Seasonal and environmental variability in leaf anatomical traits of Pistacia lentiscus among different sites in Northwestern Algeria

A. Aribi; S. Mahroug

doi:10.15421/012525

A. Aribi Djilali Liabes University
S. Mahroug Djilali Liabes University

Keywords: adaptation, leaf anatomy, seasonal and spatial variation, soil, Mediterranean climate, Algeria.

Abstract

Leaf anatomical traits such as cuticle, epidermis, palisade parenchyma, and total leaf thickness play a critical role in plant adaptation to changing environmental conditions. Mediterranean plants, including sclerophyllous species, have evolved these traits to thrive under these fluctuating conditions. The present study investigates the anatomical variations in Pistacia lentiscus L. leaves in response to environmental factors in Northwestern Algeria. Through a comparative analysis across multiple sites and seasons, we evaluated the influence of climatic and edaphic conditions on leaf structural thickness, particularly the cuticle, ep i dermis, and palisade parenchyma. The results indicate that spatial variability is mainly reflected in changes in cuticle and palisade parenchyma thickness, while seasonal variability primarily affects the epidermis and foliar parenchyma. The highest values were recorded in Bouhriz Forest, the most arid site, during winter, while the h ighest values in summer were ob served in Tessala Mou n tains, the site with the highest altitude. However, the values in Beni Saf Forest were moderate, followed by the lowest values in M'Sila Forest. These anatomical adjustments highlight the adaptive capacity of P. lentiscus to the environmental constraints of the Mediterranean climate. This study underscores the importance of abiotic factors in shaping leaf traits and contributes to a better understanding of the adaptive mechanisms of sclerophyllous species in response to climatic and edaphic variations.

References

Ait Said, S., Fernandez, C., Greff, S., Derridj, A., Gauquelin, T., & Mevy, J. P. (2011). Inter population variability of leaf morpho-anatomical and terpenoid patterns of Pistacia atlantica Desf, ssp. atlantica growing along an aridity gradient in Algeria. Flora. Morphology. Distribution. Functional Ecology of Plants, 206, 397–405.

Alyafi, J., (1979). Approche systématique et écologie du genre Pistacia L. dans la région Méditerranéenne [Systematic approach and ecology of the genus Pistacia L. in the Mediterranean region]. Université d'Aix, Marseille (in French).

Bacelar, E. A., Correia, C. M., Moutinho-Pereira, J. M., Gonçalves, B. C., Lopes, J. I., & Torres-Pereira, J. M. (2004). Sclerophylly and leaf anatomical traits of five field-grown olive cultivars growing under drought conditions. Tree Physiology, 24(2), 233–239.

Boudy, P. (1950). Economie forestier Nord-Africaine: Monographie et traitement des essences forestier [North African forest economy: Monograph and treatment of forest species] (in French).

Correia, O., & Diaz Barradas, M. C. (1998). Photosynthetic characteristics of leaves of a dioecious species (Pistacia lentiscus L.) under summer stress conditions. In: Garab, G. (Ed.). Photosynthesis: Mechanisms and Effects. Springer, Dordrecht. Pp. 4039–4042.

De Martonne (1926). Une Nouvelle fonction climatologie: L’indice d’aridité [A new climatology function: The aridity index]. La météo. Pp. 449–459 (in French).

De Mico, V., & Aronne, G. (2012). Anatomy and lignin characterization of twigs in the chaparral shrub Rhamnus californica. IAWA Journal, 33(2), 151–162.

Doghbage, A., Belhadj, S., Belhouadjeb, F.A., Boukerker, H., Mevy, J.P., Gauquelin, T., Tonetto, A., Merdas, S., Touati, B., & Saimi, F. (2023). Leaf morphological and epidermal traits variability along environmental gradients in ten natural populations of Pistacia lentiscus. Life, 13, 1617.

Doghbage, A., Belhadj, S., Derridj, A., Mevy, J. P., Gauquelin, T., Merdas, S., Tonetto, A., & Foulla Hassen, F. (2020). Comparative eco-botanical analysis of Pistacia lentiscus L. in Algeria through morphological and ultrastructural markers related to leaves and stomata. Revue Agrobiologia, 10(1), 1826–1836.

Drouineau, G. (1942). Dosage rapide du calcaire actif du sol: Nouvelles données sur la séparation et la nature des fractions calcaires [Rapid determination of active limestone in soil: New data on the separation and nature of limestone fractions]. Annales Agronomiques, 12, 441–450 (in French).

Emberger, L. (1952). Sur le Quotient pluviothermique [On the rainfall quotient]. C.R. Académie Science: Paris, 234, 2508–2510 (in French).

Filella, I., & Peñuelas, J. (1999). Altitudinal differences in UV absorbance, UV reflectance and related morphological traits of Quercus ilex and Rhododedron ferrugineum in the Mediterranean region. Plant Ecology, 145, 157–162.

Fletcher, L. R., Cui, H., Callahan, H., Scoffoni, C., John, G. P., Bartlett, M. K., Burge, D. O., & Sack, L. (2018). Evolution of leaf structure and drought tolerance in species of Californian Ceanothus. American Journal of Botany, 105, 1672–1687.

Fletcher, L. R., Cui, H., Callahan, H., Scoffoni, C., John, G. P., Bartlett, M. K., Burge, D. O., & Sack, L. (2018). Evolution of leaf structure and drought tolerance in species of Californian ceanothus. American Journal of Botany, 105, 1672–1687.

Floret, C., & Pontanier, R. (1982). L’aridité en Tunisie présaharienne: Climat, sol, végétation et aménagement [Aridity in pre-Saharan Tunisia: Climate, soil, vegetation and management]. Travaux et documents de L’Orstom, 150 (in French).

Fritz, C. O., Morris, P. E. & Richler, J. J. (2012). Effect size estimates: Current use, calculations, and interpretation. Journal of Experimental Psychology: General, 141(1), 2–18.

Galmés, J., Flexas, J., Savé, R., & Medrano, H. (2007). Water relations and stomatal characteristics of Mediterranean plants with different growth forms and leaf habits: Responses to water stress and recovery. Plant and Soil, 290, 139–155.

Gaouar, A. (1980). Hypothèses et réflexions sur la dégradation des écosystèmes forestiers dans la région de Tlemcen (Algérie) [Hypotheses and reflections on the degradation of forest ecosystems in the Tlemcen region (Algeria)]. Forêt Méditerranéenne, 2(2), 131–146 (in French).

Gee, G., & Or, D. (2002). Particle size analysis. In: Dane, J. H., & Topp, G. C. (Eds.). Methods of soil analysis. Part 4. Physical methods. SSSA Book Series Madison, Wisconsin. Pp. 255–293.

Giorgi, F., & Lionello, P. (2008). Climate change projections for the Mediterranean region. Global and Planetary Change, 63, 90–104.

Guerfel, M., Baccouri, O., Boujnah, D., Chaibi, W., & Zarrouk, M. (2009). Impacts of water stress on gas exchange, water relations, chlorophyll content and leaf structure in two main Tunisian olive (Olea europaea L.) cultivars. Scientia Horticulturae, 119, 257–263.

Haffani, S., Mezni, M., Nasri, M. B., & Chaibi, W. (2017). Comparative leaf water relations and anatomical responses of three vetch species (Vicia narbonensis L., V. sativa L., and V. villosa Roth.) to cope with water stress. Crop and Pasture Science, 68, 691–702.

Iozia, L. M., Crisafulli, V., & Varone, L. (2023). Climatic variations along an aridity gradient drive significant trait intraspecific variability in Mediterranean plant species. Journal of Arid Environments, 217, 105042.

Lambers, H., Chapin, F. S. III, & Pons, T. L. (2008). Plant physiological ecology. 2nd ed. Springer.

Limousin, J. M., Misson, L., Lavoir, L. M., Martin, N. K., & Rambal, S. (2010). Do photosynthetic limitations of evergreen Quercus ilex leaves change with long-term increased drought severity? Plant, Cell and Environment, 33, 863–875.

Liu, S., & Zheng, J. (2024). Adaptive strategies based on shrub leaf stem anatomy and their environmental interpretations in the Eastern Qaidam Basin. BMC Plant Biology, 24, 323.

Mahroug, S., Courdavault, V., Thiersault, M., St-Pierre, B., & Burlat, V. (2006). Epidermis is a pivotal site of at least four secondary metabolic pathways in Catharanthus roseus aerial organs. Planta, 223, 1191–1200.

Miranda, J. D., Armas, C., Padilla, F. M., & Pugnaire, F. I. (2011). Climatic change and rainfall patterns: Effects on semi-arid plant communities of the Iberian Southeast. Journal of Arid Environments, 75(12), 1302–1309.

Nelson, D. W., & Sommers, L. E. (1996). Total carbon, organic carbon, and organic matter. In: Sparks, D. L. (Eds.). Methods of soil analysis. Part 3. Chemical Methods. SSSA Book Series Madison, Wisconsin. Pp. 961–1010.

Nevo, E., Bolshakova, M. A., Martyn, G. I., Musatenko, L. I., Sytnik, K., Pavlíèek, T., & Beharav, A. (2000). Drought and light anatomical adaptative leaf strategies in three woody species caused by microclimatic selection at "Evolution Canyon", Israel. Israel Journal of Plant Sciences, 48(1), 33–46.

Niinemets, U. (2001). Global-scale climatic controls of leaf dry mass per area, density, and thickness in trees and shrubs. Ecology, 82(2), 453–469.

Sardans, J., & Peñuelas, J. (2013). Plant-soil interactions in Mediterranean forest and shrublands: Impacts of climatic change. Plant and Soil, 365, 1–33.

Sardans, J., Peñuelas, J., & Rodà, F. (2006). Plasticity of leaf morphological traits, leaf nutrient content, and water capture in the Mediterranean evergreen oak Quercus ilex subsp. ballota in response to fertilization and changes in competitive conditions. Écoscience, 13(2), 258–270.

Simões, R., Miranda, I., & Pereira, H. (2023). Variation in leaf cutin content and chemical composition along one annual cycle in the Mediterranean cork oak (Quercus suber L.). Forests, 14(2), 334.

Sperlich, D., Chang, C. T., Peñuelas, J., Gracia, C., & Sabaté, S. (2015). Seasonal variability of foliar photosynthetic and morphological traits and drought impacts in a Mediterranean mixed forest. Tree Physiology, 35(5), 501–520.

Tattini, M., Remorini, D., Pinelli, P., Agati, G., Saracini, E., Traversi, M. L., & Massai, R. (2006). Morpho-anatomical, physiological and biochemical adjustments in response to root zone salinity stress and high solar radiation in two Mediterranean evergreen shrubs, Myrtus communis, and Pistacia lentiscus. New Phytologist, 170(4), 779–794.

Tian, M., Yu, G., He, N., & Hou, J. (2016). Leaf morphological and anatomical traits from tropical to temperate coniferous forests: Mechanisms and influencing factors. Scientific Reports, 6(1), 19703.

Tiantian, C., Junjie, P., Minjie, Q., Xian, S., Jingjia, D., Feng, L., & Kaibing, Z. (2023). The effects of enhanced Ultraviolet-B radiation on leaf photosynthesis and submicroscopic structures in Mangifera indica L. cv. ‘Tainong N°1. Horticulturae, 9(1), 83.

Vally, L., Janet, F. B., & George, K. (2002). The ability of abaxial and adaxial epidermis of sun and shade leaves to attenuate UV-B radiation in relation to UV absorbing capacity of the whole leaf methanolic extracts. Physiologia Plantarum, 117(1), 33–43.

Weemstra, M., Roumet, C., Cruz-Maldonado, N., Anthelme, F., Stokes, A., & Freschet, G. T. (2022). Environmental variation drives the decoupling of leaf and root traits within species along an elevation gradient. Annals of Botany, 130(3), 419–430.

Wei, T., & Simko, V. (2024). R package 'corrplot': Visualization of a Correlation Matrix (Version 0.95).

West, A. G., Dawson, T. E., February, E. C., Midgley, G. F., Bond, W. J., & Aston, T. L. (2012). Diverse functional responses to drought in a Mediterranean-type shrublands in South Africa. New Phytologist, 195, 396–407.

Yaoqi, L., Dongting, Z., Nawal S., Xiaoting, X., Qinggang, W., Wen, J., & Zhiheng, W. (2020). Spatiotemporal variation in leaf size and shape in response to climate. Journal of Plant Ecology, 13(1), 87–96.

Yavas, I., Jamal, M. A., Ul Din, K., Ali, S., Hussain, S., & Farooq, M. (2024). Drought-induced changes in leaf morphology and anatomy: Overview, implications and perspectives. Polish Journal of Environmental Studies, 33(2), 1517–1530.

Zandalinas, S. I., Mittler, R., Balfagón, D., Arbona, V., & Gómez-Cadenas, A. (2018). Plant adaptations to the combination of drought and high temperatures. Physiol Plantarum, 162(1), 2–12.