Physicochemical composition and antioxidant potential of bee pollen from different botanical sources in Alagoas, Brazil

Bee pollen results from the mixture of pollen and floral nectar with the salivary substances of bees and has increasingly been used as a food with therapeutic properties. In this study, 30 samples of bee pollen from Apis mellifera apiaries in three mesoregions of Alagoas (Brazil) - Mata Atlântica, South Coast and Caatinga, were collected during the dry season of 2008/09 and analysed. Mata Atlântica and Caatinga had good production of bee pollen. In the same season, Mata Atlântica contained a higher diversity of pollen types for feeding bees with a predominance of herbaceous pollen (63%), whereas the Caatinga samples contained monofloral pollen. Physicochemical data were analysed with the nonparametric Kruskal-Wallis statistical test. The Caatinga samples were analysed to determine their contents of total phenolic compounds (25.85 ± 10.80 mg gallic acid eq/g) and flavonoids (45.62 ± 32.19 mg quercetin eq/g) and their antioxidant activity (for instance, 70.62 ± 4.50% in the DPPH test), which were possibly affected by the environmental conditions of this biome.

Index terms:
Apis mellifera; total phenolics; floral origin.

Authorship

Maria Raphaella dos Santos Vasconcelos

Universidade Federal de Alagoas/UFAL, Instituto de Química e Biotecnologia/IQB, Maceió, AL, BrasilUniversidade Federal de Alagoas/UFALBrazilMaceió, AL, BrazilUniversidade Federal de Alagoas/UFAL, Instituto de Química e Biotecnologia/IQB, Maceió, AL, Brasil

Alysson Wagner Fernandes Duarte

Universidade Federal de Alagoas/UFAL, Arapiraca, AL, BrasilUniversidade Federal de Alagoas/UFALBrazilArapiraca, AL, BrazilUniversidade Federal de Alagoas/UFAL, Arapiraca, AL, Brasil

Elane Pereira Gomes

Silvio Chagas da Silva

Universidade Federal de Alagoas/UFAL, Instituto de Ciências da Computação, Maceió, AL, BrasilUniversidade Federal de Alagoas/UFALBrazilMaceió, AL, BrazilUniversidade Federal de Alagoas/UFAL, Instituto de Ciências da Computação, Maceió, AL, Brasil

Ana Maria Queijeiro López ^**Corresponding author: amql@qui.ufal.br

^*Corresponding author: amql@qui.ufal.br

SCIMAGO INSTITUTIONS RANKINGS

Universidade Federal de Alagoas/UFAL, Arapiraca, AL, BrasilUniversidade Federal de Alagoas/UFALBrazilArapiraca, AL, BrazilUniversidade Federal de Alagoas/UFAL, Arapiraca, AL, Brasil

Figures | Tables

Figures (2)
Tables (5)

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Figure 1:
The average bee pollen daily production during the dry season (2008/09) in apiaries from Mata Atlântica (“MA”), South Coast (“SC”) and Caatinga (“C”) mesoregions of Alagoas, Brazil.

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Figure 2:
Photomicrographs of pollen types (magnitude 640 ×) in bee pollen collected during the dry season (2008/09) from different mesoregions of Alagoas (Northeastern Brazil). 1-2: Prosopis juliflora (Sw.) DC.; 3: Mimosa misera Benth.; 4-6: M. tenuiflora (Willd.) Poir; 7: M. caesalpinifolia Benth.; 8: Croton moritibensis Baill.; 9-10: Ziziphus joazeiro Mart; 11-12: Erythrina velutina Willd; 13: Centratherum punctatum Cass.; 14: Hyptis suaveolens (L.) Poit; 15: Maytenus rigida Mart.; 16: Sida sp.; 17-18: Elephantopus mollis Kunth.; 19-20: Coutarea hexandra(Jacq.)K. Schum.; 21: Spondias mombin L.; 22: Piptadenia macrocarpa Benth.; and 23: Croton sonderianus Muell.

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Table 1:
Average altitude, temperature, and daily rainfall precipitation (dry season) in the Mata Atlântica (MA), Caatinga (C) and South Coast (SC) mesoregions of Alagoas, Brazil where the bee-pollen of Africanized bees were collected (dry season - 2008/09).

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Table 2:
Botanical species/family and their relative frequencies (%) of pollen found during the dry season (2008/09) in apiaries from the mesoregions of Mata Atlântica (“MA”), Caatinga (C) and South Coast (“SC”) of Alagoas, Brazil.

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Table 3:
Total proteins, carbohydrates and lipids in bee pollen collected during the dry season (2008/09) in the mesoregions Mata Atlântica (“MA”), South Coast (“SC”) and Caatinga (C) of Alagoas, Brazil.

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Table 4:
Total content of phenolics, flavonoids and antioxidants (determined by the FRAP method and percentage inhibition of free radicals by the DPPH assay) from bee pollen samples collected from Mata Atlântica (“MA”), Caatinga (“C”) and the South Coast (“SC”) of Alagoas, Brazil during the dry season (2008/09).

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Table 5:
Spearman coefficient correlation between the parameters evaluated in the bee pollen samples collected from the mesoregions of Mata Atlântica (“MA”), South Coast (“SC”) and Caatinga (“C”) of Alagoas, Brazil during the dry season (2008/09).

Figure 1: The average bee pollen daily production during the dry season (2008/09) in apiaries from Mata Atlântica (“MA”), South Coast (“SC”) and Caatinga (“C”) mesoregions of Alagoas, Brazil.

Figure 2: Photomicrographs of pollen types (magnitude 640 ×) in bee pollen collected during the dry season (2008/09) from different mesoregions of Alagoas (Northeastern Brazil). 1-2: Prosopis juliflora (Sw.) DC.; 3: Mimosa misera Benth.; 4-6: M. tenuiflora (Willd.) Poir; 7: M. caesalpinifolia Benth.; 8: Croton moritibensis Baill.; 9-10: Ziziphus joazeiro Mart; 11-12: Erythrina velutina Willd; 13: Centratherum punctatum Cass.; 14: Hyptis suaveolens (L.) Poit; 15: Maytenus rigida Mart.; 16: Sida sp.; 17-18: Elephantopus mollis Kunth.; 19-20: Coutarea hexandra(Jacq.)K. Schum.; 21: Spondias mombin L.; 22: Piptadenia macrocarpa Benth.; and 23: Croton sonderianus Muell.

Table 1: Average altitude, temperature, and daily rainfall precipitation (dry season) in the Mata Atlântica (MA), Caatinga (C) and South Coast (SC) mesoregions of Alagoas, Brazil where the bee-pollen of Africanized bees were collected (dry season - 2008/09).

Cities (Mesoregions)	Samples (Code)	Altitude (m) ^a		Temperature (°C) ^a		Rainfall (mm) ^a
Viçosa (Mata Atlântica - MA)	MA	210		29		1500.0
Batalha (Caatinga - C)	C	256		31		481.3
Barra de São Miguel (South Coast - SC)	SC	2		29		2050.0
		Average daily precipitation (mm/day) ^a
		Months (October - February)
	(Code)	Oct	Nov	Dec	Jan	Feb
Viçosa (Mata Atlântica - MA)	MA	0.61	0	0	0.1	0.1
Batalha (Caatinga - C)	C	0	0	0	1.11	0
Barra de São Miguel (South Coast - SC)	SC	0.3	0.3	0.7	1.5	6.8

^aSecretaria de Recursos Hídricos e Meio Ambiente do Estado de Alagoas (SRHMA, 2009).

Table 2: Botanical species/family and their relative frequencies (%) of pollen found during the dry season (2008/09) in apiaries from the mesoregions of Mata Atlântica (“MA”), Caatinga (C) and South Coast (“SC”) of Alagoas, Brazil.

Mesoregions	Samples (Codes)	Harvesting Month	Bee pollen Botanical species/Family	Relative Frequency (%)
Mata Atlântica (MA)	MA 1	September	Mimosa misera / Mimosaceae	68%
	MA 2	October	Mimosa misera / Mimosaceae	92%
	MA 3	October	Mimosa misera / Mimosaceae	79%
	MA 4	November	Mimosa misera / Mimosaceae	72%
	MA 5	November	Mimosa misera / Mimosaceae	70%
	MA 6	December	Mimosa caesalpinifolia / Mimosaceae	38%
	MA 7	December	Mimosa caesalpinifolia / Mimosaceae	25%
	MA 8	January	Erythrina velutina / Fabaceae	51%
	MA 9	January	Ziziphus joazeiro / Rhamnaceae	78%
	MA 10	February	Not identified /--	100%
Caatinga (C)	C 1	October	Prosopis juliflora / Fabaceae	100%
	C 2	October	Prosopis juliflora / Fabaceae	100%
	C 3	November	Prosopis juliflora / Fabaceae	50%
	C 4	November	Prosopis juliflora / Fabaceae	50%
	C 5	November	Mimosa tenuiflora / Mimosaceae	100%
	C 6	December	Piptadenia macrocarpa / Fabaceae	45%
	C 7	December	Piptadenia macrocarpa / Fabaceae	100%
	C 8	January	Not identified 1	49%
	C 9	January	Not identified 2	50%
	C 10	February	Not identified 1	97%
South Coast (SC)	SC 1	October	Coutarea hexandra / Rubiaceae	60%
	SC 2	October	Hyptis suaveolens / Lamiaceae	76%
	SC 3	October	Hyptis suaveolens / Lamiaceae	64%
	SC 4	November	Coutarea hexandra / Rubiaceae	80%
	SC 5	November	Hyptis suaveolens / Lamiaceae	68%
	SC 6	December	Coutarea hexandra / Rubiaceae	52%
	SC 7	December	Coutarea hexandra / Rubiaceae	70%
	SC 8	January	Not identified/-	78%
	SC 9	January	Maytenus rígida / Celastraceae	76%
	SC 10	February	Coutarea hexandra / Rubiaceae	100%

Table 3: Total proteins, carbohydrates and lipids in bee pollen collected during the dry season (2008/09) in the mesoregions Mata Atlântica (“MA”), South Coast (“SC”) and Caatinga (C) of Alagoas, Brazil.

Samples	Harvesting Month	Proteins (mg. Eq BSA/g)	Carbohydrates (mg/g)	Lipids (%)^*	pH
MA 1	September	138.0	422.0	4.38	4.9
MA 2	October	122.0	355.0	4.38	4.9
MA 3	October	222.0	504.0	5.46	5.1
MA 4	November	214.0	520.0	5.46	5.2
MA 5	November	228.0	556.0	5.62	5.6
MA 6	December	125.0	228.0	5.62	5.5
MA 7	December	170.0	296.0	4.07	5.6
MA 8	January	135.0	376.0	4.07	5.8
MA 9	January	129.0	385.0	5.00	5.7
MA10	February	129.0	225.0	5.00	5.7
Mean (MA) ± SD		162.0 ± 43.0 ^a	386.7 ± 106.2	4.91 ± 0.006 ^a	5.4 ± 0.3
C 1	October	148.0	412.0	5.07	5.8
C 2	October	127.0	506.0	5.07	5.8
C 3	November	152.0	384.0	4.92	6.3
C 4	November	131.0	528.0	4.92	6.1
C 5	November	125.0	403.0	7.74	6.0
C 6	December	83.0	377.0	7.74	6.4
C 7	December	117.0	339.0	6.38	6.4
C 8	January	112.0	458.0	6.38	6.1
C 9	January	111.0	405.0	5.50	6.2
C10	February	116.0	509.0	5.50	5.9
Mean (C) ± SD		122.0 ± 19.0 ^a	432.1 ± 64.3	5.92 ± 0.010 ^a	6.1 ± 0.2
SC 1	October	154.0	338.0	3.39	4.9
SC 2	October	132.0	539.0	3.39	5.2
SC 3	October	150.0	549.0	2.98	5.3
SC 4	November	138.0	469.0	2.98	5.1
SC 5	November	121.0	541.0	3.37	5.5
SC 6	December	168.0	401.0	3.37	5.5
SC 7	December	124.0	520.0	2.98	5.7
SC 8	January	225.0	535.0	2.98	5.9
SC 9	January	332.0	470.0	3.02	5.9
SC10	February	212.0	252.0	3.02	5.9
Mean (SC) ± SD		176.0 ± 65.0 ^a	461.4 ± 100.9	3.15 ± 0.002 ^a	5.5 ± 0.3

*Total lipids evaluated every two samples. a 95% significance (p<0.05) according to the Kruskal-Wallis test.

Table 4: Total content of phenolics, flavonoids and antioxidants (determined by the FRAP method and percentage inhibition of free radicals by the DPPH assay) from bee pollen samples collected from Mata Atlântica (“MA”), Caatinga (“C”) and the South Coast (“SC”) of Alagoas, Brazil during the dry season (2008/09).

Samples	Harvesting Month	Phenolics (mg GA eq/g)	Flavonoids (mg Q eq/g)	FRAP (mg GA eq/g)	DPPH (%)
MA 1	September	7.90	6.04	4.73	66.95
MA 2	October	7.97	22.38	4.73	69.64
MA 3	October	19.24	30.60	16.85	63.03
MA 4	November	20.73	33.64	27.08	68.05
MA 5	November	22.76	25.20	61.17	77.96
MA 6	December	20.85	71.72	83.14	77.60
MA 7	December	20.48	37.74	85.03	72.46
MA 8	January	21.05	52.68	88.06	76.86
MA 9	January	21.60	64.80	123.67	75.55
MA10	Februar	20.55	67.40	141.85	76.55
Mean (MA) ±SD		18.31 ± 5.54 ^a	41.22 ± 21.94	63.63 ± 49.02 ^a	72.46 ± 5.25 ^a
C 1	October	21.88	17.62	101.32	75.03
C 2	October	16.22	26.70	77.08	66.95
C 3	November	18.54	38.18	88.44	70.62
C 4	November	20.80	28.00	109.66	66.95
C 5	November	16.84	81.68	89.96	68.05
C 6	December	29.71	53.98	225.94	66.95
C 7	December	46.25	107.00	237.31	66.58
C 8	January	21.20	13.28	250.19	66.95
C 9	January	43.78	73.46	81.63	75.57
C10	February	23.31	16.32	53.22	78.58
Mean (C) ± SD		25.85 ± 10.80 ^a	45.62 ± 32.19	131.47 ± 75.08 ^a	70.22 ± 4.50 ^a
SC 1	October	8.12	22.82	40.71	70.62
SC 2	October	8.66	16.10	10.03	42.59
SC 3	October	6.54	1.82	46.40	42.35
SC 4	November	5.94	34.28	41.09	50.30
SC 5	November	7.37	8.52	35.41	53.36
SC 6	December	6.01	28.00	37.30	63.89
SC 7	December	7.20	34.06	61.92	74.66
SC 8	January	5.85	26.92	73.67	54.71
SC 9	January	13.98	24.54	103.22	75.47
SC10	February	6.05	34.28	43.75	74.67
Mean (SC) ± SD		7.57 ± 2.45 ^a	23.13 ± 11.18	49.35 ± 25.21^a	60.26 ± 13.23^a

^a95% significance, (p<0.05), according to the Kruskal-Wallis test.

Table 5: Spearman coefficient correlation between the parameters evaluated in the bee pollen samples collected from the mesoregions of Mata Atlântica (“MA”), South Coast (“SC”) and Caatinga (“C”) of Alagoas, Brazil during the dry season (2008/09).

Chemical Parameters	Proteins (mg BSA eq/g)	Carbohydrates (mg/g)	Lipids (%)	Phenolics (mg GA eq/g)	Flavonoids (mg Q eq/g)	FRAP (mg GA eq/g)	DPPH (%)
Proteins (mg BSA eq/g)	1.000	0.124	-0.150	-0.412 ^a	-0.191	-0.311	-0.058
Carbohydrates (mg/g)		1.000	0.159	0.080	-0.141	0.256	0.037
Lipids (%)			1.000	0.660 ^b	0.648 ^b	0.375	0.202
Phenolics (mg GA eq/g)				1.000	0.361	0.582 ^b	0.515 ^b
Flavonoids (mg Q eq/g)					1.000	0.488 ^b	0.330
FRAP (mg GA eq/g)						1.000	0.317
DPPH (%)							1.000

^a 95% significance, (p<0.05); ^b 99% significance, (p<0.01).

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Physicochemical composition and antioxidant potential of bee pollen from different botanical sources in Alagoas, Brazil

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[1] ^*Corresponding author: amql@qui.ufal.br