedisappeared addition of fertilizer (Table 3 and Figure 3). One There E. was uniflora between 150 seed dispersion or high predation prior to initiating On the 60 day, three seedlings of other species were observed, two of Eugenia uniflora L. and one of days and one year. Allophylus edulis (A. St.-Hil.) Niederl. One E. uniflora seedling disappeared between 150 days and one year. the experiment. Furthermore, data on sowed plots In October, 2010, all the seedlings presented signs of frost damage, which caused loss of the shoot apex and In October, 2010, all the seedlings present- showed that emergence continued after 150 days the absence of lateral bud expansion. ed signs of frost damage, which caused loss of the (after April, 2010), a sure indication that the winshoot apex and the absence of lateral bud expansion. ter of that year was not severe enough to hinder the R = removal of vegetation without fertilizer, RF = removal of vegetation with fertilizer, NR = without both vegetation th course of seedling emergence. Curiously, although local seed rain was apparently insufficient, the production of seeds was high during 2009 and A. glazioveana is abundant in the vicinity, reaching dominance above the quota 405 m. a. s. L., 70 m from the experiment (7). The addition of fertilizer caused no increase in seedling growth during the first year. As a rule, pioneer tree species respond to fertilization with an increase in growth, whereas late succesFigure 2. As a sum of all treatments, accumulated emergence (dashed line) and survival (solid line) of A. glazioveana Table 3. Two-factor ANOVA results for theall variable ‘diameter’; comparison among treatments R, RF (with vegetation Figure 2. As a sum of treatments, accumulated emersional species respond either weakly or insignifiseedlings in direct sowing, Mato do Silva, Chiapetta, State of Rio Grande do Sul, 2009-2010. removal) and NR, NRF (without vegetation removal). * indicates P < 0.05. gence (dashed line) and survival (solid line) of A. glaziocantly (21). To several species, with direct sowing, Source of Variation Df Mean square F P 5 Mato veana seedlings in direct sowing, do Silva, ChiaInteraction 1 1.19 0.834 0.368 both in greenhouse (3), and in the field (14), the petta, State of Rio Grande do Sul, 2009-2010. Vegetation removal 1 6.25 * 4.375 0.045 * addition of fertilizers or organic soil increases Fertilizer added 1 0.358 0.251 0.620 seedling growth. Table ANOVA results for the variable Residual 3. Two-factor 30 1.43 The removal of vegetation induced an in‘diameter’; comparison among treatments R, RF (with vegetation removal) and NR, NRF (without vegetation crease in stem diameter, since the presence of herTable 3. Two-factor ANOVA results for the variable ‘diameter’; comparison among treatments R, RF (with vegetation removal). * indicates P < 0.05. baceous plants can reduce light intensity, a possible removal) and NR, NRF (without vegetation removal). * indicates P < 0.05. cause of thinner stems. In spite of such low-lightSource of Variation Df Mean square F P Interaction 1 1.19 0.834 0.368 intensity conditions are capable of inducing an inVegetation removal 1 6.25 * 4.375 0.045 * crease in height, damage to the shoot apex caused by Fertilizer added 1 0.358 0.251 0.620 the frosts of 2010 supposedly prevented differences Residual 30 1.43 among treatments. Shoot-apex damage, which suggests sensitivity to frost in the seedling stage, could have been a limiting factor to species settlement. The experiment was located 150 meters from, and less than one meter above, the Inhacorá River, thus favorable to the occurrence of subzero temperatures, since cold air tends to move to lower topographic levels (20). The species is considered only moderately tolerant to cold, whereby it presents growth limitations Figure 3. Stem basal diameter (mm) of A. glazioveana seedlings after oneof year A. of direct sowing in Mato do Silva, Figure 3. Stem basal diameter (mm) glazioveana subjected to heavy frosts during experimental Chiapetta county, State of Rio Grande do Sul, 2010. Treatments R and RF are with vegetation removal, treatmentswhen NR seedlings after one year of direct sowing in Mato do and NRF, without. The gray columns indicate the addition of fertilizer (33 g/m of NPK 4:20:12). Vertical bars indicate planting (6). Furthermore, as wind intensity can be standard error. Silva, Chiapetta, State of Rio Grande do Sul, 2010. Treatlow in the bottom of valleys, seed dispersion is less 6 ments R and RF are with vegetation removal, treatments and consequently recruitment reduced. NR and NRF, without. The gray columns indicate the ad2 dition of fertilizer (33 g/m of NPK 4:20:12). Vertical bars Seedling height after one year of experiindicate standard error. mentation can be considered low when compared 2 38 Figure 3. Stem basal diameter (mm) of A. glazioveana seedlings after one year of direct sowing in Mato do Silva, Revista SEB Ano 14 Final.indd 38 09/10/2012 13:43:58 Brazilian Journal of Ecology ISSN 1516-5868 with other experimental studies with direct sowing. For example: Soares & Rodrigues (2008) recorded a wide variation in the heights of Fabaceae tree species sowed in abandoned cropland, of 30 cm for Bowdichia virgilioides Kunth to 3 m for Acacia polyphylla DC, after 13 months; Mattei & Rosenthal (2002) registered heights between 29 and 66 cm for Peltophorum dubium (Spreng.) Taub., in secondary forest enrichment through direct sowing, after 18 months; Engel & Parrotta (2001) observed heights ranging from 20 cm (Ceiba speciosa [A. St.-Hil] Ravenna) to 170 cm for Schizolobium parahyba (Vell.),Blake, after two years of direct sowing in Botucatu, São Paulo; Camargo et al. (2002),noted heights ranging between 38 and 85 cm for Caryocar villosum Aubl., and 20 and 45 cm for Parkia multijuga Benth. in Amazonia, after one year of direct sowing; and finally, Ferreira et al. (2007) reported heights ranging from 200 to 250 cm after 15 months of direct sowing for Trema micrantha (L.) Blüme, Senna multijuga (L. C. Rich) Irwin & Barneby, S. macranthera (Collad.) Irwin & Barneby, and Solanum mauritianum Scopoli. Data indicate that the regeneration of A. glazioveana through direct sowing is viable, even without vegetation removal. On the other hand, the occurrence of severe frosts car hamper species survival and recruitment. Direct sowing, though being a low-cost restoration method, requires a longer period of monitoring, in order to check whether plants can reach sufficient densities, to so establish a viable forest structure. ACKNOWLEDGEMENTS To Ilsi Boldrini (UFRGS) for helping with taxonomic identification. To Jorge Schirmer (IRDeR/UNIJUÍ) for assistance in the determination of seed germination capacity. To Andressa Felipin for the English revision. RESUMO Emergência e crescimento de plântulas de Ateleia glazioveana Baill. em semeadura direta em um estágio sucessional inicial. Ateleia glazioveana (Fabaceae) é uma espécie arbórea pioneira que ocorre no Sul e Sudeste do Brasil, alcançando grandes densidades populacionais na Floresta Es- tacional. O objetivo deste trabalho foi analisar a emergência, crescimento e sobrevivência de plântulas de A. glazioveana em condições naturais. O ensaio foi instalado em uma área agrícola abandonada por 11 anos, com vegetação herbácea em fase inicial de sucessão secundária. As parcelas tinham 2 x 3 m, com 4 repetições, em 4 blocos casualizados. O desenho experimental foi um fatorial de 2 x 2 x 2, com duas diferentes condições de manejo da vegetação (com e sem remoção da vegetação herbácea e arbustiva), dois níveis de fertilização (adição de 33 g/m 2 de NPK 4:20:12 e sem adição de fertilizante) e com ou sem adição de sementes. As parcelas com semeadura receberam 200 sementes, o que corresponde a 33 sementes/m 2. O registro de dados de emergência e sobrevivência foi feito aos dois, cinco e 12 meses. Os dados de crescimento (diâmetro do colo e altura) foram obtidos após 12 meses. A emergência espontânea de A. glazioveana foi nula. A emergência produzida pela semeadura direta atingiu um total de 48 (1,5%) plântulas após dois meses e 77 (2,4%) plântulas após 12 meses. Destas, 56 plântulas sobreviveram após 12 meses, o que corresponde 5.883 plântulas por hectare. Os tratamentos não diferiram quanto à altura e sobrevivência, entretanto os tratamentos submetidos à retirada da vegetação apresentaram plântulas com maior diâmetro do colo. A adição de fertilizante não gerou diferenças significativas. A altura média das plântulas após 12 meses foi de 11,96 cm (± 4,08). A semeadura direta se mostrou viável, porém todas as mudas apresentaram danos causados pela geada após o inverno de 2010, indicando limitações microclimáticas ao recrutamento. Palavras chave: sucessão secundária, restauração florestal, Floresta Estacional Semidecidual. REFERENCES 1- BAGGIO, A. J. Timbó: uma alternativa para a produção perene de adubo verde. Circular Técnica 68 (EMBRAPA Florestas), Curitiba, p. 1-8, 2002. 2- BENVENUTI-FERREIRA, G.; COELHO, G. C. Floristics and structure of the tree component in a Seasonal Forest remnant, Chiapetta, Rio Grande do Sul State, Brazil. Revista Brasileira 39 Revista SEB Ano 14 Final.indd 39 09/10/2012 13:43:58 Brazilian Journal of Ecology ISSN 1516-5868 de Biociências, Porto Alegre, v. 7, n. 4, p. 344353, 2009. 3- BRAGA, A J.; GRIFFITH, J. J.; PAIVA, H. N.; SILVA, F. C.; CORTE, V. B.; MEIRA-NETO, J. A. A. Enriquecimento do sistema solo-serapilheira com espécies arbóreas aptas para recuperação de áreas degradadas. Revista Árvore, Viçosa, v. 31, n. 6, p. 1145-1154, 2007. 4- BURKART, R. & FERNÁNDEZ, J. G. 2002. Introducción. In: BURKART, R., CINTO, J. P., CHÉBEZ, J. C., FERNÁNDEZ, J. G. & RIEGELHAUPT, E. (Eds.) La Selva Misionera – opciones para su conservación y uso sustentable. Buenos Aires: FUCEMA. p. 11-16. 5- CAMARGO, J. L. C.; FERRAZ, I. D. K.; IMAKAWA, A. M. Rehabilitation of degraded areas of Central Amazonia using direct sowing of forest tree seeds. Restoration Ecology, Malden, v. 10, n. 4, p. 636-644, 2002. 6- CARVALHO, P. E. R., 1994. Espécies florestais brasileiras: recomendações silviculturais, potencialidades e uso da madeira. EMBRAPACNPF: Brasília, 1994, 640 p. 7- COELHO, G. C.; RIGO, M. S.; LIBARDONI, J. B.; OLIVEIRA, R.; BENVENUTI-FERREIRA, G. Understory structure in two successional stages of a Semi-deciduous Seasonal Forest remnant of Southern Brazil. Biota Neotropica, Campinas, vol. 11, n. 3, p. 63-74, 2011. 8- CLARK, J. S., BECKAGE, B., CAMILL, P., CLEVELAND, B., HILLERISLAMBERS, J., LICHTER, J., MCLACHLAN, J., MOHAN, J., & WYCKOFF, P. Interpreting recruitment limitation in forests. American Journal of Botany, Columbus, v. 86, n. 1, p. 1–16, 1999. 9- CONNELL, J. H.; SLATYER, R. O. Mechanisms of succession in natural communities and their role in community stability and organization. The American Naturalist, Chicago, v. 111, n. 982, p. 1119-1144, 1977. 10-ENGEL, V. L.; PARROTTA, J. A. An evaluation of direct seeding for reforestation of degraded lands in central São Paulo state, Brazil. Forest Ecology and Management, Amsterdam, v. 152, n. 1/3, p. 169-181, 2001. 11- FERREIRA, R. A.; DAVIDE, A. C.; BEARZOTI, E.; MOTTA, M. S. Semeadura direta com espécies arbóreas para recuperação de ecossiste- mas florestais. Cerne, Lavras, v. 13, n. 3, p. 271279, 2007. 12-GEEVES, G., SEMPLE, B., JOHNSTON, D., JOHNSTON, A., HUGHES, J., KOEN, T., YOUNG, J. Improving the reliability of direct seeding for revegetation in the Central West of New South Wales. Ecological Management & Restoration, Carlton, v. 9, n. 1, p. 68-71, 2008. 13-GOTELLI, N. J. 2009. Ecologia. 4ª ed. Londrina, Ed. Planta. 14-HÜLLER, A.; COELHO, G. C.; MENEGHELLO, G. E.; PESKE, S. T. Semeadura direta de Schinus terebinthifolius Raddi e Citharexylum solanaceum Chamisso na recuperação de áreas degradadas no Bioma Mata Atlântica. In: VIII CONGRESSO NACIONAL DE RECUPERAÇÃO DE ÁREAS DEGRADADAS, 2010, Guarapari. Anais... Guarapari: SOBRADE, 2010, CD-ROM. 15-KAGEYAMA, P. Y.; GANDARA, F. B. 2000. Recuperação de áreas ciliares. In RODRIGUES, R. R.; LEITÃO FILHO, H. F. (Eds.). Mata ciliares: uma abordagem multidisciplinar. EDUSP/ FAPESP, São Paulo, p. 249-269. 16-KNOWLES, O. H.; PARROTTA, J. A. Amazonian forest restoration: an innovative system for native species selection based on phenological data and field performance indices. Commonwealth Forestry Review, Oxford, v. 74, n. 3, p. 230-243, 1995. 17-MALUF, J. R. T. Nova classificação climática do Estado do Rio Grande do Sul. Revista Brasileira de Agrometeorologia, Santa Maria, v. 8, n. 1, p. 141-150, 2000. 18-MATTEI, V. L.; ROSENTHAL, M. D. Semeadura direta de canafístula (Peltophorum dubium (Spreng.) Taub.) no enriquecimento de capoeiras. Revista Árvore, Viçosa, v.26, n. 6, p.649654, 2002. 19-ODUM, E. P. Ecologia. 1ª Ed., Rio de Janeiro: Guanabara Koogan, 1988. 434 p. 20-OMETTO, J. C. Bioclimatologia vegetal. São Paulo: Ceres, 1981. 425 p. 21-RESENDE, A. V.; FURTINI NETO, A. E.; CURI, N. Mineral nutrition and fertilization of native tree species in Brazil: research progress and suggestions for management. Journal of Sustainable Forestry, New Haven, v. 20, n. 2, p. 40 Revista SEB Ano 14 Final.indd 40 09/10/2012 13:43:58 Brazilian Journal of Ecology ISSN 1516-5868 45-81, 2005. 22-SOARES, P. G.; RODRIGUES, R. R. Semeadura direta de leguminosas florestais: efeito da inoculação com rizóbio na emergência de plântulas e crescimento inicial no campo. Scientia Forestalis, Piracicaba, v. 36, n. 78, p. 115-121, 2008. 23-SCHENKEL, V.; GASS, S. L. B.; LUCCHESE, O. A.; COELHO, G. C. 2003. Levantamento de cobertura florestal no noroeste rio-grandense: o diagnóstico das APP’s a partir de microbacias hidrográficas. In: LUCCHESE, O. A.; COELHO, G. C. (Eds.). Reflorestamento e Recupe- ração Ambiental: Biodiversidade e Culturas - a gestão ambiental em foco. Ijuí: Editora da UNIJUÍ, p. 192-201. 24-SHONO, K.; DAVIES, S. J.; CHUA, Y. K. Performance of 45 native tree species on degraded lands in Singapore. Journal of Tropical Forest Science, Kuala Lumpur, v. 19, n. 1, p. 25–34, 2007. 25-STEVENSON, B. A.; SMALE, M. C. Seed bed treatment effects on vegetation and seedling establishment in a New Zealand pasture one year after seeding with native woody species. Ecological Management & Restoration, Carlton, v. 6, n. 2, p. 124-131, 2005. 41 Revista SEB Ano 14 Final.indd 41 09/10/2012 13:43:58 Brazilian Journal of Ecology ISSN 1516-5868 42 Revista SEB Ano 14 Final.indd 42 09/10/2012 13:43:58 Brazilian Journal of Ecology ISSN 1516-5868 Plant richness in exotic tree plantations in Rio Grande municipality, Rio Grande do Sul State, Brazil Quenie Januário, Universidade Federal do Rio Grande, Instituto de Ciências Biológicas Caroline Igansi Duarte, Universidade Federal do Rio Grande, Instituto de Ciências Biológicas Geraldo Ceni Coelho, Universidade Federal da Fronteira Sul, (cenicoelho@gmail.com) Ubiratã Soares Jacobi *, Universidade Federal do Rio Grande, Instituto de Ciências Biológicas, (dmbbira@furg.br) ABSTRACT The aim was to investigate vegetal richness inside two exotic tree-species plantations, as well as to analyze the influence of light and litter. One of the areas was a 30 ha plantation of Eucalytus tereticornis Sm. and E. robusta Sm., and the other a 3 ha plantation of Pinus elliottii Engelm. In each, twenty-five 5x10 m plots were marked out, so as to investigate the structure of the vegetal community. The presence of tree, bush, epiphyte, climbing and herb species was registered. 25 samples of litter from each area were collected by way of square frames measuring 625 cm². Light intensity was measured in all the plots. Spatial richness and the distribution of species were correlated with the distance from the plantation-edge, litter-disposal and light-intensity. Richness was measured and analyzed according to the number of species. The area of Eucalyptus spp. presented 18 species and that of P. elliottii 14. Tillandsia aeranthos Desf. ex Steud., the most frequent species in both areas, was registered in all the plots. In the P. elliottii plantation, richness diminished with the increase in distance from the edge and with the reduction in light-intensity. In both study-areas, the number of species decreased in accordance with the increase of litter. Concomitantly, richness presented a higher correlation with light intensity. The data indicate the need for monitoring and amplifying the intensity of light as a strategy for regenerating vegetal communities. Key-words: richness, invasive tree species; exotic-species monoculture; Pinus; Eucalyptus. INTRODUCTION The coastal regions of Rio Grande do Sul State, Brazil, through comprising a varied assortment of environments, such as swamps, salt marshes, dunes and prairies, facilitate the formation of distinct vegetal configurations with high plant diversity, herbaceous plants and trees amongst others (15). Recent anthropic activities have caused negative impacts and disturbance. Exotic tree and rice cultivation, cattle raising and real estate expansion are among the human activities accountable for degradation in the southern Rio Grande do Sul coastal region (6, 4). The introduction of exotic-tree species is one of the greatest threats to local biodiversity, through the introduction of pathogens, competition, allelopathy and the formation of physical barriers (19). Exotic species are defined as those that occur outside the natural and historically known limits, as a result of accidental or intentional human dispersion. Invasive species are those which, once having been introduced and adapted to the new environment, begin spontaneous reproduction and occupy the space of native species, thereby inducing modifications in 43 Revista SEB Ano 14 Final.indd 43 09/10/2012 13:43:58 Brazilian Journal of Ecology ISSN 1516-5868 ecological processes, reaching to dominance (26). Biological contamination is pointed out as being the second main cause of extinction worldwide, surpassed only by fragmentation and habitat loss (19). Pinus species, natives of the Northern Hemisphere, are among those with the highest invasive potential worldwide. Around the 1950’s, they were introduced into Brazil for pulp production, their culture being largely stimulated by tax incentives. Pinus spp. is cultivated in the coastal region of Rio Grande do Sul State for resin production. It is anemophilous and wind-dispersed, with a dispersal range of 25 km. The more than 90% seedling emergence facilitates its adaptation to any ecosystem. Furthermore, it is highly fire resistant. The slow degradation and accumulation of pine needles in layers more than 20 cm deep acidifies the soil (19, 25). The genus Eucalyptus, native of Oceania, was introduced into Brazil at the end of the nineteenth century. Eucalyptus species were widely used for railroad sleepers, fence posts, lamp posts, the drainage of bogs and marshes, and as windbreaks. Besides the fast growth rate, their extensive cultivation was much favored by their innate capacity for adaptation to various soil types and fertility levels (13). Since the 1970’s, they have been used for pulp production, recently with the inclusion of genetically modified species. In 2000, Eucalytpus cultivation occupied an area of 3.0 million hectares of the 4.8 million dedicated to forestry in Brazil (1). Whereas some authors advocate the importance of planting exotic trees in the regeneration of native vegetation (8, 20, 23), little research has been carried out to measure the impact of Pinus or Eucalyptus homogeneous plantations on local biodiversity (26, 16, 21), with a complete lack along the Southern Brazilian coastal region. The aim was to describe the richness and structure of the plant communities inside two exotic plantations, one of Pinus elliottii Engelm. and the other of Eucalyptus tereticornis Sm. and E. robusta Sm. The correlations among litter accumulation, light intensity and plant spatial patterns were also analyzed. METHODOLOGY Rio Grande municipality, Rio Grande do Sul State. According to the Köppen system, the climate is Cfa humid subtropical. The average temperatures are: annual 17.9 °C., in the hottest month 23.3 °C; and in the coldest month 12.7 °C. The average annual rainfall is 1,252 mm, and relative humidity around 80%. The predominant wind direction in all seasons is northeast (18). Plantations were with 2x3m spacing and with no commercial exploitation. The study took place between April, 2008 and November, 2009. The nearly 25-year-old P. elliottii plantation, within an area of three ha, was located in the campus of the Rio Grande Federal University (FURG), 2 meters above sea level, at the coordinates 32º 04’ 58.67” S and 52º 09’21.10”W. The adjacent areas were meadows, urban areas, and other Pinus and Eucalyptus cultivations. The nearly 30-year-old Eucalyptus spp. plantation, comprising two species, E. tereticornis and E. robusta, was located in an area of 35 ha in the 6th Industrial District of Rio Grande, within the coordinates 32º 07’ 40.54”S and 52º 08’21.60” W, 19 meters above sea level. The adjacent areas consisted of meadows, woody fields, swamps, and a sandbank forest inside a conservation area. Richness was measured and analyzed through species quantification. Frequency and the number of species were estimated using the fixed-plot method (14). Five demarked areas of 5x50m were each divided into five plots, to a total of 25 plots of 50 m 2 and 1250 m 2 of total sampled area in the two sites. Within each spot, two plots of 1 x 1 m were delimited for herbaceous sinusia sampling. The demarked areas were placed so that the first were situated on the border and those subsequent towards the interior (Figure 1). For herbaceous sinusia, plants smaller than 30 cm high were recorded. For tree sampling, plants with DBH (diameter breast height) ≥ 5.0 cm at a height of 1.30 m above ground level were included. All epiphytic plants observed in the plots were recorded, this including hemi-epiphytic species. Terrestrial plants that use others as support were included as climbing plants, together with woody lianas (10). The sample was evaluated through the sample sufficiency curve. The sites are located on the coastal plains of 44 Revista SEB Ano 14 Final.indd 44 09/10/2012 13:43:58 Brazilian Journal of Ecology ISSN 1516-5868 Border Border Figure 1 – Distribution of plots in the plantations, ‘b’ is the sampling spot used for herbs, and ‘a’ the spot for other sinusiae. Table 1 - Absolute (FA) and relative (FR) frequency of the species recorded in the Eucalyptus spp. plantation. Other observed Lifeinside the FAplantaSpecies species (Family) form Origin FR Eucalyptus spp. (Myrtaceae) AR EX 100 26,32 tions, but not encountered in the plots, were100regisTillandsia aeranthos Desf. ex Steud. (Bromeliaceae) E N 26,32 (Raddi) Kuhlm. (Poaceae) N 76 20 tered Axonopus to sofissifolius complement the floristicH survey. Microgramma vacciniifolia (Langsd. & Fisch.) Copel. (Polypodiaceae) E N 40 10,53 Species were identified according Eleocharis bicolor Chapm. (Cyperaceae) H N 12to the 3,16 Ficus cestrifolia Schott ex Spreng. (Moraceae) Eh N 12 3,16 literature, and by consulting herbaria (HURG), exSmilax campestris Griseb. (Smilacaceae) T N 12 3,16 MyrsineDigital parvifolia A.DC. Data (Primulaceae)Bank of the AR/ABBrazilian N 8 Flora 2,11 perts, the Pycreus polystachyos (Rottb.) P.Beauv. (Cyperaceae) H N 4 1,05 Species Checklist, theN New Dichanthelium sabulorum (Lam.) Gould Flora & C.A. ClarkBrasiliensis, (Poaceae) H 4 York 1,05 Pleopeltis pleopeltifolia (Raddi) Alston (Polypodiaceae) E N 4 1,05 Botanical Garden, and the Missouri Botanical GarCentella asiatica (L.) Urb. (Apiaceae) H C 4 1,05 Citharexylum (Spreng.) Moldenke of (Verbenaceae) AR/AB family N 1,05 4 den. Themontevidense delimitation taxa at the level is Lithrea brasiliensis Marchand (Anacardiaceae) AB N - - Hydrocotyle bonariensis Lam. (Araliaceae) H N - - E N according to the proposition for the Angiosperm Phylogeny Group III (3). Litter was estimated by way of 25 samples obtained by a square iron frame with 25 cm sides. Samples were dried in a stove at 70 ºC, and weighed with a precision balance (15). Light intensity (expressed as µ mol s -1 m-2) was estimated with a LI-COR Radiation Sensor in each sampling spot. The Spearman rank correlation was determined for analyzing relationships between richness, litter and light intensity. RESULTS In the Eucalyptus plantation, there were 18 species belonging to 15 families (Table 1), two species each from Cyperaceae, Poaceae and Polypodiaceae, and only one each from the others. Sixteen (88%) species were native, one exotic and one cosmopolitan (Table 1). Senecio brasiliensis (Spreng.) Less. (Asteraceae) H N frequency - of the species recorded in the Eucalyptus spp. plantation. Table 1 - Absolute (FA) and relative (FR) Rhipsalis teres (Vell.) Steud. (Cactaceae) N SpeciesAR/AB (Family) - - - - Life form Origin FA FR Eucalyptus spp. (Myrtaceae) AR EX 100 26,32 Tillandsia aeranthos Desf. ex Steud. (Bromeliaceae) E N 100 26,32 Axonopus fissifolius (Raddi) Kuhlm. (Poaceae) H N 76 20 Microgramma vacciniifolia (Langsd. & Fisch.) Copel. (Polypodiaceae) E N 40 10,53 Eleocharis bicolor Chapm. (Cyperaceae) H N 12 3,16 Ficus cestrifolia Schott ex Spreng. (Moraceae) Eh N 12 3,16 Smilax campestris Griseb. (Smilacaceae) T N 12 3,16 Myrsine parvifolia A.DC. (Primulaceae) AR/AB N 8 2,11 Pycreus polystachyos (Rottb.) P.Beauv. (Cyperaceae) H N 4 1,05 Dichanthelium sabulorum (Lam.) Gould & C.A. Clark (Poaceae) H N 4 1,05 Pleopeltis pleopeltifolia (Raddi) Alston (Polypodiaceae) E N 4 1,05 Centella asiatica (L.) Urb. (Apiaceae) H C 4 1,05 Citharexylum montevidense (Spreng.) Moldenke (Verbenaceae) AR/AB N 4 1,05 Lithrea brasiliensis Marchand (Anacardiaceae) AB N - - Hydrocotyle bonariensis Lam. (Araliaceae) H N - - Senecio brasiliensis (Spreng.) Less. (Asteraceae) H N - - Rhipsalis teres (Vell.) Steud. (Cactaceae) E N - - Daphnopsis racemosa Griseb. (Thymelaeaceae) AR/AB N - - Daphnopsis racemosa Griseb. (Thymelaeaceae) AB= tree; AR= shrub; E= epiphyte; H= herb; T= climbings; N= native; C= cosmopolitan; Ex= exotic; Eh = hemiepiphyte; - = species observed out the sampling plots. AB= tree; AR= shrub; E= epiphyte; H= herb; T= climbings; N= native; C= cosmopolitan; Ex= exotic; Eh = hemiepiphyte; - = species observed out the sampling plots. 45 Revista SEB Ano 14 Final.indd 45 09/10/2012 13:43:58 Brazilian Journal of Ecology ISSN 1516-5868 In the Eucalyptus site, the lowest values for accumulated litter were in the edge plots and the highest in the intermediate (Figure 3), whereas species richness was inversely proportional to litter levels (Figure 3 on left), with r = -0.60. For P. elliottii, there were 14 species belonging to 12 families (Table 2), among which 11 (79%) were native and 3 (21%) exotic. There were two species each from Fabaceae and Myrtaceae, and only one each from the other 10 (Table 2). Table 2 - Absolute (FA) and relative (FR) frequency of the species recorded in the Pinus elliottii plantation. Species (Family) Life form Origin FA FR Table 2 - Absolute (FA) and relative (FR) frequency of the species recorded in the Pinu Pinus elliottii Engelm. (Pinaceae) AB EX 100 32,47 Tillandsia aeranthos Desf. ex Steud. (Bromeliaceae) E Species (Family) N 100 Pinus elliottii Engelm. (Pinaceae) 32,47 Life form Origin AB EX E N Axonopus fissifolius (Raddi) Kuhlm. (Poaceae) H N ex Steud. 40(Bromeliaceae) 12,99 Tillandsia aeranthos Desf. Acacia longifolia (Andrews) Willd. (Fabaceae) AR/AB EX 16 (Poaceae) 5,18 Axonopus fissifolius (Raddi) Kuhlm. H N Schinus terebinthifolius Raddi (Anacardiaceae) Acacia longifolia (Andrews) Willd. AB N 16 (Fabaceae) 5,19 AR/AB EX Ipomoea cairica (L.) Sweet (Convolvulaceae) Schinus terebinthifolius T N Raddi (Anacardiaceae) 12 3,90 AB N Desmodium adscendens (Sw.) DC. (Fabaceae) Hydrocotyle bonariensis Lam. (Araliaceae) Ipomoea cairica (L.) Sweet (Convolvulaceae) T N Desmodium adscendens (Sw.) DC. (Fabaceae) H N Hydrocotyle bonariensis Lam. (Araliaceae) H N H N H N 8 2,60 H N 4 1,30 Rumohra adiantiformis (G.Forst.) Ching (Dryopteridaceae) H N 4 1,30 Rumohra adiantiformis (G.Forst.) Ching (Dryopteridaceae) Sida rhombifolia L. (Malvaceae) H rhombifolia N L. (Malvaceae) 4 1,30 Sida Syzygium cumini (L.) Skeels (Myrtaceae) AR/AB EX Skeels (Myrtaceae) 4 1,30 Syzygium cumini (L.) H N AR/AB EX Sapium glandulosum (L.) Morong (Euphorbiaceae) Sapium glandulosum (L.) AB N Morong (Euphorbiaceae) - AB N Myrsine parvifolia A.DC. (Primulaceae) Myrsine parvifolia N A.DC. (Primulaceae) AR/AB - AR/AB N AB N Eugenia uniflora L. (Myrtaceae) Eugenia uniflora L. (Myrtaceae) AB N - - AB= tree; AR= shrub; E= epiphyte; H= herb; T= climbing; N= native; C= cosmopolitan; Ex= exotic; Eh = h AB= tree; AR= shrub; E= epiphyte; H= herb; T= climbing; N= observed native; C=out cosmopolitan; Ex= exotic; Eh = hemiepiphyte; - = species the sampling plots. observed out the sampling plots. The two sites contained four species in Table 3 – Richness and sinusia in the sampling plots common: Tillandsia aeranthos, Hydrocotyle bonar- on each site Table 3 – Richness and sinusia in the sampling plots on each site. iensis, Myrsine parvifolia, Axonopus fissifolius. Sinusia Eucalyptus Pinus Table species 3 – Richness andrecorded sinusia inin thethe sampling plots on each site. Seven woody were two sites, Herbs 5 (38%) 5 (46%) Sinusia Eucalyptus four in the P. elliottii (Table 2) and another three in Pinus Trees 2 (15%) 2 (18%) the Eucalytptus (Table Herbs 1). 5 (38%) 5 (46%) Shrubs 1 (8%) 2 (18%) Tillandsia aeranthos was present in all the Trees 2 (15%) 2 (18%) Epiphytes 4 (34%) 1 (9%) plots in both sites. Axonopus fissifolius was the secShrubs 1 (8%) 2 (18%)Climbing 1 (8%) 1 (9%) ond most common species (Table 1 and 2). Epiphytes only plots, 4 (34%) 13 11 On considering the Eucalyp- 1 (9%) Total Climbing (8%) 11 species, 1 (9%) tus and Pinus sites presented 131 and 46 S p e c ie s S p e c ie s Litter accumulation in the Pinus site was 11 higher than in the Eucalyptus, and was inversely 12 14 proportional to the distance from the edge (Figure 12 10 3). 10Furthermore, species richness was inversely 8 8 proportional to accumulated litter (Figure 3 on the 12 6 6 right), 10with r = -0.87. 4 4 In the Eucalyptus site, the lowest light in2 8 2 0 tensity was registered in the intermediate plots. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 0 6 There was a significantPlotscorrelation of richness with1 4 light intensity (r = 0.90) (Figure 4 on the left). S p e c ie s S p e c ie s respectively. All the represented in Totalsinusiae were 13 both areas, with the predominance of herbs (Table 3). Although epiphytes comprised the second richest sinusia in the Eucalyptus site, only one was observed in the Pinus. 14 Whereas12 in the Eucaplyptus site sample sufficiency analysis10indicated stabilization in the seven8 teenth spot (Figure 2), in the Pinus the absence of a 6 clear stabilization (Figure 2) could be related to dif4 ferences in richness between edge and interior plots. 2 3 4 5 6 7 2 2 0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 Plots 0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 Plots Revista SEB Ano 14 Final.indd 46 09/10/2012 13:43:58 8 9 10 11 Epiphytes Epiphytes Climbing Climbing 4 (34%) 4 (34%) 1 (9%) 1 (9%) 1 (8%) 1 (8%) 1 (9%) 1 (9%) TotalTotal 13 13 1111 14 14 12 12 10 10 6 12 12 10 10 8 8 8 S p ec ies S p e c ie s 8 S p e c ie s S p ec ie s Brazilian Journal of Ecology ISSN 1516-5868 6 6 6 4 4 2 2 4 4 2 2 0 1 0 8 11 9 12 10 11 2 3 1 4 2 53 64 75 86 97 10 13 12 14 13 15 14 16 15 17 16 18 1719 18201921202221232224232524 2625 26 0 0 14 15 15 16 16 17 17 18 18 19 20 21 1 12 23 34 45 56 6 7 7 8 8 9 9 10101111 1212 1313 14 21 22 22 23 23 24 24 25 25 2626 Plots Plots lots PPlots Figure 2 – Cumulative curve of species per spot in a monoculture Eucalyptus area (on the left) and a Pinus area (on the right). 30 30 1200 1200 25 25 1000 1000 S Species pecies 20 20 800 800 1200 1200 600 600 L itter L itter 30 30 15 15 25 25 10 10 20 20 5 5 15 15 0 0 1 1 10 10 5 5 0 0 1 1000 1000 400 400 S pecies S pecies 800 800 200 200 L itter L itter 30 30 5000 25 25 4500 4000 15 15 25 25 10 10 20 20 3 3 4 4 5 5 66 P lots P lots 3500 3500 1500 3000 3000 1000 2500 2500 500 2000 0 2000 55 15 15 600 600 00 2 2 3500 5000 5000 3000 4500 4500 2500 4000 4000 2000 20 20 30 30 400 400 00 10 10 200 200 5 5 0 0 0 0 11 22 33 44 22 pecies ies SS pec itter LLitter SSpec pecies ies L Litter itter 1500 1500 1000 1000 5 lots PPlots 500 500 00 2 2 3 3 4 4 5 5 6 6 2 2 3 3 plantation 44 5 5(on the left) and in the Figure 3 -1 Relationship between accumulated litter and richness in 1the1 Eucalyptus P lotsP lots P lots P lots 30 80 30 300 3030 (on the right). 300 Pinus pecies SSpecies 200 200 300 300 15 2515 25 150 150 250 250 10 2010 20 100 100 200 200 5 5 15 15 50 50 150 150 0 0 10 10 11 5 5 0 0100 100 0 22 33 44 55 50 50 Plots Plots 0 0 1 1 2 2 3 3 4 4 5 25 25 lightht lig 20 20 30 30 15 15 S pecies S pecies 25 25 10 10 lig ht lig ht 20 20 55 15 15 00 10 10 0 5 Plots Plots 70 SS pecies pec ies 60 508080 lig light ht µ m o l s ˉ¹ m ˉ² µ m o l s ˉ¹ m ˉ² µ m o l s ˉ¹ m ˉ² 20 3020 30 o l s ˉ¹ m ˉ² µ m o l s ˉ¹ m ˉ²µµ m m o l s ˉ¹ m ˉ² 250 250 µ m o l s ˉ¹ m ˉ² 2525 407070 306060 205050 104040 11 22 5 5 33 4 SSpec ies pecies lig light ht 0 3030 5 2020 1010 Plots Plots 0 0 00 1 1 2 2 33 44 55 Plots Plots Figure 4 – Correlation between light intensity (triangles) and richness (squares) in the Eucalyptus site (on the left) and in the Pinus site (on the right). In the Pinus site, light intensity was closely related to distance from the border. This pattern was accompanied by a significant correlation of richness with light intensity (r=0.97) (Figure 4 on right). DISCUSSION In spite of difficulties related to differences in method, the richness observed in our study could be considered low for both the Eucalyptus and Pinus sites, when compared to other inventories in the same or other regions. It should be emphasized that, at the most, no more than one sinusia had been studied in those other inventories. In native coastal ecosystems, plant richness is normally high, much more so than that noted in the present report. On recording the presence of 78 vascular plant species (including three endangered ones) in the Lagoa Verde Environmental Protection Area, Rio Grande municipality, Batista et al. (2007) used this to emphasize the extreme human disturbance in the area. Marangoni (2003) recorded 29 vascular spe- 47 Revista SEB Ano 14 Final.indd 47 09/10/2012 13:43:59 Brazilian Journal of Ecology ISSN 1516-5868 cies in a site in the Lagoa dos Patos estuary. Porto & Dillenburg (1986) registered 151 vascular plants in two forest formations, one in a swamp and the other in sandy soil, located in the Taim Ecological Station. Kindel (2002) reported 158 vascular plants in a swampy forest in Torres municipality, Rio Grande do Sul State. In the Lagoa do Peixe National Park, Záchia (2006) recorded 100 plant species and Dorneles & Waechter (2004) 21 tree species. Neri et al. (2005) recorded 47 species in a Eucalyptus site in the Brazilian Cerrado. The authors stressed that such low diversity, when compared to Cerrado diversity in general, could be attributed to shading. In another similar study in the Cerrado, Saporetti et al. (2003) encountered 39 woody species. The authors, on pointing out that Eucalypti hinder the arrival of zoochoric and wind-dispersed native species, proposed Eucalyptus girdling and the permanence of dead trees to serve as perches. Floristic studies of Pinus monocultures are few, in spite of species of this genus pointedly possessing high invasive potential and causing local diversity loss (26, 19). Even so, Andrae et al. (2005) reported understory establishment of 121 woody-plant species under 25-30-year-old pines in plantations in the Central Region of Rio Grande do Sul State. Generally speaking, scientific papers refer to Pinus, Eucalytus and other exotic tree species plantations as ‘planted forest’, ‘commercial planted forest’ (23) or ‘reforestation’ (2). Notwithstanding, a forest is a complex ecosystem, in which, not only one or two, but several species of plants, animals, fungi, protists and bacteria are involved. Some studies indicate examples of Pinus and Eucalyptus as facilitating native forest regeneration (23). Nonetheless, the commercial management of such areas implies the use of agrochemicals to control plants, animals, fungi and bacteria, thereby hampering their complete development, whence the origin of the so-called “green deserts”. The above mentioned studies were actually developed in non-commercial or abandoned areas of exotic tree plantations, thus where agrochemicals are no longer used, and where fallen trees generate gaps, thereby inducing native plant species development, beginning at the edges. According to light availability, native plant regeneration could further expand to the interior, thus characterizing true restoration. Nonetheless, even in noncommercial areas, the absence of patches of native forest, in regions with extensive Pinus and Eucalyptus plantations, could be a hinderance to native forest regeneration, since this requires seeds and propagules originating from other areas. In the Pinus site, it was noted that the lowest plant richness was correlated to the highest litter accumulation, which, in turn, increased from the edges towards the interior. On the other hand, plant richness was positively correlated to light intensity. The scenario was similar in the Eucalyptus plantation. As plant richness was more highly correlated with light intensity than with litter accumulation and distance from the border, it can be deduced that a reduction in richness is strongly linked to the prevailing shade. However, the complementary contribution of litter to the decrease in richness cannot be discarded. Although some authors point to the possibility of regeneration in homogeneous stands of exotic species through shading (2, 16, 21), this would be impossible in old plantations with trees of 30-meters or more in height. Hinderance would be especially stronger for tree species, when considering the observed predominance of herbs and epiphytes. In the Eucalyptus area only one tree species presented individuals with DBH ≥ 5.0 cm at 1.3 m above ground level, and in the Pinus, only one exotic woody species (A. longifolia) was observed, whence it is impossible to demonstrate regeneration in a plant community. Considering the importance of biodiversity conservation, the adequate management of exotictree-species plantations, focusing native plant community restoration, requires top priority. This could be achieved through techniques that increase light intensity, such as tree girdling, as also proposed by previous authors (22). However, the lower diversity found in exotic species monoculture may be due to other factors, such as allelopathy, a phenomenon in which substances released by the leaves and branches of tree species may hinder the development of other surrounding plants (9). In Canada, Newmaster et al. (2006) proposed reforestation with native conifers, as the first step towards rehabilitating conifer forests that had been converted to agriculture and then abandoned. However, in Brazil, Pinus may interfere in plant diversity, since its 48 Revista SEB Ano 14 Final.indd 48 09/10/2012 13:43:59 Brazilian Journal of Ecology ISSN 1516-5868 own regeneration is stimulated in detriment of native plants, insofar as light availability increases (5). On the other hand, abandoned non-commercial plantations that present well-developed understories, could serve as a source of seeds or seedlings for environmental restoration projects, an issue that needs further evaluation in the Atlantic Rain Forest Biome. CONCLUSION Plant richness, reduced inside Eucalyptus and Pinus plantations, when compared to wild environments in the coastal ecoregion, is directly correlated to light intensity and inversely correlated to litter accumulation inside the plantations. ACKNOWLEDGMENTS To Adriano Jacobi and Andressa Felipin for the English revision. RESUMO Este estudo teve como objetivo investigar a riqueza vegetal no interior de dois plantios de espécies arbóreas exóticas, analisando também as influências da luz e serrapilheira. Uma das áreas foi um plantio de Eucalytus tereticornis Sm. e E. robusta Sm., com 30 ha. A outra área foi um plantio de Pinus elliottii Engelm. com três ha. Em cada área foram demarcadas 25 parcelas de 5 x 10 m para investigar a estrutura da comunidade vegetal. Registrou-se a presença de espécies arbóreas, arbustivas, epifíticas, trepadeiras e herbáceas. Foram coletadas 25 amostras de serrapilheira de cada área com o auxílio de uma moldura quadrada com 625 cm². A intensidade de luz foi medida em todas as parcelas. A riqueza e a distribuição espacial das espécies foram correlacionadas com a distância da borda, a deposição da serrapilheira e a intensidade de luz. A riqueza foi mensurada e analisada através da quantidade de espécies. A área de Eucalyptus spp. apresentou 18 espécies e a área de P. elliottii 14 espécies. Tillandsia aeranthos Desf. ex Steud. foi a espécie mais freqüente em ambas as áreas, sendo registrada em todas as parcelas. Na plantação de P. elliottii a riqueza diminuiu com o aumento da distância da borda e com a redução da intensidade de luz. O número de espécies diminui de acordo com o aumento de ser- rapilheira nas duas áreas. Em ambas as áreas a riqueza apresentou maior correlação com a intensidade luminosa. Os dados indicam a necessidade de monitorar e ampliar a intensidade luminosa como estratégia para a regeneração das comunidades vegetais. Palavras-chave: riqueza, espécies arbóreas invasivas; monocultura de espécies exóticas; Pinus; Eucalyptus. REFERENCES 1-ALMEIDA, A. C.; SOARES, J. V. Comparação entre uso de água em plantações de Eucalyptus grandis e floresta ombrófila densa (Mata Atlântica) na costa leste do Brasil. Revista Árvore, Viçosa, v. 27, n 2, p. 159-170, 2003. 2-ANDRAE, F. H.; PALUMBO, R.; MARCHIORI, J. N. C.; DURLO, M. A. O sub-bosque de reflorestamentos de pinus em sítio degradados da região da floresta estacional decidual do Rio Grande do Sul. Ciência Florestal, Santa Maria, v. 15, n 1, p. 43-63, 2005. 3-APG III. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Botanical Journal of the Linnean Society, London, v. 141, p. 105-121, 2009. 4-BATISTA, T. L.; CANTEIRO, R. C. A.; DORNELES, L. P. P.; COLARES, I. G. Levantamento florístico das comunidades vegetais na Área de Proteção Ambiental da Lagoa Verde, Rio Grande, RS. Revista Brasileira de Biociências, Porto Alegre, v. 5, supl. 2, p. 225-227, 2007. 5-BECHARA, F. C., REIS. A. Recomendações de manejo para a substituição de Pinus pela restauração das restingas do Parque Florestal do Rio Vermelho. In: TRES, D. R.; REIS, A. Perspectivas sistêmicas para a conservação e restauração ambiental: do pontual ao contexto. 1. ed. - Itajaí: Herbário Barbosa Rodrigues, 2009, p. 165-170. 6-BURGER, M. I. Situação e Ações Prioritárias para a Conservação de Banhados e Áreas Úmidas da Zona Costeira. Porto Alegre: Fundação Zoobotânica do RS, 2000. 60 p. 7-DORNELES, L. P. P.; WAECHTER, J. L. Fitossociologia do componente arbóreo na floresta turfosa do parque Nacional da Lagoa do Peixe, Rio Grande do Sul, Brasil. Acta Botanica Brasilica, Feira de Santana, v. 18, n 4, p. 815–824, 2004. 49 Revista SEB Ano 14 Final.indd 49 09/10/2012 13:43:59 Brazilian Journal of Ecology ISSN 1516-5868 8-FEYERA, S.; BECK, E.; LÜTTGE, U. Exotic trees as nurse-trees for the regeneration of natural tropical forests. Trees-Structure and function, Berlim, v. 16, n. 4-5, p.245–249, 2002. 9-JACOBI, U. S.; FERREIRA, A. G. Efeitos alelopáticos de Mimosa bimucronata (DC) sobre espécies cultivadas. Pesquisa Agropecuária Brasileira, Brasília, v. 26, n. 7, p. 935-43, 1991. 10-KINDEL, A. Diversidade e estratégias de dispersão de plantas vasculares da floresta paludosa do Faxinal, Torres, RS. 2002. 102 f. Tese (Doutorado em Botânica) – Instituto de Biociências, Universidade Federal do Rio Grande do Sul, Porto Alegre, 2002. 11-KLEINPAUL, I. S.; SCHUMACHER, M. V.; BRUN, E. J.; BRUN, F. G. K.; KLEEINPAUL, J. J. Suficiência amostral para coletas de serrapilheira acumulada sobre o solo em Pinus elliottii Engelm, Eucalyptus sp. e floresta estacional decidual. Revista Árvore, Viçosa, v. 29, n. 6, p.965972, 2005. 12-MARANGONI, J. C. Caracterização da paisagem de uma área de preservação: Estudo de caso da Lagoinha (Rio Grande, RS). Atlântica, Rio Grande, v. 25, n. 2, p.163-169, 2003. 13-MATTEI, V. L. & LONGHI S. J. Avaliação da Regeneração Natural de Eucalyptus paniculata Smith. Ciência Florestal, Santa Maria, v. 11, n. 1, p.55-65, 2001. 14-MUELLER-DOMBOIS, D.; ELLENBERG, H. Aims and Methods of Vegetation Ecology. New York: Wiley, 1974. 547 p. 15-MÜLLER, S. C.; WAECHTER, J. L. Estrutura sinusial dos componentes herbáceo e arbustivo de uma floresta costeira subtropical. Revista Brasileira de Botânica, São Paulo, v. 24, n. 4, p 395-406, 2001. 16-NERI, A. V.; CAMPOS, E. P.; DUARTE, T. G.; NETO, J. A. A. M.; SILVA, A. F.; VALENTE, G. E. Regeneração de espécies nativas lenhosas sob plantio de Eucalyptus em área de Cerrado na Floresta Nacional de Paraopeba, MG, Brasil. Acta Botanica Brasilica, Feira de Santana, v. 19, n. 2, p. 369-376, 2005. 17-NEWMASTER, S.G.; BELL, F.W.; ROOSENBOOM, C.R.; COLE, H.A.; TOWILL, W.D. Restoration of floral diversity through plantations on abandoned agricultural land. Canadian Journal of Forest Research, v. 36, p. 1218–1235, 2006. 18-PORTO, M. L.; DILLENBURG, L. R. Fisionomia e Composição Florística de uma Mata de Restinga da Estação Ecológica do Taim, Brasil. Ciência e Cultura, v. 38, n. 7, p. 1228-1236, 1986. 19-REIS, A.; ROGALSKI, J. M.; TRÊS, D. R.; SIMINSKI, A.; HMELJEVSKI, K.; BOURCHEID, K.; SCARIOT, E.; WIESBAUER, M. B.; SANTA ANNA, C. Novos Aspectos na Restauração de Áreas Degradadas. Florianópolis: UFSC, 2006. 106 p. 20-SAPORETTI, A. W.; NETO, J. A. A. M.; ALMADO, R. Fitossociologia de Sub-bosque de Cerrado em Talhão de Eucalyptus grandis W. Hill ex Maiden no Município de Bom Despacho – MG. Revista Árvore, Viçosa, v. 27, n. 6, p. 905910, 2003. 21-SIMÕES-JESUS, M. F.; CASTELLANI, T. T. Avaliação do potencial facilitador de Eucalyptus sp. na restinga da Praia da Joaquina, Ilha de Santa Catarina, SC. Biotemas, Florianópolis, v. 20, n. 3, p. 27-35, 2007. 22-TRES, D. R.; REIS, A. Perspectivas sistêmicas para a conservação e restauração ambiental: do pontual ao contexto. 1. ed. - Itajaí: Herbário Barbosa Rodrigues, 2009. 374 p. 23-VIANI, R.A.G.; DURIGAN, G.; MELO, A.C.G. A regeneração natural sob plantações florestais: desertos verdes ou redutos de Biodiversidade? Ciência Florestal, Santa Maria, v. 20, n. 3, p. 533-552, 2010. 24-ZACHIA, R. A. Diferenciação de Componentes Herbáceos e Arbustivos em Florestas do Parque Nacional da Lagoa do Peixe, Tavares – Rio Grande do Sul. 2006. 164 f. Tese (Doutorado em Botânica), Instituto de Biociências, Universidade Federal do Rio Grande do Sul, Porto Alegre. 2006. 25-ZANCHETTA, A. D.; PINHEIRO, L. S. Análise biofísica dos processos envolvidos na invasão biológica de sementes de Pinus elliottii na Estação Ecológica de Itirapina – SP e Alternativas de Manejo. Climatologia e Estudos da Paisagem, Rio Claro, v. 2, n. 1, p. 72, 2007. 26-ZILLER, S. R.; GALVÃO, F. A Degradação da estepe gramíneo-lenhosa no Paraná por contaminação biológica de Pinus elliottii e P. taeda. Revista Floresta, Curitiba, v. 32, n. 1, p. 41-44, 2002. 50 Revista SEB Ano 14 Final.indd 50 09/10/2012 13:43:59 Brazilian Journal of Ecology ISSN 1516-5868 The Influence of feeding tree spatial distribution and fruit abundance in the location of sleeping trees in the common marmoset, Callitrix jacchus (Primates: Callitrichidae). Gustavo André Fernandes Silveira - Universidade Federal do Rio Grande do Norte. (email:gustavoandrefs@yahoo.com.br) Carla Soraia Soares de Castro - Universidade Federal da Paraíba, Campus IV, Rio Tinto, Departamento de Engenharia e Meio Ambiente (email: carlasoraia@ccae.ufpb.br) ABSTRACT Security against predators, the proximity of food sources and cohesion within the group are factors which can have an influence on the localization of sleeping trees in primates. The aim was to investigate the influence of spatial distribution of gum and fruit trees, and the abundance of fruit in the localization of sleeping trees in the common marmoset. Two groups of marmosets living in the Parque das Natal, Rio Grande do Norte State were studied. Instantaneous scan sampling was used to register, at 5 minute intervals, their position on maps of the area, and to identify the localization of sleeping trees. Frequency of use of the same trees was also recorded. The species of trees used for fruit consumption, the extraction of gum and for sleeping were identified. Phenological data were collected monthly to determine the periods of fruit abundance. Sleeping trees were randomly distributed, without any apparent relationship to the aggregated distribution of gum and fruit trees. 38, Nonetheless, the abundance of fruit seemed to be an important factor in the use of space and in the localization of sleeping trees. Both, the presence of potential predators and the nonconsecutive use of sleeping trees, seem to indicate protection against predators as being another important factor in the localization of sleeping trees in the study-area. Key words: common marmoset; sleeping trees; food sources; predators INTRODUCTION Arboreal primates typically sleep in trees. They use either the forks of branches, holes in the trunk (38, 43) the surface of leaves (23, 47, 5), nests they themselves build (26) or even bird´s nests (29) in the process. Predator risk has been defined as the main determinant in the location of sleeping trees (15, 25, 22, 1, 17, 7, 3, 37). Nevertheless, other variables, such as the proximity of food and water resources, ranging patterns and territoriality aspects, security from falls, physical comfort, hygiene, parasite avoidance, group cohesion, resource availability and thermoregulation, are also important (16, 20, 44, 4, 23, 1, 3, 27, 14, 5). Some species of primates (e.g. Ateles geoffroyi (11), Colobus guereza (46), Hylobates pileatus (36), Saguinus fuscicollis and S. mystax (40), Trachypithecus leucocephalus (28) prefer to sleep close to available food resources. The strategy to wake up close to food, decrease the time and energy spent in foraging. Apparently, in the case of these species, this factor is more important than sleeping in safety against predators. The common marmoset (Callitrix jacchus) is a primate species endemic to the Brazilian northeast. Although its distribution was 51 Revista SEB Ano 14 Final.indd 51 09/10/2012 13:43:59 Brazilian Journal of Ecology ISSN 1516-5868 originally restricted to this part, introduced populations can now be found in other regions of Brazil (43). It is now found in Atlantic Forest fragments, in the Caatinga (21), and in mangrove swamps (32). Through its adaptability to various environments, by living in the Atlantic Forest, this species inhabits one of the most threatened biomes in the world. This biome has been extensively transformed into a fragmented landscape (35), through convertion to alternative land usage, such as agriculture and pasture (45). Incidentally, several studies of small fragments of this forest have reported on the proximity of trees that serve for sleeping to feeding trees (1,8). OBJECTIVES Under this perspective, the aim was to investigate the influence of gum and fruit tree spatial distribution, and fruit abundance in the location of sleeping trees. METHODOLOGY Study area The study took place in a conservation area, in the Parque Estadual das Dunas (PED), in northeast Brazil (5° 48’ S – 35° 12’ W). PED comprises a 1.175 ha fragment of the Atlantic Forest, 7 ha of which corresponding to a public area (24). There are large trees, extensive plant cover, a vast and continuous canopy, and high epiphyte density. With an idea to conservation, access is restricted to research and educational trails, with daily, though partial, monitoring. The public area, with many exotic plants and gaps, harbors around a thousand tree species. There is also a touristic infrastructure for receiving more than 2.000 people daily. Each year, about 65.000 visitors find entertainment in the structure of the park itself, walking trails and picnicking, or simply by enjoying nature. There are records of the presence of boa constrictors (Boa constrictor), black vultures (Coragyps atratus), turkey vultures (Cathartes aura), roadside hawks (Buteo magnirostris), great black hawks (Buteogallus urubutinga), white-tailed kites (Elanus leu- curus), and the southern carcara (Polyborus plancus) (24), all liable Callithrix jacchus predators. Data collection From January to December, 2007, two groups of common marmosets (A and L) came under observation. Both inhabited the public area, and only used the forest area sporadically. In the former, there are trees conducing to fruit and gum consumption, and sleeping. Both groups were accustomed to the presence of researchers, and had already undergone capture and individual identification in previous years. Instantaneous scan sampling (2), at 5-minute intervals, was chosen for recording the location of the marmosets on area maps containing alphanumeric system 20x20m quadrants, and for identifying the location of sleeping trees. These data also constituted the base for calculating the home range of each group, obtained as a sum of the quadrants visited. Frequency-of-use of sleeping trees was recorded, to so determine the proportion of use, by plant species. The tree species turned to use for fruit consumption, gum extraction and sleeping, were identified taxonomically by on-the-spot floristic studies (18). Phenological data were collected monthly to determine the peak periods of fruit abundance. Fruiting was quantified using the semi-quantitative method (19), whence five classes of abundance are inferred, 0) absence of fruit; 1) 1-25% of fruit; 2) 26-50% of fruit; 3) 51-75% of fruit; and 4) 76-100% of fruit (19). Sleeping trees were identified, and measurements taken of height and diameter at breast height. The distance from the nearest neighbor (R) was used to define spatial patterns of gum and fruit tree, and sleeping tree distribution. R=1 indicates random distribution; R>1 uniform distribution, and R<1 aggregated distribution (12). The frequencies of monthly marmoset visits recorded for each quadrant in the home range were compared through one-way ANOVA (5%) and Tukey testing (5%). Spearman correlation analysis was used to investigate the relationship between frequency of use for sleeping and tree-height, frequency of use for sleeping and diameter of sleeping trees, and sleeping-tree height and diameter. 52 Revista SEB Ano 14 Final.indd 52 09/10/2012 13:43:59 Brazilian Journal of Ecology ISSN 1516-5868 RESULTS Eight different trees belonging to five species were used for sleeping. Coccoloba sp. (Polygonaceae); Bowdichia virgilioides HBK, (Fabaceae); Cassia apoucoita Aubl. (Leg. Caesalpinoideae) and Pouteria grandiflora (Sapotaceae) were used by group L, and Coccoloba sp.; Buchenavia capitata (Combretaceae) and Pouteria grandiflora by group A. Diameters at breast height (DBH) ranged from 28.3 to 236.82 cm, and heights from 12 to 24 m (Table I). No significant correlations were found between DBH and height of sleeping trees (r=0,02; p=0,95 N=16 ), DBH and frequency of use of sleeping trees (r=0,09; p=0,82; N=16), and height and frequency of use of sleeping trees (r=0,59; p=0,12; N=16), whereby the inference of other variables influencing choice. Gum trees were located between 10 and 42 meters from sleeping trees, whereas fruit trees were between 8 and 27 meters away. Of the eight trees used by groups for sleeping, two were located at the edge of the main forest (n=3) and six in the Table I – Identification of species, height and location of sleeping trees by groups of common marmosets. Species Nº Height Records of use Location as sleeping trees (n) Coccoloba sp. 1 12 m 3 Public area Coccoloba sp. 2 14 m 5 Public area Bowdichia virgilioides 3 17,5 m 4 Public area Bowdichia virgilioides of species, height and 4location 24 of m sleeping trees6 by groups Public area marmosets. Table I – Identification of common Species Aubl. of use Location Edge of remnant Cassia apoucoita 5 20Nºm Height Records 1 as sleeping trees Coccoloba sp. 6 18 m 3 Public area (n) Buchenavia capitata Eichl. 7 17 m 2 Edge of remnant Coccoloba sp. 1 12 m 3 Public area Pouteria grandiflora 8 22 m 5 Public area Coccoloba sp. 2 14 m 5 Public area Bowdichia virgilioides 3 17,5 m 4 Public area For sleeping purposes, Group L showed a public area (n=26) between 20 and 80 meters from Bowdichia virgilioides 4 24 m 6 Public area preference (50)% for Bowdichia virigiloides,, where- the main forest edge (Table I). Sources of fruit, gum remnant Cassia apoucoita Aubl. Fruiting 5 20 m Family Species Group 1 LocationEdge of offruit as Group A preferred (75%) Coccoloba sp.. Although and sleeping trees were distributed over the 0.94 ha trees Coccoloba sp. 6 18 m 3 Public area re-use of sleeping trees was detected February on severaltooccaand 1.3 ha + 0.7 (+ stanCecropiaceae Cecropia adenopus March7 + 0.417(+mstandard L deviation) Buchenavia capitata Eichl. 2 PA/F Edge of remnant sions, this did not occur on consecutive days. dard deviation) areas, corresponding to the home Campomanesia Pouteria grandiflora 22 m March and April 8 L/A 5 PA/F Public area Myrtaceae dichotoma Table 2– Fruiting periods and location of trees used by groups L and A for fruit consumption. Myrtaceae Hexaclamys itatiaiae January, February and March L/R PA/F Where PA = Public area and F = February Forest and March Poligonaceae Coccoloba sp. L/A PA/F Boraginaceae January Fruiting A Family Cordia superba Species Rhamnaceae Zizyphus joazeiro December and January A January,February February, Cecropiaceae Cecropia adenopus to March and A Myrtaceae Sizygium jambolanum Campomanesia April March and April Myrtaceae Anacardium November, December, dichotoma L/A Anacardiaceae occidentale January Myrtaceae Hexaclamys itatiaiae January, February and March December, January Poligonaceae February and Marchand A Anacardiaceae MangiferaCoccoloba indica sp. Boraginaceae Cordia superba FebruaryJanuary MyrtaceaeRhamnaceae Eugenia malaccensis Zizyphus joazeiroDecember December and January A Myrtaceae Sizygium jambolanum Anacardiaceae Anacardium occidentale Anacardiaceae Mangifera indica Myrtaceae Eugenia malaccensis January, February, March and April November, December, January December, January and February December PA Group PA/F L PA L/A PA L/R L/APA A A PA PA/F PA/F PA PA/F A PA L/A PA A PA A PA Location of fruit trees PA/F PA/F 53 Revista SEB Ano 14 Final.indd 53 09/10/2012 13:43:59 Brazilian Journal of Ecology ISSN 1516-5868 ranges of groups A and L, respectively. The fruit consumed by both groups came from ten tree-species with overlapping fruiting periods (Table II). There were significant differences in the frequency of monthly visits to the various quadrants, mainly as regards group A (F=3.48 df= 4; p=0.01). Visits were significantly higher in January, February and March, when a higher number of fruiting species was recorded. Most visited quadrants were those containing fruiting trees, with overlapping where at least one sleeping site was located. Trees for fruit consumption and gum extraction were distributed in the aggregate (R A=0.78 and RL=0.71), and sleeping trees randomly (R A=1.27 and RL= 1.23). Despite the presence of marmoset predators, no actual predation was recorded in the study area. Nonetheless, marmosets were vigilant on a number of occasions. Upon perceiving a great black hawk (Buteogallus urubitinga) in flight, they vocally warned other members of the group, before hiding behind branches and foliage. DISCUSSION In the present study, gum and fruit trees were distributed in the aggregate and sleeping trees randomly. Aggregate distribution signifies the individual tendency to stay together at particular sites in the environment, whereas in random distribution, there is the likelihood of individual disposition at any point whatsoever (13). On the other hand, distances between gum, sleeping and fruit trees were short, to so facilitate marmoset locomotion to neighboring areas when searching for food, thereby reducing overall travel costs. A similar pattern has already been noted in several primates, such as Ateles geoffroyi (11), Saguinus mystax and Saguinus fuscicollis (23) and Callithrix jacchus (33). The home range of primates from the Callitrix genus varies from 0.5 to 5 ha, with C. jacchus presenting the smallest ever recorded. The home range in this case is closely related to the distribution pattern of gum and fruit trees (38).The aggregate-type pattern of both justifies the establishment of two small territories wherever they occur. Above all, even though C. jacchus requires a minimum area to survive, the adequate availability of gum trees is essential (39). Differences in visit-frequency to quadrants in the home range, clearly shows the influence of fruit abundance on space-use patterns and sleepingtree location. The strong influence of gum trees and fruit abundance on the use of space, is especially manifest in groups of marmosets living in forest remnants or orchards (9) Common marmosets may sleep in trees with or without dense foliage or epiphyte cover (1, 33), high up in palm trees (30), or much lower in the canopy (8, 33). The sleeping trees used by marmosets in the PED area were robust, with DBH ranging between 28,3 and 236,82 cm, and heights ranging from 12 to 22 m. They slept in the forks of branches, where group members aggregated in a ball-like formation. This behavior probably serves to confuse possible predators through taking on the appearance of either a much larger animal or even a termite nest (16). According to an early study, the sleeping trees used by Callitrix flaviceps varied in height from 8 to more than 20 m. Through being densely overgrown with climbers, they were relatively isolated from the surrounding vegetation, thus offering safe sleepingquarters for the group members huddled together in a large ball (17). There are many potential marmoset predators in the PED. A study of an area where predators had been eradicated demonstrated that sleeping trees were located in the sites of highest feedingtree concentration (33). Regardless of its structure, the authors considered that the key variable defining sleeping-site location was the availability and location of immediate food sources. In the present study the availability of food, especially fruits, was more important than the location of their sources. Although there are no records of common marmoset predation in PED, their response to potential aerial predators, such as the black hawk (Buteogallus urubutinga), presupposes that marmosets are capable of recognizing the characteristic flight profile of falconiforms, with the consequential and immediate reaction through avoidance. This response to potential aerial predators has been recorded in Callitrix jacchus (29), and C. flaviceps (17). The loud alarm call sometimes elicits a response from other group members, while in the act of taking cover and remaining completely motionless. On taking cover at relatively low levels in the forest, the 54 Revista SEB Ano 14 Final.indd 54 09/10/2012 13:43:59 Brazilian Journal of Ecology ISSN 1516-5868 animals normally move to the underside of the supporting branch by way of a rapid lateral movement. Other studies have recorded a collared forest-falcon (Micrastur semitorquatus) predating an adult marmoset (1), a roadside hawk (Rupornis magnirostris) predating an infant (29), and an unsuccessful attempt on a group (8). Earlier studies identified aspects related to the structure and location of sleeping trees in areas where predators were present. Totally hidden by a dense entangled mass of lianas, climbers and epiphytes (1, 43, 6,17), and located at the edge of the forest, bordering open fields (42, 41), they were distributed throughout the home range, and remained without use for several successive nights (41). This is in accordance with the present findings, in that the sleeping trees used by both groups in PED were close to the forest edge and not used on consecutive days. Sleeping tree location is crucial for survival where predation risk is high, albeit less so, where predators are extinct (33). In the latter case, dailyfood acquisition, rather than predators, would be the limiting factor. In the case of PED, and in spite of the importance of fruit abundance in space-usage and sleeping-tree location, the local presence of predators, and the non-consecutive use of sleeping trees, point to protection as an important factor in the location of sleeping trees among marmosets. Differences in these results and those obtained in earlier studies (31, 8, 34, 33) reveal diversity in the strategies adopted by the common marmoset to selectively locate sleeping trees under the prevailing circumstances. CONCLUSION This study offers important contributions to an understanding of the prevailing strategies among primates, when selectively locating sleeping trees. Location, as employed by two groups of marmosets in the Parque das Dunas, was not influenced by the distribution pattern of gum and fruit trees, but by fruit abundance and the presence of potential predators, thereby showing the relationship between the strategy adopted and the type of pressure encountered. Finally, the understanding of resource distribution and sleeping tree location, perceptibly furnishes relevant factors towards the conservation of primates, in that their correct management could contribute to primate population viability. ACKNOWLEDGEMENT We are grateful to Mary Savage Praxedes and Alexandre Gusmão, managers of the Parque Estadual das Dunas, for permission to carry out this study in the Conservation area, as well as to the Instituto de Defesa do Meio Ambiente do Rio Grande do Norte (IDEMA) for financial support. RESUMO A segurança contra os predadores, a proximidade das fontes de alimento e a coesão do grupo são fatores que podem influenciar a localização de árvores de dormir em primatas. Este estudo objetivou investigar a influência da distribuição de árvores de goma e de frutos e a abundância de frutos na localização das árvores de dormir dos sagüis. Dois grupos de sagüis que vivem no Parque Estadual das Dunas, em Natal, RN, foram estudados. A varredura instantânea de amostragem foi utilizada para registrar a cada 5 min a localização dos sagüis nos mapas da área e para identificar a localização das árvores para dormir. A freqüência de uso de árvores para dormir foi registrada. As espécies das árvores utilizadas para o consumo de frutas, extração de goma e dormitório foram identificadas, e os dados fenológicos foram coletados mensalmente para determinar os períodos de abundância de frutos. As árvores de dormir estavam distribuídas aleatoriamente, aparentemente não possuindo relação com a distribuição agregada das árvores de goma e de frutos. No entanto, a abundância de frutos se apresentou como um fator importante na utilização do espaço e na localização das árvores para dormir. A presença de pontenciais predadores do sagüi, e o uso não-consecutivo de árvores de dormir apontam a proteção contra os predadores como um outro fator importante na localização das árvores de dormir na área do estudo. REFERENCES 1- ALONSO, C.; LANGGUTH, A.. Ecologia e comportamento de Callithrix jacchus (Primates: Callithrichidae) numa ilha de floresta Atlântica. 55 Revista SEB Ano 14 Final.indd 55 09/10/2012 13:43:59 Brazilian Journal of Ecology ISSN 1516-5868 Revista Nordestina de Biologia, v. 6, n. 2, p. 105–137, 1989. 2- ALTMANN, J. Observational study of behavior: Sampling methods. Behaviour, v. 49, n. 3/4, p. 227-267, 1974. 3- ANDERSON, J. R. Sleep, sleeping sites, and sleep-related activities: awakening to their significance. Am. J. Primatol. v. 46, p. 63–75, 1998. 4- AQUINO, R.; ENCARNACIÓN, F. Characteristics and use of sleeping sites in Aotus (Cebidae: Primates) in the Amazon lowlands of Peru. Am. J. Primatol. v. 11, p. 319–331, 1986. 5- BITETTI, M.S.; VIDAL, E.M.; BALDOVINO, M.C. & BENESOVSKY, V. Sleeping site preferences in tufted capuchin monkeys (Cebus apella nigritus). Am. J. Primatol. v. 50, p. 257-274, 2000. 6- CABRAL, M. C. C. Uso da área domiciliar de um grupo de Callithrix jacchus (Callithrichidae, Primates) na Estação Ecológica do Tapacurá- Pernambuco, Brazil. BSc thesis, Federal Rural University of Pernambuco, Brazil, 1989. 7- CAINE, N.G.; POTTER, M.P.; MAYER, K.E. Sleeping site selection by captive tamarins (Saguinus labiatus). Ethology v. 90, p. 63–71, 1992. 8- CAMAROTTI, F. L. M.; MONTEIRO DA CRUZ, M. A. O. Fatores ecológicos e comportamentais implicados na seleção e uso dos locais de pernoite de grupos de Callithrix jacchus em ambiente natural, p. 27–42, 1997. In: SOUZA, M.B.C.; MENEZES, A.A. L. (Eds). A Primatologia no Brazil 6. Natal, Editora da Universidade Federal do Rio Grande do Norte. 9- CASTRO, C. S. S. Tamanho da área de vida e padrão de uso do espaço em grupos de sagüis, Callithrix jacchus, Linaeus, 1758 (Primates, Callitrichidae). Revista Brasileira de Zoologia, Curitiba-PR, v. 20, n. 1, p. 91-96, 2003. 10- CASTRO, C. S. S.; ARAÚJO, A. Diet and Feeding behavior of marmoset, Callithrix jacchus. Brazilian Journal of Ecology v. 10, p. 16-21, 2007. 11- CHAPMAN, C. A.; CHAPMAN, L. J.; MCLAUGHLIN, R. L. Multiple central place foraging by spider monkeys: travel consequences of using many sleeping sites. Oecologia v. 79, p. 506–511, 1989. 12- CLARK, P. J.; EVANS, F. C. Distance to Nearest Neighbor as a Measure of Spatial Relationships in Populations. Ecology v. 35, n. 4, p. 445-453, 1954. 13- DALE, M.R.T.; Spatial pattern analysis in plant ecology. Cambridge: Cambridge University Press, 1999, p. 326. 14- DAY, R. T.; ELWOOD, R. W. Sleeping site selection by the golden-handed tamarin Saguinus midas midas: The role of predation risk, proximity to feeding sites, and territorial defence. Ethology v. 105, p. 1035-1051, 1999. 15- DAWSON, G.A. Behavioral ecology of the Panamanian tamarin, Saguinus oedipus. Unpubl. Ph.D. dissertation, Michigan State Univ., East Lansing, 1976. 16- DAWSON, G.A. The use of time and space by the Panamanian tamarin Saguinus oedipus. Folia Primatol. v. 31, p. 253-284, 1979. 17- FERRARI, S. F.; LOPES-FERRARI, M.A. Predator avoidance behaviour in the buffy-headed marmoset, Callithrix flaviceps. Primates v. 31, p. 323–338, 1990. 18- FREIRE, M. S. B. Levantamento Florístico do Parque Estadual Dunas de Natal. Acta Botânica Brasilica v. 4, n. 2, p. 131-142, 1990. 19- FOURNIER, L.A. Un método cuantitativo para la medición de características fenológicas en árboles. Turrialba v. 24, p. 422-423, 1974. 20- HAUSFATER, G.; MAEDE, B. J. Alternation of sleeping groves by yellow baboons (Papio cynocephalus) as a strategy for parasites avoidance. Primates v. 23, p. 287–297, 1982. 21- HERSHKOVITZ, P. Living New World monkeys (Platyrrhini) with an introduction to Primates. Chicago, University of Chicago Press, 1977, p. 117. 22- HEYMANN, E.W. A field observation of predation on a moustached tamarin (Saguinus mystax) by an anaconda. Int. J. Primatol. v. 8, p. 193-195, 1987. 23- HEYMANN, E.W. Sleeping habits of tamarins, Saguis mystax and Saguinus fuscicollis (Mammalia; Primates: Callitrichidae in north-eastern Peru. J. Zool. Lond. v. 237, p. 211–226, 1995. 24- IDEC/IDEMA, Plano de manejo: Parque Estadual Dunas do Natal, 1989. - Available online at: http.//www.idema.rn.gov.br [Acessed: 08/02/2010] 56 Revista SEB Ano 14 Final.indd 56 09/10/2012 13:44:00 Brazilian Journal of Ecology ISSN 1516-5868 25- IZAWA, K. A field study of the ecology and behavior of the black-mantle tamarin (Saguinus nigricollis). Primates v. 19, p. 241-274, 1978. 26- JONES, C.; JONES C.A.; JONES JR, J.K. & WILSON, D.E. Pan troglodytes. Mammalian Species v. 529, p. 1-9, 1996. 27- KAPELLER, P. M. Nests, tree holes, and the evolution of primate life histories. Am. J. Primatol. v. 46, p. 7–33, 1998. 28- LI, D., ZHOU, Q., TANG X., HUANG H., HUANG C., Sleeping site use of the whiteheaded langur Trachypithecus leucocephalus: The role of predation risk, territorial defense, and proximity to feeding sites Current Zoology(formerly Acta Zoologica Sinica),  v. 57, n. 3, p. 260 – 268, 2011. 29- LYRA-NEVES, R.M.; OLIVEIRA, M.A.B.; TELINO-JÚNIOR; W.R. & DOS SANTOS, E. M. . Comportamentos Interespecíficos entre Callithrix jacchus (Linnaeus) (Primates, Callitrichidae) e algumas aves de Mata Atlântica, Pernambuco, Brasil. Revista Brasileira de Zoologia v. 24, n. 3, p. 709-716, 2007. 30- MENEZES, M.O.T. The Use of Date Palms (Phoenix sp.) as Resting and Sleeping Sites by Callithrix jacchus in Northeastern Brazil. Neotropical Primates v. 12, n. 2, p. 53-55, 2004. 31- MENDES PONTES, A. R. Influência dos fatores ambientais e comportamentais na dinâmica de um grupo selvagem de Callithrix jacchus (Callitrichidae, Primate) na mata de Dois Irmãos, Recife, Pernambuco, Brazil. BSc thesis, Federal University of Pernambuco, Brazil, 1989. 32- MENDES PONTES, A.R.; MONTEIRO DA CRUZ, M. A. O. Home range, intergroup transfers and reproductive status of common marmosets Callithrix jacchus in a forest fragment in Northeastern Brazil. Primates v. 36, p. 335-347, 1995. 33- MENDES PONTES, A.R.M.; LIRA SOARES, M. Sleeping sites of common marmosets (Callithrix jacchus) in defaunated urban forest fragments: a strategy to maximize food intake. J. Zool. London. v. 266, p. 55-63, 2005. 34- MONTEIRO DA CRUZ, M. A. O. Dinâmica reprodutiva de uma população de sagüis-do-nordeste (Callithrix jacchus) na Estação Ecológica de Tapacurá. PhD thesis, University of São Pau- lo, 1998. 35- MORI, S. A. Eastern, extra-Amazonian Brazil. p. 428–454, 1989. in Campbell, D. G. & Hammond, H. D. (Eds). Floristic inventory of tropical countries: the status of plant systematics, collections, and vegetation, plus recommendations for the future. New York Botanical Garden, New York. 36- PHOONJAMPA, R., KOENIG, A., BORRIES C., GALE, G.A., SAVIN,T. Selection of Sleeping Trees in Pileated Gibbons (Hylobates pileatus). American Journal of Primatology, v. 72, p. 617–625, 2010. 37- REICHARD, U. Sleeping sites, sleeping places, and the presleep behaviour of gibbons. Am. J. Primatol. v. 46, p. 35–62, 1998. 38- RYLANDS, A.B.; FARIA, D.S. Habitats, feeding, and home range size in the genus Callithrix, p. 262-272, 1993. In: RYLANDS, A.B. (Ed). Marmosets and Tamarins (Systematics, Behaviour, and Ecology). New York, Oxford Univ. Press, p. 396. 39- SCANLON, C. E.; CHALMERS, N. R.; MONTEIRO DA CRUZ, M. A. O. Home range use and the explotation of gum in the marmoset Callithrix jacchus jacchus. Intern. J. Primatol, v. 10, p. 123-136, 1989. 40- SMITH A.C., KNOGGE C., HUCK M., LÖTTKER P., BUCHANAN-SMITH H.M. Long-term patterns of sleeping site use in wild saddleback Saguinus fuscicollis and mustached tamarins S. mystax: effects of foraging, thermoregulation, predation, and resource defense constraints. American Journal of Physical Anthropology v. 134, p. 340–353, 2007. 41- SNOWDON, C. T.; SOINI, P. The tamarins genus. In Ecology and behaviour of Neotropical Primates: p. 246–248, 1988. In: MITTERMEIER, R. A., RYLANDS, A. B., COIMBRA-FILHO, A. F. ; FONSECA, G. A. B. (Eds).Washington, DC:WorldWildlife Fund. 42- SOINI, P. The pygmymarmoset, genus Cebuella.In Ecology and behaviour of Neotropical Primates: p. 79–129, 1988 In: (Eds).Washington, DC:WorldWildlife Fund. 43- STEVENSON, M.F.; A.B. RYLANDS. The marmosets, genus Callithrix, p. 131-211, 1988. In: MITTERMEIER, R. A., RYLANDS, A. B., COIM- 57 Revista SEB Ano 14 Final.indd 57 09/10/2012 13:44:00 Brazilian Journal of Ecology ISSN 1516-5868 BRA-FILHO, A. F.; FONSECA, G. A. B. (Eds). Ecology and Behavior of Neotropical Primates. Washington, D.C., World Wildlife Fund, p. 610. 44- TILSON, R. L.; TENAZA, R. R. Interspecific spacing between gibbons (Hylobates klossii) and langurs (Presbytis potenziani) on Siberut island, Indonesia. Am. J. Primatol. v. 2, p. 355– 361, 1982. 45- VIANA, V. M.; TABANEZ, A. J.; BATISTA, J. L. Dynamics and restoration of forest fragments in the Brazilian Atlantic moist forest. p. 351–365, 1997. in Laurance, W. F. & Bierregaard, R. O. Jr (Eds). Tropical forest remnants: ecology, management, and conservation of fragmented communities. University of Chicago Press, Chicago. 46- VON HIPPEL, F.A. Use of sleeping trees by black and white colobus monkeys Colobus guereza in the Kekamega forest, Kenya. American Journal of Primatology v. 45, p. 281–290, 1998. 47- ZHANG, S.Y. Sleeping habits of brown capuchin monkeys (Cebus apella) in French Guiana. Am. J. Primatol. v. 36, p. 327-335, 1995. 58 Revista SEB Ano 14 Final.indd 58 09/10/2012 13:44:00 Brazilian Journal of Ecology ISSN 1516-5868 Environmental impacts caused by roads and trails in the Altomontana Private Reserve, Itamonte, Minas Gerais. Ana Cristina Magalhães de França - Universidade Federal de Lavras, Departamento de Biologia/Setor de Ecologia (e-mail: anafranca.bio@gmail.com) Felipe Santana Machado - Universidade Federal de Lavras, Departamento de Ciências Florestais (e-mail: epilefsama@hotmail.com) Rosângela Alves Tristão Borém - Universidade Federal de Lavras, Departamento de Biologia/Setor de Ecologia (e-mail: tristao@dbi.ufla.br) Luís Antônio Coimbra Borges - Universidade Federal de Lavras, Departamento de Ciências Florestais (email: luis.borges@dcf.ufla.br) ABSTRACT The adequate planning and management of highways contribute to reducing environmental impacts. In conservation units, the evaluation of possible environmental impacts caused by roads has facilitated the adoption of preventive action, with a view to avoiding biodiversity loss. In this sense, impacts caused by roads and trails in the Altomontana Private Reserve, Itamonte, Minas Gerais State, Brazil, were assessed, as a means of obtaining information for improving road and trail management in the unit, as well as mitigating those impacts that generate local environmental degradation. Internal roadways of the property were scoured, and points along the altitude gradient marked. A grading impact array was used for standardizing observations. Marks of 0 to 3 were attributed to characterizing the intensity of impacts, with positive or negative signs added, according to the type of impact. Among the observed environmental impacts caused by roads, erosion, the most outstanding variable, occurred at all altitudes, with discarded waste as runner up. All told, local vegetation appeared to be well-conserved, with the variation in altitude favoring the formation of various physiognomies, thereby constituting an appropriate environment for developing local community activities as part of environmental education programs. Key words: Environmental impact assessment; roads; conservation unit. INTRODUCTION The divulgation of environmental damage by organizations dedicated to the protection of the environment has contributed decisively towards consolidating the Evaluation of Environmental Impacts (EEI), as a tool for registering data applied to measuring the consequences arising from anthropic activities in natural ecosystems, and as a forerunner of means for taking the necessary steps towards maintaining the quality of the environment (22). Following the United Nations Conference on the Environment, in 1972, there have been modifications in the policies for development and economic intervention, which are no longer exclusively orientated by economic-financial parameters. From there on, environmental and socio-economic questions have also been inserted (9), thereby leading to the publication of literature specialized in evaluation and reports on environmental impacts (25, 23, 17). 59 Revista SEB Ano 14 Final.indd 59 09/10/2012 13:44:00 Brazilian Journal of Ecology ISSN 1516-5868 Around this time, the EEI turned up in Brazil, as a prerequisite for financial research by international organizations (24). Subsequently, this was inserted into the National Policy for the Environment (NPE), regulated according to the Federal Law 6.938/81. This later became obligatory on licensing processes involving polluting activities or those modifying the natural environment (22). The advance in the protection of Brazilian ecosystems continued with the Federal Law 9.605|98. Law of Environmental Crimes (5), and the Federal Law 9.985|00, which instituted the National System of Nature Conservation Units (6) thereby establishing criteria and norms for the creation, implantation and management of Conservation Units (CU). Among these, and within the group Sustainable Use, the Private Reserve of Natural Patrimony (PRNP) is a private area which aims at perpetually conserving biodiversity, and, according to article 21, permits scientific research, as well as tourism, recreation and educational visits. The evaluation of impacts caused by roads is a recent line of research, and over the past few years, studies have been developed with the aim of acquiring knowledge on the possible effects on ecosystems (4, 8, 15, 18, 7). According to Gumier-Costa & Sperber (200), some of these have emphasized the impact of routes inside CUs, when considering that trails and roads possibly induce the isolation and fragmentation of environments, besides animal-hits when crossing. The impacts pointed out by Forman & Alexander (1998) include difficulty in dispersion by native plants, the introduction of exotic species, noise, changes in the levels of lighting, the attraction and repulsion of fauna, problems with drainage, erosion, atmospheric pollution through the emission of gases from fuel combustion, and the increase of dust in the air. The evaluation of environmental impacts caused by roads in CUs would effectively contribute towards the improvement of management planning, thereby facilitating the adoption of preventive and corrective action. The aim was to assay and analyze environmental impacts caused by roads and trails inside the Altomontana PRNP, in Itamonte, Minas Gerais State, Brazil. As this unit is in the initial creation phase, this study will contribute with relevant information towards the elaboration of management planning. The specific aims were: a) describe environmental impacts caused by roads; b) analyze and systematize data referring to road impacts, to so improve CU management; and c) propose mitigating solutions for degraded areas. METHODOLOGY Study Area The study took place in the Altomontana PRNP, in Itamonte county, Minas Gerais State (22º21’51”S and 44º48’29”W). The steep altitude gradient varies from 1.450 to 2.400 meters. An inner road gives access to water slides, where the altitude reaches 2.140 meters. Close to the buildings at the entrance of the unit, trails lead away to the waterfalls. The total CU area is 672 hectares, comprising a mosaic of phytophysiognomies, that of semi deciduous seasonal forest being the most representative (sensu 27). The climate is of the Köppen Cwb type, and mesothermic, with dry winters and mild, rainy summers. The average annual temperature varies from 17.4ºC to 19.8ºC. The dry season extends from May to September, with the driest period occurring in June and July, and the rainiest during December and January (21). The PRNP, a private property inserted within the Area of Environmental Protection (AEP) of the Serra da Mantiqueira, contains a large area with remnant Atlantic Rain Forest. Sampling The inner roads (main and adjacent, as well as trails) were scoured and points marked at the extremities and along the altitude gradient, by means of GPS Garmin GPSMAP® 76Csx apparatus. Collected data was systematized in an impact grading matrix, adapted from Leopold et al. (1971), for standardizing observations and analyzing impacts. Impacts were characterized and analyzed by way of spot road-width measurements and respective intervention on roadside vegetation. The height of the embankment was evaluated in accordance with the roadside-presence of developed and adult native tree species, and vegetal soil cover. Visual and risk characterization of the occurrence of impacts, such as fire, erosion and waste, as well as other anthropic activities, were also investigated. The impacts were quantitatively classified as to magnitude; points 60 Revista SEB Ano 14 Final.indd 60 09/10/2012 13:44:00 Brazilian Journal of Ecology ISSN 1516-5868 from zero to three were attributed for characterization, and qualitatively as to intrinsic value, to which were added positive and negative signs, according to the type of impact. Summation indicated the most impacted sights. Employees were interviewed as to outstanding natural events prior to the study period, with visual documentation (photographs) of the impact. RESULTS Impacts caused by anthropic activity, such as visits, animal raising, the traffic of vehicles, and the points of erosion arising from these activities, were the most marked negative environmental impacts encountered along the road crossing the property. Vegetal conservation and soil cover were the most relevant positive aspects, these acquiring the highest marks. Environmental impacts analyzed on the inner road of the CU appear in Table 1. According to summation, the most impacted environment was located at point 1, close to the entrance of the PRNP. As informed, the largest area of erosion (Point 1), acquired its present form due to a land-slide that occurred in 2005, thereby starting the formation of a roadside ravine, at the moment 30 meters wide at the northern end, and with a 13-meter-wide crater in the south (Figures 1A and 1B). Points of erosion were also noted at higher altitudes, this type of visual impact being the most remarkable. In some spots of the road, the incorrect drainage of rainwater has given rise to large natural ruts, thereby indicating the formation of fresh points of erosion (Figure 1C). Artificial ditches for better rain-water drainage were also seen. Although small areas of erosion were noted in points 2 and 3, generally speaking, final summation of positive and negative impacts indicated adequate conservation of the stretch of road, roadside vegetation and height of embankments. A large clump of bamboo was noted at a higher level (Point 4). Its origin is unknown, and further studies are required, as it was impossible to relate it to the presence of a road (Figure 1D). The highest negative impact caused by anthropic activities along the road was in point 6, where an artificial clearing had been made for the installation of a telecommunication antenna. At this point, besides complete soil exposure, there was a considerable amount of remnant material. At the highest point, 2.140 meters (Point 7), vestiges of unauthorized camping were found, clear evidence of area vulnerability. This included signs of a bonfire (Figure 3), non-biodegradable packaging, and the opening of a trail in the vegetation. Old scrawls on the rocks were noted as a main negative visual impact (Figure 3). Table 1: Environmental impacts on the road inside the Altomontana PRNP, Itamonte/MG. Sampling points 1 2 3 4 5 6 7 Altitude (m) 1.533 1.560 1.645 1.800 1.960 2.130 2.140 Erosion -3 -1 -1 -1 0 -1* 0 Fire 0 0 0 0* 0 0 -2* Waste -1 -1 0 0 0 -3 -3* Anthropic activity -2 -1 -1 0 0 -3 -1* Preservation of +1 +2 +2 +1 +3 +1 +2* vegetation Height of canopyt +3 +2 +1 +1 +3 0 0 Soil vegetation cover +1 +2 +2 0 +3 0 +3 Visual impact -3 -1 +2 -1 +3 -3 +2 Total impact at the -4 +2 +5 0 +12 -9 +1 point Extent of roadside 10,20 9,50 6,50 8,00 7,70 ** ** vegetation (m) Road-width (m) 5,40 5,30 4,30 5,00 4,40 ** ** Legend: Types of impact: [-] Negative impact; [+] Positive impact Intensity of the impact: [0] None; [1] Low; [2] Medium; [3] High *Vulnerable; **Artificial clearing Summation -7 -2 -8 -8 +12 +10 +11 -1 +7 41,90 24,40 61 Revista SEB Ano 14 Final.indd 61 09/10/2012 13:44:00 Brazilian Journal of Ecology ISSN 1516-5868 Apart from the main road, there are two trails, the Trail to the Waterfall (Points 10, 11 and 12) and to the Forest of the Elves (Points 14,15 and 16). Both were scoured for signs of impacts (Table 2). The main vestiges found were the residues of a bonfire, discarded non-biodegraded objects and small points of erosion. Around the higher-placed waterfall, the visual impact was great, due to stone arches built by the former proprietor (Figure 4B). This did not occur at the better conserved, lowerplaced waterfall. Positive points were the presence of alcoves appropriate for leisure, with wellinstalled grills. Nonetheless, the wrongly placed bonfire residues close to the waterfall was a clear indication of the need for dedicating more attention to visitor orientation on the best use of the area. All 62 Revista SEB Ano 14 Final.indd 62 09/10/2012 13:44:00 Brazilian Journal of Ecology ISSN 1516-5868 along the trail, the well-preserved vegetation (Figures 4C and 4D) with enclosing canopy, and the appearance of pioneer plants along the edges, were clear indications of initial regeneration processes (Figure 4A). Nowhere on the trails or around the waterfalls were there garbage cans for the selective collection of waste. 8 9 10 11 In point 9, 1.563 meters high, there is an 8-meter-wide road, adjacent to the main one and leading to an abandoned building. The road is around 800 meters long, and has been out of use for more than 5 years. It is in the regeneration stage, with the beginning of soil coverage by creepers. Sampling points 12 13 Altitude (m) 2.110 1.563 1.490 1.465 Erosion 0 -3 0 -1 Fire 0* 0 0 0 Waste 0 -2 0 0 Anthropic activity 0 -2 0 0 Preservation of +3 +3 +3 +3 vegetation Height of canopy +1 +3 +3 +3 Vegetation soil cover +3 +3 +3 +2 Visual impact +1 -2 +3 -1 Point total impact +8 0 +12 +6 5,80 4,50 4,40 2,80 Extent of roadside vegetation (m) Road-width (m) 3,00 4,00 2,40 2,00 Legend: Types of impact: [-] Negative impact; [+] Positive impact Impact Intensity: [0] None; [1] Low; [2] Medium; [3] High *Vulnerable; **Artificial clearing 14 15 16 Summation 1.455 0 -3 -3 -3 +3 1.475 -2 0 -2 -3 +1 1.490 0 0 0 0 +3 1.445 -1 0 0 -3 +1 1.435 -1 0 0 -3 +1 +3 +2 -2 -3 2,00 0 0 -2 -8 ** +3 +3 +1 +10 3,00 0 +1 -2 -4 6,00 0 +1 -2 -4 6,00 +16 +18 -6 +17 34,50 2,00 ** 3,00 6,00 6,00 28,40 -8 -3 -7 -17 +21 63 Revista SEB Ano 14 Final.indd 63 09/10/2012 13:44:00 Brazilian Journal of Ecology ISSN 1516-5868 Several points of erosion were also observed, with heights varying between 1,80 and 3 meters on the northern edge. In some points inclined trees and marked root exposure were apparent (Figure 4E). The vegetation in this area is well-preserved with an estimated 15-meter canopy (Figure 4F). The negative points for visual impact were the occurrence of non-biodegraded waste, mainly around the abandoned building. Tires, cans of oil and several types of plastic packaging were also found. No indicative signs or indications of strategic planning, to facilitate animal crossing or avoid accidents with the local fauna, were observed in any of the points evaluated. DISCUSSION The most impacted areas are located at either end of the main road, the outstanding points being the presence of erosion, discarded material and the remains of fire. This could be related to the permanence of people, seeing that the road is used only for passage between the lower part and the gliding ramps. One factor that may have contributed to the advance of erosion on the main road could be the recent entrance of heavy vehicles, for the installation of telecommunication antennas. This occurred before the present assaying. The crater cause by the landslide in 2005 presented visible signs of instability. Moreover, before this, the road was 10 meters wide, whereas now it is only 5,40m. Small landslides were noted and it is interesting to point out the possibility of the crater increasing in size, since vegetation is not in the process of regeneration. The slope of the land could be the main cause of erosion, thus corroborating Oliveira et al., (2010a), and Antonangelo & Fenner (2005), who pointed out declivity as being one of the generating factors of erosion. Further studies are required, with specific methodologies on declivity and erosion, to evaluate local vulnerability and instability. Concrete gutters were built along the road to improve rainwater drainage. However, their inef- 64 Revista SEB Ano 14 Final.indd 64 09/10/2012 13:44:01 Brazilian Journal of Ecology ISSN 1516-5868 ficiency was apparent, seeing that incorrect drainage was the means of accelerating erosion in some points. Surface drainage of rainwater is a preponderant factor in the formation of erosive processes, according to WEPP (Water Erosion Prediction Project), and as cited by Machado et al. (2003) and Garcia (2001). The adoption of preventive measures and the subsequent monitoring are attitudes which are simple, efficient and financially cheaper, when compared to corrective measures (20) Certain measures can be taken, such as the recuperation and contention of canopy, the maintenance of adequate gutters, planting seedlings of native plants where erosion is in an advanced stage (20), programs of environmental education, supervision in areas of easy access, and studies on the influence of vehicle traffic on vertebrate communities, as suggested by Bager & Rosa (2010), who proposed specific studies and the use of an index for implanting mitigating measures against wild-fauna hits. The presence of discarded non-biodegraded material, such as tires, oil cans, glass bottles and plastic packaging, was observed in isolated points. Even though it was impossible to estimate the time this material has been in the area, their very presence is a sign of vulnerability. The withdrawal of this material is indispensable, since these residues are prejudicial, both visually and to the native fauna. Although roads are necessary structures for the flow of material and people, their very existence can negatively affect the fauna (4, 7, 15, 26). Some studies, besides outlining the high diversity and abundance of biota, demonstrate their fragility in the face of anthropic impacts caused in their environment. Thus, it can be perceived that the Altomontana PRNP does not present the necessary structure or the required preventive measures against the loss of biodiversity through the ingestion of residues, the isolation of subpopulations, or road-hits, whence the need for undertaking appropriate studies in this field. The presence of well-preserved vegetation, the various phytophysiognomies encountered on the altitudinal gradient and the wide expanse of the CU, go well towards affirming that the PRNP had reached a high level of environmental heterogeneity and complexity. Similar situations have been the focus of a series of studies, such as by August (1983) and Vera Y Conde & Rocha (2006). Heterogeneity in any environment is represented by the vertical stratum developed. Apart from the characteristics of woody plants, the presence of epiphytes is considered a positive factor as it concerns environmental heterogeneity. According to Gatti (2000), they are extremely important as indicators of the maintenance of biological diversity and the interactive equilibrium among species, since their successful establishment and diversity is highly dependent on environmental conditions (13). Through their sensitivity to anthropic impacts, their role as indicators of environmental quality is further enhanced. Thus, the presence of epiphytic plants was a clear indication of preservation along roads and trails. . The presence of a bamboo grove at a fixed altitude caused a visual impact. As it extended over the areas of other properties, always at the same variations in altitude, its origin can probably be associated to a natural occurrence. Even so, additional more detailed studies are required to better understand the occurrence. As the management plan for the CU is in the elaboration phase, and together with the results of this evaluation of impacts, the proposal is to charge an entrance fee for recreational visits and access to water slides, as a form of maintaining the roads and trails on the property, since, through being a CU of sustainable use, the use of areas for recreation and environmental education is permitted. Nevertheless, it is recommended that the entrance of visitors be limited, and selective garbage cans installed in the entrance of the reserve, in the areas of recreation at the waterfalls, and alongside water slides. The elaboration of environmental education programs should also become an alternative for the better enlightenment of visitors, as to the preservation of the area. CONCLUSION Among the various environmental impacts caused by the road, erosion at all altitudes is extremely prominent, with the presence of discarded waste as a close runner up. The vegetation on the edges of trails and roads was found to be well-preserved, thus comprising a propitious environment for the development of insertion activities among the local community, as part of programs on environmental edu- 65 Revista SEB Ano 14 Final.indd 65 09/10/2012 13:44:01 Brazilian Journal of Ecology ISSN 1516-5868 cation. The most impacted strips are the extremities of roads and trails, where preventive supervision is required. The proposal is the adoption of a series of measures, such as the control of visitor entrance, the creation of educational activities on environmental conservation for PRPN-user enlightenment, the supervision of critical points, the restoration of unstable points of erosion with native plants, signs at various points on the road, with emphasis on the existence of fauna, and the need to reduce speed, as administrative tools to better conserve the area. ACKNOWLEDGEMENT Thanks are extended to the owners of the Altomontana PRPN for logistic support and accompaniment throughout the work . RESUMO Planejamento e gestão adequada de estradas contribuem para a redução dos impactos ambientais. Em Unidades de Conservação, a avaliação de possíveis impactos ambientais causados pelas estradas permite a adoção de ações preventivas, visando evitar a perda de biodiversidade. Nesse intuito, foi realizado um levantamento de impactos causados pelas estradas e trilhas da RPPN Altomontana, Itamonte (MG/Brasil), objetivando fornecer informações para um melhor manejo das estradas e trilhas da unidade de conservação, bem como mitigar impactos que geraram degradação ambiental da área. As extensões das estradas internas da propriedade foram percorridas, sendo marcados pontos nos extremos e ao longo do gradiente altitudinal. Uma matriz de gradação de impactos foi utilizada para padronizar as observações. Foram atribuídas notas de zero a três para caracterizar a intensidade dos impactos, acrescidos dos sinais positivo e negativo conforme o tipo de impacto. Dentre os impactos ambientais observados causados pelas estradas, a erosão foi a variável de maior destaque, ocorrendo em todas as faixas de altitude da propriedade, seguida da presença de lixo descartado. De modo geral, a vegetação da área encontra-se bem conservada e a variação de altitude favorece a formação de diferentes fitofisionomias, sendo um ambiente propício ao desenvolvimento de atividades de inserção da comunidade local em programas de educação ambiental. Palavras-chave: avaliação de impacto ambiental, estradas, Unidade de conservação. REFERENCES 1- ANTONANGELO, A., FENNER, P. T. Identificação dos riscos de erosão em estradas de uso florestal através do critério do fator topográfico LS. Energia na Agricultura, Botucatu, v. 20, n. 3, p. 1-20, 2005. 2- AUGUST, P. V. The role of habitat complexity and heterogeneity in structuring tropical mammal communities. Ecology, New York, v. 64, n. 6, p. 1495-1507, 1983. 3- BAGER, A., ROSA, C. A. Priority ranking of Road sites for mitigating wildlife roadkill. Biota Neotropica, São Paulo, v. 10, n. 4, p. 149-153, 2010. 4- BENÍTEZ-LÓPEZ, A., ALKEMADE, R., PITA, A. V. The impacts of roads and other infrastructure on mammal and bird populations: a metaanalysis. Biological Conservation, v. 143. p. 1307-1316, 2010. 5- BRASIL, 1998. Lei Federal 9.605 de 12 de fevereiro de 1998. Lei de crimes Ambientais. Disponível em <http://www.planalto.gov.br/ccivil/ Leis/L9605.htm> acessado em 10 maio 2011. 6- BRASIL, 2000. Lei Federal 9.985 de 18 de julho de 2000. Sistema Nacional de Unidades de Conservação. Disponível em <http://www.planalto. gov.br/ccivil_03/Leis/L9985.htm> acessado em 10 maio 2011. 7- CLEVENGER, A.P., CHRUSZCZ, B. & GUNSON, K. E. Spatial patterns and factors influencing small vertebrate fauna road-kill aggregations. Biological Conservation, v. 109, p. 15-26, 2003. 8- CORREA, C. M. C., CRUZ, J, Erosão real e estimada através da Rusle em estradas florestais, em relevo ondulado a fortemente ondulado. Revista Árvore, Viçosa, v. 34, n. 4, p. 587-595, 2010. 9- FERREIRA, R. M. A. Avaliação de Impacto Ambiental e a Legislação Brasileira. Informe Agropecuário, Belo Horizonte, v. 21, n. 202, p.5-11, 2000. 10-FORMAN, R. T. T., ALEXANDER, L .E. Roads and their major ecological effects. Annual Review of Ecology and Systematics, v. 29, p. 207-231, 1998. 66 Revista SEB Ano 14 Final.indd 66 09/10/2012 13:44:01 Brazilian Journal of Ecology ISSN 1516-5868 11-GARCIA, A. R. Uso do modelo WEPP (Water Erosion Prediction Project) modificado para estimar taxas de erosão em estradas florestais. 2001. 96 f. Tese (Doutorado em Ciência Florestal) – Universidade Federal de Viçosa, Viçosa. 2001. 12-GATTI, A. L. S. O componente epifítico vascular da Reserva Natural de Salto Morato, Guaraqueçaba, PR. 2000. 93f. Dissertação (Mestrado em Botânica) - Universidade Federal do Paraná, Curitiba, PR. 2000. 13-GIONGO, C., WAECHTER, J. L. Composição florística e estrutura comunitária de epifíticos vasculares em uma floresta de galeria na Depressão Central do Rio Grande do Sul. Revista Brasileira de Botânica, São Paulo, v. 27, n. 3, p. 563-572, 2004. 14-GUMIER-COSTA, F., SPERBER, C. F. Atropelamentos de vertebrados na Floresta Nacional de Carajás, Pará, Brasil. Acta Amazonica, Manaus, v. 39, n. 2, p. 459- 466, 2009. 15-HELS, T., BUCHWALD, E. The effect of road kills on amphibian population. Biological Conservation, v. 99, p.331-340, 2001. 16-LEOPOLD, L. B.; CLARKE, F. S.; HANSHAW, B. B.; BALSEY-JR,T. A. Procedure for evaluating environmental impact. Washington: U. S. Geological Survey, 1971. 13p. 17-MACHADO, C. C., GARCIA, A. R., SILVA, E., FONTES, A. M. Comparação de taxas de erosão em estradas florestais estimadas pelo modelo WEPP (Water Erosion Prediction Project) modificado em relação a medições experimentais. Revista Árvore, Viçosa, v. 27, n. 3, p. 295-300, 2003. 18-MARCELINO, F. A. Avaliação dos sistemas de redes viárias florestais em função dos custos e riscos de erosão. 2007. 129 f. Tese (Doutorado em Agronomia) – Universidade Estadual Paulista, Botucatu. 2007. 19-OLIVEIRA, F. P., SILVA, M. L. N., AVANZI, J. C., CURI, N., LEITE, F. P. Avaliação das perdas do solo em estradas florestais não pavimentadas no Vale do Rio Doce, Minas Gerais. Scientia Forestalis, Piracicaba, v. 38, n. 87, p. 331-339, 2010[a]. 20-OLIVEIRA, A. H., SILVA, M. L. N., AVANZI, J. C., SILVA, M. A., CURI, N. Erosão hídrica em estradas florestais: causas e controle. Revista de Geografia, Recife, v. 27, n. 2, p. 126-140, 2010[b]. 21-PANE, E. Estudo Hidrológico, Hidrogeológico e Geofísico no município de Itamonte - MG. 2001. 84 f. Dissertação (Mestrado) – Universidade Estadual de Campinas, Campinas, SP. 2001. 22-PEREIRA, J. A. A.; BORÉM, R. S. T., SANT’ANA, C. M. Análise e avaliação de impactos ambientais. Lavras: UFLA/FAEPE, 2001, 147p. 23-RODRIGUES, G. S., CAMPANHOLA, C. Sistema integrado de avaliação de impacto ambiental aplicado a atividades do Novo Rural. Pesquisa Agropecuária Brasileira, Brasília, v. 38, n. 4, p. 445-451, 2003. 24-ROHDE, M. G. Estudos de impacto ambiental: a situação brasileira. In: VERDUM, R., MEDEIROS, R. M. V. [org.] RIMA, Relatório de Impacto Ambiental: Legislação, elaboração e resultados. 3ªed. ampl. Porto Alegre: Ed. Universidade/UFRGS, 1995, p. 20-36. 25-SILVEIRA NETO, S., MONTEIRO, R. C., ZUCCHI, R. A., MORAES, R. C. B. Uso de análise faunística de insetos na avaliação de impactos ambientais. Scientia Agricola, Piracicaba, v. 52, n.1, p. 9-15, 1995. 26-TROMBULAK, S. C., FRISSELL, C. A. Review of ecological effects of roads on terrestrial and aquatic communities. Conservation Biology, v.14, n. 1, p.18-30, 2000. 27-VELOSO, H. P., RANGEL-FILHO, A. L. R., LIMA, J. C. A. Classificação da vegetação brasileira, adaptada a um sistema universal. Rio de Janeiro: Fundação Instituto Brasileiro de Geografia e Estatísitica – IBGE. 1991, 124p. 28-VERA Y CONDE, C. F., ROCHA, C. F. D. Habitat disturbance and small mammal richness and diversity in an Atlantic Rainforest area in Southeastern Brazil. Brazilian Journal of Biology, São Carlos, v. 66, n. 4, p. 983-990, 2006. 67 Revista SEB Ano 14 Final.indd 67 09/10/2012 13:44:01 Brazilian Journal of Ecology ISSN 1516-5868 68 Revista SEB Ano 14 Final.indd 68 09/10/2012 13:44:01 Brazilian Journal of Ecology ISSN 1516-5868 FlorIstic and spatial distribution of Orchidaceae species in the Serra do Mucambo, Conceição do Coité, Bahia, Brazil *Denis Nunes de Carvalho, Centro Universitário Jorge Amado (email: denisnunis-@hotmail.com) Cássio van den Berg, Universidade Estadual de Feira de Santana (email: vcassio@gmail.com) Camila Magalhães Pigozzo, Centro Universitário Jorge Amado (email: camilapigozzo@yahoo.com.br) ABSTRACT The aim of the present study was to evaluate the Orchidaceae family in the Serra do Mucambo, Conceição do Coité, Bahia and to describe the local population distribution patterns, as well as discuss local factors that influenced species distribution. Sixteen species in 14 genera were found. The genera Trichocentrum and Vanilla presented the highest number of species, with two each. All species displayed aggregated distribution. The highest abundance and species richness were found at higher altitudes. Availability of resources is possibly the main factor influencing species distribution. Key-words: resources, elevation, abundance IntroduCTION The Orchidaceae family contains around 850 genera and 20,000 species, amongst which, 235 genera and 2,419 species have been registered in Brazil (6). Distribution of the family is cosmopolitan, Pantropical, and probably the second largest among the angiosperms (5), with the main centers of diversity in the tropical regions of America and Asia (9). Besides taxonomic representability, the family is valued by the ornamental potential of the flowers (16). The use of the flowers for ornamentation purposes represents one of the threats to orchid species diversity, through removal from their natural habitats. Another ominous factor is the constant destruction of habitats through the advance of agriculture (16, 22). Thus, extinction could also be a consequence of the reduction in area of occupancy, since only larger areas sustain large populations. (18) In a plant community, plants are aggregated according to the various intra and interspecific associations throughout their natural distribution (14). Besides anthropic alterations, which incur vegetal impacts, there are also natural alterations arising from differences in the soil, and variations in humidity and altitude, which contribute to floristically characterizing certain areas of the mountain range (34). Altitude, a possible relevant factor, can induce a soil and climate grid, an important aspect in the repartition of the various floristic aggregates, thereby contributing to the different vegetation patterns in the landscape (24, 10). The distribution of the different ecological substrata and refuges is related to the degree of local shade or illumination, whence the selective process of appropriate environments for the development of certain types of vegetation in detriment of others (10). Through humidity, as well as the presence of a substratum, being limiting factors in the distribution of epiphytic orchids (7), epiphyte diversity can be used as an ecological indicator of the quality and conservation of humid forests (22). On the whole, in Bahia, botanical studies in the field are concentrated in the Chapada Diamantina (3, 4, 12, 19, 20, 32, 36, 40, 37), with only a few studies having been undertaken in the centerwestern part of the state (15). Further on, the find- 69 Revista SEB Ano 14 Final.indd 69 09/10/2012 13:44:01 Brazilian Journal of Ecology ISSN 1516-5868 ings will be commented on, since a list of citations without contents would not be informative. Studies on Orchidaceae spatial distribution are still scarce, especially in northeast Brazil. On considering the work done on orchid spatial distribution, the importance of the family, the threats to its diversity, the scarcity of studies of northeast Bahia, and the need for a better understanding of the factors that influence the distribution of these species, the aim of the present study was to undertake a floristic survey of orchid species in the Serra do Mucambo, thereby identifying the spatial distribution of populations and investigating factors defining their occurrence and distribution. METODOLOGY Characterization of the study area – Conceição do Coité is located in the northeastern part of Bahia State (11°31’ S and 39°19’ W). The study area was at the highest point of the municipality, at an altitude of 575 meters. The surroundings and some parts of the Serra have already been deforested for sisal (Agave sisalana Perrine) hemp production and cattle raising. The climate is semiarid, with temperatures ranging from 16.1 to 33ºC, and an average rainfall of 500 to 800 mm. Vegetation is mixed, with elements from the arboreal Caatinga and arborealbushy Caatinga, and with the presence of palm trees (Arecaceae) of the species Syagrus coronata (Mart.) Becc. Collection of data – 20 fixed and noncontiguous quadrats measuring 10×10m, in total 2.000m², were marked out according to methodology developed by Almeida et al., (2007), but with modifications, with random distribution at various altitudes, an irregular number at each, along a sloping gradient of 449 to 575m, with no fixed difference between. Elevation and coordinates were obtained with a GPS Garmin eTrex Vista HCx, Personal Navigator. The fertile orchids in each quadrant were collected, pressed, identified and quantified. The amount of available resources was also measured, taking into account, trees, lianas, soil and palm trees. Rock, as a source, was eliminated. Trees and lianas were measured as to the percentage of cover, and soil, as to the available area. Palm trees were counted. The total of available resources was obtained by substituting scarce, abundant and very abundant by the numbers 2, 3 and 4, respectively, and with the summation of values attributed to soil, trees and lianas, and the number of palm trees. As regards epiphyte species, even individuals that had accidentally fallen, and were still alive on the soil and remained fixed to dry branches, were included. Collections took place from January to December, 2010, thus twelve in total. Specimens were deposited in the herbarium of the Universidade Estadual de Feira de Santana (HUEFS). Analysis of data – species identification was from specialized literature by Pabst & Dungs (1975, 1977). When necessary, the material was compared to specimens from the collection of HUEFS. Species binomials were standardized in accordance with the World Check List of Selected Plant Families, the Royal Botanic Gardens, Kew (http://apps.kew.org/wcsp/qsearch.do). The Morisita index (27) was used for identifying species distribution patterns. Absolute taxon frequency was calculated by the formula described by Maracajá et al.(2003): where FAt is the absolute taxon frequency, Pt the number of plots where the taxa occurred, and P the number of sampled plots. Analysis of correlations between the amount of resources and orchid frequency was performed to evaluate the influence of resource availability. Cluster analysis of qualitative and quantitative data with the UPGMA method in the PCORD 4.0 software, using the Sorensen Index for qualitative, and the Morisita-Horn Index for quantitative, was used to evaluate whether more similar quadrants, in terms of resources, would be more similar as to floristic composition. Correlation analysis with SPSS for Windows was to evaluate the relationships between abundance and richness among species at different altitudes. . 70 Revista SEB Ano 14 Final.indd 70 09/10/2012 13:44:01 Brazilian Journal of Ecology ISSN 1516-5868 Results patterns, respectively. Individuals of G. barbata, C. micranthum and Sampling involved 821 individuals belong- Notylia sp. represented 67% of those sampled (Table. ing to 14 genera and 16 species (Table 1). On con- 1), whereas individuals of O. maculata, V. palmarum sidering the two habits, epiphytes were found to be and T. cebolleta together represented 22%, and the reevaluate whether There more similar terms of resources, would more similar as to most floristic composition. maining 10bespecies 11%. The abundant species thetomost common. were quadrants, only fiveinterrestrial Correlation analysis with SPSS for Windows was to evaluate the relationships between abundance and1).richness among were also the most frequent (Table species and one facultative. species Average at differentabundance altitudes. among quadrants was Groups of qualitative (Figure 2) and quanti. 41.5, with standard deviation of ± 44.56 individu- tative (Figure 3) similarity were formed in the same als each. Richness varied from 1 to 10 species per quadrants in both dendrograms. Whereas the first RESULTS group was formed by quadrants without the presence quadrant; the most frequent was two species each. Formatado: Sampling involved 821 individuals belonging to 14 genera and 16 species (Table 1). On considering the two habits, epiphytes were found to be the most common. There were only five terrestrial species and one facultative. Average abundance among quadrants was 41.5, with standard deviation of ± 44.56 individuals each. Richness varied from 1 to 10 species per quadrant; the most frequent was two species each. Table 1. List of the species from the family Orchidaceae found in the Serra do Mucambo, Conceição do Coité, Bahia, Brazil. Legend: N. IND = number of individuals sampled, MI= Morisita Index, AF= absolute frequency, Epi. = epiphyte, Ter.= terrestrial, Fa.Epi= facultative epiphyte. Species Campylocentrum micranthum (Lindl.) Rolfe Catasetum luridum Lindl. Cyrtopodium saintlegerianum Rchb.f. Eltroplectris triloba (Lindl.) Pabst Encyclia oncidioides (Lindl.) Schltr. Gomesa barbata (Lindl.) M.W.Chase & N.H.Williams Notylia sp. Oeceoclades maculata (Lindl.) Lindl. Pelexia trachyglossa (Kraenzl.) Pabst. Polystachya concreta (Jacq.) Garay& H. R. Sweet Prescottia sp. Sarcoglottis sp. Trichocentrum cebolleta (Jacq.) M. W. Chase & N. H. Williams Trichocentrum pumilum (Jacq.) M. W. Chase & N. H. Williams . Formatado: N. IND. M.I A.F. % 191 27 5 4 17 272 109 74 13 2 1 14 51 3 22,5 4,2 3,3 3,3 4,9 33,6 27,8 9,3 4,2 2 1 4,5 8,8 0,9 55 35 10 15 20 60 45 55 15 5 5 20 60 15 Vanilla bahiana Hoehne 10 4,9 10 Vanilla palmarum (Salzm ex. Lindl.) Lindl. 60 14 30 Habit Voucher Epi. Epi. Epi. Ter. Epi. Epi. Epi. Ter. Ter. Epi. Ter. Ter. Epi. Epi. Epi. Fa. Epi. HUEFS 166693 HUEFS 166683 HUEFS 166689 HUEFS 166686 HUEFS 166694 HUEFS 166680 HUEFS 166678 HUEFS 166679 HUEFS 166688 HUEFS 166685 Formatado: HUEFS 166692 HUEFS 166690 HUEFS 166682 of C. luridum, in thethan second, this G. species was present No inall allthe thequadrants, quadrants, Nospecies species occurred occurred in andand only four occurred in more half, viz., barbata and T. all,relative together with S. among coronata, the only phorophyte only four occurred in more than half,and viz., barbata(55%).in In cebolleta (60%), and C. micranthum O.G. maculata abundance the total of individuals studied, G. barbata 32.3%, C. micranthum 22.3%, O. maculata 8.8%, T. cebolleta 2.3%, and the remaining 10 was also and T. cebolleta (60%), and C. micranthum and O. to be used by this species. This phorophytespecies 11.7% were noteworthy. maculata (55%). In relative abundance among the total the only one on which V. palmarum and C. saintlegeAlthough the quadrants at higher altitudes presented arianum significantly higher abundance of to individuals (r = 0.547; occurred. According the Sorensen Index, of individuals studied, G. barbata 32.3%, C. micranp < 0.05), no significant correlation between species richness and elevation could be found (r = 0.419; p > 0.05). thum 22.3%, O. maculata 8.8%, T. cebolleta 2.3%, and the most similar quadrants were P6 and P7 (Figure. Most of the species presented aggregated distribution (14 species), and only two, T. pumilum and Prescottia 2), with 100% similarity in floristic composition, folthe remaining 10 species 11.7% were noteworthy. sp., presented random and uniform patterns, respectively. Although the quadrants at higher altitudes lowed by P1 and P20 with more than 90%. As regards Individuals of G. barbata, C. micranthum and Notylia sp. represented 67% of those sampled (Table. 1), presented a significantly higher abundance of indi- qualitative-quantitative similarity, and as indicated whereas individuals of O. maculata, V. palmarum and T. cebolleta together represented 22%, and the remaining 10 viduals (r = 0.547; p < 0.05), no significant correla- by the Morisita-Hom Index, the most similar quadspecies 11%. The most abundant species were also the most frequent (Table 1). tion between species richness and elevation could rants were P3, P6 and P7, with 100% similarity. and orchid abundance (r = 0.223; beGroups found of (r =qualitative 0.419; p (Figure > 0.05).2) and quantitative (Figure 3) similarityResource were formed in the same quadrants in both p> 0.05),theand resource orchid-species richness Most Whereas of the species presented aggregated dendrograms. the first group was formed by quadrants without presence of C.and luridum, in the second, this = - 0.317;topbe > 0.05) were not correlated. distribution species), and only two, T. pumilum species was (14 present in all, together with S. coronata, the only(rphorophyte used by this species. This phorophyte and Prescottia sp., presented random and uniform 71 Revista SEB Ano 14 Final.indd 71 09/10/2012 13:44:01 was also the only one on which V. palmarum and C. saintlegerianum occurred. According to the Sorensen Index, the most similar quadrants were P6 and P7 (Figure. 2), with 100% similarity in floristic composition, followed by P1 and P20 with more than 90%. As regards qualitative-quantitative similarity, and as indicated by the Morisita-Hom Index, the most similar quadrants were P3, P6 and P7, with 100% similarity. Brazilian Journal of Ecology ISSN 1516-5868 was also the oneabundance on which V. C. saintlegerianum occurred. According to the(r Sorensen the Resource andonly orchid (r =palmarum 0.,223; p and > 0.,05), and resource and orchid-species richness = - 0.,317;Index, p > 0.,05) most quadrants were P6 and P7 (Figure. 2), with 100% similarity in floristic composition, followed by P1 and weresimilar not correlated. saintlegerianum, O. maculata, P. concreta, T. cebolleta, Trichocentrum pumilum and V. bahiana were not correlated. have been registered by Batista and Bianchetti (2003) among species occurring in the Brazilian Federal District. T. pumilum is also encountered in areas of the ‘Cerrado’ in São Paulo (16). Campylocentrum micranthum, O. maculata, P concreta and T. pumilum have been registered in the Serra de São José, Minas Gerais State (2) as well as Figure 2. Floristic similarity dendogram, by the UPGMA method and using the Sorensen Index, based on data on the in riverine forests in Rio Grande do Sul State (39). presence or absence Orchidaceae in quadrants in the Serra do Mucambo, Conceição Coité,UPGMA Bahia, Brazil. Figure 2.ofFloristic similarity dendogram, bydothe Species richness observed in the present method and using the Sorensen Index, based on data on study can be considered small when compared to the presence or absence of Orchidaceae in quadrants in the Figure 2. Floristic similarity dendogram, by the UPGMA method and using the Sorensen Index, based on data on the Serra doofMucambo, Conceição Coité, Bahia, presence or absence Orchidaceae in quadrants in the Serra dodo Mucambo, Conceição do Coité,Brazil. Bahia, Brazil. that in plant corridors in the Cerrado, where 100 species were registered (9), and the 226 species registered in the Parque Nacional do Itatiaia, in the Serra da Mantiqueira (5). Nonetheless, many studies presented richness values close to those encountered herein, such as the 25 species found in an area undergoing regeneration in the Montane Figure 3. Floristic similarity dendogram by the UPGMA method and using the Morisita-Index, based on data onDense Ombrophilous Forest (34), or the nine, even Orchidaceae species abundance in quadrants on the Serra do Mucambo, Conceição do Coité, Bahia, Brazil. 10, species found in vegetal isles in parts of the Morro do Pai Inácio Plateau, also in Bahia (1, 20). Figure 3. Floristic similarity dendogram by the UPGMA method and using the Morisita-Index, based on data on Indeed, although Orchidaceae species richness Figure 3. Floristic similarity dendogram by the UPGMA Orchidaceae species abundance in quadrants on the Serra do Mucambo, Conceição do Coité, Bahia, Brazil. is high in humid and montane regions, it is much method and using the Morisita-Index, based on data on Orchidaceae species abundance in quadrants on the Serra lower in dry and seasonal areas. do Mucambo, Conceição do Coité, Bahia, Brazil. Cyrtopodium saintlegerianum was registered as a rare species in dry forests, O. DiscussION maculata as common in both dry and humid forests, T. cebolleta occasional in dry forests, T. pumulum Most of the sampled orchids are widely rare in dry forests, P. concreta occasional in dry distributed geographically, some of them even forests, and V. bahiana occasional in both dry and occurring in other countries, as well as in various humid forests (8). biomes, such as restingas, rocky outcrops, mountain The species O. maculata was very frequent forests, ecotone areas, semideciduous forests and in shady or well-illuminated spots in areas with dense ombrophilous forests. bushy and arboreal vegetation. The high frequency The species C. micranthum, C. luridum, E. indices of this species have been associated to triloba, O. maculata, P. concreta and V. bahiana are efficient reproductive organisms, such as autogamy to be found in the ‘restingas’ of Espírito Santo State and anemochorous dispersion (40). O. maculata and (23). Campylocentrum micranthum also occurs in E. triloba were encountered in sheltered spots inside the same ecosystem in the state of São Paulo (28) closed formations and in open areas (23), thereby as well as in rocky ground in Mucugê, Bahia State corroborating their occurrence in both ‘restinga’ as (3). The species E. oncidioides, V. bahiana and P. well as dry forests, as was the case in the present concreta are incidental in the ecotonal area between study. This indicates the capacity of these species the Atlantic Rain Forest and the ‘Cerrado’ in São to inhabit areas with various grades of luminosity. Paulo (22). Vanilla palmarum occurs in remnants of Species that occur in the lower and upper part of the Atlantic Rain Forest in the south of Bahia (21). trunks possibly prefer or tolerate more humid and Gomesa barbata occurs in semiarid shadier environments (39). regions in Pernambuco State (38). Cyrtopodium Rogalski and Zanin (2002) noted the P20 with more than 90%. As regards qualitative-quantitative similarity, and as indicated by the Morisita-Hom Index, the most similar quadrants were P3, P6 and P7, with 100% similarity. Resource and orchid abundance (r = 0.,223; p > 0.,05), and resource and orchid-species richness (r = - 0.,317; p > 0.,05) Formatado: Inglês (Estados Unidos) Formatado: Inglês (Estados Unidos) Formatado: Inglês (Estados Unidos) Formatado: Inglês (Estados Unidos) 72 Revista SEB Ano 14 Final.indd 72 09/10/2012 13:44:02 Brazilian Journal of Ecology ISSN 1516-5868 existence of two groups, those that required less luminosity and more humidity, and those that tolerate higher luminosity and less humidity. Some species, such as E. oncidioides, were more present in tree canopies than in the lower part of the trunks where vegetation was more closed and large-sized. The species C. luridum, V. palmarum, and C. saintlegerianum always occurred associated with S. coronata, in quadrants with more open vegetation and higher solar radiation. Species requirements limit their distribution. A possible motive for this association could be the substratum conditions that this phorophyte offers, this favoring the growth and maintenance of symbiontic mycorrhizic fungi, and self maintenance as a microecosystem with the adequate luminosity and humidity for the development of these species. It was confirmed that, as cover becomes more open, other species begin to appear, especially those which are more tolerant to luminosity (23). Gonçalves & Waechter (2002) attributed high diaspore production and resistance against isolation to the outstanding capacity for colonizing and high abundance of vascular epiphytes. Lower species richness could be related to environments with microclimatic instability (higher solar radiation and wind exposure), and to the lower exposal of phorophytes to epiphyte diaspores (13). In other words, where there are more aged phorophytes, species richness is generally higher in the regions closer to the climax. Higher abundance, density and diversity is expected in canopy epiphytic orchids in mature forest fragments (35). Cavatti (2007) related distribution of the terrestrial species Epidendrum sp. to the abundance of litter in the soil. This factor could also be related to the distribution of other terrestrial orchid species. In the ‘Caatinga’, the production of litter is not high, as it is in other ecosystems. Even so, in the present study, some areas notably accumulated a large amount of substratum in the soil, appropriate for the establishment of terrestrial species, such as E. triloba, P. trachyglossa, Prescottia sp., Sarcoglottis sp. and O. maculata . Although no relationship between elevation and species richness was found, there was a positive relationship between elevation and abundance. Jacquemyn (2005) encountered higher diversity between 400 and 800 meters, presumably due to the presence of an altitudinal distribution zone with many overlapping species. The high diversity between 500 and 2,000 meters is supposedly a result of high habitat diversity (41). In the present study, no relationship was found between habitat availability (resources) and species richness abundance. High richness and diversity can be characterized as effected by climate (25). Temperature can be a limiting factor, whereas climate changes can contribute to changes in distribution and abundance in orchid populations (17). Thus, less richness and abundance in quadrants where temperature and humidity have been modified by human action, can be expected, as is the case of those near the edges in lower areas, where there is less humidity, and variations in the temperature, besides being greater during the day, are seasonal. This interference of the edge-effect was aggregated to the grid of elevation-liable humidity. Possibly, these two factors are directly linked with less abundance at lower placed areas undergoing the edge effect. As observed by Pereira and Ribeiro (2004), members of Orchidaceae maintained aggregate distribution in three areas in the process of regeneration, as also occurred with young and old individuals of the species Mesadenella cuspidata (Lindl.) Garay (14). Thus, the present study confirms a tendency which has already been observed in orchids. The aggregation of these populations could be due to the incidence of light, or characteristics of the substratum, such as trunk texture and specificity in arboreal species (35). Some phorophytes harbored numerous epiphytes in a few quadrants, whereas others harbored very few. Among the factors that exert an influence on orchid spatial distribution, two are of extreme importance, viz., seed dispersion and an adequate substratum for germination and growth. Seed dispersion is a critical process in plant life, since these need to arrive at adequate substrata (31) in forest areas, protected from wind dispersal, and where young seedlings are always capable of germinating and growing close to the mother plant, thereby forming groups. This is especially the case of terrestrial orchids that form large groups on the soil. Furthermore, infection and colonization of the 73 Revista SEB Ano 14 Final.indd 73 09/10/2012 13:44:02 Brazilian Journal of Ecology ISSN 1516-5868 habitat by compatible micorrhizic fungi is obligatory for supplying the necessary carbohydrates for seedling germination, initial growth, and nutrition on the substratum (11). Thus, only seeds which have fallen onto the adequate substratum are viable. Even though Orchidaceae populations, on the whole, give evidence of being sensitive to human environmental interference, it cannot be said that this is the only factor influencing the distribution of individuals. Environmental alterations in the Serra do Mucambo still need to be studied, through the monitoring of other local populations and communities. Resumo O presente estudo objetivou inventariar a família Orchidaceae na Serra do Mucambo, Conceição do Coité, Bahia e descrever a distribuição das populações na área, discutindo os fatores que influencia na distribuição das espécies. Foram encontradas 16 espécies e 14 gêneros. Os gêneros com maior número de espécies foram Trichocentrum e Vanilla, com duas espécies cada. As espécies distribuíram-se de forma agregada. As maiores abundâncias e riqueza específica foram encontradas nas maiores elevações. A disponibilidade de recursos pode ser o fator que influencia na distribuição destas espécies. Palavras-chave: recursos, elevação, abundância ReferENCES 1- ALMEIDA, A.;FELIX,W. J. P.; ANDRADE, L. A.; FELIX, L. P. A família Orchidaceae em inselbergs da Paraíba, Nordeste do Brasil. Revista Brasileira de Biociências, Porto Alegre, v. 5, n. 2, p. 753-755, 2007. 2- ALVES, R. J. V.; KOLBEK, J. Summit vascular flora of Serra de São José, Minas Gerais, Brasil. Check List, v. 5, n. 1, p. 35-73, 2009. 3- AZEVEDO, C. O.;VAN DEN BERG, C. Análise comparativa de áreas de campo rupestre da Cadeia do Espinhaço (Bahia e Minas Gerais, Brasil) baseadas em espécies de Orchidaceae. Sitientibus série ciências biológicas,Feira de Santana, v.7, n. 3, p. 199-210, 2007. 4- BASTOS, C. J. P.; YANO, O.;VILAS BOAS- BASTOS, S. B. Briófitas de campos rupestres da Chapada Diamantina, Estado da Bahia, Brasil. Revista brasileira de Botânica, São Paulo, v.23, n.4, p. 359-370, 2000. 5- BARBAREMA, F. F. V. A. Orchidaceae no Parque Nacional do Itatiaia, sudeste do Brasil: listagem e estudos taxonômicos na tribo Laeliinae. 2010. 149 f. (Tese de mestrado em botânica) - Instituto de Pesquisas Jardim Botânico do Rio de Janeiro Escola Nacional de Botânica Tropical Programa de Pós-graduação Stricto Sensu, Rio de Janeiro, 2010. 6- BARROS, F.; VILHOS, F.; RODRIGUES, V. T.; BARBAREMA, F. F. V. A.; FRAGA, C. N. Orchidaceae in Lista de Espécies da Flora do Brasil. Jardim Botânico do Rio de Janeiro. 2010. - BATAGHIN, F. A.; BARROS, F. PIRES, J. S. R.. Distribuição da comunidade de epífitas vasculares em sítios com diferentes graus de perturbação na Floresta Nacional do Ipanema, São Paula, Brasil. Revista brasileira de Botânica, São Paulo, v. 33, n. 3, p. 501-512, 2010 8- BATISTA, J. A. N.; BIANCHETTI, A. B. Lista atualizada das Orchidaceae do Distrito Federal. Acta Botânica Brasilica, Feira de Santana, n. 17, v. 2, p. 183-201, 2003. 9- BATISTA, J. A. N.; BIANCHETTI, L. B.; PELLIZZARO, K. F. Orchidaceae na Reserva Ecológica do Guará, DF, Brasil. Acta Botânica Brasilica,Feira de Santana, v. 19, n. 2, p. 221232, 2005. 10-BISPO, P. C.; VALERIANO, M. M.; KUPLICH, T. M. Relação entre as variáveis morfométricas extraídas de dados SRTM (Shuttle Radar Topography Mission) e a vegetação do Parque Nacional de Brasília. Acta Botânica Brasílica, Feira de Santana,v. 204 n. 1, p. 96-103, 2010. 11-BOLDRINI, R. F.; SANTOS, W. O.; CRUZ Z. M. A.; RAMOS, A. C. Bases de associação micorrízica orquidóide. Natureza on Line, Santa Tereza, v. 8, n. 3, p. 140-145, 2010. 12-BORBA, E. L.; FUNCH, R. R.; RIBEIRO, P. L.; SMIDT, E, C.; SILVA-PEREIRA, V. Demografia variedade morfológica e genética e conservação de Cattleya tenuis (Orchidaceae), espécie ameaçada de extinção na Chapada Diamantina, Sitientibus série ciências Biológicas,Feira de Santana, v. 7, n. 3, p. 211-222, 2007. 74 Revista SEB Ano 14 Final.indd 74 09/10/2012 13:44:02 Brazilian Journal of Ecology ISSN 1516-5868 13-BORGO, M.; SILVA, S. M. Epífitos vasculares em fragmentos de Floresta Ombrófila Mista, Curitiba, Paraná, Brasil. Revista brasileira de Botânica, São Paulo, v. 26, n. 3, p. 391-401, 2003. 14-BUDKE, J. C.et al. Distribuição espacial de Mesadenella cuspidata (Lindl.) Garay (Orchidaceae) em uma floresta ribeirinha em Santa Maria, RS, Brasil, Acta Botanica Brasilica,Feira de Santana, v. 18, n. 1, p. 31- 35. 2004. 15-CARDOSO, D. B. O. S.; FRANÇA, F.; NOVAIS, J. S.; FERREIRA, M. H. S.; SANTOS, R. M.; CARNEIRO, V. M. S.; GONÇALVES J. M. Composição florística e análise fitogeográfica de uma floresta semiadecídua na Bahia, Brasil, Rodriguesia, Rio de Janeiro, v. 60, n. 4, p. 10551076, 2009. 16-CARDOSO, J. C.; ISRAEL, M. Levantamento de espécies de Orchidaceae em Águas de Sta. Bárbara (SP) e seu cultivo. Horticultura brasileira, Brasília, v. 23, n.2, p. 169-173, 2005. 17-CAREY, P. D. Changes in the distribution and abundance of Himantoglossum hircinum (L.) Sprengel (Orchidaceae) over the last 100 years. Watsonia,New York, v. 22, p. 353-364, 1999. 18-CAVATTI, F. S.; BOINA C. D.; GONÇALVES, J. O. VOLTOLINI, J. C.; MOTTA, L. B.; CARDOSO, M. F. D.; FONSECA, R. M. Distribuição de Epidedrum sp. (Orchidaceae) em formações de ilhas de restinga do Parque Estadual Paulo César Vinha, Guarapiri, Es. Anais do VIII Congresso ecologia do Brasil, Caxambu, 2007. 19-CERQUEIRA, C.; FUNCH, L. S.; BORBA, E. L. Fenologia de Syngonanthus mucugensis Giulsubsp. mucugensis e S. curralensis Moldenke (Euricaulaceae), nos municípios de Mucugê e Morro do Chapéu, Chapada Diamantina, BA, Brasil.Acta Botânica Brasilica, Feira de Santana, v. 22, n. 4, p. 962-969, 2008. 20-CONCEIÇÃO, A. A.; GIULIETTI, A. M.; MEIRELES, S. T. Ilhas de vegetação em afloramentos quatzito-arenito no Morro do Pai Inácio, Chapada Diamantina, Bahia, Brasil. Acta Botanica Brasilica, Feira de Santana, v. 21, n. 2, p. 255-347. 2007. 21-COSTA, L. C. B.; ROCHA, E. A.; SILVA, L. A. M.; JARDIM, J. G.; SILVA, D. C.; GAIAO, L. O.; MOREIRA, R. C. T.. Levantamento preliminar de espécies vegetais com potencial econômi- co no Parque Municipal de Boa Esperança, Ilhéus, Bahia, Brasil. Acta Farm. Bonaerense, v. 25, n. 2, p. 184-191, 2006. 22-FERREIRA, A. W. C. ; LIMA, M. I. S. ; PANSARIN, E. R. Orchidaceae da região central de São Paulo, Brasil. Robriguésia, Rio de Janeiro, v. 61, n. 2, p. 243-259. 2010. 23-FRAGA, C. N.; PEIXOTO, A. L. Florística e ecologia das Orchidaceae do Espírito Santo. Rodriguésia, Rio de Janeiro, v. 55. n. 84, p. 5-20, 2004. 24-GOMES, A. P. S.; RODAL, M. J. N.; MELO, A. L. Florística e fitogeografia da vegetação arbustiva subcaducifólia da Chapada de São José, Buíque, PE, Brasil. Acta Botanica Brasilica,Feira de Santana, v. 20, n. 1, p. 37-48, 2006. 25-GONÇALVES, C. N.; WAECHTER, J. L. Epífitos vasculares sobre espécimes de Ficus orgamensis isolados no norte da planície costeira do Rio Grande do Sul: padrões de abundância e distribuição. Acta Botanica Brasílica, Feira de Santana,v. 16, n. 4, p. 429-441, 2002. 26-JAQUEMYN, H.; MICHENEAU, C.; PAILLER, T.. Elevational gradients of species diversity, breeding system and floral traits of orchid species on Reunion Island. Jounal of Biogeography, v. 32, p. 1751-1761, 2005. 27-KREBS, C. J. Ecological Methodology. Harper Collins, New York. 1989, 620p.    28-MANIA, L. F.; MONTEIRO, R. Florística e ecologia de epífitas vasculares em um fragmento de floresta de restinga, Ubatuba, SP, Brasil. Rodriguesia, Rio de Janeiro, v. 61, n. 4, p. 705-713, 2010 29-MARACAJA, P. B.; BASTISTA, C. H. F.; SOUSA A. H.; VASCONCELOS, W. E. Levantamento florístico e fitossociológico do estrato arbustivo-arbóreo de dois ambientes na Vila Santa Catarina, Serra do Mel, RN. Revista de Biologia e Ciências da Terra, v. 3, n. 2, 2003. 30-MORAES, C. P.; DOMINGUES, E.; PREZZI, L. E.; SOUZA LEAL, T.; ZAMBOM, R. I.; BRESCANSIN, R. L.; RAMOS, P. A. B. Florsitica e fitossociologia da família Orchidaceae no Centro de Educação Ambiental “Francisco Mendes, município de Mogi Guaçu, SP, Brasil. Scientia plena, v. 6, n. 1, p. 1-5, 2010. 31-MURREN, C. J.; ELLISON, A. M. Seed dispersal characteristics of Brassavola nodosa (Orchi- 75 Revista SEB Ano 14 Final.indd 75 09/10/2012 13:44:02 Brazilian Journal of Ecology ISSN 1516-5868 daceae). American Journal of Botany, v. 85, n. 5, p. 675-680, 1998. 32-NEVES, S. P. S.; CONCEIÇAO, A. A. Campo rupestre recém-queimado na Chapada Diamantina, Bahia, Brasil: plantas de rebrota e sementes, com espécies endêmicas na rocha. Acta Botanica Brasilica, Feira de Santana,v. 24, n. 3, p. 697-707, 2010. 33-PABST, G. F. J.; DUNGS, F. Orchidaceae brasiliensis. Hildesheim Brucke V1 & V2. 1975-1977, 1.408 p. 34-PANSARIN, E. R.; PANSARIN, L. M. A família Orchidaceae na Serra do Japi, São Paulo, Brasil. Rodriguésia, Rio de Janeiro, v. 59, n. 1, p. 99-111, 2008. 35-PEREIRA, U. Z.; RIBEIRO, L. Caracterização da comunidade de Orchidaceae em fragmentos em Floresta Ombrófila Densa Montana em diferentes estágios de regeneração em Santa Tereza, Espírito Santo, Brasil. Natureza on Line, Santa Tereza, v. 2, n. 2, p. 52-60, 2006. 36-QUEIROZ, L. P.; SENA, T. S. N.; COSTA, M. J. S. L. Flora vascular da Serra da Jibóia, Santa Terezinha, Bahia: campo rupestre. Sientitibus série ciências biologicas, Feira de Santana, n. 15, p. 27- 40, 1996. 37-RIBEIRO, P. L.; BORBA, E. L.; TOSCANO- DE-BRITO, A. L. V. O gênero Bulbophylum Thouars (ORCHIDACEAE) na Chapada Diamantina, Bahia, Brasil. Revista Brasileira de Botânica, São Paulo, v. 28, n. 3, p. 423-439, 2005. 38-RODAL, M. J. N.; NASCIMENTO L. M. N. Levantamento florístico da floresta serrana da reserva biológica de Serra Negra, Macrorregião de Itapiraca, Pernambuco, Brasil. Acta Botanica Brasilica, Feira de Santana, v. 16, n. 4, p. 481500, 2002. 39-ROGALSKI, J. M.; ZANIN, E. M. Composição florística de epífitos vasculares no estreito de Augusto César, Floresta Estacional Decidual do Rio Urugiai, RS, Brasil. Revista Brasileira de Botânica, São Paulo, v. 26, n. 4, p. 551-556, 2003. 40-WATANABE, M. T. C.; ROQUE, N.; RAPINI, A. Apocynaceae sensu strictum no Parque Municipal de Mucugê, Bahia, Brasil, incluindo a publicação válida de dois nomes de Mandevilla Lindl. Iheringa, Porto Alegre, v, 64, n. 1, p. 6375, 2009. 41-WOLF, J. H. D.; FLAMENCO, A. Patterns in species richness and distribution of vascular epiphytes in Chiapas, Mexico.Journal of Biogeography, v. 30, p. 1689-1707, 2003. 76 Revista SEB Ano 14 Final.indd 76 09/10/2012 13:44:02 Brazilian Journal of Ecology ISSN 1516-5868 Fluctuating Asymmetry in three Basileuterus (Passeriformes, Parulidae) species in a semideciduous forest fragment in the Brazilian Cerrado Vanessa Fonseca Gonçalves - Universidade Federal de Uberlândia, Instituto de Biologia, Programa de Pós-graduação em Ecologia e Conservação de Recursos Naturais (email: vanessinha_fg@hotmail.com) Celine de Melo - Universidade Federal de Uberlândia, Instituto de Biologia (email: celine@inbio.ufu.br) ABSTRACT Habitat fragmentation in small remnants may compromise aptitude in some bird species. Fluctuating Asymmetry (FA) is the morphological alteration of bilateral characters caused by genetic or environmental stress, this can be used in environmental biomonitoring studies and programs. The objectives were to define FA levels of tarsus and wing in three species of genus Basileuteurus (B. hypoleucus, B. flaveolus and B. leucophrys), and to verify the hypothesis of FA being more pronounced in birds that inhabit fragment edges than those inside. The highest FA values in wing were found in B. flaveolus and B. hypoleucus, and for tarsus in B. hypoleucus. Basileuterus leucophrys was the least assymetric for both characters. FA values were different, both among the three Basileuterus species and between environments, thereby indicating that the characteristics of the environment in which the species concentrates its activities appear to be the most important factor in determining character stability. Key words: morphometry; avifauna; forest fragment INTRODUCTION Habitat fragmentation is a process in which a large and continuous patch of vegetation is split into two or more isolated fragments that function as islands surrounded by nonforested habitats (24). Various techniques have been used for monitoring the effects of habitat fragmentation on biota. One of these is Fluctuating asymmetry (FA) analysis. This deals with random differences between the two sides of characters with bilateral symmetry (23, 8). FA has proved to be one of the most used indices when describing phenotypic variations caused, not only by disturbances of an environmental nature, such as susceptibility to habitat degradation, parasites, or disease, but also genetic factors, as a result of genic disharmony caused by endogamy, heterozygosity or recombination (15, 8, 11). Bird fluctuating symmetry has been proposed as a tool in the studies of the conservation of natural and forest fragment populations. In Passeriformes of Atlantic Rain Forest, the highest FA levels occurred in the more fragmented areas when compared to the continuous, thereby demonstrating that wing FA levels are higher in smaller areas (2). In Passeriformes in Minas Gerais State, symmetric fluctuation in coracoids, ulnae, tarsi and femurs was a clear indication that intense regional deforestation affected populations (1). FA is a practical and trustworthy conservation index, due to the facility in obtaining data and superiority in relation to other indices (2). On considering the susceptibility of asymmetry levels to individual localization, higher in populations whose activities are more concentrated on the edges (20), the differentiated use of the environment by species furnishes data for studies of environmental quality. 77 Revista SEB Ano 14 Final.indd 77 09/10/2012 13:44:02 Brazilian Journal of Ecology ISSN 1516-5868 In the Cerrado, three species of the genus Basileuterus (B. hypoleucus, B. flaveolus and B. leucophrys) are potentially apt for testing this model. They are sympatric and essentially forest species, with spatial niche partitioning as a result of competition exclusion (12). Birds of the genus Basileuterus (Passeriformes, Parulidae) are insectivores, with differentiated usage of the environment (19). OBJECTIVES To determine fluctuating asymmetry levels in three species of Basileuterus, viz., Basileuterus hypoleucus, Basileuterus flaveolus, and Basileuterus leucophrys), and to verify the hypothesis of FA being more accentuated in individuals inhabiting regions closer to the fragment forest edge than those inside. METHODOLOGY Study site: Captures occurred from November, 2007 to June, 2008, and from August, 2008 to October, 2008 in fragment of semideciduous forest fragment (37 hectares) in the Glória Experimental Farm, Uberlândia, Minas Gerais (18º57’06.31”S and 48º12’17.12”W). According to Köppen classification, the climate is megathermic, with rainy summers and dry winters (17) Collection: Mist nets (12,0m x 3,0m and 6,0m x 2,5m) were placed at the edge of and inside the dry and flooded interior of a forest fragment. After being ringed (CEMAVE/ICMBio), the captured birds were then weighed with manual dynamometers (30 g and 60 g).The length of each wing and tarsus was sequentially measured twice with a manual calliper kingtools (0,1mm precision) in the following order: left wing, left tarsus, right wing, right tarsus. The animals were released immediately after the measurements. The arithmetic mean of the measurements of each character was determined later. According to Straube and Bianconi (2008), the capture effort was calculated by the simple multiplication of the area of each net by the time of exposure, plus the number of nets. The total effort was the sum of daily samplings. Statistic analysis Fluctuating asymmetry (FA) was evaluated separately for the wing and tarsus of each species, following calculations defined by Palmer and Strobeck (1986) for the wings and tarsi separately: [ | R – L | / (R + L / 2) ], where: R= average of the right-side measurement for each individual, and L=average of the left-side measurement for each individual. According to Palmer & Strobeck (1986), it is necessary to distinguish FA from other types of asymmetry, such as directional asymmetry and antisymmetry. For this, t-tests were used to verify that the difference in the mean measures of the right and the left (D - E) was significantly equal to zero and the Kolmogorov-Smirnov test was used to examine the normality of the (D - E) distribution. When the average of the measure of the right and left sides was equal to zero and normally distributed, the occurrence of directional asymmetry and antisymmetry was discarded, respectively. The dependence of FA on the size of the original measure was tested for each sample using a Pearson correlation between the |FA| and the average of the measure on the right side (13). Kruskal-Wallis was used to verify the interspecific differences in the FA values for wings and tarsi and Mann-Whitney was used to compare the differences between FA values for birds captured in the edge and inside. The species with the most pronounced FA was also that which presented the highest FA value for wing and tarsus. RESULTS Twenty two individuals of the genus Basileuterus were captured, of which five were B. hypoleucus, seven B. flaveolus and ten B. leucophrys, in 80.199,3 hours.m 2. The distribution by wings and tarsi was not normal. According to Babbit et al. (2006), there can be a slight deviation in the distribution of data frequency, without impeding the occurrence of fluctuating asymmetry. Directional asymmetry was discarded, or rather, the data presented averages equal to zero for both the wings (t = 0,462; df = 21; p = 0,150) and tarsi (t = 0,246; df = 21; p = 0,220). FA values for wing did not correlate with the average of the original mea- 78 Revista SEB Ano 14 Final.indd 78 09/10/2012 13:44:02 Brazilian Journal of Ecology ISSN 1516-5868 AF média surements (rs = -0,327; gl = 22; p > 0,05), as neither did tarsus FA values (rs = -0,036; gl = 22; p > 0,05). There were differences between interspecific FA levels for wing (H= 1,728; p= 0,004; N= 22) and tarsus (H= 6,271; p= 0,009; N= 22). The highest FA values for wing were found in B. flaveolus (AF= 0,0142 + 0,0135) and B. hypoleucus (0,0130 + 0,0122), and for tarsi in B. hypoleucus (AF= 0,0573 + 0,0728). Basileuterus leucophrys was the least 0,14asymmetric for both characters (Figure 1). 0,12 AF média 0,14 0,10 0,12 0,08 0,10 0,06 0,08 0,04 0,06 0,02 0,04 0,00 0,02 B. hypoleucus asa tarso B. leucophrys B. flaveolus Espécies 0,00 B. hypoleucus B. leucophrys B. flaveolus Espécies AF média AF média 0,14 0,12 0,10 0,08 0,06 0,04 0,02 0,00 AF média Figure 1: Fluctuating asymmetry (FA) (average± stan0.07 dard error) in the wings and tarsi of Basileuterus hyinterior 0.06 poleucus, B. leucophrys and B. flaveolus, captured in borda AF média 0.07 0.05 semideciduous forest in the Gloria Experimental Farm, 0.06 0.04 Uberlândia, MG. 0.05 0.03 AF média 0,14 0.02 0.04 Of the 22 individuals captured, one B. hypo0.03 0.01 asa leucus and four 0,10 0.02 B. flaveolus were caught in the edges 0 tarso asa tarso 0.01 of fragment, whereas B. leucophrys individuals were 0,08 Carácter 0 from 0,06 the inside. Although there was a significant asa tarso difference between edge and interior, for FA levels 0,04 Carácter for wing 0,02 (U= 35; p= 0,025; N= 22), this was not the B. hypoleucus B. leucophrys B. flaveolus case for 40; p= 0,41; N= 22) (Figure 2). FA 0,00 tarsi (U= Espécies B. hypoleucus B. leucophrys B. flaveolus for wing was higher in species captured on the edge Espécies (AF= 0,0194 + 0,0161), and lower in individuals from the inside (AF= 0,0075 + 0,0063). 0,12 0.07 0.06 0.05 0.04 0.03 0.02 0.01 0 interior AF média 0.07 borda 0.06 0.05 0.04 0.03 0.02 0.01 asa 0 tarso Carácter asa tarso Carácter Figure 2: Fluctuating asymmetry (FA) (AF) (average± standard error) in individuals from three species of Basileuterus captured in Semideciduous Forest in the Gloria Experimental Farm, Uberlândia, MG. DISCUSSION The interspecific difference between fluctuating asymmetry (FA) values for wings and tarsi in the individuals implies that the differentiated use of characters is a factor that exerts an influence on FA levels (2). According to Balmford et al. (1993), the FA of a character depends on its functional importance, whereby the possible appearance of different values between characters and species. Furthermore, FA specificity for a character (13, 14) is asa liable to generate variations among characters in the tarso same individual, and even among characters related to morphological structure development (7). Basileuterus hypoleucus and Basileuterus flaveolus presented the highest wing FA levels, which is probably associated to the expressive allocation of time for flight in these species (4). Tarsi in Basileuterus hypoleucus were more asymmetric. The use, by this bird, of various strata interior (19), and its greater movement inside forest fragborda ments, possibly more frequently expose wings and tarsi to the prevailing environmental conditions, with the consequentially high FA levels (12, 2). Basileuterus flaveolus and B. hypoleucus, asa through being capable of foraging on forest edges tarso where the microenvironment is different from the inside, and levels of light, temperature and wind higher (16), undergo environmental stress which would influence FA values. According to Van Valen (1962) and Lomônaco & Germanos (2001), FA has become the most used index for describing phenotypic variations caused by environmental noise. In their studies, Evans and Marshall (1996) presented a correlation between fitness and asymmeinterior try,borda in which FA increases with environmental and genetic stress. A possible mechanism of the relationship between FA and stress is that organisms require more energy to compensate stress, thereby resulting in less expenditure with reproduction and growth (10), or, in other words, stress reduces the available energy for the development of character precision (21). Thus, higher levels of habitat disturbance could increase population asymmetry levels prior to a decrease in survival becoming apparent (9). 79 Revista SEB Ano 14 Final.indd 79 09/10/2012 13:44:02 Brazilian Journal of Ecology ISSN 1516-5868 Species that presented higher FA levels, such as B. hypoleucus and B. flaveolus, could represent groups which are more sensitive to disturbance in the process of character development (2). The effects of genetic and environmental stress are cumulative. Hence, organisms under genetic stress are useful as biological indicators of environmental stress quantified through FA, and can thus be efficiently employed in biomonitoring programs (5, 15). Basileuterus leucophrys is more exigent as regards the microhabitat, and so, in this study, was only captured inside the forest, and thus presented the lowest wing and tarsus FA values. The interior of a forest fragment is more isolated from edge-effects ((16), thus anthropic disturbance has less influence on the development of character stability (20). Furthermore, FA levels are often higher among individuals undergoing environmental stress and located in ecologically marginal habitats (22). CONCLUSION Fluctuations in asymmetry values varied among the three species of Basileuterus, and between environments (interior and edge), this being more so in B. hypoleucus and B. flaveolus species, which use the edge for foraging, and less so in B. leucophrys species, which were captured only inside the forest fragment. Thus, the characteristics of the environment in which the species concentrates its activities appear to be the predominating factor in determining character stability, whence the usefulness of FA in the relative diagnosis of impacts arising from forest fragmentation. ACKNOWLEDGMENT Thanks are extended to Professors Dr. Oswaldo Marçal Júnior and Dr. Cecília Lomônaco for the corrections and criticisms, and to my collegues Eurípedes Luciano da Silva Júnior, Péricles Rocha da Silva and Giâncarlo Ângelo Ferreira for the help in collecting data. RESUMO A fragmentação do habitat em pequenos remanescentes pode comprometer a aptidão de algumas espécies de aves. A assimetria flutuante (AF) é uma alteração morfológica em caracteres bilaterais causada por estresse genético ou ambiental, que pode ser utilizada em estudos e programas de biomonitoramento ambiental. Os objetivos deste trabalho foram: determinar os níveis de AF de asas e tarsos em três espécies de Basileuterus (B. hypoleucus, B. flaveolus e B. leucophrys) e testar a hipótese da AF ser mais acentuada em aves que habitam regiões mais próximas da borda do fragmento daquelas restritas ao interior de um remanescente florestal. Os maiores valores de AF para asa foram encontrados em B. flaveolus e B. hypoleucus, e para tarso foi em B. hypoleucus. Basileuterus leucophrys foi o menos assimétrico para ambos os caracteres. Os valores de AF foram diferentes entre as três espécies de Basileuterus e entre os ambientes indicando que a característica do ambiente no qual a espécie concentra suas atividades parece ser o fator mais importante na determinação da estabilidade do carácter. Palavras chave: morfometria; avifauna; fragmento florestal REFERENCES 1- ALMEIDA, R. C. V. Assimetria flutuante em esqueletos de aves Passeriformes do Estado de Minas Gerais: aspectos metodológicos e implicações sobre a utilização de coleções osteológicas como objeto de estudos de variação temporal de comunidades. 2003. 59 f Dissertação (Mestrado em Zoologia de Vertebrados) - Pontifícia Universidade Católica de Minas Gerais, Belo Horizonte. 2003. 2- ANCIÃES, M.; MARINI, M. Â. Assimetria flutuante em Passeriformes da Mata Atlântica. In: ALVES, M. A. S., SILVA; J. M. C., VAN SLUYS; M., BERGALLO, H. G.; ROCHA; C. F. D. (Orgs). A ornitologia no Brasil: pesquisa atual e perspectivas. Rio de Janeiro: Editora da Universidade Federal do Rio de Janeiro, 2000. 3- BABBITT, G. A.; KILTIE, R.; BOLKER, B. Are Fluctuating Asymmetry Studies Adequately Sampled? Implications of a New Model for Size Distribution. The American Naturalist, v. 167, 2006. 4-BALMFORD, A.; JONES, I. L.; THOMAS, A. L. R. On avian asymmetry: evidence of natu- 80 Revista SEB Ano 14 Final.indd 80 09/10/2012 13:44:02 Brazilian Journal of Ecology ISSN 1516-5868 ral selection for symmetrical tails and wings in birds. Proceedings of the Royal Society, v. 252, p. 245-251, 1993. 5- CLARKE, G.M. Fluctuating asymmetry: a technique for measuring developmental stress of genetic and environmental origin. Acta Zoologica Fennica 191:31-35. 1992. 6- EVANS, A.S.; MARSHALL, M. Developmental instability in Brassica campestris (Cruciferae): fluctuatin asymmetry of foliar and floral traits. Journal Evolution of Biology 9:717-736. 1996. 7- KLINGENBERG, C. P.; MACINTYRE, G. S. Geometric morphometrics of developmental instabilitity: analyzing patterns of fluctuanting asymmetry with procrustes methods. Evolution, v. 52, p. 1363-1375, 1998. 8- LEARY, R.F.; ALLENDORF, F.W. Fluctuating asymmetry as indicator of e stress: implications for conservation biology. Trends in Ecology & Evolution 4:214-217. 1989 9- LENS, L., DONGEN, S.V.; MATTHYSEN, E. Fluctuating asymmetry as an early warningsystem in the critically endangered Taita Thrush. Conservervation. Biology 16:479-487. 2002. 10-LEUNG, B.; FORBES, M. R.; HOULE, D. Fluctuating asymmetry as a bioindicator of stress: comparing efficacy of analyses involving multiple traits. The American Naturalist, v. 155, n. 1, p. 101-115, 1999. 11-LOMÔNACO, C.; GERMANOS, E. Variações fenotípicas em Musca domestica L. (Diptera: Muscidae) em resposta à competição larval por alimento. Neotropical Entomology, v. 30, n. 2, p. 223-231, junho 2001. 12-MARINI, M. A.; CAVALCANTI, R. B. Habitat and foraging substrate use of three Basileuterus warblers from Central Brazil. Ornitologia Neotropical, v. 4, n. 2, p. 69-76, 1993. 13-Palmer, A. R.; Strobeck, C., Fluctuating asymmetry: measurement, analysis, patterns. Annual Review of Ecology and Systematics, p. 391-421. 1986. 14-PARSONS, P.A. Fluctuating asymmetry: an epigenetic measure of stress. Biological Review, v. 65, p. 131-145, 1990. 15-PARSONS, P.A. Fluctuating asymmetry: a biological monitor of environmental and genomic stress. Heredity 68:361-364. 1992. 16-PRIMACK, R. B.; RODRIGUES, E. Biologia da conservação. Londrina: Editora Planta, 2001. 327 p. 17-ROSA, R.; LIMA, S. C.; ASSUNÇÃO, W. L. Abordagem preliminar das condições climáticas de Uberlândia (MG). Sociedade & Natureza, p. 91-108, 1991. 18-STRAUBE, F. C.; BIANCONI, G. V. Sobre a grandeza e a unidade utilizada para estimular esforço de captura com utilização de redes de neblina. Chiroptera Neotropical, v. 8, p. 150152, 2008. 19-SICK, H. Ornitologia brasileira. Rio de Janeiro: Editora Nova Fronteira, 1997. 912 p. 20-SIIKAMÄKI, P.; LAMMI, A. Fluctuating asymmetry in central and marginal populations of Lychnis viscaria in relation to genetic and environmental factors. Evolution, v. 52, p. 1285 1292, 1998. 21-SOMMER, C. Ecotoxicology and developmental stability as an in situ monitor of adaptation. Ambio, v.25, p. 374-376, 1996. 22-SOULÉ, M.; BAKER, B. Phenetics of natural populations IV: The population asymmetry parameter in the butterfly Coenonympha tullia. Hereditery, v. 23, p. 611-613, 1968. 23-VAN VALEN, L. A study of fluctuating asymmetry. Evolution, v. 16, p. 125-142, 1962. 24-WILCOVE, D.S., McLELLAN, C.H.; DOBSON, A.P. Habitat fragmentation in the temperate zone. Conservantion Biology, p. 237-256. 1986. 25-ZAR, J.H. Biostatistical analysis. New Jersey: Prentice Hall, 1984. 947 p. 81 Revista SEB Ano 14 Final.indd 81 09/10/2012 13:44:03 Brazilian Journal of Ecology ISSN 1516-5868 82 Revista SEB Ano 14 Final.indd 82 09/10/2012 13:44:03 Brazilian Journal of Ecology ISSN 1516-5868 Vascular plant diversity and substratum parameters as indicators of ecologically based degraded-area recuperation Maria Luiza Porto - Universidade Federal do Rio Grande do Sul, Departamento de Ecologia (e-mail: mlporto@ecologia.ufrgs.br). Marisa Azzolini † - Universidade Federal do Rio Grande do Sul, Departamento de Plantas de Lavoura, in memoriam Cíntia Silva Beauvalet - Universidade Federal do Rio Grande do Sul, Departamento de Ecologia, bolsista IC/PIBIC. Telmo Focht - Universidade Federal do Rio Grande do Sul, Bolsista recém-doutor - CNPq - Departamento de Ecologia (email: tefocht@gmail.com) ABSTRACT In order to be characterized as restoration on an ecological basis, the recovery of a degraded area should increase natural biodiversity. The aim was to establish experiments that reveal the processes involved in the advance of spontaneous vegetation in areas degraded by coal mining. Plant species were first planted for primary coverage of a substratum formed by a coal refuse deposit already covered by regional B-horizon soil, the two pioneer species, Cynodon dactylon (L.) Pers. and Indigofera campestris Bong. ex Benth, being those chosen. Spontaneous plant species diversity was monitored by three abundance and cover surveys. The experiment consisted of two plots, one for each species, divided into 9 sub-plots. From April, 2009 to February, 2011, C. dactylon cover dropped from around 40 to 5%, thereby facilitating the establishment of a higher number of local spontaneous plants. In each survey, I. campestris covered around 80% of the soil. Shannon index between the two species differed significantly (f=0.0141, α=0.05). According to substratum fertility analysis, both at the beginning and the end of the experiments, fertility in organic material increased throughout, with a reduction in acidity at the end of the experiment. Although both species retained substratum, I. campestris contributed towards its more pronounced fertilization, whereas C. dactylon facilitated natural succession and diversity. Hence the latter is more adequate for restoration. Key words: recovery on an ecological basis: degraded area recuperation; species diversity; mining areas; coal INTRODUCTION The criteria applied in recuperation processes, besides being variable, will initially depend on the characteristics of the degraded area. Independently, recuperation, at least over long-term, should re-establish ecological interactions, thereby facilitating the increase of local biodiversity. Only after these prerequisites have been fulfilled, will it be possible to affirm that recovery, on an ecological basis, has begun. As also stated by Ser (2004), the recovery of an area on an ecological basis consists of reestablishing the dynamics of ecosystem processes, 83 Revista SEB Ano 14 Final.indd 83 09/10/2012 13:44:03 Brazilian Journal of Ecology ISSN 1516-5868 through actions and procedures based on natural principles, and for ecological restoration in itself, and not simply for detaining certain processes of substratum loss by the use of any form of vegetal cover. The principle of recovery on an ecological basis will make it possible to reach a state of equilibrium, even though only close to that prior to the disturbance. In order to accomplish this, it is very important that, at the very beginning, vegetal cover of the areas to be restored be preferentially adopted from native species (13). Nonetheless, there are occasions in which the environment to be restored is so adverse to local species, that the use of exotic species, or even a mixture of these with domesticated exotic plants, and on the prior condition of their not presenting characteristics of invaders (7), is more appropriate, as a means of modifying the environment, in such a way as to facilitate the posterior establishment of native species (5, 3, 1), thereby giving continuity to the succession process. However, simply promoting vegetal cover, without necessarily taking into account ecological processes, could be considered as only recovering with vegetation or simply recuperation. Connell and Slatyer (1977) presented three mechanisms, viz., facilitation, tolerance and inhibition, for explaining the process of vegetal succession. In the first, facilitation is defined as the modification of an environment by pioneer species, in such a way that this would facilitate the establishment of species characteristic of a more advanced stage in succession. Through tolerance, there is initial modification, but without affecting the recruitment of species of posterior succession stages. Finally, through inhibition, pioneer species modify the environment with such intensity, that this becomes only little or less adequate for any species of subsequent succession stages. Of the three mechanisms, that which would be more detectable is facilitation, especially in the initial stages of a succession. Even though it is not always possible to detect whether any one of the mechanisms is functioning alone in a succession, or even whether this is possible, probably all the three play their respective role throughout the succession process (9). With these mechanisms in mind, over long term, restoration should not only re-establish those ecological interactions which facilitate succession and system efficacy, but also induce local biodiversity (13, 12). In this study, vegetal species diversity is considered, as a possible indicator of the initial phases of the ecological-based recovery process of degraded areas, according to Connell and Slatyer (1977) criteria, as to the first mechanism (facilitation), and Reis et al., (2003) criteria as to biodiversity inducement. Thus, the establishment of new species follows a dynamically sequential and natural process of substitution and entrance of organisms, as outlined by Rogalski et al., (2005), until reaching an equilibrium phase, in accordance to local and regional environmental conditions (climatic and geomorphological). The different types of interaction among living organisms, as, for example, predation, herbivority, pathogeny, mutualism and decomposition, at the different trophic levels, are prerequisites for characterizing an ecological restoration process (11), through inducing natural processes, such as vegetal succession, by the establishment of facilitating pioneer species in the processes of species entrance and substitution in the system (1). The processes unleashed in this first sequential phase will facilitate the entrance of spontaneous species from the native fauna, thus increasing diversity in vegetal species, to be followed by those of the associated fauna (14). Nonetheless, success in a recuperation process carried out on an ecological basis, also depends on the initial conditions of the abiotic component of an ecosystem. An important point which should be considered – and contemplated – is soil retention against possible erosion. During the process of soil degradation, with the accompanying modifications in structure, and chemical and biological composition, organic-matter loss, as the main consequence, tends to retard the natural restoration process. One way of incrementing available organic matter is by transposing soil from neighboring areas, thereby recomposing fertility with mineral and organic nutrients and ionic exchange capacity, as well as part of the biota of this compartment of the ecosystem (13, 19). Furthermore, the seed bank and other propagules present in the transported soil can increase the diversity of colonizing species in the new environment (19). 84 Revista SEB Ano 14 Final.indd 84 09/10/2012 13:44:03 Brazilian Journal of Ecology ISSN 1516-5868 By the aforementioned motives, substratum fertility at two moments (initial and final), as well as the loss of this substratum through surface drainage during the period of observation, were chosen as additional indicators of the process. In the phenomenon studied here, a descriptive approach on a temporal scale was chosen, starting from a completely bare substratum (time zero), although, through dealing with inedited knowledge and an emergent topic for subtropical areas in the south of Brazil, there were limits to a deeper statistical approach. In the present case, deeper statistical analysis would require having accompanied the process over several years, with direct dependence on environmental dynamics. Nonetheless, in spite of the short period of observation (32 months), clear tendencies of the established processes towards recovery on an ecological basis, were observed. OBJECTIVE The aim was to obtain experimental data on the initial processes which lead to the recovery of degraded areas on an ecological basis, having as the substratum, refuse from the processes of washing and beneficiating mineral coal in Treviso county, southern Santa Catarina State. METHODOLOGY The area chosen for field experiments corresponds to the taluses built by Mineradora Metropolitana, Treviso, SC, for the recuperation of areas of mineral coal deposits, whose geographic coordinates are 28º29’02.33”S and 49º27’33.53”W. Refuse from washing and beneficiating deposited coal, and accumulated at the base of each talus, has been covered by B horizon soil from the region. These taluses are encountered in an environment of the Atlantic Forest. They are located on various platforms placed around the heap of refuse, each platform measuring around 2000 m in length (Figure 1). The experiments were begun at the moment zero (control), in bare substratum, and consisted of setting up two plots on the taluses (Figure 2) for recovery experiments. Area for setting Áreaupde theimplantação recovery plots (bare substratum) Figure 1. Delimitation of the refuse deposit and location of the study area on the deposit. Initially, two species, C. dactylon and I. campestris. were implanted, one each, into two plots, each measuring 10 m x 20 m (Figure 2B). Planting took place on May 6th, 2008. Stolons were planted at a distance of 0.40m between rows and 0.20m between each plant (Figure 2A), in substratum without any correction of acidity or the addition of any type of manure. It is important to point out that the substratum used in this area for covering refuse had been taken from local B horizon soil, with low organic matter and nutrient rates, especially of nitrogen (Table 1). The collection of substratum compound samples was by boring till a depth of 20cm. This was done in each of the two plots in the beginning (zero moment – control), on May 6th, 2008, and at the end (32 months) of the experiment. This substratum was analyzed for fertility, according to the method described by Tedesco et al., (1995). Soil pH was defined with a potentiometer in a soil-water suspension, at a proportion of 1:1. The organic matter rate was defined by humid digestion, using potassium dicromate and sulfuric acid. The micronutrients were obtained according to the methods described in Cqfs - Comissão de Química e Fertilidade do Solo (2004). Due to high seedling mortality, in September it became necessary to plant more seedlings in both plots. In order to evaluate the amount of sediments through artificial drainage, 0.5 m x 5 m troughs were installed in both plots (Figure 2A). As a form of comparing the efficiency of each species in substratum coverage and inducing colonization by new species, after the seedlings of both species had reached an adequate growth, sur- 1 85 Revista SEB Ano 14 Final.indd 85 09/10/2012 13:44:03 Brazilian Journal of Ecology ISSN 1516-5868 veys of abundance and cover, according to BraunBlanquet (1979), but modified, were carried out in April and October, 2009 and February, 2011, in 9 sub-plots measuring 0.5m x 0.5m (0.25m²), with systematic selection procedures for localizing planted pioneer species in each plot (Figure 2B). Species diversity was estimated according to the Shannon index (1948) in both planted plots. As a complement, the t test was applied for estimating the significance of results between the two species. Both the significance test and diversity index were obtained with PAST software (10). Area for setting Áreaupde theimplantação recovery plots (bare substratum) Area for setting RESULTS Área upde theimplantação recovery plots (bare The substratum substratum) analyzed corresponded to material used for covering refuse from coal mining (B horizon of local soil). Thus, generally speaking, fertility was very low and acidity high (pH = 4.5). The initial degree of organic matter was almost zero (0,3%). Nonetheless, an increase in organic matter and a drop in acidity were noted following planting and the subsequent advance in revegetation. The same could be observed through the increase in ions that are important for vegetal development and growth, and the decrease in the concentration of some heavy metals and aluminum, whereby the inference that the species planted are capable of contributing to the phytoremediation process, i.e., the absorption of toxic ions by tolerant plants. Table 1. Physical and chemical characteristics of the substratum (B horizon local soil) used for covering carboniferous refuse in the area of implanting recovery plots, obtained in the beginning and at the end of experiments. Rates Dec - 2008 Feb – 2011 Talus/bare Cynodon indigofera Substratum fertility area dactylon campestris Clay (%) 15 13 13 pH 4.5 4.7 4.8 SMP Index 4.7 4.7 4.8 4.5 2.1 1.7 Phosphorus (mg dm-3) 127 142 153 Potassium (mg dm-3) Organic matter (%) 0.3 1.9 2.6 8.3 3.0 2.7 Changeable aluminum (cmolc dm-3) 0.7 2.4 3.6 Changeable calcium (cmolc.dm-3) 0.9 1.9 2.8 Changeable magnesium (cmolc dm-3) 19.4 19.4 17.3 Aluminum + Hydrogen (cmolc.dm-3) 21.4 24.1 24.1 Cation change capacity (CCC) (cmolcdm-3) CCC saturation as bases (%) 9 19 28 CCC saturation as Al (%) 80.9 38.9 28.3 Correlations Ca/Mg 0.8 1.3 1.3 Correlations Ca/K 2.1 7 9 Correlations Mg/K 2.8 5 7 84 45 31 Súlfur (mg dm-3) 2.6 1.8 1.4 Zinc (mg dm-3) 14.0 1.2 0.8 Copper (mg dm-3) 0.3 0.6 0.6 Boron (mg dm-3) 22 25 28 Manganese (mg dm-3) Substratum analysis by the Soil Laboratory of the Faculty of Agronomy/UFRGS – a member of the Oficial Network Soil Analysis Laboratories (ROLAS) – in accordance with Tedesco et al. (1995) and Cqfs Comissão de Química e Fertilidade do Solo (2004). Figure 2. General view of the plots at the time of planting in May, 2008, with surface drainage gutter (A) and the scheme of experimental delimitation in plots and sub-plots (B). Substratum analysis by the Soil Laboratory of the Faculty of Agronomy/UFRGS – a member of the Oficial Network Soil Analysis Laboratories (ROLAS) 1 – in accordance with Tedesco et al., (1995) and Cqfs -Comissão de Química e Fertilidade do Solo (2004). The species I. campestris afforded a quicker and more uniform recoverture of the area, leading to a reduction in drainage in the respective plot, when compared to that with C. dactylon. Nonetheless, as I. campestris is more sensitive to frosts than C. dactylon, from July on, it was noted that drainage 86 2 Revista SEB Ano 14 Final.indd 86 09/10/2012 13:44:03 Rates Rates Dec - 2008 Feb – 2011 Dec - 2008 Feb – 2011 Talus/bare Cynodon indigofera Talus/bare Cynodon indigofera Substratum fertility Substratum fertility area dactylon area dactylon campestris Brazilian Journal of Ecology campestris ISSN 1516-5868 Clay (%) 1515 1313 1313 Clay (%) pHsimilar 4.54.5 the same 4.7 4.84.8 cover pH 4.7 was in both plots (Figure 3). winter. Over period, I. campestris SMP Index 4.74.7 4.74.7 4.84.8 SMP Index -3 The (mg peaks in) -3)sediment production oc- dropped4.5 from decomposi2.12.1but as plant1.7 Phosphorus dmdm 4.5 88 to 69%, 1.7 Phosphorus (mg -3 -3 ) 127 142 153 Potassium (mg dm curred in March tion in this species is quicker dactylon, 127 142 than in C.153 Potassium (mgfor dmthe) plot with C. dactylon, and matter 0.30.3 1.91.9 it was already 2.62.6possible Organic matter (%) I. campestris, even though in Organic April for that(%) with in the collection in October, -3 -3 ) ) 8.38.3 3.03.0 2.72.7 Changeable aluminum (cmol Changeable aluminum (cmol c dm c dm -3and there was no acalcium peak in rainfall to note an increase of 82.4 to compared ) -3) drainage. This 0.70.7 3.63.6 Changeable (cmol 2.412 species, as Changeable calcium (cmol c.dm c.dm -3 -3 ) up 1.91.9 in the plots 2.82.8 Changeable magnesium (cmol probably occurred through digging to April.0.9 In of C. dac) the soil to 0.9February, 2011, Changeable magnesium (cmol c dm c dm -3 -3 ) ) decumbens 19.4 19.4 Aluminum Hydrogen (cmol 19.4 19.4 17.320% of Aluminum + Hydrogen (cmol c.dm c.dm remove plants+ of the species (Urochloa tylon and I. campestris, there was 4717.3 and -3 -3 ) 21.4 24.1 24.1 Cation change capacity (CCC) (cmol dm ) 21.4 24.1 24.1 Cation change capacity (CCC) (cmol cdm c Stapf, synonym Brachiaria decumbens - Poaceae), uncovered richness was 1828and CCC saturation as as bases (%) 9 9soil, species19 CCC saturation bases (%) 19 28 9, and CCC saturation as Al (%) 80.9 38.9 28.3 CCC saturation as Al (%) 80.9 38.9 28.3 an exotic invader that had been used by the mining promoted cover 5 and 70%, respectively. The temCorrelations Ca/Mg 0.80.8 1.31.3 1.31.3 Correlations Ca/Mg company for revegetation in the neighborhood of poral sequence of the process of recovery over the Correlations Ca/K 2.12.1 77 99 Correlations Ca/K theCorrelations study area,Mg/K and whence had invaded the plots. two previous 2.82.8 years can 5be5 seen in Figure 7 74. Correlations Mg/K -3 -3 ) ) 84 4545 between October, 3131 2009 Súlfur (mg dmdm Súlfur (mg On an average, the production of sediAs84can be observed, -3 -3 ) ) 2.62.6 1.81.8 1.41.4 Zinc (mg dmdm Zinc (mg ments during the period analyzed was 43.5 and and February, 2011, cover in the C. dactylon plot -3 -3 ) ) 14.0 1.21.2 0.80.8 Copper (mg dmdm 14.0 Copper (mg -3 -3 in the plots with I. campestris 43.8 kg per hectare dropped from 20 to 5%, which presupposes that this 0.30.3 0.60.6 0.60.6 Boron (mg dmdm) ) Boron (mg -3 -3 ) 22 25 28 Manganese (mg dm ) 22 25 28 Manganese (mg dm and C. dactylon, respectively, thereby demonstrat- species was being dislocated by the rest in the sucSubstratum analysis byby thethe Soil Laboratory of of thethe Faculty of of Agronomy/UFRGS – a– in member thetheOficial Substratum analysis Soil Laboratory Faculty Agronomy/UFRGS a member of Oficial ing that, when growth has been completely estabcession advance, whereas the I. of campestris plot, Network (ROLAS) with et etal.al. (1995) and Network SoilAnalysis Analysis Laboratories (ROLAS)–by –in inaccordance accordance withTedesco Tedesco (1995)70% andCqfs Cqfs- lished, theSoil potential forLaboratories sediment retainment cover practically remained around throughComissão dede Química e Fertilidade dodo Solo (2004). Comissão Química e Fertilidade Solo (2004). both is similar, when growth has been completely out the period. Bare substratum remained around established. Nevertheless, these numbers do not 20%. Shannon diversity indices for C. dactylon and represent total sediment loss during the period, I. campestris plots were in April, 2009 1.263 and since some rainfall-events were discarded from 1.192, in October, 2009 0.791 and 1.260, and in Febanalysis, due to gutter overflowing, thus annulling ruary, 2011 1.594 and 1.227, respectively (Table 2). correct volume readings on these occasions. These results point to the greater contribution by C. Figure 3. Data on the production of sediments in the plots for implanted recovery in the area of the coal deposit. rf = rainfall. In April, 2009, there was 40 and 25% of uncovered soil, and species richness was 31 and 8 in the plots of C. dactylon and I. campestris, respectively (Table 2), whereas in October, 2009, uncovered soil was 44 and 25%, and species richness 19 and 12 (Table 2). In April, I. campestris soil coverture was around 25%, and C. dactylon around 40%. From April to October, 2009, although mantle cover rose from 5 to 35% in the area with C.dactylon, there was a drop of 31 to 19 species, and in cover from 40 to 20%, through the aerial part of many species dying during the dactylon in furthering vegetal diversity throughout the period evaluated. Table 2. Number of spontaneous vegetal species (Richness) in each of the recovery systems, and the respective Shannon Diversity indices (H’). 22 Period of data collection Recovery plots C. dactylon I. campestris 2009, April Shannon Species Diversity richness H’ 31 1.263 8 1.192 2009, October Shannon Species Diversity richness H’ 19 0.791 12 1.260 2011, February Shannon Species Diversity richness H’ 18 1.594 9 1.227 87 Revista SEB Ano 14 Final.indd 87 09/10/2012 13:44:03 Shannon Diversity H’ C. dactylon 31 1.263 I. Brazilian campestris 8 Journal of Ecology ISSN 1.192 1516-5868 Recovery plots Species richness Species richness 19 12 Shannon Diversity H’ 0.791 1.260 Species richness 18 9 Shannon Diversity H’ 1.594 1.227 Figure 4. Advance of the vegetation in the plots where C. dactylon and I. campestris were planted. As to the substratum, on analyzing nutrients, it was noted that, over the period December, 2008 to February, 2011, there was an increase in organic matter of 0.3% to 1.9% in the plot with C. dactylon and to 2.6% in that with I. campestris (Table 1). There was also a tendency for a reduction in acidity, especially in the I. campestris, plot, on comparing with zero moment. As to surface sediment drainage, on an average, the production of sediment from April to October was similar in both species, with 43.5 kg for the C. dactylon plot and 43.8 kg for that with I. campestris. DISCUSSION When considering the recovery of areas on an ecological basis, the species C dactylon was chosen for testing in the role of pioneer for establishing a sequential process, followed by accompaniment of diversity in other species throughout the process, as important elements in the recovery of areas impacted by the exploitation of coal. Efficiency was compared with that of another species of the family Fabaceae, i.e., I. campestris, 3 88 Revista SEB Ano 14 Final.indd 88 09/10/2012 13:44:03 Brazilian Journal of Ecology ISSN 1516-5868 which also possesses the characteristics of pioneer plant and substratum restorer. The empirical and theoretic fundamentals of the initial phase of an ecological model for coal-refuse impacted area recovery have already been defined (1). No matter how drastic the local degradation conditions, the recovery of an area should not be understood as a simplified process, with the sole aim of recovering the area, or simply making it green. When considering the serious physical and chemical limitations of areas impacted by coal mining, as revealed through substratum analyses, their recovery requires ample planning. The choice of appropriate vegetal species should be in accordance with criteria which facilitate the establishment of recovery on an ecological basis. Thus, further attention should be directed towards evaluating the capacity of the different vegetal species to colonize these environments and induce rapid soil coverture. This would consist of the contribution towards a reduction in surface and sub-surface drainage, and the fixing of toxic metallic elements, with an eye to phytoremediation, thence leading to an increase in local fauna and floral diversity (1,13). Thus, the species C. dactylon, was included in the experiments, through presenting the characteristics of tolerance to degraded terrains, as well as facilitating the entrance of new species into the community, even though it is a domesticated exotic species (17), whence its use is debatable (6). The species I. campestris was used as a pioneer, since, through being a Fabaceae, it possesses nitrobacterium nodules. This is an essential characteristic for substratum nitrogen enrichment, thereby, according to the degree of cover, reducing loss. The results obtained for sediment surface drainage indicated their higher retention in the plot planted with I. campestris, which is characterized by lower native and spontaneous species diversity, when compared with the C. dactylon plot, thus placing in evidence that one vegetal species alone would hardly possess all the necessary characteristics for recovery in ecological terms. Hence, for recovery to play a complete role, it is necessary to understand the interactions between the species and the dynamics of succession, with a view to an increase in environmental diversity and local ecological complexity. On the other hand, knowledge of the requirements for maintaining an ecosystem is not enough, but also comprehension of the methods and techniques which accelerate recovery processes in degraded areas, is essential. Among these, knowledge of facilitating species (5, 13, 9), nucleater species (13, 8), or ‘nurse plants’, that enhance recovery processes on an ecological basis, is essential, since these can also play a role in the natural advance of one type of vegetation over another, in a dynamic process of flower succession. These qualities, as observed in the experiment with C. dactylon, presuppose that this plant, even though a domesticated exotic species, is capable of exerting a facilitating role in natural sequential processes, since its substitution by other native species is possible. These characteristics contributed to higher spontaneous vegetal species richness in the plots with C. dactylon, than in those with I. campestris, as can be seen from results. Furthermore, C. dactylon, besides being heavy-metal tolerant and fast-growing in contaminated terrains (1), is capable of detaining substratum loss and partial fertilization, as was observed here. The continuation of this work would make it possible to glean further invaluable information on the contribution of the vegetal species here used, when considering further sequential phases in vegetal coverture in association with bushy and arboreal species. Thus, the dynamics of the recovery process for degraded areas, applied on an ecological basis in a region where the original landscape matrix was Atlantic Forest, would be more comprehensible. CONCLUSION On comparing the outcome in plots of C. dactylon and I. campestris, after 32 months of planting on a bare substratum, it can be concluded that C. dactylon contributed more to an increase in native spontaneous species diversity and was more involved in the natural succession process, through its role in facilitating recovery on an ecological basis. It can also be concluded that, besides substratum chemical indictors revealing a higher contribution for fertilization on the I. campestris plot, there was no significant difference in surface sediment drainage between the two, a clear indication of the same capacity for substratum retainance. 89 Revista SEB Ano 14 Final.indd 89 09/10/2012 13:44:03 Brazilian Journal of Ecology ISSN 1516-5868 RESUMO A recuperação de uma área degradada deve aumentar a biodiversidade natural para caracterizarse como restauração em bases ecológicas. Este estudo visou estabelecer experimentos que revelem os processos de avanço de vegetação espontânea em áreas degradadas pela exploração do carvão mineral. Inicialmente foram plantadas espécies para a cobertura primária deste substrato, formado por rejeitos de carvão, cobertos pelo horizonte B de solos regionais. A diversidade de espécies vegetais espontâneas foi monitorada em três levantamentos de abundância e cobertura, após o plantio das espécies com características de pioneira Cynodon dactylon (L.) Pers. e Indigofera campestris Bong. ex Benth. O experimento consistiu de uma parcela com 9 sub-parcelas para cada espécie. De abril de 2009 a fevereiro de 2011, a cobertura de C. dactylon reduziu-se de cerca de 40% para 5%, facilitando o estabelecimento de um maior número de espécies espontâneas nesta parcela. I. campestris cobriu cerca de 80% do solo em cada levantamento. O índice de Shannon diferiu significativamente entre as parcelas com as duas espécies (f=0,0141, α=0,05) no período avaliado. Análises de fertilidade do substrato foram feitas no inicio e no fim dos experimentos e demonstraram que a fertilidade teve acréscimo de matéria orgânica, e redução de acidez no final do experimento. Conclui-se que ambas as espécies retém substrato, mas I. campestris contribui para uma maior fertilização do substrato e C. dactylon facilita a sucessão natural e a diversidade, sendo esta adequada à restauração. Palavras chave: recuperação em bases ecológicas, recuperação de áreas degradadas, diversidade em espécies áreas de mineração, carvão. REFERENCES 1- AZZOLINI, M. Restauração ecológica de áreas impactadas por cinzas de carvão mineral: contribuição da mamona (Ricinus communis L.) e respostas da espécie a metais pesados. 2008. 181 f. Tese (Doutorado em Botânica) - Instituto de Biociências, Universidade Federal do Rio Grande do Sul, Porto Alegre. 2008. Disponível em: <http://hdl.handle.net/10183/17470>. 2- BRAUN-BLANQUET, J. Fitosociología. Ma- drid: H. Blume, 1979. 820 p. 3- CALLAWAY, R. M.; WALKER, L. R. Competition and facilitation: a synthetic approach to interactions in plant communities. Ecology v. 78, n. 7, p. 1958-1965, 1997. 4- Cqfs - Comissão de Química e Fertilidade do Solo. Manual de Adubação e de Calagem para os Estados do Rio Grande do Sul e de Santa Catarina. Porto Alegre: Sociedade Brasileira de Ciência do Solo/Núcleo Regional Sul, 2004. 394p. 5- CONNELL, J. H.; SLATYER, R. O. Mechanisms of sucession in natural communities and their role in community stability and organization. The American Naturalist v. 111, n. 982, p.1119-1144, 1977. 6- D’ANTONIO, C.; MEYERSON, L. A. Exotic plant species as problems and solutions in ecological restoration: a synthesis. Restoration Ecology v. 10, p. 703-713, 2002. 7- EWEL, J. J.; PUTZ, F. E. A place for alien species in ecosystem restoration. Frontiers of Ecology and Environment v. 2, n. 7, p. 354-360, 2004. 8- FORNECK, E. D. Estrutura e dinâmica da expansão florestal em mosaico natural de floresta-savana no morro Santana, Porto Alegre, RS, Brasil. 2007. 85 f. Tese (Doutorado em Ecologia) - Instituto de Biociências, Universidade Federal do Rio Grande do Sul, Porto Alegre. 2007. Disponível em: <http://hdl.handle.net/10183/29983>. 9- GUREVITCH, J.; SCHEINER, S. M.; FOX, G. A. Ecologia Vegetal. Porto Alegre: Artmed, 2ª ed., 2009. 592 p. 10- HAMMER, Ø.; HARPER, D. A. T.; RYAN, P. D. 2001. PAST - Palaeontological Statistics. Disponível em: <http://www.uv.es/~pardomv/ pe/2001_1/past/pastprog/past.pdf>. Acesso em: 20 de abril de 2011. 11- KARDOL, P.; WARDLE, D. A. How understanding aboveground–belowground linkages can assist restoration ecology. Trends in Ecology and Evolution v. 25, n. 11, p. 670-679, 2010. 12- PALMER, M. A., FALK, D. A., ZEDLER, J. B. Ecological theory and restoration ecology. In: FALK, D. A., PALMER, M. A., ZEDLER, J. B. (Org.). Foundations of Restoration Ecology. Washington: Island Press, 2006. p 1-10. 13- PODGAISKI, L. R.; RODRIGUES, G. G. Leaflitter decomposition of pioneer plants and detri- 90 Revista SEB Ano 14 Final.indd 90 09/10/2012 13:44:03 Brazilian Journal of Ecology ISSN 1516-5868 tivore macrofaunal assemblages on coal ash disposal sites in southern Brazil. European Journal of Soil Biology, v. 46, p. 394-400, 2010. 14- PORTO, M. L.; AZZOLINI, RODRIGUES, G. G.; M.; ZOCCHE, J. J.; FOCHT, T.; FLORES, M. da S.; FRANCISCO, P. B.; MARTINHAGO, K.; COSTA, K. M.; BEAUVALET, C. S. Uso de indicadores biológicos para avaliação do sucesso de restauração ecológica. Disponível em: <http://www.seb-ecologia.org.br/2009/resumos_ixceb/192.pdf>. 15- REIS, A.; BECHARA, F. C., ESPÍNDOLA, M. B. de, VIEIRA, N. K., SOUZA, L. L. de. Restauração de áreas degradadas: a nucleação como base para incrementar os processos sucessionais. Natureza e Conservação v. 1, n. 1, p. 28-36, 2003. 16- ROGALSKI, J. M.; BERKENBROCK, I. S.; REIS, A.; REIS, M. S. Sucessão e diversidade como fundamentos básicos na restauração am- biental. In: SIMPÓSIO NACIONAL E CONGRESSO LATINO-AMERICANO DE RECUPERAÇÃO DE ÁREAS DEGRADADAS, 6., Curitiba. Anais..., Curitiba, 2005. p. 433-439. 17- Ser. 2004. Society for Ecological Restoration. Disponível em <http://www.ser.org/content/ecological_restoration_primer.asp>. Acesso em 30 de setembro de 2011. 18- SHANNON, C. E. A mathematical theory of communication". Bell System Technical Journal v. 27, p. 379-423, 1948. 18- TEDESCO, M. J.; VOLKWEISS, S. J.; BOHNEN, H. Análise de solo, plantas e outros materiais. Porto Alegre: UFRGS, Faculdade de Agronomia, Departamento de Solos. Boletim Técnico, n. 5. 174p, 1995. 19- VÉCRIN, M. P.; MULLER, S. Top-soil translocation as a technique in the re-creation of species-rich meadows. Applied Vegetation Science v. 6, p. 271-278, 2003. 91 Revista SEB Ano 14 Final.indd 91 09/10/2012 13:44:04 Brazilian Journal of Ecology ISSN 1516-5868 92 Revista SEB Ano 14 Final.indd 92 09/10/2012 13:44:04 Brazilian Journal of Ecology ISSN 1516-5868 Floration phenology of a Bromeliaceae community of an EPA in the restinga of Maricá (RJ, Brasil) as compared to other habitats of the southeastern Brazilian Atlantic Rain Forest OF AN ENVIRONMENTAL PROTECTION AREA (EPA) Camila V. Suizani¹ (camilavsu@hotmail.com) Heloísa A. de L. Carvalho¹ (heloisa.alc@gmail.com) Ana Tereza A. Rodarte¹ (atrodarte@gmail.com) Cristine Benevides¹ (crisbenevides@yahoo.com.br) ¹Universidade Federal do Rio de Janeiro/Museu Nacional - Departamento de Botânica, Lab. De Biologia Reprodutiva de Angiospermas. ABSTRACT A study was made of a community of Bromiliaceae in the EPA of a restinga in Maricá, Rio de Janeiro State, Brazil. The collected data revealed the intensity (2010-2011) and activity (2004-2011) of flowering phenology. Tests of the correlation between flowering and environmental factors, such as temperature, rainfall, relative humidity of the air and insolation, were applied, besides comparisons between these periods of the phenophase for the same species in other habitats of the Brazilian southern Atlantic Rain Forest. Aechmea nudicaulis (L.) Griseb., Billbergia amoena (Lodd.) Lindl., Neoregelia cruenta (Graham) L.B. Sm., Tillandsia gardneri Lindl., Tillandsia stricta Sol. ex Sims. and Vriesea neoglutinosa Mez., presented sequential flowering, with the peaks concentrated in the restinga rainy season. The abiotic factors tested revealed no statistically significant correlation with the periods of flowering in the majority of the species, with the exception of T. stricta and B. amoena. In the first, there was a significant positive correlation with medium and minimum temperatures, and the second, with the relative humidity of the air. Through bibliographic surveys, thereby comparing other habitats, three of the six species presented notable variations in the period and duration of flowering. There were also variations in floral visitor guilds, almost exclusively represented by hummingbirds in forested areas, but also including insects (bees and butterflies) in the area of the restinga. It was concluded that abiotic and intrinsic factors, such as phylogenetic constraints, are not the main determinants in the flowering periods of some bromeliads, thereby presupposing that abiotic factors, such as pollination could be more significant. Key words: Bromeliaceae, phenology, sequential flowering, restinga, phylogenetic constraints INTRODUCTION Even though phenological studies of Bromeliaceae have been included in those involving the Atlantic Rain Forest (15, 12, 14), caatinga (19), upland swamps (23), Amazon Forest (17) and rocky ground (21), these are scarce for the restinga (15, 3, 6). Humming birds have been shown to be the main pollen vectors for around 85% of the Bromeliaceae species investigated (24). Many authors have indicated that sequential flowering is common among sympatric bromeliads of the same floral syndrome. This could arise from pollinator competitive activity, as a selective force, thereby giving rise to 93 Revista SEB Ano 14 Final.indd 93 09/10/2012 13:44:04 Brazilian Journal of Ecology ISSN 1516-5868 divergence in species flowering peaks in the same locality throughout the evolutive process (3, 12, 14). It has been said of the family Bromeliaceae, that rainy and dry season periodicity has a strong influence on the flowering pattern (5), with peak predominance in the rainy season, as registered in the Atlantic Rain Forest (12, 14) and the Caatinga (19). However, in upland swampy environments, bromeliad community behavior has proven to be otherwise, with the peak occurring predominantly in the dry season (23). Differences in the beginning and extension of the flowering period of the same species, although in different localities, could indicate that environmental factors are more important for phenology in tropical areas than intrinsic factors, such as phylogenetic constraint and evolutive history (11, 12). OBJECTIVES The aim was to characterize the flowering phenology of a bromeliad community in the EPA (Environmental Protection Area) of a restinga in Maricá, Rio de Janeiro State, Brazil, by investigating the occurrence of species sequential flowering, as well as the correlation between environmental factors, such as rainfall, temperature, relative humidity and insolation, with the flowering periods registered. Furthermore, attention was given to comparing the periods of flowering and floral visitors of these species in different ecosystems of the Brazilian southeastern Atlantic Rain Forest, through the use of the available bibliographic records. The intention was to contribute towards clarifying the question of which factors exert a greater influence on Bromilaceae phenology, intrinsic, i.e., phylogenetic relations or group evolutive history, or environmental, i.e., rainfall, temperature, photoperiod, relative humidity, pollinator availability and competitiveness. METHODOLOGY The study was carried out in an EPA in the restinga of Maricá, Rio de Janeiro State (22°52' to 22°54’S and 42°48' to 42°54’W), along a transect (320m) on an inner sandy cordon, parallel to the beach, and passing through two vegetal forma- tions, an open bushy (shrublike) and closed bushy (22) areas, both not liable to flooding. According to Köeppen (1948) classification, the climate of the region is Aw tropical rainy, with the rains concentrated in the summer, and reduced in the winter. According to data from INMET (National Institute of Metereology), the average temperature during the year of studies ( from May, 2010 to April, 2011) was 23,5°C, with a maximum average of 34,4°C and minimum 16,1°C. The total annual rainfall was 1.251,6 mm, with 65,6% occurring from October, 2010 to April, 2011. Fortnightly one-or-two-day field visits took place between May, 2010 and April, 2011, during one year of observation. Considering each florescence as a single individual, bromeliads in flower and up to 1 meter on each side of the transect were marked. Records of each of the six bromeliad populations studied were of the absence or presence of the flowering phenophase (activity – 4). The intensity of the event was estimated by the number of individuals in flower, taking into consideration the three classes, low, medium and high, in accordance with the minimum and maximum number of individuals in flower (9 with modifications). Floral visitors were observed with the naked eye at various distances from the plant, during 5 to 15 minutes each visit, in sessions between 6 a.m. and 7 p.m. Visitors were identified only at the genus or family level. Monthly rainfall (mm), maximum, minimum and average temperatures (ºC), relative humidity of the air (%), and total monthly insolation (hours) were taken into account, when checking correlations with the intensity of flowering of each species. The two latter parameters refer to historic averages for Maricá between 1986 and 2008 (Station n. 83089). The Spearmen correlation test, considering p<0,01, and with the STATISTICA version 7 program, was applied for testing the correlations of average temperature and rainfall, taking into account 1 and 2 months prior to the event (7). Use was made of data collected during the study, as well as data on flowering phenological activity in bromeliads collected between 2004 and 2010 by Rodarte (2008 – and unpublished data), in the same area and for the same species, for testing flowering period regularity. Bibliographic references 94 Revista SEB Ano 14 Final.indd 94 09/10/2012 13:44:04 Brazilian Journal of Ecology ISSN 1516-5868 ing the years 2005, 2007 and 2010. In accordance with the data on flowering intensity, obtained for the years 2010|2011, although the bromeliads of the Maricá restinga presented sequential flowering peaks (Table 2), these were concentrated from the end of the rainy season during transition to the sub-dry (January to May). During the study period, there was a long period (July to December), in which Bromeliaceae species intensity and activity were low, with no register of flowering in October and November, 2010 (Table 2; Figure 1). The intensity of flowering (Figure 1) presented no significant correlation with the factors total rainfall, average, minimum and maximum temperature, relative humidity of the air, and total insolation for most of the species, except for T. stricta, whose peak of flowering was positively and significantly correlated with the average (Spearman coefficient = 0,76, for p=0,0039) and minimum (Spearman coefficient = 0,74, for p=0,0054) temperatures, and B. amoena with the relative humidity of the air (Spearman coefficient = 0,83, for p=0,0008). containing data on the species in question (15, 12, 14) were also consulted, in order to compare flowering periods and bromeliad floral visitors in the restinga with other habitats in the Atlantic Rain Forest in the Brazilian southeast. After analyzing the areas of the reference studies, the following habitats of the Atlantic Rain Forest were considered: 1) granitic outcrops at sea level, known as rocky shores (15); 2) upland plains at over 1.400 m, this including two habitats proposed by Marques and Lemos Filho (2008), viz., altitudinal mesic and stoney xeric; 3) forest mesic between 1.200 and 1.300 m; and 4) mixed ombrophilous forest, an ecotonal zone between Araucaria forest and the forest environment itself (12). RESULTS The bromeliad community studied included all the species found in the transect, viz., Aechmea nudicaulis (n= 260), Billbergia amoena (n= 20) and Neoregelia cruenta (n= 61), of the subfamily Bromelioideae, and Tillandsia gardneri, T. Table 1. Records of the flowering phenophase in six bromeliad species of the EPA in the restinga of Maricá, RJ, during the period January, 2004 to April, 2011. Espécies 2004 2005 2006 2007 2008 2009 2010 2011 J F MA MJ J A S O N D J F MA MJ J A S O N D J F MA MJ J A S O N D J F MA MJ J A S O N D J F MA MJ J A S O N D J F MA MJ J A S O N D J F MA MJ J A S O N D J F MA A. nudicaulis Espécies • • • • • 2004 • •• B. amoena • J• F• M A M J J A S • • N. cruentaA. nudicaulis• • • •• •• • • B. amoena • •• T. gardneri • • • N. cruenta • • • •• T. stricta T. gardneri• • • • • • V. neoglutinosa T. stricta • • • • •• •• •• • • • • • V. neoglutinosa 2007 • • • • • • • 2005 • • • • • • • • •2006 • • • •• • • • • • • •• • • • • • • • • •• • •• • • • • •• •• •• • • • • • • • • •• •• • • • • • • • • • • • • • •• • •• • • • • • • • • • • •• • • • • •• • • • • • • • • • • • ••• •• • • • • • • • •• •• •• •• • • • • • • •• •• •• • • • • • •• •• •• • 2008 • • •• • • • • • •• •• •• • • • • • • • • • •• • • •• • •• • • • • • • • •2009 • • • • • • • • • • 2010 • • • • • • • 2011 •• • •• • • • • •• •• • ••• •• •• • • • • • • • • • • • •• •• • • • • • • •• • • • • • • • • •• • • • • • • • •• •• • • • • • •• • • • • • • •• • O N D J F MA MJ J A S O N D J F MA MJ J A S O N D J F MA MJ J A S O N D J F MA MJ J A S O N D J F MA MJ J A S O N D J F MA MJ J A S O N D J F MA • •• • ••• •• •• • • • • • • • • •• • • • • • • •• • • • •• • • • •• • • • •• • • • •• • • • • • • • • • • • • • •• • • • •• • • • • • •• • • •• • • • •• • • • • • • • •• • •• • • • •• • • Table Flowering intensity five bromeliad species EPAofinMaricá, the restinga Maricá, (May, 2010 Table 2.2.Flowering intensity in five in bromeliad species of the EPA inof thethe restinga RJ (May,of 2010 to April,RJ 2011) Intensities Table 2. Flowering intensity in five bromeliad species of the EPA in the restinga of Maricá, RJ (May, 2010 to April, 2011) Intensities to April, 2011) Intensities - High Low Medium High - Low Medium - Low Medium High MM JJ JJ A SS OO N N D D J J F FM M A A Vriesea neoglutinosa Vriesea neoglutinosa Tillandsia stricta Tillandsia stricta Aechmea nudicaulis Aechmea nudicaulis Billbergia amoena Billbergia amoena Neoregelia Neoregelia Estação subseca Estação chuvosa Estação subseca Sub-dry season Afloramentos Sub-dry season Estação chuvosa Rainy season Restinga Campos de (todas as estações) (estação quente e chuvosa) Mésico Floresta Rainy season species studied, there stricta. (n= 54) and Vriesea neoglutinosa (n= 25), florestal OmbrófilaInmistathree of the six Referências altitude graníticos Afloramentos Floresta Restinga Campos de Mésico (nível do mar) (nível doSince mar) (altitute > 1.400m) (altitude 1.200m) 900m) was (altitude appreciable variation in the period and duraof the Aechmea subfamily Tillandsioideae. 2004, speReferências nudicaulis jan - dez nov - fev nov - dez mista altitude graníticos florestal Ombrófila tion of flowering, which very often took place in cies annual flowering periods relatively (nível do mar) (nívelhave do mar) been (altitute > 1.400m) (altitude 1.200m) (altitude 900m) ACHADO & SEM IR (2006), M ARQUES & LEM OS FILHO (2007) Billbergia amoena abr - jun mar - mai abrnov - mai- dez Aechmea nudicaulis jan - dez nov - fev different seasons, Mwhen compared to occurrence in regular, varying(todas from short to long (Table 1). The as estações) (estação quente e chuvosa) (estação quente e chuvosa) habitats in the Atlantic Rain Forest (Table 3). exception was T. gardneri, which presented a su- mar -other fev - mai M ACHADO & SEM IR (2006), M ARQUES & LEM OS FILHO (2007) Billbergia Neoregelia amoena cruenta abr - jun mai abr - mai (estação fria e seca) (estação fria e seca) The rainy (October to March) and dry (April to Seppra-annual pattern, through failing to flower dur- (transição) M ACHADO & SEM IR (2006), M ARQUES & LEM OS FILHO (2007) (estação quente e chuvosa) M ACHADO & SEM IR (2006), M ARQUES & LEM OS FILHO (2007) (estação fria e seca) (transição) (estação fria e seca) * Não foram encontradas referências (transição) Tillandsia gardneri jul - ago Neoregelia cruenta fev - mai fev -(estação mai fria e seca) MARQUES & LEM OS FILHO (2007) * Não foram encontradas referências (transição) (transição) Tillandsia stricta Tillandsia gardneri dez - mar mai - set ago - set (estação jul - agoquente e chuvosa) (estação e seca) fev - fria mai (estação estação fria e seca) (estação fria e seca) Vriesea neoglutinosa Tillandsia stricta Revista SEB Ano 14 Final.indd 95 ago - mar jan - mar (transição e estação (estação quente e chuvosa) dez -quente mar e chuvosa) (estação quente e chuvosa) M ACHADO & SEM IR (2006), M ARQUES & LEM OS FILHO (2007) (transição) 95 MARQUES & LEM OS FILHO (2007) M ARTINELLI (1994) mai - set ago - set (estação fria e seca) (estação estação fria e seca) M ACHADO & SEM IR (2006), M ARQUES & LEM OS FILHO (2007) 09/10/2012 13:44:04 Brazilian Journal of Ecology ISSN 1516-5868 tember) periods are the same in all the areas stud- ing pattern, by appearing as annual in the uplands 2004 Tillandsia 2005 stricta flowers 2006 2008 in the restinga 2009 ied.Espécies In the restinga, be- 2007 and supra-annual (Table 2010 1 and 2).2011 The J F MA MJ J A S O N D J F MA MJ J A S O N D J F MA MJ J A S O N D J F MA MJ J A S O N D J F MA MJ J A S O N D J F MA MJ J A S O N D J F MA MJ J A S O N D J F MA A. nudicaulis • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • •• tween December and March, hot and rainy months, only species that presented coinciding flowering peB. amoena ••• •••• •••• ••• ••• ••• ••• • N. cruenta whereas in up-lands and •mixed ombrophylous forriods in •all Billbergia ••••• •••• ••• ••• • • the • • habitats • • • of • • occurrence• were •• • T. gardneri ••• •• • • ests, and September, colder amoena, April T. strictathis occurs • • • between•May •• •••• ••• • • •between • • • and June in • • the restinga • • •and V. neoglutinosa • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • ••••••••• •••••••• ••••• •• ••••• months and with less rainfall. Aechmea nudicaulis ombrophyilous forest, and Vriesea neoglutinosa, bealso presents in uplands and mixed ombrophylous tween August and March, in the restinga and rocky Table 2. flowering Flowering intensity five bromeliad species of the EPA in the restinga of Maricá, RJ (May, 2010of to April, 2011) Intensities forests periodinfrom November to February, shores (Table 3). No records Neoregelia cruenta when hot and rainyHigh (Table 3). This period is were encountered in comparative studies. - Low it is also Medium relatively short compared toMthe restinga, birds J JwhereAthe S O Although N Dhumming J F (Throchilidae) M A event extends throughout practically the entire year, were observed visiting all the bromeliads that flowVriesea neoglutinosa with the peak in April and May (Table 2; Figure 1), ered throughout this study, visits by butterflies were Tillandsia stricta of transition to the colder and less also recorded (Nymphalidae, Lycaenidae and Pieriwhich are months rainy season. Apart from differences in the flower- dae) in A. nudicaulis and V. neoglutinosa, as well as Aechmea nudicaulis ing period among the habitats compared (Table 3), bees, viz., Euglossa sp.and Xylocopa sp. in A. nudiBillbergia amoena T. gardneri also presented differences in the flower- caulis, and Euglossa sp. and Trigona sp. in N. cruenta. Neoregelia Table 3: Flowering periods of six bromeliad species in various habitats in the Brazilian southeast Atlantic Rain Estação subseca Estação chuvosa Forest Sub-dry season Restinga (nível do mar) jan - dez Aechmea nudicaulis Campos de Mésico Floresta graníticos altitude florestal Ombrófila mista Referências (altitude 900m) nov - dez M ACHADO & SEM IR (2006), M ARQUES & LEM OS FILHO (2007) (nível do mar) (altitute > 1.400m) (altitude 1.200m) nov - fev (todas as estações) Billbergia amoena Rainy season Afloramentos (estação quente e chuvosa) (estação quente e chuvosa) abr - jun mar - mai abr - mai (estação fria e seca) (transição) (estação fria e seca) Neoregelia cruenta M ACHADO & SEM IR (2006), M ARQUES & LEM OS FILHO (2007) fev - mai * Não foram encontradas referências (transição) Tillandsia gardneri jul - ago fev - mai (estação fria e seca) (transição) Tillandsia stricta MARQUES & LEM OS FILHO (2007) dez - mar mai - set ago - set (estação quente e chuvosa) (estação fria e seca) (estação estação fria e seca) Vriesea neoglutinosa ago - mar jan - mar (transição e estação (estação quente e chuvosa) M ACHADO & SEM IR (2006), M ARQUES & LEM OS FILHO (2007) M ARTINELLI (1994) quente e chuvosa) Temperatura (ºC) Temperatura máxima 30 20 10 0 Umidade relativa do ar (%) 100 80 60 40 20 0 C. Temperatura mínima 40 B. 96 Temperatura média 100 mai jun jul ago set Insolação out nov dez jan Umidade relativa do ar fev mar abr 300 250 200 150 100 50 0 300 250 200 150 100 50 0 Insolação (horas/mês) Precipitação Precipitação (mm) A. Aechmea nudicaulis 50 Revista SEB Ano 14 Final.indd 96 0 09/10/2012 13:44:04 Insolação Umidade relati do ar (%) 100 C. Umidade relativa do ar 300 250 200 150 100 Brazilian Journal of Ecology ISSN50 1516-5868 0 lação (horas/mês) 100 80 60 40 20 0 Aechmea nudicaulis 50 0 10 D. Billbergia amoena 5 0 30 E. Nº de indivíduos em flor F. tillandsia stricta 20 10 0 60 neoregelia cruenta 40 20 0 10 G. vriesea neoglutinosa 5 H. 0 150 Comunidade 100 50 0 mai jun jul ago set DISCUSSION On comparing various habitats in the Atlantic Rain Forest, all in the southeast of Brazil, bromeliad species flowering phenology was found to be considerably variable. Kochmer and Handel (1986) attribute the regulation of flowering in temperate regions mainly to intrinsic factors, which they denominate phylogenetic constraints, and affirm that competition by pollinators would be responsible for only small and temporary adjustments during flowering periods. From the present study, it was possible out nov dez jan fev mar abr to indicate that, in tropical areas, these constraints are possibly less important in determining phenological patterns than local selective pressure. In all the bibliographies used for comparative studies (15, 12, 14), the six species studied presented ornithophylic characteristics, such as exposed inflorescences, with attractive bracts tubular and inodorous flowers with contrasting colors and daily anthesis (7), with records of hummingbirds as their main pollen vectors. Sequential and continuous flowering of species with the same floral syndrome has been pointed out as being an important 97 Revista SEB Ano 14 Final.indd 97 09/10/2012 13:44:04 Brazilian Journal of Ecology ISSN 1516-5868 strategy in the maintenance of pollinators throughout the year, thereby maximizing the reproduction of these vegetal species (2, 12, 14). Nonetheless, the records of bromeliad flowering in the Maricá restinga have shown a period of the year with very low intensity, or even the total absence of floral activity, with the consequential lack of available nectar for hummingbirds. Notably, bromeliad species represented around 60% of the ornithophyles within the study area (18). In other words, they represent the main resource for these birds. Notwithstanding, there are records of low throchili diversity, with only Amazilia fimbriata Elliot and Eupetomena macroura Gmelin as floral visitors in the Maricá (13) and Jurubatiba (8) restingas. Possibly this diversification in the guild of bromeliad pollinators, this including insects, in the restinga, may have favored the successful reproducibility of these plants. In the Marica restinga, by presenting a high fruit|flower ratio (around 90%), A. nudicaulis is not self-compatible (Suizani, unpublished data). In other words, fruit production depends on the pollinator. This could be the consequence of the large number of visits by at least four species of butterflies and two species of bees supplanting the number of visits by hummingbirds. Schmid et al. (2011) reported that both bees and hummingbirds are responsible for the pollination of A. nudicaulis in an area of the restinga in Santa Catarina State. Besides hummingbirds, Almeida et al. (2004) also registered bees as the most frequent visitors (93,3%) of Tillandsia stricta in the Jurubatiba restinga. Apparently, hummingbirds were the only, or at least always the most frequent, floral visitors of the species studied in other habitats of the Atlantic Rain Forest (15, 12, 14). These data presuppose that, in the restinga environment, the pollination of some bromeliad species tends to be more generalist. As the restingas are geologically recent and their fauna mainly composed of species that have migrated from adjacent, humid forests (3), possibly more generalist pollination systems selectively arose, thus guaranteeing more successful reproducibility, as it is improbable that specialized pollinators migrated together with specific vegetal species (1). Thus, it is presupposed that pollinator competition was possibly different in the two areas, thereby giving rise to flowering period variation. CONCLUSIONS Divergence in flowering periods between the areas compared, and the rare cases of significant correlations between flowering and factors, such as temperature, rainfall, photoperiod and relative humidity of the air in the restinga, indicate that phylogenetic constraints and abiotic environmental factors are possibly not the main determinants of this phenophase in some bromeliad species. This presupposes that biotic factors, as variations in the pollinating scenario, could possibly be related to variations in the distribution and extent of flowering periods in species of this family, whose occurrence includes restinga and forest areas. RESUMO O estudo foi feito na APA da restinga de Maricá, RJ, Brasil, em uma comunidade de Bromeliaceae. Os dados coletados focaram a intensidade (2010-2011) e atividade (2004-2011) da fenologia da floração. Foram aplicados testes de correlação entre floração e os fatores ambientais temperatura, precipitação, umidade relativa do ar e insolação, além de comparações entre os períodos dessa fenofase para as mesmas espécies em outros habitats da Mata Atlântica do sudeste brasileiro. Aechmea nudicaulis (L.) Griseb., Billbergia amoena (Lodd.) Lindl., Neoregelia cruenta (Graham) L.B. Sm., Tillandsia gardneri Lindl., Tillandsia stricta Sol. ex Sims. e Vriesea neoglutinosa Mez. apresentaram floração sequencial, com picos concentrados na estação chuvosa da restinga. Os fatores abióticos testados não mostraram correlação estatística significativa com os períodos de floração da maioria das espécies. As exceções foram T. stricta e B. amoena, onde a primeira apresentou correlação positiva significativa com a temperatura média e mínima, e a segunda com a umidade relativa do ar. Três das seis espécies apresentaram variações notáveis no período e duração da floração quando comparadas a outros habitats, através dos levantamentos bibliográficos. Também foram observadas variações na guilda de visitantes florais, quase que exclusivamente representada por beija-flores em áreas de mata, mas incluindo insetos (abelhas e borboletas) em área de restinga. Concluímos que fatores abióti- 98 Revista SEB Ano 14 Final.indd 98 09/10/2012 13:44:05 Brazilian Journal of Ecology ISSN 1516-5868 cos e intrínsecos (como restrições filogenéticas) não sejam os principais determinantes nos períodos de floração de algumas bromélias, sugerindo que fatores abióticos como a polinização possam ser mais significativos. Palavras chave: Bromeliaceae, fenologia, floração sequencial, restinga, restrições filogenéticas REFERENCES 1 -ALMEIDA, E. M.; STORNI, A.; RITTER, P. D.; ALVES, M. A. S. Floral visitors of Tillandsia stricta Sol. (Bromeliaceae) at Restinga of Jurubatiba, Macaé, Rio de Janeiro, Brazil. Vidalia, Viçosa, v. 2, n. 1, p. 30-35, 2004. 2 -ARAÚJO, A. C.; FISCHER, E. A.; SAZIMA, M. Floração sequencial e polinização de três espécies de Vriesea (Bromeliaceae) na região de Juréia, sudeste do Brasil. Revista Brasileira de Botânica, São Paulo, v. 17, n. 2, p. 113-118, 1994. 3 - ARAÚJO, D. S. D. Análise florística e fitogeográfica das restingas do estado do Rio de Janeiro. 2000. 176 f. Tese (Doutorado em Ecologia) - Instituto de Biologia, Universidade Federal do Rio de Janeiro, Rio de Janeiro. 2000. 4 -BENCKE, C. S. C.; MORELLATO, L. P. C. 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. 269-275. 2002. 5 -BENZING, D. H. Bromeliaceae: Profile of an adaptive radiation. Cambridge: Cambridge University Press, 2000. 690 p. 6 -BONATO, R. R.; MURANO, N. D. Aspectos fenológicos e reprodutivos de Vriesea incurvata Gaudich (Bromeliaceae). Acta Scientiarum Biological Sciences, Maringá, v. 28, n. 2, p. 95-102, 2006. 7 -FAEGRI, K ; PIJL, L. The principles of pollination ecology. New York: Pergamon Press, 1976. 291 p. 8-FONSECA, L. C. N.; ALVES, M. A. S. Assembleia de plantas utilizada por beija-flores (aves: Trochilidae) em área de restinga aberta de Clusia no Parque Nacional da Restinga de Jurubatiba, Sudeste do Brasil. In: CONGRESSO BRASILEIRO DE ECOLOGIA, 8, 2007, Caxambu – MG. Anais... Caxambu: SEB, 2007. 09-FOURNIER, L. A. Un método cuantitativo para la medición de características fenológicas en árboles. Turrialba, San José, v. 24, p. 422-423, 1974. 10-KÖEPPEN, W. Climatologia: com um estúdio de los climas de La tierra. México: Fondo de Cultura Econômica, 1948. 479 p. 11-KOCHMER, J. P.; HANDEL, S. N. Constraints and competition in the evolution of flowering phenology. Ecological monographs, Wasshington, v. 56, n. 4, p. 303-325, 1986. 12-MACHADO, C. G; SEMIR, J. Fenologia da Floração e biologia floral de bromeliáceas ornitófilas de uma área da Mata Atlântica do Sudeste brasileiro. Revista Brasileira de Botânica, São Paulo, v. 29, n. 1, p. 163-174, 2006. 13-MACIEL, N. C. A fauna da restinga do estado do Rio de Janeiro: passado, presente e futuro. Proposta de preservação. In: SIMPÓSIO SOBRE RESTINGAS BRASILEIRAS, 1984, Niterói. Anais... Niterói: CEUFF, 1984. p. 285-304. 14-MARQUES, A. R; LEMOS FILHO, J. P. Fenologia reprodutiva de espécies de bromélias na Serra da Piedade, MG, Brasil. Acta Botanica Brasilica, São Paulo, v. 22, n. 2, p. 417-424, 2008. 15-MARTINELLI, G. Reproductive biology of bromeliaceae in the atlantic rainforest of southeastern Brazil. 1994. 197 f. Tese (Doctorate in Philosophy) - School of Biological and Medical Sciences, University of St. Andrews, St. Andrews. 1994. 16-MATALLANA, G.; WENDT, T.; ARAÚJO, D. S. D.; SCARANO, F. R. High abundance of dioecious plants in a tropical coastal vegetation. American Journal of Botany, Saint Louis, v. 92, n. 9, p. 1513-1519, 2005. 17-NARA, A. K.; WERBER, A. C.; Biologia floral e polinização de Aechmea beeriana (Bromeliaceae) em vegetação de baixio na Amazônia Central. Acta Amazonica, Manaus, v. 32, n. 4, p. 571-588, 2002. 18-ORMOND, W. T.; PINHEIRO, M. C. B.; LIMA, H. A.; CORREIA, M. C. R.; PIMENTA, M. L. Estudo das recompensas florais das plantas da restinga de Maricá- Itaipuaçu, RJ. I- Nectaríferas. Bradea, Rio de Janeiro, v. 6, n. 21, p. 179195, 1993. 19-PEREIRA, F. R. L.; QUIRINO, Z. G. M. Fenologia e biologia floral de Neoglaziovia variegata 99 Revista SEB Ano 14 Final.indd 99 09/10/2012 13:44:05 Brazilian Journal of Ecology ISSN 1516-5868 (Bromeliaceae) na caatinga da Paraíba. Rodriguesia, Rio de Janeiro, v. 59, n. 4, p. 835-844, 2008. 20-RODARTE, A. T. A. Caracterização espacial, temporal e biologia floral das espécies de restinga, com ênfase nos recursos florais. 2008. 685 f. Tese (Doutorado em Ciências Biológicas – Botânica) - Departamento de Botânica, UFRJ/ Museu Nacional, Rio de Janeiro. 2008. 21-SANTANA, C. S.; MACHADO, C. G. Fenologia de floração e polinização de espécies ornitófilas de bromeliáceas em uma área de campo rupestre da Chapada da Diamantina, BA, Brasil. Revista Brasileira de Botânica, São Paulo, v. 33, n. 3, p. 469-477, 2010. 22-SCHMID, S.; SCHMID, V. S.; ZILLIKENS, A.; HARTER-MARQUES, B.; STEINER, J. Bimodal pollination system of the bromeliad Aechmea nudicaulis involving hummingbird and bees. Plant Biology, Freiburg, v. 13, p. 41-50, 2011. 23-SIQUEIRA FILHO, J. A.; MACHADO, I. C. Síndrome de polinização de uma comunidade de Bromeliaceae e biologia floral de Vriesea psittacina (Hooker) Lindley (Bromeliaceae) em Brejo dos Cavalos, Caruaru, Pernambuco. Revista Brasileira de Zoologia, Curitiba, v. 24, p. 277-284, 2007. 24-SNOW, D. W.; SNOW, B. K. Feeding ecology of hummingbirds un the Serra do Mar, southeastern Brazil. El Hornero, Buenos Aires, v. 12, p. 286-450, 1986. 100 Revista SEB Ano 14 Final.indd 100 09/10/2012 13:44:05 Brazilian Journal of Ecology ISSN 1516-5868 Floral Biology and Pollination Ecology of Chrysobalanus icaco L. (Chrysobalanaceae) in an Environmental Protection Area (EPA) within the Restinga of Barra do Rio Mamanguape, Paraíba, Brazil. Túlio Freitas Filgueira de Sá- Graduado em Ecologia, Laboratório de Ecologia Vegetal Departamento de Engenharia e Meio Ambiente – Centro de Ciências Aplicadas e Educação UFPB (email:tulio_filgueira@hotmail.com) Evelise Locatelli- Laboratório de Ecologia Vegetal, Departamento de Engenharia e Meio Ambiente, Centro de Ciências Aplicadas e Educação – UFPB. (email: evelise.locatelli@pq.cnpq.br) ABSTRACT (Floral Biology and Pollination Ecology of Chrysobalanus icaco (Chrysobalanaceae) in an Environmental Protection Area (EPA) within the Restinga of Barra do Rio Mamanguape, Paraíba, Brazil). The aim was to investigate floral biology and pollination ecology of Chrysobalanus icaco (Chrysobalanaceae) in an EPA of Barra do Rio Mamanguape - Rio Tinto (6º 70’72’’S and 34º 90’21’’W). Data was obtained during the period July 30th, 2009 to September 30th, 2010. 10 individuals, distributed among dunes in the study area inside the open restinga, were selected. Chrysobalanus icaco presents continuous flowering, daily anthesis, clear-colored flowers, and a small amount of nectar, viz., 1-5µl with an average concentration of 20 to 55%. The flowers were visited by 11 insect species, belonging to the orders Hymenoptera, Lepdotera and Coleoptera. The most common visitors were wasps of the family Crabonidae. The bee Apis mellifera was also another. Although only 3,3% of fruit formation was obtained in spontaneous self-pollination treatments (n=1.452), the test control (n=1.064) was more successful with 9,5%. As the species is a generalist, hence visited by various groups of insects, it is important as a resource for the local fauna. Key words: Restinga; Chrysobalanus icaco; pollination. INTRODUCTION The Atlantic Rain Forest biome formerly consisted of an area of 1.306.000 km², or around 15% of what is now known as, Brazilian territory. After 500 years of continuous exploitation, less than 4% of the original primary forest, plus 4% of secondary forest, still remain. Apart from this widespread devastation, the forest harbors one of the most important assemblages of plants and animals worldwide (45, 44). Ecologically, the restinga is considered a mosaic of various vegetal formations belonging to the Atlantic Rain Forest, located on the Brazilian coastal plateau (35). According to Suguio & Tessler (1984), the denomination ‘restinga’, as employed in the Brazilian literature, has several meanings, and can be used as much for designating various types of coastal deposits, as well as other coastal, and even vegetal, features. According to Azevedo (2005), the adaptability of the species encountered in coastal ecosystems demonstrates their importance in the maintenance of dune relief, which is constantly undergoing modifications, mainly wind induced. The family Chrysobalanaceae, distributed throughout tropical and subtropical regions, is comprised of 20 genera and 500 species, form shrublike to arboreal (29). The species Chrysobalanus icaco 101 Revista SEB Ano 14 Final.indd 101 09/10/2012 13:44:05 Brazilian Journal of Ecology ISSN 1516-5868 L., a shrub, is essential for fixing dunes in areas of the restinga. In Brazil, this species is also used in the treatment of diabetes, its hypoglycemic and diuretic effects having been pharmacologically proven (13, 7, 2). As, to date, there are few studies of floral biology and pollination ecology of the Chrysobalanaceae family, and with the aim of obtaining additional information, an investigation of these specific aspects in Chrysobalanus icaco was undertaken, in an Environmental Protection Area (EPA) in Barra do Rio Mamanguape, in Rio Tinto county, Paraíba State, one of the most important conservation units in the Brazilian northeast. . METHODOLOGY Study area The study was carried out in the EPA of Barra do Rio Mamanguape (6º46’55,814” S and 35º03’46,732’’ W), in Rio Tinto county, Paraíba State. The EPA perimeter is around 80 km, encompassing a total area of 14.460 ha (34). According to Köppen, the climate of the region is tropical rainy (Aw), and the average annual temperature varies between 24ºC and 27ºC. The average annual rainfall along the north Paraiba coast is around 1.500mm, with the rains concentrated in the trimester April to June (28). Sampling planning Data were obtained during the period July 30th, 2009 to September 30th, 2010, during monthly visits to a natural population of C. icaco. In the study area, 10 individuals, 5 to 10 meters, apart were selected. These were distributed in an area of dunes in an open part of the restinga at about 50 meters from the beach (6º 70’72’'S and 34º 90’21’'W Datum SAD-69). The flowers collected from five individuals were conserved in alcohol 70% for subsequent analysis and morphometry of floral structures (n=20) through stereomicroscopy. The average number of flowers per inflorescence was estimated (n=40), and the number of open flowers in three randomly chosen individuals counted. Floral anthesis and resources offered to visitors were verified in the field. For the former, buds in the pre-anthesis stage were marked for posterior accompaniment until floral se- nescence. Stygma receptivity was tested in the field using H2O2, and with the aid of a magnifying glass (18). Sugar concentration in the nectar was noted with the aid of a pocket refractometer (0 - 90% Atago®), and the volume measured with micro-syringes of 5 µl and 10 µl (Microliter®) from buds which had been previously bagged during pre-anthesis. In order to check the rate of floral nectar production in six groups of inflorescences, each group containing four flowers, use was made of cloth-bagged inflorescences, thereby impeding floral-visitor contact. At 7 a.m., nectar was extracted from the first group, at 9:00 a.m., from the second, and so on, the final extraction from the sixth group beginning at 5:00 p.m. The pollen grains from each anther were colored with safranine and counted directly (14) with the aid of a squared laminator and stereomicroscope (16x magnification). Pollinic viability was estimated using acetic carmine 2% (33). Ten buds in the pre-anthesis stage from three specimens were used throughout the whole process. The ovary wall was cut open to facilitate ovule counting. For obtaining phenological data, ten individuals were observed by monthly accompaniment over the period July, 2009 to Sepetember, 2010, whereby data referring to flowering and fruition were collected (17). The flowering pattern was classified according to Newstrom et al. (1994). Normality testing of data was through Shapiro – wilk, followed by Pearson linear correlation testing of the relationship of the flowering and fruition phenophases with precipitation. During the study period, 85 hours of observation, distributed throughout seven consecutive days from 5:00 a.m. to 5:00 p.m., were exclusively dedicated to recording and observing visitors, as to visiting time, frequency and duration, and their behavior towards the flowers. During this period, visitors were classified as rare (0 to 5% of the visits), common (6 to 15% of the visits), and very common (16 to 45% of the visits), as well as effective pollinator (eP) – all those that contacted the stigmatic area and the anthers -, and occasional pollinators (oP) – stigmas and anthers only rarely or not contacted - . The spot of pollen placement on the visitor’s body was analyzed according to visiting behavior. Some visitors from each visiting species were collected and dry-mounted for structure analysis and identifi- 102 Revista SEB Ano 14 Final.indd 102 09/10/2012 13:44:05 Brazilian Journal of Ecology ISSN 1516-5868 cation, prior to depositing in the Laboratory of Vegetal Ecology – LABEV – of the Federal University of Paraíba, campus IV. For defining reproductive strategy, C.icaco flowers were subjected to experiments involving manual self-pollination, spontaneous pollination, xenogamy, natural pollination and apomixis. Buds, previously randomly selected among the ten individuals under study, were marked with a colored tape, to be so identified as test controls. The exsiccates produced from sample specimens were deposited in the Laboratory of Vegetal Ecology – LABEV – of the Federal University of Paraíba, campus IV. RESULTS Chrysobalanus icaco is a shrublike species, from 1,5 to 3 meters high, and generally placed 2 to 10 meters apart, one from the other. Flowering occurs throughout the year (27), the peak of highest concentration of inflorescences and flowers per individual occurring in the dry season, from September to December, with little rain (66 mm), and an average temperature of 27°C (Figure 1). Generally speaking, when compared to other species, C. icaco flowering and fruition is extremely irregular, with the regular occurrence of individuals presenting all the different stages at the same time, thereby generating mutual asynchronism. Whereas some individuals presented flowers, others, which had already ceased to flower, had reached the fruit maturation stage, and some even presented overlapping cycles of flowering-production of fruits-seeds in one and the same plant. Rainfall Flowering Fruition Time of extraction of nectar Group 07:00 09:00 11:00 13:00 15:00 17:00 µl 5,1 ± 5,0 1,5 ± 1,2 2,3 ± 2,2 % 42 1 2,5± 2,0 1,5 ± 1,3 1,0 ± 0,7 1,5 ± 1,0 1,0 ±0,7 0,7 ±0,5 fruition Figure 1.µlFournier Intensity of the flowering and % 15 15 32 35 42 55 phenophases, as well as precipitation, of the ten Chryso2 µl 4,0 ± 3,9 1,3 ± 1,2 1,4 ± 1,2 0,9 ± 0,8 0,7 ± 0,6 32 42 34 55 55 balanus %icaco individuals during the period July, 2009 to 3 µl 4,5 ± 4,2 1,9 ± 1,6 1,3 ± 1,2 1,3 ± 1,1 September, 2010. % 42 42 55 55 4 5 6 42 55 µl 4,7 ± 4,4 3,3 ± 3,4 % 42 5,4 ± 5,2 % 55 Revista SEB Ano 14 Final.indd 103 Order|Family Genus|species Frequency Behavior 103 55 µl The production and development of C. icaco fruits occurs throughout the year with a peak of release from December to February (Figure 1). As regards size, this attained around 7 mm (N=50) in a fortnight, thereon varying between 12,8 and 19,6 mm (DP 2,13, N=44), until reaching maturation, ready for dispersion, at the end of 45 days, with sizes varying between 26,8 and 29,3 mm (DP 1,33, N=20). Data on flowering (p= 0.1026), fruition (p=0.6722) and precipitation (p=0.41497) were considered normal. There was a significant negative correlation between flowering and precipitation (r =-2.1611, p < 0,005), contrary to fruition and precipitation where the correlation was significantly positive (r = 1.4265, p > 0,005). C. icaco inflorescences are terminal cymoid. The number of flowers that open every day, per inflorescence, varied between five and eight (DP 1,41, N=40), there being a certain variation in the number among individuals. The 7 to 11 mm long (DP 1,4 – N=20) flowers are hermaphroditic and urceolate, whose floral parts are arranged in whorls (cyclic). The 10 mm-long gynoecium, which possesses a pilose semi-detached ovarium and is unilocular, uniovular and stileto-like, positions the stygma over and opposed to the stamina. The androecium, formed by 22 four-to-six mm long (DP 1,2, N=20), polystem, heterodynamic and external stamina, possesses yellow-colored anthers and a longitudinal opening. The fruit is berrylike, 5 cm in diameter and red and orange colored with a soft white pulp. Anthesis lasts three days. On the first day, the flowers are light colored and attractive. On the second and during the morning, the petals, which have acquired an orange tone, drop off. The opening of the buds is asynchronous, the production of nectar initiating even before the petals are fully open. Some flowers already begin to open at around 8:00 a.m. Protogyny occurs in the first two hours of opening, and when the flower is in the feminine phase. Spontaneous opening of the anthers begins gradually and asynchronously from 10 o’clock on, thereby initiating the bisexual phase of the flower. At both instants, the petals are attractive and there is the production of nectar, with average viability reaching 95% (+ 2,0). C. icaco flowers begin to produce nectar at 7:00 a.m., with an average volume of 2,5± 2,0 µl Substance 09/10/2012 13:44:06 Brazilian Journal of Ecology ISSN 1516-5868 per flower. In other words, even before the flower is totally open, production has already begun, only dropping off at the end of the afternoon. However, although the production of nectar takes place in the first ten hours of anthesis, there is only an increase in the concentration of sugar towards the end of the afternoon. The small amount of nectar produced (1-5 ml) is stored on the nectariferous disc at the filament insertion, and is limited to the first day of anthesis. In the present case, nectar sugar concentration was 15-55%. The production of nectar of the last group of flowers tested reached 5,4 ± 5,2 ml, 55% of the total volume of nectar accumulated (Table 1). The extraction of nectar did not affect its production. With a constant daily production of nectar for visitors, the number of these per flower was naturally higher. Keeping in mind that the plant is a generalist, the production of nectar was consequentially higher. The average production of nectar was around 1,0 ± 1,5 ml. For extraction at the six times indicated, there must have been re-absorption, notable through the similar quantities of nectar momentarily available. The first group began with a concentration of 15%, this reaching 55% towards the end. In the second group, this began with 32%, had already reached 42% until 11: a.m., and gradually dropped until 1:00 p.m. Oscillations in production possibly occurred throughout. The C. icaco flowers were visited by 11 insect species belonging to the orders Hymenoptera (8), Lepidoptera (2) and Coleoptera (1). The visitors, their behavior and the resource sought appear in Table 2. The first visits began at 7:00 a.m., even before the flowers were completely open. The most common visitor was a species of wasp of the family Crabronidae. When on the flowers, these wasps were shown to be extremely territorial. After initially flying over the plant, they then alighted on a flower, even when not completely open, whereupon they introduced the buccal apparatus to suck out nectar. On passing through the inflorescences, the ventral part of the abdomen entered in contact with the anthers and stigma. Although the visit to each flower lasted around 2-3 seconds, permanence among the inflorescences themselves depended on the number of open flowers. The wasps of this family can be considered as the effective pollinators, since, through seasonal independence, their behavior and frequency was stable throughout the year. Bees of the species Apis mellifera L. entered in contact with the reproductive structures when collecting nectar. During the rainy season, their visiting peak was between 10:00 and 11:00 a.m. in the morning, and 2:00 to 3:00 p.m. in the afternoon. The duration of each visit was extremely variable, extending to 9 seconds per flower, during which there were short and continuous flights among the inflorescences. . Table 1. Volume and concentration of nectar in Chrysobalanus icaco, measured by group of flowers subjected to extraction. Time of extraction of nectar Group 1 2 3 4 5 6 07:00 09:00 11:00 13:00 15:00 17:00 µl 2,5± 2,0 1,5 ± 1,3 1,0 ± 0,7 1,5 ± 1,0 1,0 ±0,7 0,7 ±0,5 % 15 15 32 35 42 55 µl 4,0 ± 3,9 1,3 ± 1,2 1,4 ± 1,2 0,9 ± 0,8 0,7 ± 0,6 % 32 42 34 55 55 µl 4,5 ± 4,2 1,9 ± 1,6 1,3 ± 1,2 1,3 ± 1,1 % 42 42 55 55 µl 5,1 ± 5,0 1,5 ± 1,2 2,3 ± 2,2 % 42 42 55 µl 4,7 ± 4,4 3,3 ± 3,4 % 42 55 µl 5,4 ± 5,2 % 55 104 Order|Family Revista SEB Ano 14 Final.indd 104 Genus|species Frequency Behavior 09/10/2012 Substance 13:44:07 Brazilian Journal of Ecology ISSN 1516-5868 Bees of the species Trigona spinipes Fabri- of sexual system among the angiosperms (31). The concentration of sugar in nectar is also cius were often observed collecting nectar. In this case, the bee perforated the chalice, thereby harm- associated with the type of floral visitor (6, 15, 31). Time of extraction of nectar ing the flower, since some lepidoptera, which before Flowers visited by bees and wasps present a high conGroup 07:00 09:00 11:00 13:00 15:00 17:00 collected legitimately, began to introduce their ap- centration (13-50%), which was the case of C. icaco in 1 µl 2,5± 2,0 1,5 ± 1,3 1,0 ± 0,7 1,5 ± 1,0 1,0 ±0,7 0,7 ±0,5 the present study, with an even higher concentration paratus through the hole thus made. % 15 15 32 35 42 55 (55%) than the interval established by Baker (1975). In the reproductive experiments (Table 2 µl 4,0 ± 3,9 1,3 ± 1,2 1,4 ± 1,2 0,9 ± 0,8 0,7 ± 0,6 C. icaco visitors used nectar as the main 3), it could be observed that, whereas spontaneous % 32 42 34 55 55 due to its high conself-pollination treatment 3 µlwas successful in 3,3% 4,5foraging ± 4,2 1,9resource, ± 1,6 1,3possibly ± 1,2 1,3 ± 1,1 centration. Besides being the most important floof the cases, in the test control this reached 9,5%. % 42 42 55 55 ral reward pollen Although the fecundation 4 µlobtained by self-pollina5,1 ±offered 5,0 1,5to ± 1,2 2,3 biotic ± 2,2 vectors (23), metabolized by tion indicated species compatibility, this was inex- nectar is easily % 42 42 55all classes of flo4,7 ±requiring 4,4 3,3 ±high 3,4 energetic expressive, due to the5 smallµlnumber of fruits formed ral visitors, without % plant for 55 its production (38). (3,3%). Low fruit productivity was characterized penditure from the 42 6 µl 5,4 ± 5,2could be related The reduced production of nectar through reproductive testing. % 55 Table 2. Visitors to Chrysobalanus icaco flowers. Ep – Effective pollinator, Op – Occasional pollinator, N – Nectar; P – Pollen. R = rare (till 5% of the visits); C = common (6% to 15% of the visits) and VC = very common (16% to 45% of the visits). Order|Family Genus|species Hymenoptera/Crabronidae Hymenoptera/Apidae Hymenoptera/Apidae Hymenoptera/Apidae Hymenoptera/Vespidae Hymenoptera Hymenoptera Hymenoptera/Apidae Coleoptera/Coccinellidae Lepidóptera 1 Lepidóptera 2 Morfoespécie I Centris nitens Lepeletier, 1841 Apis mellifera Linnaeus, 1758 Xylocopa frontalis Olivier, 1789 Polistes canadensis Linnaeus, 1758 Pepsis sp. Vespa sp. Trigona spinipes Fabricius, 1793 Não identificado Não identificada Não identificada Frequency of visits VC C VC R R C C VC R R R Behavior Ep Op Op Op Op Ep Op Op Op Op Op Substance collected N N/P N/P N/P N N/P N N/P N N N Table 3. Formation of fruits from controlled pollination. Treatment Control Spontaneous autogamy Manual autogamy Xenogamy Apomixis Total N. of flowers N. of Fruits Success (%) Tested 1064 1452 43 36 25 2620 Obtained 101 47 0 0 0 148 9,5 3,3 0 0 0 5,9 DISCUSSION The floral attributes presented by Chrysobalanus icaco, such as diurnal anthesis, a short corola, light color, low production of nectar (2,5± 2,0 µl), several flowers per inflorescence and sweet odor, are all associated to the syndrome of entomophily (15). Morphological analysis of the flowers indicated hermaphroditism, the most common type to a species strategy, thereby forcing visitors to carry out the search among several flowers to satisfy their wants, with the consequential cross pollination (26,37). The association of low production with high concentration is essential for a plant to benefit by pollination. Whereas the high concentration of nectar sugar serves in attracting pollinators, its constant availability throughout the day maintains their presence. 105 Revista SEB Ano 14 Final.indd 105 09/10/2012 13:44:07 Brazilian Journal of Ecology ISSN 1516-5868 Various patterns of nectar secretion during anthesis can occur in vegetal species; on the one side, only one secretion occurs throughout the entire anthesis, whereas on the other, secretion can continue after each removal by a visitor, with the consequential replacement of volume (19). This is what occurred with C. icaco, whose continuous secretion guarantees a constant flow and larger number of visitors per flower, also the case of Couepia uiti (Chrysobalanaceae), as noted by Paulino Neto (2007). The concentration of nectar in C. icaco flowers is high and similar to that of other generalist entomophylous plant-species (8, 24, 29, 35), which makes this resource a very attractive energy source for visitors. According to Baker (1975), flowers visited by wasps and bees present high nectar sugar concentration (16-50%). Furthermore, the increase in this concentration could be related to changes in temperature and relative humidity (12). Although the volume of nectar produced per flower in C. icaco is low, this is compensated by the high concentration of sugar, which, in this case, reached its peak at the end of the afternoon. C. icaco presents generalist entomophylous pollination. The most frequent visitors were wasps of the family Crabronidae and bees of the species Apis mellifera and Centris nitens. Flowers adapted to pollination by bees and wasps are denominated entomophylous (15, 9, 31). Wasps of the family Crabronidae, even though less frequent, are considered legitimate visitors, by their constant pollination throughout the year, independent of the season, thus different from the bees Apis mellifera and Centris nitens, which are seasonal. According to Proctor et al. (1996) and Heithaus (1979), flowers pollinated by wasps are open, small and opaque-colored, with a shallow corola, hence facilitating access to the nectarines, whereas in flowers where corollas are deep and narrow, access is restricted (1). To date, there are no studies or citations of floral visits by species of the family Crabronidae. Wasps are cited as effective pollinators in various studies (32, 46, 25, 22, 1). Flowering in C. icaco is continuous and abundant, thus offering a high availability of resources for the anthophilous fauna of the area. Plants with massive flowering, the case of C. icaco, attract opportunist visitors, capable of quickly responding to the ephemeral availability of resources (20, 11, 10). Furthermore, according to Augspurger (1980 and 1981), abundant flowering not only attracts a large number of floral visitors, but also increases the rate of visits and transportation of pollen among plants, thus elevating pollination levels. Chrysobalanus icaco is characterized by low fruit production (Fruits|Flowers=9,5% reproductive success). A certain amount of the formed fruits drop off while still in the green stage, without reaching maturity, when the fruit is purple-reddish. As expressed by the average Fruit|Flower proportion of 42,1% (42), hermaphrodite plants produce an excess of flowers which do not reach the fruit stage. Hypotheses have been presented, in the attempt to clarify this pattern of low fruit production, among which, limitation in the amount of pollen, number of pollinators, or amount of maternal nutrients, or even selective abortion, are outstanding (40, 41). In the species under study, there appears to be no limitation in the amount of pollen or pollinators, since the occurrence of flower visits is intense. Furthermore, the gradual release of pollen grains favors their availability throughout anthesis. The reproductive success of spontaneous self-pollination (3,3%) was less than that under natural conditions (9,5%), or rather, even though selffecundatory, cross pollination in C. icaco places in evidence the extreme importance of pollinating agents for the species and its genic flow. In species of the family Chrysobalanaceae, such as Couepia uiti (30) and Couepia bracteosa, self-incompatibility was evident (16). Work on the reproductive system of this family is, as yet, scarce, whereby the urgent necessity for further pertinent studies. As regards the pollen|ovulum rate, the more efficient the transference of pollen, the lower is the rate (14). In C. icaco, xenogamy is obligatory, thus the pollen|ovulum rate is very high. Hence, on analyzing self-pollination test data, the extremely high dependency on pollinators for accomplishing reproductive efficiency becomes evident. Continuous flowering in C. icaco, added to its floral characteristics, makes this a key species, due to its ecological role as a source of trophic resources 106 Revista SEB Ano 14 Final.indd 106 09/10/2012 13:44:07 Brazilian Journal of Ecology ISSN 1516-5868 throughout the year, both for its own pollinators, as well as other insect species, which, in turn, act in pollinating numerous other plants in the ecosystem. ACKNOWLEDGEMENT Thanks are extended to Dr. Celso Feitosa for the identification of the wasps and bees (UFPB); to MSc. Maria do Céo R. Pessoa (UFPB) for identification of the vegetal species studied; to the Instituto Chico Mendes de Conservação da Biodiversidade – ICMBio, and to CNPq for the Scientific Initiation grant for the first author, and for the grant Productivity in Research for the second. RESUMO (Biologia Floral e Ecologia da Polinização de Chrysobalanus icaco (Chrysobalanaceae) em uma área de Restinga na Área de Proteção Ambiental (APA) da Barra do Rio Mamanguape, Paraíba, Brasil). O presente estudo teve como objetivo investigar a biologia floral e ecologia da polinização de Chrysobalanus icaco (Chrysobalanaceae) na APA da Barra do Rio Mamanguape Rio Tinto (6º 70’72’'S e 34º 90’21’'W). Os dados foram obtidos no período de 30 de julho de 2009 a 30 de setembro de 2010. Na área de estudo foram selecionados 10 indivíduos distribuídos em área de duna na formação aberta de restinga. Chrysobalanus icaco apresenta uma floração contínua, antese diurna, flores claras e uma pequena quantidade de néctar, 1-5ml com concentração média 20 a 55 %. As flores foram visitadas por 11 espécies de insetos pertencentes às ordens Hymenóptera, Lepdóptera e Coleoptera. Os visitantes mais comuns foram vespas da família Crabronidae e a abelha Apis mellifera. Nos tratamento de autopolinização espontânea (n=1452) obteve-se 3,3% de formação de frutos, mas no teste controle (n=1064) obteve-se um maior sucesso com 9,5%. Por ser uma espécie visitada por vários grupos de insetos, possuindo, portanto, um sistema de polinização generalista, a espécie é importante como fonte de recursos para fauna local. Palavras chave: Restinga; Chrysobalanus icaco; polinização. REFERENCES 1- AGUIAR, C. M. L.; SANTOS G. M. M. Compartilhamento de recursos florais por vespas sociais (Hymenoptera:Vespidae) e abelhas (Hymenoptera: Apoidea) em uma área de Caatinga. Neotropica Entomology, v. 36, p. 836–842, 2007. 2- AGRA, M. F.; FRANÇA, P. F.; BARBOSAFILHO, J. M. Synopsis of the plants known as medicinal and poisonous in Northeast of Brazil. Revista Brasileira de Farmacognosia, v. 17, p. 114- 140, 2007 3- AUGSPURGER, C. K. Mass-flowering of a tropical shrub (Hybanthus prunifolius): influence of pollination attraction and movement. Evolution, v. 34, p. 475-488, 1980. 4- AUGSPURGER, C. K. Reproductive synchrony of a tropical plant: experimental effects of pollinators and seed predators on Hybanthus prunifolius (Violaceae). Ecology, v. 62, p. 775-788, 1981. 5- AZEVEDO, D. V. Propostas de Manejo para a APA das Dunas de Lagoinha-Paraipaba- Ceará. 2005. 124 f. Dissertação (Mestrado em Desenvolvimento e Meio Ambiente). Prodema- Programa Regional de Pós-Graduação em Desenvolvimento e Meio Ambiente, Pró-Reitoria de Pesquisa e Pós-Graduação, Universidade Federal do Ceará, Ceará, 2005. 6- BAKER, H. G. Sugar concentrations in nectar fromhummingbird flowers. Biotropica, v. 7, p. 37-41, 1975. 7- BARBOSA-FILHO, J. M. et al. Plants and their active constituents from South, Central, and North America with hypoglycemic activity. Revista Brasileira de Farmacognosia, v. 15, p. 392413, 2005. 8- BARBOSA, A. A. A.; SAZIMA, M. Biologia reprodutiva de plantas herbáceo-arbustivas de uma área de Campo Sujo de Cerrado. In: SANO, S. M; ALMEIDA, S. P.; RIBEIRO, J. F (Ed.). Cerrado: Ecologia e Flora. Brasília: Embrapa Cerrados, 2007. p. 291-307. 9- BARTH, F. G. Insects and flowers – The biology of a partnership. Princeton: Princeton University Press, 1991. 408 p. 10- BARRET, S. C. H. & SHORE, J. S. Dimorphic incompatibility in Turnera hermannioides 107 Revista SEB Ano 14 Final.indd 107 09/10/2012 13:44:07 Brazilian Journal of Ecology ISSN 1516-5868 Camb. (Turneraceae). Annals of the Missouri Botanical Garden, 72:259-263, 1985. 11- BAWA, K. S. Evolution of dioecy in flowering plants. Annual Review of Ecology and Systematics, v. 11, p. 15-39, 1980. 12- CORBET, S. A. et al. Post-secretory determinants of sugar concentration in nectar. Plant Cell Environ, v. 2, p. 293-308, 1979. 13- COSTA, O. A. Brazilian plants with hypoglycaemic effects. Leandra, v. 7, p. 63-75, 1977. 14- CRUDEN, R. W. Temporal dioecism; systematic breadth, associated traits, and temporal patters. Botanical Gazzete, v.149, p. 1-15, 1977. 15- FAEGRI, K.; VAN DER PIJL, L. The principles of pollination ecology. London: PergamoPress, 1979. 244 p. 16- FALCÃO, M. A.; LLERAS, E.; KERR, W. E. Aspectos fenológicos, ecológicos e de produtividade do pajurá (couepia bracteosa Benth.). Acta Amazonica, 11(3): 473-482, 1981. 17- FOURNIER, L. A. Un método cuantitativo para la medición de características fenológicas en arbores. Turrialba, vol. 4, p. 22-423. 1974. 18- GALEN, C.; PLOWRIGH, R. C. Testing the accuracy of using peroxidase actity to indicate stigma receptive. Canadian Journal of Botany, v. 65, p. 11-107, 1987. 19- GALETTO, L.; BERNARDELLO, G. Rewards in flowers. Nectar. In: DAFNI, A.; KEVAN, P. G.; HUSBAND, B. C. (Eds.). Practical Pollination Biology. Ontario: Cambridge, 2005. p. 261312. 20- GENTRY, H. A. Flowering phenology and diversity in tropical Bignoniaceae. Biotropica, 6: p. 64-68, 1974. 21- HEITHAUS, E. R. Flower visitation records and resource overlap of bees and wasps in northest Costa Rica. Brenesia, v. 16, p. 9-52, 1979. 22- HERMES, M. G.; KÖHLER, A. The flowervisiting social wasps (Hymenptera, Vespidae, Polistinae) in two areas of Rio Grande do Sul State, southern Brazil. Revista Brasileira de Entomologia, v. 50, n. 2, p. 268-274, 2006. 23- KEVAN P.G.; BAKER H. G. Insects as flower visitors and pollinators. Annual Review of Entomology, v. 28, p. 407-453, 1983. 24- MACHADO, A. O.; OLIVEIRA, P. E. Biologia floral de Casearia grandiflora Camb. (Flacour- tiaceae). Revista Brasileira de Botânica, v. 23, p. 283-290, 2000. 25- MECCHI, M. R. Comunidade de vespas Aculeata (Hymenoptera) e suas fontes florais. In: PIVELLO, V. R.; VARANDA, E. M. (Eds.), O cerrado Pé-de-Gigante: ecología e consevação, Parque Estadual de Vassununga. 2005. p. 255-266. 26- NAVARRO, L. Pollination ecology and effect of nectar removal in Macleania bullata (Ericaceae). Biotropica, v. 4, p. 618-625, 1999. 27- NEWSTROM, L. E., FRANKIE, GW. ; BAKER, H. G. A new classification for plant phenology based on flowering patterns in lowland tropical rain forest trees at La Selva, Costa Rica. Biotropica vol. 26, p.141-159, 1994. 28 - NIMER, E. Climatologia do Brasil. 2.ed. IBGE, Departamento de Recursos Naturais e Estudos Ambientais. Rio de Janeiro, p.422, 1989. 29- OLIVEIRA, P. E.; GIBBS, P. E. Reproductive biology of woody plants in a cerrado community of Central Brazil. Flora, v. 195, p. 311-329, 2000. 30- PAULINO-NETO H. F. Pollination and the breeding system of Couepia uiti (Mart and Zucc) Benth. (Chrysobalanaceae) in the Pantanal da Nhecolândia. Braz. J. Bot., v. 67, p.715719, 2007. 31- PROCTOR, M.; YEO, P.; LACK, A. The Natural History of Pollination. Portland: Timber Press, 1996. 479 p. 32- QUIRINO, Z. G. M.; MACHADO, I. C. Biologia da Polinização e da Reprodução de três Espécies de Combretum Loefl. (Combretaceae). Revista Brasileira de Botânica, v 24, n2, 181193, 2001. 33- RADFORD, A. E. et al.; Vascular Plant Systematics. New York: Harper & Row Publishers, 1974. 891 p. 34- RODRIGUES, I. A.; ANTUNES, L. R.; RODOVALHO, R. B. Perfis social, econômico e ecológico da área de influência da APA da Barra do Rio Mamanguape (PB): bases para a classificação e seleção de estabelecimentos rurais para gestão ambiental. In: RODRIGUES, G. S.; BUSCHINELLI, C. C. de A.; RODRIGUES, I. A.; MARCON NEVES, M. C. (Ed.). Avaliação de impactos ambientais para gestão da APA da Barra do Rio Mamanguape/PB. Jaguariúna: Embrapa Meio Ambiente, 2005. p. 39-73. 108 Revista SEB Ano 14 Final.indd 108 09/10/2012 13:44:07 Brazilian Journal of Ecology ISSN 1516-5868 35- SANTOS, M. J. L. & MACHADO, I. C. Biologia floral e heterostilia em Vismia guianensis (Aubl.) Choisy (Clusiaceae). Acta Botânica Brasílica 12 (suplemento):451-464, 1998. 36- SCARANO, F. R. Structure, function and florístic relationships of plant communities in stressful habitats marginal to the Brazilian Atlantic Rainforest. Annals of Botany, v. 90, p. 517-524, 2002. 37- SIGRIST, M. R.; SAZIMA, M. Ruellia brevifolia (Pohl) Ezcurra (Acanthaceae): fenologia da floração, biologia da polinização e reprodução. Revista Brasileira de Botânica, v. 25, p.35-42, 2002. 38- SIMPSON, B. B.; NEFF, J. L. Floral rewards: alternatives to pollen and nectar. Annual Missouri Botanical Garden, 68: 301-322, 1983. 39- SOUZA, V. C.; LORENZI, H. Botânica Sistemática: Guia ilustrado para identificação das famílias de angiospermas da flora brasileira, baseado em APG II. Ed Instituto Platarum, Nova Odessa, p.639, 2005 40- STEPHENSON, A. G. Flower and fruit abortion: proximate causes and ultimate functions. Annual Review of Ecology and Systematics, v. 12, p. 253-279, 1981. 41- SUTHERLAND, S. Why hermaphroditic plants produc many more flowers than fruits: experimental testes with Agave mckelveyana. Evolution, v. 4, n. 4, p. 750-759, 1987. 42- SUTHERLAND, S.; DELPH, L. F. On the importance of male fitness in plants; patterns of fruit-set. Ecology, v. 65, n. 4, p. 1093-1104, 1984. 43- SUGUIO, K.; TESSLER, M. G. Planícies de cordões litorâneos quaternários do Brasil: Origem e nomenclatura. In: LACERDA, L. D.; ARAÚJO, D. S. D.; CERQUEIRA, R.; TURQ, B. Restingas: Origem, estrutura e processos. Niterói: CEUFF, 1984. p. 15-26. 44- TABARELLI, M., L. P. Pinto, J. M. C. Silva & C. M. R. Costa. The Atlantic Forest of Brazil: endangered species and conservation planning. In: C. Galindo-Leal & I.G. Câmara (eds.). The Atlantic Forest of South America: biodiversity status, trends, and outlook. Center for Applied Biodiversity Science e Island Press, Washington, D.C, p.86-94, 2003. 45- TERBORGH, J. Maintenance of biodiversity in tropical forests. Biotropica, v. 24, p. 283-292, 1992. 46- VITALI-VEIGA, M. J.; & MACHADO, V. L. L. Entomofauna Visitante de Gleiditsia triacanthos L. – Leguminosae durante o seu período de floração. Revista Bioikos, v.15, n.1, p. 29-38, 2001. 109 Revista SEB Ano 14 Final.indd 109 09/10/2012 13:44:07 Brazilian Journal of Ecology ISSN 1516-5868 110 Revista SEB Ano 14 Final.indd 110 09/10/2012 13:44:07 Brazilian Journal of Ecology ISSN 1516-5868 Analysis of the landscape structure of the Coqueiral Environmental Protected Area, Coqueiral, MG Carolina Gusmão Souza - Universidade Federal de Lavras, Departamento de Ciências Florestais (email: carolinagusmaosouza@gmail.com) Rosângela Alves Tristão Borém - Universidade Federal de Lavras, Departamento de Biologia (email: tristao@dbi.ufla.br) Lisiane Zanella - Universidade Federal de Lavras, Departamento de Biologia (email: lisianezanella@gmail.com) Luis Marcelo Tavares de Carvalho - Universidade Federal de Lavras, Departamento de Ciências Florestais (email: passarinho@dcf.ufla.br) Rafaela Vidal Ambrosio - Universidade Federal de Lavras, Departamento de Biologia (email: rafavidalambrosio@yahoo.com.br). ABSTRACT This study analyzed the landscape structure of the Coqueiral Protected Area, located in southern Minas Gerais. We aimed to evaluate the landscape structure in the study area, based on landscape metrics and indicate priority areas for conservation. We use Geographic Information Systems and Remote Sensing tools to construct a land use map from a HCR SPOT 5 satellite image. Landscape structure analysis was carried out through Fragstats software and used landscape metrics. Results showed pasture class was considered as the landscape matrix and occupied almost half of the protected area. Landscape structure analysis showed the landscape is dominated by agropastoral activities. The landscape presented 704 units. Mean patch size area was higher for pasture than semideciduous forest, while semideciduous forest presented higher patch density. Land use classes showed complex shapes indicating higher edge effects. Pasture had the lower patch isolation. Data obtained in this study are relevant for decision making and environmental planning of the Coqueiral Protected Area, allowing suggest priority areas for conservation. Keywords: Landscape ecology, Landscape metrics, Geographic Information Systems. INTRODUCTION Over the past years, there have been profound technological, social, economic, and mainly, environmental modifications worldwide. Man-made modifications in the landscape have given rise to intense habitat fragmentation. The fragmentation of natural habitats has been defined by Metzger (1999), as a process of rupture in the spatial continuity of natural areas, thereby representing a serious threat to the maintenance of biological diversity. The transformation of these continuous areas has generated a landscape composed of natural vegetal remnants, split up into various patches that vary in size, shape, degree of isolation, and types of connectivity and environmental matrix (29). The fragmentation process in Brazil gained momentum from 1970 on, with essentially negative impacts on biodiversity, as confirmed by several authors, such as Primack & Rodrigues (2001) and Tabarelli & Gascon (2005). According to Metzger (2009), with the reduction into small, spaced out fragments, degradation in the Atlantic Rainforest biome has reached such a high degree, that, accord- 111 Revista SEB Ano 14 Final.indd 111 09/10/2012 13:44:07 Brazilian Journal of Ecology ISSN 1516-5868 ing to Tabarelli and Gascon (2005), the consequential alteration in natural ecosystems can be considered as the greatest threat to biodiversity. As has been shown by several authors, the deforestation of tropical forests has caused profound modifications in their respective ecosystems. The main consequences of fragmentation are increased edge-effects, habitat loss, alterations in ecological interactions and reproductive processes of various species, the isolation of vegetal formations, increased predation and competition, the loss of micro-habitats, the extinction of species, and the loss in biodiversity (3, 27, 30, 14). Within this context, landscape ecology could offer a contribution, since, according to Metzger (2001), the proposal of dealing with anthropic mosaics would be a way of understanding the occurrent human-induced structural and functional modifications in the landscape, as a whole. By way of landscape structure analysis and interpretation, it is possible to compile efficient information for the planning of an area, thereby making it possible to identify probable negative impacts, as well as seek solutions compatible with the ecological, socio-economical and cultural spheres (31). Information regarding the effects on landscape structure in tropical communities is still scarce, accounting for only 14% of published works (20) Therefore, it is of crucial importance, not only for developing the appropriate research, but also to better understand the fundamental patterns and processes of certain organisms. This would enable working on a local scale, since each area presents different landscape characteristics, whereby the need for ample knowledge on regional ecological relationships, contriving to facilitate a more efficient action for its gestation and conservation. In view of this need for understanding landscape structure, as a means of undertaking adequate measures for biodiversity conservation, the Coqueiral Environment Protection Area (EPA Coqueiral) was chosen for the study, since, as it deals with an established conservation unit, there is the required management structure to make the use, protection, conservation and monitoring of natural and socioeconomic resources of the area, feasible. OBJECTIVE The aim of this study was to analyze landscape structure and fragmentation in the Coqueiral Environmental Protection Area, as a means of supplying subsidies for the management of natural vegetal remnants, and to point out priority conservation areas. METHODOLOGY Study area The Environmental Protection Area (EPA) of Coqueiral is located in Coqueiral county, in the south of Minas Gerais State. Comprising 6.836,21 hectares in the Rio Grande basin in the micro-region of Lavras, it is partly surrounded by the lake formed by the Furnas reservoir, and the remainder by the counties of Boa Esperança, Aguanil, Campo Belo and Nepomuceno, between the geographic coordinates 45°19’37,5” and 45°26’16,3” longitude west and 21°03’52,7” and 21°09’30,8” latitude south (11). The main productive activities are coffee, cattle raising and small farms. The Coqueiral EPA, created on May 17th, 2002, occupies around 25% of the area of Coqueiral county. The income of the approximately 400 families that occupy the area is mainly based on coffee culture and cattle raising (8). As a large part is covered by shallow soils on a highly irregular relief, there are many restrictions to agricultural activities (13), therefore, there is a fundamental need for studies of the suitability and adequacy of land use, when attempting to conciliate an increase in the income of the population with environmental conservation. Study Area mapping Reconnaissance of the study area was the first step taken, followed by acquisition of a SPO5 satellite image, with 2,5m spatial resolution, encompassing the whole area of the county. The orthorectified image, acquired with radiometric preprocessing and geometric pattern (SPOTMAP), served as a base for mapping forest fragments, as well as land use and occupation. The three image bands used for visual interpretation, viz., the two visible and the panchromatic of the electromagnetic spectrum, referred to the green (0,5 to 0,6 μm), red (0,6 to 0,7 μm) and 112 Revista SEB Ano 14 Final.indd 112 09/10/2012 13:44:07 Brazilian Journal of Ecology ISSN 1516-5868 panchromatic (0,48 to 0,71μm) wave lengths. A ed in the field, accuracy being evaluated by the Kappa index. Confusion matrices were calculated false-color composite (RGB-12PAN) was used. Thematic vector graph maps were obtained by cross tabulation between the plans of matrix through Geo-referenced Information Processing information of image-derived land use, and data with SPRING 5.1.5. (5). Visual interpretation was from field sampling, according to the methodolthrough the simultaneous observation of recognition ogy described by Moreira (2003). Kappa index elements, such as tone, color, texture, shape, size pat- evaluation was with a table adapted from Landis tern, shade, and the association of available evidence, & Koch (1977) (Table 1). as described by Marchetti & Garcia (1997). Based on visual interpretation criteria, real use was mapped Table 1: Value for evaluating the degree of concoraccording to class, as follows: (i) Semidecidual sea- dance, starting from the Kappa index sonal forest: dense forest formations and gallery Kappa value Kappa value Concordance forest at the edge of streams, neglected/abandoned Poor < 0,20 < 0,20 fields; (ii) Cerrado: cerrado formations; (iii) CofWeak 0,21 – 0,40 0,21 – 0,40 fee: cultures at the non-productive Moderate 0,41 – 0,60 stage, i.e., under 0,41 – 0,60 3 years, and over three-years-old; Good 0,61 – 0,80(iv) Exposed rock: 0,61 – 0,80 Very good 0,81 – 1,00 0,81 – 1,00 areas with visible rock formation; (v) Pasture: areas of natural and formed pasture; (vi) Other cultures: areas with annual cultures in various stages of development; (vii) Other uses: urban areas and those with Landscape configuration Variables Variables Definition Definition improvements; (viii) Reforestation: areas set aside Landscape configuration, computed from Total area of the landscape (ha). Total area of the landscape (ha). A A foraplanting eucalyptus; and (ix) Water bodies: water toArea the type soil by(class) means landscape indices, Kappa value Concordance Area (ha) of the fragment ij. Iaijrefers the (ha)cover of offragment themap fragment ij. and Iofrefers j to to thethe number type ofoffragment fragments (cli ij Poor < 0,20 bodies, rivers,landscape. streams and reservoirs. was calculated with FRAGSTAS 3.3 (18) software. landscape. Weak 0,21 – 0,40 true features of the land Four were used, viz., (m) between twowere fragments, basedmetric on(m) theconfigurations between distance two between fragments, the edges basedarea, ofontwo thefragments distance aijs The Distance aijs con- Distance Moderate 0,41 – 0,60 calculated from the center of one pixel calculated to the center from of the another. center of one pixel to the center of another firmed by field visits. 500,61 points density, shape andGood proximity/isolation (28, 6, 33) – 0,80of each land-useTotal length of the edge (m) in the landscape Total length between of the fragments edge (m) type in i the and landscape k. between fragment e e ik were sampled using ik 0,81 –a1,00 class GPSMAP Garmin (Tables 2 and 3) Very good Distance (m) from fragment hijij to the Distance nearest fragment (m) fromoffragment the sameijtype to the of nearest habitat fragment (class), based of theo distance from edge to edge, and computed distance fromfrom cell-center edge to(pixel) edge, to andcell-center computed(pixel). from cell-center (pix Distance between the cells (pixels) ijrDistance (located between within the thefragment cells (pixels) ij) and ijrthe (located centroid within thefrag fra of the hijr hijr Variables ij, based on the distance cell center (pixel) ij,Definition based to celloncenter the distance (pixel).cell center (pixel) to cell center (pixel) Totalof areafragments of the landscape A Number of a(ha). determined type Number of habitat of fragments (class) iofinathe determined landscape. type of habitat (class) i in nij nij Area (ha) of the fragment ij. I refers to the type of fragment (class) and j to the number of fragments in the aij Proportion of the landscape occupied by Proportion fragmentsofofthe a determined landscape occupied class (i). by fragments of a determ Pi Pi landscape. of(m) thebetween fragment ij measured Perimeter number of the offragment cellthe(pixel) measured surfaces. by the pij pij basedby Distance two fragments, on the the distance between edgesij of two fragments, and number of cell (pi aijs Perimeter Represents metric that will Represents in athemetric formula that ofwill average, be calculated average inof the the formul area u xij xpixel ij be calculatedafrom the center of one to thecalculated center of another. standard deviance, and coefficient consideration, of variation. standard Total length of the edge (m) in the landscape between fragments type i and k. deviance, and coefficient of variation. eik consideration, Distance (m) from fragment tozthe nearestNumber fragment ofofthecells same(pixels) type of habitat based on of cells (pixels) in ijthe fragment ij. in the(class), fragment ij.the hij Number z hij hijr nij Pi pij Indicesx ij z distance from edge to edge, and computed from cell-center (pixel) to cell-center (pixel). Distance between the cells (pixels) ijr (located within the fragment ij) and the centroid of the fragment ij, based on the distance cell center (pixel) to cell center (pixel). Number of fragments of a determined type of habitat (class) i in the landscape. Proportion of the landscape occupied by fragments of a determined class (i). Perimeter of the fragment ij measured bySign the number and of cell (pixel) surfaces. Sign and Formula Formula Meaning Represents a metric that will Indices be interval calculated (unit) in the formula of average, average ofinterval the area (unit) under consideration, standard deviance, and coefficient of variation. Number of cells (pixels) in the fragment ij. CA>0 (ha) Class area (CA) Class area (CA) This is a measure of landscape composition. This is aHigh mea CA>0 (ha) CA values indicate matrix dominance. CA values ind 76CSx receiver, together with a TOPCON GPS RESULTS indices were obtained by means of points collect- This is of a measure of landscape composition. Higher classes land-use. By occupying 49,19% of the total Quantifies the proportional abundance Quantifies of each type the Percentage of Percentage precision receiver, hiper GGD model. All the of Sign and patch in the landscape. The interpretation patch of in PLAN the l thegeoinformation landscape in the landscape in Indices thus generated Formula Meaning was included in(unit) a occupation PLAND>0 (%) Land use and PLAND>0 (%) interval is the same as that described for CA, but is the expressed same as eachofclass each class bank geographic data. Visual interpretation hit It was possible to classify the area into nine percentages. percentages. (PLAND) (PLAND) CA>0 (ha) Class area (CA) Number of patchesPercentage (NP) of the landscape in each class Revista SEB Ano 14 Final.indd 113 (PLAND) NP = nj CA values This indicateismatrix dominance. a simple measure of the degreeThis of division is a simp 113 fragmentation. Higher NP≥1 values indicate fragmentation high NumberNP≥1 of = nj abundance of each type of theNP proportional (dimensional) (dimensional) fragmentation, and lower values landscape the unio fra patches (NP) Quantifies landscape patch in the landscape. The interpretation of PLAND or extinction of fragments of the same class. or extinction PLAND>0 (%) is the same as that described for CA, but expressed in 09/10/2012 percentages. 13:44:08 hijr nij Pi pij xij Brazilian Journal z Distance between the cells (pixels) ijr (located within the fragment ij) and the centroid of the fragment ij, based on the distance cell center (pixel) to cell center (pixel). Number of fragments of a determined type of habitat (class) i in the landscape. Proportion of the landscape occupied by fragments of a determined class (i). Perimeter of the fragment ij measured by the number of cell (pixel) surfaces. Represents a metric that will be calculated in the formula of average, average of the area under of Ecology standard ISSN 1516-5868 consideration, deviance, and coefficient of variation. Number of cells (pixels) in the fragment ij. Table 3: Indices of landscape ecology generated by FRAGSTATS (version 3.3) software for quantifying landscape structure Sign and interval (unit) Meaning Class area (CA) CA>0 (ha) This is a measure of landscape composition. Higher CA values indicate matrix dominance. Percentage of the landscape in each class (PLAND) PLAND>0 (%) Quantifies the proportional abundance of each type of patch in the landscape. The interpretation of PLAND is the same as that described for CA, but expressed in percentages. NP≥1 (dimensional) This is a simple measure of the degree of division or fragmentation. Higher values indicate higher landscape fragmentation, and lower values the union or extinction of fragments of the same class. Patch density (PD) PD>0 (number per 100 ha) Represents the number of fragments of the class in 100 hectares of landscape. The interpretation of PD is the same as that described for NP. Largest patch index (LPI) 0<LPI<100 (%) The highest value favors dispersers, pollinators and propagule dispersion, supplying smaller fragments. Average area fragmentation (AREA_MN) AREA_MN>0 (ha) Indicates the degree of fragmentation according to the number of fragments and the total area occupied by a certain class. Index of distance average shape from (SHAPE_MN) the nearest SHAPE_MN≥1 (adimensional) Lower values indicate a simple type ENN_MN≥0 fragmentation, thus beneficial for conservation. Indices Number of patches (NP) Average neighbor Average distance from (ENN_MN) the nearest neighbor (ENN_MN) Formula NP = nj ENN_MN≥0 (m) (m) of Lower values indicate fragment aggre Lower values indicate fragment aggregation. area (Figure 1), pasture was the predominant. Of the others, 28,95% of the area was covered by native vegetation (semidecidual seasonal forest and cerrado), 11,35% dedicated to coffee culture, 0,6% by other forms of culture, and 0,9% to reforestation, 6.836,21 ha, in total (Table 4). A small part of the EPA corresponds to water bodies, representing 5.67% of the total area. Of this, 5% is part of the Furnas lake inside the reserve limits, with 52.37% of preserved secondary forest. The Kappa accuracy index obtained in this classification was 95.75%. Analysis of landscape structure Through evaluating landscape indices, it can be seen that the four classes; pasture, coffeeClasses land-use culture, other cultures and of reforestation occupy an Coffee area of 4273.13 ha (CA), corresponding to 62.49% Cerrado Water bodies (PLAND) of the total area (Table 5). The landscape Semidecidual Seasonal Forest percentage index (LPI) shows that, whereas the Other Cultures Other Uses class Pasture ‘pasture’ occupies the largest fragment, i.e., Reforesting 114Exposed Rock Coffee Revista SEB Ano 14 Final.indd 114 Cerrado Classes of land-use Percentage 11,35% 1,52% 5,67% 27,46% 0,6% Figure 1: Map of land-use 0,75%and occupation of the Coqueiral EPA, 2010 49,19% 0,9% 2,56% Percentage 11,35% 09/10/2012 13:44:09 1,52% Brazilian Journal of Ecology ISSN 1516-5868 Table 4: Percentage of distribution in land-use in the Coqueiral EPA Classes of land-use asonal Forest Classes of land-use Coffee Classes of land-use Coffee Cerrado Cerrado Water bodies Water bodies Semidecidual Semidecidual Seasonal Forest Seasonal Other CulturesOther Cultures Other Uses Other Uses Pasture Reforesting Pasture Exposed RockReforesting Forest Exposed Rock Percentage Percentage 11,35% 11,35% 1,52% 1,52% 5,67% 5,67% 27,46% 27,46% 0,6% 0,6% 0,75% 0,75% 49,19% 49,19% 0,9% 2,56% 0,9% 2,56% Table 5: Landscape indices for the classes, land use and occupation Classes asses asonal Forest CA (ha) NP PD LPI(%) AREA_MN SHAPE_MN ENN_MN Water bodies 387,56 26 0 2,95 14,91 1,00 545,77 Pasture 3378,96 130 1,01 25,99 16,15 21,02 CA (ha) NPClasses PD LPI(%) 17,99 AREA_MN CA (ha) NPSHAPE_MN PD LPI(%) ENN_MN ARE Semidecidual Seasonal Forest 1844,01 265 2,06 2,45 6,96 6,11 38,24 387,56bodies 26 50,870 102 2,95 14,91 Other culturesWater 0 0 387,56 0 26 1,84 0 1,00 280,782,95 545,77 3378,96 Pasture 130 776,17 1,01 83 17,99 25,99 1,0116,15 17,99 21,02 Coffee 0 0 3378,96 9,35 130 2,26 184,20 Other uses 1844,01 52,46 Forest 25 0 0 1844,01 2,1 265 1,88 489,122,45 38,24 Semidecidual 265Seasonal 2,06 2,45 6,96 2,06 6,11 Reforestation 67,13 26 0 0 2,58 2,37 398,8 Other 50,87cultures 102 0 0 50,87 0 102 0 1,84 0 280,78 Cerrado 103,72 13 0 0 7,98 2,92 492,84 776,17 83 175,290 34 9,35 Exposed rockCoffee 0 0 0 776,17 5,16 83 2,92 0 2,26 168,98 0 184,20 Other 52,46uses 25 0 17,99%, the class ‘semidecidual seasonal forest’ Reforestation 67,13 26 0 represents only 2,45%, much like that of the class Cerrado 103,72 0 ‘water bodies’, with 2,95% . 13 The entire landscape was composed Exposed 175,29 rock 34 0 of 704 patches distributed among the different classes of land-use. The most outstanding, with the largest number of fragments, were semidecidual seasonal forest, with 265 patches, and pasture with 130. The classes ‘other cultures’ and ‘coffee’ were also significantly represented, with 102 and 83 patches, respectively. The class ‘cerrado’ was almost inexpressive, with only 13 patches, adding up to 103.72 ha, throughout the entire landscape. The classes of use that presented the smallest average sizes (AREA_MN) were those that presented the highest patch density (PD). They were: pasture (AREA_MN = 25.99; PD = 1.01 fragments|100 ha) and semidecidual seasonal forest (AREA_MN = 6.96; PD = 2.06 fragments|100 ha (Table 5).) 0 52,462,1 25 0 1,88 According to shape indices (SHAPE_ 0 67,13 2,58 26 0 2,37 MN), on a whole, landscape patches were of the 0 complex 103,72 7,98 13 shapes,0 as2,92 most and irregular clearly shown values for the34 different types of land 0 by the175,29 5,16 0 2,92 use. Fragment irregularity in the class semidecidual seasonal forest was the highest at 2.23 (Table 5), although ‘cerrado’ was also high (1.95). Whereas only the classes ‘water bodies’ (1.0) and ‘other cultures’ (1.84) presented simple regular-shaped patches, the remainder were more complex-shaped, with results over 2. The average distance from the nearest neighbor (ENN_MN) (Table 5) differed in the various classes. The lowest values were ‘pasture’ with 21.02 m and semidecidual seasonal forest with 38.24 m, a clear indication of intense clustering in both. On the other hand, through presenting few fragments (n=13), at 492.84, the ENN_MN for the class ‘cerrado’was extremely high. 0 0 0 0 489,12 398,8 492,84 168,98 115 Revista SEB Ano 14 Final.indd 115 09/10/2012 13:44:09 Brazilian Journal of Ecology ISSN 1516-5868 DISCUSSION Land use and occupation The analysis of land use and occupation indicated that, overall the landscape was mainly dedicated to agro-pastoral activities, such as pasture and coffee growing. Pasture covered the largest part of the EPA (49.19%), thus confirming cattle breeding to be the main local economic activity. Coffee culture, run on a family basis and occupying 11.35%, was another important economic source, with a large number of people depending on this activity for a livelihood. Other agricultural activities, such as ‘other cultures’ and reforesting, occupied smaller areas of the landscape, to a total of 1.5%. Donald (2004) stated that agricultural activities constituted the main threat towards maintaining biodiversity in the tropics. Areas of native vegetation are distributed throughout the EPA in the form of small and middlesized fragments. This very patchy landscape poses a grave risk for species extinction (22), through the consequential changes in both the micro-climate and fragment physical structure, and the reduction in environmental heterogeneity, thereby inducing lower local biodiversity (32). By crossing field data, it was possible to analyze the outcome of visual classification using the Kappa index (16), based on the construction of error or contingency matrices. The Kappa accuracy index obtained in this classification was 95.75%, which, according to Landis & Koch, is an excellent result. According to field observation, areas dedicated to farming are very often badly conserved, due to inadequate, and, in most cases, badly planned management, thereby posing a serious problem for populations that depend on this as their source of income. This dependency could also account for the low percentage of semidecidual seasonal forest and cerrado, since, as a means of increasing production, areas set aside for permanent preservation are very often used as a means of increasing production. Analysis of landscape structure According to landscape evaluation indices, agro-pastoral activities, viz., pasture, coffee culture, other cultures and reforestation, were predominant. Similar results were obtained by Tonial (2003), with 47.19% of the area with pasture, and by Valente & Vettorazzi (2005), who allocated between 2% and 4% for native vegetation in a study area in a region of São Paulo State. This further corroborates the thesis that, the predominance of agricultural activities in the EPA landscape, by hindering local forest remnant conservation, is detrimental to local biodiversity. The similar results encountered in other sustainable-use conservation units (2005), clearly show that, in a large part of these areas, consecration to agro-pastoral activities interferes with local environmental conservation. . By inference, on analyzing the number of landscape patches, and based on occupied area, although the class semidecidual seasonal forest notably presented a higher number of fragments than pasture, these were distributed in smaller-sized patches. Thus, by pasture occupying an appreciably larger area, the notion of landscape agricultural predominance was confirmed. According to Tabarelli & Gascon (2005), high forest fragmentation diminishes its biodiversity. The average size of patches (AREA_ MN) is considered a trustworthy indication of the degree of fragmentation, when considering the number of fragments and the total area occupied by natural vegetation (18, 17). When evaluated together with patch density (PD), the different aspects of a landscape, including forest fragmentation, become comprehensible, thereby facilitating the formation of a profile of the prevailing degree of this feature. Patch density values were similar to those encountered by Oliveira (2000), i.e., 3.3 fragments per 100 ha, for fragments with an average size of 1.7 ha, when evaluating a landscape with highly fragmented semidecidual seasonal forest, and by Valente & Vettorazzi (2005), in hydrographic basin landscapes. In her study area, the first author encountered the following results: sub-basins of the Mid Corumbataí (AREA_MN = 2,1 ha; PD = 3,35 fragments/100 ha); the Lower Corumbataí (AREA_MN = 3,2 ha; PD = 2,88 fragments/100ha), and the Ribeirão Claro (AREA_MN = 3,5 ha; PD = 2,48 fragments/100ha), whence the conclusion of intense landscape fragmentation. According to land-use, shapes were very irregular, mainly so in the case of semidecidual 116 Revista SEB Ano 14 Final.indd 116 09/10/2012 13:44:09 Brazilian Journal of Ecology ISSN 1516-5868 seasonal forest fragments. According to Forman (1997), in relation to diversity and sustainability, the analysis of forest fragment shape is as important as size, since the more irregular the fragment, the more susceptible it is to the edge-effect, especially so in the case of smaller areas, due to their higher interaction with the matrix (7). With the increase in edgeeffect, there is a proportional reduction in fragment nuclear area, which, over short, medium or long term, will possibly have an effect on the structural quality of the ecosystem, as a whole. Tonial (2003) arrived at the same results, with 2.40 for the same class, whereas in the case of Calegari et al. (2010), the distinct results revealed more regular-shaped fragments. Apparently, higher shape-complexity indicates a higher level of disturbance, as a result of greater interaction with the matrix, through the increase in the area subject to the edge-effect (23). According to the Almeida (2008) classification, used here for evaluating the average distance from the closest neighbor, distances between patches of 60, 120, 200 and >200 m were classified as low, medium, high, and very high isolation, respectively. Thus, for the landscape studied, isolation in the classes semidecidual seasonal forests and pasture was low, and for the remainder very high. Distinct results were encountered by Calegari et al. (2010), Basile (2006) and Tonial (2003) for the area ‘natural vegetation, with distances of 244.5, 410 and 119 m, respectively. Valente & Vettorazzi (2005) came up with similar results for ‘cerrado’, with 156.65 m. Thus, the results indicate the lower commitment of the class semidecidual seasonal forest, by demonstrating the small inter-fragment distances of this class, and the higher capacity of the species for colonization towards forest patches, thus an inducement to local genic flow (32). According to some authors, the construction or maintenance of biodiversity corridors is an important mitigatory measure for perpetuating connectivity between vegetal fragments, through facilitating the creation of a system of meta-populations (10, 24). CONCLUSIONS The use of geographic information systems has facilitated the generation and organization of geo-referenced information, in such a way as to enable the characterization and analysis of the structural elements of the EPA Coqueiral landscape, with its mosaic of semidecidual seasonal forest and cerrado remnants. The use of a land-use and occupation map facilitated the characterization and quantification of areas of the different types of use, as well as quantification of the number of natural vegetal fragments (semidecidual seasonal forest and cerrado) of the Coqueiral EPA. Even so, landscape ecology indices were still required for characterizing their composition and configuration. The groups of indices that proved to be efficient for this characterization were area, density, size, shape, proximity and isolation, and connectivity. In the study region, there is a tendency for agropastoral activities in small rural properties. These activities account for the high regional fragmentation. The maintenance of the small fragments in the EPA is fundamental, as they are liable for connectivity between natural vegetal remnants, and for conservation of the larger-sized fragments, thereby aiding in the persistence of local species. Restoration of EPAs is obviously necessary, since this type of vegetation can function as ecological corridors, thereby facilitating the movement of fauna and flora. Furthermore, EPAs can also contribute towards the socio-economic potential of the community, if economically important species, such as fruit plants, are used. . In regards to conservation, through harboring greater biodiversity, the largest-sized fragments should be considered as priority. The construction of vegetation corridors should be considered as a means of increasing interfragment connectivity, as well as metapopulation auxiliary systems, within the EPA. ACKNOWLEDGEMENT We wish to extend our thanks to the Universidade Federal de Lavras, and the Geosoil Laboratory, Epamig/Lavras for support and incentives, as well as to CAPES for the grant and FAPEMIG for financing the project. 117 Revista SEB Ano 14 Final.indd 117 09/10/2012 13:44:09 Brazilian Journal of Ecology ISSN 1516-5868 RESUMO Este trabalho analisou a estrutura da paisagem da Área de Proteção Ambiental Coqueiral, localizada na região Sul de Minas Gerais. O objetivo foi avaliar a estrutura da paisagem a partir de métricas e princípios da Ecologia da Paisagem e apontar áreas prioritárias para a conservação. Foram utilizados Sistemas de Informação Geográfica e Sensoriamento Remoto para elaborar um mapa de uso da terra a partir de uma imagem de satélite SPOT 5 HCR. A análise da estrutura da paisagem foi realizada através do software Fragstats, utilizando métricas de paisagem. Os resultados mostraram que a classe pastagem foi considerada como a matriz da paisagem e ocupou quase metade da unidade de conservação. A análise da estrutura da paisagem mostrou que a paisagem é dominada por atividades agropastoris. A paisagem apresenta 704unidades. O tamanho médio dos fragmentos foi maior para o pasto do que para a floresta estacional semidecidual, enquanto que a floresta estacional semidecidual apresentou maior densidade de fragmentos. Classes de uso da terra mostraram formas complexas indicando maiores efeitos de borda. Pastagens apresentaram menor isolamento entre os fragmentos. Os dados obtidos neste estudo são relevantes para a tomada de decisão e planejamento ambiental da Área de Proteção Ambiental de Coqueiral, permitindo sugerir áreas prioritárias para sua conservação. Palavras-chave: Ecologia de paisagens, Métricas da paisagem, Sistemas de Informação Geográfica. REFERENCES 1- ALMEIDA, C. G. Análise espacial dos fragmentos florestais na área do Parque Nacional dos Campos Gerais, Paraná.2008. 72 f. Dissertação (Mestrado em Gestão do Território) – Univ. Estadual de Ponta Grossa, Ponta Grossa, 2008. 2- BASILE, A. Caracterização estrutural e física de fragmentos florestais no contexto da paisagem da Bacia do Rio Corumbataí, SP. 2006. 86 p. Dissertação (Mestrado em Ecologia Aplicada) – Univ. de São Paulo, Piracicaba, 2006. 3- BIERREGAARD, R. O.; LOVEJOY, T. E.; KAPOS, V.; SANTOS, A. A.; HUTCHINGS, R. W. The biological dynamics of tropical rainforest fragments. Bioscience, Washington,v. 42, n. 1, p. 859-866, 1992. 4- CALEGARI, L.; MARTINS, S. V.; GLERIANI, J. M.; SILVA, E.; BUSATO, L. C. Análise da dinâmica de fragmentos florestais no município de Carandaí, MG, para fins de restauração florestal. Revista Árvore, Viçosa, MG, v. 34, n. 5, p. 871-880, 2010. 5- CAMARA, G. et al. Spring: Integrating remote sensingand GIS by object-oriented data modelling. Computers & Graphics, New York, v. 20, n. 3, p. 395-403, 1996. 6- CARVALHO, F. M. V.; MARCO-JÚNIOR, P. D.; FERREIRA, L. G. The cerrado into-pieces: Habitat fragmentation as a function of landscape use in the savannas of central Brazil. BiologicalConservation, Boston, v. 142, n. 7, p. 1392-1403, 2009. 7- CEMIN, G.; PERICO, E.; REMPEL, C. Composição e configuração da paisagem da sub-bacia do Arroio Jacaré, Vale do Taquari, RS, com ênfase nas áreas de florestas. RevistaÁrvore, Viçosa, MG, v. 33, n. 4, p. 705-711, 2009. DONALD, P. F. Biodiversity impacts of some agricultural commodity production systems. ConservationBiology, Boston, v. 18, n. 1, p. 17-37, 2004. 8- EMPRESA DE ASSISTÊNCIA TÉCNICA E EXTENSÃO RURAL DE MINAS GERAIS EMATER. Área de proteção ambiental do município de Coqueiral. Belo Horizonte, 2002. 9- FORMAN, T. T. Land mosaics: the ecology of landscapes and regions. New York: Cambridge University, 1997. 632 p. 10- FORMAN, R. T. T.; SPERLING, D.; BISSONETTE, J. A.; et al. Road ecology: science and solutions. Washington: Island Press, 2003. 481 p. 11- INSTITUTO BRASILEIRO DE GEOGRAFIA E ESTATÍSTICA. Cartografia. Rio de Janeiro, 2010. Disponível em: <http://www.ibge.gov. br/home/geociencia /cartografia/default.shtm> Acesso em: 26 out. 2010. 12- LANDIS, J.; KOCH, G. G. The measurements of agreement for categorical data. Biometrics, Washington, v. 33, n. 3, p. 159-179, 1977. 13- LIMA, V. M. P. Qualidade estrutural e intervalo hídrico ótimos de solos cultivados em área de proteção ambiental do sul de Minas Gerais. 2008. 85 f. Dissertação (Mestrado em Ciências do Solo) – Univ. Federal de Lavras, Lavras, 2008. 118 Revista SEB Ano 14 Final.indd 118 09/10/2012 13:44:09 Brazilian Journal of Ecology ISSN 1516-5868 14- LINDENMAYER, D. B.; HOBBS, R. J.; DRAKE, R. M.; et al. A checklist for ecological management of landscapes for conservation. EcologyLetters, Oxford, v. 11, n. 1, p. 78-91, 2008. 15- MARCHETTI, D. A. B.; GARCIA, G. J. Princípios de fotogrametria e fotointerpretação. São Paulo: Nobel, 1996. 264p. 16- MOREIRA, M. A. Fundamentos do sensoriamento remoto e metodologias de aplicação. São José dos Campos: INPE, 2003. 307p 17- MCGARIGAL, K.; CUSHMA, S. A.; NEEL, M. C.; ENE, E. Fragstats: spatial pattern analysis program for categorical maps. Amherst: University of Massachusetts, 2002. 18- MCGARIGAL, K.; MARKS, B. J. Fragstats: spatial patterns analysis program for guantifiying landscape structure. Portland: Pacific Northwest Research Station, 1995. 122p. 19- METZGER, J. P. Editorial conservation issues in the Brazilian Atlantic forest. Biological Conservation, Boston, v. 142, n. 6, p. 1138-1140, 2009. 20 -METZGER, J. P. Landscape ecology: perspectives based on the 2007 IALE world congress. LandscapeEcology, Dordrecht, v. 23, n. 5, p. 501-504, 2008. 21- METZGER, J. P. O que é ecologia de paisagens? Biota Neotropica, Campinas, v. 1, n. 1-2, p. 1-9, 2001. 22- METZGER, J. P.Estrutura da paisagem e fragmentação: análise bibliográfica.Anais da Academia Brasileira de Ciências,Rio de Janeiro, v.71, n.3, p.445-463, 1999. 23- NASCIMENTO, M. C.; SOARES, V. P.; RIBEIRO, C. A. A. S.; SILVA, E. Mapeamento dos fragmentos de vegetação florestal nativa da Bacia hidrográfica do rio Alegre, Espírito Santo, a partir de imagens do Satélite Ikonos II. Revista Árvore, Viçosa, MG, v. 30, n. 3, p. 389-398, 2006. 24- NG, S. J.; DOLE, J. W.; SAUVAJOT, R. M.; et al. Use of highway undercrossings by wildlife in southern California. BiologicalConservation, v. 115, p. 499-507, 2004. 25- OLIVEIRA, E. M. Caracterização e qualidade ambiental em dois fragmentos florestais na perspectiva da conservação de Alouatta guariba (Humboldt, 1812) no interior do Estado de São Paulo. 2009. 93 f.Tese (Doutorado em Ciências) - Universidade Federal de São Carlos, São Carlos, 2009. 26- OLIVEIRA, L. T. Fragmentos de floresta Atlântica Semidecidual no município de Lavras: uma comparação ecológica entre a cobertura atual e a cobertura exigida pela legislação. 2000. 103 f. Monografia (Graduação em Engenharia Florestal) – Universidade Federal de Lavras, Lavras, 2000. 27- Primack, R. B.; Rodrigues, E. Biologia da conservação.Londrina: Viva, 2001. 328p. 28- RIBEIRO, M. C.; METZGER, J. P.; MARTENSEN, A. C.; PONZONI, F. J.; HIROTA, M. M. The Brazilian Atlantic Forest: how much is left, and how is the remaining forest distributed? Implications for conservation. Biological Conservation, Boston, v. 142, n. 6, p. 1141-1153, 2009. 29- SAUNDERS, D.A.;HOBBS R.J.;MARGULES, C. R. Biological consequences of ecosystem fragmentation: a review. Conservation Biology, Essex, v. 5, n. 1, p. 18-32, 1991. 30- SILVA, W. G. S. METZGER, J.P..; SIMÕES, S.; SIMONETTI, C. Relief influence on the spatial distribution of the Atlantic Forest cover at the Ibiúna Plateau, SP. BrazilianJournalofBiology, Rio de Janeiro, v. 67, n. 3, p. 403-411, 2007. 31- SOUZA, C. G. Caracterização Ambiental e Análise da Estrutura da Paisagem da Área de Proteção Ambiental de Coqueiral, Minas Gerais. 2011. 119 f. Dissertação (Mestrado em Ecologia Aplicada) – Universidade Federal de Lavras, Lavras, 2011. 32- TABARELLI, M.; GASCON, C. Lições da pesquisa sobre fragmentação aperfeiçoando políticas e diretrizes de manejo para a conservação da biodiversidade. Megadiversidade, Belo Horizonte,v. 1, n. 1, p. 181-188, 2005. 33-TONIAL, T. M. Dinâmica da paisagem da região nordeste do Estado do Rio Grande do Sul. 2003. 311 f. Tese (Doutorado em Ecologia e Recursos Naturais) - Universidade Federal de São Carlos, São Carlos, 2003. 34-VALENTE, R. O. A; VETTORAZZI, C. A. Avaliação da estrutura florestal na Bacia do Rio Corumbatai, SP. ScientiaForestalis (IPEF), Piracicaba, v. 68, p. 45-57, 2005. 119 Revista SEB Ano 14 Final.indd 119 09/10/2012 13:44:10 Brazilian Journal of Ecology ISSN 1516-5868 120 Revista SEB Ano 14 Final.indd 120 09/10/2012 13:44:10 Brazilian Journal of Ecology ISSN 1516-5868 MACROALGA SPECIES RICHNESS IN CONSOLIDATED ARENITE SUBSTRATA AND REEF-POOLS WITH SANDY BOTTOMS AT BEACHES IN PIAUÍ. Voltolini1, J.C; Batista2, M.G.S; Nascimento3, E.F.I.; Campos2, K.C.G.C.; Resende4, J.S.S.; Machado5, R.A.; Souza6, L.O.; De Oliveira7, D.; Paiva-Silva8, K.; Lopes-Filho3, E.S. 1 – Group on Research and Teaching in Conservation Biology (ECOTROP), University of Taubaté. 2 - Department of Biology, IB-UESPI, Teresina, PI. 3 - Department of Ecology, IB-USP. 4 - Biologist, Environmental Council. Teresina, PI. 5 – Member of the City Council of Parnaíba (PI), Environmental Vigilance. 6 - Souza & Silva Assessors, Parnaíba. 7 - UFPI, Aberra do Piauí University. Buriti dos Lopes, PI. 8 – Ilha Ativa Committee (CIA), Ilha Grande. ABSTRACT Sessile-organism dependence on substrate structure is capable of conducing, both the manner in which biological communities colonize new environments, as well as richness and abundance patterns. Comparison of the frequency of macroalga species frequency on two beaches in Piauí (northeastern Brazil), was the means of testing the hypothesis that species richness would be higher on a rocky (Barra Grande) than sandy (Coqueiro) beach. Of the 21 macroalga species recorded, most revealed low occurrence, with Hypnea spinella and H. musciformis as those predominant. Whereas all were recorded on the Coqueiro beach, only 7 were on the Barra Grande. Hence, our hypothesis remained unproven. Nonetheless, as Barra Grande beach is subject to a more intense human impact than Coqueiro, this could vindicate this pattern. Keywords: Landscape ecology, Landscape metrics, Geographic Information Systems. Introduction Benthonic coastal ecosystems, which comprise one of the most productive marine environments, planet-wide, present high richness in organisms of outstanding ecological and economic importance, such as mussels, oysters, crustaceans and fishes, as well as various seaweeds which play an important ecological role by supplying oxygen, food, shelter and substratum, while at the same time functioning as nurseries for various organisms at several trophic levels in the food chain (Batista, 2011). Marine algae are ephemeral or perennial benthonic organisms, which live attached, consolidated or not, to solid substrata. The richest areas in macroalgae, both in diversity and biomass, are rocky shores, rocky beaches and reefs (Oliveira et al., 2001). The distribution of seaweeds along the Brazilian coast is a result of the complex interaction of factors, such as substratum availability, the presence of fresh water flows, biotic interactions, water mass characteristics, and historical and biogeographical factors (Oliveira et al., 2001). Brazil, considered as the country with the highest biodiversity planet-wide (Bicudo & Shepherd, 1998), possesses a coastline which extends from the tropics to regions of warm-temperate waters. The great challenge is diversity and conservation quantification. In the case of benthonic marine algae, Oliveira Filho (1977), when compiling the first Brazilian infrageneric taxa, listed 327 Rhodophyta, 113 Chlorophyta and 64 Phaeophyta, 504 species, all told. Subsequently, Horta et al. (2001), when updating the data base on 121 Revista SEB Ano 14 Final.indd 121 09/10/2012 13:44:10 Brazilian Journal of Ecology ISSN 1516-5868 Brazilian alga diversity, listed 642 taxa, distributed among 388 Rhodophyta, 166 Chlorophyta and 88 Phaeophyta. According to more recent research, there are 774 infrageneric taxa, corresponding to 482 Rhodophyta, 191 Chlorophyta and 101 Phaeophyta (Fujii et al.,2008), with at least 700 species among coraline reefs alone (Figueiredo et al., 2008). The Brazilian southeast is the most studied region. On the other hand, whereas in the north and northeast the flora is somewhat better-known in states such as Bahia and Pernambuco, this is not the case in others, such as Sergipe, Alagoas, Piauí, Pará and Amapá. This is a direct reflection on the fewer species known in these regions in comparison to the southeast. Notwithstanding, the extent of each state must be taken into account, when comparing these numbers (Fujii et al., 2008). In spite of the large diversity of Brazilian marine macroalgae, most studies have mainly focused on either the morphological, biochemical or systematic aspects, or associated invertebrate fauna. To date, few studies have been dedicated to information on certain aspects of Brazilian macroalgae, such as community ecology (Oliveira Filho & Ugadim, 1976; Pedrini et al., 1989; Gestinari et al., 1998; Yokoya et al., 1999; de Paula et al., 2005; Amado Filho et al., 2006; Figueiredo et al., 2008; and Marins et al., 2008), populations (Guimaraens et al., 1996; Yokoya et al., 1999; Amado Filho et al., 2006; Loureiro & Reis 2008; and Marins et al., 2008 {although many of these studies have mainly dealt with communities, there is also information on the ecology of populations}), succession (Eston et al., 1992), and conservation (Figueiredo et al., 2008). Worthy of note; most of the cited studies of communities are really botanic surveys without registration of factors which might interpret those processes linked to community structure and dynamics. Published studies on macroalga population dynamics are almost non-existent. At the same time, the Brazilian coast presents problems of pollution and the invasion by exotic species, whereby the need for further studies of marine microalgae conservation. Through floristic surveys on macroalgae over the last decade along the Piauí coast, it can be assumed that this presents a characteristic tropical region flora (Batista, 2011), which is undergoing gradual alteration, since banks of Sargassum were visibly encountered, and nowadays Gracilaria have become perceptibly predominant. The coastline of the state of Piauí, the smallest along the Brazilian coast, with only 66 km in extent, to a large degree corresponds to a strip of recently formed sediments associated to a series of islands, basins and channels, all along the coastline, with sand bars, dunes, mangroves and some cliffs (Santos-Filho, 2009), all of which subject to the expressive influence of the Parnaíba delta. In spite of the observed richness in biodiversity, and being an Environmental Protection Area (EPA), there are few studies of the local algae. The Coqueiro and Barra Grande beaches are both located along the Piauí coast. The former, in Luiz Correia county, is mainly characterized by its rocky formation, propitious for the development of seaweeds and well-protected from wave-motion, thus ideal for the formation of microhabitats (Batista, 2011), whereas the latter, in Cajueira da Praia county, is noted by rocky formation intercalated with sandy pools. There is a certain degree of anthropic occupation in both, which, together with biotic and abiotic attributes, exert an influence on local floral composition. Objetive The aim was to compare the number of macroalgae species on consolidated arenite substrata, as well as in sandy-bottom reef pools along the beaches of Piauí. Our hypothesis was that species richness would be higher on that with a consolidated substratum, which would be more stable for the fixing and establishment of seaweeds, as a whole. Methodology Study site Alga samples came from two locations on the Piauí coast. The Barra Grande district is located in the northern part of the state of Piauí (02º55’40” S and 41º24’40” W), in Cajueiro da Praia county. The 4-km-long beach, containing the mouths of four major rivers, viz., Timonha, Ubatuba, Camurupim and Cardoso, is mainly formed by associations of 122 Revista SEB Ano 14 Final.indd 122 09/10/2012 13:44:10 Brazilian Journal of Ecology ISSN 1516-5868 marine and continental quartz sands, together with mangroves, all part of a transition coastal ecosystem between marine and terrestrial environments. In the case of Barra Grande beach, there is a consolidated arenite substratum below the high tide mark (PIAUÍ, 1996). The climate is alternatively humid|dry tropical, with the dry period lasting six months, and an average temperature between 25 ºC and 32 ºC (CEPRO, 1990). On an average, the sand contains 10-30cmsized fragments of consolidated segment (’rocks’), water temperature is 30ºC, and salinity 35ppm. The distance between the collecting station and the water-line was 530m. Collections took place on August 19th, 2012 (0.1 tide at 11:0 0 a.m.). Coqueiro Beach, situated in Luís Correia county (02º54’35” S and 41º32’03” O), with a high flow of tourists, is characterized by rocky outcropping harboring a rich biodiversity. The local climate is alternatively humid|dry tropical, with an average temperature between 25ºC and 32º, and the characteristic vegetation of dunes and restinga (CEPRO, 2001). The sand is fine. Water temperature at the time was 28ºC and salinity 35ppm. The distance between the collecting station and the water-line was 5 km. Collections took place on August 20th, 2012 (0.2 tide at 11:30 a.m.). Sampling planning Seaweeds were first collected all along the reef of the two beaches chosen for the study. A species list was compounded after species identification. A 10mx10m grid with 200 quadrates (parcels) of 50cmx50cm was set up (Figure 1). 10 parcels of 50cmx50cm were raffled, using a random-number table. Seaweed-species collected within each parcel were then registered. Specimens were individually identified by species on the spot. In the case of doubt, subsequent laboratory identification was carried out at the Piauí State University (UESPI). As a means of comparing the two parcels, calculations of the percentage of those containing each seaweed species, as well as the Jaccard similarity index (Sj), were carried out. An estimate of species richness was calculated through the Chão 1 method on Estimate S software. Results 21 seaweed species were registered on the two beaches. Whereas all the species were present on Coqueiro Beach, only 7 were on Barra Grande (Table 1; Figures 2 and 3). Similarity between the two communities was only % (Sj=0,29). Hypnea spinella was the only species present in all the ten parcels at both sights, whereas the species Hypnea musciformis was only present in all the parcels in Coqueiro Beach (Figure 3). Most of the species were present in less than 50% of the parcels, 16 (76% of the 21 species) in Coqueiro Beach, and 6 (86% of the 7 species) in Barra Grande. Richness estimates showed Coqueiro Beach to be richer than Barra Grande, the latter proving to be a poorer and more homogeneous system (Figure 4). Furthermore, the number of species at both sites having already reached stabilization, with a little more than half of the sampling effort having been employed, was a clear indication that the number of parcels was sufficient for estimating richness. Figure 1 – Parcels, one at Barra Grande Beach with fragments of consolidated sediment (left), and the other at Coqueiro Beach with fine sand (right). Revista SEB Ano 14 Final.indd 123 Chlorophyta Acetabularia calyculus Acetabularia crenulata Barra Grande X Coqueiro X X 123 09/10/2012 13:44:10 Brazilian Journal of Ecology ISSN 1516-5868 Chlorophyta Acetabularia calyculus Acetabularia crenulata Caulerpa mexicana Cladophora membranacea Enteromorpha muscoides Ulva fasciata Ulva lactuca Valonia aegagropila Barra Grande X X Phaeophyta Dictyopteris delicatula Dictyota menstrualis Padina gymnospora Rhodophyta Acanthophora spicifera Gelidiella acerosa Gracilaria birdiae Gracilaria domingensis Haloplegma duperreyi Hypnea musciformis Hypnea spinella Jania subulata Laurencia dendroidea Palisada perforata Coqueiro X X X X X X X X X X X X X X X X X X X X X X X X X X Figure 2 – Illustration of the seaweed species registered on the beaches of Coqueiro and Barra Grande. Figure 3 – Percentage of parcels containing each of the seaweed species sampled in the beaches of Coqueiro and Barra Grande in Piauí. 124 Revista SEB Ano 14 Final.indd 124 09/10/2012 13:44:10 Brazilian Journal of Ecology ISSN 1516-5868 Figure 4 – Estimates of species richness (S) at the beaches of Barra Grande and Coqueiro. Discussion Macroalga diversity is directly related to environmental conditions, especially to the type of substratum available for spore fixation, and the quality of the water. The various reproduction strategies function in combination with high spore dispersion ability, and the capacity for regeneration, as well as certain aspects of intra and inter-specific competition, thereby very often facilitating rapid substratum colonization, both organic or inorganic and natural or artificial. In reef ecosystems, seaweeds occur upon a large number of species that are fixed on the various substrata, such as shells, corals and other algae (Dorigo et al., 2005). Hence, reef substrata are eminently appropriate for the fixation of spores, and consequently, the efficient development of grasps. Nonetheless, the initial hypothesis remained unproven, since a larger number of macroalga species were registered on Coqueiro Beach, where the substratum is sandy. This pattern was the contrary to those encountered by other authors. In a Papua New Guinea study, less alga cover, richness and abundance was registered on arenite substrata with marine monocotyledon banks (Heijs, 1987). In the Antarctic, less seaweed cover (Richardson, 1979) and biomass (Quartino et al., 2001) was also observed on arenite substrata. In the Baltic Sea, Russia, there was accumulation on the bottom of the Neva estuary, due to human drainage and sand filling, with the con- sequential lessening of seaweed biomass (Gubelit, 2012). In Brazil, the patterns encountered by Aquino (2012) in Ceará, were also substratum formation in the form of sandy reefs. On comparing the beaches of Flexeiras and Manguinhos, Trairi county, it was noted that reef heterogeneity exerted an influence on seaweed distribution, with Manguinhos presenting higher species richness than Flexeiras. Pollution, brought about by the direct release of home and industrial pollutants onto beaches via river courses and the movement of shipping along the coast, can be cited among the main factors contributing to the decrease in marine diversity (Oliveira et al., 2011). At Barra Grande, there is a greater flux of both people and boats throughout the year, when compared to Coqueiro, which is situated in a region where summer tourism predominates, thereby undergoing less yearly impact. Furthermore, Barra Grande is subject to the influence of four main rivers, viz., Timonha, Ubatuba, Camurupim and Cardoso, as well as mangroves (CEPRO, 1990), with the consequential inducement of low species richness through the impact of fresh water. Conclusion Species richness was greater at Coqueiro Beach, with more sand, than at Barra Grande Beach, which, although with more rocks, is subject to higher human impact. At Barra Grande, there is the adverse influence of four rivers and an inappropriate substratum for fixation in the case of most species. It is also possible that, depending on tide and wind conditions, those consolidated are also subject to rolling and abrasion. On the other hand, at Coqueiro Beach, salinity is probably stable and the substratum more appropriate for seaweed fixation (consolidated sandy rocks). In this case, the sandy bottom represents a sand deposit, with seaweed stems possibly being fixed below the sand on the hard substratum. Acknowledgement The present study was developed as part of the activities involved in a Field Course on Marine Ecology. Whence, we wish to thank the Piauí State University (UESPI) for logistic support, Dr. Sérgio 125 Revista SEB Ano 14 Final.indd 125 09/10/2012 13:44:10 Brazilian Journal of Ecology ISSN 1516-5868 Rosso (Department of Ecology, USP) for talks and suggestions on sampling methods, and Prof. Dr. Mutue Toyota Fujii (Institute of Botany, São Paulo), Dr. Estela Maria Plastino (Department of Botany, USP) and Dr. Carlos Wallace do Nascimento Moura (Department of Biological Sciences, UEFS), for help in species identification. References 1- AMADO FILHO, G.M.; HORTA P.A.; BRASILEIRO, P.S.; BARROS-BARRETO, M.B. & M.T. FUJII. Subtidal benthic marine algae of the Marine State Park of Laje de Santos (São Paulo, Brazil). Brazilian Journal of Oceanography. 54, 4:225-234, 2006. 2- BATISTA, M.G.S. Algas Marinhas Bentônicas do Litoral do Piauí: contribuição do conhecimento e preservação. In SANTOS FILHO, F. S & SOARES, A. F. C. L. (Organizadores) Biodiversidade do Piauí: Pesquisas & Perspectivas. 1 edição. Curitiba, PR: CRV. 2011. 3- BICUDO C.E.M. & SHEPHERED G.J. Biodiversidade do Estado de São Paulo, Brasil. Fungos macroscópicos & plantas. FAPESP, São Paulo, 79p. 1998 4- CEPRO. Macrozoneamento costeiro do estado do Piauí: Relatório geoambiental e socioeconômico. Teresina: Secretária de Planejamento do Piauí. 1990. 5- CEPRO. Macrozoneamento costeiro do estado do Piauí: Relatório geoambiental e socioeconômico. Teresina: Secretária de Planejamento do Piauí. Disponível em: http://www.cepro.pi.gov. br/download/201102/CEPRO16_9ab2acbd08. pdf. 2001. 6- CORREIA, M.D., SOVIERZOSKI, H.H. Ecossistemas marinhos: recifes, praias e manguezais. edUFAL/Maceió. Alagoas. 2005. 7- DE PAULA, A.F.; FIGUEIREDO, M.A.O.; & J.C. CREED. Structure of the Macroalgal Community Associated with the Seagrass Halodule wrightii Ascherson in the Abrolhos Marine National Park, Brazil. Botanica Marina. 46, 5: 413424. 2005. 8- ESTON, V.R.; BRAGA, R.A.; CORDEIROMARINO, M.; FUJII, M.T. & N.S. YOKOYA. Macroalgal colonization patterns on artificial substrates inside southeastern Brazilian mangroves. Aquatic Botany, Elsevier Science Publishers B.V., Amsterdam. 42: 315-325. 1992. 9- FUJII, M.T., BARATA D., CHIRACAVA S. & GUIMARÃES S.M.P.B. Cenário brasileiro da diversidade de algas marinhas bentônicas e sua contribuição para a política de conservação dos recursos naturais e do meio ambiente. In: 59° Congresso Nacional de Botânica: Atualidades, Desafios e Perspectivas da Botânica no Brasil. Imagem Gráfica e Editora Ltda. p. 375-377. 2008. 10-GESTINARI, L. M.S.; NASSAR, C.A.G; ARANTES, P.V.S. Algas marinhas bentônicas da Reserva Biológica da Praia do Sul, Ilha Grande, Angra dos Reis, Rio de Janeiro, Brasil. Acta Botânica Brasileira, 12, 1: 67-76. 1998. 11-GUBELIT Y.I. Factors, influencing on macroalgal communities in the Neva estuary (eastern Baltic Sea). Baltic International Symposium (BALTIC), 2012 IEEE/OES. 8-10 May 2012. 12-GUIMARAENS, M.A.; COIMBRA, C.A. & R. COUTINHO. Modeling competition between Laurencia obtusa (Ceramiales, Rhodophyta) and Hypnea spinella (Gigartinales, Rhodophyta) at Cabo Frio Island, Rio de Janeiro, Brazil. Hydrobiologia. 326-327, 1:273-276. 1996 13-HAROUN, R.J. & PRUD´HOMME van REINE, W.F. A Biogeographycal study of Laurencia and Hypnea species of the Macaronesian region. Courier Forsch – Inst Sencknberg 159: 119-125. 1993. 14-HEIJS, F. Community structure and seasonality of macroalgae in some mixed seagrass meadows from Papua New Guinea. Aquatic Botany, Elsevier Science Publishers B.V., Amsterdam. 27: 139-158. 1989. 15-HORTA P.A., AMANCIO E., COIMBRA C.S. & OLIVEIRA E.C. Considerações sobre a distribuição e origem da flora de macroalgas marinhas Brasileiras. Hoehnea 28: 243-265. 2001 16-LOUREIRO, R.L. & R.P. REIS. Efeito do gradiente de salinidade na taxa fotossintética de Polysiphonia subtilissima, Cladophora vagabunda e Ulva flexuosa subsp. flexuosa na Lagoa Rodrigo de Freitas, Rio de Janeiro, Brasil. Rodriguésia 59, 2:291-296. 2008 17-MARINS, B. V.; BRASILEIRO, P. S.; BARRETO, M. B. B.; NUNES, J. M. C; YONESHIGUEVALENTIM, Y. & AMADO FILHO, G.M. 126 Revista SEB Ano 14 Final.indd 126 09/10/2012 13:44:10 Brazilian Journal of Ecology ISSN 1516-5868 Subtidal Benthic Marine Algae of the Todos os Santos Bay, Bahia State, Brazil. Oecologia Brasiliensis. 12, 2: 229-242. 2008. 18-OLIVEIRA FILHO, E.C. & Y. UGADIM. A survey of the marine algae of Atol das Rocas (Brazil). Phycologia: 15, 1: 41-44. 1976. 19-OLIVEIRA, E. C. Macroalgas marinhas da costa brasileira - Estado do conhecimento, uso e conservação biológica. Congresso Brasileiro de Botânica. Acesso em 10 ago., 2010, http://www. ib.usp.br/algamare-br/macroalgas.html. 2002. 20-OLIVEIRA, E.C., HORTA, P.A., AMANCIO, E. & ANNA, C.L.S. Algas e angiospermas marinhas bênticas do litoral brasileiro. In: Ministério do Meio Ambiente. (Org.). Macrodiagnóstico da Zona Costeira do Brasil,RJ. 2001 21-OLIVEIRA-FILHO, E.C. Algas marinhas bentônicas do Brasil. Tese de livre docência. Universidade de São Paulo, São Paulo. 1977. 22-PEDRINI A.G.; GONCALVES J.E.A.; FON- SECA M.C.S.; ZAU A.S. & C.C. LACORTE. A survey of the marine algae fo Trindade Island, Brazil. Botanica marina. 32, 2:97-99. 1989. 23-PIAUÍ. Secretaria de Planejamento. Fundação CEPRO. Macrozoneamento costeiro do Estado do Piauí. Fundação CEPRO, Fundação Rio Parnaíba. Teresina. 1996. 24-QUARTINO, M.L., H. KLOSER, I.R. SCHLOSS & C. WIENCKE. Biomass and associations of benthic marine macroalgae from the inner Potter Cove (King George Island, Antarctica) related to depth and substrate. Polar Biol. 24: 349–355. 2001 25-RICHARDSON, M.G. The distribution of Antarctic marine macroalgae related to depth and substrate. Br. Antarct. Surv. Bull. 49: 1-13. 1979. 26-SANTOS-FILHO, F. S. Composição florística e estrutural da vegetação de restinga do Estado do Piauí, (Tese de Doutorado em Botânica) - Universidade Federal Rural de Pernambuco, Recife. 2009. 127 Revista SEB Ano 14 Final.indd 127 09/10/2012 13:44:10 Brazilian Journal of Ecology ISSN 1516-5868 128 RevistaView SEB Ano 14 publication statsFinal.indd 128 09/10/2012 13:44:10