Palynological and physico‐chemical characterisation of honeys from the north‐west of Santa Cruz (Argentinean Patagonia)

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  Abstract Thirty Apis mellifera L. honey samples collected between 2004 and 2008 were analysed. Most of the samples had a moderate to low pollen content (number of pollen grains in 10 g of honey: NPG 0555 654), with the honeydew indicators scarce or
  Journal of Food, Agriculture & Environment, Vol.7 (3&4), July-October 2009  667 Palynological and physicochemical characterization of  Apis mellifera  L.bee pollen in the Southern region of Brazil Solange T. Carpes 1* , Ingridy S. R. Cabral 2 , Cynthia Fernandez P. Luz  3 , Jailson P. Capeletti 4 ,Severino Matias Alencar 2  and Maria L ú ciaMasson 5 1 Federal Technological University of Paraná (UTFPR), CEP 85503-390, Pato Branco/PR, Brazil. 2  Department of Agri-Food  Industry, Food and Nutrition, “Luiz de Queiroz” College of Agriculture, University of São Paulo (USP), Piracicaba/ SP, Brazil. 3  Environmental Secretary of São Paulo State, Botanical Institute, Section of Dicotyledons, São Paulo/SP, Brazil. 4 UniversityCatolic of Rio Grande do Sul, Porto Alegre/RS, Brazil. 5 Federal University of Paraná, Post-graduation Program in Food Technology, Curitiba/PR, Brazil. *   Received 10 July 2009, accepted 2 October 2009. Abstract Bee pollen has been used for many years in both traditional medicine and supplementary nutrition, as well as in alternative diets, mainly due to itsnutritional properties and health benefits. Bee pollen production is a recent activity in Brazil, having begun in the late 1980s. However, the countryhas the potential of being a large world producer of high quality pollen, particularly because of the great diversity of tropical flora and the resistanceof the Brazilian  Apis mellifera bee races. Thirty-six samples of bee pollen from the Southern region of Brazil were analyzed regarding pollen typesand physicochemical and nutritional composition. Only one sample was considered monofloral, which was exclusively composed by pollen from theAsteraceaefamily). The State of Paraná showed a greater variety of pollen types, 18 in total, representing 82% of the total number identified in thisstudy. The bee pollen in the States of Rio Grande do Sul and Paraná showed a higher number of samples with humidity content above the standardpermitted by the Brazilian legislation, i.e. over 4%. The bee pollen was characterized by its high protein content with average values of 20.47%. Theanalysis regarding humidity, lipids and sugar showed no statistical differences among the samples (p<0.05). The pollen samples had a highconcentration of reducible sugars (48%). The predominant minerals in the samples PR, SC and RS were phosphorus (7102.29, 6873.40, 6661.73 mg/ kg of pollen), followed by potassium (5383.73, 4997.77, 4773.26 mg/kg of pollen), calcium (1179.05, 961.93, 848.36 mg/kg of pollen) and magnesium(818.02, 679.01, 725.89 mg/kg of pollen). Statistical analysis (Tukey test) demonstrated no significant difference between the contents of calcium,copper, iron, phosphorus and sodium in the pollen samples of the South of Brazil. However, the samples from the State of Paraná contained thehighest contents of potassium and differed statistically from the samples of the State of Rio Grande do Sul.  Key words:  Chemical composition, bee pollen,  Apis mellifera , minerals, Asteraceae family.   Journal of Food, Agriculture & Environment Vol.7 (3&4) : 667-673. 2009 WFL Publisher Science and Technology Meri-Rastilantie 3 B, FI-00980Helsinki, Finlande-mail: Introduction Bee pollen is an agglomerate of pollen grains from various botanicalsources, which are collected by the bees and mixed with nectarand secretion from the hypopharyngeal glands, such as α  and β -glycosidase enzymes. Pollen contains nutrients, such ascarbohydrates, proteins, amino acids, lipids, vitamins and minerals,in addition to carotenoids, flavonoids and phytosterols, which isthe reason why it is used by humans as an alternative food sourceand/or food supplement 1 . Each pollen type has its own specific characteristics related tothe genetics of the floral species and plantations visited by thebees. During the pollen harvest (collection) the bees might showpreferences regarding the floral sources 2, 3 .The nutritional qualityof the pollen is one of the factors that makes it attractive to bees 4 .Honeybees collect a substantial quantity of pollen, approximately30 mg, at each visit to the field and to obtain such a load they haveto visit many flowers 5 . Bee pollen can be monofloral , characterizedby single botanic taxonomy in the pollen load of the “corbiculae”,that maintains the constant organoleptic and biochemicalproperties of the srcinal plant. When the bees visit other flowers,or mix the “pollen loads” from various flowers, these are called heterofloral  and present a variety of biochemical properties 6 . Diversity and frequency of pollen grains in bee pollen can bedetermined by means of pollen analysis of the morphologicalcharacteristics, which indicates the probable srcinal botanicalspecies. The quantity of each pollen type can also be an indicationof the quality of the product. In Brazil, cooperatives and apicultureassociations don’t use palynological analyses to qualify themarket’s apicultural products 7 . Pollen, as well as other apiculture products, such as propolisand honey, have gained attention due to their antibacterial 8, 9 ,antifungal 10 , anti-inflammatory 11 , antioxidant andimmunomodulatory therapeutic properties 12 . Pollen extract(Cernilton®) is often used in the treatment of some cases of benignprostatitis 12  and in reducing oral sensitivity in children with pollenallergy 13 . The objective of this study was to identify the pollen component   668Journal of Food, Agriculture & Environment, Vol.7 (3&4), July-October 2009 types and to verify the monofloral and heterofloral conditions of each sample and further to determine the physicochemical andnutritional composition of the dehydrated bee pollen from threestates in the Southern region of Brazil. Materials and Methods  Materials: All solvents were of analytical grade and obtainedfrom Merck (Merck KGaA Frankfurter, Darmstadt, Germany). Thirty-six dehydrated apicultural pollen samples were collected fromdifferent apiaries in locations in the Southern region of Brazil,sixteen being from the State of Paraná (PR samples), ten from theState of Santa Catarina (SC samples) and ten from the State of RioGrande do Sul (RS samples), during the period from August 2005to April 2006 (Fig. 1). After collection, each sample was separatelycrushed, homogenized and stored at 5ºC in a freezer for lateranalysis. All analyses were performed in triplicate.  Palynology:  Scanning electronic microscopy (SEM) analysis of the pollen grains was performed in the laboratory facilities of theNucleus of Support for Research in electronic microscopy appliedto cattle raising research (NAP/MEPA) at ESALQ-USP, Piracicaba-S ã o Paulo. Approximately 2 g of each sample was consideredrepresentative for pollen analysis 14 . The pollen loads weregrouped up into subsamples according to their coloring and eachsubsample was weighed and metallized with gold and thenanalyzed by scanning electronic microscopy (SEM) in DigitalScanning Microscope DSM 940 A (Zeiss Co.). In this experimentapproximately 350 pollen grains of each sample were identifiedand counted and from this total the percentage of each pollentype was established as: “Predominant pollen” or “dominant”(> 45% do total) (PD); “Accessory or secondary pollen” (16-45%)(PA); “Important isolated pollen” (3-15%) (PII) and “Occasionalisolated pollen” (<3%) (PIO)  15 .  Determination of physicochemical characteristics: The humiditycontent was determined in an oven at 60ºC, until a constant weightof a previously crushed 2 g pollen dry basis sample was obtained 16 . Total nitrogen was determined by the Kjeldahl method from a0.7 g crushed pollen sample, using a factor of 6.25 for conversioninto protein 16 . The total lipids were determined by gravimetry from 2 g of crushed pollen extracted with petroleum ether in a Soxhletapparatus for approximately 4 hours 17 . The total sugar and reducible sugar contents were determinedspectrophotometrically at 510 nm, in accordance with theSomogyi-Nelson method with a few modifications 18 . The minerals Fe, Ca, Zn, K, Na, Cu, Mg and Mn were determinedafter incineration of 1.5 g of pollen at 550 ºC, until a constantweight was obtained. The ash was solubilized with 25 ml of HNO 3 50%, heated in a water bathfor 30 min, filtered and the mineralswere determined by atomic absorption spectrophotometry (VarianModel Spectra AA 100 & 200). The phosphorus content wasdetermined by an ultraviolet spectrophotometer (Shimadzu ModelUV-1601 PC ) at 650 nm 16 . Statistical analysis: Data was submitted to analysis of variance(ANOVA). The Student’s t-  test was used to assess the significantdifferences between means, sixteen of which from the State of Paraná (PR samples), ten from the State of Santa Catarina (SCsamples) and ten from the State of Rio Grande do Sul (RS samples),(comparison of means) at the level of p<0.05, using the softwareSAS V9.  Results and Discussion According to Barth 19 , studies regarding pollen analysis of apicultural products in Southern Brazil are not frequent.Nevertheless, it is known that honey from this region ispredominantly of Asteraceae (Compositae), especially Seneciobrasiliensis, “ maria-mole” and  Lithrea sp. “aroeira” 15 . In otherstudies, Barth and Dutra 7, 19 confirmed that the pollen types of various species of Asteraceae,  Eucalyptus, Myrcia  and  Mimosascabrella, frequently occur in the honey from the Southern regionof Brazil.The “pollen loads” had a mixture of pollen types frommany different floral species, whose coloring varied fromlight yellow to darker colors, such as purple and brown.Twenty-two pollen types were identified in the 36 beepollen samples from the Southern region of Brazil. Withexception of sample PR 12, which was classified asmonofloral, all the other samples of bee pollen presentedat least two pollen types. The bee pollen PR 12 from oneof the apiaries in União da Vitória, State of Paraná, hadpollen exclusively from the  Baccharis  type (Asteraceae)(Table 1). Pollen from the Euphorbiaceae family (Fig. 2, Image 1)and Asteraceae (  Elephantopus type) (Fig. 2, Image 2)were dominant (>45%) only in samples PR 01 and PR 09,respectively (Table 1). Thus, with exception of samplesRS 06 and RS 08, all the samples from the State of RioGrande do Sul contained the  Elephantopus  type asaccessory pollen (15 - 45%) and important isolated pollen(3 – 15%) (Table 3, Fig. 2, Image 2). In the States of Paraná and Santa Catarina the  Eupatorium  type was present in 50% of the samples,while in Rio Grande do Sul the  Elephantopus  type waspresent in 80% of the samples (Tables 1, 2 and 3). The  Figure 1.  Collection sites of bee pollen in the Southern region of Brazil. PR:State of Paraná; SC: State of Santa Catarina; RS: State of Rio Grande do Sul.  Journal of Food, Agriculture & Environment, Vol.7 (3&4), July-October 2009  669pollen type  Mimosa scabrella , characteristic from the CuritibaParaná region, appeared as accessory pollen (15-45%) only insamples PR 02 (Lapa), PR 06 (União da Vitória) and PR 14(Curitiba). However, this pollen type was not found in the otherstates of the Southern region (Table 1, Fig. 2, Image 8). In the sample PR 11 was detected the Gochnatia  (Asteraceae)type (Table 1, Fig. 2, Image 4) in the accessory pollen categoryand the  Eucalyptus  (Myrtaceae) type as isolated pollen (Fig. 2,Image 7). The State of Paraná (PR samples) showed the biggest variety(18 pollinic types) representing 82% of the total identified in thisstudy (Table 1). These results corroborate other studies with  Apis mellifera,  that confirmed the presence of  Allophylus, Baccharis, Campomanesia, Cecropia , Citrus, Eucalyptus, Matayba, Mimosa scabrella, Paspalum  and  Vernonia  in thehoney from the State of Paraná, and found it to be a basicallyheterofloral product, but according to the results of this author,the highest occurrence was of  Eucalyptus 2 . The pollen type Brassicaceae (Fig. 3, Image 10) was found inthe bee pollen of three states in the Southern region of Brazil butin the State of Rio Grande do Sul it only appeared in 30% of thesamples as dominant pollen (>45%). However, the  Eucalyptus type was the dominant one, being present in 20% of the samplesfrom the State of Santa Catarina (Table 2). The State of SantaCatarina is also an important producer of honey, bee pollen andpropolis, but knowledge about the pollen grains found in theseproducts is poor 19 . The bracatinga (  Mimosa scabrella ) is a veryimportant apicultural plant in the State of Santa Catarina 15  andits honey was analyzed and classified as melato honey 20 . Melatocontains enzymes derived from salivary gland secretions andfrom the intestine of the plant sucker insects and it has alwaysbeen classified as inferior honey compared with floral honey onthe internal market, by being less attractive due to its dark colorand strong flavor, however, since the 80’s the German markethas shown great interest in this product 20 . Pollen from the Leguminosae (Table 2, Fig. 3, Image 16) andArecaceae (Table 2, Fig. 4, Image 18) families appearedindividually in only one of the 36 analyzed samples. These pollentypes were found in the PR 05 sample, collected in the PatoBranco region, and the in PR 15 sample, collected in the BalsaNova region, both in the State of Paraná. In sample RS 06  Eucalyptus  was the dominant pollen, however,the pollen type from the Rosaceae family was observed asaccessory pollen, and was unprecedented among the 36 analyzedsamples of bee pollen (Table 3, Fig. 4, Image 21). The pollen type Struthanthus  (Loranthaceae) was present only as isolated pollen(3-15%) in the sample RS 09 (Table 3, Fig. 4, Image 22). The humidity content in the samples ranged from 1.69% to7.84%, with a mean of 4.19% (between 36 samples). Results showedthat 47% of the samples were outside the Brazilian Legislationstandards, which only allows the sale of dehydrated pollen with amaximum humidity content of 4% 21 . The bee pollen in the Statesof Rio Grande do Sul (RS) and Paraná (PR) presented the largestnumber of samples with humidity levels outside the BrazilianLegislation standard, which corresponds to 60 and 50% of thesamples, respectively. However, there were no statisticaldifferences among the bee pollen samples in the three analyzedstates (Table 4).    B  e  e  p  o   l   l  e  n  s  a  m  p   l  e  s   f  r  o  m   t   h  e   S   t  a   t  e  o   f   P  a  r  a  n  a   *   I  m  a  g  e   P  o   l   l  e  n   t  y  p  e  s   0   1   0   2   0   3   0   4   0   5   0   6   0   7   0   8   0   9   1   0   1   1   1   2   1   3   1   4   1   5   1   6   1   E  u  p   h  o  r   b   i  a  c  e  a  e   P   D    2   A  s   t  e  r  a  c  e  a  e    E   l  e  p   h  a  n   t  o  p  u  s    P   I   I    P   I   O    P   D    P   I   O    3   A  s   t  e  r  a  c  e  a  e    E  u  p  a   t  o  r   i  u  m     P   D    P   D    P   A   P   I   O   P   A    P   D    P   I   I    P   A   4   A  s   t  e  r  a  c  e  a  e    G  o  c   h  n  a   t   i  a     P   I   I    P   I   O    P   A    5   A  s   t  e  r  a  c  e  a  e    B  a  c  c   h  a  r   i  s     P   D    P   D    P   I   I    6   S  a  p   i  n   d  a  c  e  a  e    M  a   t  a  y   b  a    P   I   I    7   M  y  r   t  a  c  e  a  e    E  u  c  a   l  y  p   t  u  s     P   I   I    P   A    P   A    P   A   8   M   i  m  o  s  a  c  e  a  e    M   i  m  o  s  a  s  c  a   b  r  e   l   l  a     P   A    P   A    P   A    9   V  e  r   b  e  n  a  c  e  a  e    A  e  g   i  p   h   i   l  a     P   I   I    1   0   B  r  a  s  s   i  c  a  c  e  a  e    P   D    P   I   I    P   I   I   P   D   P   A    1   1   A  r  e  c  a  c  e  a  e   T  y  p  e   I    P   I   I    P   D    P   A    1   2   A  r  e  c  a  c  e  a  e   T  y  p  e   2    P   A    1   3   A  n  a  c  a  r   d   i  a  c  e  a  e    S  c   h   i  n  u  s     P   A    1   4   A  n  a  c  a  r   d   i  a  c  e  a  e   T  y  p  e   I    P   I   I    1   5   A  n  a  c  a  r   d   i  a  c  e  a  e    A  s   t  r  o  n   i  u  m     P   I   O    P   I   I    1   6   L  e  g  u  m   i  n  o  s  a  e    P   I   O    1   7   B  o  r  a  g   i  n  a  c  e  a  e    C  o  r   d   i  a     P   A    1   8   A  r  e  c  a  c  e  a  e    P   D     T  a   b   l  e   1 .    P  o   l   l  e  n   t  y  p  e  s  o   f   b  e  e  p  o   l   l  e  n  s  a  m  p   l  e  s  o   b  s  e  r  v  e   d   i  n   t   h  e   S   t  a   t  e  o   f   P  a  r  a  n   á .     *   I  m  a  g  e  s   f  r  o  m   t   h  e   S  c  a  n  n   i  n  g   E   l  e  c   t  r  o  n   i  c   M   i  c  r  o  s  c  o  p  y   (   S   E   M   )  ;   D   P  =   d  o  m   i  n  a  n   t  p  o   l   l  e  n   (   >   4   5   %   )  ;   P   A  =  a  c  c  e  s  s  o  r  y  p  o   l   l  e  n   (   1   5  -   4   5   %   )  ;   P   I   I  =   i  m  p  o  r   t  a  n   t   i  s  o   l  a   t  e   d  p  o   l   l  e  n   (   3  –   1   5   %   )  ;   P   I   O  =  o  c  c  a  s   i  o  n  a   l   i  s  o   l  a   t  e   d  p  o   l   l  e  n   (   <   3   %   ) .   670Journal of Food, Agriculture & Environment, Vol.7 (3&4), July-October 2009 2 20µm(x 900) 6 5 µm (x 2000) 3 10 µm (x 1800) 7 20 µm (x 650) 8 10 µm (x 1400) 4 10 µm (x 1000) 5 10 µm (x 1850) 1 20µm(x 800)  Figure 2.  Pollen types observed in pollen loads in the Southern region of Brazil. Images:1.Euphorbiaceae; 2. Asteraceae  Elephantopus ; 3. Asteraceae  Eupatorium ; 4. Asteraceae Gochnatia ; 5.Asteraceae  Baccharis ; 6. Sapindaceae  Matayba ; 7. Myrtaceae  Eucalyptus ; 8. Mimosaceae  Mimosa scabrella . Bee pollen samples from the State of Santa Catarina *Image Pollen types 01 02 03 04 05 06 07 08 09 10 1 Euphorbiaceae PA PII PII 2 Asteraceae  Elephantopus  PII PA 3 Asteraceae  Eupatorium  PD PII PA PA PA 4 Asteraceae Gochnatia  PII PII PD PII 5 Asteraceae  Baccharis  PII PA PII PII 7 Myrtaceae  Eucalyptus  PD PD 10 Brassicaceae PD PII 11 Arecaceae Type I PII PD 14 Anacardiaceae Type I PA PII 16 Leguminosae PA 19 Anacardiaceae Type 2 PA PA PII 20 Rosaceae  Prunus  PD Table 2.  Pollen types observed in the samples of bee pollen in the State of Santa Catarina. * Images from the Scanning Electronic Microscopy (SEM); DP = dominant pollen (> 45%); PA = accessory pollen (15 - 45 %); PII = important isolatedpollen (3 – 15%); PIO = occasional isolated pollen (< 3%). 10 10 µm (x 1450) 9 10 µm (x 1750) 12 20µm(x 850) 13 10 µm (x 1650) 14 10 µm (x 1750) 15 20 µm (x 750) 16 20µm(x 625) 11 20µm(x 925)  Figure 3.  Pollen types observed in pollen loads in the Southern region of Brazil. Images: 9 Verbenaceae  Aegiphila ; 10. Brassicaceae; 11. Arecaceae Type I, on black arrow Pinus ; 12. Arecaceae Type 2; 13. Anacardiaceae Schinus ; 14. Anacardiaceae Type I; 15. Anacardiaceae  Astronium ; 16. Leguminosae.  Journal of Food, Agriculture & Environment, Vol.7 (3&4), July-October 2009  671 The total protein content ranged from 15.04 to 27.69 % with amean of 20% (between 36 samples), and the protein contents of the samples from the State of Santa Catarina (SC) differedstatistically from those from the States of Rio Grande do Sul (RS)and Paraná (PR) (Table 4). All the analyzed samples presented aprotein content of above 8%, thus being in accordance with theBrazilian technical regulation 21 . Protein contents higher than 25.9%content have also been found in bee pollen produced in MinasGerais 22  and in Southeast Australia 23 . The greatest part of thenitrogen present in pollen is found in the protein fraction, whichis the second most abundant group of nutrients, after thecarbohydrates. The high protein content (20.34, 22.60 and 18.55%), reduciblesugars (50.01, 47.43 and 48.18 g/100 g) and low lipid content (5.07,4.59 and 4.80%) found in the PR, SC and RS samples, make pollenan excellent food supplement (Table 4). These results corroboratethose of Almeida-Muradian et al. 24 , who assessed ten samplesfrom the Southern region of Brazil and found contents of humidity,proteins, lipids and ash of 7.4, 20, 6 and 2.2%, respectively. Thehigh reducible sugar content in pollen can be explained by thepresence of honey or nectar in the fluid that cements the pollengrains 25 . The lipid content from the 36 samples of bee pollen (4.86±0.65 g/100 g) was similar to that described by Somerville 26 , whofound a variation of 0% of lipids for  Eucalyptus macrorhyncha pollen and 11.2% for  Hypochoerisradicata pollen in the southeastof Australia .  The predominant minerals in the samples from PR, SC and RSwere phosphorus (7102, 6873 and 6662 mg/kg of pollen), followedby potassium (5384, 4998 and 4773 mg/kg of pollen), calcium (1179,962 and 848 mg/kg of pollen) and magnesium (818, 679 and 726 mg/ kg of pollen). Statistical analysis through the Tukey test showedno significant difference between the contents of calcium, copper,iron, phosphorus, magnesium and sodium in the pollen samplesfrom the South of Brazil. However, regarding potassium, the samplesfrom State of Paraná (PR) presented the highest contents and differedstatistically from the samples from State of Rio Grande do Sul (RS)(Table 4). The mean zinc content was 55.22±2.88 mg/kg of pollenfrom the State of Rio Grande do Sul (RS) and differed statisticallyfrom the samples from the State of Santa Catarina (SC) (p<0.05). Theiron and zinc contents corresponded to 15% of the recommendeddaily allowance (RDA) (Table 4). According to Wesh and Marston 27 the presence of zinc, copper, iron and a high rate of potassium/ sodium make bee pollen an interesting food for diets with a definedelectrolytic balance. With the exception of the zinc content, theother minerals from bee pollen in the State of Paraná were shown tohave higher mineral contents than that in the other states of theSouthern region. Bee pollen samples from the State of Rio Grande do Sul *Image Pollen types 01 02 03 04 05 06 07 08 09 10 2 Asteraceae  Elephantopus  PA PII PII PII PA PII PA PII 3 Asteraceae  Eupatorium  PA PA PII PII 4 Asteraceae Gochnatia  PA 5 Asteraceae  Baccharis  PA 6 Sapindaceae Matahyba  PA PD PD 7 Myrtaceae  Eucalyptus  PD PA PD 10 Brassicaceae PA PA PD PD PD 11 Arecaceae Type I PA PA PA PA 20 Rosaceae  Prunus  PIO 21 Rosaceae PA 22 Loranthaceae Struthanthus  PII Table 3.  Pollen types of bee pollen samples observed in the State of Rio Grande do Sul. * Images from the Scanning Electronic Microscopy (SEM); DP = dominant pollen (> 45%); PA = accessory pollen (15 - 45 %); PII = important isolated pollen(3 – 15%); PIO = occasional isolated pollen (< 3%). 20 10 µm (x 1000) 19 10   m (x 1000) 18 20µm(x 800) 21 20µm(x 650) 22 20 µm (x 850) 17 20 µm (x 500)  Figure 4.  Pollen types observed in pollen loads in the Southern region of Brazil.Images: 17. Boraginaceae Cordia ; 18. Arecaceae; 19. Anacardiaceae Type 2; 20. Rosaceae Prunus ; 21. Rosaceae; 22. Loranthaceae Struthanthus.
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