PHENOLOGY AND BIOCHEMICAL COMPOUNDS OF PRUNUS SPINOSA L. FRUITS WITH REGARD TO THE IMPACT OF AIR TEMPERATURE AND PRECIPITATION
Keywords:
blackthorn, adaptability, functionality, antioxidant capacity of fruits, ecosystem services, heatwaves, ecotones
Abstract
Phenology is the study of periodic biological changes that plants undergo, under the influence of geographic and ecological conditions, particularly climatic variables. The aims of the research were to determine the variability of the phenological patterns of Prunus spinosa L. natural populations in the ecotones of the southeastern part of the Balkan Peninsula and to create an informational database regarding the impact of air temperature and precipitation on the phenology of the species, based on research conducted during the period from 2007 to 2024. The obtained data were analysed using descriptive and multivariate statistical methods. The results show that the onset of spring phenological phases has been significantly accelerated by the increase in air temperature, especially in 2024, when flowering started 31 days earlier, the flowering phase was 13 days longer, and fruit ripening occurred 65 days earlier compared to the period 2007–2023. Given that blackthorn significantly contributes to ecosystem services as a honey plant and a species used in the food industry and phytotherapy, the content of phenols, flavonoids, anthocyanins, and antioxidant activity was determined in fruit in distilled water and 70% ethanol. The analysed extracts contain a high percentage of phenols and demonstrate significant antioxidant activity. Based on the conducted research, valuable information was obtained regarding the variability of phenological patterns and the antioxidant capacity of blackthorn fruits, which are important for developing guidelines for ecosystem service conservation programmes, enrichment, and management plans.
References
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Cosmulescu, S., & Gavrila Calusaru, F. (2020). Influence of temperature on blackthorn (Prunus spinosa L.) phenophases in spring season. Journal of Agricultural Meteorology, 76, 53–57. https://doi.org/10.2480/agrmet.D-19-00030
Cosmulescu, S., & Ionescu, M.B. (2018). Phenological calendar in some walnut genotypes grown in Romania and its correlations with air temperature. International Journal of Biometeorology, 62, 2007–2013. https://doi.org/10.1007/s00484-018-1606-3
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Floret, C., Galan, M., LeFloc'h, E., Orshan, G., & Romane, F. (1990). Growth forms and phenomorphology traits along an environmental gradient: tools for studying vegetation? Journal of Vegetation Science, 1, 71-80. https://doi.org/10.2307/3236055
Flynn, D.F.B., & Wolkovich, E.M. (2018). Temperature and photoperiod drive spring phenology across all species in a temperate forest community. New Phytologist, 219, 1353–1362. https://doi.org/10.1111/nph.15232
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Ilhan, G. (2023). Sensory Evaluation, Biochemical, Bioactive and Antioxidant Properties in Fruits of Wild Blackthorn (Prunus spinosa L.) Genotypes from Northeastern Türkiye. Horticulturae, 9, 1052. https://doi.org/10.3390/horticulturae9091052
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Nagavani, V., & Raghava Rao, T. (2010). Evaluation of antioxidant potential and qualitative analysis of major polyphenols by RP-HPLC in Nymphaea nouchali Brum flowers. International Journal of Pharmacy and Pharmaceutical Sciences 2, (SUPPL. 4), 98–104.
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Ocokoljić, M., Petrov, Dj., Galečić, N., Skočajić, D., Košanin, O., & Simović, I. (2023b) Phenological Flowering Patterns of Woody Plants in the Function of Landscape Design: Case Study Belgrade. Land, 12 (3), 706. https://doi.org/10.3390/land12030706
Ocokoljić, M., Petrov, Dj., Vujičić, D., & Galečić, N. (2023a). Effects of climate parameters on blackthorn in agroforestry ecotones as green road infrastructure elements. XIV International Scientific Agriculture Symposium “AGROSYM 2023”, Book of proceedings, ISBN 978-99976-816-1-4 pp. 853-858.
Opriş, O., Soran, M.L., Lung, I., Stegarescu, A., Guţoiu, S., Podea, R., & Podea, P. (2021). Optimization of Extraction Conditions of Polyphenols, Antioxidant Capacity and Sun Protection Factor from Prunus spinosa Fruits. Application in Sunscreen Formulation. Journal of the Iranian Chemical Society, 18, 2625–2636. https://doi.org/10.1007/s13738-021-02217-9
Petrov, Dj., Ocokoljić, M., Galečić, N., Skočajić. D., & Simović, I. (2024). Adaptability of Prunus cerasifera Ehrh. to Climate Changes in Multifunctional Landscape. Atmosphere, 15, 335. https://doi.org/10.3390/atmos15030335
Pinacho, R., Cavero, R.Y., Astiasarán, I., Ansorena, D., & Calvo, M.I. (2015). Phenolic compounds of blackthorn (Prunus spinosa L.) and influence of in vitro digestion on their antioxidant capacity. Journal of Functional Foods, 19, 49–62. https://doi.org/10.1016/J.JFF.2015.09.015
Price, T.D., Qvarnström, A., & Irwin, D.E. (2003). The role of phenotypic plasticity in driving genetic evolution. Proceedings of the Royal Society of London. Series B: Biological Sciences, 270, 1433-1440. https://doi.org/10.1098/rspb.2003.2372
Przybylski, R., Lee, Y.C., & Eskin, N.A.M. (1998). Antioxidant and radical-scavenging activities of buckwheat seed components. JAOCS, Journal of the American Oil Chemists’ Society, 75(11), 1595–1601. https://doi.org/10.1007/s11746-998-0099-3
Quade, D. (1974). Nonparametric partial correlation. Chapter 13 in Measurement in the Social Sciences: Theories and Strategies. (ed. by HM Blalock, Jr.) Aldine, Chicago, USA.
Rahman, M.A., Moser, A., Rötzer, T., & Pauleit, S. (2017). Microclimatic differences and their influence on transpirational cooling of Tilia cordata in two contrasting street canyons in Munich, Germany. Journal of Agricultural Meteorology, 232, 443–456. https://doi.org/10.1016/j.agrformet.2016.10.006
Re, R., Pellegrini, N., Proteggente, A., Pannala, A., Yang, M., & Rice-Evans, C. (1999). Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radical Biology and Medicine, 26, 1231-1237. https://doi.org/10.1016/S0891-5849(98)00315-3
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Roloff, A., Grundmann, B., & Korn, S. (2013). Trockenstress-Toleranz bei Stadtbäumen – Anpassungs- und Schutzstrategien/Arteneignung. Jahrbuch der Baumpflege (ed. by Dujesiefken D), Haymarket Media, Braunschweig, Germany, pp 173–185.
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Rustum, R., Adeloye, A.J., & Mwale, F. (2017). Spatial and temporal Trend Analysis of Long Term rainfall records in data-poor catchments with missing data, a case study of Lower Shire floodplain in Malawi for the Period 1953-2010. Hydrology and Earth System Science discussion. https://doi.org/10.5194/hess-2017-601.
Ružičkova, H., Halada, L., Jedlička, L., & Kalivodova, E. (1996). Biotopy Slovenksa [Biotopes of Slovakia]. Ustavkrajinnej ekologie SAV, Bratislava, Slovakia.
Sjöman, H., Gunnarsson, A., Pauleit, S., & von Bothmer, R. (2012). Selection approach of urban trees for inner-city environments: learning from nature. Arboriculture & Urban Forestry, 38, 194–204. DOI: 10.48044/jauf.2012.028
Skrovankova, S., Sumczynski, D., Mlcek, J., Jurikova, T., & Sochor, J. (2015). Bioactive compounds and antioxidant activity in different types of berries. International Journal of Molecular Sciences, 16(10), 24673-24706. https://doi.org/10.3390/ijms161024673
Stilinović, S. (1985). Semenarstvo šumskog i ukrasnog drveća i žbunja [Seed production of forest and ornamental trees and shrubs]. Šumarski fakultet Beograd, Belgrade, Serbia.
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Teskey, R., Wertin, T., Bauweraerts, I., Ameye, M., McGuire, M.A., & Steppe, K. (2015). Responses of tree species to heat waves and extreme heat events. Plant, Cell & Environment, 38, 1699–1712. https://doi.org/10.1111/pce.12417
Vander Mijnsbrugge, K., Depypere, L., Michiels, B., & De Cuyper, B. (2016a). Genetic and temporal plastic variation in bud burst, bud set and flower opening responses of local versus non-local provenances of Prunus spinosa in a provenance trial. Basic and Applied Ecology, 17, 262–272. https://doi.org/10.1016/j.baae.2015.11.005
Vander Mijnsbrugge, K., Turcsán, A., Depypere, L., & Steenackers, M. (2016b). Variance, Genetic Control, and Spatial Phenotypic Plasticity of Morphological and Phenological Traits in Prunus spinosa and Its Large Fruited Forms (P.×fruticans). Frontiers of plant science, 7, 1641. https://doi.org/10.3389/fpls.2016.01641
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WMO (2021). State of the Global Climate 2021: WMO Provisional Report. World Meteorological Organization (WMO), 47 https://library.wmo.int/ doc_num.php?explnum_id=10859 (Accessed on 10. Oktobra 2024)
Arnot, C., Fisher, P.F., Wadsworth, R., & Wellens, J. (2004), Landscape Metrics with Ecotones: Pattern under Uncertainty. Landscape Ecology, 19, 181–195. DOI:10.15835/nbha47411709
Batrićević, A., & Batanjski, V. (2014). Zaštita životinja u Srbiji – kaznenopravni i ekološki aspekti [Animal protection in Serbia - criminal law and ecological aspects]. Institut za kriminološka i sociološka istraživanja. Belgrade, Serbia.
Benzie, I., & Strain, J. (1996), The Ferric Reducing Ability of Plasma (FRAP) as a Measure of “Antioxidant Power: The FRAP Assay”. Analytical Biochemistry, 239, 70-76. http://dx.doi.org/10.1006/abio.1996.0292
Cosmulescu, S., & Gavrila Calusaru, F. (2020). Influence of temperature on blackthorn (Prunus spinosa L.) phenophases in spring season. Journal of Agricultural Meteorology, 76, 53–57. https://doi.org/10.2480/agrmet.D-19-00030
Cosmulescu, S., & Ionescu, M.B. (2018). Phenological calendar in some walnut genotypes grown in Romania and its correlations with air temperature. International Journal of Biometeorology, 62, 2007–2013. https://doi.org/10.1007/s00484-018-1606-3
Crane, M.B., & Lawrence, W.J. (1952). The Genetics of Garden Plants. 4th ed. MacMillan & Company, London, UK.
Floret, C., Galan, M., LeFloc'h, E., Orshan, G., & Romane, F. (1990). Growth forms and phenomorphology traits along an environmental gradient: tools for studying vegetation? Journal of Vegetation Science, 1, 71-80. https://doi.org/10.2307/3236055
Flynn, D.F.B., & Wolkovich, E.M. (2018). Temperature and photoperiod drive spring phenology across all species in a temperate forest community. New Phytologist, 219, 1353–1362. https://doi.org/10.1111/nph.15232
Horvat, J., & Mijoč, J. (2012). Osnove statistike [Basics of statistics]. Naklada Ljevak d.o.o., Zagreb, 482.
Ilhan, G. (2023). Sensory Evaluation, Biochemical, Bioactive and Antioxidant Properties in Fruits of Wild Blackthorn (Prunus spinosa L.) Genotypes from Northeastern Türkiye. Horticulturae, 9, 1052. https://doi.org/10.3390/horticulturae9091052
Jiménez, S., Jiménez-Moreno, N., Luquin, A., Laguna, M., Rodríguez-Yoldi, M.J., & Ancín-Azpilicueta, C. (2017). Chemical composition of rosehips from different Rosa species: an alternative source of antioxidants for the food industry. Food Additives & Contaminants: Part A, 34(7), 1121-1130. https://doi.org/10.1080/19440049.2017.1319071
Klein, T. (2014). The variability of stomatal sensitivity to leaf water potential across tree species indicates a continuum between isohydric and anisohydric behaviours. Functional ecology, 28, 1313–1320. https://doi.org/10.1111/1365-2435.12289
Lalić, B., Ejcinger, J., Dalamarta, A., Orlandini, S., Firanj Sremac, A., & Paher, B. (2021). Meteorologija i klimatologija za agronome [Meteorology and climatology for agronomists]. Univerzitet u Novom Sadu-Poljoprivredni fakultet. Novi Sad, Srbija, 219 p.
LWG (2018). Forschungsprojekt Stadtgrün 2021. Neue Bäume braucht das Land. www.lwg.bayern.de. (Accessed 20. Avgust 2024)
Marakoglu, T., Arslan, D., Ozcan, M., & Hacıseferogulları, H. (2005). Proximate Composition and Technological Properties of Fresh Blackthorn (Prunus spinosa L. Subsp Dasyphylla (Schur.)) Fruits. Journal Of Food Engineering, 68, 137–142. https://doi.org/10.1016/j.jfoodeng.2004.05.024
Markham, K.R. (1989). Methods in Plant Biochemistry. Academic Press, London, UK, pp.197–237.
Meier, U. (1997). BBCH-Monograph Growth Stages of Plants. [Entwicklungsstadien von Pflanzen. Estadios de las Plantas. Stades De Développement des Plantes]; Blackwell Wissenschafts-Verla: Berlin, Germany; Vienna, Austria.
Memete, A.R., Sarac, I., Teusdea, A.C., Budau, R., Bei, M., & Vicas, S.I. (2023). Bioactive Compounds and Antioxidant Capacity of Several Blackberry (Rubus spp.) Fruits Cultivars Grown in Romania. Horticulturae, 9, 556. https://doi.org/10.3390/horticulturae9050556
Nagavani, V., & Raghava Rao, T. (2010). Evaluation of antioxidant potential and qualitative analysis of major polyphenols by RP-HPLC in Nymphaea nouchali Brum flowers. International Journal of Pharmacy and Pharmaceutical Sciences 2, (SUPPL. 4), 98–104.
Ocokoljić, M., & Petrov, Dj. (2022). Dekorativna Dendrologija [Decorative Dendrology]. Univerzitet u Beogradu—Šumarski Fakultet: Belgrade, Serbia, p. 409. (In Serbian) ISBN 978-86-7299-339-4.
Ocokoljić, M., Petrov, Dj., Galečić, N., Skočajić, D., Košanin, O., & Simović, I. (2023b) Phenological Flowering Patterns of Woody Plants in the Function of Landscape Design: Case Study Belgrade. Land, 12 (3), 706. https://doi.org/10.3390/land12030706
Ocokoljić, M., Petrov, Dj., Vujičić, D., & Galečić, N. (2023a). Effects of climate parameters on blackthorn in agroforestry ecotones as green road infrastructure elements. XIV International Scientific Agriculture Symposium “AGROSYM 2023”, Book of proceedings, ISBN 978-99976-816-1-4 pp. 853-858.
Opriş, O., Soran, M.L., Lung, I., Stegarescu, A., Guţoiu, S., Podea, R., & Podea, P. (2021). Optimization of Extraction Conditions of Polyphenols, Antioxidant Capacity and Sun Protection Factor from Prunus spinosa Fruits. Application in Sunscreen Formulation. Journal of the Iranian Chemical Society, 18, 2625–2636. https://doi.org/10.1007/s13738-021-02217-9
Petrov, Dj., Ocokoljić, M., Galečić, N., Skočajić. D., & Simović, I. (2024). Adaptability of Prunus cerasifera Ehrh. to Climate Changes in Multifunctional Landscape. Atmosphere, 15, 335. https://doi.org/10.3390/atmos15030335
Pinacho, R., Cavero, R.Y., Astiasarán, I., Ansorena, D., & Calvo, M.I. (2015). Phenolic compounds of blackthorn (Prunus spinosa L.) and influence of in vitro digestion on their antioxidant capacity. Journal of Functional Foods, 19, 49–62. https://doi.org/10.1016/J.JFF.2015.09.015
Price, T.D., Qvarnström, A., & Irwin, D.E. (2003). The role of phenotypic plasticity in driving genetic evolution. Proceedings of the Royal Society of London. Series B: Biological Sciences, 270, 1433-1440. https://doi.org/10.1098/rspb.2003.2372
Przybylski, R., Lee, Y.C., & Eskin, N.A.M. (1998). Antioxidant and radical-scavenging activities of buckwheat seed components. JAOCS, Journal of the American Oil Chemists’ Society, 75(11), 1595–1601. https://doi.org/10.1007/s11746-998-0099-3
Quade, D. (1974). Nonparametric partial correlation. Chapter 13 in Measurement in the Social Sciences: Theories and Strategies. (ed. by HM Blalock, Jr.) Aldine, Chicago, USA.
Rahman, M.A., Moser, A., Rötzer, T., & Pauleit, S. (2017). Microclimatic differences and their influence on transpirational cooling of Tilia cordata in two contrasting street canyons in Munich, Germany. Journal of Agricultural Meteorology, 232, 443–456. https://doi.org/10.1016/j.agrformet.2016.10.006
Re, R., Pellegrini, N., Proteggente, A., Pannala, A., Yang, M., & Rice-Evans, C. (1999). Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radical Biology and Medicine, 26, 1231-1237. https://doi.org/10.1016/S0891-5849(98)00315-3
Reaumur, R.A.F. (1735). Observations du thermomètre faites à Paris pendant l' année 1735 comparée sa veccelles quiontété faitessous la ligne à l' Ile de France, à Algere tenquelques-unes de nos îles de l’ Amérique. Académie Royale des Sciences, 545–580.
Roloff, A., Grundmann, B., & Korn, S. (2013). Trockenstress-Toleranz bei Stadtbäumen – Anpassungs- und Schutzstrategien/Arteneignung. Jahrbuch der Baumpflege (ed. by Dujesiefken D), Haymarket Media, Braunschweig, Germany, pp 173–185.
Ruiz-Rodríguez, B.M., De Ancos, B., Sánchez-Moreno, C., Fernández-Ruiz, V., de Cortes Sánchez-Mata, M., Cámara, M., & Tardío, J. (2014). Wild blackthorn (Prunus spinosa L.) and hawthorn (Crataegus monogyna Jacq.) fruits as valuable sources of antioxidants. Fruits, 69(1), 61-73. https://doi.org/10.1051/fruits/2013102
Rustum, R., Adeloye, A.J., & Mwale, F. (2017). Spatial and temporal Trend Analysis of Long Term rainfall records in data-poor catchments with missing data, a case study of Lower Shire floodplain in Malawi for the Period 1953-2010. Hydrology and Earth System Science discussion. https://doi.org/10.5194/hess-2017-601.
Ružičkova, H., Halada, L., Jedlička, L., & Kalivodova, E. (1996). Biotopy Slovenksa [Biotopes of Slovakia]. Ustavkrajinnej ekologie SAV, Bratislava, Slovakia.
Sjöman, H., Gunnarsson, A., Pauleit, S., & von Bothmer, R. (2012). Selection approach of urban trees for inner-city environments: learning from nature. Arboriculture & Urban Forestry, 38, 194–204. DOI: 10.48044/jauf.2012.028
Skrovankova, S., Sumczynski, D., Mlcek, J., Jurikova, T., & Sochor, J. (2015). Bioactive compounds and antioxidant activity in different types of berries. International Journal of Molecular Sciences, 16(10), 24673-24706. https://doi.org/10.3390/ijms161024673
Stilinović, S. (1985). Semenarstvo šumskog i ukrasnog drveća i žbunja [Seed production of forest and ornamental trees and shrubs]. Šumarski fakultet Beograd, Belgrade, Serbia.
Tanasijević, Đ. (1963) Pedološka karta Srbije, list Bepgrad 1, razmera 1:50.000 [Pedological map of Serbia, sheet Bepgrad 1, scale 1:50.000]. Institut za proučavanje zemljišta Beograd i “Geokarta” Beograd.
Teskey, R., Wertin, T., Bauweraerts, I., Ameye, M., McGuire, M.A., & Steppe, K. (2015). Responses of tree species to heat waves and extreme heat events. Plant, Cell & Environment, 38, 1699–1712. https://doi.org/10.1111/pce.12417
Vander Mijnsbrugge, K., Depypere, L., Michiels, B., & De Cuyper, B. (2016a). Genetic and temporal plastic variation in bud burst, bud set and flower opening responses of local versus non-local provenances of Prunus spinosa in a provenance trial. Basic and Applied Ecology, 17, 262–272. https://doi.org/10.1016/j.baae.2015.11.005
Vander Mijnsbrugge, K., Turcsán, A., Depypere, L., & Steenackers, M. (2016b). Variance, Genetic Control, and Spatial Phenotypic Plasticity of Morphological and Phenological Traits in Prunus spinosa and Its Large Fruited Forms (P.×fruticans). Frontiers of plant science, 7, 1641. https://doi.org/10.3389/fpls.2016.01641
Veličković, J.M., Kostić, D.A., Stojanović, G.S., Mitić, S.S., Mitić, M.N., Randelović, S.S., & Đorđević, A.S. (2014). Phenolic composition, antioxidant and antimicrobial activity of the extracts from Prunus spinosa L fruit. Hemijska Industrija, 68(3), 297-303. https://doi.org/10.2298/HEMIND130312054V
WMO (2021). State of the Global Climate 2021: WMO Provisional Report. World Meteorological Organization (WMO), 47 https://library.wmo.int/ doc_num.php?explnum_id=10859 (Accessed on 10. Oktobra 2024)
Published
2025/10/03
Section
Original Scientific Paper