Iranian Journal of Forest

Iranian Journal of Forest

Structural Adaptations of Prunus argentea (Lam.) Rehder) to Browsing in the Semi-Arid Zagros Forests: Evidence from Anatomical Alterations in the Leaf Stomata and Trichomes

Document Type : Research Paper

Authors
1 Dep. of Forest Sciences, Ilam University, Ilam, Iran
2 Dep. of Forest Sciences, Faculty of Agriculture, University of Ilam, Iran
10.22034/ijf.2026.547734.2073
Abstract
Introduction: The forests of western Iran are among the natural ecosystems whose regeneration has been severely disrupted by anthropogenic and natural factors. Among these, livestock browsing is one of the most significant drivers of vegetation degradation and morphological alterations in plant species. This biotic stress can impair plant competitive ability by damaging photosynthetic organs, reducing growth, and altering leaf structure. This study was conducted to investigate the effects of livestock grazing on the anatomical traits of leaf stomata and trichomes in Prunus argentea (Lam.) Rehder, a shrub species native to the region. Given the limited experimental and laboratory-based studies on the micro-morphological responses of this species to environmental stressors, the present study aims to elucidate how browsing induces changes in leaf microstructure, thereby triggering distinct adaptive responses that may reflect divergent survival strategies under browsing pressure. Furthermore, the study identifies which leaf traits exhibit the highest degree of plasticity in response to the stress. The findings may contribute to improved forest management and conservation of valuable tree species that are also important forage resources.
Materials and Methods: In each of two study sites near Ilam City (Darreh-ye Arghavan and Choghasabz), three individual Prunus argentea shrubs exposed to continuous livestock browsing were randomly selected (six shrubs in total). For each selected shrub, leaf samples were collected from both lower branches (accessible to browsing animals) and upper branches (out of reach of browsers). Sampling was conducted along the dominant slope direction at each site. Overall, six samples per site (three shrubs × two vertical canopy positions) were collected. From each shrub, 10 leaves were randomly collected from lower (browsed-accessible) and 10 from upper (non- browsed) branches. To enhance observation of stomata and trichomes, photosynthetic pigments were removed from the abaxial leaf surface. Following staining and preparation of microscopic sections, 11 anatomical traits related to stomata, trichomes, and vein density were measured using a digital camera equipped with image analysis software. All measurements were repeated to ensure high repetition and accuracy.
Results: The results indicated that livestock browsing significantly altered most leaf anatomical traits. Specifically, the mean length and width of stomata, stomatal pore length, stomatal density, and stomatal pore index were significantly reduced under browsing pressure. In contrast, trichome dimensions, including length, width, and density, showed a significant increase in browsing conditions. Principal component analysis (PCA) revealed that traits such as stomatal density and stomatal pore index contributed most to the separation of non- browsed samples, whereas vein density and trichome width were more influential in distinguishing browsed samples. Furthermore, leaf trichome traits exhibited higher phenotypic plasticity compared to stomatal traits in Prunus argentea.
Conclusion: Overall, livestock browsing exerted significant effects on all anatomical traits of stomata and leaf trichomes, leading to notable changes in both the size and density of these structures. The high plasticity observed in trichome-related traits suggests a strong adaptive capacity of Prunus argentea in response to browsing-induced stress and altered environmental conditions. Therefore, anatomical modifications in leaves likely impact plant performance and physiological efficiency, potentially reducing overall productivity.
Keywords
Subjects

Abbasi, L., Shakeri, Z., Shabanian, N., & Bahari, M. (2015). Pollarding effects on Lebanon oak (Quercus libani Oliv.) leaf properties in Baneh forests. Iranian Journal of Forest7(1), 87-97. (In Persian).
Ahmadi Sani, N., Babaie Kafaky, S., Mataji, A., & Razaghnia, L. (2017). Investigation on the multipurpose planning in Zagros forests. Forest and Wood Products, 69(4), 735-745. (In Persian).
Bolger, T.P., & Turner, N.C. (1998). Transpiration efficiency of three Mediterranean annual pasture species and wheat. Oecologia, 115, 32–38.
Brodribb, T.J., & Field, T.S. (2010). Leaf hydraulic evolution led a surge in leaf photosynthetic capacity during early angiosperm diversification. Ecology Letters, 13, 175–183. https://doi.org/10.1111/j.1461-0248.2009.01410.x
Bucher, S.F., Auerswald, K., Tautenhahn, S., Geiger, A., Otto, J., Müller, A., & Römermann, C. (2016). Inter- and intraspecific variation in stomatal pore area index along elevational gradients and its relation to leaf functional traits. Plant Ecology, 217(3), 229–240. https://doi.org/10.1007/s11258-016-0564-2.
Case, A.L., & Barrett, S.C.H. (2001). Ecological differentiation of combined and separate sexes of Wurmbea dioica (colchicaceae) in sympatry. Ecology, 82(9), 2601–2616.
Chen, S.P., Bai, Y.F., Lin, G.H., Liang, Y., & Han, X.G. (2005). Effects of grazing on photosynthetic characteristics of major steppe species in the Xilin River Basin, Inner Mongolia, China. Photosynthetica, 43(4), 559–565.
Doheny-Adams, T., Hunt, L., Franks, P.J., Beerling, D.J., & Gray, J.E. (2012). Genetic manipulation of stomatal density influences stomatal size, plant growth and tolerance to restricted water supply across a growth carbon dioxide gradient. Philosophical Transactions of the Royal Society B. Biological Sciences 367(1588), 547–555. https://doi:10.1098/rstb.2011.0272.
Escobar-Sandoval, M., Paques, L., Fonti, P., Martinez-Meier, A., & Rozenberg, P. (2021). Phenotypic plasticity of European larch radial growth and wood density along a-1,000 m elevational gradient. Plant-Environment Interactions, 2, 45–60. https://doi.org/10.1002/pei3.10040.
Field, T.S., Brodribb, T.J., Iglesias, A., Chatelet, D.S., Baresch, A., Upchurch, G.R., Gomez, B., Mohr, B.A.R., Coiffard, C., Kvacek, J., & Jaramillo, C. (2011). Fossil evidence for Cretaceous escalation in angiosperm leaf vein evolution. Proceedings of the National Academy of Sciences of the United States of America, 108(20), 8363–8366. https://doi.org/10.1073/pnas.101445610.
Flexas, J., Scoffoni, C., Gago, J., & Sack, L. (2013). Leaf mesophyll conductance and leaf hydraulic conductance: an introduction to their measurement and coordination. Journal of Experimental Botany, 64(13), 3965–3981. https://doi.org/10.1093/jxb/ert319.
Fornoni, J. (2011). Ecological and evolutionary implications of plant tolerance to herbivory. Functional Ecology, 25(2), 399–407.
Fricker, M., & Willmer, C. (1996). Stomata. Berlin: Springer Science & Business Media. 375p. https://doi.org/10.1007/978-94-011-0579-8.
Gianoli, E., & Hannunen, S. (2000). Plasticity of leaf traits and insect herbivory in Solanum incanum L. (Solanaceae) in Nguruman. African Journal of Ecology, 38, 183–187.
Heidarlou, H.B., Shafiei, A.B., Erfanian, M., Tayyebi, A., Alijanpour, A. (2019). Effects of preservation policy on land use changes in Iranian Northern Zagros forests. Land use policy, 81, 76-90.
Jahanbazy Goujani, H., Hosseini Nasr, S.M., Sagheb-Talebi, K., & Hojjati, S.M. (2013). Effect of drought stress induced by altitude, on four wild almond species. Iranian Journal of Forest and Poplar Research21(2), 373-386. doi: 10.22092/ijfpr.2013.3864. (In Persian).
Jazirehi, M.H., & Ebrahimi Rostaghi, M. (2003). Silviculture in Zagors. University of Tehran Press, 508p. (In Persian).
Kamakura, M., Kosugi, Y., Takanashi, S., Matsumoto, K., Okumura, M., & Philip, E. (2011). Patchy stomatal behavior during midday depression of leaf CO2 exchange in tropical trees. Tree physiology, 31, 160–168. https://doi.org/10.1093/treephys/tpq102.
Kerchev, P., Fenton, B., Foyer, C., & Hancock, R. (2012). Plant responses to insect herbivory: interactions between photosynthesis, reactive oxygen species and hormonal signaling pathways. Plant Cell and Environment, 35(2), 441–453. https://doi.org/10.1111/j.1365-3040.2011.02399.x
Klancnik, K., & Gaberscik, A. (2015). Leaf spectral signatures differ in plant species colonizing habitats along a hydrological gradient. Journal of Plant Ecology, 9, 442–450. https://doi.org/10.1093/jpe/rtv068.
Kozlowski, T.T. (1999). Soil compaction and growth of woody plants. Scandinavian Journal of Forest Research, 14(6), 596-619.
Leonard, H.E., Ciambrone, M., & Pittermann, J. (2024). Species-specific responses drive browsing impacts on physiological and functional traits in Quercus agrifolia and Umbellularia californica. PLoS ONE, 19 (7), e0287160. https://doi.org/10.1371/journal.pone.0287160.
Machado, R.A.R., Robert, C.A.M., Arce, C.C.M., Ferrieri, A.P., Xu, S., Jimenez-Aleman, G.H., an, T., Baldwin, I.T., & Erb, M. (2016). Auxin Is Rapidly Induced by Herbivore Attack and Regulates a Subset of Systemic, Jasmonate-Dependent Defenses. Plant Physiology, 172(1), 521–32. https://doi.org/10.1104/pp.16.00940.
Mbagwu, F.N., & Edeoga, H.O. (2006). Leaf Anatomy of Some Nigerian Species of Vigna Savi (Leguminosae Papilionoideae). Agricultural Journal, 1, 5-7.
Mirdavoodi, H.R. (2014). Effect of grazing and environmental factors on the structure of Brant`s oak stands of Zagros (Case study: Dalab Park, Ilam). Iranian Journal of Forest and Poplar Research22(3), 461-472. https://doi: 10.22092/ijfpr.2014.12428. (In Persian).
Mohammadpour, M., Tatian, M.R., Tamartash, R., & Hosseinzadeh, J. (2018). Investigating the effects of grazing intensity on the structure and diversity of woody species in the Ilam Strait Dalab forest. Iranian Journal of Forest and Poplar Research, 26(3), 306-318. https://doi: 10.22092/ijfpr.2018.117735. (In Persian).
Mousa, Z., Soheili, F., oladi, R., & Naji, H.R. (2025). Anatomy of branch wood of Amygdalus orientalis Mill.: responses to livestock damage in the Zagros semi-arid forest (Ilam). Iranian Journal of Forest, 17(3), 395-408. https://doi: 10.22034/ijf.2025.506013.2044. (In Persian)
Mozaffarian, V.A. (2008). Flora of Ilam, Tehran: Farhang Moaser Publication.
Naji, H.R., & Taher Pour, M. (2019). The effect of simulated dust storm on wood development and leaf stomata in Quercus brantii L. Desert, 24(1), 43-49. https://doi.org/10.22059/JDESERT.2019.72435.
Naji, H.R., Janbakhshi, M., Heydari, M., Shirkhani, M.N., Azizi, K., & Woodward, S. (2022). Plasticity of Leaf Morphological Traits Impacted by Livestock Grazing on Trees in Zagros Semi-Arid Forest. Environmental Sciences Proceedings22(1), 60. https://doi.org/10.3390/IECF2022-13092
Nardini, A., Pedà, G., & Rocca, N.L. (2012). Trade-offs between leaf hydraulic capacity and drought vulnerability: morpho-anatomical bases, carbon costs and ecological consequences. New Phytologist, 196, 788–798. https://doi.org/10.1111/j.1469-8137.2012.04294.x
Niu, K., Messier, J., He, J.S., & Lechowicz, M.J. (2015). The effects of grazing on foliar trait diversity and niche differentiation in Tibetan alpine meadows. Ecosphere, 6(9), 150. https://doi.org/10.1890/ES14-00547.1
Ocheltree, T.W., Nippert, J.B., & Prasad, P.V.V. (2012). Changes in stomatal conductance along grass blades reflect changes in leaf structure. Plant, Cell & Environment,
35, 1040–1049. https://doi.org/10.1111/j.1365-3040.2011.02470.x
Ouyang, W., Struik, P.C., Yin, X., & Yang, J. (2017). Stomatal conductance, mesophyll conductance, and transpiration efficiency in relation to leaf anatomy in rice and wheat genotypes under drought. Journal of Experimental Botany, 68, 5191–5205. https://doi.org/10.1093/jxb/erx314
Panda, N., & Khush, G.S. (1995). Host Plant Resistance to Insects. CAB International, Wallingford, UK. 431p.
Peng, Y., Jiang, G.M., Liu, X.H., Niu, S.L., Liu, M.Z., & Biswas, D.K. (2007). Photosynthesis, transpiration and water use efficiency of four plant species with grazing intensities in Hunshandak Sandland, China. Journal of Arid Environments, 70(2), 304–315.
Pittermann, J., Lance, J., Poster, L., Baer, A., & Fox, L.R. (2014). Heavy browsing affects the hydraulic capacity of Ceanothus rigidus (Rhamnaceae). Oecologia, 175(3), 801–10. https://doi.org/10.1007/s00442-014-2947-1.
Polley, W., H., Frank, A.B., Sanabria, J., & Phillips, R.L. (2008). Inter-annual variability in carbon dioxide fluxes and flux–climate relationships on grazed and ungrazed northern mixed-grass prairie. Global Change Biology, 14, 1620–1632.
Ren, W., Hu, N., Hou, X., Zhang, J., Guo, H., Liu, Z., Kong, L., Wu, Z., Wang, H., & Li, X. (2017). Long-term overgrazing-induced memory decreases photosynthesis of clonal offspring in a perennial grassland plant. Frontiers in Plant Science, 8, 1331. https://doi: 10.3389/fpls.2017.00419.
Sagheb Talebi, Kh., Sajedi, T., & Pourhashemi, M. (2014). Forests of Iran: A treasure from the past, a hope for the future. Springer, Netherlands, 152p. https://doi.org/10.1007/978-94-007-7371-4
Shen, H.H., Wang, S.P., & Tang, Y.H. (2013). Grazing alters warming effects on leaf photosynthesis and respiration in Gentiana straminea, an alpine forb species. Journal of Plant Ecology, 6, 418–427. https://doi.org/10.1093/jpe/rtt010.
Soheili, F., Panahi, P., Hatamnia, A.A., Woodward, S., Abdul-Hamid, H., & Naji, H.R. (2023a). Leaf Microstructure and Adaptation Relationships in Ten Woody Species from the Semi-Arid Forests. Iranian Journal of Forest15, 53-72. https://doi: 10.22034/ijf.2022.330879.1853. (In Persian).
Soheili, F., Heydari, M., Woodward, S., & Naji, H.R. (2023b). Adaptive mechanism in Quercus brantii Lindl. leaves under climatic differentiation: morphological and anatomical traits. Scientific Reports, 13, 3580. https://doi.org/10.1038/s41598-023-30762-1.
Soheili, F., Heydari, M., Woodward, S., Abdul-Hamid, H., & Naji, H.R., (2023c). Adaptive plasticity of morphological and anatomical traits of Brant’s oak (Quercus brantii Lindl.) leaves under different climates and elevation gradients. Forest Science and Technology. https://doi.org/10.1080/21580103.2023.2182369.
Tabassum, M.A., Ye, Y., Yu, T., Zhu, G., Rizwan, M.S., Wahid, M.A., Peng, Sh., & Li, Y. (2016). Rice (Oryza sativa L.) hydraulic conductivity links to leaf venation architecture under well-watered condition rather than PEG-induced water deficit. Acta Physiologiae Plantarum, 38, 92. https://doi.org/10.1007/s11738-016-2109-7.
Rausher, M.D. (1979). Larval habitat suitability and oviposition preference in three related butterflies. Ecology, 60, 503– 511.
Staver, A.C., Bond, W.J., Cramer, M.D., & Wakeling, J.L. (2012). Top-down determinants of niche structure and adaptation among African Acacias. Ecology Letters, 15 (7), 673–9. https://doi.org/10.1111/j.1461-0248.2012.01784.x.
Staver, A.C., & Bond, W.J. (2014). Is there a ‘browse trap’? Dynamics of herbivore impacts on trees and grasses in an African savanna. Journal of Ecology, 102 (3), 595–602. https://doi.org/10.1111/1365-2745.12230
Valipour, A., Plieninger, T., Shakeri, Z., Ghazanfari, H., Namiranian, M., & Lexer, M. J. (2014). Traditional silvopastoral management and its effects on forest stand structure in northern Zagros, Iran. Forest Ecology and Management, 327, 221-230.
Vitasse, Y., Hoch, G., Randin, C.F., Lenz, A., Kollas, C., Scheepens J.F., & Keorner, C. (2013). Elevational adaptation and plasticity in seedling phenology of temperate deciduous tree species. Oecologia, 171(3), 663–678. https://doi.org/10.1007/s00442-012-2580-9
Wadgymar, S.M., & Austen, E.J. (2019). Shifting perspectives on the impacts of phenotypic plasticity. New Phytologist, 224(3), 1009–1011. https://doi.org/10.1111/nph.16210.
Wang, X., Chen, S., Yang, X., Zhu, R., Liu, M., Wang, R., & He, N. (2024). Adaptation mechanisms of leaf vein traits to drought in grassland plants. Science of Total Environment, 20(917), 170224. doi: 10.1016/j.scitotenv.2024.170224.
Xiong, D., Yu, T., Zhang, T., Li, Y., Peng, S., & Huang, J.L. (2015). Leaf hydraulic conductance is coordinated with leaf morpho-anatomical traits and nitrogen status in the genus Oryza. Journal of Experimental Botany, 66, 741–748. https://doi.org/10.1093/jxb/eru434.
Xiong, D., & Nadal, M. (2020). Linking water relations and hydraulics with photosynthesis. The Plant Journal, 101, 800–815. https://doi.org/10.1111/tpj.14595.
Yang, L., Han, M., Zhou, G., & Li, J. (2007). The changes of water-use efficiency and stoma density of Leymus chinensis along Northeast Chin transect, Shengtai Xuebao. Acta Ecologica Sinica, 27(1), 16–24.
Yin, J., Li, X., Guo, H., Zhang, J., Kong, L., & Ren, W. (2020). Legacy effects of historical grazing alter leaf stomatal characteristics in progeny plants. PeerJ, 8, e9266. https://doi.org/10.7717/peerj.9266
Zhang, Y., & Turner, J.G. (2008). Wound-Induced Endogenous Jasmonates Stunt Plant Growth by Inhibiting Mitosis. Plos one, 3(11), 1–9. https://doi.org/10.1371/journal.pone.0003699.
Zuo, X., Zhang, J., Lv, P., Wang, S., Yang, Y., Yue, X., Zhou, X., Li, Y., Chen, M., Lian, J., Qu, H., Liu, L., & Ma, X. (2018). Effects of plant functional diversity induced by grazing and soil properties on above- and below ground biomass in a semiarid grassland. Ecological Indicators, 93, 555–561. https://doi.org/10.1016/j.ecolind.2018.05.032.
Volume 18, Issue 1 - Serial Number 1
Summer 2026
Pages 111-128

  • Receive Date 21 September 2025
  • Revise Date 03 October 2025
  • Accept Date 16 November 2025