ABSTRACT
The importance of understory vegetation cannot be denied as an integral component of forest ecosystems, but there is a dearth of studies to explore the effects of environmental variables and canopy species on its diversity and composition. Here we investigated the effects of environmental variables and overstory stand structure on the understory vegetation in old-growth Monotheca buxifolia dominated forests with considerable co-dominance of other broadleaved by using ecologically standardized data collection methods across Pakistan. Multivariate analyses were used to examine the vegetation composition and different species assemblages with multiple influencing variables. We found a total of 58 understory species belonging to 55 genera and 30 families mostly representing pluriregional (33.89 %) chorological affinities with therophytic (17 species) life-form dominance and microphyll (34.48 %) leaf-size spectrum. Likewise, significant differences were observed in species richness and diversity indices between different understory community types. Attributes such as elevation, aspect, soil properties, and tree canopy structure were most strongly correlated with the Redundancy Analysis (RDA-ordination), indicating that several factors exert the strongest influence and explained the spatial pattern of understory vegetation. The findings of this research can assist forestry resources managers, forest biologists and ecologists in restoration and conservation plans for understory vegetation in the region.
Keywords:
canopy species; redundancy analysis; floristic composition; edaphic variables; Community types
Introduction
The complex interaction among individuals of different species and several environmental components leads to spatial diversities in plant species communities (Márialigeti et al. 2016Márialigeti S, Tinya F, Bidló A, Ódor P. 2016. Environmental drivers of the composition and diversity of the herb layer in mixed temperate forests in Hungary. Plant Ecology 217: 549-563.; Ullah et al. 2021Ullah R, Khan N, Rahman A. 2021. Comparison of invaded and non-invaded sites: a case study of rough cocklebur (Xanthium strumarium L.) An alien invasive species. Applied Ecology and Environmental Research 19: 1533-1548.). Vegetation-environmental relations are scale-dependent (Qiu et al. 2013Qiu B, Zeng C, Chen C, Zhang C, Zhong M. 2013. Vegetation distribution pattern along altitudinal gradient in subtropical mountainous and hilly river basin, China. Journal of Geographical Sciences 23: 247-257. ; Huo et al. 2014Huo H, Feng Q, Su YH. 2014. The influences of canopy species and topographic variables on understory species diversity and composition in coniferous forests. The Scientific World Journal 2014. https://doi.org/10.1155/2014/252489
https://doi.org/10.1155/2014/252489...
) and largely influenced by certain environmental factors such as topographic variables (elevation, slope, aspect), soil features, and stand condition at a local scale (Cheng et al. 2021Cheng X, Ping T, Li Z, Wang T, Han H, Epstein HE. 2021. Effects of environmental factors on plant functional traits across different plant life forms in a temperate forest ecosystem. New Forests: 1-18.; Deák et al. 2021Deák B, Kovács B, Rádai Z, et al. 2021. Linking environmental heterogeneity and plant diversity: the ecological role of small natural features in homogeneous landscapes. Science of the Total Environment 763: 144199.), but at a regional scale, the role of climatic variables are more significant (Jarvis et al. 2013Jarvis S, Woodward S, Alexander IJ, Taylor AFS. 2013. Regional scale gradients of climate and nitrogen deposition drive variation in ectomycorrhizal fungal communities associated with native Scots pine. Global Change Biology 19: 1688-1696.). Microclimate and resource availability below the tree canopy can also be heavily affected by topography (Koorem & Moora 2010Koorem K, Moora M. 2010. Positive association between understory species richness and a dominant shrub species (Corylus avellana) in a boreonemoral spruce forest. Forest ecology and management 260: 1407-1413. ; Dölle et al. 2017Dölle M, Petritan AM, Biris IA, Petritan IC. 2017. Relations between tree canopy composition and understorey vegetation in a European beech-sessile oak old growth forest in Western Romania. Biologia 72: 1422-1430. ), which leads to the diversification of understory floral composition and diversity. Likewise, the topography has highly influenced the distribution of plant species (Khan et al. 2015Khan N, Ali F, Ali K, Shahid S. 2015. Composition, structure and regeneration dynamics of Olea ferruginea Royle forests from Hindukush range of Pakistan. Journal of Mountain Science 12: 647-658.), due to its linkages with other factors (e.g., light intensity, precipitation, and soil physio-chemical properties) which directly affect plant accessible resources like, soil moisture, and nutrients (Carboni et al. 2010Carboni M, Thuiller W, Izzi F, Acosta A. 2010. Disentangling the relative effects of environmental versus human factors on the abundance of native and alien plant species in Mediterranean sandy shores. Diversity and Distributions 16: 537-546. ; Yu & Sun 2013Yu M, Sun OJ. 2013. Effects of forest patch type and site on herb-layer vegetation in a temperate forest ecosystem. Forest ecology and management 300: 14-20. ). The effects of the aforementioned variables are of major importance for the species distribution and normal functions of its life cycle (Ullah et al. 2020Ullah S, Khan N, Ali F, Badshah L, Asghar A, Muhammad N. 2020. An ecological assessment of Justicia adhatoda L. in Malakand Division, Hindukush range of Pakistan. Bioscience Research 17: 1082-1094) apart from field management, natural and anthropogenic disturbances (Khan et al. 2013Khan SM, Page S, Ahmad H, Harper D. 2013. Identifying plant species and communities across environmental gradients in the Western Himalayas: Method development and conservation use. Ecological Informatics 14: 99-103.; Ullah et al. 2021Ullah R, Khan N, Rahman A. 2021. Comparison of invaded and non-invaded sites: a case study of rough cocklebur (Xanthium strumarium L.) An alien invasive species. Applied Ecology and Environmental Research 19: 1533-1548.).
Understory vegetation is highly important in sustaining forest ecosystems composition, structure, and function (Augusto et al. 2003Augusto L, Dupouey JL, Ranger J. 2003. Effects of tree species on understory vegetation and environmental conditions in temperate forests. Annals of Forest Science 60: 823-831.; Mölder et al. 2008Mölder A, Bernhardt-Römermann M, Schmidt W. 2008. Herb-layer diversity in deciduous forests: raised by tree richness or beaten by beech? Forest ecology and management 256: 272-281.), easing energy flow, nutrients cycle, and supporting the canopy development as a forest ecosystem driver (Nilsson & Wardle 2005Nilsson MC, Wardle DA. 2005. Understory vegetation as a forest ecosystem driver: evidence from the northern Swedish boreal forest. Frontiers in Ecology and the Environment 3: 421-428. ). Although the understory flora shares comparatively less to the total forest plant biomass (Gilliam 2007Gilliam FS. 2007. The ecological significance of the herbaceous layer in temperate forest ecosystems. BioScience 57: 845-858.), it explains a major part of the floral diversity (Roberts & Gilliam 2003Roberts MR, Gilliam FS. 2003. Response of the herbaceous layer to disturbance in eastern forests. The herbaceous layer in forests of eastern North America 21: 302-320.; Bartels & Chen 2010Bartels SF, Chen HY. 2010. Is understory plant species diversity driven by resource quantity or resource heterogeneity? Ecology 91: 1931-1938.). Moreover, understory vegetation with a varied range of species promotes forest structural complexity and also provides habitat and energy for other organisms, thereby increasing its diversification (Dauber et al. 2003Dauber J, Hirsch M, Simmering D, Waldhardt R, Otte A, Wolters V. 2003. Landscape structure as an indicator of biodiversity: matrix effects on species richness. Agriculture, Ecosystems & Environment 98: 321-329.). The understory flora is also predominantly significant to forest natural regeneration (Jouveau et al. 2020Jouveau S, Toïgo M, Giffard B, et al. 2020. Carabid activity‐density increases with forest vegetation diversity at different spatial scales. Insect Conservation and Diversity 13: 36-46.), as it has a visible effect on the germination process, survivability, and development of juveniles, due to resources limitation (Augusto et al. 2003Augusto L, Dupouey JL, Ranger J. 2003. Effects of tree species on understory vegetation and environmental conditions in temperate forests. Annals of Forest Science 60: 823-831.; Messier et al. 2008Messier C, Parent S, Bergeron Y. 2008. Effects of overstory and understory vegetation on the understory light environment in mixed boreal forests. Journal of Vegetation Science 9: 511-520.). In this sense, extra focus has been given recently to the forest's understory flora and factors affecting its structure, composition, and distribution which are vital for environmental maintenance and forest protection (Bartels & Chen 2010Bartels SF, Chen HY. 2010. Is understory plant species diversity driven by resource quantity or resource heterogeneity? Ecology 91: 1931-1938.; Yu & Sun 2013Yu M, Sun OJ. 2013. Effects of forest patch type and site on herb-layer vegetation in a temperate forest ecosystem. Forest ecology and management 300: 14-20. ).
The importance of canopy species for the understory plant diversity and composition was reported by several studies (Qian et al. 2003Qian H, Klinka K, Økland RH, Krestov P, Kayahara GJ. 2003. Understorey vegetation in boreal Picea mariana and Populus tremuloides stands in British Columbia. Journal of Vegetation Science 14: 173-184.; Dölle et al. 2017Dölle M, Petritan AM, Biris IA, Petritan IC. 2017. Relations between tree canopy composition and understorey vegetation in a European beech-sessile oak old growth forest in Western Romania. Biologia 72: 1422-1430. ) focusing on stand management (Huo et al. 2014Huo H, Feng Q, Su YH. 2014. The influences of canopy species and topographic variables on understory species diversity and composition in coniferous forests. The Scientific World Journal 2014. https://doi.org/10.1155/2014/252489
https://doi.org/10.1155/2014/252489...
), natural and anthropogenic intervention (Ababou et al. 2009Ababou A, Chouieb M, Khader M, Mederbal K, Saidi D, Bentayeb Z. 2009. Multivariate analysis of vegetation of the salted lower-Cheliff plain, Algeria. Boletín de la Sociedad Botánica de México 85: 59-69.), light resources (Ameztegui et al. 2012Ameztegui A, Coll L, Benavides R, Valladares F, Paquette A. 2012. Understory light predictions in mixed conifer mountain forests: Role of aspect-induced variation in crown geometry and openness. Forest Ecology and Management 276: 52-61. ; Lefrancois et al. 2008Lefrancois ML, Beaudet M, Messier C. 2008. Crown openness as influenced by tree and site characteristics for yellow birch, sugar maple, and eastern hemlock. Canadian Journal of Forest Research 38: 488-497.), litter properties (North et al. 2005North M, Oakley B, Fiegener R, Gray A, Barbour M. 2005. Influence of light and soil moisture on Sierran mixed-conifer understory communities. Plant Ecology 177: 13-24.; Ellsworth et al. 2004Ellsworth JW, Harrington RA, Fownes JH. 2004. Seedling emergence, growth, and allocation of Oriental bittersweet: effects of seed input, seed bank, and forest floor litter. Forest ecology and management 190: 255-264.), soil nutrients and pH (Hart & Chen 2006Hart SA, Chen HY. 2006. Understory vegetation dynamics of North American boreal forests. Critical Reviews in Plant Sciences 25: 381-397. ; Chávez & Macdonald 2010Chávez V, Macdonald SE. 2010. The influence of canopy patch mosaics on understory plant community composition in boreal mixedwood forest. Forest ecology and management 259: 1067-1075. ). Understory flora in different forests has been explained by several workers (Tuanmu et al. 2010Tuanmu MN, Viña A, Bearer S, et al. 2010. Mapping understory vegetation using phenological characteristics derived from remotely sensed data. Remote Sensing of Environment 114: 1833-1844; Kendrick et al. 2015Kendrick JA, Ribbons RR, Classen AT, Ellison AM. 2015. Changes in canopy structure and ant assemblages affect soil ecosystem variables as a foundation species declines. Ecosphere 6: 1-20.; Dölle et al. 2017Dölle M, Petritan AM, Biris IA, Petritan IC. 2017. Relations between tree canopy composition and understorey vegetation in a European beech-sessile oak old growth forest in Western Romania. Biologia 72: 1422-1430. ) and is considered as a biodiversity hub with a variety of shrubs, herbs, and grasses (Barbier et al. 2008Barbier S, Gosselin F, Balandier P. 2008. Influence of tree species on understory vegetation diversity and mechanisms involved a critical review for temperate and boreal forests. Forest ecology and management 254: 1-15.). In pure broadleaved forests, the availability of resources is more similar in comparison to mixed stands, which are useful tools for diversity in the understory vegetation (Xie et al. 2021Xie H, Tang Y, Yu M, Wang GG. 2021. The effects of afforestation tree species mixing on soil organic carbon stock, nutrients accumulation, and understory vegetation diversity on reclaimed coastal lands in Eastern China. Global Ecology and Conservation 26: e01478.), and are more crucial for water maintenance and soil conservation (Haughian et al. 2017Haughian SR, Frego KA . 2017. Does CWD mediate microclimate for epixylic vegetation in boreal forest understories? A test of the moisture-capacitor hypothesis. Forest ecology and management 389: 341-351.).
Life-form characterizes several adaptive features of a species, and thus it is an appearance of the agreement to the environmental condition of a plant (Parveen et al. 2008Perveen A, Sarwar GR, Hussain I. 2008. Plant biodiversity and phytosociological attributes of Dureji (Khirthar Range). Pakistan Journal of Botany 40: 17-24). Plant life-forms are affected both by genetic and environmental variables since the environment can influence the production of several essential forms of plants. In a specific area, the leading life-form of flora highlights the way that plants have adapted to that region (Mavhura & Mushure 2019Mavhura E, Mushure S. 2019. Forest and wildlife resource-conservation efforts based on indigenous knowledge: The case of Nharira community in Chikomba district, Zimbabwe. Forest Policy and Economics 105: 83-90.). The adaptation of a plant to certain ecological conditions determines a life-form; therefore, it is an important physiognomic characteristic that has been widely used in the analysis of vegetation (Al-Sherif et al. 2013Al-Sherif EA, Ayesh AM, Rawi SM. 2013. Floristic composition, life form and chorology of plant life at Khulais region, Western Saudi Arabia. Pakistan Journal of Botany 45: 29-38.). Life-form is the indicator of micro and macroclimate and it is characterized by plant adaptation to certain ecological conditions (Qureshi & Bhatti 2010Qureshi R, Bhatti GR. 2010. Floristic inventory of Pai forest, Nawab Shah, Sindh, Pakistan. Pakistan Journal of Botany 42: 2215-2224.). Until now, several procedures have been adopted to classify plant life-forms, in which Raunkiaerʼs system is more acceptable (Azizi & Keshavarzi 2015Azizi H, Keshavarzi M. 2015. The study of flora life form and chorotypes of the Bazjar Qalarashe, Sardasht, West Azarbaijan province, NW Iran. Journal of Applied Science Reports 10: 31-37.).
The diverse climate and rough terrain of Pakistan support the vegetation with almost 6000 documented vascular plant species (Gulzar et al. 2019Gulzar H, Hazrat A, Gulzar K, et al. 2019. Medicinal plants and their traditional uses in Thana Village, District Malakand, Khyber Pakhtunkhwa, Pakistan. International Journal of Endorsing Health Science Research 7: 11-21). The country's northern regions are considered biodiversity hubs with 42 % of the recorded flora, representing the multiplicity of the sub-region in the Sino-Japanese phytogeographical region of the world (Sher et al. 2014Sher Z, Hussain F, Badshah L. 2014. Biodiversity and ecological characterization of the flora of Gadoon rangeland, district Swabi, Khyber Pukhtunkhwa, Pakistan. Iranian Journal of Botany 20: 96-108. ; Rahman 2016Rahman AU, Khan SM, Khan S, et al. 2016. Ecological assessment of plant communities and associated edaphic and topographic variables in the Peochar Valley of the Hindu Kush Mountains. Mountain research and Development 36: 332-341. ). Climatic variability is the possible reason for such richness and diversity and is predominantly linked to the altitudinal gradients of the area (Ullah et al. 2021Ullah R, Khan N, Rahman A. 2021. Comparison of invaded and non-invaded sites: a case study of rough cocklebur (Xanthium strumarium L.) An alien invasive species. Applied Ecology and Environmental Research 19: 1533-1548.). In Pakistan, major species of the broad-leaved forests are Olea ferruginea, Quercus baloot, Acacia modesta, Monotheca buxifolia, and Punica granatum (Khan et al. 2015Khan N, Ali F, Ali K, Shahid S. 2015. Composition, structure and regeneration dynamics of Olea ferruginea Royle forests from Hindukush range of Pakistan. Journal of Mountain Science 12: 647-658.). Among them, M. buxifolia is a wild, fruit yielding broadleaved tree species providing many services to the rural and urban inhabitants. So far, studies on different aspects of this commercially and ecologically important tree species have been conducted (Khan et al. 2011Khan N, Ahmed M, Shaukat SS, Wahab M, Siddiqui MF. 2011. Structure, diversity, and regeneration potential of Monotheca buxifolia (Falc.) A. DC. dominated forests of Lower Dir District, Pakistan. Frontiers of Agriculture in China 5: 106-121.; Ali et al. 2022Ali F, Khan N, Abd_Allah EF, Ahmad A. 2022a. Species Diversity, Growing Stock Variables and Carbon Mitigation Potential in the Phytocoenosis of Monotheca buxifolia Forests along Altitudinal Gradient across Pakistan. Applied Sciences 12(3): 1292.a), but no work has been carried out yet to investigate the understory diversity, composition, underlying structure, and its influential factors. Furthermore, the tree's canopy effects in these forests are still ignored. Therefore, this study investigated the understory vegetation with environmental variables and structural attributes in 44 stands across Pakistan. We hypothesized that understory species composition and diversity would differ significantly because of varied topographic, edaphic, and overstory composition and structure. Additionally, we aimed to explore which environmental variables and forest stand factors could explain the variation in understory species composition in M. buxifolia dominated forests in the region.
Materials and Methods
Study Area
The effect of different variables including edaphic, topographic, and canopy of woody trees on the understory vegetation of M. buxifolia dominated forests were studied at different localities across Pakistan, during the period from 2018 to 2019 (Fig. 1). Pakistan is a south Asian country spreads over 80,943 km2, spinning between 60° 55′ to 75° 30′ longitude and 23° 45′ to 36° 50′ latitude (Ali et al. 2022Ali F, Khan N, Abd_Allah EF, Ahmad A. 2022a. Species Diversity, Growing Stock Variables and Carbon Mitigation Potential in the Phytocoenosis of Monotheca buxifolia Forests along Altitudinal Gradient across Pakistan. Applied Sciences 12(3): 1292.a). Uneven topography, undulant valleys, diverse slopes, hillocks, huge mountains, plains, and many water streams joining main rivers are the basic structures of the studied area. Pakistan has a diverse climate and biodiversity due to the elevation gradient ranging from the sea level to 8,611 m with more than 6000 identified plant species (Ali & Qaiser 1986Ali SI, Qaiser M. 1986. A phytogeographical analysis of the phanerogams of Pakistan and Kashmir. Proceedings of the Royal Society of Edinburgh, Section B: Biological Sciences 89: 89-101.). The hotspot flora of the studied area is distributed in thirteen natural regions i.e., Alpine pastures to Mangroves, where the endangered flora is >10 % (Shinwari 2011Shinwari ZK, Qaiser M. 2011. Efforts on conservation and sustainable use of medicinal plants of Pakistan. Pakistan Journal of Botany 43: 5-10.). M. buxifolia forests are generally distributed at diverse elevation ranges and are often found toward the north and west of the country (Ali et al. 2022Ali F, Khan N, Ali K, Khan MEH, Jones DA. 2022b. Vegetation Pattern and Regeneration Dynamics of the Progressively Declining Monotheca buxifolia Forests in Pakistan: Implications for Conservation. Sustainability 14(10): 6111.b).
Map display 44 sampling locations of M. buxifolia dominated forests in different elevation ranges across Pakistan.
Data Collection
Data on the topographic and edaphic variables, canopy species, and understory vegetation were collected from least disturbed Monotheca forests (area ≥ 1 hectare) across Pakistan (Ali et al. 2017Ali F, Khan N, Ali K, Khan I. 2017. Influence of environmental variables on the distribution of woody species in Muslim graveyards of Malakand Division, Hindukush Range Mountains of Pakistan. Pakistan Journal of Botany 49: 2357-66. ). We established 10 plots each of 15 m × 15 m = 125 m2 in 44 forests for vegetation survey at elevation ranges from 647.09 m to 1789.48 m (asl) across the natural distribution range of Monotheca in Pakistan. In every sampling plot, the individual tree with a girth of more than 5.0 DBH cm (1.3 m above ground level) was measured, and height was obtained (Ali et al. 2019Ali F, Khan N, Ahmad A, Khan AA. 2019. Structure and biomass carbon of Olea ferruginea forests in the foothills of Malakand division, Hindukush Range Mountains of Pakistan. Acta Ecologica Sinica 39: 261-266.). Density (ha-1) and total tree basal area (m2 ha-1) for the tree species were calculated in each site. For understory vegetation (shrubs, herbs, and grasses) measurement, 15 m × 15 m plot was then randomly divided into two 5 m × 5 m = 25 m2 quadrats (Wulf & Naaf 2009Wulf M, Naaf T. 2009. Herb layer response to broadleaf tree species with different leaf litter quality and canopy structure in temperate forests. Journal of Vegetation Science 20: 517-526.). Within a plot, ecological parameters such as density, cover and height for individual plant species were recorded (Russel & Flower 1999Russell FL, Fowler NL. 1999. Rarity of oak saplings in savannas and woodlands of the eastern Edwards Plateau, Texas. The Southwestern Naturalist 31-41.). Before the vegetation sampling, information like slope angle (Santo clinometers), aspect (compass), altitude (altimeter), geographical coordinator (GPS), and the presence of natural and man-made interference were documented. Three soil samples in replicates (10-30 cm depth) were arbitrarily collected from the individual plot with a stainless cylindrical steel soil sampler of 5 cm in diameter. The soil samples of each stand were then thoroughly mixed to form a composite sample for further analysis. Soil pH was measured in a 1:2.5 soil to water ratio suspension (Du et al. 2010Du Z, Ren T, Hu C. 2010. Tillage and residue removal effects on soil carbon and nitrogen storage in the North China Plain. Soil Science Society of America Journal 74: 196-202.). The volumetric ring method was used to determine the soil bulk density (Zhu et al. 2009Zhu B, Wang T, Kuang F, Luo Z, Tang J, Xu T. 2009. Measurements of nitrate leaching from a hillslope cropland in the Central Sichuan Basin, China. Soil Science Society of America Journal 73: 1419-1426.).
Laboratory Analysis
Botanical samples were collected from all individual trees, shrubs, and herbs in each plot and identified at the Botanical Garden & Herbarium (BGH) University of Malakand. The flora was classified into different life-form, and leaf-size classes following Raunkiaer (1934Raunkiaer C. 1934. The life forms of plants and statistical geographical. England. Clarendon Press.). The phytosociological attributes (i.e., relative frequency, relative density, and relative basal area) and absolutes values (i.e., stem density ha-1 and basal area m2 ha-1) of all woody species were obtained for individual stands. From the relative values of phytosociological attributes, we calculated an Importance Value Index (IVI) for each tree species following Khan et al. (2015Khan N, Ali F, Ali K, Shahid S. 2015. Composition, structure and regeneration dynamics of Olea ferruginea Royle forests from Hindukush range of Pakistan. Journal of Mountain Science 12: 647-658.). Similarly, the IVI for herbs and shrubs was also calculated using the formula described by Huo et al. (2015Huo H, Feng Q, Su YH. 2015. Shrub communities and environmental variables responsible for species distribution patterns in an alpine zone of the Qilian Mountains, northwest China. Journal of Mountain Science 12: 166-176. ). We evaluated the data for plant taxonomic composition, Simpson's Index (1/C) and Shannon-Wiener Index (H) to calculate species richness and alpha diversity for each understory community across the four distinct forest vegetation types. One-way ANOVA following Tukey's HSD test was performed to report the differences in species richness and diversity of the understory vegetation between the forest types. Soil physicochemical properties were measured in the laboratory by using a flame photometer, Kjeldahl apparatus, and Atomic absorption (Liu et al. 2009Liu G, Li L, Wu L, Wang G, Zhou Z, Du S. 2009. Determination of soil loss tolerance of an entisol in Southwest China. Soil Science Society of America Journal 73: 412-417.).
The relationships between environmental factors, measured overstory structural components, and understory species were then characterized with redundancy analysis (RDA) (ter Braak 2012ter Braak CJ, Smilauer P. 2012. Canoco reference manual and user's guide: software for ordination. Version 5.0.; Wu et al. 2021Wu HF, Gao T, Zhang W, Li G, Hao WF. 2021. Understory Vegetation Composition and Stand Are Mainly Limited by Soil Moisture in Black Locust Plantations of Loess Plateau. Forests 12: 195.). First, we performed a Detrended correspondence analysis (DCA) in order to select whether a unimodal (CCA) or linear (RDA) response curve in ordination analysis should be better. Consequently, DCA gradient length was 12.15 for axis 1, 3.41 for axis 2, and 11.33 for axis 3 with 11.63 % of the total variance in species data; therefore, both RDA and CCA were preferred to use for accurate results as suggested by Lepš & Smilauer (2003Lepš J, Šmilauer P. 2003. Multivariate analysis of ecological data using CANOCO. Cambridge, Cambridge University Press .), Jongman et al. (1995Jongman E, Jongman SRR. 1995. Data analysis in community and landscape ecology. Cambridge, Cambridge University Press.). Our analysis demonstrated that RDA explained 50 % of total variance which was higher than CCA (11.63 %). Thus, we used RDA in the final analysis as a linear interaction between species and environmental variables. Nevertheless, the presence of double zeros strongly affects the RDA with arch effect (Ababou et al. 2013Ababou A, Chouieb M, Bouthiba A, Saidi D, Bouzina MMH, Mederbal K. 2013. Spatial pattern analysis of Peganum harmala on the salted lower Chelif plain, Algeria. Turkish Journal of Botany 37: 111-121. ). In such a case, an alternative has applied either chord (Orloci 1967Orloci L. 1967. An agglomerative method for classification of plant communities. Journal of Ecology 55:193-206.) or Hellinger (Rao 1995Rao CR. 1995. A review of canonical coordinates and an alternative to correspondence analysis using Hellinger distance. Quaderns d'estadística i investigació operative 19: 1-3.) distance transformation. Tsai et al. (2016Tsai HP, Lin YH, Yang MD. 2016. Exploring long term spatial vegetation trends in Taiwan from AVHRR NDVI3g dataset using RDA and HCA analyses. Remote Sensing 8: 1-290.) showed that this approach is less sensitive to double zeros and consequently to the arch effect. After several comparisons, we chose the Hellinger transformation followed by an RDA and the most significant variables were determined by using the method Wilk’s lambda (De Sá 2007De Sá JPM. 2007. Applied statistics using SPSS, Statistica, MatLab and R. Heidelberg, Springer Science & Business Media. ; Jones et al. 2008Jones MM, Tuomisto H, Borcard D, Legendre P, Clark DB, Olivas PC. 2008. Explaining variation in tropical plant community composition: influence of environmental and spatial data quality. Oecologia 155: 593-604.). Finally, four pre-defined vegetation groups (Ali et al. 2022Ali F, Khan N, Ali K, Khan MEH, Jones DA. 2022b. Vegetation Pattern and Regeneration Dynamics of the Progressively Declining Monotheca buxifolia Forests in Pakistan: Implications for Conservation. Sustainability 14(10): 6111.b) obtained from Ward’s agglomerative clustering techniques were used because they inherit major ecological information and were easily interpretable.
Results
Floristic and chorological affinities
The study resulted in a total of 58 understory species belonging to 55 genera and 30 families (Tab. S2). Lamiaceae and Asteraceae were the major families that contributed with the greatest numbers of plant species i.e. 8 species and 7 species respectively, followed by Solanaceae (5 species), Poaceae, and Apocynaceae (4 species each). Microphyll dominated the leaf-size classes and was composed of 20 species (34.48 %), followed by nanophyll, mesophyll, leptophyll, and macrophyll respectively (Fig. 2). Of the total leaf-size classes, aphyllous (2 species, 3.89 %) had contributed the least. Likewise, the biological spectrum shows that Phanerophyte was the leading life-form (32.76 %), followed by Therophyte and Cryptophyte ones (Fig. 3). The chorological affinities of the recorded taxa revealed that 33.89 % species were pluri-regional, ranging their distribution all over the Indian and Mediterranean regions, 30.50 % were bioregional, 20.33 % cosmopolitan and only 15.25 % were monoregional (Fig. 4). Of the total species, 18.64 % were mostly native to the Iranian-Turaian region, 12.71 % were native to Euro-Siberian and 11.68 % were from the Mediterranean phytogeographical region.
Percent distribution of leaf-size spectrum of understory plant species (Monotheca buxifolia dominated forests) found in Pakistan.
Percent distribution of the understory plant species life-forms in Monotheca buxifolia dominated forests in Pakistan.
Chorology of understory plant species (%) in Monotheca buxifolia dominated forests in Pakistan.
Vegetation types
The hierarchical agglomerative clusters of the 58 understory plant species in M. buxifolia dominated forests can be interpreted in the context of their habitat characteristic and species associations. The cluster analysis of woody tree species retained 65 % of the floristic data with four groups and 10 % chaining. Group-I comprised 12 stands and 793 individuals, representing the largest number (38 species) of shrubs and herbaceous species and ranked as the richest and diverse group (Tab. 1). This group was dominated by Dodonea viscosa (Fig. 5) and Justicia adhatoda whereas, Ziziphus nummularia (IVI= 8.19±4.2 %), Perovskia abrotanoides (IVI= 5.66±4.2 %), and Gymnosporia Royleana (IVI = 6.93±4.4) were major associates. The majority of the plants (33 species) in this group occurred with importance values less than 5 %. This group was different in terms of low elevation (1038.03±68.8 m), slope inclination (21.08±2.85°), high contents of silt, low organic matter, nitrogen, phosphorus, and potassium contents (Tab. 2). Structural attributes such as basal area (53.11±8.5 m2 ha-1) of M. buxifolia, total basal area of the stand (26.91±5.1 m2 ha-1), and percent Importance value (40.61±1.6 %) were also maximum in this group.
Species richness and diversity indices for the understory vegetation’s in Monotheca dominated communities resulted from Ward’s agglomerative clustering analysis.
Understory vegetation of Monotheca forests; (A, B) Clear understory vegetation, (C, D) Understory purely dominated by Dodonaea viscosa.
A cluster of six stands (Group-II), with eighteen different species, was reported as the most species-poor and least diverse group (Tab. 1). In this group, large shrubs like D. viscosa (IVI= 36.61±17 %), Withania coagulans (IVI= 16.67±16 %), and Nannorrhops ritchiana (IVI= 13.82±9 %) were dominant. Other common understory species were Lawsonia inermis (IVI= 7.42±5.06), Solanum virginianum (IVI= 6.57±4.15), and Carthamus oxyacantha (IVI= 6.57±4.15). The characteristic features of this group included high elevation (1328±126 m) with a comparatively steep slope (28.5±1.99°). Likewise, lime content (3.04±0.84 %) in the soil was higher; therefore, this group was characterized by high pH (7.9±0.22). Similarly, electrical conductivity (µs/cm) and total dissolved solutes (182.6±17.54) were also higher in this group (Tab. 2). However, the basal area (35.25±5.97 m2 ha-1) of the dominant overstory species was the lowest, and the total tree basal area (12.56±2.27 m2 ha-1) was about half of the prior group.
The understory vegetation in group-III was distributed in 12 stands where a total of 479 individuals of shrubs and 26 herbaceous plants were documented. Results of ANOVA exposed a significant difference in species richness of this group in comparison to group-I and II. Further, the difference was confirmed by performing post hoc Tukey’s HSD. D. viscosa (IVI= 24.6±5.9 %) and Saccharum munja (IVI= 10±3.6 %) were the dominant shrubs, whereas Justicia adhatoda (IVI 9.2±4 %) and Plectranthus rugosus (IVI= 7.5±5 %), were the strong companion in this group. Out of the total understories, 24 plants were below <5 % of importance values in this group. Similar to group-I, stands in this group were located at low elevation (1031±90 m), gentle slope (23.25±2.92°), and facing toward the west. The sampled sites in this group were also characterized by low soil pH, high organic matter, potassium, and percent sand contents. The basal area of the dominant species was 39.06±8.55 m2 ha-1 whereas the total tree's basal area was lower than that of group-I and II, respectively.
Alhagi maurorum (IVI= 13.35±7 %) and Calligonum polygonoides (10.97±5 %) dominated the understory vegetation of the group-IV community. Vitex negundo and D. viscosa were the major associates with the predominant species. As in group-III, a lower number of understories (25 species) were recorded in this group with an importance value of ≤ 5 %. Among all the groups, diversity indices, like Simpson's Index (1/C) (2.95±0.49) and Shannon-Wiener Index (H) (0.95±0.18) were recorded least for group-IV (Tab. 1). Stands of this community type were located comparatively at high elevation (1275.3±80 m), slope (26.78±2.65°), and facing north. Among the edaphic variables, silts contents were the least (29.63±2.43), while sand contents (55.87±2.52) dominate the soil texture of this group.
Effect of environmental variables
The RDA ordination shows the stands as diamonds in species space with overlays of the environmental variables and structural attributes as joint plot to reflect the direction and explanatory power of linear relationships with the axes (Fig. 6). We found significant relationships for all redundancy axes, showing that species composition is strongly dependent on environmental factors. Monte Carlo permutation test for RDA ordination indicated that the eigenvalues for axis 1, 2 and 3 were 3.306, 2.581 and 2.45 respectively. The ordination explained 35.1 % of the cumulative variance in the species data by the entire axis (Tab. 3). The first axis has explained 6.6 % of the total variance and positively correlated with potassium, Monotheca importance value and negatively correlated with the total basal area (r = -0.512), total IVI (r = -0.403), available water (r = -0.306), Lime (r = -0.344) and silt (r = -0.323) respectively (Tab. S3). The second axis indicated 5.2% of the variance and was significantly correlated with aspect (°) and total tree basal area. The third axis was found to be linked with most of the topographic variables such as elevation (r = 0.549) and slope (r = 0.469). Soil silt, sand, pH, organic matter, and nitrogen were among the edaphic and physicochemical properties affecting understory species composition (Fig. 5; Tab. S3). The values of interest correlation for topographic, edaphic, and overstory vegetation are shown in Table S4.
Ordination diagram (RDA-biplot) showing the relationship between 44 Monotheca forests (stand ordination) and environmental variables. Species and environmental variables used in the analysis are abbreviated, and full names are shown in Table S2 and Table 2 respectively.
RDA-analysis of species-environmental variables operating on the understory vegetation in Monotheca-dominated forests in Pakistan.
Discussion
The present study recorded 58 plant species belonging to 55 genera and 30 families. Floristic composition in the studied area is very much affected by local activities and natural regeneration is hindered due to heavy grazing and cutting (Fig. 5). Among all plants, phanerophyte with 32.76 % was dominant and therophyte with 29.31 % was in the next order. In fact, life-forms indicate the possibility of plant adaptations to climatic conditions. The high frequency of phanerophyte is due to cold and temperate climate while therophytic life-form reflects Mediterranean climate (Khan et al. 2017Khan A, Khan N, Ali K, Rahman IU. 2017. An assessment of the floristic diversity, life-forms and biological spectrum of vegetation in Swat Ranizai, District Malakand, Khyber Pakhtunkhwa, Pakistan. Science Technology and Development 36: 61-78.). Therefore, the recorded life-form spectrum among the documented understory flora shows the influence of the Mediterranean and cold temperate climate (Azizi & Keshavarzi 2015Azizi H, Keshavarzi M. 2015. The study of flora life form and chorotypes of the Bazjar Qalarashe, Sardasht, West Azarbaijan province, NW Iran. Journal of Applied Science Reports 10: 31-37.). The low percentage of hemicryptophytes and chamaephytes shows that they are not adapted to existence climate and edaphic situations. These findings are similar to the results of Floret et al. (1990Floret C, Galan MJ, 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.); Schneider et al. (2003Schneider JV, Zipp D, Gaviria J, Zizka G. 2003. Successional and mature stands in an upper Andean rain forest transect of Venezuela: do leaf characteristics of woody species differ? Journal of tropical ecology 251-259.); Sringeswara et al. (2010Sringeswara AN, Shivana MB, Gowda B. 2010. Role of ecological factors on leaf size spectra in an evergreen forest, Western Ghats, India an ecological hotspot. International Journal of Science Nature 1: 61-66. ); and Ullah et al. (2015Ullah A, Khan N, Muhammad Z. 2015. Diversity of life form and leaf size classes at Sheikh Buddin National Park, Dera Ismail Khan, Khyber Pakhtunkhwa Pakistan. South Asian Journal of Life Sciences 3: 6-13. ). The leaf-size spectrum shows that microphyllous (34.48 %) species were dominant followed by nanophylls (25.86 %) and mesophylls (15.52 %). Microphylls are symbolic of steppes, whereas nanophylls and leptophylls are representatives of hot deserts (Cain & Castro 1959Cain SA, Castro GDO. 1959. Manual of vegetation analysis. New York, Haper and Row.). Species with large leaves occur in warm moist climates, while smaller leaves represent cold and dry climates (Khan et al. 2018Khan W, Khan SM, Ahmad H, Alqarawi AA, Shah GM, Hussain M, Abd_Allah EF. 2018. Life forms, leaf size spectra, regeneration capacity and diversity of plant species grown in the Thandiani forests, district Abbottabad, Khyber Pakhtunkhwa, Pakistan. Saudi Journal of Biological Sciences 25: 94-100.). The present study reveals that microphylls and nanophylls were present at high elevations while leptophylls were present at the lower elevation, which is an agreement to findings of Al-Sherif et al. (2013Al-Sherif EA, Ayesh AM, Rawi SM. 2013. Floristic composition, life form and chorology of plant life at Khulais region, Western Saudi Arabia. Pakistan Journal of Botany 45: 29-38.). Azizi & Keshavarzi (2015)Azizi H, Keshavarzi M. 2015. The study of flora life form and chorotypes of the Bazjar Qalarashe, Sardasht, West Azarbaijan province, NW Iran. Journal of Applied Science Reports 10: 31-37. reported a high percentage of leptophylls and nanophylls in dry subtropical semi-evergreen forests. In our case, a high percentage of microphylls represents the cool climate where the roots absorb low moisture.
The chorological affinities of the recorded flora exposed that understory vegetation of Monotheca forests supported plant species with a wide distribution representing several phytogeographical regions of the world. The understory flora of the studied area is distributed in thirteen different regions which are similar to the findings of Ali et al. (2017Ali F, Khan N, Ali K, Khan I. 2017. Influence of environmental variables on the distribution of woody species in Muslim graveyards of Malakand Division, Hindukush Range Mountains of Pakistan. Pakistan Journal of Botany 49: 2357-66. ). Phyto-geographically, Pakistan is categorized into 4 major regions: (i) Indian region (6 %), (ii) Saharo-Indian region (9.5 %), (iii) Sino-Himalayan region (10 %), and (iv) Irano-Turanian region (45 % of species) but the maximum number of species in this study were from Irano-Turanian region (18.64 %) followed by Euro-Siberian (12.71 %), which comply the findings of Ali et al. (2017)Ali F, Khan N, Ali K, Khan I. 2017. Influence of environmental variables on the distribution of woody species in Muslim graveyards of Malakand Division, Hindukush Range Mountains of Pakistan. Pakistan Journal of Botany 49: 2357-66. .
We found that understory species richness and diversity in the Monotheca forests varied significantly with canopy dominants, which is in agreement with various studies (Wang et al. 2015Wang B, Zhang G, Duan J. 2015. Relationship between topography and the distribution of understory vegetation in a Pinus massoniana forest in Southern China. International Soil and Water Conservation Research 3: 291-304.; Kobal et al. 2015Kobal M, Bertoncelj I, Pirotti F, Dakskobler I, Kutnar L. 2015. Using lidar data to analyse sinkhole characteristics relevant for understory vegetation under forest cover - Case study of a high karst area in the Dinaric Mountains. PLOS ONE 10: e0122070.; Echiverri & Macdonald 2020Echiverri LF, Macdonald SE. 2020. A topographic moisture index explains understory vegetation response to retention harvesting. Forest ecology and management 474: 118358.). Monotheca dominated forests with a maximum basal area of canopy species have high diversity in understory vegetation. Such a positive impact of canopy species on understory vegetation richness was reported by Chávez & Macdonald (2010Chávez V, Macdonald SE. 2010. The influence of canopy patch mosaics on understory plant community composition in boreal mixedwood forest. Forest ecology and management 259: 1067-1075. ). However, several studies report no or weak correlation between the canopy richness and understory vegetation (Dang et al. 2018Dang P, Gao Y, Liu J, Yu S, Zhao Z. 2018. Effects of thinning intensity on understory vegetation and soil microbial communities of a mature Chinese pine plantation in the Loess Plateau. Science of the Total Environment 630: 171-180. ). The effect of canopy species on understory vegetation richness can be linked to multiple environmental variables (Økland 1999Økland RH. 1999. On the variation explained by ordination and constrained ordination axes. Journal of Vegetation Science 10: 131-136.). Different other factors, like the level of natural and human hazards, dispersal restrictions, and stochastic events were the most predominant having an adverse effects on vegetation distribution (Berger et al. 2004Berger AL, Puettmann KJ, Host GE. 2004. Harvesting impacts on soil and understory vegetation: the influence of season of harvest and within-site disturbance patterns on clear-cut aspen stands in Minnesota. Canadian Journal of Forest Research 34: 2159-2168. ; Nie et al. 2019Nie X, Guo W, Huang B, et al. 2019. Effects of soil properties, topography and landform on the understory biomass of a pine forest in a subtropical hilly region. Catena 176: 104-111.; Kutnar et al. 2019Kutnar L, Nagel TA, Kermavnar J. 2019. Effects of disturbance on understory vegetation across Slovenian forest ecosystems. Forests 10: 1048. ). Therefore, understanding the effect of these unexplained factors could be more helpful to describe the mechanisms of species distribution. Elevation coupled with canopy potentially affects the understory floral composition (Yu et al. 2013Yu M, Sun OJ. 2013. Effects of forest patch type and site on herb-layer vegetation in a temperate forest ecosystem. Forest ecology and management 300: 14-20. ; Rana et al. 2011Rana MS, Samant SS, Rawat YS. 2011. Plant communities and factors responsible for vegetation pattern in an alpine area of the northwestern Himalaya. Journal of Mountain Science 8: 817-826.). Soil bulk density and soil slope potentially affect the understory vegetation composition (Echiverri & Macdonald 2020Echiverri LF, Macdonald SE. 2020. A topographic moisture index explains understory vegetation response to retention harvesting. Forest ecology and management 474: 118358.; Piazza et al. 2016Piazza MV, Garibaldi LA, Kitzberger T, Chaneton EJ. 2016. Impact of introduced herbivores on understory vegetation along a regional moisture gradient in Patagonian beech forests. Forest ecology and management 366: 11-22.). In the northern areas of Pakistan, species richness was highly influenced by slope and altitude (Ali et al. 2022Ali F, Khan N, Ali K, Khan MEH, Jones DA. 2022b. Vegetation Pattern and Regeneration Dynamics of the Progressively Declining Monotheca buxifolia Forests in Pakistan: Implications for Conservation. Sustainability 14(10): 6111.b; Ullah et al. 2020Ullah S, Khan N, Ali F, Badshah L, Asghar A, Muhammad N. 2020. An ecological assessment of Justicia adhatoda L. in Malakand Division, Hindukush range of Pakistan. Bioscience Research 17: 1082-1094; Qureshi & Bhatti 2010Qureshi R, Bhatti GR. 2010. Floristic inventory of Pai forest, Nawab Shah, Sindh, Pakistan. Pakistan Journal of Botany 42: 2215-2224.).
Variability of environmental conditions plays an important role in spatial segregation of the flora and structural variations in plant communities (Aikens et al. 2007Aikens ML, Ellum D, McKenna JJ, Kelty MJ, Ashton MS. 2007. The effects of disturbance intensity on temporal and spatial patterns of herb colonization in a southern New England mixed-oak forest. Forest Ecology and Management 252: 144-158.; Huo et al. 2015Huo H, Feng Q, Su YH. 2015. Shrub communities and environmental variables responsible for species distribution patterns in an alpine zone of the Qilian Mountains, northwest China. Journal of Mountain Science 12: 166-176. ; Dölle et al. 2017Dölle M, Petritan AM, Biris IA, Petritan IC. 2017. Relations between tree canopy composition and understorey vegetation in a European beech-sessile oak old growth forest in Western Romania. Biologia 72: 1422-1430. ). In the current work, we identified 4 different groups of understory vegetation based on the importance values of canopy species. Each of these groups possesses different ecological niches in the studied area, representing a unique combination of plant species. Group-I and group-III were dominated by D. viscosa, S. munja, and J. adhatoda preferred the sites of low elevations and gentle slopes. However, group-II and group-IV preferred stands of high elevation having steep slopes. Contrary to group-I and IV, group-II and III appeared to favor slightly basic soil with high contents of soil organic matter. Among the edaphic variables, group-IV was characterized by the high amount of sand content, while stands of group-I favor silty soil. Group-II dominated by D. viscosa and Withania coagulans was predominantly limited to a high elevation with more clay particles that have an adequate rate of precipitation in the studied area, indicating a mesophyte community. Several studies of vegetation classification were carried out in other high mountain ranges. For example, Huo et al. (2015)Huo H, Feng Q, Su YH. 2015. Shrub communities and environmental variables responsible for species distribution patterns in an alpine zone of the Qilian Mountains, northwest China. Journal of Mountain Science 12: 166-176. ; Siddiqui et al. (2016Siddiqui MF, Arsalan A, Ahmed M, Hussain MI, Iqbal J, Wahab M. 2016. Assessment of understorey vegetation of Malam Jabba Forest, Kpk after cleanup operation using multivariate techniques. Jurnal Teknologi 78: 4. ); Muhammad et al. (2016Muhammad Z, Khan N, Ali S, Ullah A, Khan SM. 2016. Density and taxonomic diversity of understory vegetation in relation to site conditions in natural stands of Acacia modesta in Malakand Division, Khyber Pakhtunkhwa, Pakistan. Science 35: 26-34.), and Ullah et al. (2021Ullah R, Khan N, Rahman A. 2021. Comparison of invaded and non-invaded sites: a case study of rough cocklebur (Xanthium strumarium L.) An alien invasive species. Applied Ecology and Environmental Research 19: 1533-1548.), classified plant communities of the Himalayas and found that the shrub communities were dominated by D. viscosa, Justicia adhatoda, Gymnosporia royleana, Berberis lyceum, Xanthium strumarium, and Indigofera gerardiana. These results were similar to ours due to the same eco-geographical region.
Our results show that the distribution of the understory vegetation is more likely linked to topography (elevation, slope, and aspect), soil conditions (physical and chemical), and canopy species (Importance value and basal area) as early reported by several workers (Zhang et al. 2013Zhang ZH, Hu G, Ni J. 2013. Effects of topographical and edaphic factors on the distribution of plant communities in two subtropical karst forests, South-western China. Journal of Mountain Science 10: 95-104.; Huo et al. 2014Huo H, Feng Q, Su YH. 2014. The influences of canopy species and topographic variables on understory species diversity and composition in coniferous forests. The Scientific World Journal 2014. https://doi.org/10.1155/2014/252489
https://doi.org/10.1155/2014/252489...
; Ali et al. 2017Ali F, Khan N, Ali K, Khan I. 2017. Influence of environmental variables on the distribution of woody species in Muslim graveyards of Malakand Division, Hindukush Range Mountains of Pakistan. Pakistan Journal of Botany 49: 2357-66. ; Khan et al. 2020Khan N, Bibi K, Ullah R. 2020. Distribution pattern and ecological determinants of an invasive plant Parthenium hysterophorus L., in Malakand division of Pakistan. Journal of Mountain Science 17: 1670-1683.; Ullah et al. 2021Ullah R, Khan N, Rahman A. 2021. Comparison of invaded and non-invaded sites: a case study of rough cocklebur (Xanthium strumarium L.) An alien invasive species. Applied Ecology and Environmental Research 19: 1533-1548.). Not only topography, but the species composition was also heavily affected by soil physicochemical properties due to diverse environmental factors (Ali et al. 2017Ali F, Khan N, Ali K, Khan I. 2017. Influence of environmental variables on the distribution of woody species in Muslim graveyards of Malakand Division, Hindukush Range Mountains of Pakistan. Pakistan Journal of Botany 49: 2357-66. ). Altitudes are counted as the most influential factor because it is either directly or indirectly linked with many other environmental elements (for example; precipitation, temperature, humidity, solar radiation, etc.). Previously, several workers (e.g., Khan et al. 2015; Huo et al. 2015Huo H, Feng Q, Su YH. 2015. Shrub communities and environmental variables responsible for species distribution patterns in an alpine zone of the Qilian Mountains, northwest China. Journal of Mountain Science 12: 166-176. ; Ali et al. 2017Ali F, Khan N, Ali K, Khan I. 2017. Influence of environmental variables on the distribution of woody species in Muslim graveyards of Malakand Division, Hindukush Range Mountains of Pakistan. Pakistan Journal of Botany 49: 2357-66. ; Ullah et al. 2021Ullah R, Khan N, Rahman A. 2021. Comparison of invaded and non-invaded sites: a case study of rough cocklebur (Xanthium strumarium L.) An alien invasive species. Applied Ecology and Environmental Research 19: 1533-1548.), confirmed the effect of elevation on vegetation. High elevation generally leads to an increase in precipitation and solar radiation, but in contrast to this, the relation between temperature and evapotranspiration is inverse (Odland et al. 2021Odland MC, Goodwin MJ, Smithers BV, Hurteau MD, North MP. 2021. Plant community response to thinning and repeated fire in Sierra Nevada mixed-conifer forest understories. Forest ecology and management 495: p.119361.). Elevation changes lead to changes in temperature, which influences the growing period of plants (Khan et al. 2020Khan N, Bibi K, Ullah R. 2020. Distribution pattern and ecological determinants of an invasive plant Parthenium hysterophorus L., in Malakand division of Pakistan. Journal of Mountain Science 17: 1670-1683.), and as a result plant growth and distribution are highly affected.
Soil fertility and moisture are linked to the slope and have a significant impact on spatial changes in plant composition. Low moisture contents in steep slopes of the studied area may be due to thin soil layer and can affect the vegetation adversely (Ali et al. 2019Ali F, Khan N, Ahmad A, Khan AA. 2019. Structure and biomass carbon of Olea ferruginea forests in the foothills of Malakand division, Hindukush Range Mountains of Pakistan. Acta Ecologica Sinica 39: 261-266.; Khan et al. 2020Khan N, Bibi K, Ullah R. 2020. Distribution pattern and ecological determinants of an invasive plant Parthenium hysterophorus L., in Malakand division of Pakistan. Journal of Mountain Science 17: 1670-1683.). In addition, soil texture, pH, organic matter, nutrients, bulk density, field capacity, and canopy cover were the most significant environmental and vegetation variables affecting floral distribution in this study. A similar effect was also reported in several different studies (e.g., Hou et al. 2014Huo H, Feng Q, Su YH. 2014. The influences of canopy species and topographic variables on understory species diversity and composition in coniferous forests. The Scientific World Journal 2014. https://doi.org/10.1155/2014/252489
https://doi.org/10.1155/2014/252489...
; 2015Huo H, Feng Q, Su YH. 2015. Shrub communities and environmental variables responsible for species distribution patterns in an alpine zone of the Qilian Mountains, northwest China. Journal of Mountain Science 12: 166-176. ; Dölle et al. 2017Dölle M, Petritan AM, Biris IA, Petritan IC. 2017. Relations between tree canopy composition and understorey vegetation in a European beech-sessile oak old growth forest in Western Romania. Biologia 72: 1422-1430. ; Deák et al. 2021Deák B, Kovács B, Rádai Z, et al. 2021. Linking environmental heterogeneity and plant diversity: the ecological role of small natural features in homogeneous landscapes. Science of the Total Environment 763: 144199.).
Results of the RDA ordination showed that understory species distributions were significantly influenced by aspect, soil physio-chemical properties, and canopy species, concurring with the findings of previous studies (Huo et al. 2014Huo H, Feng Q, Su YH. 2014. The influences of canopy species and topographic variables on understory species diversity and composition in coniferous forests. The Scientific World Journal 2014. https://doi.org/10.1155/2014/252489
https://doi.org/10.1155/2014/252489...
; Ullah et al. 2021Ullah R, Khan N, Rahman A. 2021. Comparison of invaded and non-invaded sites: a case study of rough cocklebur (Xanthium strumarium L.) An alien invasive species. Applied Ecology and Environmental Research 19: 1533-1548.). Contrary to findings of Augusto et al. (2003Augusto L, Dupouey JL, Ranger J. 2003. Effects of tree species on understory vegetation and environmental conditions in temperate forests. Annals of Forest Science 60: 823-831.) and Duguid et al. (2013Duguid MC, Frey BR, Ellum DS, Kelty M, Ashton MS. 2013. The influence of ground disturbance and gap position on understory plant diversity in upland forests of southern New England. Forest ecology and management 303: 148-159.), we reported no effect of soil-based variables like pH, organic matter, bulk density, lime, potassium, and total nitrogen on understory vegetation in our study. However, the importance of aspect and slope on species distribution pattern was described by several workers (Barbier et al. 2008Barbier S, Gosselin F, Balandier P. 2008. Influence of tree species on understory vegetation diversity and mechanisms involved a critical review for temperate and boreal forests. Forest ecology and management 254: 1-15.; Yu et al. 2013Yu M, Sun OJ. 2013. Effects of forest patch type and site on herb-layer vegetation in a temperate forest ecosystem. Forest ecology and management 300: 14-20. ), which is in agreement with the findings of the current study. Similarly, Ali et al. (2019Ali F, Khan N, Ahmad A, Khan AA. 2019. Structure and biomass carbon of Olea ferruginea forests in the foothills of Malakand division, Hindukush Range Mountains of Pakistan. Acta Ecologica Sinica 39: 261-266.) also reported a significant effect of topography and edaphic variables on species diversity, richness, and composition in broad-leaved evergreen forests of O. ferruginea in the Muslim graveyards of northern Pakistan. The effect of canopy species on understory vegetation was confirmed by RDA in the current study supporting the finding of Koorem & Moora 2010Koorem K, Moora M. 2010. Positive association between understory species richness and a dominant shrub species (Corylus avellana) in a boreonemoral spruce forest. Forest ecology and management 260: 1407-1413. ; Ádám et al. 2013Ádám R, Ódor P, Bölöni J. 2013. The effects of stand characteristics on the understory vegetation in Quercus petraea and Q. cerris dominated forests. Community Ecology 14: 101-109.; Zhang et al. 2013Zhang ZH, Hu G, Ni J. 2013. Effects of topographical and edaphic factors on the distribution of plant communities in two subtropical karst forests, South-western China. Journal of Mountain Science 10: 95-104.).
Conclusions
Understory vegetation holds a large proportion of plant diversity and contributes significantly to ecosystem functioning in forests. In this study, we compared understory vegetation in 4 different Monotheca dominated community types. Our findings revealed that each forest type possesses a unique understory community. The leading position of Monotheca in the canopy favour changing the understory site conditions significantly, most likely by shading the forest floor and producing a high amount of refractory litter. Results showed that understory species composition was primarily affected by canopy, topography and soil conditions. Comparing explanatory variables, canopy variables (tree basal area, IVI) had higher explanatory power than did site conditions for understory species distributions. For understory flora, there was a decline in both species richness and diversity with a decrease in the canopy species. The variance in species richness, diversity, life-form, leaf-size spectrum and chorological affinities highlights the importance of canopy species of Monotheca dominated forests in maintaining understory species diversity and community stability in broadleaved evergreen forests. Our results also ease the understanding of understory species distributions in these stands.
Acknowledgments
The authors thankfully acknowledge residents of the study area and forest officers for the provision of logistic facilities, sharing common names and locations of the plant species.
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Publication Dates
-
Publication in this collection
12 Sept 2022 -
Date of issue
2022
History
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Received
10 July 2021 -
Accepted
20 Apr 2022