Angiosperm Flora Used by Meliponine Guilds (Apidae, Meliponina) Occurring at Rainforest Edges in the State of Ceará, Brazil
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Anais da Academia Brasileira de Ciências (2014) 86(3): 1395-1409 (Annals of the Brazilian Academy of Sciences) Printed version ISSN 0001-3765 / Online version ISSN 1678-2690 http://dx.doi.org/10.1590/0001-3765201420130067 www.scielo.br/aabc Angiosperm flora used by meliponine guilds (Apidae, Meliponina) occurring at rainforest edges in the state of Ceará, Brazil LUIZ W. LIMA-VERDE1, MARIA I.B. LOIOLA1 and BRENO M. FREITAS2 1Universidade Federal do Ceará, Departamento de Biologia, Bloco 906, Av. Humberto Monte, s/n, Campus do Pici, 60455-760 Fortaleza, CE, Brasil 2Universidade Federal do Ceará, Departamento de Zootecnia, Bloco 808, Av. Humberto Monte, s/n, Campus do Pici, 60021-970 Fortaleza, CE, Brasil Manuscript received on February 22, 2013; accepted for publication on January 30, 2014 ABSTRACT Information about the use of floristic resources of the immediate edges of ombrophilous forest (Atlantic rainforest) fragments by stingless bees is not readily available in the scientific literature. Considering the importance of these plant species for local guilds of stingless bees, this study aimed to identify and characterize the flora of the immediate borders of four Atlantic rainforest fragments situated in Baturité massif, state of Ceará, used as food resource by stingless bees. We studied the growth-form of the plants, the floristic similarity between edges and the effect of rainfall on the flowering, and suggested simple techniques for handling these areas. We compiled a total of 82 plant species with a predominance of tree and shrub form. There were different floristic richness between areas and rainfall had differentiated influence on flowering, according to the edge. We concluded that the florist components of the studied edges are relevant to the stingless bee guilds, but alternative management practices are needed to conserve both plant and bee species. Key words: deciduous forest, floristics, fragmented habitat, stingless bee, trophic resource. INTRODUCTION recently Viana et al. (1997), Ramalho and Silva Over the past 40 years, knowledge of the floristic (2002), Locatelli et al. (2004), Milet-Pinheiro resources used by Brazilian native bees has been and Schlindwein (2008), Monteiro and Ramalho produced through systematic surveys of the bee (2010), in northeastern Brazil. fauna in several ecosystems. However, these Most of these studies were carried out in forest studies have mostly been made in the Southeast and fragments usually associated with long historical Southern regions, lacking information from other disturbances (Viana and Pinheiro 1998, Cerqueira parts of the country (Freitas et al. 2009). et al. 2003). The peripheral margins (edges) of Among studies that report on food resources these forest fragments suffer abrupt changes that used by bees, including meliponines, we point affect local dynamics including gene flow among out Cure et al. (1992), Souza et al. (1994), Faria- populations (Bierregaard et al. 1992, Viana et al. Mucci et al. (2003), Gonçalves and Melo (2005), 1992, Murcia 1995, Schneider et al. 2003). in southeastern and southern Brazil; and more Natural or accidental occupation by native plant species, as well as those of broad geographic Correspondence to: Breno Magalhães Freitas E-mail: [email protected] distribution, is quite common at such forest edges. An Acad Bras Cienc (2014) 86 (3) 1396 LUIZ W. LIMA-VERDE, MARIA I.B. LOIOLA and BRENO M. FREITAS This process, in general, is directly linked to differences in the richness of the flora of each area; the degree of matrix permeability (Cane 2001, iii) record the influence of rainfall on the number Scariot et al. 2003, Ewers and Didham 2006). of species in bloom, to get an idea of the food According to López-Barrera (2004), these types supply throughout the year; iv) suggest simple of low vegetation, composed mainly by shrubs management measures for these edge areas in order and grasses have several degrees of permeability, to ensure the preservation of plant and bee species. ranging from abrupt to gradual. The latter allows, MATERIALS AND METHODS more intensively, a return of several groups of animals to this matrix range. Maciel et al. (2011) STUDY AREA describe these areas as places where several species The study was carried out in the Baturité massif, can establish, mainly herbs and shrubs requiring geographic coordinates 4°-4° 30’ S 38° 45’-39° 15’ high luminosity and that present high capacity of W, position NNE-SSW, located in the northeastern vegetative regeneration and seed dispersal. part of the state of Ceará, 70 km from the coast. This Studies on the phenological aspects of the flora massif possesses a more humid windward side and a found in forest fragments in Brazil have shown that less humid lee side, which faces towards the interior the periodicity of the phenophases are more clearly (Gomes 1978, UFC/FUNCEME 1994, Souza 1997). established in environments where the weather The local climate is classified, according to Köppen’s seasonality is well defined (Morellato et al. 1989, classification, as AW’ (SEMACE 1992), with mean 1990, Morellato and Leitão-Filho 1990, Talora and annual rainfall between 1100-1700 mm, and mean Morellato 2000). In such a situation, blooming temperature below 24°C, depending on altitudinal periods generally depend upon the alternation of level (Nimer 1977, SUDENE 1982, FUNCEME seasons; and the temporal levels of humidity are 2010, INMET 2010). There are two main vegetation the main drivers to define these blooming periods. types that belong to the Atlantic rainforest Domain Despite the lack of studies specifically on the (Figueiredo and Barboza 1990, Fernandes 1998) role of forest edge flora to the stingless bees foraging which are named ombrophilous montane forest and resources, some studies made in Brazil with native seasonal semideciduous montane forest (Veloso et grasslands (Gonçalves and Melo 2005, Gonçalves al. 1991). The former occurs only on the windward et al. 2009) and rainforest fragments (Antonini et al. side and on the top, at altitudes above 600 m, while 2003) showed a positive relationship between the the latter occupies areas below 600 m, on the same surrounding flora and stingless bees, mainly those side. On the lee side, above 600 m, the seasonal species less demanding for food resources. There deciduous montane forest occurs and below 500- is a need for more studies in order to understand 600 m a thorny deciduous vegetation identified as the stingless bees’ foraging performance in the “caatinga arbórea” prevails (Fernandes 1998). forest edges. In our study areas, we identified two basic To investigate this issue we conducted a landscape units: the forest fragments and the floristic survey in the immediate edges of four anthropogenic matrix which has been without forest fragments located in the Baturité massif in agricultural use for the last 30 years, although order to: i) characterize and record, the growth- occasional animal husbandry occurs. form of the plant species supplying food resources Our study was carried out in Baturité, for stingless bees, in order to know the structure Guaramiranga and Mulungu municipalities, in four of this community botany; ii) identify floristic out of six fragments previously studied by Araújo et similarities among the studied areas to check for al. (2006a, b). These were named F1, F2, F3 and F4. An Acad Bras Cienc (2014) 86 (3) FLORA USED BY MELIPONINE GUILDS AT RAINFOREST EDGE 1397 The geographic location and characteristics of each these bees foraging on the open flowers (Menezes et site are as follows: al. 2007). Each plant was observed for approximately F1 (4°12’24.3’’ S and 38°58’14.1’’ W), at five minutes before it was harvested. Only fertile Sítio Lagoa, ombrophilous montane forest, on the branches containing buds and open flowers were windward side, 20.61 ha, at altitudes 1015-1114 m, vouchered following Fidalgo and Bononi (1989). municipality of Guaramiranga. Vouchers were deposited in the Prisco Bezerra F2 (04°15’16.0’’ S and 38°59’31.5’’ W), at Sítio Herbarium (EAC) of Universidade Federal do Salva-Vidas, seasonal deciduous montane forest, Ceará, in Fortaleza (collector numbers refer to L. 15.97 ha, on the lee side, at altitudes 670-690 m, W. Lima-Verde and J. R. Lima). municipality of Guaramiranga. To identify plant species, we consulted literature F3 (04°16’57.1’’ S and 39°00’01.1’’ W), at and the EAC Herbarium collection. Species and Sítio Jardim, seasonal deciduous montane forest, authors names were written in accordance with 26.45 ha, on the lee side, at altitudes 780- 790 m, Brummitt and Powell (1992) and W3TROPICOS municipality of Mulungu. (2010). Families were classified according to the F4 (04°18’08.35’’ S and 38°54’46.0’’ W), at Angiosperm Phylogeny Group (APG) III (Bremer Sítio Labirinto dos Taveiras, ombrophilous montane et al. 2009). forest, 6.30 ha, on the windward side, at altitudes Plants were classified into four growth-form 660- 680 m, municipality of Baturité. according to Whittaker (1975): herbs, shrubs, In order to better represent massif vegetation, we climbing (woody and herbaceous) and trees. selected two fragments of two vegetation types on each Data were organized in a binary matrix (presence/ mountain side. We used only the immediate edges of absence) of the sampled species so as to evaluate the these fragments named E1, E2, E3 and E4. The edge degree of association between floristic composition E1 was 600 m long and width varied between 1 to 2 at the edges and the influence of rainfall gradients m, E2 was 400 m long and width varied between 2 and on the number of flowering species. To interpret the 10 m, E3 was 600 m long and width between 1 to 2 floristic composition at edges, we used a similarity m and E4 was 400 m long and width between 1 to 2 coefficient (Jaccard index ≥ 0,50, Kent and Coker m.