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Biological Sciences • An. Acad. Bras. Ciênc. 85 (1) • Jan-Mar 2013 • https://doi.org/10.1590/S0001-37652013005000017   copy

Melliferous flora and pollen characterization of honey samples of Apis mellifera L., 1758 in apiaries in the counties of Ubiratã and Nova Aurora, PR

Authorship SCIMAGO INSTITUTIONS RANKINGS

Abstracts

The aim of this study was to carry out a survey of the flora with potential for beekeeping in the counties of Ubiratã and Nova Aurora-PR through the collection of plants and pollen analyses in honey samples collected monthly. 208 species of plants were recorded, distributed in 66 families. The families that showed the major richness of pollen types were: Asteraceae, Myrtaceae and Solanaceae. Approximately 80 pollen types were found in honey samples, most of them were characterized as heterofloral. Cultivated plants, such as Glycine max (soybean) and Eucalyptus spp., were representative in some months of the year. Exotic species, such as Ricinus communis and Melia azedarach, were also frequent. However, over than 50% of the pollen types belong to native species of the region, such as Schinus terebinthifolius, Baccharis spp. Alchornea triplinervia, Parapiptadenia rigida, Hexaclamys edulis, Zanthoxylum sp. and Serjania spp., indicating the importance of the native vegetation for the survival of the colonies.

beekeeping; bee plants; floral resources; floristic survey

O objetivo deste trabalho foi realizar um levantamento da flora com potencial apícola nos municípios de Ubiratã e Nova Aurora-PR, por meio da coleta de plantas e análises polínicas em amostras de mel coletadas mensalmente. Foram registradas 208 espécies de plantas, distribuídas em 66 famílias. As famílias que apresentaram maior riqueza de tipos polínicos foram Asteraceae, Myrtaceae e Solanaceae. Aproximadamente 80 tipos polínicos foram encontrados nas amostras de mel e, na maioria, foram caracterizados como heteroflorais. Plantas cultivadas, como Glycine max (soja) e Eucalyptus spp. foram representativas em alguns meses do ano. Espécies exóticas, tais como Ricinus communis and Melia azedarach também foram frequentes. No entanto, mais de 50% dos tipos polínicos pertencem a espécies nativas da região, tais como Schinus terebinthifolius, Baccharis spp., Alchornea triplinervea, Parapiptadenia rigida, Hexaclamys edulis, Zanthoxylum sp. and Serjania spp., indicando a importância da vegetação nativa para a sobrevivência das colônias.

apicultura; plantas apícolas; recursos florais; levantamento florístico

INTRODUCTION

Brazil is a country of great beekeeping potential due to its diverse flowerings and adequate climate conditions making possible the management of beehives during the entire year. Beekeeping is an interesting activity to the rural producer because it requires little initial investment (Nogueira-Couto and Couto 2006).

Plants and their associated insects present interdependence in their evolutionary history and tropical regions have greater diversity of plants with flowers than temperate regions. Therefore, bees from tropics with a rich diversity of food resources demonstrate fast answer to the changes in the availability of the food items and lesser constancy than species of temperate regions (Crane 1990Crane E. 1990. Bees and beekeeping: science, practice and world resources. Oxford: Heinemann Newness, 614 p.). The mutual benefits between bees and plants depend on the interaction with factors such as phenology and biogeography. In general, these factors are specific of each place and depend on the seasonal patterns (Hill and Webster 1995Hill D and Webster C. 1995. Apiculture and forestry (Bees and trees). Agroforestry Systems 29: 313-320.).

As the honey production and the parameters of honey depend on the vegetal species available to the beekeeping use, many studies have been carried out for the identification of the plants used by A. mellifera in different regions of the country. The authors employ mainly techniques based on the analysis of the pollen content of honey samples and/or analysis of pollen loads from corbicula of bees (Carvalho and Marchini 1999Carvalho CAL and Marchini LC. 1999. Plantas visitadas por Apis mellifera L. no vale do rio Paraguaçu, Município de Castro Alves, Bahia. Rev Bras Bot 22: 333-338., Moreti et al. 2000Moreti AC, Carvalho CAL, Marchini LC and Oliveira PCF. 2000. Espectro polínico de amostras de mel de Apis mellifera L., coletadas na Bahia. Bragantia 59: 1-6., Silva and Absy 2000Silva SJR and Absy ML. 2000. Análise do pólen encontrado em amostras de mel de Apis mellifera L. (Hymenoptera, Apidae) em uma área de savana de Roraima, Brasil. Acta Amaz 30: 579-588., Bastos et al. 2003Bastos EMAF, Silveira VM and Soares AEE. 2003. Pollen spectrum of honey produced in cerrado areas of Minas Gerais state (Brazil). Braz J Biol 63: 599-615., 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: 13-25., Luz et al. 2007Luz CFP, Thomé ML and Barth OM. 2007. Recursos tróficos de Apis mellifera L. (Hymenoptera, Apidae) na região de Morro Azul do Tinguá, Estado do Rio de Janeiro. Rev Bras Bot 30: 29-36., Mendonça et al. 2008Mendonça K, Marchini LC, Souza BA, Almeida-Anacleto D and Moreti AC. 2008. Plantas apícolas de importância para Apis mellifera L. (Hymenoptera: Apidae) em fragmento de Cerrado em Itirapina, SP. Neotropic Entomol 37: 513-521., Sodré et al. 2008Sodré GS, Marchini LC, Moreti AC and Carvalho CAL. 2008. Tipos polínicos encontrados em amostras de méis de Apis mellifera em Picos, Estado do Piauí. Ciênc Rural 38: 839-842.) and analysis of visiting bees in plants (Marchini et al. 2001Marchini LC, Moreti AC, Teixeira EW, Silva ECA, Rodrigues RR and Souza VC. 2001. Plantas visitadas por abelhas africanizadas em duas localidades do estado de São Paulo. Sci Agric 58: 413-420., Santos et al. 2006Santos RF, Kiill LHP and Araújo JLP. 2006. Levantamento da flora melífera de interesse apícola no município de Petrolina-PE. Caatinga 19: 221-227., Vieira et al. 2008Vieira GHC, Marchini LC, Souza BA and Moreti AC. 2008. Fontes florais usadas por abelhas (Hymenoptera, Apoidea) em área de Cerrado no município de Cassilândia, Mato Grosso do Sul, Brasil. Ciênc Agrotec 32: 1454-1460.).

The knowledge of the regional flora with beekeeping potential possibilities the better use of the floral resources and stimulate the utilization of species of plants with apiarist value in the restoration of the vegetation of rural areas.

This research was carried out to obtain a floristic survey in the surroundings areas of apiaries in rural area in the counties of Ubiratã and Nova Aurora (PR) to identify the floral sources used by Apis mellifera for honey production and to evaluate the pollen spectrum of the honey samples during the year.

MATERIALS AND METHODS

Area of Study

The collection areas (Figure 1) are located between 24°20′ to 24°40′S and 52°52′ to 53°26′W parallels, distributed in three rural areas in the counties of Ubiratã in the Central-Western meso-region of Paraná State and Nova Aurora in the Occidental-Centre meso region of Paraná State.

Figure 1
Location of the collection points in the counties of Nova Aurora (Point A) and Ubiratã (Points B and C) in Paraná state.

These counties are located in the phytogeographical domains of Submontane Semidecidous Tropical Forest (IBGE 1992IBGE - Fundação Instituto Brasileiro de Geografia e Estatística. 1992. Manual técnico da vegetação brasileira. Departamento de Recursos Naturais e Estudos Ambientais. – Rio de Janeiro: IBGE, 92 p.). The predominant soil is Red Latosol (Brazilian classification: Latossolo Vermelho distroférrico, Embrapa 1999Embrapa - Empresa Brasileira de Pesquisa Agropecuaria. 1999. Centro nacional de pesquisa de solos. Sistema brasileiro de classificação de solos. Brasília: Embrapa, 412 p.) and the region presents a softly waved relief, located in the third plateau of Paraná State at 550 m of height above sea level.

The climate in the region is CwB, humid subtropical, with noticeable dry winters and very rainy summers by Köppen's classification. The mean annual temperature is higher than 22°C in the warmest month and lower than 18°C in the coldest months. The pluviometric precipitation varies from 1,600 mm to 1,900 mm and the relative humidity of the air remains close to 80% (IAPAR 2009IAPAR - Instituto Agronômico do Paraná. 2009. Cartas climáticas do Paraná. Acessado em: 16 nov. 2009. Disponível em: http://www.iapar.br/modules/conteudo/conteudo.php?conteudo=677.
http://www.iapar.br/modules/conteudo/con... ).

Location of the Apiaries

The collections were carried out in three apiaries, one in the county of Nova Aurora (24°31′50″ S and 53°11′50″ W – Apiary A) and two in the county of Ubiratã -PR (24°29′41″ S and 53°02′43″ W – Apiary B and 24°36′40.8″ S and 53°00′52.6″ W – Apiary C). The sampled areas embrace forest remnants, gardens, pastures, agricultural cultivations (predominance of soybean and corn) and reforestation areas (predominance of Eucalyptus). Apiary A has a legal reserve area of 13.65 ha, Apiary B of 2.4 ha and Apiary C of 15.64 ha.

Collection and Identification of the Botanical Material

The collections were carried out biweekly from October 2008 to November 2009, totalizing 13 months. Considering that the radius of the forest remnants in the surrounding area of the apiaries did not exceed 1,000 meters and the others rural properties were composed by agricultural areas, random collections were determined inside of a radius of approximately 1,000 m around the apiaries. The vegetation survey was conducted with usual techniques of floristic surveys (Fidalgo and Bononi 1989Fidalgo O and Bononi VLR. 1989. Técnicas de coleta, preservação e herborização de material botânico. São Paulo: Instituto de Botânica., IBGE 1992IBGE - Fundação Instituto Brasileiro de Geografia e Estatística. 1992. Manual técnico da vegetação brasileira. Departamento de Recursos Naturais e Estudos Ambientais. – Rio de Janeiro: IBGE, 92 p.).

Five samples of each vegetal specie in blooming were collected and then herborized and identified (Cronquist 1981Cronquist A. 1981. An integrated system of classification of flowering plants. New York: Columbia University Press, 1262 p.) at Herbarium of the Universidade Tecnológica Federal do Paraná (HCF) in Campo Mourão. When necessary, these samples were also sent to the Botanical Museum of Curitiba (MBM) and to the Herbarium of the Botanical Department of the Universidade Federal do Paraná (UFPR) in Curitiba. The material was recorded using a digital camera Sony-DSC-H9 (8.1MP-15x of optical zoom).

The classification of the species by the habit was adopted in accordance with HCF: tree – higher than 5 m of height and small tree – lower than 5 m, both forming frustum (trunk); shrub – with woody tissue and until 5 m of height, without forming frustum; herb – with no woody tissue. The classification was done in successional stages (Reitz et al. 1978Reitz R, Klein RM and Reis A. 1978. Projeto madeira de Santa Catarina. Itajaí – Santa Catarina, n. 28-30, 320 p., 1983Reitz R, Klein RM and Reis A. 1983. Projeto madeira do Rio Grande do Sul. Sellowia n. 34-35, 525 p., SPVS 1996SPVS - Sociedade de Pesquisa em Vida Selvagem e Educação Ambiental. 1996. Nossas árvores: Manual para recuperação da reserva florestal legal. Curitiba: FNMA, 84 p., Roderjan et al. 1998Roderjan CV, Kuniyoshi YS and Galvão F. 1998. As regiões fitogeográficas do estado do Paraná. 2a ed., Curitiba: Acta For Bras v. 1.).

Collection of Honey Samples

In each apiary, three beehives were marked next to the forest remnant and to the agricultural cultures. Empty frame with beeswax foundation in the super was set up monthly to avoid the mixture of the honey produced in different months. Samples were collected from December 2008 to April 2009 and from May to November 2009 when there was honey stored in the combs, even if it was not mature (with minimum 75% of capped cells). The honeycomb was centrifuged separately in plastic packing to avoid the mixture of the different samples.

Reference Slide Collection and Pollen Analyses

Floral buds were collected and packed separately to avoid the pollen mixture. One pollen slide collection was prepared using the acetolysis method (Erdtman 1952Erdtman G. 1952. Pollen morphology and plant taxonomy-Angiosperms. Stockholm: Almqvist e Wiksel, 539 p.). This method is used to eliminate cell contents and enable observations on pollen size, shape, aperture and exine surface. A camera coupled in a microscope and the Motic images 2000 software captured images of the pollen.

To the preparation of the slides of pollen contained in the honey of each month, the samples of the three beehives of each apiary were mixed. To the samples with moisture above 20%, it was used a quantity proportionally higher. An aliquot of 10 g was diluted in 20 mL of distilled water and centrifuged to the acetolysis method. Two slides of each sample were prepared for posterior counting and identification of the pollen types.

The slides were observed in a optical microscope Motic to the qualitative analyses (determination of pollen types) and quantitative (counting of pollen grains). Pollen types were determined by comparing with the reference lamina and also by researches in the specialized bibliography (Barth 1989Barth OM. 1989. O pólen do mel brasileiro. Rio de Janeiro: Luxor, 226 p., Moreti et al. 2002Moreti AC, Marchini LC, Souza VC and Rodrigues RR. 2002. Atlas do pólen de plantas apícolas. Rio de Janeiro: Papel Virtual Editora, 93 p., Melhem et al. 2003Melhem TS, Cruz-Barros MAV, Corrêa AMS, Makino-Watanabe H, Silvestre-Capelato MSF and Golçalves-Esteves VL. 2003. Variabilidade Polínica em Plantas de Campos do Jordão (São Paulo, Brasil). Bol Inst Bot São Paulo 16: 1-104., Roubik 2010Roubik DW. 2010. Pollen and spores of Barro Colorado Island. Acessado em: 12 nov. Disponível em: http://striweb.si.edu/roubik/.
http://striweb.si.edu/roubik/... ). To the quantitative analyses, 300 to 500 pollen grains of each slide were counted and the averages of the counting of two slides of each sample were considered. The pollen types were classified in four classes of frequency (Louveaux et al. 1978Louveaux J, Maurizio A and Vorwohl G. 1978. Methods of melissopalynology. Bee World 59: 139-157., Barth 1989Barth OM. 1989. O pólen do mel brasileiro. Rio de Janeiro: Luxor, 226 p.): dominant pollen (frequency higher than 45% - D), accessory pollen (16% to 45% - A), important isolated pollen (3% to 15% - I) and occasional isolated pollen (frequency lower than 3% - O).

The Diversity Index of Shannon (H′) (Pielou 1975Pielou EC. 1975. Ecological diversity. New York: J Wiley, 165 p.) and Simpson (D) (Poole 1974Poole RW. 1974. An introduction to quantitative ecology. New York: McGraw-Hill, 532 p.) were calculated to the pollen data:

H′ = - Σ pi x ln pi, where: pi = ni/N, ni = number of individuals of the specie i, N = total number of sampled individuals.

1 - D = 1- Σ {[ni (ni-1)]/N(N-1)}, where: ni = number of individuals of n-th specie, N = total number of sampled individuals.

RESULTS

Survey of the Plants

In the floristic survey, 208 species were recorded and distributed in 66 families (Table I). Six families, Asteraceae (9.48%), Myrtaceae (7.11%), Solanaceae (5.69%), Malpighiaceae (4.27%), Bignoniaceae (5.21%) and Fabaceae (3.79%), concentrate approximately 36% of the richness of the area. Genera with higher richness of species were Solanum (seven species) and Eucalyptus (four species).

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TABLE I
Blooming period of the collected species in the counties of Nova Aurora and Ubiratã (PR) from October 2008 to November 2009.

It can be observed in Table I that 162 species (76.8%) are native and 34 species (16.1%) are exotic from identified species. Among them, there were introduced species, cultivated in the areas close to the apiaries and with economical importance, such as Eucalyptus spp. and Glycine max (soybean).

From the total of the species, 139 (67.0%) were classified as pioneer species and 52 (25.0%) as secondary. 53 arboreal species (25.5%), 41 herbs (19.7%), 40 shrubs (19.2%), 31 climbers (15.0%), 12 sub-shrubs (5.8%) and 12 small trees (5.8%) were collected.

Pollen Analyses

Considering the three areas, a total of 30 samples of honey were analyzed and 80 pollen types distributed in 31 families were identified. Three pollen types were not identified (Table II). Microscopic images of some pollen types verified in this work are shown in Figure 2. From the taxa present in the samples, 42 (52.5%) are of native species collected in the surrounding areas of the apiaries. Asteraceae and Fabaceae were the most frequent pollen types with 11 and 6 types, respectively. Euphorbiaceae and Sapindaceae presented five types each one and Mimosaceae and Myrtaceae, four types.

Fig 2
Pollen types from honey samples collected in counties of Nova Aurora and Ubiratã -PR from December 2008 to May 2009. 1- Amaranthaceae sp. 1; 2- Anacardiaceae Schinus terebinthifolius; 3- Asteraceae Conyza bonariensis; 4- Brassicaceae – Raphanus sativus; 5- Euphorbiaceae Alchornea sp.; 6- Euphorbiaceae Bernardia pulchella; 7- Euphorbiaceae Ricinus communis; 8- Fabaceae Glycine max; 9- Flacourtiaceae Casearia sylvestris; 10- Mimosaceae Parapiptadenia rigida; 11- Myrtaceae Campomanesia sp.; 12- Myrtaceae Hexaclamys edulis. Scale: 10 µm.

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TABLE II
Pollen spectrum and frequency classes in honey samples of Africanized honeybee Apis mellifera in three apiaries (A; B; C) in Nova Aurora (A) and Ubiratã –PR (B and C) collected from December 2008 to April 2009 and from May to November 2010. *Native species collected in the area.

Five pollen types identified in the samples are not present in the list of the plants collected in the area: Arecaceae sp. 1, Araceae sp. 1, Stylosanthes sp., Lygustrum sp, Borreria sp., Acacia type and Vernonia sp. Plants of Arecaceae family and of the Herbarium.

Microscopic images recorded of same pollen types are show in Figure 2.

Dominant pollen types were observed in 14 (47%) of 30 honey samples, Glycine max (soybean) in December/January, Eucalyptus spp. in February/March, May and June, Machaerium stipitatum in April, Brassicaceae sp1. in July, Melia azedarach (santa-bárbara) in August and Parapiptadenia rigida in November. Only one of the samples of the apiary A, with the largest forest area, presented the dominant pollen type of Eucalyptus in May.

The dominant pollen types G. max, Eucalyptus spp. and Brassicaceae, cultivated or ruderal plants, were found in the months with the lowest number of species collected, December, January, May, June and July (Figure 3).

Figure 3
Number of floristic species collected in the surrounding areas of three apiaries in the counties of Nova Aurora and Ubiratã (PR) from October 2008 to November 2009.

The frequency of occurrence (FO) indicates that only three pollen types were present in more than 50% of the samples: Eucalyptus sp, Arecaceae sp and Brassicaceae sp. Among them, Eucalyptus spp. was present as accessory or dominant pollen from February to July in 12 (40%) of the samples.

Twelve other pollen types were also frequent, present in 30 of 50% of the samples: Schinus terebinthifolius, Baccharis spp., Alchornea triplinervea, Glycine max, Leonurus sibiricus, type Acacia, Parapiptadenia rigida, Leucaena leucocephala, Hexaclamys edulis, type Myrcia, Piperaceae sp1., Zanthoxylum sp. and Serjania spp.

Only 14 (17.7%) of the total species showed frequency of more than 15% (accessory or dominant pollen) at least in one sample.

Pollen diversity calculated by the Index of Diversity of Shannon (Table III) indicates that the samples of the apiaries A and B presented higher diversity in relation to the samples of the apiary C.

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TABLE III
Index of Diversity of Shannon and Simpson based on pollen data from samples of three apiaries located in the counties of Nova Aurora (A) and Ubiratã-PR (B and C).

DISCUSSION

The area of study embraces rural areas that present different types of landscape, including pastures, cultivated areas and forest remnants. The results were similar to Sakuragui et al. (2011)Sakuragui CM, Alves EM, Lorenzetti ER, Janunzzi AM, Borges RAX, Toledo VAA. 2011. Bee flora of an insular ecosystem in southern Brazil. J Bot Res Inst Texas 5: 311-319. in a Semidecidous Tropical Forest modified by the anthropic action, in which it was observed predominance of Asteraceae, Rubiaceae, Solanaceae and Fabaceae; and Gasparino et al. (2006)Gasparino D, Malavasi UC, Malavasi MM and Souza I. 2006. Quantificação do banco de sementes sob diferentes usos do solo em área de domínio ciliar. Rev Árvore 30: 1-9. that noted Asteraceae, Leguminosae and Solanaceae among the predominant families in the seeds banks of areas with riparian vegetation in a county of the west region of Paraná State.

From 34 exotic species collected in the area of study, seven were classified as exotic invader species in accordance with the administrative rule 125/2009 of the Environmental Institute of Paraná (PARANÁ 2009Paraná. Instituto Ambiental do Paraná – IAP. 2009. Lista de espécies exóticas invasoras do Paraná, Portaria 125/2009. Curitiba: IAP.) that recognizes the official list of the exotic invader species to Paraná State. These species are: Leucaena leucocephala (leucena), Melia azedarach (santa-bárbara), Psidium guajava (goiaba), Ricinus communis (mamona), Tecoma stans (amarelinho), Eriobotrya japonica (nêspera) and Hovenia dulcis (uva-japão). Some of them, such as R. communis, M. azedarach and L. leucocephala, were representative in the pollen spectrum of the honey collected in the region.

Families with higher number of species in an area are also the main sources of nectar and pollen (Ramalho et al. 1990Ramalho M, Kleinert-Giovannini A and Imperatriz-Fonseca VL. 1990. Important bee plants for stingless bees (Melipona and Trigonini) and Africanized honeybees (Apis mellifera) in neotropical habitats: a review. Apidologie 21: 469-488.). Asteraceae and Labiatae species are very numerous in open vegetation areas in South America. Solanaceae, Euphorbiaceae, Palmae and Myrtaceae families are common in neotropical regions.

Asteraceae is one of the families that have the greatest number of species of apiarist importance, as this is one of the families with more species and more widely distributed among the angiosperms (Locatelli and Machado 2001Locatelli E and Machado IC. 2001. Bee diversity and their floral resources in a fragment of a tropical altitudinal wet forest (“Brejos de altitude”) in Northeastern Brazil. Acta Hort 561: 317-325.).

The families of plants with better representation in honey samples analysed in this research are similar to Asteraceae, Caesalpiniaceae (Fabaceae), Malvaceae and also Myrtaceae, observed by Carvalho et al. (1999)Carvalho CAL, Marchini LC and Ros PB. 1999. Fontes de pólen utilizadas por Apis mellifera L. e algumas espécies de Trigonini (Apidae) em Piracicaba (SP). Bragantia 58: 49-56. in São Paulo State as the best representatives; and Asteraceae, Myrtaceae, Mimosaceae and Verbenaceae found by Marchini et al. (2001)Marchini LC, Moreti AC, Teixeira EW, Silva ECA, Rodrigues RR and Souza VC. 2001. Plantas visitadas por abelhas africanizadas em duas localidades do estado de São Paulo. Sci Agric 58: 413-420. as the most representative families in São Paulo State.

Bastos et al. (2003)Bastos EMAF, Silveira VM and Soares AEE. 2003. Pollen spectrum of honey produced in cerrado areas of Minas Gerais state (Brazil). Braz J Biol 63: 599-615. reported the predominance of pollen of Asteraceae, Euphorbiaceae and Leguminosae (nowadays this one is divided into Caesalpiniaceae, Fabaceae and Mimosaceae) in an area of Cerrado in Minas Gerais State. Luz et al. (2007)Luz CFP, Thomé ML and Barth OM. 2007. Recursos tróficos de Apis mellifera L. (Hymenoptera, Apidae) na região de Morro Azul do Tinguá, Estado do Rio de Janeiro. Rev Bras Bot 30: 29-36. reported the predominance of pollen types of Arecaceae, Asteraceae, Mimosaceae and Myrtaceae in honey samples of Rio de Janeiro State. Euphorbiaceae and Myrtaceae were also found as dominant or accessory pollen types in organic honey samples collected in islands located in the frontier of Paraná, São Paulo and Mato Grosso do Sul states, and Mimosaceae, Myrtaceae and Solanaceae in non-organic honey samples (Sereia et al. 2011Sereia JA, Alves EM, Toledo VAA, Marchini LC, Sekine ES, Faquinello P, Almeida D and Moreti AC. 2011. Physicochemical characteristics and pollen spectra of organic and non-organic honey samples of Apis mellifera L. An Acad Bras Cienc 83: 1077-1090.).

In general, the most representative families observed in honey samples of this study are similar to those verified in samples collected in other regions of the country that have similar vegetation.

From dominant pollen types, G. max (soybean) and Eucalyptus are from plants cultivated in the area. The two counties are located in agricultural regions where the main crops are corn and soybean. In 2008, the soybean harvest in these counties was 79,950 ha (Ipardes 2010IPARDES - Instituto Paranaense de Desenvolvimento Econômico e Social. 2010. Cadernos Municipais. Acessado em: 16 nov. 2010. Disponível em: http://www.ipardes.gov.br/modules/conteudo/conteudo.php?conteudo=5
http://www.ipardes.gov.br/modules/conteu... ). Chiari et al. (2005Chiari WC, Toledo VAAT, Ruvolo-Takasusuki MCC, Attencia VM, Costa FM, Kotaka CS, Sakaguti ES and Magalhães HR. 2005. Floral Biology and Behavior of Africanized Honeybees Apis mellifera in Soybean (Glycine max L. Merril). Braz Arch Biol Technol 48: 367-378., 2008)Chiari WC, Toledo VAA, Hoffmann-Campo CB, Ruvolo-Takasusuki MCC, Toledo TCSOA and Lopes TS. 2008. Polinização por Apis mellifera em soja transgênica [Glycine max (L.) Merrill] Roundup Ready™ cv. BRS 245 RR e convencional cv. BRS 133 Acta Sc Agron 30: 267-271. studied the pollination in soybean by A. mellifera and concluded that the visiting of flowers by these honeybees increases the production of this crop in some varieties.

Eucalyptus species are efficient sources to the formation of one type of honey approved by the customers and is the most frequent in the Brazilian market (Komatsu et al. 2002Komatsu SS, Marchini LC and Moreti AC. 2002. Análises Análises físico-químicas de amostras de méis de flores silvestres, de eucalipto e de laranjeira, produzidos por Apis mellifera L., 1758 (Hymenoptera, Apidae) no estado de São Paulo: conteúdo de açúcares e de proteína. Cienc Tecnol Aliment 22: 143-146., Sodré et al. 2003Sodré GS, Marchini LC, Moreti AC and Carvalho CAL. 2003. Análises multivariadas com base nas características físico-químicas de amostras de méis de Apis mellifera L. (Hymenoptera: Apidae) da região litoral norte no estado da Bahia. Arch Latinoam Prod Anim 11: 129-137.). The contribution of Eucalyptus as dominant pollen in honey samples was verified in others researches developed in the southeast region by Bastos et al. (2003)Bastos EMAF, Silveira VM and Soares AEE. 2003. Pollen spectrum of honey produced in cerrado areas of Minas Gerais state (Brazil). Braz J Biol 63: 599-615. in Cerrado in the State of Minas Gerais; by Barth et al. (2005)Barth OM, Maiorino C, Benatti APT and Bastos DHM. 2005. Determinação de parâmetros físico-químicos e da origem botânica de méis indicados monoflorais do sudeste do Brasil. Cienc Tecnol Aliment 25: 229-233. in samples of the states of São Paulo and Minas Gerais; by Luz et al. (2007)Luz CFP, Thomé ML and Barth OM. 2007. Recursos tróficos de Apis mellifera L. (Hymenoptera, Apidae) na região de Morro Azul do Tinguá, Estado do Rio de Janeiro. Rev Bras Bot 30: 29-36. in samples of the State of Rio de Janeiro and by Mendonça et al. (2008)Mendonça K, Marchini LC, Souza BA, Almeida-Anacleto D and Moreti AC. 2008. Plantas apícolas de importância para Apis mellifera L. (Hymenoptera: Apidae) em fragmento de Cerrado em Itirapina, SP. Neotropic Entomol 37: 513-521. in samples of the State of São Paulo. Pollen grains of Eucalyptus and Baccharis are among the cited types as geographical indicators of honey of the south of Brazil (Ramalho et al. 1991Ramalho M, Guibu LS, Giannini TC, Kleinert-Giovannini A and Imperartriz-Fonseca VL. 1991. Characterization of some southern Brazilian honey and bee plants through pollen analysis. J Api Res 30: 81-86.).

Highly eusocial bees, such as A. mellifera, collect resources preferentially in plants that exhibit a mass-flowering syndrome, with numerous flowers opening in short time (Wilms et al. 1996Wilms W, Imperatriz-Fonseca VL and Engels W. 1996. Resource partitioning between highly eusocial bees and possible impact for the introduced Africanized honey bee on native stingless bees in the Brazilian Atlantic Rainforest. Stud Neotrop Fauna & Environm 31: 137-151.). This feature can be observed in many cultivated plants and invader species, explaining the occurrence of these pollen types in various samples, even as dominant pollen in some months.

In this research, only 17.7% of the pollen types showed frequency higher than 15% at least in one honey sample. Cortopassi-Laurino and Ramalho (1988)Cortopassi-Laurino M and Ramalho M. 1988. Pollen harvest by Africanized Apis mellifera and Trigona spinipes in São Paulo. Botanical and ecological views. Apidologie 19: 1-24., analyzing samples of pollen collected by Apis mellifera on the outskirts of São Paulo city, also observed a low percentage of plants whose pollen accounted for more than 10% in the samples.

Sources of pollen with representativeness between 1% and 10% are resources with little attractiveness, corresponding to potential or secondary sources. These sources supplement the nutritional needs of the colony and may be important in environments where food resources suffer seasonal variations (Ramalho and Kleinert-Giovannini 1986Ramalho M and Kleinert-Giovannini A. 1986. Some aspects of the utilization of pollen analysis in ecological research. Apidologie 17: 159-174.).

The large number of pollen types with low frequency in the samples shows the importance of these plants in total honey production, representing a significant resource for the beekeeping of the region.

Bees have a highly developed sense of smell and they can be trained to look for a flavor or a particular mix of aromas. Once they become conditioned to seek a kind of plant, they will continue to get it (Free 1993Free JB. 1993. Insect pollination of crops. 2nd ed., London: Academic Press, 684 p.). Bees exhibit floral constancy, as a tendency to use fewer species than would be expected considering the number of flowering plants at the site (Cane and Sipes 2006Cane JH and Sipes S. 2006. Characterizing floral specialization by bees: analytical methods and a revised lexicon for oligolecty. In: WASER NM AND OLLERTON J (Eds), Plant-pollinator interactions: from specialization to generalization, Chicago: University of Chicago Press, p. 99-122.). However, according to Wilms et al. (1996)Wilms W, Imperatriz-Fonseca VL and Engels W. 1996. Resource partitioning between highly eusocial bees and possible impact for the introduced Africanized honey bee on native stingless bees in the Brazilian Atlantic Rainforest. Stud Neotrop Fauna & Environm 31: 137-151. Africanized bees are also quite general in the exploitation of floral resources, representing a wider niche than other eusocial bees.

The high values verified by the application of the Simpson Index indicate the probability of diversity of the sampled pollen, due to the dominance of one or a few species.

Samples of honey of this state are strongly heterofloral, and reported as frequent pollen types Allophylus, Baccharis, Campomonesia, Cecropia, Citrus, Eucalyptus, Matayba and Mimosa scabrela, Paspalum e Vernonia, with greater incidence of Eucalyptus (Ramalho et al. 1991Ramalho M, Guibu LS, Giannini TC, Kleinert-Giovannini A and Imperartriz-Fonseca VL. 1991. Characterization of some southern Brazilian honey and bee plants through pollen analysis. J Api Res 30: 81-86.).

Pollen grains of the type Baccharis (Asteraceae), of Euphorbiaceae and Asteraceae and type Eupatorium, were common in samples from Paraná State. Mimosa scabrela is typical from the region of Curitiba and pollen of the type Brassicaceae was also common in the samples (Carpes et al. 2009Carpes ST, Cabral ISR, Luz CFP, Capeletti JP, Alencar SM and Masson ML. 2009. Palynological and physicochemical characterization of Apis mellifera L. bee pollen in the Southern region of Brazil. J Food Agric Environ 7: 667-673.).

Approximately 52.5% of the pollen types verified in the honey samples are from native species of the region. Native species with bee value can be used in programs of recuperation of degraded areas. Although studies about this theme are not very common, Pegoraro and Ziller (2003)Pegoraro A and Ziller SR. 2003. Valor apícola das espécies vegetais de duas fases sucessionais da Floresta Ombrófila Mista, em União da Vitória, Paraná-Brasil. Bol Pesq Fl 47: 69-82. conducted a survey of species with bee value to provide subsidies to the restoration of a legal reserve. These authors reported some genera identified in this research, such as Mimosa, Eugenia and Zanthoxylum, as important to this purpose. Baggio (1988)Baggio AM. 1988. Aroeira como potencial para usos múltiplos na propriedade rural. Bol Pesq Fl 17: 25-32. and Wolff et al. (2007)Wolff L, Cardoso J, Schwengber J and schiedeck G. 2007. Sistema agroflorestal apícola envolvendo abelhas melíferas, abelhas indígenas sem ferrão, aroeira-vermelha e videiras em produção integrada no interior de Pelotas-RS: um estudo de caso. Rev Bras Agroecol 2: 1236-1239. indicated the application of aroeira, Schinus terebinthifolius, in agroforestry systems for beekeeping.

The use of native species by the bees was confirmed by the diversity of species found in this study, highlighting the importance of preserving native vegetation for the survival of the colonies during periods of supply scarcity of the floral resources of introduced species such as G. max and Eucalyptus spp.

CONCLUSION

In general, the honey collected in the region was heterofloral. Pollen types of cultivated crops were very representative, and the dominant pollen like Glycine max in December and January and Eucalyptus spp. in May and June. From the native species, Parapiptadenia rigida was dominant in November and February and Machaerium stipitatum in April.

Pollen types of other native species, such as Alchornea iricurana, A. triplinervea, Baccharis spp., Casearia sylvestris, Hexaclamys edulis, Schinus terebinthifolius, Serjania spp. and Zanthoxylum sp. were found as accessory pollen. If other pollen types, found as isolated pollen, were considered in group, they were very representative in the samples, highlighting the importance of the native vegetation for the survival of the colonies.

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Publication Dates

  • Publication in this collection
    01 Mar 2013
  • Date of issue
    Jan-Mar 2013

History

  • Received
    26 Apr 2011
  • Accepted
    6 July 2012
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