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Biological Sciences • An. Acad. Bras. Ciênc. 86 (03) • Sept 2014 • https://doi.org/10.1590/0001-3765201420130067   copy

Angiosperm flora used by meliponine guilds (Apidae, Meliponina) occurring at rainforest edges in the state of Ceará, Brazil

Authorship SCIMAGO INSTITUTIONS RANKINGS

Abstracts

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.

deciduous forest; floristics; fragmented habitat; stingless bee; trophic resource

Informações sobre o uso dos recursos florísticos de bordas imediatas de fragmentos de floresta atlântica pelas abelhas sem ferrão não estão facilmente disponíveis na literatura científica. Considerando a importância dessas espécies vegetais para as guildas de meliponíneos locais, este estudo objetivou identificar e caracterizar a flora das bordas imediatas de quatro fragmentos florestais de mata atlântica situados no maciço de Baturité, no estado do Ceará, usada como recurso alimentar pelas abelhas sem ferrão. Estudamos as formas de crescimento das plantas, a similaridade florística entre bordas, os efeitos da pluviosidade sobre a floração e sugerimos técnicas simples para o manejo dessas áreas. Compilamos um total de 82 espécies vegetais, com predominância das formas arbóreas e arbustivas. Houve diferença na riqueza florística entre as áreas e a pluviosidade teve influência diferenciada sobre a floração, de acordo com a borda. Concluímos que os componentes florísticos das bordas estudadas são importantes para as guildas de abelhas sem ferrão, mas, práticas alternativas de manejo são necessárias para conservar as espécies vegetais e as abelhas.

floresta decídua; florística; habitat fragmentado; abelha sem ferrão; recurso trófico

INTRODUCTION

Over the past 40 years, knowledge of the floristic resources used by Brazilian native bees has been produced through systematic surveys of the bee fauna in several ecosystems. However, these studies have mostly been made in the Southeast and Southern regions, lacking information from other parts of the country (Freitas et al. 2009Freitas BM, Imperatriz-Fonseca VL, Medina LM, Kleinert AMP, Galeto L, Nates-Parra G and Quezada-Euán JJ. 2009. Diversity, threats and conservation of nativee bees in the Neotropics. Apidologie 40(3): 332-346.).

Among studies that report on food resources used by bees, including meliponines, we point out Cure et al. (1992)Cure JR, Thiengo M, Silveira FA and Rocha LB. 1992. Levantamento da fauna de abelhas silvestres na “Zona da Mata” de Minas Gerais. III. Mata secundária da região de Viçosa (Hymenoptera, Apoidea). Rev Bras Zool 9(3/4): 223-239., Souza et al. (1994)Souza VC, Cortopassi-Laurino M, Simão-Bianchini R, Pirani JR, Azoubel ML, Guibu LS and Giannini TC. 1994. Plantas apícolas de São Paulo e arredores. In: PIRANI JR AND CORTOPASSI-LAURINO M (Eds), Flores e abelhas em São Paulo, FAPESP, São Paulo, p. 43-179., Faria-Mucci et al. (2003)Faria-Mucci GM, Mel MA and Campos LAO. 2003. A fauna de abelhas (Hymenoptera, Apoidea) e plantas utilizada como fontes de recursos florais, em um ecossistema de campos rupestres em Lavras Novas, Minas Gerais, Brasil. In: MELO GAR AND SANTOS IA (Eds), Apoidea Neotropica – homenagem aos 90 anos de Jesus Santiago Moure, UNESC Edições, Criciúma, Santa Catarina, p. 241-256., Gonçalves and Melo (2005)Gonçalves RB and Melo GAR. 2005. A comunidade de abelhas (Hymenoptera, Apidae) em uma área restrita de campo natural no Parque Estadual de Vila Velha, Paraná: diversidade, fenologia e fontes florais de alimento. Rev Bras Entomol 49(4): 557-571., in southeastern and southern Brazil; and more recently Viana et al. (1997)Viana BF, Kleinert AMP and Imperatriz-Fonseca VL. 1997. Abundance and flower visits of bees in cerrado of Bahia, tropical Brazil. Stud Neotrop Fauna and Environ 32(4): 212-219., Ramalho and Silva (2002)Ramalho M and Silva M. 2002. Flora oleífera e sua guilda de abelhas em uma comunidade de restinga tropical. Sitient Série Ciên Biol 2(1/2): 34-43., Locatelli et al. (2004)Locatelli E, Machado ICS and Medeiros P. 2004. Riqueza de abelhas e a flora apícola em um fragmento da mata serrana (Brejo de Altitude) em Pernambuco, Nordeste do Brasil. In: PÔRTO KC, CABRAL JJP AND TABARELLI M (Eds), Brejos de altitude em Pernambuco e Paraíba – História Natural, Ecologia e Conservação, Ministério do Meio Ambiente, Brasília, DF, p. 153-177., Milet-Pinheiro and Schlindwein (2008)Milet-Pinheiro P and Schlindwein C. 2008. Comunidade de abelhas (Hymenoptera, Apoidea) e plantas em uma área do agreste pernambucano, Brasil. Rev Bras Entomol 52(4): 625-636., Monteiro and Ramalho (2010)Monteiro D and Ramalho M. 2010. Abelhas generalistas (Meliponina) e o sucesso reprodutivo de Stryphnodendron pulcherrimum (Fabales: Mimosaceae) com florada em massa na Mata Atlântica, BA. Neotrop Entomol 39(4): 519-526., in northeastern Brazil.

Most of these studies were carried out in forest fragments usually associated with long historical disturbances (Viana and Pinheiro 1998Viana VM and Pinheiro AFV. 1998. Conservação da biodiversidade em fragmentos florestais, Série Téc. IPEF 12(32): 25-42., Cerqueira et al. 2003Cerqueira R, Brant A, Nascimento MT and Pardini R. 2003. Fragmentação: alguns conceitos, In: RAMBALDI DM AND OLIVEIRA DAS (Eds), Fragmentação de ecossistemas: causas, efeitos sobre a biodiversidade e recomendações de políticas públicas, Ministério do Meio Ambiente, Brasília, DF, p. 23-40.). The peripheral margins (edges) of these forest fragments suffer abrupt changes that affect local dynamics including gene flow among populations (Bierregaard et al. 1992Bierregaard RO, Lovejoy TE, Kapos V, Santos AA and Hutchings RW. 1992. The biological dynamics of tropical rainforest fragments. Bioscience 42(11): 859-866., Viana et al. 1992Viana VM, Tabanez AJA and Martinez JLA. 1992. Restauração e manejo de fragmentos florestais. In: Anais do II Congresso Nacional sobre Essências Nativas - Conservação da biodiversidade, Instituto Florestal, São Paulo, p. 400-406., Murcia 1995Murcia C. 1995. Edge effects in fragmented forests: implication for conservation Trends Ecol Evol 10(2): 58-62., Schneider et al. 2003).

Natural or accidental occupation by native plant species, as well as those of broad geographic distribution, is quite common at such forest edges. This process, in general, is directly linked to the degree of matrix permeability (Cane 2001Cane JH. 2001. Habitat fragmentation and native bees: a premature verdict? Conserv Ecol 5(1): 3., Scariot et al. 2003Scariot A, Freitas SR, Neto EM, Nascimento MT, Oliveira LC, Sanaiotti T, Sevilha AC and Villela DM. 2003. Efeitos da fragmentação sobre a biodiversidade-vegetação e flora. In: RAMBALDI DM AND OLIVEIRA DAS (Eds), Fragmentação de ecossistemas – causas, efeitos sobre a biodiversidade e recomendações de políticas públicas, Ministério do Meio Ambiente/ SBF, Brasília, DF, p. 103-123., Ewers and Didham 2006Ewers RM and Didham RK. 2006. Confounding factors in the detection of species responses to habitat fragmentation. Biol Rev 81(1): 117-142.). According to López-Barrera (2004)López-Barrera F. 2004. Estructura y función en bordes de bosques. Ecosistems 13(1): 67-77., these types of low vegetation, composed mainly by shrubs and grasses have several degrees of permeability, ranging from abrupt to gradual. The latter allows, more intensively, a return of several groups of animals to this matrix range. Maciel et al. (2011)Maciel LA, Siles MFR and Bitencourt MD. 2011. Alterações na vegetação herbácea de floresta ombrófila densa decorrentes do uso em uma trilha turística na Serra do Mar em São Paulo, Brasil. Acta Bot Bras 25(3): 628-632. describe these areas as places where several species can establish, mainly herbs and shrubs requiring high luminosity and that present high capacity of vegetative regeneration and seed dispersal.

Studies on the phenological aspects of the flora found in forest fragments in Brazil have shown that the periodicity of the phenophases are more clearly established in environments where the weather seasonality is well defined (Morellato et al. 1989Morellato LPC, Rodrigues RR, Leitão-Filho HF and Joly CA. 1989. Estudo fenológico comparativo de espécies arbóreas de floresta de altitude e floresta mesófila semidecídua na Serra do Japi, Jundiaí, SP. Rev Bras Bot 12(1/2): 85-98., 1990Morellato LPC and Leitão-Filho HF. 1990. Estratégias fenológicas de espécies arbóreas em floresta mesófila na Serra do Japi, Jundiaí, SP. Braz J Biol 50(1): 163-173., Morellato and Leitão-Filho 1990Morellato LPC and Leitão-Filho HF. 1990. Estratégias fenológicas de espécies arbóreas em floresta mesófila na Serra do Japi, Jundiaí, SP. Braz J Biol 50(1): 163-173., Talora and Morellato 2000Talora DC and Morellato LPC. 2000. Fenologia de espécies arbóreas em floresta de planície litorânea do sudeste do Brasil. Rev Bras Bot 23(1): 13-26.). In such a situation, blooming periods generally depend upon the alternation of seasons; and the temporal levels of humidity are the main drivers to define these blooming periods.

Despite the lack of studies specifically on the role of forest edge flora to the stingless bees foraging resources, some studies made in Brazil with native grasslands (Gonçalves and Melo 2005Gonçalves RB and Melo GAR. 2005. A comunidade de abelhas (Hymenoptera, Apidae) em uma área restrita de campo natural no Parque Estadual de Vila Velha, Paraná: diversidade, fenologia e fontes florais de alimento. Rev Bras Entomol 49(4): 557-571., Gonçalves et al. 2009Gonçalves RB, Melo GAR and Aguiar AJC. 2009. A assembleia de abelhas (Hymenoptera, Apidae) de uma área de campos naturais do Parque Estadual de Vila Velha, Paraná e comparações com áreas de campos e cerrados. Pap Avul Zool 49(14): 163-181.) and rainforest fragments (Antonini et al. 2003Antonini Y, Accacio GM, Brant A, Cabral BC, Fontenelle JCR, Nascimento MT, Thomazini APBW and Thomazini MJ. 2003. Efeitos da fragmentação sobre a biodiversidade – insetos. In: RAMBALDI DM AND OLIVEIRA DAS (Eds), Fragmentação de ecossistemas: causas, efeitos sobre a biodiversidade e recomendações de políticas públicas, Ministério do Meio Ambiente, Brasília, DF, p. 239-273.) showed a positive relationship between the surrounding flora and stingless bees, mainly those species less demanding for food resources. There is a need for more studies in order to understand the stingless bees' foraging performance in the forest edges.

To investigate this issue we conducted a floristic survey in the immediate edges of four forest fragments located in the Baturité massif in order to: i) characterize and record, the growth-form of the plant species supplying food resources for stingless bees, in order to know the structure of this community botany; ii) identify floristic similarities among the studied areas to check for differences in the richness of the flora of each area; iii) record the influence of rainfall on the number of species in bloom, to get an idea of the food supply throughout the year; iv) suggest simple management measures for these edge areas in order to ensure the preservation of plant and bee species.

MATERIALS AND METHODS

Study Area

The study was carried out in the Baturité massif, geographic coordinates 4°-4° 30' S 38° 45'-39° 15' W, position NNE-SSW, located in the northeastern part of the state of Ceará, 70 km from the coast. This massif possesses a more humid windward side and a less humid lee side, which faces towards the interior (Gomes 1978Gomes MAF. 1978. O maciço de Baturité – uma abordagem ecológica. In: Anonymous (Eds), Anais do III Encontro Nacional de Geógrafos, AGB/UFC, Fortaleza, p. 39-59., UFC/FUNCEME 1994, Souza 1997Souza MJN. 1997. Geomorfologia. In: IPLANCE (Eds), Atlas do Ceará, IPLANCE, Fortaleza, p. 18-19.). The local climate is classified, according to Köppen's classification, as AW' (SEMACE 1992SEMACE – Superintendência Estadual do Meio Ambiente do Estado do Ceará. 1992. Zoneamento ambiental da APA da serra de Baturité: diagnósticos e diretrizes, SEMACE, Fortaleza, 109 p.), with mean annual rainfall between 1100-1700 mm, and mean temperature below 24°C, depending on altitudinal level (Nimer 1977Nimer E. 1977. Relevo. In: Galvão MV (Ed), Geografia do Brasil: Região Nordeste, IBGE, Rio de Janeiro, p. 47-84., SUDENE 1982SUDENE – Superintendência do Desenvolvimento do Nordeste. 1982. Climatologia e balanço hídrico. Ceará. Dados pluviométricos. Temperaturas do Ceará estimadas por regressão múltipla: altitude, latitude e distância do mar, Projeto de Delimitação e Regionalização do Brasil Semiárido, Fortaleza, 30 p., FUNCEME 2010, INMET 2010). There are two main vegetation types that belong to the Atlantic rainforest Domain (Figueiredo and Barboza 1990Figueiredo MA and Barboza MA. 1990. A vegetação e a flora da serra de Baturité, Ceará, Coleção Mossoroense (Série B) 747: 1-10., Fernandes 1998Fernandes A. 1998. Fitogeografia brasileira, Multigraf, Fortaleza, 340 p.) which are named ombrophilous montane forest and seasonal semideciduous montane forest (Veloso et al. 1991Veloso HP, Rangel-Filho ALR and Lima JCA. 1991. Classificação da vegetação brasileira, adaptada a um sistema universal, IBGE, Rio de Janeiro, 124 p.). The former occurs only on the windward side and on the top, at altitudes above 600 m, while the latter occupies areas below 600 m, on the same side. On the lee side, above 600 m, the seasonal deciduous montane forest occurs and below 500-600 m a thorny deciduous vegetation identified as “caatinga arbórea” prevails (Fernandes 1998Fernandes A. 1998. Fitogeografia brasileira, Multigraf, Fortaleza, 340 p.).

In our study areas, we identified two basic landscape units: the forest fragments and the anthropogenic matrix which has been without agricultural use for the last 30 years, although occasional animal husbandry occurs.

Our study was carried out in Baturité, Guaramiranga and Mulungu municipalities, in four out of six fragments previously studied by Araújo et al. (2006aAraújo FS, Gomes VS, Silveira AP, Figueiredo MA, Oliveira RF, Bruno MMA, Lima-Verde LW, Silva EF, Otutumi AT and Ribeiro KA. 2006a. Efeito da variação topoclimática na fisionomia e estrutura da vegetação da serra de Baturité, Ceará. In: OLIVEIRA TS AND ARAÚJO FS (Eds), Diversidade e conservação da biota na serra de Baturité, Ceará, UFC/COELCE, Fortaleza, Ceará, p. 73-136., b)Araújo FS, Gomes VS, Lima-Verde LW, Figueiredo MA, Bruno MMA, Nunes EP, Otutumi AT and Ribeiro KA. 2006b. Efeito da variação topoclimática na composição e riqueza da flora fanerogâmica da serra de Baturité, Ceará. In: OLIVEIRA TS AND ARAÚJO FS (Eds), Diversidade e conservação da biota na serra de Baturité, Ceará, UFC/COELCE, Fortaleza, Ceará, p. 137-162.. These were named F1, F2, F3 and F4. The geographic location and characteristics of each site are as follows:

F1 (4°12'24.3″ S and 38°58'14.1″ W), at Sítio Lagoa, ombrophilous montane forest, on the windward side, 20.61 ha, at altitudes 1015-1114 m, municipality of Guaramiranga.

F2 (04°15'16.0″ S and 38°59'31.5″ W), at Sítio Salva-Vidas, seasonal deciduous montane forest, 15.97 ha, on the lee side, at altitudes 670-690 m, municipality of Guaramiranga.

F3 (04°16'57.1″ S and 39°00'01.1″ W), at Sítio Jardim, seasonal deciduous montane forest, 26.45 ha, on the lee side, at altitudes 780- 790 m, municipality of Mulungu.

F4 (04°18'08.35″ S and 38°54'46.0″ W), at Sítio Labirinto dos Taveiras, ombrophilous montane forest, 6.30 ha, on the windward side, at altitudes 660- 680 m, municipality of Baturité.

In order to better represent massif vegetation, we selected two fragments of two vegetation types on each mountain side. We used only the immediate edges of these fragments named E1, E2, E3 and E4. The edge E1 was 600 m long and width varied between 1 to 2 m, E2 was 400 m long and width varied between 2 and 10 m, E3 was 600 m long and width between 1 to 2 m and E4 was 400 m long and width between 1 to 2 m. The four edges summed up 1.11 ha. The vegetation found in the four edges showed the same patterns: low vegetation, bushy-herbaceous composition and variable degrees of permeability. Arboreal species, remnants of their respective forest fragments, were also present in punctual distribution throughout these edges.

Data Collection and Analyses

Field work was carried out monthly from March 2008 to August 2009. Botanical material was collected along a transect walked for one hour, twice in the morning and twice in afternoon shift, between 7 and 17 h. Therefore, all edges were sampled for four hours per day, totaling 72 h per edge during the whole study. In all edges, we sampled solely plants that stingless bees used for pollen or nectar, by direct observation of these bees foraging on the open flowers (Menezes et al. 2007Menezes C, Silva CI, Singer RB and Kerr WE. 2007. Competição entre abelhas durante forrageamento em Schefflera arboricola (Hayata) Merr. Jornal de Biociências 23(1): 63-69.). Each plant was observed for approximately five minutes before it was harvested. Only fertile branches containing buds and open flowers were vouchered following Fidalgo and Bononi (1989)Fidalgo O and Bononi VLR. 1989. Técnicas de coleta, preservação e herborização de material botânico, Instituto de Botânica (série documentos), São Paulo, 62 p.. Vouchers were deposited in the Prisco Bezerra Herbarium (EAC) of Universidade Federal do Ceará, in Fortaleza (collector numbers refer to L. W. Lima-Verde and J. R. Lima).

To identify plant species, we consulted literature and the EAC Herbarium collection. Species and authors names were written in accordance with Brummitt and Powell (1992)Brummitt RK and Powell CE. 1992. Authors of plant names, Royal Botanic Gardens, Kew, London, 732 p. and W3TROPICOS (2010). Families were classified according to the Angiosperm Phylogeny Group (APG) III (Bremer et al. 2009Bremer B, Bremer K, Chase MW, Fay MF, Reveal JL, Soltis DS, Soltis PS and Stevens PF. 2009. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Bot J Linn Soc 161(2): 105-121.).

Plants were classified into four growth-form according to Whittaker (1975)Whittaker RH. 1975. Communities and ecosystems, Collier-Macmillan Ltda., New York, 385 p.: herbs, shrubs, climbing (woody and herbaceous) and trees.

Data were organized in a binary matrix (presence/absence) of the sampled species so as to evaluate the degree of association between floristic composition at the edges and the influence of rainfall gradients on the number of flowering species. To interpret the floristic composition at edges, we used a similarity coefficient (Jaccard index ≥ 0,50, Kent and Coker 1992Kent M and Coker P. 1992. Vegetation description and analysis, a practical approach, Belhaven Press, London, 363 p.) and a cluster analysis (UPGMA), using Estimate S (Colwell 2006Colwell RK. 2006. Estimate S: Statistical estimation of species richness and schared species from samples, Version 8.0, User's Guid and Application, University of Connecticut, (Available at: < http://purl.oclc.org/estimate>).
http://purl.oclc.org/estimate... ) and Biodiversity Pro version 2.0 (McAleece 1997McAleece N. 1997. Bio Diversity Professonal versão 2.0, The Natural History Museum and The Schottish Association for Marine Science, Oban, Scotland. (Available at: <http://gcmd.nasa.gov/KeywordSearch>).
http://gcmd.nasa.gov/KeywordSearch... ). Pearson's correlation (P ∈ [- 1, 1], Zar 1984Zar JH. 1984. Biostatistical analysis, Prentice-Hall, New Jersey, 718 p.) was used to test the rainfall effects on species flowering using the software R (R Development Core Team 2010R Development Core Team. 2010. R: A language and environment for statistical computing, R Foundation for Statistical Computing, Vienna, (Available at: <http://www.R-project.org.>).
http://www.R-project.org... ).

The seasonality of floristic resources was plotted as a function of monthly mean rainfall for each municipality. We considered a period of 12 months (January-December), to define the two local well-marked seasons: the wet season (November-June) and the dry season (July-October). In this case we used the data pertaining to rainfall from March to December 2008 and January to February 2009. Historical monthly rainfall ranges were recorded for 1974-2010 (FUNCEME 2010, INMET 2010).

RESULTS

Taxonomic Pattern in the Flora

In all study areas we recorded a total of 82 plant species, 72 genera and 33 families used as food resource by stingless bees (Table I). Five species were identified only at the genus level.

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TABLE I
Plant species used by stingless bees in four fragment edges of Atlantic rainforest at Baturité massif, state of Ceará, Brazil. E1 = Sítio Lagoa, ombrophilous montane forest (windward); E2 = Sítio Salva-Vidas, seasonal deciduous montane forest (leeward); E3 = Sítio Jardim, seasonal deciduous montane forest (leeward); E4 = Sítio Labirinto dos Taveiras, ombrophilous montane forest (windward). Habit (herb = herbaceous, shr =shrubby, cli = climbing, arb = arboreal), flowering period (Jan = January, Feb = February, Mar = March, Apr = April, May = May, Jun = June, Jul = July, Aug = August, Sep = September, Oct = October, Nov = November, Dec = December).

At the edge of each study area, we recorded 32 species, 30 genera and 18 families in E1; 25 species, 25 genera and 16 families in E2; 36 species, 32 genera and 18 families in E3; and 16 species, 16 genera and 11 families in E4.

The most common botanical families whose species were used by stingless bees in the four edges were Fabaceae (11 genera and 17 spp.) and Asteraceae (8 genera and 8 spp.), followed by Bignoniaceae (4 genera and 4 spp.), Myrtaceae (3 genera and 4 spp.), Solanaceae (2 genera and 4 spp.), Apocynaceae (3 genera and 3 spp.), Convolvulaceae (3 genera and 3 spp.), Euphorbiaceae (2 genera and 3 spp.), Salicaceae (3 genera and 3 spp.) Melastomataceae (3 genera and 3 spp.) and Rubiaceae (3 genera and 3 spp.). It is worth mentioning that we did not record Asteraceae in E4. These families represented 67.07% of the species visited by stingless bees.

The seven most species-rich genera were Senna, Inga, Solanum, Croton, Bauhinia, Piptadenia and Myrcia. The first three genera had three species each, while the remaining had two species each (Table I).

Food Supply Pattern

The plant species Spermacoce verticillata (Rubiaceae), Libidibia ferrea (Fabaceae), Serjania lethalis (Sapindaceae) Vernonanthura brasiliana (Asteraceae), Cynophalla flexuosa (Capparaceae), Senna splendida (Fabaceae) and Wedelia scaberrima (Asteraceae), offered most of the food resource to a total of 20 stingless bee species recorded (L.W. Lima-Verde and B.M. Freitas, unpublished data). S. verticillata occurred in all areas and offered resources to 60% (12 spp.) of visitors. L. ferrea occurred only in E3 and was visited by 35% (7 spp.) of the bees. S. lethalis and V. brasiliana recorded in E1 and E3, and E1, E2 and E3, respectively, were visited by 30% (6 spp.) of the bee species. C. flexuosa occurred in E2 and E3 and offered resources to 25% (5 spp.) of the bees. S. splendida (E3) and W. scaberrima (E2 and E3), offered, each one, resources to 20% (4 spp.) of the meliponine bees.

Growth-Form Pattern of Flora

Trees and shrubs were the predominant growth-form in the edges studied, however in E3 the climbing plant richness matched that of the trees, both with ten species (Fig. 1).

Figure 1 -
Number of plant species per growth-form in four fragment edges of the Atlantic rainforest at Baturité massif, state of Ceará, Brazil. H = herbaceous; S = shrubby; C = climbing; A = arboreal. E1 = Sítio Lagoa, ombrophilous montane forest (windward); E2 = Sítio Salva-Vidas, seasonal deciduous montane forest (leeward); E3 = Sítio Jardim, seasonal deciduous montane forest (leeward); E4 = Sítio Labirinto dos Taveiras, ombrophilous montane forest (windward).

Floristic Similarity

The cluster analysis among the flora of all edges ranged from 2.04% to 31.11% for the Jaccard index (Table II).

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TABLE II
Floristic similarity and distance (km) between four fragment edges of Atlantic rainforest at Baturité massif, state of Ceará, Brazil. E1 = Sítio Lagoa, ombrophilous montane forest (windward); E2 = Sítio Salva-Vidas, seasonal deciduous montane forest (leeward); E3 = Sítio Jardim, seasonal deciduous montane forest (leeward); E4 = Sítio Labirinto dos Taveiras, ombrophilous montane forest (windward).

The dendrogram of similarity among the edges (Fig. 2) formed two groups. Clearly, this was more related to vegetation typologies and to the mountain sides (on the windward ombrophilous montane forest, for E1 x E4, and on the leeward seasonal semideciduous montane forest, for E2 x E3).

Figure 2 -
Dendrogram of floristic similarity between four fragment edges of the Atlantic rainforest at Baturité massif, state of Ceará, Brazil. E1 = Sítio Lagoa, ombrophilous montane forest (windward); E2 = Sítio Salva-Vidas, seasonal deciduous montane forest (leeward); E3 = Sítio Jardim, seasonal deciduous montane forest (leeward); E4 = Sítio Labirinto dos Taveiras, ombrophilous montane forest (windward).

The pattern of flora distribution in the study areas also showed that only S. verticillata, Solanum paniculatum and V. brasiliana (3.66% of the total recorded species) occurred in at least three edges, suggesting a high plasticity of these species in relation to geographical location. A total of 28.05% of species (23 spp.) were present at only two edges and 68.29% (56 spp.) were unique to an edge (Table I).

Flowering Versus Rainfall

Analysis of the number of flowering species related to annual rainfall also showed somewhat different features in the study areas (Figs. 3 and 4).

Figure 3 -
Dendrogram of dispersion and flowering chronology of the plant species surveyed at edges E1 and E2 of the Atlantic rainforest at Baturité massif, state of Ceará, Brazil. R = Rain; F = Flowering species. Rains from March to December 2008 and from January to February 2009, based on the historical average from 1974 to 2010. E1 = Sítio Lagoa, ombrophilous montane forest (windward); E2 = Sítio Salva-Vidas, seasonal deciduous montane forest (leeward).

Figure 4 -
Dendrogram of dispersion and flowering chronology of the plant species surveyed at edges E3 and E4 of the Atlantic rainforest at Baturité massif, state of Ceará, Brazil. R = Rain; F = Flowering species. Rains from March to Dezember 2008 and from January to February 2009, based on the historical average from 1974 to 2010. E3 = Sítio Jardim, seasonal deciduous montane forest (leeward); E4 = Sítio Labirinto dos Taveiras, ombrophilous montane forest (windward).

In E1, there was a negative correlation (r = - 0.68; p = 0.01). In E2, results were not statistically significant, with a low correlation (r = 0.18; p = 0.58). In E3 and E4 correlations were highly positive (r = 0.64, p = 0.02 r = 0.71, p = 0.009, respectively), especially in E4.

Regarding flowering periods, we found that the fragment edges had suites of species with an overlapping flowering sequence, which can offer resources to bees through the year.

Edge E1: Norantea guianensis (December-February), Scoparia dulcis (March-July), Acnistus arborescens (April-November), Spermacoce verticillata (May-October), Inga bollandii (September-November), Vernonanthura brasiliana (November-December), Serjania lethalis (November-December).

Edge E2: Cardiospermum corindum (January-December), Senegalia poliphylla (February-March), Wedelia scaberrima (February-May), Spermacoce verticillata (May-August), Capparis flexuosa (November-December), Anadenathera colubrina (December-January), Vernonanthura brasiliana (August-January).

Edge E3: Scoparia dulcis (February-July), Wedelia scaberrima (March-May), Spermacoce verticillata (March-August), Senna uniflora (May-July), Vernonanthura brasiliana (June-December), Senna splendida (July-September), Serjania lethalis (October-December), Capparis flexuosa (November-December), Spondias mombin (December-January).

Edge E4: Manihot glaziovii (December-March), Heliconia psittacorum (March-November), Albizia polycephala (March-April), Miconia cecidophora (March-April), Spermacoce verticillata (May-September), Inga ingoides (September-October), Myrcia splendens (October-November).

DISCUSSION

Taxonomic Pattern Among the Flora

Our results showed a wide range of trophic sources for stingless bees, owing to high floristic diversity (82 species, 72 genera and 33 families).

Our findings are similar to those few studies on plant species important as food resources to the bees from Atlantic forest in this portion of Brazil (Milet-Pinheiro and Schlindwein 2008Milet-Pinheiro P and Schlindwein C. 2008. Comunidade de abelhas (Hymenoptera, Apoidea) e plantas em uma área do agreste pernambucano, Brasil. Rev Bras Entomol 52(4): 625-636., 87 species, 76 genera and 38 families; and Locatelli et al. 2004Locatelli E, Machado ICS and Medeiros P. 2004. Riqueza de abelhas e a flora apícola em um fragmento da mata serrana (Brejo de Altitude) em Pernambuco, Nordeste do Brasil. In: PÔRTO KC, CABRAL JJP AND TABARELLI M (Eds), Brejos de altitude em Pernambuco e Paraíba – História Natural, Ecologia e Conservação, Ministério do Meio Ambiente, Brasília, DF, p. 153-177., 63 species, 50 genera and, 29 families). In addition, in this same region, our results are also in agreement with Oliveira et al. (2006)Oliveira FX, Andrade LA and Félix LP. 2006. Comparações florísticas entre comunidades de Floresta Ombrófila Aberta com diferentes idades, no Município de Areia, PB. Acta Bot Bras 20(4): 861-873., who studied edges with types of low vegetation (“capoeira”) (90 species, 74 genera and 74 families).

Among the eleven most common botanical families whose species were used by stingless bees, Fabaceae and Asteraceae had the largest number of species. Fabaceae also had the most species-rich genera, such as Senna, Inga, Bauhinia and Piptadenia (Table I).

These two families stand out in several studies in tropical region, due to their wide geographic distribution and the considerable number of species among the Angiospermae Cronquist 1981Cronquist A. 1981. An integrated system of classification of flowering plants. Columbia University Press, New York, 1262 p.). In Brazil, this pattern of richness has also been reported in many ecosystems through floristic and hymenopteran surveys (e.g.: Viana et al. 1997Viana BF, Kleinert AMP and Imperatriz-Fonseca VL. 1997. Abundance and flower visits of bees in cerrado of Bahia, tropical Brazil. Stud Neotrop Fauna and Environ 32(4): 212-219., in the Cerrado, Aguiar 2003Aguiar CML. 2003. Utilização de recursos florais por abelhas (Hymenoptera, Apoidea) em uma área de caatinga (Itatim, Bahia). Rev Bras Zool 20(3): 457-467., in the Caatinga, Faria-Mucci et al. 2003Faria-Mucci GM, Mel MA and Campos LAO. 2003. A fauna de abelhas (Hymenoptera, Apoidea) e plantas utilizada como fontes de recursos florais, em um ecossistema de campos rupestres em Lavras Novas, Minas Gerais, Brasil. In: MELO GAR AND SANTOS IA (Eds), Apoidea Neotropica – homenagem aos 90 anos de Jesus Santiago Moure, UNESC Edições, Criciúma, Santa Catarina, p. 241-256., in the Campos Rupestes, Viana and Kleinert 2006Viana BF and Kleinert AMP. 2006. Structure of bee-flower in the coastal sand dune of Abaeté, northeastern Brazil. Rev Bras Entomol 50(1): 53-63., in the Restinga, Locatelli et al. 2004Locatelli E, Machado ICS and Medeiros P. 2004. Riqueza de abelhas e a flora apícola em um fragmento da mata serrana (Brejo de Altitude) em Pernambuco, Nordeste do Brasil. In: PÔRTO KC, CABRAL JJP AND TABARELLI M (Eds), Brejos de altitude em Pernambuco e Paraíba – História Natural, Ecologia e Conservação, Ministério do Meio Ambiente, Brasília, DF, p. 153-177. and Milet-Pinheiro and Schlindwein 2008Milet-Pinheiro P and Schlindwein C. 2008. Comunidade de abelhas (Hymenoptera, Apoidea) e plantas em uma área do agreste pernambucano, Brasil. Rev Bras Entomol 52(4): 625-636., in the Atlantic Forest Domain).

Food Supply Pattern

The most important species that offer food resources to stingless bees (S. verticillata, L. ferrea, S. lethalis, V. brasiliana, C. flexuosa, S. splendida, W. scaberrima) must initially be taken into account when managing these areas.

In forest patch edges in the Baturité massif, these species are believed to ensure the maintenance of several species of local stingless bees as well as enabling, in part, a successful local meliponiculture.

Among these seven species mentioned above, S. verticillata is noteworthy for being the most important for the stingless bees. Its spectrum of flowering ranged from four to six months between March and October, at the edge of each forest fragment, showing therefore, a period of supply of food resources, both in the months of highest rainfall, as those less rainy in Baturité massif. S. verticillata has also presented a considerable adaptive plasticity to habitat and soil types at different levels of degradation, showing how their subjects are rustic to the diversity of the medium. Studies in similar Brazilian ecosystems with bees census (Wilms et al. 1996Wilms W, Imperatriz-Fonseca VL and Engels W. 1996. Resource partitioning between highly eusocial bees and possible impact of the introduced africanized honey bee on native stingless bees in the brazilian atlantic rainforest, Stud Neotrop Fauna Environ 31(3/4): 137-151., Gonçalves and Melo 2005Gonçalves RB and Melo GAR. 2005. A comunidade de abelhas (Hymenoptera, Apidae) em uma área restrita de campo natural no Parque Estadual de Vila Velha, Paraná: diversidade, fenologia e fontes florais de alimento. Rev Bras Entomol 49(4): 557-571., Viana et al. 2006Viana BF, Silva FO and Kleinert AMP. 2006. A flora apícola de uma área restrita de dunas litorâneas, Abaeté, Salvador, Bahia. Rev Bras Bot 29(1): 13-25.) also showed the importance of S. verticillata for this group of Hymenoptera.

Growth-Form Pattern of the Flora

Owing to the criteria used for definition of edges, the shrub and arboreal growth-form were prevalent (Fig. 1), both for having the highest species richness at the immediate edges and for distribution in the rest of the matrix.

In the field it was observed that the shrub species were more or less enclosed space edges with a higher degree of degradation. Studies such as Bierregaard et al. (1992)Bierregaard RO, Lovejoy TE, Kapos V, Santos AA and Hutchings RW. 1992. The biological dynamics of tropical rainforest fragments. Bioscience 42(11): 859-866. and Murcia (1995)Murcia C. 1995. Edge effects in fragmented forests: implication for conservation Trends Ecol Evol 10(2): 58-62. show that the transformations undergone by these environments radically alter levels of light, humidity, temperature and air currents. In this case, the structure and species richness of vegetation edge depend heavily on the type of surrounding matrix and the edge effect.

In summary, the successful occupation of these areas by species groups are associated with different abiotic conditions of the edges and consequently with greater or lesser difficulty of dispersal of propagules of some species (Scariot et al. 2003Scariot A, Freitas SR, Neto EM, Nascimento MT, Oliveira LC, Sanaiotti T, Sevilha AC and Villela DM. 2003. Efeitos da fragmentação sobre a biodiversidade-vegetação e flora. In: RAMBALDI DM AND OLIVEIRA DAS (Eds), Fragmentação de ecossistemas – causas, efeitos sobre a biodiversidade e recomendações de políticas públicas, Ministério do Meio Ambiente/ SBF, Brasília, DF, p. 103-123.).

In general, species of degraded fragments forest are characterized by the requirement in brightness due to its high regeneration capacity and dispersion vegetative propagules (Maciel et al. 2011Maciel LA, Siles MFR and Bitencourt MD. 2011. Alterações na vegetação herbácea de floresta ombrófila densa decorrentes do uso em uma trilha turística na Serra do Mar em São Paulo, Brasil. Acta Bot Bras 25(3): 628-632.).

The environmental conditions of the collection sites also seem to bring different responses to the predominance of growth-forms. Studies of Locatelli et al. (2004)Locatelli E, Machado ICS and Medeiros P. 2004. Riqueza de abelhas e a flora apícola em um fragmento da mata serrana (Brejo de Altitude) em Pernambuco, Nordeste do Brasil. In: PÔRTO KC, CABRAL JJP AND TABARELLI M (Eds), Brejos de altitude em Pernambuco e Paraíba – História Natural, Ecologia e Conservação, Ministério do Meio Ambiente, Brasília, DF, p. 153-177. and Milet-Pinheiro and Schlindwein (2008)Milet-Pinheiro P and Schlindwein C. 2008. Comunidade de abelhas (Hymenoptera, Apoidea) e plantas em uma área do agreste pernambucano, Brasil. Rev Bras Entomol 52(4): 625-636. demonstrated this possibility by recording the herbaceous growth-form was prevalent in the first study, and herbaceous and shrub were more predominant in the second.

Floristic Similarity

Our data showed a considerable degree of heterogeneity in the floristic compositions (Table I), which was evidenced by the low values in the cluster analysis (Jaccard's index).

In Table I, we note that the distances between edges did not significantly account for floristic similarity among them. However, vegetation type explained better this floristic similarity in all areas. Groupings E1 x E4 and E2 x E3 (Fig. 2) were defined, respectively, by their vegetation types (ombrophilous montane forest and the seasonal semideciduous montane forest) and, consequently, by mountain side orientation (windward or leeward).

The difference in species number between areas may be associated with the conservation status and with matrix permeability. The matrix characteristics are usually related to the degree of disturbance, to inadequate soil management, to a greater or lesser light incidence, as well as to the size of the area (Cane 2001Cane JH. 2001. Habitat fragmentation and native bees: a premature verdict? Conserv Ecol 5(1): 3., Scariot et al. 2003Scariot A, Freitas SR, Neto EM, Nascimento MT, Oliveira LC, Sanaiotti T, Sevilha AC and Villela DM. 2003. Efeitos da fragmentação sobre a biodiversidade-vegetação e flora. In: RAMBALDI DM AND OLIVEIRA DAS (Eds), Fragmentação de ecossistemas – causas, efeitos sobre a biodiversidade e recomendações de políticas públicas, Ministério do Meio Ambiente/ SBF, Brasília, DF, p. 103-123., Ewers and Didham 2006Ewers RM and Didham RK. 2006. Confounding factors in the detection of species responses to habitat fragmentation. Biol Rev 81(1): 117-142.).

However, one must consider local topoclimatic factors. Gentry (1982Gentry AH. 1982. Patterns of Neotropical plants species diversity. Evol Biol 15: 1-84., 1988)Gentry AH. 1988. Changes in plant community diversity and floristic composition on environment and geographical gradients. Ann Mo Bot Gard 75(1): 1-34. and Murphy and Lugo (1986)Murphy PG and Lugo AE. 1986. Ecology of tropical dry forest. Annu Rev Ecol Syst 17(1): 67-88. verified, in neotropical forest fragments, that the greatest plant species richness is positively correlated with the levels of annual rainfall and climate seasonality. As for Baturité massif remnants, Araújo et al. (2006b)Araújo FS, Gomes VS, Lima-Verde LW, Figueiredo MA, Bruno MMA, Nunes EP, Otutumi AT and Ribeiro KA. 2006b. Efeito da variação topoclimática na composição e riqueza da flora fanerogâmica da serra de Baturité, Ceará. In: OLIVEIRA TS AND ARAÚJO FS (Eds), Diversidade e conservação da biota na serra de Baturité, Ceará, UFC/COELCE, Fortaleza, Ceará, p. 137-162. found that an increase in floristic richness was correlated with the elevation of the altitudinal gradient. This floristic richness could also be related with the local rainfall gradient, which, according to Nimer (1989), in mountains like Baturité massif increases with increasing altitude.

We also noted that species richness was correlated to climatic and altitudinal conditions. In E2, located between 670 and 690 m, we recorded 25 species, while in E3 (780-790 m) we recorded 36 species. We found similar results in E1 (1015-1114 m) and E4 (660-680 m) where we recorded 32 and 16 species, respectively.

Flowering Versus Rainfall Correlation

All the edges showed different magnitudes with relation to the number of flowering species as indicated by Pearson's coefficients (Figs. 3 and 4).

In E1, there was a high negative correlation (r = -0.68), thus showing a low number of flowering species during the period of greater rainfall. In this case, the flowering peak occurred between September and January, during the dry season.

In E2, the low positive correlation was not statistically significant and seems to indicate that in this area the flowering season is more evenly distributed throughout the year. However, we found that the flowering peak tended to occur between May and August, when rainfall began to decrease.

In the last two areas (E3 and E4), the correlations were high and positive (r = 0.64 and r = 0.71, respectively), which indicates that the number of flowering species responded better to annual rainfall. The number of flowering species decreased as rainfall decreased. For these edges a second flowering peak occurred, chiefly in the last months of the year.

Numerous environmental factors may be operating in these areas, however, those related to climate and topography are more easily perceptible to the conditions of the Baturité massif as the observations of Araújo et al. (2006aAraújo FS, Gomes VS, Silveira AP, Figueiredo MA, Oliveira RF, Bruno MMA, Lima-Verde LW, Silva EF, Otutumi AT and Ribeiro KA. 2006a. Efeito da variação topoclimática na fisionomia e estrutura da vegetação da serra de Baturité, Ceará. In: OLIVEIRA TS AND ARAÚJO FS (Eds), Diversidade e conservação da biota na serra de Baturité, Ceará, UFC/COELCE, Fortaleza, Ceará, p. 73-136., b)Araújo FS, Gomes VS, Lima-Verde LW, Figueiredo MA, Bruno MMA, Nunes EP, Otutumi AT and Ribeiro KA. 2006b. Efeito da variação topoclimática na composição e riqueza da flora fanerogâmica da serra de Baturité, Ceará. In: OLIVEIRA TS AND ARAÚJO FS (Eds), Diversidade e conservação da biota na serra de Baturité, Ceará, UFC/COELCE, Fortaleza, Ceará, p. 137-162..

In Brazil, phenological studies covering all aspects of the flora of forest types, such as Atlantic forest, have shown that in environments with seasonally defined climates, the flowering periods of most species generally depend on the alternation of seasons (Morellato et al. 1989Morellato LPC, Rodrigues RR, Leitão-Filho HF and Joly CA. 1989. Estudo fenológico comparativo de espécies arbóreas de floresta de altitude e floresta mesófila semidecídua na Serra do Japi, Jundiaí, SP. Rev Bras Bot 12(1/2): 85-98., 1990Morellato LPC and Leitão-Filho HF. 1990. Estratégias fenológicas de espécies arbóreas em floresta mesófila na Serra do Japi, Jundiaí, SP. Braz J Biol 50(1): 163-173., Morellato and Leitão-Filho 1990Morellato LPC and Leitão-Filho HF. 1990. Estratégias fenológicas de espécies arbóreas em floresta mesófila na Serra do Japi, Jundiaí, SP. Braz J Biol 50(1): 163-173., Talora and Morellato 2000Talora DC and Morellato LPC. 2000. Fenologia de espécies arbóreas em floresta de planície litorânea do sudeste do Brasil. Rev Bras Bot 23(1): 13-26.). These species depend, therefore, on climatic factors, mainly related to the humidity and temperature, to trigger their phenophases of flowering.

Suggestions for Management

Maintenance of forest or remnant forest patch edges under proper management conditions would enable in situ biological conservation, especially benefiting meliponine bees, as well as other pollinators.

Antonini et al. (2003)Antonini Y, Accacio GM, Brant A, Cabral BC, Fontenelle JCR, Nascimento MT, Thomazini APBW and Thomazini MJ. 2003. Efeitos da fragmentação sobre a biodiversidade – insetos. In: RAMBALDI DM AND OLIVEIRA DAS (Eds), Fragmentação de ecossistemas: causas, efeitos sobre a biodiversidade e recomendações de políticas públicas, Ministério do Meio Ambiente, Brasília, DF, p. 239-273. indicate the need for maintaining the successional vegetation around forest fragments as an essential preservation measure for bees in general. On the other hand, Britez et al. (2003) highlight that when planning management activities around forest fragments, one must consider the landscape itself, proper management techniques, monitoring diagnostics of the flora and fauna, water resources and the physical environment.

At present, the main issue study areas is human and animal trampling, especially cattle, which has a seasonal grazing schedule. In this case, it is important that we develop some techniques for environmental protection to be used on the occasion of procedures for monitoring these areas.

A simple and practical suggestion, in conformity with López-Barrera (2004)López-Barrera F. 2004. Estructura y función en bordes de bosques. Ecosistems 13(1): 67-77., is to try to conserve these areas as important wildlife and wild land preserves in the category of low vegetation, with soft permeability and high light incidence. Such measures would maintain these edges in this status quo, so that more effective preservation measures, such as ecological corridors or connecting isolated patches, can be established and benefit these forest fragments as a whole.

CONCLUSIONS

The large number of Meliponina species which visited the flowers of plant species occurring at the forest fragment edges proves the importance of this flora as a trophic resource for the stingless bees in the Baturité massif.

Forest fragment edges in the Baturité massif constitute an ample spectrum of trophic resources to a degraded environment providing 82 plant species visited by Meliponina bees.

The species Spermacoce verticillata, Libidibia ferrea, Serjania lethalis, Vernonanthura brasiliana, Cynophalla flexuosa, Senna splendida and Wedelia scaberrima outstand the others as providers of food resources to the stingless bees and S. verticillata can be considered the most important of them, both for its plasticity being preset in the four studied edges, as well as for offering resources for 12 out of the 20 Meliponina species present in the area.

Despite occurring in the same massif formation, the four forest fragment edges bear heterogeneous flora, suggesting a differentiated geographic distribution of these plant species in the edges studied.

The distinct effects of rain levels on the blooming of plant species found at each fragment edge determines how flowering phenology takes place in these areas and also shows how each floristic component presents its temporal alternative of trophic resources to the guilds of local stingless bees.

The authors thank BNB/ETENE/FUNDECI (project 1835/2008), Fundação Cearense de Apoio ao Desenvolvimento Científico e Tecnológico (Funcap) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Brasília/Brazil) for financial support, a D.Sc. scholarship to L.W. Lima-Verde and a research grant to B.M. Freitas (#305062/2007-7), respectively. We also acknowledge the biologists Francyregis Araújo Nunes, Alípio José de Souza Pacheco Filho and Andréa Pereira Silveira for their support in organizing the statistical calculations and the graphics. Finally, we are grateful to all the landowners for allowing us to collect data within their properties.

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Publication Dates

  • Publication in this collection
    Sept 2014

History

  • Received
    22 Feb 2013
  • Accepted
    30 Jan 2014
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