Impact of mistletoe infestation on tree water status in Anatolian black pine trees in a semi-arid Mediterranean forest stand

Yıl 2025, Cilt: 26 Sayı: 3, 310 - 318, 30.09.2025

Mehmet Said Özçelik , Şükran Oğuzoğlu

https://doi.org/10.18182/tjf.1770211

Öz

Mistletoes can adversely affect the hydraulic functioning of their host trees by continuously extracting water and nutrients. This study investigated the effects of pine mistletoe (Viscum album subsp. austriacum) on water status in Anatolian black pine (Pinus nigra subsp. pallasiana) trees in a natural forest stand in Mediterranean Region, Türkiye, where mistletoe-infected and non-infected trees coexisted. Continuous stem radius change measurements were obtained throughout the 2024 growing period using automatic band dendrometers to compare maximum daily shrinkage (MDS) and tree water deficit (TWD) between infected and non-infected trees. Simultaneously, soil water potential was measured, and meteorological variables were recorded by a nearby station. Mistletoe-infected trees exhibited 92% higher TWD and 12% higher MDS compared to non-infected trees. In both groups, TWD and MDS were closely associated with meteorological variables. TWD showed significant correlations with soil water potential, global radiation, and vapor pressure deficit, while MDS was mainly related to air temperature, solar radiation, and soil water potential. Precipitation influenced MDS in non-infected trees but had no significant effect on infected trees. Moreover, correlation coefficients with environmental factors were consistently higher in infected trees. These findings indicate that pine mistletoe is associated with a marked deterioration in host water status, suggesting increased drought sensitivity and reduced physiological resilience under Mediterranean climatic conditions. Overall, this highlights the potential ecological risk posed by mistletoe infestation in drought-prone forest ecosystems.

Anahtar Kelimeler

Drought stress , Maximum daily shrinkage , Pinus nigra , Tree water deficit , Viscum album parasitism

Yarı kurak bir Akdeniz orman ekosisteminde ökse otunun karaçam ağaçlarının su durumu üzerindeki etkisi

Öz

Ökse otları, konukçu ağaçtan sürekli su ve mineral madde alarak konukçu ağacın hidrolik işlevini olumsuz etkileyebilmektedir. Bu çalışma, çam ökse otunun (Viscum album subsp. austriacum) karaçam (Pinus nigra subsp. pallasiana) ağaçlarının su durumu üzerindeki etkilerini araştırmayı amaçlamaktadır. Araştırma, Türkiye’nin Akdeniz Bölgesi’nde, hem ökse otu ile enfekte olmuş hem de sağlıklı karaçam bireylerinin bir arada bulunduğu doğal bir meşcerede yürütülmüştür. 2024 yılı büyüme dönemi boyunca, enfekte ve sağlıklı ağaçlara kurulan otomatik şerit dendrometreler ile gövde yarıçapı değişiklikleri sürekli olarak kaydedilmiş; bu veriler kullanılarak maksimum günlük daralma (MGD) ve ağaç su açığı (ASA) parametreleri hesaplanmıştır. Eşzamanlı olarak toprak su potansiyeli ölçülmüş ve sahaya kurulan meteoroloji istasyonu aracılığıyla meteorolojik değişkenler izlenmiştir. Sonuçlar, enfekte ağaçların sağlıklı ağaçlara kıyasla %92 daha yüksek ASA ve %12 daha yüksek MGD değerlerine sahip olduğunu göstermiştir. Hem enfekte hem de sağlıklı ağaçlardaki ASA ve MGD değerlerinin meteorolojik değişkenlerle yakından ilişkili olduğu belirlenmiştir. ASA, toprak su potansiyeli, küresel radyasyon ve buhar basıncı açığı ile güçlü korelasyon gösterirken, MGD hava sıcaklığı, güneş radyasyonu ve toprak su potansiyeli ile ilişkili bulunmuştur. Yağış, sağlıklı ağaçların MGD’si üzerinde etkili olurken, enfekte ağaçlar üzerinde anlamlı bir etkisi gözlenmemiştir. Ayrıca, ağaç su durumu parametreleri ile çevresel faktörler arasındaki korelasyon katsayılarının enfekte ağaçlarda daha yüksek olduğu tespit edilmiştir. Bulgular, ökse otunun karaçam ağaçlarında su durumunu olumsuz etkilediğini, bu durumun Akdeniz iklim koşullarında enfekte ağaçların kuraklığa duyarlılığını artırabileceğini ve fizyolojik dayanıklılığını azaltabileceğini ortaya koymaktadır.

Anahtar Kelimeler

Kuraklık stresi , Maksimum günlük daralma , Pinus nigra , Ağaç su açığı , Viscum album parazitizmi

Kaynakça

• Alderotti, F., Bussotti, F., Brunetti, C., Ferrini F., Gori, A., Pollastrini, M., 2024. Linking patterns of forest dieback to triggering climatic and weather events: an overview on Mediterranean forests. iForest, 17: 309-316.
• Ali, E., Cramer, W., Carnicer, J., Georgopoulou, E., Hilmi, N.J.M., Le Cozannet, G., and Lionello, P., 2022. Cross-Chapter Paper 4: Mediterranean Region. In: Climate Change 2022: Impacts, Adaptation and Vulnerability. Contribution of Working Group II to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change, (Eds: Pörtner, H.O., Roberts, D.C., Tignor, M., Poloczanska, E.S., Mintenbeck, K., Alegría, A., Craig, M., Langsdorf, S., Löschke, S., Möller, V., Okem, A., Rama, B.), Cambridge University Press, Cambridge and New York, pp. 2233–2272. doi:10.1017/9781009325844.021.Amutenya, A., Kwembeya, E., Shikangalah, R., Tsvuura, Z., 2023. Photosynthesis, chlorophyll content and water potential of a mistletoe-host pair in a semi-arid savanna. South African Journal of Botany,163: 311-315.
• Aryal, S., Häusser, M., Grießinger, J., Fan, Z., Bräuning, A., 2020. “dendRoAnalyst”: A tool for processing and analysing dendrometer data. Dendrochronologia, 64:125772.
• Bachofen, C., Tumber-Dávila, S.J., Mackay, D.S., McDowell, N.G., Carminati, A., Klein, T., Stocker, B.D., Mencuccini, M., Grossiord, C., 2024. Tree water uptake patterns across the globe. New Phytologist, 242: 1891-1910.
• Baysal, İ., 2023. Batı Karadeniz Bölgesi Kazdağı göknarı ormanlarında göknar ökseotu bulunma ve bulaşma durumu: Kökez Orman İşletme Şefliği örneği. Türk Ormancılık Dergisi, 24(3): 241- 250.
• Bilgili, E., Öztürk, M., Coşkuner, K. A., Baysal, İ., Serdar, B., Yavuz, H., Eroğlu, M., Usta, Y., 2018. Quantifying the effect of pine mistletoe on the growth of scots pine. Forest Pathology, 48: e12435.
• Bilgili, E, Coşkuner K.A., Öztürk M., 2020. Leaf area – sapwood area relationship in Scots pine (Pinus sylvestris L.) under mistletoe (Viscum album ssp. austriacum) infection. Dendrobiology, 84: 1-11.
• Cocoletzi, E., Angeles, G., Briones, O., Ceccantini G., Ornelas J.F., 2020. The ecophysiology of a neotropical mistletoe depends on the leaf phenology of its tree hosts. American Journal of Botany, 107(9): 1225–1237.
• Conejero, W., Alarcón, J. J., García-Orellana, Y., Abrisqueta, J. M., Torrecillas, A., 2007. Daily sap flow and maximum daily trunk shrinkage measurements for diagnosing water stress in earlymaturing peach trees during the post-harvest period. Tree Physiology, 27(1): 81–88.
• Çatal, Y., Carus, S., 2011. Effect of pine mistletoe on radial growth of crimean pine (Pinus nigra) in Turkey. Journal of Environmental Biology, 32(3): 263-270.
• Deslauriers, A., Rossi, S., Anfodillo, T., 2007. Dendrometer and intra-annual tree growth: What kind of information can be inferred? Dendrochronologia, 25(2): 113-124.
• Dunkleberger, R., Sauchyn, D.J., Vanderwel, M.C., 2023. Using thermal imagery and changes in stem radius to assess water stress in two coniferous tree species. Agricultural and Forest Meteorology, 341:109686.
• Drew, D.M., Richards, A.E., Downes, G.M., Cook, G.D., Baker, P.B., 2011. The development of seasonal tree water deficit in Callitris intratropica. Tree Physiology, 31(9): 953–964.
• Garkoti, S.C, Akoijam, S.B., Singh, S.P., 2002. Ecology of water relations between mistletoe (Taxillus vestitus) and its host oak (Quercus floribunda). Tropical Ecology, 43(2): 243-249.
• Gentilesca, T., Camarero, J.J., Colangelo, M., Nolè, A., Ripullone F., 2017. Drought-induced oak decline in the western Mediterranean region: an overview on current evidences, mechanisms and management options to improve forest resilience. iForest, 10: 796-806.
• Glatzel, G., Geils B.W., 2009. Mistletoe ecophysiology: Host-parasite interactions. Botany, 87: 10-15.
• Göl, Ç., Serdar, B., Öztürk, M., Coşkuner, K.A., Bilgili, E, 2018. Viscum album L. subsp. austriacum (Wiesb.) Vollman (Çam ökse otu)'un Pinus sylvestris L. (Sarıçam)'in odun elemanlarına etkisi. Düzce Üniversitesi Bilim ve Teknoloji Dergisi, 6: 1354-1363.
• Griebel, A., Peters, J.M.R., Metzen, D., Maier, C., Barton, C.V.M., Speckman, H.N., Boer, M.M., Nolan, R.H., Choat, B., Pendall, E., 2022. Tapping into the physiological responses to mistletoe infection during heat and drought stress. Tree Physiology, 42(3): 523–536.
• Grossiord, C., Buckley, T.N., Cernusak, L.A., Novick, K.A., Poulter, B., Siegwolf, R.T.W., Sperry, J.S., McDowell, N.G., 2020. Plant responses to rising vapor pressure deficit. New Phytologist, 226: 1550-1566.
• Güney, A., Gülsoy, S., Şentürk, Ö., Niessner, A., Küppers, M., 2020a. Environmental control of daily stem radius increment in the montane conifer Cedrus libani. Journal of Forestry Research, 31: 1159–1171.
• Güney, A., Zweifel, R., Türkan, S. Zimmermann, R., Wachendorf, W., Güney, C.O., 2020b. Drought responses and their effects on radial stem growth of two co-occurring conifer species in the Mediterranean mountain range. Annals of Forest Science, 77: 105.
• Hawksworth F. G., 1977. The 6-Class Dwarf Mistletoe Rating System. USDA Forest Service, General Technical Report, RM-48.
• Hidalgo-Triana, N., Solakis, A., Casimiro-Soriguer, F., Choe, H., Navarro, T., Pérez-Latorre, A.V., Thorne, J.H., 2023. The high climate vulnerability of western Mediterranean forests. Science of The Total Environment, 895:164983.
• Kanat, M., Alma, M.H., Sivrikaya, F., 2010. The Effect of Viscum album L. on annual diameter increment of Pinus nigra Arn. African Journal of Agricultural Research, 5(2): 166-171.
• Kubov, M., Fleischer, P., Jr., Rozkošný, J., Kurjak, D., Konôpková, A., Galko, J., Húdoková, H., Lalík, M., Rell, S., Pittner, J., Fleischer, P., Sr., 2020. Drought or severe drought? Hemiparasitic yellow mistletoe (Loranthus europaeus) amplifies drought stress in sessile oak trees (Quercus petraea) by altering water status and physiological responses. Water, 12(11): 2985. https://doi.org/10.3390/w12112985
• Kumbaşlı, M., Keten, A., Beskardes, V., Makineci, E., Özdemir, E., Yilmaz, E., Zengin, H., Sevgi, O., Yilmaz, H. C., Caliskan, S., 2011. Hosts and distribution of yellow mistletoe (Loranthus europaeus Jacq. (Loranthaceae)) on northern Strandjas oak forests-Turkey. Scientific Research and Essays, 6(14): 2970-2975.
• Lionello, P., Scarascia, L., 2018. The relation between climate change in the Mediterranean region and global warming. Regional Environmental Change, 18: 1481–1493.
• Makowski, D., Ben-Shachar, M.S, Patil, I., Lüdecke, D., 2020. Methods and algorithms for correlation analysis in R. Journal of Open Source Software, 5(51): 2306.
• Mathiasen, R.L., Nickrent, D.L., Shaw, D.C., Watson, D.M., 2008.
• Mistletoes: pathology, systematics, ecology, and management. Plant Disease, 92(7): 988-1006.
• Muche, M., Muasya, A.M., Tsegay, B.A., 2022. Biology and resource acquisition of mistletoes, and the defense responses of host plants. Ecological Processes, 11,:24.
• Mutlu, S., Ilhan, V., Turkoglu, H, I, 2016. Mistletoe (Viscum album) infestation in the Scots pine stimulates drought-dependent oxidative damage in summer. Tree Physiology, 36(4): 479–489.
• Nadkarni M.N., Merwin, M.C., Nieder J., 2001. Forest Canopies: Plant Diversity. In: Encyclopedia of Biodiversity (Ed: Levin, S.), Academic Press, San Diego, pp. 516-527, ISBN 9780123847201.
• Ortuño, M.F., García-Orellana, Y., Conejero, W., Ruiz-Sánchez, M.C., Mounzer, O., Alarcón, JJ., Orrecillas, A., 2006. Relationships between climatic variables and sap flow, stem water potential and maximum daily trunk shrinkage in lemon trees. Plant and Soil, 27: 229–242.
• Özdemir, S., Özkan, K., Mert, A., 2020. An ecological perspective on climate change scenarios. Biological Diversity and Conservation, 13(3): 361-371. DOI: 10.46309/biodicon.2020. 762985.
• Özkan, K., Makineci, E., Gülsoy S., Özdemir, S., 2021. Orman ekosistemleri ve iklim değişimi. Ekoloji ve Ekonomi Ekseninde Ormancılık (Ed: Pakdemirli, B., Küçük, Ö., Bayraktar, Z., Takmaz, S.), Sonçağ Yayıncılık, Ankara, pp. 359-405. ).
• Öztürk, M., Coskuner, K. A., Usta, Y., Serdar, B., Bilgili, E., 2019. The effect of mistletoe (Viscum album) on branch wood and needle anatomy of Scots pine (Pinus sylvestris). IAWA Journal, 40(2): 352-365.
• Öztürk, M., Coskuner, K.A., Serdar, B., Atar, F., Bilgili E., 2022. Impact of white mistletoe (Viscum album ssp. abietis) infection severity on morphology, anatomy and photosynthetic pigment content of the needles of cilicican fir (Abies cilicica). Flora, 294: 152135.
• Öztürk, M. 2023. Ökseotunun Toros Göknarı büyüme ve gelişme parametreleri üzerine etkileri. Doktora tezi, Karadeniz Teknik Üniversitesi, Fen Bilimleri Enstitüsü, Trabzon.
• Perron, N., Baltzer, J. L., Detto, M., Nehemy, M., Spence, C., Hould‐Gosselin, G., Alcock, H., Hadiwijaya, B., Laroque, C.P., Sonnentag O., 2024. Radiation, air temperature, and soil water availability drive tree water deficit across temporal scales in Canada's western boreal forest. Geophysical Research Letters, 51: e2023GL107477.
• Peters, R.L., Basler, D., Zweifel, R., Steger, D.N., Zhorzel, T., Zahnd, C., Hoch, G., Kahmen, A., 2025. Normalized tree water deficit: an automated dendrometer signal to quantify drought stress in trees. New Phytologist, 247: 1186-1198. https://doi.org/10.1111/ nph.70266
• Pieruschka, R., Huber, G., Berry, J.A., 2010. Control of transpiration by radiation. Proceedings of the National Academy of Sciences of the United States of America, 107(30): 13372-13377.
• Raftoyannis, Y., Radoglou, K., Bredemeier, M., 2015. Effects of mistletoe infestation on the decline and mortality of Abies cephalonica in Greece. Annals of Forest Research, 58(1): 55-65.
• Sala A., Carey E.V., Callaway R.M., 2001. Dwarf mistletoe affects whole-tree water relations of Douglas fir and western larch primarily through changes in leaf to sapwood ratios. Oecologia, 126: 42–52.
• Sakıcı, O.E., Ozcan G.E., Saglam F., Seki, M., 2022. The effect of White Mistletoe (Viscum album subsp. abietis (Wiesb.) Abromerit) on diameter increment in Kazdağı fir stands. Journal of Biometry Studies, 2(1):15-23.
• Sakıcı O.E., Ozcan, G.E., Seki, M., Saglam, F., 2023. The effects of Pine Mistletoe (Viscum album subsp. austriacum) on the growth of Scots pine and Crimean pine in Turkey. Forest Pathology, 53(2): e12802.
• Senf, C., Buras, A., Zang, C.S., Ramming, A., Seidl, R., 2020. Excess forest mortality is consistently linked to drought across Europe. Nature Communications, 11: 6200.
• Sönmez, T., 2014. Sarıçam (Pinus sylvestris L.) gelişimi üzerine ökseotu’nun etkisi. Artvin Çoruh Üniversitesi Orman Fakiltesi Dergisi, 15, 1: 64-72.
• Shapira, O., Hochberg, U., Joseph, A., McAdam, S., Azoulay-Shemer, T., Brodersen, C.R., Holbrook, N.M., Zait, Y., 2024. Wind speed affects the rate and kinetics of stomatal conductance. The Plant Journal, 120: 1552-1562.
• Szmidla, H., Tkaczyk, M., Plewa, R., Tarwacki, G., Sierota, Z., 2019. Impact of common mistletoe (Viscum album L.) on Scots pine forests—A call for action. Forests, 10(10): 847.
• Szurpnicka, A., Kowalczuk, A., Szterk, A., 2020. Biological activity of mistletoe: in vitro and in vivo studies and mechanisms of action. Archives of Pharmacal Research, 43: 593–629.
• Teshome, D.T., Elija, Z.G., Sanushka, N., 2020. The threat of the combined effect of biotic and abiotic stress factors in forestry under a changing climate. Frontiers in Plant Science, 11: 6101009.
• Ullmann, I., Lange, O.L., Ziegler, H., Ehleringer, J., Schulze E.D., Cowan, I.R., 1985. Diurnal courses of leaf conductance and transpiration of mistletoes and their hosts in Central Australia. Oecologia, 67: 577–587.
• Urban, J., Gebauer, R., Nadezhdina, N., Cermak, J., 2012. Transpiration and stomatal conductance of mistletoe (Loranthus europaeus) and its host plant, downy oak (Quercus pubescens). Biologia, 67: 917–926.
• Usta, A., Yılmaz, M., 2021. Effects of land use and topographic variables on distribution of pine mistletoe (Viscum album subsp. austriacum (Wiesb.) Vollm.) in northeastern Turkey. Cerne, 27: e-102618.
• Üstüner, T., 2018. Investigation of symptoms and hosts of semi parasite plant species in east Mediterranean and entral Anatolia region of Turkey. Kahramanmaraş Sütçü İmam University Journal of Agriculture and Nature, 21(3): 438-446.
• Vatandaşlar, C., Türkeş, M., Semerci, A., Karahan, A., 2023. Analyzing climate-induced mortality of Taurus fir based on temporal forest management plans and climatic variations and droughts in the Central Mediterranean sub- region of Turkey. European Journal of Forest Research, 142: 61–89.
• Wickham, H., François, R., Henry, L., Müller, K., 2022. dplyr: A grammar of data manipulation. R package version 1.1.4, https://dplyr.tidyverse.org.
• Yang, D., Goldstein, G., Wang M., Zhang, W., Wang A-Y., Liu, Y-Y., Hao, G-Y. 2017. Microenvironment in the canopy rivals the host tree water status in controlling sap flow of a mistletoe species. Tree Physiology, 37(4): 501–510.
• Yüksel, B., Akbulut, S., Keten A., 2005. Çam ökseotu (Viscum album ssp. austriacum (Wiesb.) Vollman)'nun zararı, biyolojisi ve mücadelesi. Süleyman Demirel Üniversitesi Orman Fakültesi Dergisi, 6(2): 111-124 (In Turkish).
• Zuber, D., 2004. Biological flora of central Europe: Viscum album L. Flora-Morphology, Distribution, Functional Ecology of Plants, 199(3): 181-203.
• Zweifel., R., Zimmermann., L., Newbery., D.M., 2005. Modeling tree water deficit from microclimate: an approach to quantifying drought stress. Tree Physiology, 25(2): 147–156.
• Zweifel, R., Bangerter, S., Rigling, A., Sterck, F.J., 2012. Pine and mistletoes: How to live with a leak in the water flow and storage system? Journal of Experimental Botany, 63: 2565-2578.
• Zweifel, R., Haeni, M., Buchmann, N., Eugster, W., 2016. Are trees able to grow in periods of Stem shrinkage? New Phytologist, 211: 839- 849.