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Anais da Academia Brasileira de Ciências

Print version ISSN 0001-3765

An. Acad. Bras. Ciênc. vol.85 no.1 Rio de Janeiro Mar. 2013  Epub Mar 01, 2013

http://dx.doi.org/10.1590/S0001-37652013005000017 

Biological Sciences

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

ELIZABETE S. SEKINE1 

VAGNER A.A. TOLEDO2 

MARCELO G. CAXAMBU1 

SUZANE CHMURA1 

ELIZA H. TAKASHIBA3 

MARIA JOSIANE SEREIA1 

LUÍS C. MARCHINI4 

AUGUSTA C.C.C. MORETI5 

1Universidade Tecnológica Federal do Paraná/ UTFPR, BR 369, Km 0,5, 87301-006, Campo Mourão, PR, Brasil

2Departamento de Zootecnia, Universidade Estadual de Maringá/ UEM, Av. Colombo, 5790, 87020-900, Maringá, PR, Brasil

3Departamento de Ciências Florestais, Universidade Federal de Santa Maria (UFSM), Av. Roraima, 1000, 97105-900, Santa Maria, RS, Brasil

4Departamento de Entomologia e Acarologia, Escola Superior de Agricultura Luiz de Queiroz, Esalq/USP, Avenida Pádua Dias, 11, 13418-900, Piracicaba, SP, Brasil

5Instituto de Zootecnia, Rua Heitor Penteado, 56, 13460-000, Nova Odessa, SP, Brasil


ABSTRACT

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.

Key words: beekeeping; bee plants; floral resources; floristic survey

RESUMO

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.

Palavras-Chave: 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 1990). 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 1995).

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 1999, Moreti et al. 2000, Silva and Absy 2000, Bastos et al. 2003, Viana et al. 2006, Luz et al. 2007, Mendonça et al. 2008, Sodré et al. 2008) and analysis of visiting bees in plants (Marchini et al. 2001, Santos et al. 2006, Vieira et al. 2008).

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 1992). The predominant soil is Red Latosol (Brazilian classification: Latossolo Vermelho distroférrico, Embrapa 1999) 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 2009).

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 1989, IBGE 1992).

Five samples of each vegetal specie in blooming were collected and then herborized and identified (Cronquist 1981) 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. 1978, 1983, SPVS 1996, Roderjan et al. 1998).

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 1952). 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 1989, Moreti et al. 2002, Melhem et al. 2003, Roubik 2010). 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. 1978, Barth 1989): 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 1975) and Simpson (D) (Poole 1974) 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).

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

HCF Family/Specie Ordinary name Hb O SE B Months
J F M A M J J A S O N D
Acanthaceae
7282 Justicia brasiliana Roth. B N P
Alstroemeriaceae
7528 Bomarea edulis (Tuss.)Herb. ST N P
Amaranthaceae
7820 Alternanthera ficoidea (L.) P. Beauv. H .
Amaranthaceae
7827 Chamissoa altissima (Jacq.) H. B. Kunth H .
7919 Chamissoa sp. B N .
7280 Hebanthe paniculata Mart. ginseng B N P
Anacardiaceae
7980 Mangifera indica L. 4 mangueira T E P +
7754 Schinus terebinthifolius Raddi 2,4,6 aroeira pimenteira S N P +
Apiaceae
7645 Hydrocotyle leucocephala Cham. & Schltdl 3,4 acariçoba H N S +
Apocynaceae
7261 Condylocarpon isthmicum (Vell.) A. DC. ST N P
7646 Prestonia coalita (Vell.) Woodson Cipo-de-leite ST N P/S
7507 Rauwolfia sellowii Muell. Arg.
7243 Tabernaemontana catharinensis A.DC leiteiro T N P
Asclepiadaceae
7288 Asclepias curassavica L. H N P
Asteraceae
7536 Ageratum conyzoides L. H N S
7531 Baccharis dracunculifolia DC. 6,8 vassoura B N P +
7921 Baccharis microdonta DC. 1,2,8 vassoura B N P × ♦?
7266 Bidens pilosa L. 2,3,4 picão preto H N P +
8168 Calea pinnatifida (R.Br.) Less. SB N P
7819 Calyptocarpus biaristatus (DC.) H. Rob. H N S
7292 Centratherum punctatum Cass. H N P
7643 Chromolaena pedunculosa (Hook. & Arn.)R.M.&H. H N P
7523 Conyza bonariensis (L.) Cronquist 6 voadeira H N P ×
7920 Dasyphyllum brasiliense (Spr.) Cabr. sucará SB N Sl
7291 Elephantopus mollis Kunth6 sarsuiá H N P ×
7267 Emilia sonchifolia (L.) DC.2,3,4 emilia H N P +
8173 Galinsoga parviflora Cav. H N P
8109 Mikania cordifolia (L.f)Willd.4 cipó-guaco ST N P +
7752 Mikania micrantha Kunth9 cipó-guaco ST N P/Si ×
7651 Parthenium hysterophorus L.3 losna-branca H N P +
7247 Senecio brasiliensis (Spreng.) Less.2,4,6,7 berneira H N P +
8112 Sonchus asper (L.)Hill. Serralha-brava H N P
8111 Sonchus oleraceus L.4 serralha H N P +
7278 Wedelia subvelutina DC. H N P
Begoniaceae
7390 Begonia cucullata Willd. azedinha H N S
7242 Adenocalymma marginatum (Cham.) DC. CT N P
7548 Arrabidaea chica (Humb. & Bonpl.) B.Verlot CT N P
B.Verlot
7505 Arrabidaea selloi (Spreng.) Sandw. CT N P
8172 Clytostoma sciuripabulum Bareau & K.Schum CT N P
8169 Jacaranda puberula Cham.5 caroba T N P ×
7549 Macfadyena unguis-cati (L.) A. H. Gentry unha-de-gato CT N P
7391 Mansoa difficilis (Cham.) Bureau. & K.Schum.8 mansoa CT N S ×
7276 Pyrostegia venusta (Ker Grawl) Miers4,6,9 cipó-de-são-joão CT N P +
8211 Tecoma stans (L.)Adr. Juss. ex Kunth B E P
7253 Tynanthus micranthus Mello ST N P/Si
Bixaceae
7530 Bixa orelana L.5 urucum T N P +
Boraginaceae
7527 Cordia ecalyculataVell. Café de bugre S N P
7751 Cordia trichotoma (Vell.) Arrab. ex Steud.4 óleo-pardo, louro-pardo T N P +
7251 Heliotropium transalpinium Vell. H N P
Brassicaceae
8059 Brassica napus L. H .
8064 Raphanus sativus L. H .
Cactaceae
7400 Brasiliopuntia brasiliensis (Willd.) Berg. cacto SB N P
7644 Pereskia aculeata Mill. ora-pronobilis SB N P/S
8105 Rhipsalis cereuscula (How)Volguin Rabo-de-rato EPI N S
Caesalpinaceae
7521 Bauhinia forficata Link2,4,5,8 pata-de-vaca S N P ×
7750 Phanera microstachya (Raddi) L.P. CT N . ×
8217 Caesalpinia peltophoroides Benth.1,2,3,4,5,8 sibipiruna T N P +
7822 Senna neglecta (Vogel) Irwin & Barneby4,5 chuva-de-ouro B N P ×
Caricaceae
7525 Carica papaya L.4 mamoeiro T E P +
Cecropiaceae
7509 Cecropia pachystachya Trécul.8 embaúba T N P ×
Clusiaceae
7399 Clusia sp. B E P
Combretaceae
7538 Combretum fruticosum (Loef.) Stunz escova-de-macaco TE N P
Combretaceae
8163 Terminalia australis Cambess4 amarilho, sarandi T N S ×
Commelinaceae
7534 Dichorisandra hexandra (Aubl.) Standl H N Sl
7641 Tripogandra diuretica (Mart.) Handlos H N P/S
Convolvulaceae
7826 Ipomoea nil (L.)Roth4 corda-de-viola ST N P ×
Convolvulaceae
7647 Ipomoea quamoclit L.4 esqueleto ST N P ×
Cucurbitaceae
7376 Momordica charatia L.4 CT E P +
7260 Wilbrandia longisepala Cogn. CT N P
Cyperaceae
7386 Cyperus luzulae (L.) Retz N P
Ebenaceae
8219 Diospyrus kaki L.f. caqui E P
Ericaceae
7373 Rhododendron simsii Planch.4 azaléia B E S +
Euphorbiaceae
8214 Alcalypha gracilis Spreng.3 tapa-buraco H N S ×
7924 Alchornea iricurana Cass.8 fruta-de-pombo T N P ×
7252 Alchornea triplinervia (Spreng.) M. Arg.8 tapiá, tanheiro T N P ×
7650 Bernardia pulchella (Baill.) Muell. Arg. B N S
7285 Dalechampia stipulacea Muell. Arg. Cipó-urtiga ST N P
7979 Manihot esculenta Crantz.6 mandioca B N P +
7262 Ricinus communis L.2,5,6,8 mamona S E P +
7992 Sebastiania brasiliensis Spreng. leiteiro, branquilho S N S ×
Fabaceae
7504 Dalbergia frutescens (Vell.) Britton. cipó-rabo-de-bugio N P/Sl
7392 Desmodium incanum DC.1,2,3 carrapicho N P ×
7384 Glycine max (L.) Merr.4 Soja E P +
7506 Lonchocarpus campestris Mart. ex Benth. paufarinha T N P
7378 Lonchocarpus subglaucescens Benth. N Sl
7818 Machaerium stipitatum (DC.) Vogel8 sapuva N P/S ×
8171 Myrocarpus frondosus Fr. Allem. T N S
7749 Vigna venusta (Piper) Maréchal & al. ST P
Flacourtiaceae
7283 Banara tomentosa Clos. T N Sl
8060 Casearia sylvestris Sw. cafezeiro-bravo T N P
7254 Prockia crucis P. Browne ex L. T N S
Iridaceae
7289 Sisyrinchium luzula Klotzsch H N P
Lamiaceae
7245 Leonurus sibirucus L.4 rubi H E P ×
7821 Hyptis mutabilis (L.C.Rich) Briq.6,8 boldo-branco H N P ×
Lauraceae
7397 Nectandra lanceolata Nees & Mart. ex Nees canela-amarela T N S
8065 Nectandra megapotamica (Spr.) Mez T .
7918 Ocotea puberula (Rich.) Nees T N P
8110 Persea americana Mill.4,6,8 abacateiro T E P +
Liliaceae
7916 Asparagus setaceus (Kunth.) Jessop. aspargo-ornamental ST E P
Loganiaceae
7290 Strychnos brasiliensis (Spr.) Mart. anzol-de-lontra B N P/Si
Lythraceae
7377 Lagerstroemia indica L. Resedá T E P
7372 Punica granatum L. romã B E P
Malpighiaceae
7526 Banisteriopsis adenopoda (Adr.Juss) B.Gates SB N P
7522 Banisteriopsis parviflora (Adr.Juss.) Gates6 SB N P ×
7503 Dicella nucifera Chodat SB N P
7533 Heteropterys intermedia (Adr. Juss.) Griseb ST N P
7244 Mascagnia ovatifolia (Kunth.) Griseb. .
7540 Stigmaphyllon jatrophifolium Adr. Juss. ST N P
7753 Indeterminada sp.5 .
Malvaceae
7375 Abutilon striatum Dicks ex Lindl. lanterna-japonesa B N P
7978 Bastardiopsis densiflora (Hook. & Arn.) Hassler T N P
7264 Malvastrum coromandeliam (L.) Garcke4 guanxuma SB N P +
7287 Sida rhombifolia L.3,6 guanxuma H N P +
7381 Wissadula subpeltata (OK)R.E.Fries4 malva-estrela B N P +
Marantaceae
7539 Maranta sobolifera L. Anderss. H N Si
Melastomataceae
7274 Ossaea amygdaloides (DC.) Triana B N .
Meliaceae
8213 Cabralea canjarana (Vell.) Mart. canjarana T N P
8113 Melia azedarach L. santa-bárbara T E P
7257 Trichilia elegans A.Juss B N S
Meliaceae
8004 Trichilia pallida Swartz. B N S
Mimosaceae
8164 Calliandra foliolosa Benth.4 esponjinha S N S +
7265 Enterolobium contorstisiliquum (Vell.) Morong orelha-de-nego, T N Si +
7277 Leucaena leucocephala (Lam.) de Wit.1,2,3,4 leocena S E P +
7394 Mimosa pudica L.1,4,6,8 dormideira T N P +
7268 Parapiptadenia rigida (Benth.) Brenan angico-vermelho T N P
Moraceae
7284 Maclura tinctoria (L.) D.Don ex Steud. amora-branca T N S
Myrtaceae
7990 Calycorectes psidiiflorus (O.Berg) Sobral B N Si
7250 Campomanesia guazumifolia (Camb.) O. Berg. sete-capotes T N P
7371 Campomanesia xanthocarpa O Berg. guabiroba T N S
7993 Casearia gossypiosperma Briq (Salicaceae) .
(Salicaceae)
7828 Eucalyptus saligna Smith.3,4,6,8,9 eucalipto T E P +
7529 Eucalyptus viminalis Labill.3,4,6,8,9 eucalipto T E P ×
7547 Eucalyptus sp.1 3,4,6,8,9 eucalipto T E P ×
7395 Eucalyptus sp.2 3,4,6,8,9 eucalipto T E P ×
7914 Eugenia hiemalis Cambess.4 jabuticabeira T N P ×
8099 Eugenia sp.2,4,5 N P × ♦?
7270 Hexaclamys edulis (O. Berg) Kausel & D. Legrand pêra-do-mato B N P
8167 Myrcia laruotteana Cambess6,9 guamirim B N . ×
7273 Psidium guajava L.1,3,4 goiabera S N P +
8166 Indeterminada sp.1 .
8215 Indeterminada sp.2 .
Onagraceae
7823 Ludwigia octovalvis (Jacq.) Raven Cruz-de-malta SB N P
7855 Ludwigia sp. Cruz-de-malta SB N P
Orchidaceae
8114 Dendrobium nobile Lindl. orquidea EPI E P
Oxalidaceae
7915 Averrhoa carambola L. carambola T E P
8100 Oxalis sp 1.4 trevo H N P ×
8103 Oxalis sp 2. trevo H P
Passifloraceae
7913 Passiflora amethystina Mikan Maracujá-de-raposa CT N P
Pedaliaceae
7917 Sesamum indicum L.4 gergelim H E P +
Phytolaccaceae
7532 Seguieria guaranitica Spegazzini ST N P
Piperaceae
7246 Piper amalago L.8 parapiroba B N P ×
7255 Piper gaudichaudianum Kunth.8 parapiroba B N P ×
Polygonaceae
7824 Polygonum punctatum Elliot. H N P
7293 Ruprechtia laxiflora Meissn. B N .
Polypodiaceae
8107 Pleopeltis angusta Humb. & Bonpl. Ex Willd. H N S
Portulacaceae
7398 Talinum paniculatum (Jacq.) Gaertn. H E S
Rhamnaceae
7825 Gouania ulmifolia Hook. et Arn. CT N P
7272 Hovenia dulcis Thunberg4 uva-japão T E P +
Rosaceae
7649 Eriobotrya japonica Lindley nespera; ameixa-amarela T E P
8005 Prunus mume Sielbold & Zucc. umê T E P ×
7829 Prunus persica (L.) Batsch.4,5 pessegueiro T E P +
7275 Prunus sellowii Koehne pessegueiro-bravo T N P +
8218 Rubus ulmifolius Schott groselha B N P
7295 Rubus urticaefolius Poiret amora-silvestre B N P
Rubiaceae
7396 Manettia luteo-rubra (Vell.) Benth. N P
7258 Psychotria carthagenensis Jacq.3 café-de-bugre AB N Si +
Rutaceae
8001 Citrus limonia Osbeck3,4,5,9 limão-rosa S E P + ♦?
8006 Citus sinensis (L.) Osbeck1,4,6,9 laranja T E P +
8002 Pilocarpus pennatifolius Lemaire S N S
8165 Zanthoxylum caribaeum Lam.14, 8 mamica-de-porca T N P ×
8174 Zanthoxylum fagara (L.) Sarg.4,8 Mamica-de-porca T N P ×
Sapindaceae
8102 Allophylus edulis (St.Hil.)Radlk. 4,8 vacum, chau-chau S N S +
7544 Cardiospermum grandiflorum Sweet. saco-de-padre CT N P
7923 Cupania vernalis Camb. camboatá T N Si
8212 Matayba elaeagnoides Radlk. camboatá-branco T N Si +
7271 Paullinia meliifolia Adr.juss. N P
7854 Serjania acoma Radlk cipó-timbó CT N P
7922 Serjania multiflora Camb.6,9 cipó-timbó CT N Si ×
Sapindaceae
7524 Serjania reticulata Cambess. cipó-timbó CT N Sl
Scrophulariaceae
7981 Paulownia tomentosa (Thunb.)Steud. kiri T E P
Simaroubaceae
7991 Castela tweedii Planchon B N P
Solanaceae
7537 Brugmansia suaveolens (Willd.) Bercht. & Presl. copo-de-leite B E Si
7379 Capsicum baccatum L. pimenteira B N P
8062 Cestrum corymbosum Sch. coerana B N Si
7502 Cestrum strigillatum Ruiz & Pavón coerana SB N P
7249 Solanum americanum Mill. 4 maria-preta H N P +
7387 Solanum atropurpureum Schrank2,3 jurubeba H N P ×
7279 Solanum mauritianum Scop.2,3 fumo-bravo T N Si x ♦?
7545 Solanum paniculatum L.2,3 jurubeba B N Si x
7543 Solanum sanctae-catharinae Dunal. 2,3 juá-manso S N P x
7248 Solanum sisymbriifolium Lam.2,3 juá SB N P x
7551 Vassobia breviflora (Sandtn.) A.T. Hunziker N P
8063 Indeterminada sp.1 .
Symplocaceae
8216 Symplocos uniflora (Pohl.) Benth. Orelha-de-onça T .
Tiliaceae
8003 Heliocarpus americanus L.5 jangada B N P +
7642 Luehea divaricata Mart. 4 açoita-cavalo T N P +
Ulmaceae
7263 Trema micrantha (L.) Blume4 pau-de-polvora B N P +
Urticaceae
7259 Boehmeria caudata Sw. B N P
7501 Urera baccifera (L.) Gaudich ex Wedd. urtiga-mansa B N P
Verbenaceae
8061 Aegiphila mediterranea Vell. tamanqueiro T N P
7389 Aegiphila sp. T N P
7269 Aloysia virgata (R. & P.) A.L. Juss.3,4 lixeirinha B N P + ♦?
7374 Clerodendron x speciosum Tiejism. & Binn.4 lágrima-de-n. senhora ST E P x
7382 Duranta repens L.4 pingo-de-ouro B N P/Si +
7256 Lantana camara L.4 lantana B N P +
8162 Petrea subserrata Cham.4 petrea B N Sl x
7294 Stachytarpheta cayennensis (L.C.Rich)Vahl. H N S
Violaceae
7550 Hybanthus bigibbosus (A. St. Hil.)Hassl. canela-de-veado B N Si
7546 Hybanthus communis (A. St. Hil.)Taub. canela-de-veado H N Si

Plants of apiarist importance in the South and southeast regions:

1 Cortopassi-Laurino and Ramalho (1988);

2 Ramalho et al. (1990);

3 Carvalho et al. (1999);

4 Marchini et al. (2001);

5 Agostini and Sazima (2003);

6 Bastos et al. (2003);

7 Barth (2004);

8 Luz et al. (2007);

9 Mendonça et al. (2008). Hb = Habit: B = bush, CT = climber with tendrils, Ep = epiphyte, H = herb, S = small tree, SB = sub-bush, ST = stem twiners, T = three; O = origin place: N = native species; E = exotic species; SE = Ecological succession: P = pioneer, S= secondary, Si = initial secondary, Sl = late secondary; B = bee plant: species (+) or genera (×) reported in the literature as with apiarist importance; ♦ = Plants photographed and collected in this work; • = Plants collected to Paraná state, with Register at the Herbarium of the Universidade Tecnológica Federal do Paraná in Campo Mourão (HCF).

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. 

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. 

Family Pollen type Dec Jan Fev/Mar Apr May Jun Jul Aug Sep Oct Nov FO
A B A B C A B C A B C A B C A B C A B A C A B C A B C A B C
Amaranthaceae Amaranthaceae type 1 O O O I I O 20
Amaranthaceae type 2 O O O O 10
Anacardiaceae *Schinus terebinthifolius O O I O O O I I O A A 37
Mangifera indica O 3
Arecaceae Arecaceae type O A I I I O I O O I I I I I A A O A O A A O I 77
Asteraceae *Baccharis spp. I I O I O I I O O O O 37
*Bidens spp. O O 7
*Centratherum punctatum O 3
*Calyptocarpus biaristatus O O 7
*Conyza bonariensis O 3
*Chromolaena pedunculosa I O I O I I O 23
*Mikania spp. I I O O I I 20
*Senecio brasiliensis O I 7
*Sonchus sp. O O O O O 17
Asteraceae type O O 7
Vernonia sp. I O O O O O O O 27
Araceae Araceae type O A O O 13
Bignoniaceae Bignoniaceae type I 3
Boraginaceae *Cordia ecalyculata O 3
*Cordia trichotoma O I I 10
Brassicaceae Brassicaceae spp. I I O O O O A O I D A I A A A O A I 60
Caesalpinaceae *Bauhinia forficata O O O O 13
*Bauhinia sp. O O 7
Combretaceae *Combretum fruticosum O O 7
*Terminalia australis I I O I 13
Convolvulaceae Convolvulaceae type O I O O 13
Euphorbiaceae *Alchornea iricurana A A I 10
*Alchornea triplinervea A O O O O O A I O 30
Euphorbiaceae *Bernardia pulchela O O 7
Ricinus communis O O I O I O O O 27
*Sebastiania brasiliensis I I O O O 17
Fabaceae Glicyne Max I D A D A O A O A O I 37
*Lonchocarpus sp. I I I O O I 20
Fabacea type O O O 10
*Machaerium stipitatum A D O I O 17
*Myrocarpus frondosus I O I 10
Stylosanthes sp. I O O I 13
Flacourtiaceae *Casearia sylvestris O I O O A I I 23
Lamiaceae Leonurus sibiricus O O O O O O I O O O 33
*Hyptis mutabilis O
Malpighiaceae Malpighiaceae type O 3
Malvaceae *Wissadula subpeltata O O O O 13
Meliaceae Melia azedarach O A D I O O 20
Mimosaceae *Acacia type O O O I O I I I O I 30
*Parapiptadenia rigida O O O O D I I I O A A D D 43
*Mimosa sp. O O I O O O O 23
Leucaena leucocephala O O O O O O O O O 30
Moraceae Tipo Moraceae O O 7
Myrtaceae Eucalyptus spp. O O O I O O I D A A A D D D A D D A A I I I I I I I O 90
*Campomanesia spp. I O O 10
*Hexaclamys edulis I O I I O I I I O 30
*Myrcia type O O I O A O O A I 30
Oleaceae Ligustrum sp. O O O O 13
Piperaceae *Tipo Piperaceae A O O O A I I O I O 33
Rhamnaceae *Gouania I I 7
Hovenia dulcis O O O O 13
Rhamnaceae type I A A O 13
Rosaceae Rosaceae type O 3
Eriobotrya japônica O I I 10
*Prunus sellowii O O I I I O 20
Rubiaceae Borreria sp. O O 13
*Psychotria carthagenensis O 7
Rutaceae Citrus sp. 1 O 7
Citrus sp. 2 O O 13
*Zanthoxylum sp. O I O O I I I O I 30
Sapindaceae *Allophylus edulis O I O I 13
*Cardiospermum grandiflorum O 7
*Cupania vernalis O 7
*Matayba elaeagnoides O O 13
*Serjania spp. I O O I O O I O I O O O I O 47
Solanaceae *Solanum sanctae-catharinae O 3
Solanaceae type O 3
*Solanum mauritianum O 3
Tiliaceae *Luehea divaricata O 3
*Heliocarpus americanus I O 7
Ulmaceae *Trema micrantha O O I 10
Non identified 1 I 3
Non identified 2 I I 7
Non identified 3 A A 7

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.

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). 

Index Apiary A Apiary B Apiary C
Shannon 3.893a 3.770a 3.603b
Simpson 0.975 0.971 0.967

Values followed by the same letters, in the same line, did not differ among themselves at the level of 5% of significance.

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) 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) 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 2009) 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. 1990). 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 2001).

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) in São Paulo State as the best representatives; and Asteraceae, Myrtaceae, Mimosaceae and Verbenaceae found by Marchini et al. (2001) as the most representative families in São Paulo State.

Bastos et al. (2003) 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) 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. 2011).

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 2010). Chiari et al. (2005, 2008) 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. 2002, Sodré et al. 2003). 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) in Cerrado in the State of Minas Gerais; by Barth et al. (2005) in samples of the states of São Paulo and Minas Gerais; by Luz et al. (2007) in samples of the State of Rio de Janeiro and by Mendonça et al. (2008) 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. 1991).

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. 1996). 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), 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 1986).

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 1993). 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 2006). However, according to Wilms et al. (1996) 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. 1991).

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. 2009).

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) 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) and Wolff et al. (2007) 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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Received: April 26, 2011; Accepted: July 6, 2012

Correspondence to: Elizabete Satsuki Sekine, E-mail: essekine@gmail.com

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