The Investigation Propolis Foraging Preference of Different Honey Bee
Year 2021,
, 133 - 141, 30.03.2021
Nazife Eroğlu
Merve Kambur
,
Meral Kekeçoğlu
Abstract
In this study, it was investigated whether different bee breeds prefer different plant sources to collect propolis. For this purpose four different honey bee race (Apis mellifera caucasica, A. m. carnica, A. m. syriaca and A. m. anatoliaca) naturally have been in Turkey were placed in the same isolated apiary; and Propolis was harvested from these races. chemical contents of alcoholic extractions of the harvested propolis were were analyzed by liquid chromatography-tandem mass spectrometry (LCMS / MS). In addition that, the pollen content of the same propolis samples were determined with a microscope. According to the LCMS / MS results the propolis samples collected by different honey bee race differed significantly in terms of quercetin and ferulic acid. Data obtained from polen analyses revealed that Fabaceae and Apiaceae (PD >45%) families were mostly detected in propolis samples obtained from different races. Although the polen from the Campanulaceae family was dedected only in the propolis samples from A. m. anatoliaca race, thr polen from Caryophyllaceae family was found in other propolis samples collected by A. m caucasica races. The results of this study showed that different honey bee races tend to different plant sources and the content of propolis may differ according to the bee races.
Supporting Institution
1The Scientific and Research Council of Turkey, Marmara Research Center (TÜBİTAK)
Thanks
This study was fully supported by The Scientific and Technological Research Council of Turkey (TÜBİTAK), BIDEB-2232 Project No: 113C036, Institution Code: 5134103 under the name of “Investigation of important honey bee, Apis mellifera L. (Hymenoptera, Apidae), subspecies and ecotypes in Turkey considering propolis collection capacity and chemical characterization of Turkish propolis.”
References
- Aliyazicioglu, R., Sahin, H., Erturk, O., Ulusoy, E., and Kolayli, S. (2013). Properties of phenolic composition and biological activity of propolis from Turkey. International Journal of Food Properties 16, 277-287. doi.org/10.1080/10942912.2010.551312.
- Bankova, V.S., Popov, S. S., Marekov, N. L. (1989). Isopentenyl cinnamates from poplar buds and propolis. Phytochemistry 28, 871-873. doi.org/10.1016/0031-9422(89)80133-5.
- Bankova, V., Dyulgerov, A., Popov, S., Evstatieva, L., Kuleva, L., Pureb, O., Zamjansan, Z. (1992). Propolis produced in Bulgaria and Mongolia: phenolic compounds and plant origin. Apidologie 23, 79-85. doi.org/10.1051/apido:19920109.
- Bankova, V., Popova, M., Bogdanov, S., Sabatını, A.G. (2002). Chemical composition of European propolis: expected and unexpected results. Zeitschrift für Naturforschung C 57, 530-533. doi.org/10.1515/znc-2002-5-622.
- Bankova, V. (2005). Recent trends and important developments in propolis research. Evid. Based Complement. Alternative Medicine 2, 29-32. doi.org/10.1016/j.jep.2005.05.004.
- Bankova, V., Popova, M.; Trusheva, B. (2006). Plant sources of propolis: an update from a chemist's point of view. Natural Product Communications: SAGE Journals, 1, 1023-1028. doi.org/10.1177/1934578X0600101118.
- Barth, O. M. (1998). Pollen analysis of Brazilian propolis. Grana 37, 97-101. doi.org/10.1080/00173139809362650.
- Bertrams, J., Kunz, N., Muller, M., Kammerer, D., Stintzing, F. C. (2013). Phenolic compounds as marker compounds for botanical origin determination of German propolis samples based on TLC and TLC-MS. Journal of Applied Botany and Food Quality, 86, 1. doi:10.5073/JABFQ.2013.086.020.
- Chen, C., Meyermans, H., Burggreave, B. (2000). Cell-specific and conditional expression of caffeoyl-coenzyme A-3-O-methyltransferase in poplar. Plant Physiology 123, 853–868. doi.org/10.1104/pp.123.3.853.
- De Sousa, J. P., Bueno, P. C., Gregório, L.E., Da Silva Filho, A. A., Furtado, N. A., De Sousa, M. L., Bastos, J. K. (2007). A reliable quantitative method for the analysis of phenolic compounds in Brazilian propolis by reverse phase high performance liquid chromatography. Journal of Separation Science 30, 2656-2665. doi.org/10.1002/jssc.200700228.
- Dulger, C. (1997). Kafkas, Orta Anadolu ve Erzurum Balarısı (Apis mellifera L.) genotiplerinin Erzurum koşullarındaki performanslarının belirlenmesi ve morfolojik özellikleri. Doctoral Dissertation, Ataturk University, Department of Zootechny, Erzurum, Turkey.
- Gençay, O., Sorkun, K. (2006). Microscopic Analysis of Propolis Samples Collected from East Anatolia (Kemaliye, Erzincan). FABAD Journal of Pharmaceutical Sciences 31, 192.
- Ghisalberti, E.L. (1979). Propolis: a review. Bee world 60, 59-84.
- Greenaway, W., Scaysbrook, T., Whatley, F. R. (1987). The Analysis of Bud Exudate of Populus euramericana, and of Propolis, by Gas Chromatography-Mass Spectrometry. Proceedings of the Royal society of London. Series B. Biological sciences 232, 249-272. doi.org/10.1098/rspb.1987.0073.
- Kartal, M., Kaya, S., Kurucu, s. (2002). GC-MS analysis of propolis samples from two different regions of Turkey. Zeitschrift für Naturforschung C, 57, 905-909. doi.org/10.1515/znc-2002-9-1025.
- Kartal, M., Yildiz, S., Kaya, S., Kurucu, S., Topcu, G. (2003). Antimicrobial activity of propolis samples from two different regions of Anatolia. Journal of Ethnopharmacology 86, 69-73. doi.org/10.1016/S0378-8741(03)00042-4.
- Kumazawa, S., Yoneda, M., Shibata, I., Kanaeda, J., Hamasaka, T., Nakayama, T. (2003). Direct evidence for the plant origin of Brazilian propolis by the observation of honeybee behavior and phytochemical analysis. Chemical and Pharmaceutical Bulletin 51(6), 740-742. doi.org/10.1248/cpb.51.740.
- Kutluca, S. (2003). Propolis uretim yöntemlerinin koloni performansı ve propolisin kimyasal özellikleri üzerine etkileri Doctoral Dissertation, Department of Zootechny, Ataturk University, Erzurum, Turkey. Available from www.tez.yok.gov.tr Turkey YOK Dissertations and Theses database. p. 145.
- Louveaux, J., Maurizio, A., Vorwohl, G. (1970). Methodik der Melissopalynologie. Apidologie 1, 193-209.
- Marcucci, M. C. (1995). Propolis: chemical composition, biological properties and therapeutic activity. Apidologie 26, 83-99.
- Miguel, M. G., Antunes, M. D. (2011). Is propolis safe as an alternative medicine? Journal of Pharmacy & Bioallied Sciences 3, 479. doi.org/10.4103 / 0975-7406.90101.
- Moreira, L., Dias, L. G., Pereira, J. A., Estevinho, L. (2008). Antioxidant properties, total phenols and pollen analysis of propolis samples from Portugal. Food Chemical Toxicology 46, 3482-3485. doi.org/10.1016/j.fct.2008.08.025.
- Park, Y. K., Paredes, Guzman, J. F., Aguiar, C. L., Alencar, S. M., Fujiwara, F. Y. (2004). Chemical constituents in Baccharis dracunculifolia as the main botanical origin of southeastern Brazilian propolis. Journal of Agricultural and Food Chemistry 52, 1100-1103. doi.org/10.1021/jf021060m.
- Pellati, F., Orlandini, G., Pinetti, D., Benvenuti, S. (2011). HPLC-DAD and HPLC-ESI-MS/MS methods for metabolite profiling of propolis extracts. Journal of Pharmaceutical and Biomedical Analysis 55, 934-948. doi.org/10.1016/j.jpba.2011.03.024.
- Pernal, S. F., Currie, R. W. (2002). Discrimination and preferences for pollen-based cues by foraging honeybees, Apis mellifera L. Animal Behaviour 63, 369-390. doi.org/10.1006/anbe.2001.1904.
- Popova, M., Silici, S., Kaftanoglu, O., Bankova, V. (2005). Antibacterial activity of Turkish propolis and its qualitative and quantitative chemical composition. Phytomedicine 12, 221-228. doi.org/10.1016/j.phymed.2003.09.007.
- Popova, M. P., Graikou, K., Chinou, I., Bankova, V. S. (2010). GC-MS profiling of diterpene compounds in Mediterranean propolis from Greece. Journal of Agricultural and Food Chemistry 58, 3167-3176. 3167-3176. doi.org/10.1021/jf903841k.
- Sahinler, N., Gul, A. (2005). The effects of propolis production methods and honeybee genotypes on propolis yield. Pakistan Journal of Biological Sciences 8, 1212-1214.
- Salatino, A., Fernandes-Silva, C. C., Righi, A. A., Salatino, M. L. F. (2011) . Propolis research and the chemistry of plant products. Natural Product Reports 28, 925-936. doi.org/10.1039/C0NP00072H.
- Sforcin, J.M. (2007). Propolis and the immune system: a review Journal of Ethnopharmacology 113, 1-14. doi.org/10.1016/j.jep.2007.05.012.
- Silici, S., Kutluca, S. (2005). Chemical composition and antibacterial activity of propolis collected by three different races of honeybees in the same region. Journal of Ethnopharmacology 99, 69-73. doi:10.1016/j.jep.2005.01.046.
- Silva, B. B., Rosalen, P. L., Cury, J. A., Ikegaki, M., Souza, V. C., Esteves, A., Alencar, S. M. (2008). Chemical composition and botanical origin of red propolis, a new type of Brazilian propolis. Evidence-Based Complementary and Alternative Medicine 5, 313-316.
- Simone-Finstrom, M. D., Spivak, M. (2012). Increased resin collection after parasite challenge: a case of self-medication in honey bees? PLoS One 7, 34601. doi:10.1371/journal.pone.0034601.
- Tomas-Barberan, F. A., Garcia-Viguera, C., Vit-Olivier, P., Ferreres, F., Tomás-Lorente, F. (1993). Phytochemical evidence for the botanical origin of tropical propolis from Venezuela. Phytochemistry 34, 191-196. doi.org/10.1016/S0031-9422(00)90804-5.
- Uzel, A., Oncag, O., Cogulu, D., Gencay, O. (2005). Chemical compositions and antimicrobial activities of four different Anatolian propolis samples. Microbiological Research 160, 189-195. doi.org/10.1016/j.micres.2005.01.002.
- Warakomska, Z., Maciejewicz, W. (1992). Microscopic analysis of propolis from Polish regions. Apidologie 23, 277-283. doi.org/10.1051/apido:19920401.
- Wilson, M. B., Spivak, M., Hegeman, A. D., Rendahl, A., Cohen, J. D. (2013). Metabolomics reveals the origins of antimicrobial plant resins collected by honey bees. PloS one 8, 77512. doi.org/10.1371/journal.pone.0077512.
- Wollenweber, E., Buchmann, S. L. (1997). Feral honey bees in the Sonoran Desert: Propolis sources other than poplars (Populus spp.). Zeitschrift für Naturforschung C 52, 530-535. doi.org/10.1515/znc-1997-7-817.
- Yang, W.Q., Xu, W., Yin, Y., Zhang, X. Y., Chen, H. L., Xin, Z. H., Shen, C. Y., Zhang, R. (2013). Determination of nitrofuran metabolite residues in propolis by LC-MS/MS. Chinese Journal of Analysis Laboratory 3, 012.
- Zohary, M. (1973). Geobotanical foundations of the Middle East. Stuttgart, Germany: Fischer.
Farklı Bal Arısı Irklarının Propolis Toplama Tercihlerinin Araştırılması
Year 2021,
, 133 - 141, 30.03.2021
Nazife Eroğlu
Merve Kambur
,
Meral Kekeçoğlu
Abstract
Bu çalışmada farklı arı ırklarının propolis toplamak için farklı bitki kaynaklarını tercih edip etmediği araştırılmıştır. Bu amaçla Türkiye’de doğal olarak bulunduğu bilinen 4 farklı bal arısı ırkı (Apis mellifera caucasica, A. m. carnica, A. m. syriaca and A. m. anatoliaca) izole edilmiş aynı arılığa yerleştirilmiş ve bu ırklardan propolis hasadı yapılmıştır. Hasat edilen propolislerin alkolik ekstraksiyonları yapılarak sıvı kromatogram kütle spektrofotometrisi (LCMS/MS) ile kimyasal içerikleri analiz edilmiştir. Aynı zamanda aynı propolislerin mikroskop ile polen içeriği belirlenmiştir. Elde edilen sonuçlara göre farklı bal arısı ırklarının topladığı propolisler kuersetin ve ferulik asit bakımından önemli düzeyde farklılık göstermiştir. Farklı ırklardan elde edilen propolis örneklerinde en fazla Fabaceae and Apiaceae (PD >45%) familyasından polenlere reslanırken, Campanulaceae familyasından polene yalnızca A. m. anatoliaca ırkının topladığı polenlerde ve Caryophyllaceae familyasından polenlere ise sadece A. m. caucasica ırkının topladığı propolislerde raslanmıştır. Bu çalışmanın sonuçları farklı arı ırklarının farklı bitki kaynaklarına yönelme davranışında bulunduğunu ve ırka göre propolis içeriğinin değişebileceğini göstermiştir
References
- Aliyazicioglu, R., Sahin, H., Erturk, O., Ulusoy, E., and Kolayli, S. (2013). Properties of phenolic composition and biological activity of propolis from Turkey. International Journal of Food Properties 16, 277-287. doi.org/10.1080/10942912.2010.551312.
- Bankova, V.S., Popov, S. S., Marekov, N. L. (1989). Isopentenyl cinnamates from poplar buds and propolis. Phytochemistry 28, 871-873. doi.org/10.1016/0031-9422(89)80133-5.
- Bankova, V., Dyulgerov, A., Popov, S., Evstatieva, L., Kuleva, L., Pureb, O., Zamjansan, Z. (1992). Propolis produced in Bulgaria and Mongolia: phenolic compounds and plant origin. Apidologie 23, 79-85. doi.org/10.1051/apido:19920109.
- Bankova, V., Popova, M., Bogdanov, S., Sabatını, A.G. (2002). Chemical composition of European propolis: expected and unexpected results. Zeitschrift für Naturforschung C 57, 530-533. doi.org/10.1515/znc-2002-5-622.
- Bankova, V. (2005). Recent trends and important developments in propolis research. Evid. Based Complement. Alternative Medicine 2, 29-32. doi.org/10.1016/j.jep.2005.05.004.
- Bankova, V., Popova, M.; Trusheva, B. (2006). Plant sources of propolis: an update from a chemist's point of view. Natural Product Communications: SAGE Journals, 1, 1023-1028. doi.org/10.1177/1934578X0600101118.
- Barth, O. M. (1998). Pollen analysis of Brazilian propolis. Grana 37, 97-101. doi.org/10.1080/00173139809362650.
- Bertrams, J., Kunz, N., Muller, M., Kammerer, D., Stintzing, F. C. (2013). Phenolic compounds as marker compounds for botanical origin determination of German propolis samples based on TLC and TLC-MS. Journal of Applied Botany and Food Quality, 86, 1. doi:10.5073/JABFQ.2013.086.020.
- Chen, C., Meyermans, H., Burggreave, B. (2000). Cell-specific and conditional expression of caffeoyl-coenzyme A-3-O-methyltransferase in poplar. Plant Physiology 123, 853–868. doi.org/10.1104/pp.123.3.853.
- De Sousa, J. P., Bueno, P. C., Gregório, L.E., Da Silva Filho, A. A., Furtado, N. A., De Sousa, M. L., Bastos, J. K. (2007). A reliable quantitative method for the analysis of phenolic compounds in Brazilian propolis by reverse phase high performance liquid chromatography. Journal of Separation Science 30, 2656-2665. doi.org/10.1002/jssc.200700228.
- Dulger, C. (1997). Kafkas, Orta Anadolu ve Erzurum Balarısı (Apis mellifera L.) genotiplerinin Erzurum koşullarındaki performanslarının belirlenmesi ve morfolojik özellikleri. Doctoral Dissertation, Ataturk University, Department of Zootechny, Erzurum, Turkey.
- Gençay, O., Sorkun, K. (2006). Microscopic Analysis of Propolis Samples Collected from East Anatolia (Kemaliye, Erzincan). FABAD Journal of Pharmaceutical Sciences 31, 192.
- Ghisalberti, E.L. (1979). Propolis: a review. Bee world 60, 59-84.
- Greenaway, W., Scaysbrook, T., Whatley, F. R. (1987). The Analysis of Bud Exudate of Populus euramericana, and of Propolis, by Gas Chromatography-Mass Spectrometry. Proceedings of the Royal society of London. Series B. Biological sciences 232, 249-272. doi.org/10.1098/rspb.1987.0073.
- Kartal, M., Kaya, S., Kurucu, s. (2002). GC-MS analysis of propolis samples from two different regions of Turkey. Zeitschrift für Naturforschung C, 57, 905-909. doi.org/10.1515/znc-2002-9-1025.
- Kartal, M., Yildiz, S., Kaya, S., Kurucu, S., Topcu, G. (2003). Antimicrobial activity of propolis samples from two different regions of Anatolia. Journal of Ethnopharmacology 86, 69-73. doi.org/10.1016/S0378-8741(03)00042-4.
- Kumazawa, S., Yoneda, M., Shibata, I., Kanaeda, J., Hamasaka, T., Nakayama, T. (2003). Direct evidence for the plant origin of Brazilian propolis by the observation of honeybee behavior and phytochemical analysis. Chemical and Pharmaceutical Bulletin 51(6), 740-742. doi.org/10.1248/cpb.51.740.
- Kutluca, S. (2003). Propolis uretim yöntemlerinin koloni performansı ve propolisin kimyasal özellikleri üzerine etkileri Doctoral Dissertation, Department of Zootechny, Ataturk University, Erzurum, Turkey. Available from www.tez.yok.gov.tr Turkey YOK Dissertations and Theses database. p. 145.
- Louveaux, J., Maurizio, A., Vorwohl, G. (1970). Methodik der Melissopalynologie. Apidologie 1, 193-209.
- Marcucci, M. C. (1995). Propolis: chemical composition, biological properties and therapeutic activity. Apidologie 26, 83-99.
- Miguel, M. G., Antunes, M. D. (2011). Is propolis safe as an alternative medicine? Journal of Pharmacy & Bioallied Sciences 3, 479. doi.org/10.4103 / 0975-7406.90101.
- Moreira, L., Dias, L. G., Pereira, J. A., Estevinho, L. (2008). Antioxidant properties, total phenols and pollen analysis of propolis samples from Portugal. Food Chemical Toxicology 46, 3482-3485. doi.org/10.1016/j.fct.2008.08.025.
- Park, Y. K., Paredes, Guzman, J. F., Aguiar, C. L., Alencar, S. M., Fujiwara, F. Y. (2004). Chemical constituents in Baccharis dracunculifolia as the main botanical origin of southeastern Brazilian propolis. Journal of Agricultural and Food Chemistry 52, 1100-1103. doi.org/10.1021/jf021060m.
- Pellati, F., Orlandini, G., Pinetti, D., Benvenuti, S. (2011). HPLC-DAD and HPLC-ESI-MS/MS methods for metabolite profiling of propolis extracts. Journal of Pharmaceutical and Biomedical Analysis 55, 934-948. doi.org/10.1016/j.jpba.2011.03.024.
- Pernal, S. F., Currie, R. W. (2002). Discrimination and preferences for pollen-based cues by foraging honeybees, Apis mellifera L. Animal Behaviour 63, 369-390. doi.org/10.1006/anbe.2001.1904.
- Popova, M., Silici, S., Kaftanoglu, O., Bankova, V. (2005). Antibacterial activity of Turkish propolis and its qualitative and quantitative chemical composition. Phytomedicine 12, 221-228. doi.org/10.1016/j.phymed.2003.09.007.
- Popova, M. P., Graikou, K., Chinou, I., Bankova, V. S. (2010). GC-MS profiling of diterpene compounds in Mediterranean propolis from Greece. Journal of Agricultural and Food Chemistry 58, 3167-3176. 3167-3176. doi.org/10.1021/jf903841k.
- Sahinler, N., Gul, A. (2005). The effects of propolis production methods and honeybee genotypes on propolis yield. Pakistan Journal of Biological Sciences 8, 1212-1214.
- Salatino, A., Fernandes-Silva, C. C., Righi, A. A., Salatino, M. L. F. (2011) . Propolis research and the chemistry of plant products. Natural Product Reports 28, 925-936. doi.org/10.1039/C0NP00072H.
- Sforcin, J.M. (2007). Propolis and the immune system: a review Journal of Ethnopharmacology 113, 1-14. doi.org/10.1016/j.jep.2007.05.012.
- Silici, S., Kutluca, S. (2005). Chemical composition and antibacterial activity of propolis collected by three different races of honeybees in the same region. Journal of Ethnopharmacology 99, 69-73. doi:10.1016/j.jep.2005.01.046.
- Silva, B. B., Rosalen, P. L., Cury, J. A., Ikegaki, M., Souza, V. C., Esteves, A., Alencar, S. M. (2008). Chemical composition and botanical origin of red propolis, a new type of Brazilian propolis. Evidence-Based Complementary and Alternative Medicine 5, 313-316.
- Simone-Finstrom, M. D., Spivak, M. (2012). Increased resin collection after parasite challenge: a case of self-medication in honey bees? PLoS One 7, 34601. doi:10.1371/journal.pone.0034601.
- Tomas-Barberan, F. A., Garcia-Viguera, C., Vit-Olivier, P., Ferreres, F., Tomás-Lorente, F. (1993). Phytochemical evidence for the botanical origin of tropical propolis from Venezuela. Phytochemistry 34, 191-196. doi.org/10.1016/S0031-9422(00)90804-5.
- Uzel, A., Oncag, O., Cogulu, D., Gencay, O. (2005). Chemical compositions and antimicrobial activities of four different Anatolian propolis samples. Microbiological Research 160, 189-195. doi.org/10.1016/j.micres.2005.01.002.
- Warakomska, Z., Maciejewicz, W. (1992). Microscopic analysis of propolis from Polish regions. Apidologie 23, 277-283. doi.org/10.1051/apido:19920401.
- Wilson, M. B., Spivak, M., Hegeman, A. D., Rendahl, A., Cohen, J. D. (2013). Metabolomics reveals the origins of antimicrobial plant resins collected by honey bees. PloS one 8, 77512. doi.org/10.1371/journal.pone.0077512.
- Wollenweber, E., Buchmann, S. L. (1997). Feral honey bees in the Sonoran Desert: Propolis sources other than poplars (Populus spp.). Zeitschrift für Naturforschung C 52, 530-535. doi.org/10.1515/znc-1997-7-817.
- Yang, W.Q., Xu, W., Yin, Y., Zhang, X. Y., Chen, H. L., Xin, Z. H., Shen, C. Y., Zhang, R. (2013). Determination of nitrofuran metabolite residues in propolis by LC-MS/MS. Chinese Journal of Analysis Laboratory 3, 012.
- Zohary, M. (1973). Geobotanical foundations of the Middle East. Stuttgart, Germany: Fischer.