applied sciences

Article

Plant Species Classification and Diversity of the UnderstoryVegetation in Oak Forests of Swat Pakistan

Ataur Rahman 1 Nasrullah Khan 1 Kishwar Ali 2 Rafi Ullah 1 Muhammad Ezaz Hasan Khan 2David Aaron Jones 2 and Inayat Ur Rahman 3

Citation Rahman A Khan N Ali

K Ullah R Khan MEH Jones

DA Rahman IU Plant Species

Classification and Diversity of the

Understory Vegetation in Oak Forests

of Swat Pakistan Appl Sci 2021 11

11372 httpsdoiorg103390

app112311372

Academic Editor Claudio De

Pasquale

Received 2 October 2021

Accepted 26 November 2021

Published 1 December 2021

Publisherrsquos Note MDPI stays neutral

with regard to jurisdictional claims in

published maps and institutional affil-

iations

Copyright copy 2021 by the authors

Licensee MDPI Basel Switzerland

This article is an open access article

distributed under the terms and

conditions of the Creative Commons

Attribution (CC BY) license (https

creativecommonsorglicensesby

40)

1 Department of Botany University of Malakand Chakdara Dir Lower 18800 KP Pakistansar850gmailcom (AR) rafiullah198773gmailcom (RU)

2 School of General Education College of the North Atlantic Qatar Arab League Street Doha 24449 Qatarkishwaralicna-qatareduqa (KA) mdezazhasankhancna-qatareduqa (MEHK)davidaaronjonescna-qatareduqa (DAJ)

3 Department of Botany Hazara University Mansehra 21300 KP Pakistan hajibotanistoutlookcom Correspondence nasrullahuomgmailcom

Abstract The forest ecosystem has understory vegetation that plays a vital role in sustaining diversityproviding nutrients and forming a useful association for developing a balanced ecosystem Thecurrent study provides detailed insights into the plant biodiversity and species classification of theunderstory vegetation of Swat Pakistan The floral diversity of the area was comprised of 58 plantspecies belonging to 32 families The physiognomy of the studied area was dominated by herbaceousgrowth form with 47 species The dominant life-form class was hemicryptophytes with 19 species(33) followed by nanophanerophytes with 15 species (26) and therophytes with 13 species (22)Of the 58 species 43 plant species were associated with group III clustered by applying Wardrsquosagglomerative clustering that indicated wide sociability of the species in the studied oak-dominatedforests Group III had higher species richness (103) α-diversity (274) and β-diversity (985) andMargalef index values (395) While the group I had maximum Pielous and Simpson index values of097 and 713 respectively Redundancy analysis revealed that seven variables (ie latitude elevationclay wilting point bulk density saturation and electric conductivity) were significantly influentialconcerning the understory vegetation of oak-dominated forests The understory vegetation of theseforests plays an important role in the forest ecosystem of the region The present study reveals floraldivergence and physiognomic scenario of the unexplored study area which could be an importantreference for future ethnobotanical phytosociological and conservational endeavors Moreover thisinformation is important to the success of efforts intended to prevent the loss of species diversity inthese forests by destroying their natural habitats

Keywords biodiversity Quercus floristic composition Raunkiaer classification chorology speciesdiversity environmental variables

1 Introduction

The most useful source of botanical information of a particular area is its floristic check-lists [12] Since floristic composition is a decent floristic marker any changing floristiccomposition in various endogenous milieus highlights the presence of various environmen-tal variables prompting entomb and intra-particular variations [3] The floristic structure ofa specific territory provides fundamental However information about the plant dissemina-tion and motherland show diversity in landscapes topographies and biologicalecologicalzones bolstering the distinctive floristic composition [4] To contemplate the vegetation of aterritory it is essential to oversee the plantrsquos life-form which is an indicator for both micro-and macroclimate [5] As indicated by Raunkiaer [6] the biological spectrum is divided intofive major classes (ie phanerophytes hemicryptophytes cryptophytes chamaephytesand therophytes)

Appl Sci 2021 11 11372 httpsdoiorg103390app112311372 httpswwwmdpicomjournalapplsci

Appl Sci 2021 11 11372 2 of 17

The plant species are also categorized based on leaf size classes which are also ex-tremely helpful for association mapping of vegetation it may also be helpful for compre-hension of the plant communities and their physiological processes [78] Leaf sizes andshapes (physiognomy) connect unequivocally with moisture and temperature from world-wide to neighborhood scales [9] Leaf characteristics assume an especially imperative partin carbon absorption water relations and vitality adjust (energy balance) [9] Furthermorea life-form and leaf size spectra provide a clear picture of an area Therefore climaticconditions of a certain region may accurately be referred from such observations [10]These physiognomic characters have been widely used in vegetation investigations inanthropogenic and naturally vulnerable areas [510]

The understory vegetation plays a major role in sustaining the structure and functionof forest ecosystems [1112] promoting energy transfer and nitrogen cycles and shapingthe canopy succession of forest ecosystems [1314] The understory makes comparativelylittle contribution to the overall biomass of forest plants [1315] it promotes the greatestproportion in floristic diversity [16] In addition diversified understory vegetation booststhe structural complexity of forests and provides other biotic groups with habitats and foodincreasing their diversity [17] For forest regeneration understory vegetation is extremelycrucial as it can influence the germination survival and development of tree seedlingsby competing for light water and nutrients [111518] Therefore increasing attention isbeing paid to forest understory vegetation [16] It is essential to know about the mostinfluential variables affecting their distribution for ecological protection conservation andforest management [121619]

Numerous studies have shown the effect on the species composition and diversityof understory flora These include flora canopy species and structure [20] stand man-agement [21] soil disturbances [22] light resources [23] litter properties [2024] and soilnutrients and pH [2325] Topography can dramatically change microclimates and theavailability of energy under the tree canopy [2326] and in turn affect the composition anddiversity of understory species [1227] In coniferous forests hardwood forests and mixed-wood forests understory vegetation has been well studied [2528] The latter two typesof forests are generally agreed to create more favorable conditions for their biodiversityconservation and restoration than coniferous forests [21] In general broad-leaved ever-green forest and oak forest have been ignored in understory vegetation and its compositionBeg and Mirza [29] studied oak-dominated forests in the Hindukush-mountain region Inthe study four oak species have been reported from the region ie Quercus lanata SmQuercus robur L Quercus baloot Griff and Quercus semecarpifolia Sm The research work alsoreported thirty-six understory species in the oak-dominated forest So far no comprehen-sive study has investigated the details of phytosociological attributes and environmentalvariables in association with those understories aiming to understand its diversity Forestecosystemsrsquo floristic composition geographic distribution and ecological conditions areessential for a rational management plan In this study the understory species compo-sition is considered to differ significantly among the major groups concerning speciesrichness and diversity Additionally attempts were made to determine the extent to whichphysiographic and edaphic variables could explain variation in the understory speciescomposition and major distinct groups of oak-dominated forests

2 Materials and Methods21 Study Site

Swat district is located in northwest of Pakistan in Khyber Pakhtunkhwa (KP) province(Figure 1) It is a well-known summer resort in the country for national and internationaltourists and visitors It lies between 340prime34rdquo and 350prime55rdquo north latitudes and 720prime08rdquoand 720prime50rdquo east longitudes The total area of the district is 5337 Km2 Most of the areaconsists of mountainous regions belonging to the Hinduraj series of Hindukush mountainsThe climate of Swat is relatively warm in the lower parts but cooler and refreshing in theupper parts of the Valley Summers are short and moderate temperatures seldom rise

Appl Sci 2021 11 11372 3 of 17

above 37 C Annual rainfall ranges from 800 to 900 mm and snowfall during winter is theconstant feature of upper Swat [30]

Appl Sci 2021 11 x FOR PEER REVIEW 3 of 18

72deg0prime08Prime and 72deg0prime50Prime east longitudes The total area of the district is 5337 Km2 Most of the

area consists of mountainous regions belonging to the Hinduraj series of Hindukush

mountains The climate of Swat is relatively warm in the lower parts but cooler and re-

freshing in the upper parts of the Valley Summers are short and moderate temperatures

seldom rise above 37 degC Annual rainfall ranges from 800 to 900 mm and snowfall during

winter is the constant feature of upper Swat [30]

Figure 1 Showing sampling points in oak-dominated forests of Swat Pakistan

22 Field Investigation

Extensive field surveys were carried out during the flowering and fruiting stages

Timings for the fieldwork were carefully selected according to the plantrsquos growth phases

and collection season A handheld (Garmin manufactured in Germany) Geographical Po-

sitioning System (GPS) recorded the study area coordinates A total of 300 plots having

an area of 20 m times 20 m were established in thirty stands (10 plotsstand) of the oak forest

at an elevation ranging from 1000 to 2900 m The understory vegetation is defined as

shrubs and herbaceous plants growing on the forest floor Each 20 times 20 m plot was divided

into four 10 times 10 m quadrats three of which were chosen at random to survey shrub spe-

cies Five 1 times 1 m quadrats one in the middle and four at the corners of the 20 times 20 m plot

Figure 1 Showing sampling points in oak-dominated forests of Swat Pakistan

22 Field Investigation

Extensive field surveys were carried out during the flowering and fruiting stagesTimings for the fieldwork were carefully selected according to the plantrsquos growth phasesand collection season A handheld (Garmin manufactured in Germany) GeographicalPositioning System (GPS) recorded the study area coordinates A total of 300 plots havingan area of 20 m times 20 m were established in thirty stands (10 plotsstand) of the oak forestat an elevation ranging from 1000 to 2900 m The understory vegetation is defined asshrubs and herbaceous plants growing on the forest floor Each 20 m times 20 m plot wasdivided into four 10 m times 10 m quadrats three of which were chosen at random to surveyshrub species Five 1 m times 1 m quadrats one in the middle and four at the corners of the20 m times 20 m plot were used to study herbaceous plants Phytosociological parametersie height and density with the percent coverrsquos visual calculations were measured [3132]The life-form classes and leaf spectra of all plant species were determined and classifiedaccording to Raunkiaer [7] Plants reported and collected were identified by expert planttaxonomists and were then rechecked with the Royal Botanical Garden Kew online web(httpwwwplantsoftheworldonlineorg accessed on 14 November 2021) and the Flora

Appl Sci 2021 11 11372 3 of 17

above 37 C Annual rainfall ranges from 800 to 900 mm and snowfall during winter is theconstant feature of upper Swat [30]

Appl Sci 2021 11 x FOR PEER REVIEW 3 of 18

72deg0prime08Prime and 72deg0prime50Prime east longitudes The total area of the district is 5337 Km2 Most of the

area consists of mountainous regions belonging to the Hinduraj series of Hindukush

mountains The climate of Swat is relatively warm in the lower parts but cooler and re-

freshing in the upper parts of the Valley Summers are short and moderate temperatures

seldom rise above 37 degC Annual rainfall ranges from 800 to 900 mm and snowfall during

winter is the constant feature of upper Swat [30]

Figure 1 Showing sampling points in oak-dominated forests of Swat Pakistan

22 Field Investigation

Extensive field surveys were carried out during the flowering and fruiting stages

Timings for the fieldwork were carefully selected according to the plantrsquos growth phases

and collection season A handheld (Garmin manufactured in Germany) Geographical Po-

sitioning System (GPS) recorded the study area coordinates A total of 300 plots having

an area of 20 m times 20 m were established in thirty stands (10 plotsstand) of the oak forest

at an elevation ranging from 1000 to 2900 m The understory vegetation is defined as

shrubs and herbaceous plants growing on the forest floor Each 20 times 20 m plot was divided

into four 10 times 10 m quadrats three of which were chosen at random to survey shrub spe-

cies Five 1 times 1 m quadrats one in the middle and four at the corners of the 20 times 20 m plot

Figure 1 Showing sampling points in oak-dominated forests of Swat Pakistan

22 Field Investigation

Extensive field surveys were carried out during the flowering and fruiting stagesTimings for the fieldwork were carefully selected according to the plantrsquos growth phasesand collection season A handheld (Garmin manufactured in Germany) GeographicalPositioning System (GPS) recorded the study area coordinates A total of 300 plots havingan area of 20 m times 20 m were established in thirty stands (10 plotsstand) of the oak forestat an elevation ranging from 1000 to 2900 m The understory vegetation is defined asshrubs and herbaceous plants growing on the forest floor Each 20 m times 20 m plot wasdivided into four 10 m times 10 m quadrats three of which were chosen at random to surveyshrub species Five 1 m times 1 m quadrats one in the middle and four at the corners of the20 m times 20 m plot were used to study herbaceous plants Phytosociological parametersie height and density with the percent coverrsquos visual calculations were measured [3132]The life-form classes and leaf spectra of all plant species were determined and classifiedaccording to Raunkiaer [7] Plants reported and collected were identified by expert planttaxonomists and were then rechecked with the Royal Botanical Garden Kew online web(httpwwwplantsoftheworldonlineorg accessed on 14 November 2021) and the Flora

Appl Sci 2021 11 11372 4 of 17

of Pakistan [3334] The Herbarium specimens were submitted to the Department of BotanyUniversity of Malakand

23 Soil Analysis

A stainless-steel cylindrical soil sampler with a diameter of 5 cm was used to collectfive topsoil samples (0ndash10 cm depth) at random sites from each plot The samples werethen carefully combined to create a composite sample for analysis The hybrid soil sampleswere air-dried and sieved to 02 mm for soil organic carbon (SOC) and total nitrogen (TN)tests and 2 mm for soil pH tests prior to analysis The updated Mebius approach wasused to examine SOC [35] The Kjeldahl procedure was used to evaluate TN [36] In a125 soil to water suspension the pH of the soil was determined [37] The volumetric ringprocedure was used to determine the bulk density of the soil [38] Soil textural propertieswere determined using Bouyoucos hydrometer [39] while electrical conductivity wascalculated using a conductometer (Model CON 5) Important nutrients like potassiumphosphorus and lime were determined by following standard procedures adopted by [38]

24 Data Analysis

The relative important value (IV) and importance value index (IVI) of each species inthe understory plant community was calculated as follows

IV (x) = F3 (x) + D3 (x) + C3 (x) (1)

IVI (x) =IV (x)

300times 100 (2)

where F3 (x) relative frequency D3 (x) relative density and C3 (x) relative coverIVI (x) represents the computed importance value index of understory species and

seedling sapling of tree species while IV (x) represents the computed importance value ofthe associated understory species The species richness and α-diversity (Shannon index HEvenness index E Margalefrsquos index M and Simpsonrsquos index 1D) were used to describeplot diversity and β-diversity for changes in community structure across sites withincontrasting forest types

Hprime = sumSi=1 pi Inpi (3)

E =Hprime

InS(4)

M = S minus 1In N (5)

1D = 1Σ (pi2) (6)

β = Sta (7)

where pi = proportion of the species (i) to total number of species In = natural logarithmS = species richness N = total number of species St = number of species in all plots anda = total number of plots

Wardrsquos agglomerative cluster analysis was used for classification of the understoryvegetation stands as the species distribution varies across the elevation gradient thereforecluster analysis was preferred in comparison with other technique available in Pc-ordversion 6 in which Euclidean distance was opted for measuring distance using Wardrsquoslinkage method [40] Redundancy analysis (RDA) evaluated the effects of different en-vironmental and understory parameters using PC-ord version 6 The suitability of RDAanalysis was assessed by using published literature in which first DCA-ordination wasperformed [41] to elucidate whether unimodal [4243] or linear [44] response curve shouldbe used in ordination analysis The gradient length on DCA-axes 1 was 12 which is morethan 41 and therefore the use of Canonical Correspondence analysis (CCA) or RDA wastested In the choice between CCA and RDA-ordination we prefer the RDA as the age variance was (30) and stands distribution was uniform in biplot compared to CCA

Appl Sci 2021 11 11372 5 of 17

ordination having variance of 19 Ms-Excel 2010 was used for data tabulation and graphicpresentation while SPSS version 22 was used for statistical analysis The significance ofthe variables was tested at p lt 005 In addition post hoc honestly significant differences(HSD) test was used for variation between the groups

3 Results31 Understory Species Composition

A total number of 58 understory plant species belonging to 32 families was identifiedat 30 different locations in the Hindukush ranges of Swat The physiognomy was domi-nated by herbaceous growth form with 47 plant species (81) followed by shrubs with10 (17) and trees with a single plant species (2) Herbaceous dominancy may be due toaltitudinal and geographical variations indicating the herbaceous florarsquos climatic factorsAmong the families Fabaceae was the leading family with eight plant species followed byAsteraceae and Lamiaceae with seven species each Further seven families (ie Amaran-thaceae Malvaceae Poaceae Plantaginaceae Polygonaceae Pteridaceae and Rosaceae)were recorded with two plant species each The remaining 22 families are represented byindividual species (Table 1)

Table 1 List of the plant species with the family names growth formhabit chorotype life-form and leaf size classes thatwere recorded in understory vegetation of oak-dominated forests of Swat Pakistan

Taxon Family Habit Chorotype Life-Form Leaf Size

Achyranthes aspera L Amaranthaceae Herb Plurireg Th NAdiantum venustum D Don Pteridaceae Herb Cosm G N

Ajuga bracteosa Wall ex Benth Lamiaceae Herb Unireg H MiAmaranthus viridis L Amaranthaceae Herb Cosm Th Mi

Arabidopsis thaliana (L) Heynh Brassicaceae Herb Cosm Th LArenaria serpyllifolia L Caryophyllaceae Herb Cosm Th NArtemisia vulgaris L Asteraceae Herb Plurireg Th N

Asplenium trichomanes L Aspleniaceae Herb Bireg H NAstragalus grahamianus Benth Fabaceae Herb Unireg Ch L

Atropa acuminata Royle ex Lindl Solanaceae Herb Plurireg G MiBerberis lycium Royle Berberidaceae Shrub Unireg NPh L

Bidens cernua L Asteraceae Herb Bireg H MiBuddleja asiatica Lour Scrophulariaceae Shrub Cosm NPh Mi

Calamintha vulgaris (L) H Karst Lamiaceae Herb Plurireg Th NChenopodium album L Chenopodiaceae Herb Cosm H NConvolvulus arvensis L Convolvulaceae Herb Cosm H NErigeron canadensis L Asteraceae Herb Cosm Th L

Cynodon dactylon (L) Pers Poaceae Herb Plurireg H LDaphne mucronata Royle Thymelaeaceae Shrub Bireg NPh N

Dioscorea deltoidea Wall ex Griseb Dioscoreaceae Herb Unireg H MiDodonaea viscosa Jacq Sapindaceae Shrub Cosm NPh Mi

Dryopteris stewartii Fraser-Jenk Dryopteridaceae Herb Bireg G MeElaeagnus angustifolia L Elaeagnaceae Shrub Bireg NPh MiFestuca gigantea (L) Vill Poaceae Herb Bireg G LFragaria indica Andrews Rosaceae Herb Plurireg H NGalium asperifolium Wall Rubiaceae Herb Unireg Th L

Hibiscus syriacus L Malvaceae Shrub Plurireg NPh MiIndigofera gerardiana Graham ex Baker Fabaceae Herb Unireg NPh NIndigofera heterantha Wall ex Brandis Fabaceae Herb Unireg NPh L

Isodon rugosus (Wall ex Benth) Codd Lamiaceae Herb Unireg NPh MiJusticia adathoda L Lamiaceae Herb Plurireg NPh MeLamium album L Lamiaceae Herb Unireg Th Mi

Lespedeza juncea (L f) Pers Fabaceae Herb Unireg H NLotus corniculatus L Fabaceae Herb Bireg H MiMalva neglecta Wallr Malvaceae Herb Unireg H MiMedicago lupulina L Fabaceae Herb Plurireg Ch N

Appl Sci 2021 11 11372 6 of 17

Table 1 Cont

Taxon Family Habit Chorotype Life-Form Leaf Size

Myrsine africana L Primulaceae Shrub Bireg NPh LOriganum vulgare L Lamiaceae Herb Unireg Th N

Otostegia limbata (Benth) Boiss Lamiaceae Herb Unireg NPh LOxytropis mollis Royle ex Benth Fabaceae Herb Unireg H L

Plantago lanceolata L Plantiganaceae Herb Plurireg H MiPlantago major L Plantaginaceae Herb Plurireg H Mi

Polygonatum verticillatum (L) All Asparagaceae Herb Plurireg Th NPteris cretica L Pteridaceae Herb Plurireg G Mi

Ranunculus laetus Salisb Ranunculaceae Herb Unireg H MeRosa webbiana Wall ex Royle Rosaceae Herb Plurireg NPh NRumex denticulatus K Koch Polygonaceae Herb Bireg H Me

Rumex nepalensis Spreng Polygonaceae Herb Bireg H MeSarcococca saligna (DDon) MuumlllArg Buxaceae Shrub Bireg NPh Mi

Smilax lanceolata L Smilacaceae Herb Bireg L MiSolidago virgaurea L Asteraceae Herb Unireg H Mi

Tagetes minuta L Asteraceae Herb Bireg Th MiTaraxacum officinale (L) Weber ex

FHWigg Asteraceae Herb Cosm H Mi

Trifolium repens L Fabaceae Herb Cosm G NViburnum grandiflorum Wall ex DC Viburnaceae Shrub Unireg NPh Ma

Viola serpens Wall ex Ging Violaceae Shrub Plurireg G MiYoungia japonica (L) DC Asteraceae Herb Cosm Th Mi

Zanthoxylum armatum DC Rutaceae Tree Cosm MPh Mi

Plurireg (Pluriregional) Unireg (Uniregional) Cosm (Cosmopolitan) Bireg (Biregional) Th (Therophyte) G (Geophytes) NPh (Nano-phanerophyte) H (Hemicryptophyt) MPh (Microphanerophytes) Ch (Chamaephyte) Mi (Microphyllous) Ma (Megaphyllous) N(Nanophyllous) L (Leptophyllous) Acronyms were assigned by following Shehata [45] except Raunkiaer life-form

The present study identified seven different life-form classes in the study area (Figure 2)The most dominant life-form was hemicryptophytes with 19 species (33) followedby nanophanerophytes with 15 species (26) therophytes with 13 species (22) andgeophytes with 7 species (12) Two species of chamaephytes (3) and one species (2)of nanophanerophytes and liana were also recorded (Table 1)

Appl Sci 2021 11 x FOR PEER REVIEW 7 of 18

Figure 2 Life-form classes of the plant species recorded in the understory vegetation of oak-domi-

nated forests of Swat Pakistan

32 Leaf Size Spectra

Results of leaf size spectra trait revealed that species with microphyllous leaves dom-

inated the area with 24 species (41) followed by nanophyll 17 species (29) leptophyll

11 species (19) and mesophyll 5 species (9) (Figure 3) Single species (2) with meg-

aphyllous leaf size was also recorded A high rate of microphylls may be identified within

the cool environment of the sub-elevated and snowcapped areas Here the top layer was

less settled it contained a slim sheet that may deny them the entrance of roots The micro-

phyllous and nanophyllous leaves species were inexhaustible because of the biological

variety for this dry condition

Figure 3 Leaf size classes of the plant species recorded in the understory vegetation of oak-domi-

nated forests of Swat Pakistan

The chorotype of the species varies from uniregional to cosmopolitan ie 22 were

cosmopolitan 26 pluriregional 23 bioregional and 29 were uniregional

26

33

22

12

3 2 2

Life forms

Nanophanerophytes

Hemicryptophytes

Therophytes

Geophytes

Chamaephytes

Microphanerophytes

Lianas

19

2941

9

2

Leaf size class

Leptophylls

Nanophylls

Microphylls

Mesophylls

Megaphylls

Figure 2 Life-form classes of the plant species recorded in the understory vegetation of oak-dominated forests of Swat Pakistan

Appl Sci 2021 11 11372 7 of 17

32 Leaf Size Spectra

Results of leaf size spectra trait revealed that species with microphyllous leaves domi-nated the area with 24 species (41) followed by nanophyll 17 species (29) leptophyll11 species (19) and mesophyll 5 species (9) (Figure 3) Single species (2) with mega-phyllous leaf size was also recorded A high rate of microphylls may be identified withinthe cool environment of the sub-elevated and snowcapped areas Here the top layer wasless settled it contained a slim sheet that may deny them the entrance of roots The mi-crophyllous and nanophyllous leaves species were inexhaustible because of the biologicalvariety for this dry condition

Appl Sci 2021 11 x FOR PEER REVIEW 7 of 18

Figure 2 Life-form classes of the plant species recorded in the understory vegetation of oak-domi-

nated forests of Swat Pakistan

32 Leaf Size Spectra

Results of leaf size spectra trait revealed that species with microphyllous leaves dom-

inated the area with 24 species (41) followed by nanophyll 17 species (29) leptophyll

11 species (19) and mesophyll 5 species (9) (Figure 3) Single species (2) with meg-

aphyllous leaf size was also recorded A high rate of microphylls may be identified within

the cool environment of the sub-elevated and snowcapped areas Here the top layer was

less settled it contained a slim sheet that may deny them the entrance of roots The micro-

phyllous and nanophyllous leaves species were inexhaustible because of the biological

variety for this dry condition

Figure 3 Leaf size classes of the plant species recorded in the understory vegetation of oak-domi-

nated forests of Swat Pakistan

The chorotype of the species varies from uniregional to cosmopolitan ie 22 were

cosmopolitan 26 pluriregional 23 bioregional and 29 were uniregional

26

33

22

12

3 2 2

Life forms

Nanophanerophytes

Hemicryptophytes

Therophytes

Geophytes

Chamaephytes

Microphanerophytes

Lianas

19

2941

9

2

Leaf size class

Leptophylls

Nanophylls

Microphylls

Mesophylls

Megaphylls

Figure 3 Leaf size classes of the plant species recorded in the understory vegetation of oak-dominatedforests of Swat Pakistan

The chorotype of the species varies from uniregional to cosmopolitan ie 22 werecosmopolitan 26 pluriregional 23 bioregional and 29 were uniregional

33 Understory Classification

A total of 58 plant species were recorded as associates in the understory vegeta-tion and clustered into three major groups by applying Wardrsquos agglomerative clustering(Figure 4 and Table 2) Among 58 species 43 plant species were found in association withgroup III clearly indicating the speciesrsquo wide sociability in the studied oak-dominatedforests Moreover the analysis reveals that IVI of Berberis lycium Royle (782) Convolvulusarvensis L (687) and Asplenium trichomanes L (66) were the most abundant species ingroup III Group II was recorded intermediately diverse in understory species having25 plant species with Calamintha vulgaris (L) H Karst Dryopteris stewartii Fraser-Jenkand Plantago lanceolata L as the dominant associates having IVI of 115 934 and 986respectively The results revealed group I as the less diverse in terms of species (18 species)and B lycium having IVI of 986 A trichomanes (914) and Indigofera heterantha Wall exBrandis (893) were the most abundant species

Appl Sci 2021 11 11372 8 of 17

Appl Sci 2021 11 x FOR PEER REVIEW 8 of 18

33 Understory Classification

A total of 58 plant species were recorded as associates in the understory vegetation

and clustered into three major groups by applying Wardrsquos agglomerative clustering (Fig-

ure 4 and Table 2) Among 58 species 43 plant species were found in association with

group III clearly indicating the speciesrsquo wide sociability in the studied oak-dominated

forests Moreover the analysis reveals that IVI of Berberis lycium Royle (782) Convolvulus

arvensis L (687) and Asplenium trichomanes L (66) were the most abundant species in

group III Group II was recorded intermediately diverse in understory species having 25

plant species with Calamintha vulgaris (L) H Karst Dryopteris stewartii Fraser-Jenk and

Plantago lanceolata L as the dominant associates having IVI of 115 934 and 986 respec-

tively The results revealed group I as the less diverse in terms of species (18 species) and

B lycium having IVI of 986 A trichomanes (914) and Indigofera heterantha Wall ex Brandis

(893) were the most abundant species

Figure 4 Cluster dendrogram classifying understory vegetation into three distinct groups Note G

(Group) St (Stand)

Table 2 Understory flora associated with oak-dominated forest recorded in the three clusters separated by Wardrsquos ag-

glomerative clustering procedure

Species Name Code Cluster I Cluster II Cluster III

M plusmn SE M plusmn SE M plusmn SE

Achyranthes aspera L As 241 plusmn 241 - -

Adiantum venustum D Don Av - - 077 plusmn 077

Ajuga bracteosa Wall ex Benth Ab 387 plusmn 265 - -

Amaranthus viridis L Am 510 plusmn 323 - 241 plusmn 144

Arabidopsis thaliana (L) Heynh At - - 116 plusmn 079

Arenaria serpyllifolia L Am - - 053 plusmn 053

Artimisia vulgaris L Av 72 plusmn 471 - -

Figure 4 Cluster dendrogram classifying understory vegetation into three distinct groups NoteG (Group) St (Stand)

Table 2 Understory flora associated with oak-dominated forest recorded in the three clusters separated by Wardrsquosagglomerative clustering procedure

Species Name CodeCluster I Cluster II Cluster III

M plusmn SE M plusmn SE M plusmn SE

Achyranthes aspera L As 241 plusmn 241 - -Adiantum venustum D Don Av - - 077 plusmn 077

Ajuga bracteosa Wall ex Benth Ab 387 plusmn 265 - -Amaranthus viridis L Am 510 plusmn 323 - 241 plusmn 144

Arabidopsis thaliana (L) Heynh At - - 116 plusmn 079Arenaria serpyllifolia L Am - - 053 plusmn 053

Artimisia vulgaris L Av 72 plusmn 471 - -Asplenium trichomanes L As 914 plusmn 471 423 plusmn 423 66 plusmn 26

Astragalus grahamianus Benth Ag - - 053 plusmn 053Atropa acuminata Royle ex Lindl Aa 34 plusmn 346 - 242 plusmn 243

Berberis lycium Royle B 986 plusmn 549 766 plusmn 491 782 plusmn 354Bidens cernua L Bc - 171 plusmn 171 -

Buddleja asiatica Lour Ba 093 plusmn 093 - 169 plusmn 117Calamintha vulgaris (L) H Karst Cv - 115 plusmn 411 346 plusmn 166

Chenopodium album L Ca - 44 plusmn 442 -Convolvulus arvensis L Ca 25 plusmn 252 42 plusmn 274 687 plusmn 176Erigeron canadensis L Co 085 plusmn 085 - -

Cynodon dactylon (L) Pers Cd 7 plusmn 5 617 plusmn 617 488 plusmn 332Daphne mucronata Royle Dm 383 plusmn 383 - 194 plusmn 134

Dioscorea deltoidea Wall ex Griseb Dd 183 plusmn 183 - -Dodonaea viscosa Jacq Do 142 plusmn 142 - -

Dryopteris stewartii Fraser-Jenk Ds - 986 plusmn 986 -Elaeagnus angustifolia L Ea 23 plusmn 23 - -Festuca gigantea (L) Vill Fg - - 046 plusmn 046

Appl Sci 2021 11 11372 9 of 17

Table 2 Cont

Species Name CodeCluster I Cluster II Cluster III

M plusmn SE M plusmn SE M plusmn SE

Fragaria indica Andrews Fi - 271 plusmn 271 553 plusmn 222Galium asperifolium Wall Ga 436 plusmn 436 - 134 plusmn 134

Hibiscus syriacus L Hs - - 06 plusmn 062Indigofera gerardiana Graham ex Baker Ig - - 365 plusmn 286Indigofera heterantha Wall ex Brandis Ih 893 plusmn 893 - -Isodon rugosus (Wall ex Benth) Codd Ir - 82 plusmn 82 -

justica adathoda L Ja - - 196 plusmn 145Lamium album L La - - 053 plusmn 053

Lespedeza juncea (L f) Pers Lj 502 plusmn 502 - 291 plusmn 291Lotus corniculatus L Lc 25 plusmn 25 - 252 plusmn 157Malva neglecta Wallr Mn - - 106 plusmn 106Medicago lupulina L Ml - - 121 plusmn 121Myrsine africana L Ma 45 plusmn 37 185 plusmn 185 596 plusmn 253

Origanum vulgare L Ov - 26 plusmn 268 -Otostegia limbata (Benth) Boiss Ol - - 160 plusmn 113Oxytropis mollis Royle ex Benth Om 363 plusmn 363 171 plusmn 171 336 plusmn 197

Plantago lanceolata L Pl 23 plusmn 23 934 plusmn 615 605 plusmn 329Plantago major L Pm - 59 plusmn 4 046 plusmn 046

Polygonatum verticillatum (L) All Pv - 171 plusmn 171 -Pteris cretica L Pc - - 167 plusmn 118

Ranunculus laetus Salisb Rl - - 093 plusmn 093Rosa webbiana Wall ex Royle Rw - - -Rumex denticulatus K Koch Ru - - 449 plusmn 257

Rumex nepalensis Spreng Rn - 357 plusmn 357 053 plusmn 053Sarcococca saligna (DDon) MuumlllArg Ss - - 053 plusmn 053

Smilax lanceolata L Sl 1 plusmn 12 - 308 plusmn 179Solidago virgaurea L Sv - - 053 plusmn 053

Tagetes minuta L Tg 502 plusmn 502 - 121 plusmn 121Taraxacum officinale (L) Weber ex

FHWigg To - - 06 plusmn 061

Trifolium repens L Tr - - 136 plusmn 095Viburnum grandiflorum Wall ex DC Vg - - 228 plusmn 228

Viola serpens Wall ex Ging Vs - - 135 plusmn 094Youngia japonica (L) DC Yj - 27 plusmn 272 -

Zanthoxylum armatum DC Za - - 106 plusmn 106

Note - Represent absence of specie in particular group

34 Understory Species Diversity and Richness

Significant differences in species richness (p lt 0015) ShannonndashWiener Margalef(p lt 000076) Simpson (p lt 0040) and Beta indexes were detected among three majorgroups of the understory layer of oak-dominated forests (Table 3) Nonetheless Pielousevenness was found non-significantly different (p gt 005) among the three major groups ofunderstory vegetation Group III had the highest species richness (103) α-diversity (274)and β-diversity (985) and the highest value of Margalef index (395) On the contrary thegroup I had the highest Pielous and Simpson index values with 097 and 713 respectively(Table 3)

Appl Sci 2021 11 11372 10 of 17

Table 3 Species richness and diversity indexes of oak-dominated forests of Swat Pakistan

IndexesGroup I Group II Group III

F pMean plusmn SE Mean plusmn SE Mean plusmn SE

Total number of Species (S) 587 plusmn 066 b 4 plusmn 037 a 1032 plusmn 15 b 485 0015ShannonndashWiener Index (H) 184 plusmn 019 a 13 plusmn 011 a 274 plusmn 020 b 1393 697 times 10minus5

Pielous Index (J) 097 plusmn 001 095 plusmn 001 093 plusmn 001 209 014Margalef Index (M) 29 plusmn 033 a 14 plusmn 021 a 395 plusmn 042 b 948 000076

Simpson Index (1D) 713 plusmn 110 a 368 plusmn 042 b 6 plusmn 061 a 361 004Beta diversity (B = Sa) 641 plusmn 127 a 368 plusmn 043 a 985 plusmn 054 b 1645 213 times 10minus5

Note Different superscript letters mean significant variation at p lt 05 tested by post hoc Tukey HSD insignificant variations haveno superscript

35 Influence of Physiographic and Edaphic Variables on the Understory Species Composition

In the ordination analysis the permutation test revealed that the eigenvalues for thefirst axis and those for all canonical axes were significant (p lt 001) and indicated thatunderstory species composition was influenced by physiographic and edaphic variables(Figure 5) All three axes explained 65 of the cumulative variance and 308 of thevariance in the relationship among understory species composition (Table 4) Forwardselection of the RDA ordination revealed that seven variables (ie latitude elevationclay wilting point bulk density saturation and electric conductivity) were the significantinfluential among all 23 variables in relation to the understory vegetation of oak-dominatedforests (Table 5) Group I (Quercus balootndashPinus roxburghii community) which lies at anintermediate elevation among the three communities has lower quantities of organic matterLime Nitrogen and Potassium In contrast group II (Quercus semecarpifoliandashQuercus rubur)which lies at a higher elevation has higher quantities of these nutrients Moreover in theordination axes summery the first axis was significantly associated with total importancevalue index (r = 0639) potassium (r = 0363) and elevation (r = 0239) The second axiswas found in close relation with QIVI (r = minus0414) wilting point (r = minus0374) and clay(r = minus0369) While the third axis was found in close correlation with silt (r = 0381) lime(r = 0395) and available water (r = minus0377) (Table 6)

Table 4 Ordination analysis of the understory vegetation concerning physiographic andedaphic variables

Axis Axis 1 Axis 2 Axis 3

Eigenvalue 3327 2512 2396

Variance in species data

of variance explained 1242 941 9Cumulative explained 1241 2181 3082

Pearson Correlation Response-Pred 100 098 1Kendall Correlation Response-Pred 096 081 099

Symbol of steric show signidicant of the data

Table 5 Average values (Mean plusmn stand error) of the environmental variables ie topographic edaphic and soil in thethree community types (vegetation groups) separated by Wardrsquos agglomerative cluster analysis The three groups wereGroup I (Quercus balootndashPinus roxburghii) Group II (Quercus semecarpifoliandashQuercus robur) and Group III (QuercuslanatandashOlea ferruginea)

Environmental Variables CodeGroup I Group II Group III

F-Value p-ValueMean plusmn SE Mean plusmn SE Mean plusmn SE

Latitude () Lat 350 plusmn 012 a 349694 plusmn 019 b 3458 plusmn 0050 b 557 0009Longitude () Long 7228 plusmn 003 7229 plusmn 0023 7225 plusmn 0016 172 019Elevation (m) Elev 201775 plusmn 20523 a 22895 plusmn 24022 b 16594 plusmn 6448 a 487 0015

Slope () Slope 418 plusmn 181 4114 plusmn 255 3866 plusmn 114 115 033Clay () CLY 1637 plusmn 117 a 175 plusmn 22 a 1211 plusmn 102 b 465 001

Appl Sci 2021 11 11372 11 of 17

Table 5 Cont

Environmental Variables CodeGroup I Group II Group III

F-Value p-ValueMean plusmn SE Mean plusmn SE Mean plusmn SE

Silt () SLT 2444 plusmn 220 26 plusmn 36 2903 plusmn 274 066 052Sand () SND 5918 plusmn 266 5638 plusmn 342 5885 plusmn 308 017 084pH (15) pH 64 plusmn 012 66 plusmn 017 626 plusmn 013 125 030

Organic matter () OM 221 plusmn 078 462 plusmn 076 261 plusmn 054 292 007Lime () L 316 plusmn 052 406 plusmn 061 361 plusmn 038 066 052

Nitrogen (mgKg) N 012 plusmn 004 018 plusmn 003 016 plusmn 003 0503 060Phosphorus (mgKg) P 824 plusmn 063 744 plusmn 112 1294 plusmn 446 061 054Potassium (mgKg) K 14625 plusmn 2707 23342 plusmn 3752 18633 plusmn 2633 155 022

Wilting point (mLgm) WP 0114 plusmn 042 011 plusmn 009 009 plusmn 0004 436 002Field capacity (mLgm) FC 022 plusmn 061 023 plusmn 009 021 plusmn 007 131 028

Bulk density (gcm3) BD 14 plusmn 011 a 146 plusmn 002 a 152 plusmn 001 ab 343 004Saturation Point (0 kPa) SP 044 plusmn 052 a 044 plusmn 0008 a 042 plusmn 006 ab 341 004

Electrical Conductivity (mSm) EC 1241 plusmn 163 a 128 plusmn 003 a 2346 plusmn 280 b 544 001Available water () AW 010 plusmn 038 011 plusmn 0005 011 plusmn 004 046 063

Temperature minimum (C) Tpmi 1430 plusmn 192 1188 plusmn 037 1189 plusmn 017 213 014Temperature maximum (F) Tpma 2898 plusmn 875 2789 plusmn 533 3646 plusmn 575 211 014

Precipitation (mm) Preci 4984 plusmn 121 4916 plusmn 186 5184 plusmn 097 132 028Relative humidity () RH 4984 plusmn 122 4916 plusmn 187 5184 plusmn 098 132 028

Water Holding capacity () WHC 5212 plusmn 182 5482 plusmn 198 5347 plusmn 289 018 083

Note Different superscript letters mean significant variation at p lt 05 tested by post hoc Tukey HSD insignificant variations haveno superscript

Table 6 Results of the RDA showed correlation coefficients between the physiographic and edaphicvariables and the RDA axes and biplot scores of each variable on all the three axes

S No VariablesCorrelation Biplot Scores

Axis 1 Axis 2 Axis 3 Axis 1 Axis 2 Axis 3

1 Lat minus006 minus049 minus002 minus055 minus394 minus01552 Long minus019 018 minus022 minus181 148 minus1743 E 023 minus039 006 218 minus309 05184 ASP 008 minus009 016 074 minus074 1255 CLY 019 minus036 minus019 177 minus292 minus1486 SLT minus020 029 038 minus183 228 2957 SND 009 minus009 minus026 085 minus072 minus2038 pH 022 minus022 minus021 197 minus172 minus1639 OM 009 016 minus0003 088 126 minus002

10 L 021 017 minus039 196 132 minus30511 N 022 009 minus002 182 075 minus01812 P 0007 minus013 020 007 minus106 15613 K 036 minus004 minus012 331 minus031 minus09614 WP 018 minus037 minus018 166 minus296 minus13915 FC 003 minus013 009 027 minus105 07216 BD minus010 030 005 minus093 237 04217 SP 0104 minus031 minus005 095 minus238 minus03718 EC minus0121 043 013 minus111 341 100419 AW minus0176 025 038 minus160 197 29220 TIVI minus063 minus047 002 minus583 minus379 01721 QIVI 0162 minus041 013 148 minus328 09722 BA minus0025 minus011 022 minus023 minus088 15523 Dha 0112 minus022 minus017 102 minus178 minus12824 TpMi minus0246 minus009 minus004 minus224 minus077 minus03425 TpMa minus0185 001 032 minus168 011 24826 Preci 0259 minus009 003 236 minus071 02427 RH 0102 minus005 minus004 0935 minus037 minus03528 WHC minus0273 0005 0079 minus249 004 061

Note (p lt 005) (p lt 001)

Appl Sci 2021 11 11372 12 of 17Appl Sci 2021 11 x FOR PEER REVIEW 12 of 18

Figure 5 RDA ordination of physiographic and edaphic variables concerning stands and the understory vegetation Note

Blue square represent the species point in the ordination biplot St (Stand number)

Table 6 Results of the RDA showed correlation coefficients between the physiographic and edaphic

variables and the RDA axes and biplot scores of each variable on all the three axes

S No Variables Correlation Biplot Scores

Axis 1 Axis 2 Axis 3 Axis 1 Axis 2 Axis 3

1 Lat minus006 minus049 minus002 minus055 minus394 minus0155

2 Long minus019 018 minus022 minus181 148 minus174

3 E 023 minus039 006 218 minus309 0518

4 ASP 008 minus009 016 074 minus074 125

5 CLY 019 minus036 minus019 177 minus292 minus148

6 SLT minus020 029 038 minus183 228 295

7 SND 009 minus009 minus026 085 minus072 minus203

8 pH 022 minus022 minus021 197 minus172 minus163

9 OM 009 016 minus0003 088 126 minus002

10 L 021 017 minus039 196 132 minus305

11 N 022 009 minus002 182 075 minus018

12 P 0007 minus013 020 007 minus106 156

13 K 036 minus004 minus012 331 minus031 minus096

Figure 5 RDA ordination of physiographic and edaphic variables concerning stands and the understory vegetation NoteBlue square represent the species point in the ordination biplot St (Stand number)

4 Discussion

Vegetation is a group of plants growing together in a particular locality [43] and it mayalso be defined as a unit that retains its unique structure and physiognomic characteristicsin an adequately great and sufficient way to permit their distinction from other units [46]The understory plant species in the oak-dominated forests consist of 58 species belongingto 32 families at 30 different locations in the Hindukush ranges of Swat The physiognomyof the studied area was dominated by herbaceous growth form with 47 plant species (81)followed by shrubs with 10 plant species (17) and trees with individual plant species(2) Herbaceous dominancy and less tree percentage might be due to altitudinal andgeographical variations which indicates that the climatic factors favor the herbaceous floraOur findings are associated with researchers in allied neighboring and national regions inwhich the species reported were mostly herbaceous [4748] Among all families Fabaceaewas recorded as the leading family with eight plant species followed by Asteraceae andLamiaceae with seven species each For instance several researchers [532ndash343846] forinstance [31] have documented Asteraceae and Fabaceae as the two most important fami-lies While other researchers [38] cited Lamiaceae and Rosaceae and [48] cited LamiaceaeMoraceae and Asteraceae as dominant plant families from Darra Adam Khel KP Pakistan

Appl Sci 2021 11 11372 13 of 17

Plant life-forms and vegetation are indicators of the climate [6] According to Meher-Homji [49] life-forms are reflective of the bioclimates of an area Raunkiaer [6] designedthree major phytoclimates based on life-form spectra on the earth It includes phanerophyticclimate for the tropics therophytic for the xeric environments and hemicryptophytic forthe cold temperate region The present study identified seven different life-form classes inthe study area The most dominant life-form was hemicryptophytes with 19 species (33)followed by nanophanerophytes with 15 species (26) and therophytes with 13 species(22) Hemicryptophytes usually prevail in open physiognomies while phanerophytesare mainly in closed ones [5051] Biological spectra are important in comparing geographyand habitats and might change due to biotic influences viz grazing human activities andclimatic changes [52ndash54] Hemicryptophytes lose their aboveground parts during mostsummer and winter months while therophytes remain seeded to avoid summer droughtand cold winter stresses

Furthermore the flora of the study area is under anthropogenic pressure in the formof overgrazing and deforestation by nomadic and native people Nasir and Sultan [55]reported a similar finding from District Chakwal where therophytes were the dominantbiological spectra A community that therophytes dominate can be a characteristic fea-ture of a highly disturbed area under anthropogenic pressure [4854] In addition [56]reported therophytes as the dominant plant species of the rangeland district Tank Pak-istan and [57] assessed that therophytes is the leading life-form of Lahor District SwabiPakistan showing that the results of the current study are in compliance with the findingsof several other studies

Results of leaf size spectra trait revealed that species with microphyllous leaves domi-nated the area (with 24 species 41) followed by nanophylls (17 species 29) leptophylls(11 species 19) and mesophyll (5 species 9) Nonetheless 2 with megaphyllousleaf size was also recorded Microphyllous leaf size class is normally the characteristicfeature of meadow plant species while leptophylls and nanophylls are illustrative of hotdeserts [754] Comparable outcomes where microphylls and nanophylls overwhelmedthe vegetation and were reported in the work of researchers [7] and [45] where the authorslinked these two leaf size classes with the physiognomies of mild ranges A high rate ofmicrophylls may be identified with cool atmospheres of the sub-elevated and snowcappedareas Here as well the top layer was less settled containing a slim sheet that is notconclusive about the entrance of roots Microphyllous and nanophyllous leaves specieswere inexhaustible because of the biological variety for this dry condition The presentresults concur with [58] who detailed that microphylls and nanophylls predominance inthe dry mild atmosphere of District Quetta Our inferences additionally uncovered that thehigh extent in leaf size class changes with increasing altitude and the rate of microphyllswas emphatically connected with this as well [5960]

Among the 58 species documented 43 plant species were found in association withgroup III clustered by applying Wardrsquos agglomerative clustering which indicates widesociability of the species in the studied oak-dominated forests Moreover the analysisreveals that B lycium (782) C arvensis (687) and A trichomanes (66) were the mostabundant species in group III Group II was less diverse in terms of understory speciesnumbering in total of 25 plant species In this group Calamintha vulgaris (L) H KarstDryopteris stewartii Fraser-Jenk and Plantago lanceolata L were dominant (115 934 and986 respectively) Plant species in the understory with varying degrees of resistance tothese factors prefer a specific forest type Since certain plant species are limited to a specificforest type the extinction of that forest could result in the extinction of certain understoryplants [2761]

According to a recent analysis the richness and diversity of understory species inoak forests differed greatly depending on canopy dominants Herbaceous species abun-dance and α-diversity were highest in the oaks forest but there was less heterogeneity(β-diversity) across sites and major groups These findings highlight the importance of oakforests in protecting habitat and plant composition in the understory vegetation An herb

Appl Sci 2021 11 11372 14 of 17

layer with higher species abundance and diversity in oak forests may be due to highersolar radiation on south-facing slopes which is better for herbaceous species [62ndash64]

Environmental variables such as geographic parameters and physiochemical soilcharacteristics are important in determining the community structure and composition [65]In particular latitude and altitude were found to vary significantly in the understory groupsClay particles in soil texture and bulk density saturation point and electrical conductivityvaried significantly in the understory vegetation Similarly in the same region [66] thesoil parameters in understory vegetation of Pinus wallichiana AB Jacks dominated foresthave been studied revealing that elevation slope and phosphorus are vital factors indetermining the understory vegetation An oak species Q rubur L was also reported asa major associated species Furthermore many other researchers from other parts of theworld have reported that edaphic factors can significantly affect the species compositionand species diversity in plant communities [1066ndash68]

Forward selection of the RDA ordination revealed that latitude elevation clay wiltingpoint bulk density saturation and electric conductivity were significantly influential indetermining the understory vegetation of oak-dominated forests These results followthe findings of many other previous studies [12596970] Ali and Begum [62] also in-vestigated the vegetation of Swat and determined congruent results by stating a strongrelationship between vegetation and edaphic factors Many other researchers worldwidehave recorded that soil characteristics matter more than canopy organisms in decidingunderstory vegetation [62ndash6470] The study of species composition analysis in the oak-dominated forest revealed a general pattern of variation in the community diversity andspecies composition A similar pattern of species composition was also reported by [65] inP wallachiana understory from the same region The species diversity was found to increasewith time as Beg and Mirza [29] reported only 36 understory species due to the increase inanthropogenic activities

5 Conclusions

The current study reveals that Swat oak forests have rich floristic diversity with domi-nance of the therophytic life-form and microphyllous leaf size class indicating sub-tropicaland moist temperate type climates The species diversity was observed to increase duringthe spring and summer seasons and decreased later in the autumn As the winter seasonapproaches the decline in diversity was observed associated with dry environmentalconditions slow growth rate and other climatic factors Nonetheless critical impactsof seasonal variation on life-forms and overall species diversity were evident Among58 species 43 plant species were associated with group III clustered by applying Wardrsquosagglomerative clustering indicating the wide sociability of the species in the studied oak-dominated forests The understory vegetation of these forests plays an important role inthe forest ecology of the region

Moreover the environmental and soil variables ie latitude elevation clay percent-age wilting point electrical conductivity and potassium (mgKg) affect the understoryvegetation In addition important overstory variables like Quercus IVI and Total IVI ofoverstory were also found to affect the understory vegetation in oak-dominated forestsFurther it is concluded that the area is vulnerable due to the pressure from the localinhabitants in the form of overgrazing and deforestation which may significantly affectthe understory vegetation This information is particularly important for the success ofefforts intended to prevent the loss of genetic diversity of species within these forestsby destroying their natural habitats Moreover it is imperative to conserve the arearsquosbiodiversity and provide alternative means of livelihood for the local communities thatmay allow sustainable utilization and conservation of the invaluable biodiversity of thisarea for future generations

Appl Sci 2021 11 11372 15 of 17

Author Contributions The research work was designed and supervised by NK AR carried outthe field and laboratory work data analysis and manuscript writing RU also contributed tomanuscript writing and data collection KA DAJ and MEHK provided valuable informationand comments on the initial draft and refine the text in addition to language editing and data analysisIUR provided valuable suggestions during the write-up process and data analysis All authorshave read and agreed to the published version of the manuscript

Funding The research was conducted as a PhD project and did not receive support from anyfunding agency

Institutional Review Board Statement Not applicable

Informed Consent Statement Not applicable

Data Availability Statement All the data analyzedgenerated are included and available inthis manuscript

Acknowledgments We express our gratitude towards the Master students enrolled in the Depart-ment of Botany and the people of Malakand Division who helped with the fieldwork for this projectWe thank Achim Braumluning (Institute of Geography Department of Geography and GeosciencesFriedrich-Alexander-University (FAU) Erlangen-Nuremberg Erlangen Germany) for insightfulcomments that substantially improved the early version We also acknowledged the anonymous re-viewers and editors of the Applied Sciences journal for their valuable comment and language editing

Conflicts of Interest We hereby declare that all the authors have participated in this study and thedevelopment of the manuscript All the authors have read the final version and consent for the articleto be published in the Applied Sciences

References1 Musarella CM Mendoza-Fernaacutendez AJ Mota JF Alessandrini JFMA Bacchetta G Brullo GBS Caldarella O

Ciaschetti OCG Conti F Di Martino FCL et al Checklist of gypsophilous vascular flora in Italy Phyto Keys 2018 103 61ndash82[CrossRef] [PubMed]

2 Perrino EV Signorile G Checklist of the vascular flora from the Monopoli coast (Apulia) Ital Bot 2009 41 263ndash2793 Shah M Farrukh HSyed NMSImran AHumaira W Life Form And Floristic Characteristics Along Altitudinal Gradient Of

Humid Temperate Forests Located In Remote Area Of Pakistan Glob J Biodivers Sci Manag 2013 3 276ndash2814 Rafaqat M An Annotated Checklist of Amphibians and Reptiles of Margalla Hills National Park Pakistan Pak J Zool 2011 43

1041ndash10485 Shimwell DW Festuco-Brometea Br-Bl amp R Tx 1943 in the British isles The Phytogeography and Phytosociology of Limestone

Grasslands Part I (A) General Introduction(B) Xerobromion in England Vegetatio 1971 23 1ndash276 Raunkiaer C The Life Forms of Plants and Statistical Plant Geography Being the Collected Papers of C Raunkiaer In The Life

Forms of Plants and Statistical Plant Geography Being the Collected Papers of C Raunkiaer Clarendon Press Oxford UK 19347 Oosting HJ Hess DW Microclimate and a relic stand of Tsuga canadensis in the lower piedmont of North Carolina Ecology

1956 37 28ndash39 [CrossRef]8 Bailey IW Sinnott EW A botanical index of Cretaceous and Tertiary climates Science 1915 41 831ndash834 [CrossRef]9 Cain SA De Oliveira Castro GM Manual of Vegetation Analysis Haper and Row New York NY USA 195910 Augusto L Dupouey JL Ranger J Effects of tree species on understory vegetation and environmental conditions in temperate

forests Ann For Sci 2003 60 823ndash831 [CrossRef]11 Gracia M Montaneacute F Piqueacute J Retana J Overstory structure and topographic gradients determining diversity and abundance

of understory shrub species in temperate forests in central Pyrenees (NE Spain) For Ecol Manag 2007 242 391ndash397 [CrossRef]12 Gilliam FS The ecological significance of the herbaceous layer in temperate forest ecosystems Bioscience 2007 57 845ndash858

[CrossRef]13 Messier C Parent S Bergeron Y Effects of overstory and understory vegetation on the understory light environment in mixed

boreal forests J Veg Sci 1998 9 511ndash520 [CrossRef]14 Nilsson MC Wardle DA Understory vegetation as a forest ecosystem driver Evidence from the northern Swedish boreal

forest Front Ecol Environ 2005 3 421ndash428 [CrossRef]15 Bartels SF Chen HYH Is understory plant species diversity driven by resource quantity or resource heterogeneity Ecology

2010 91 1931ndash1938 [CrossRef] [PubMed]16 Dauber J Hirsch M Simmering D Waldhardt R Otte A Wolters V Landscape structure as an indicator of biodiversity

Matrix effects on species richness Agric Ecosyst Environ 2003 98 321ndash329 [CrossRef]17 Duguid MC Frey BR Ellum DS Kelty M Ashton MS The influence of ground disturbance and gap position on understory

plant diversity in upland forests of southern New England For Ecol Manag 2013 303 148ndash159 [CrossRef]

Appl Sci 2021 11 11372 5 of 17

ordination having variance of 19 Ms-Excel 2010 was used for data tabulation and graphicpresentation while SPSS version 22 was used for statistical analysis The significance ofthe variables was tested at p lt 005 In addition post hoc honestly significant differences(HSD) test was used for variation between the groups

3 Results31 Understory Species Composition

A total number of 58 understory plant species belonging to 32 families was identifiedat 30 different locations in the Hindukush ranges of Swat The physiognomy was domi-nated by herbaceous growth form with 47 plant species (81) followed by shrubs with10 (17) and trees with a single plant species (2) Herbaceous dominancy may be due toaltitudinal and geographical variations indicating the herbaceous florarsquos climatic factorsAmong the families Fabaceae was the leading family with eight plant species followed byAsteraceae and Lamiaceae with seven species each Further seven families (ie Amaran-thaceae Malvaceae Poaceae Plantaginaceae Polygonaceae Pteridaceae and Rosaceae)were recorded with two plant species each The remaining 22 families are represented byindividual species (Table 1)

Table 1 List of the plant species with the family names growth formhabit chorotype life-form and leaf size classes thatwere recorded in understory vegetation of oak-dominated forests of Swat Pakistan

Taxon Family Habit Chorotype Life-Form Leaf Size

Achyranthes aspera L Amaranthaceae Herb Plurireg Th NAdiantum venustum D Don Pteridaceae Herb Cosm G N

Ajuga bracteosa Wall ex Benth Lamiaceae Herb Unireg H MiAmaranthus viridis L Amaranthaceae Herb Cosm Th Mi

Arabidopsis thaliana (L) Heynh Brassicaceae Herb Cosm Th LArenaria serpyllifolia L Caryophyllaceae Herb Cosm Th NArtemisia vulgaris L Asteraceae Herb Plurireg Th N

Asplenium trichomanes L Aspleniaceae Herb Bireg H NAstragalus grahamianus Benth Fabaceae Herb Unireg Ch L

Atropa acuminata Royle ex Lindl Solanaceae Herb Plurireg G MiBerberis lycium Royle Berberidaceae Shrub Unireg NPh L

Bidens cernua L Asteraceae Herb Bireg H MiBuddleja asiatica Lour Scrophulariaceae Shrub Cosm NPh Mi

Calamintha vulgaris (L) H Karst Lamiaceae Herb Plurireg Th NChenopodium album L Chenopodiaceae Herb Cosm H NConvolvulus arvensis L Convolvulaceae Herb Cosm H NErigeron canadensis L Asteraceae Herb Cosm Th L

Cynodon dactylon (L) Pers Poaceae Herb Plurireg H LDaphne mucronata Royle Thymelaeaceae Shrub Bireg NPh N

Dioscorea deltoidea Wall ex Griseb Dioscoreaceae Herb Unireg H MiDodonaea viscosa Jacq Sapindaceae Shrub Cosm NPh Mi

Dryopteris stewartii Fraser-Jenk Dryopteridaceae Herb Bireg G MeElaeagnus angustifolia L Elaeagnaceae Shrub Bireg NPh MiFestuca gigantea (L) Vill Poaceae Herb Bireg G LFragaria indica Andrews Rosaceae Herb Plurireg H NGalium asperifolium Wall Rubiaceae Herb Unireg Th L

Hibiscus syriacus L Malvaceae Shrub Plurireg NPh MiIndigofera gerardiana Graham ex Baker Fabaceae Herb Unireg NPh NIndigofera heterantha Wall ex Brandis Fabaceae Herb Unireg NPh L

Isodon rugosus (Wall ex Benth) Codd Lamiaceae Herb Unireg NPh MiJusticia adathoda L Lamiaceae Herb Plurireg NPh MeLamium album L Lamiaceae Herb Unireg Th Mi

Lespedeza juncea (L f) Pers Fabaceae Herb Unireg H NLotus corniculatus L Fabaceae Herb Bireg H MiMalva neglecta Wallr Malvaceae Herb Unireg H MiMedicago lupulina L Fabaceae Herb Plurireg Ch N

Appl Sci 2021 11 11372 6 of 17

Table 1 Cont

Taxon Family Habit Chorotype Life-Form Leaf Size

Myrsine africana L Primulaceae Shrub Bireg NPh LOriganum vulgare L Lamiaceae Herb Unireg Th N

Otostegia limbata (Benth) Boiss Lamiaceae Herb Unireg NPh LOxytropis mollis Royle ex Benth Fabaceae Herb Unireg H L

Plantago lanceolata L Plantiganaceae Herb Plurireg H MiPlantago major L Plantaginaceae Herb Plurireg H Mi

Polygonatum verticillatum (L) All Asparagaceae Herb Plurireg Th NPteris cretica L Pteridaceae Herb Plurireg G Mi

Ranunculus laetus Salisb Ranunculaceae Herb Unireg H MeRosa webbiana Wall ex Royle Rosaceae Herb Plurireg NPh NRumex denticulatus K Koch Polygonaceae Herb Bireg H Me

Rumex nepalensis Spreng Polygonaceae Herb Bireg H MeSarcococca saligna (DDon) MuumlllArg Buxaceae Shrub Bireg NPh Mi

Smilax lanceolata L Smilacaceae Herb Bireg L MiSolidago virgaurea L Asteraceae Herb Unireg H Mi

Tagetes minuta L Asteraceae Herb Bireg Th MiTaraxacum officinale (L) Weber ex

FHWigg Asteraceae Herb Cosm H Mi

Trifolium repens L Fabaceae Herb Cosm G NViburnum grandiflorum Wall ex DC Viburnaceae Shrub Unireg NPh Ma

Viola serpens Wall ex Ging Violaceae Shrub Plurireg G MiYoungia japonica (L) DC Asteraceae Herb Cosm Th Mi

Zanthoxylum armatum DC Rutaceae Tree Cosm MPh Mi

Plurireg (Pluriregional) Unireg (Uniregional) Cosm (Cosmopolitan) Bireg (Biregional) Th (Therophyte) G (Geophytes) NPh (Nano-phanerophyte) H (Hemicryptophyt) MPh (Microphanerophytes) Ch (Chamaephyte) Mi (Microphyllous) Ma (Megaphyllous) N(Nanophyllous) L (Leptophyllous) Acronyms were assigned by following Shehata [45] except Raunkiaer life-form

The present study identified seven different life-form classes in the study area (Figure 2)The most dominant life-form was hemicryptophytes with 19 species (33) followedby nanophanerophytes with 15 species (26) therophytes with 13 species (22) andgeophytes with 7 species (12) Two species of chamaephytes (3) and one species (2)of nanophanerophytes and liana were also recorded (Table 1)

Appl Sci 2021 11 x FOR PEER REVIEW 7 of 18

Figure 2 Life-form classes of the plant species recorded in the understory vegetation of oak-domi-

nated forests of Swat Pakistan

32 Leaf Size Spectra

Results of leaf size spectra trait revealed that species with microphyllous leaves dom-

inated the area with 24 species (41) followed by nanophyll 17 species (29) leptophyll

11 species (19) and mesophyll 5 species (9) (Figure 3) Single species (2) with meg-

aphyllous leaf size was also recorded A high rate of microphylls may be identified within

the cool environment of the sub-elevated and snowcapped areas Here the top layer was

less settled it contained a slim sheet that may deny them the entrance of roots The micro-

phyllous and nanophyllous leaves species were inexhaustible because of the biological

variety for this dry condition

Figure 3 Leaf size classes of the plant species recorded in the understory vegetation of oak-domi-

nated forests of Swat Pakistan

The chorotype of the species varies from uniregional to cosmopolitan ie 22 were

cosmopolitan 26 pluriregional 23 bioregional and 29 were uniregional

26

33

22

12

3 2 2

Life forms

Nanophanerophytes

Hemicryptophytes

Therophytes

Geophytes

Chamaephytes

Microphanerophytes

Lianas

19

2941

9

2

Leaf size class

Leptophylls

Nanophylls

Microphylls

Mesophylls

Megaphylls

Figure 2 Life-form classes of the plant species recorded in the understory vegetation of oak-dominated forests of Swat Pakistan

Appl Sci 2021 11 11372 7 of 17

32 Leaf Size Spectra

Results of leaf size spectra trait revealed that species with microphyllous leaves domi-nated the area with 24 species (41) followed by nanophyll 17 species (29) leptophyll11 species (19) and mesophyll 5 species (9) (Figure 3) Single species (2) with mega-phyllous leaf size was also recorded A high rate of microphylls may be identified withinthe cool environment of the sub-elevated and snowcapped areas Here the top layer wasless settled it contained a slim sheet that may deny them the entrance of roots The mi-crophyllous and nanophyllous leaves species were inexhaustible because of the biologicalvariety for this dry condition

Appl Sci 2021 11 x FOR PEER REVIEW 7 of 18

Figure 2 Life-form classes of the plant species recorded in the understory vegetation of oak-domi-

nated forests of Swat Pakistan

32 Leaf Size Spectra

Results of leaf size spectra trait revealed that species with microphyllous leaves dom-

inated the area with 24 species (41) followed by nanophyll 17 species (29) leptophyll

11 species (19) and mesophyll 5 species (9) (Figure 3) Single species (2) with meg-

aphyllous leaf size was also recorded A high rate of microphylls may be identified within

the cool environment of the sub-elevated and snowcapped areas Here the top layer was

less settled it contained a slim sheet that may deny them the entrance of roots The micro-

phyllous and nanophyllous leaves species were inexhaustible because of the biological

variety for this dry condition

Figure 3 Leaf size classes of the plant species recorded in the understory vegetation of oak-domi-

nated forests of Swat Pakistan

The chorotype of the species varies from uniregional to cosmopolitan ie 22 were

cosmopolitan 26 pluriregional 23 bioregional and 29 were uniregional

26

33

22

12

3 2 2

Life forms

Nanophanerophytes

Hemicryptophytes

Therophytes

Geophytes

Chamaephytes

Microphanerophytes

Lianas

19

2941

9

2

Leaf size class

Leptophylls

Nanophylls

Microphylls

Mesophylls

Megaphylls

Figure 3 Leaf size classes of the plant species recorded in the understory vegetation of oak-dominatedforests of Swat Pakistan

The chorotype of the species varies from uniregional to cosmopolitan ie 22 werecosmopolitan 26 pluriregional 23 bioregional and 29 were uniregional

33 Understory Classification

A total of 58 plant species were recorded as associates in the understory vegeta-tion and clustered into three major groups by applying Wardrsquos agglomerative clustering(Figure 4 and Table 2) Among 58 species 43 plant species were found in association withgroup III clearly indicating the speciesrsquo wide sociability in the studied oak-dominatedforests Moreover the analysis reveals that IVI of Berberis lycium Royle (782) Convolvulusarvensis L (687) and Asplenium trichomanes L (66) were the most abundant species ingroup III Group II was recorded intermediately diverse in understory species having25 plant species with Calamintha vulgaris (L) H Karst Dryopteris stewartii Fraser-Jenkand Plantago lanceolata L as the dominant associates having IVI of 115 934 and 986respectively The results revealed group I as the less diverse in terms of species (18 species)and B lycium having IVI of 986 A trichomanes (914) and Indigofera heterantha Wall exBrandis (893) were the most abundant species

Appl Sci 2021 11 11372 8 of 17

Appl Sci 2021 11 x FOR PEER REVIEW 8 of 18

33 Understory Classification

A total of 58 plant species were recorded as associates in the understory vegetation

and clustered into three major groups by applying Wardrsquos agglomerative clustering (Fig-

ure 4 and Table 2) Among 58 species 43 plant species were found in association with

group III clearly indicating the speciesrsquo wide sociability in the studied oak-dominated

forests Moreover the analysis reveals that IVI of Berberis lycium Royle (782) Convolvulus

arvensis L (687) and Asplenium trichomanes L (66) were the most abundant species in

group III Group II was recorded intermediately diverse in understory species having 25

plant species with Calamintha vulgaris (L) H Karst Dryopteris stewartii Fraser-Jenk and

Plantago lanceolata L as the dominant associates having IVI of 115 934 and 986 respec-

tively The results revealed group I as the less diverse in terms of species (18 species) and

B lycium having IVI of 986 A trichomanes (914) and Indigofera heterantha Wall ex Brandis

(893) were the most abundant species

Figure 4 Cluster dendrogram classifying understory vegetation into three distinct groups Note G

(Group) St (Stand)

Table 2 Understory flora associated with oak-dominated forest recorded in the three clusters separated by Wardrsquos ag-

glomerative clustering procedure

Species Name Code Cluster I Cluster II Cluster III

M plusmn SE M plusmn SE M plusmn SE

Achyranthes aspera L As 241 plusmn 241 - -

Adiantum venustum D Don Av - - 077 plusmn 077

Ajuga bracteosa Wall ex Benth Ab 387 plusmn 265 - -

Amaranthus viridis L Am 510 plusmn 323 - 241 plusmn 144

Arabidopsis thaliana (L) Heynh At - - 116 plusmn 079

Arenaria serpyllifolia L Am - - 053 plusmn 053

Artimisia vulgaris L Av 72 plusmn 471 - -

Figure 4 Cluster dendrogram classifying understory vegetation into three distinct groups NoteG (Group) St (Stand)

Table 2 Understory flora associated with oak-dominated forest recorded in the three clusters separated by Wardrsquosagglomerative clustering procedure

Species Name CodeCluster I Cluster II Cluster III

M plusmn SE M plusmn SE M plusmn SE

Achyranthes aspera L As 241 plusmn 241 - -Adiantum venustum D Don Av - - 077 plusmn 077

Ajuga bracteosa Wall ex Benth Ab 387 plusmn 265 - -Amaranthus viridis L Am 510 plusmn 323 - 241 plusmn 144

Arabidopsis thaliana (L) Heynh At - - 116 plusmn 079Arenaria serpyllifolia L Am - - 053 plusmn 053

Artimisia vulgaris L Av 72 plusmn 471 - -Asplenium trichomanes L As 914 plusmn 471 423 plusmn 423 66 plusmn 26

Astragalus grahamianus Benth Ag - - 053 plusmn 053Atropa acuminata Royle ex Lindl Aa 34 plusmn 346 - 242 plusmn 243

Berberis lycium Royle B 986 plusmn 549 766 plusmn 491 782 plusmn 354Bidens cernua L Bc - 171 plusmn 171 -

Buddleja asiatica Lour Ba 093 plusmn 093 - 169 plusmn 117Calamintha vulgaris (L) H Karst Cv - 115 plusmn 411 346 plusmn 166

Chenopodium album L Ca - 44 plusmn 442 -Convolvulus arvensis L Ca 25 plusmn 252 42 plusmn 274 687 plusmn 176Erigeron canadensis L Co 085 plusmn 085 - -

Cynodon dactylon (L) Pers Cd 7 plusmn 5 617 plusmn 617 488 plusmn 332Daphne mucronata Royle Dm 383 plusmn 383 - 194 plusmn 134

Dioscorea deltoidea Wall ex Griseb Dd 183 plusmn 183 - -Dodonaea viscosa Jacq Do 142 plusmn 142 - -

Dryopteris stewartii Fraser-Jenk Ds - 986 plusmn 986 -Elaeagnus angustifolia L Ea 23 plusmn 23 - -Festuca gigantea (L) Vill Fg - - 046 plusmn 046

Appl Sci 2021 11 11372 9 of 17

Table 2 Cont

Species Name CodeCluster I Cluster II Cluster III

M plusmn SE M plusmn SE M plusmn SE

Fragaria indica Andrews Fi - 271 plusmn 271 553 plusmn 222Galium asperifolium Wall Ga 436 plusmn 436 - 134 plusmn 134

Hibiscus syriacus L Hs - - 06 plusmn 062Indigofera gerardiana Graham ex Baker Ig - - 365 plusmn 286Indigofera heterantha Wall ex Brandis Ih 893 plusmn 893 - -Isodon rugosus (Wall ex Benth) Codd Ir - 82 plusmn 82 -

justica adathoda L Ja - - 196 plusmn 145Lamium album L La - - 053 plusmn 053

Lespedeza juncea (L f) Pers Lj 502 plusmn 502 - 291 plusmn 291Lotus corniculatus L Lc 25 plusmn 25 - 252 plusmn 157Malva neglecta Wallr Mn - - 106 plusmn 106Medicago lupulina L Ml - - 121 plusmn 121Myrsine africana L Ma 45 plusmn 37 185 plusmn 185 596 plusmn 253

Origanum vulgare L Ov - 26 plusmn 268 -Otostegia limbata (Benth) Boiss Ol - - 160 plusmn 113Oxytropis mollis Royle ex Benth Om 363 plusmn 363 171 plusmn 171 336 plusmn 197

Plantago lanceolata L Pl 23 plusmn 23 934 plusmn 615 605 plusmn 329Plantago major L Pm - 59 plusmn 4 046 plusmn 046

Polygonatum verticillatum (L) All Pv - 171 plusmn 171 -Pteris cretica L Pc - - 167 plusmn 118

Ranunculus laetus Salisb Rl - - 093 plusmn 093Rosa webbiana Wall ex Royle Rw - - -Rumex denticulatus K Koch Ru - - 449 plusmn 257

Rumex nepalensis Spreng Rn - 357 plusmn 357 053 plusmn 053Sarcococca saligna (DDon) MuumlllArg Ss - - 053 plusmn 053

Smilax lanceolata L Sl 1 plusmn 12 - 308 plusmn 179Solidago virgaurea L Sv - - 053 plusmn 053

Tagetes minuta L Tg 502 plusmn 502 - 121 plusmn 121Taraxacum officinale (L) Weber ex

FHWigg To - - 06 plusmn 061

Trifolium repens L Tr - - 136 plusmn 095Viburnum grandiflorum Wall ex DC Vg - - 228 plusmn 228

Viola serpens Wall ex Ging Vs - - 135 plusmn 094Youngia japonica (L) DC Yj - 27 plusmn 272 -

Zanthoxylum armatum DC Za - - 106 plusmn 106

Note - Represent absence of specie in particular group

34 Understory Species Diversity and Richness

Significant differences in species richness (p lt 0015) ShannonndashWiener Margalef(p lt 000076) Simpson (p lt 0040) and Beta indexes were detected among three majorgroups of the understory layer of oak-dominated forests (Table 3) Nonetheless Pielousevenness was found non-significantly different (p gt 005) among the three major groups ofunderstory vegetation Group III had the highest species richness (103) α-diversity (274)and β-diversity (985) and the highest value of Margalef index (395) On the contrary thegroup I had the highest Pielous and Simpson index values with 097 and 713 respectively(Table 3)

Appl Sci 2021 11 11372 10 of 17

Table 3 Species richness and diversity indexes of oak-dominated forests of Swat Pakistan

IndexesGroup I Group II Group III

F pMean plusmn SE Mean plusmn SE Mean plusmn SE

Total number of Species (S) 587 plusmn 066 b 4 plusmn 037 a 1032 plusmn 15 b 485 0015ShannonndashWiener Index (H) 184 plusmn 019 a 13 plusmn 011 a 274 plusmn 020 b 1393 697 times 10minus5

Pielous Index (J) 097 plusmn 001 095 plusmn 001 093 plusmn 001 209 014Margalef Index (M) 29 plusmn 033 a 14 plusmn 021 a 395 plusmn 042 b 948 000076

Simpson Index (1D) 713 plusmn 110 a 368 plusmn 042 b 6 plusmn 061 a 361 004Beta diversity (B = Sa) 641 plusmn 127 a 368 plusmn 043 a 985 plusmn 054 b 1645 213 times 10minus5

Note Different superscript letters mean significant variation at p lt 05 tested by post hoc Tukey HSD insignificant variations haveno superscript

35 Influence of Physiographic and Edaphic Variables on the Understory Species Composition

In the ordination analysis the permutation test revealed that the eigenvalues for thefirst axis and those for all canonical axes were significant (p lt 001) and indicated thatunderstory species composition was influenced by physiographic and edaphic variables(Figure 5) All three axes explained 65 of the cumulative variance and 308 of thevariance in the relationship among understory species composition (Table 4) Forwardselection of the RDA ordination revealed that seven variables (ie latitude elevationclay wilting point bulk density saturation and electric conductivity) were the significantinfluential among all 23 variables in relation to the understory vegetation of oak-dominatedforests (Table 5) Group I (Quercus balootndashPinus roxburghii community) which lies at anintermediate elevation among the three communities has lower quantities of organic matterLime Nitrogen and Potassium In contrast group II (Quercus semecarpifoliandashQuercus rubur)which lies at a higher elevation has higher quantities of these nutrients Moreover in theordination axes summery the first axis was significantly associated with total importancevalue index (r = 0639) potassium (r = 0363) and elevation (r = 0239) The second axiswas found in close relation with QIVI (r = minus0414) wilting point (r = minus0374) and clay(r = minus0369) While the third axis was found in close correlation with silt (r = 0381) lime(r = 0395) and available water (r = minus0377) (Table 6)

Table 4 Ordination analysis of the understory vegetation concerning physiographic andedaphic variables

Axis Axis 1 Axis 2 Axis 3

Eigenvalue 3327 2512 2396

Variance in species data

of variance explained 1242 941 9Cumulative explained 1241 2181 3082

Pearson Correlation Response-Pred 100 098 1Kendall Correlation Response-Pred 096 081 099

Symbol of steric show signidicant of the data

Table 5 Average values (Mean plusmn stand error) of the environmental variables ie topographic edaphic and soil in thethree community types (vegetation groups) separated by Wardrsquos agglomerative cluster analysis The three groups wereGroup I (Quercus balootndashPinus roxburghii) Group II (Quercus semecarpifoliandashQuercus robur) and Group III (QuercuslanatandashOlea ferruginea)

Environmental Variables CodeGroup I Group II Group III

F-Value p-ValueMean plusmn SE Mean plusmn SE Mean plusmn SE

Latitude () Lat 350 plusmn 012 a 349694 plusmn 019 b 3458 plusmn 0050 b 557 0009Longitude () Long 7228 plusmn 003 7229 plusmn 0023 7225 plusmn 0016 172 019Elevation (m) Elev 201775 plusmn 20523 a 22895 plusmn 24022 b 16594 plusmn 6448 a 487 0015

Slope () Slope 418 plusmn 181 4114 plusmn 255 3866 plusmn 114 115 033Clay () CLY 1637 plusmn 117 a 175 plusmn 22 a 1211 plusmn 102 b 465 001

Appl Sci 2021 11 11372 11 of 17

Table 5 Cont

Environmental Variables CodeGroup I Group II Group III

F-Value p-ValueMean plusmn SE Mean plusmn SE Mean plusmn SE

Silt () SLT 2444 plusmn 220 26 plusmn 36 2903 plusmn 274 066 052Sand () SND 5918 plusmn 266 5638 plusmn 342 5885 plusmn 308 017 084pH (15) pH 64 plusmn 012 66 plusmn 017 626 plusmn 013 125 030

Organic matter () OM 221 plusmn 078 462 plusmn 076 261 plusmn 054 292 007Lime () L 316 plusmn 052 406 plusmn 061 361 plusmn 038 066 052

Nitrogen (mgKg) N 012 plusmn 004 018 plusmn 003 016 plusmn 003 0503 060Phosphorus (mgKg) P 824 plusmn 063 744 plusmn 112 1294 plusmn 446 061 054Potassium (mgKg) K 14625 plusmn 2707 23342 plusmn 3752 18633 plusmn 2633 155 022

Wilting point (mLgm) WP 0114 plusmn 042 011 plusmn 009 009 plusmn 0004 436 002Field capacity (mLgm) FC 022 plusmn 061 023 plusmn 009 021 plusmn 007 131 028

Bulk density (gcm3) BD 14 plusmn 011 a 146 plusmn 002 a 152 plusmn 001 ab 343 004Saturation Point (0 kPa) SP 044 plusmn 052 a 044 plusmn 0008 a 042 plusmn 006 ab 341 004

Electrical Conductivity (mSm) EC 1241 plusmn 163 a 128 plusmn 003 a 2346 plusmn 280 b 544 001Available water () AW 010 plusmn 038 011 plusmn 0005 011 plusmn 004 046 063

Temperature minimum (C) Tpmi 1430 plusmn 192 1188 plusmn 037 1189 plusmn 017 213 014Temperature maximum (F) Tpma 2898 plusmn 875 2789 plusmn 533 3646 plusmn 575 211 014

Precipitation (mm) Preci 4984 plusmn 121 4916 plusmn 186 5184 plusmn 097 132 028Relative humidity () RH 4984 plusmn 122 4916 plusmn 187 5184 plusmn 098 132 028

Water Holding capacity () WHC 5212 plusmn 182 5482 plusmn 198 5347 plusmn 289 018 083

Note Different superscript letters mean significant variation at p lt 05 tested by post hoc Tukey HSD insignificant variations haveno superscript

Table 6 Results of the RDA showed correlation coefficients between the physiographic and edaphicvariables and the RDA axes and biplot scores of each variable on all the three axes

S No VariablesCorrelation Biplot Scores

Axis 1 Axis 2 Axis 3 Axis 1 Axis 2 Axis 3

1 Lat minus006 minus049 minus002 minus055 minus394 minus01552 Long minus019 018 minus022 minus181 148 minus1743 E 023 minus039 006 218 minus309 05184 ASP 008 minus009 016 074 minus074 1255 CLY 019 minus036 minus019 177 minus292 minus1486 SLT minus020 029 038 minus183 228 2957 SND 009 minus009 minus026 085 minus072 minus2038 pH 022 minus022 minus021 197 minus172 minus1639 OM 009 016 minus0003 088 126 minus002

10 L 021 017 minus039 196 132 minus30511 N 022 009 minus002 182 075 minus01812 P 0007 minus013 020 007 minus106 15613 K 036 minus004 minus012 331 minus031 minus09614 WP 018 minus037 minus018 166 minus296 minus13915 FC 003 minus013 009 027 minus105 07216 BD minus010 030 005 minus093 237 04217 SP 0104 minus031 minus005 095 minus238 minus03718 EC minus0121 043 013 minus111 341 100419 AW minus0176 025 038 minus160 197 29220 TIVI minus063 minus047 002 minus583 minus379 01721 QIVI 0162 minus041 013 148 minus328 09722 BA minus0025 minus011 022 minus023 minus088 15523 Dha 0112 minus022 minus017 102 minus178 minus12824 TpMi minus0246 minus009 minus004 minus224 minus077 minus03425 TpMa minus0185 001 032 minus168 011 24826 Preci 0259 minus009 003 236 minus071 02427 RH 0102 minus005 minus004 0935 minus037 minus03528 WHC minus0273 0005 0079 minus249 004 061

Note (p lt 005) (p lt 001)

Appl Sci 2021 11 11372 12 of 17Appl Sci 2021 11 x FOR PEER REVIEW 12 of 18

Figure 5 RDA ordination of physiographic and edaphic variables concerning stands and the understory vegetation Note

Blue square represent the species point in the ordination biplot St (Stand number)

Table 6 Results of the RDA showed correlation coefficients between the physiographic and edaphic

variables and the RDA axes and biplot scores of each variable on all the three axes

S No Variables Correlation Biplot Scores

Axis 1 Axis 2 Axis 3 Axis 1 Axis 2 Axis 3

1 Lat minus006 minus049 minus002 minus055 minus394 minus0155

2 Long minus019 018 minus022 minus181 148 minus174

3 E 023 minus039 006 218 minus309 0518

4 ASP 008 minus009 016 074 minus074 125

5 CLY 019 minus036 minus019 177 minus292 minus148

6 SLT minus020 029 038 minus183 228 295

7 SND 009 minus009 minus026 085 minus072 minus203

8 pH 022 minus022 minus021 197 minus172 minus163

9 OM 009 016 minus0003 088 126 minus002

10 L 021 017 minus039 196 132 minus305

11 N 022 009 minus002 182 075 minus018

12 P 0007 minus013 020 007 minus106 156

13 K 036 minus004 minus012 331 minus031 minus096

Figure 5 RDA ordination of physiographic and edaphic variables concerning stands and the understory vegetation NoteBlue square represent the species point in the ordination biplot St (Stand number)

4 Discussion

Vegetation is a group of plants growing together in a particular locality [43] and it mayalso be defined as a unit that retains its unique structure and physiognomic characteristicsin an adequately great and sufficient way to permit their distinction from other units [46]The understory plant species in the oak-dominated forests consist of 58 species belongingto 32 families at 30 different locations in the Hindukush ranges of Swat The physiognomyof the studied area was dominated by herbaceous growth form with 47 plant species (81)followed by shrubs with 10 plant species (17) and trees with individual plant species(2) Herbaceous dominancy and less tree percentage might be due to altitudinal andgeographical variations which indicates that the climatic factors favor the herbaceous floraOur findings are associated with researchers in allied neighboring and national regions inwhich the species reported were mostly herbaceous [4748] Among all families Fabaceaewas recorded as the leading family with eight plant species followed by Asteraceae andLamiaceae with seven species each For instance several researchers [532ndash343846] forinstance [31] have documented Asteraceae and Fabaceae as the two most important fami-lies While other researchers [38] cited Lamiaceae and Rosaceae and [48] cited LamiaceaeMoraceae and Asteraceae as dominant plant families from Darra Adam Khel KP Pakistan

Appl Sci 2021 11 11372 13 of 17

Plant life-forms and vegetation are indicators of the climate [6] According to Meher-Homji [49] life-forms are reflective of the bioclimates of an area Raunkiaer [6] designedthree major phytoclimates based on life-form spectra on the earth It includes phanerophyticclimate for the tropics therophytic for the xeric environments and hemicryptophytic forthe cold temperate region The present study identified seven different life-form classes inthe study area The most dominant life-form was hemicryptophytes with 19 species (33)followed by nanophanerophytes with 15 species (26) and therophytes with 13 species(22) Hemicryptophytes usually prevail in open physiognomies while phanerophytesare mainly in closed ones [5051] Biological spectra are important in comparing geographyand habitats and might change due to biotic influences viz grazing human activities andclimatic changes [52ndash54] Hemicryptophytes lose their aboveground parts during mostsummer and winter months while therophytes remain seeded to avoid summer droughtand cold winter stresses

Furthermore the flora of the study area is under anthropogenic pressure in the formof overgrazing and deforestation by nomadic and native people Nasir and Sultan [55]reported a similar finding from District Chakwal where therophytes were the dominantbiological spectra A community that therophytes dominate can be a characteristic fea-ture of a highly disturbed area under anthropogenic pressure [4854] In addition [56]reported therophytes as the dominant plant species of the rangeland district Tank Pak-istan and [57] assessed that therophytes is the leading life-form of Lahor District SwabiPakistan showing that the results of the current study are in compliance with the findingsof several other studies

Results of leaf size spectra trait revealed that species with microphyllous leaves domi-nated the area (with 24 species 41) followed by nanophylls (17 species 29) leptophylls(11 species 19) and mesophyll (5 species 9) Nonetheless 2 with megaphyllousleaf size was also recorded Microphyllous leaf size class is normally the characteristicfeature of meadow plant species while leptophylls and nanophylls are illustrative of hotdeserts [754] Comparable outcomes where microphylls and nanophylls overwhelmedthe vegetation and were reported in the work of researchers [7] and [45] where the authorslinked these two leaf size classes with the physiognomies of mild ranges A high rate ofmicrophylls may be identified with cool atmospheres of the sub-elevated and snowcappedareas Here as well the top layer was less settled containing a slim sheet that is notconclusive about the entrance of roots Microphyllous and nanophyllous leaves specieswere inexhaustible because of the biological variety for this dry condition The presentresults concur with [58] who detailed that microphylls and nanophylls predominance inthe dry mild atmosphere of District Quetta Our inferences additionally uncovered that thehigh extent in leaf size class changes with increasing altitude and the rate of microphyllswas emphatically connected with this as well [5960]

Among the 58 species documented 43 plant species were found in association withgroup III clustered by applying Wardrsquos agglomerative clustering which indicates widesociability of the species in the studied oak-dominated forests Moreover the analysisreveals that B lycium (782) C arvensis (687) and A trichomanes (66) were the mostabundant species in group III Group II was less diverse in terms of understory speciesnumbering in total of 25 plant species In this group Calamintha vulgaris (L) H KarstDryopteris stewartii Fraser-Jenk and Plantago lanceolata L were dominant (115 934 and986 respectively) Plant species in the understory with varying degrees of resistance tothese factors prefer a specific forest type Since certain plant species are limited to a specificforest type the extinction of that forest could result in the extinction of certain understoryplants [2761]

According to a recent analysis the richness and diversity of understory species inoak forests differed greatly depending on canopy dominants Herbaceous species abun-dance and α-diversity were highest in the oaks forest but there was less heterogeneity(β-diversity) across sites and major groups These findings highlight the importance of oakforests in protecting habitat and plant composition in the understory vegetation An herb

Appl Sci 2021 11 11372 14 of 17

layer with higher species abundance and diversity in oak forests may be due to highersolar radiation on south-facing slopes which is better for herbaceous species [62ndash64]

Environmental variables such as geographic parameters and physiochemical soilcharacteristics are important in determining the community structure and composition [65]In particular latitude and altitude were found to vary significantly in the understory groupsClay particles in soil texture and bulk density saturation point and electrical conductivityvaried significantly in the understory vegetation Similarly in the same region [66] thesoil parameters in understory vegetation of Pinus wallichiana AB Jacks dominated foresthave been studied revealing that elevation slope and phosphorus are vital factors indetermining the understory vegetation An oak species Q rubur L was also reported asa major associated species Furthermore many other researchers from other parts of theworld have reported that edaphic factors can significantly affect the species compositionand species diversity in plant communities [1066ndash68]

Forward selection of the RDA ordination revealed that latitude elevation clay wiltingpoint bulk density saturation and electric conductivity were significantly influential indetermining the understory vegetation of oak-dominated forests These results followthe findings of many other previous studies [12596970] Ali and Begum [62] also in-vestigated the vegetation of Swat and determined congruent results by stating a strongrelationship between vegetation and edaphic factors Many other researchers worldwidehave recorded that soil characteristics matter more than canopy organisms in decidingunderstory vegetation [62ndash6470] The study of species composition analysis in the oak-dominated forest revealed a general pattern of variation in the community diversity andspecies composition A similar pattern of species composition was also reported by [65] inP wallachiana understory from the same region The species diversity was found to increasewith time as Beg and Mirza [29] reported only 36 understory species due to the increase inanthropogenic activities

5 Conclusions

The current study reveals that Swat oak forests have rich floristic diversity with domi-nance of the therophytic life-form and microphyllous leaf size class indicating sub-tropicaland moist temperate type climates The species diversity was observed to increase duringthe spring and summer seasons and decreased later in the autumn As the winter seasonapproaches the decline in diversity was observed associated with dry environmentalconditions slow growth rate and other climatic factors Nonetheless critical impactsof seasonal variation on life-forms and overall species diversity were evident Among58 species 43 plant species were associated with group III clustered by applying Wardrsquosagglomerative clustering indicating the wide sociability of the species in the studied oak-dominated forests The understory vegetation of these forests plays an important role inthe forest ecology of the region

Moreover the environmental and soil variables ie latitude elevation clay percent-age wilting point electrical conductivity and potassium (mgKg) affect the understoryvegetation In addition important overstory variables like Quercus IVI and Total IVI ofoverstory were also found to affect the understory vegetation in oak-dominated forestsFurther it is concluded that the area is vulnerable due to the pressure from the localinhabitants in the form of overgrazing and deforestation which may significantly affectthe understory vegetation This information is particularly important for the success ofefforts intended to prevent the loss of genetic diversity of species within these forestsby destroying their natural habitats Moreover it is imperative to conserve the arearsquosbiodiversity and provide alternative means of livelihood for the local communities thatmay allow sustainable utilization and conservation of the invaluable biodiversity of thisarea for future generations

Appl Sci 2021 11 11372 15 of 17

Author Contributions The research work was designed and supervised by NK AR carried outthe field and laboratory work data analysis and manuscript writing RU also contributed tomanuscript writing and data collection KA DAJ and MEHK provided valuable informationand comments on the initial draft and refine the text in addition to language editing and data analysisIUR provided valuable suggestions during the write-up process and data analysis All authorshave read and agreed to the published version of the manuscript

Funding The research was conducted as a PhD project and did not receive support from anyfunding agency

Institutional Review Board Statement Not applicable

Informed Consent Statement Not applicable

Data Availability Statement All the data analyzedgenerated are included and available inthis manuscript

Acknowledgments We express our gratitude towards the Master students enrolled in the Depart-ment of Botany and the people of Malakand Division who helped with the fieldwork for this projectWe thank Achim Braumluning (Institute of Geography Department of Geography and GeosciencesFriedrich-Alexander-University (FAU) Erlangen-Nuremberg Erlangen Germany) for insightfulcomments that substantially improved the early version We also acknowledged the anonymous re-viewers and editors of the Applied Sciences journal for their valuable comment and language editing

Conflicts of Interest We hereby declare that all the authors have participated in this study and thedevelopment of the manuscript All the authors have read the final version and consent for the articleto be published in the Applied Sciences

References1 Musarella CM Mendoza-Fernaacutendez AJ Mota JF Alessandrini JFMA Bacchetta G Brullo GBS Caldarella O

Ciaschetti OCG Conti F Di Martino FCL et al Checklist of gypsophilous vascular flora in Italy Phyto Keys 2018 103 61ndash82[CrossRef] [PubMed]

2 Perrino EV Signorile G Checklist of the vascular flora from the Monopoli coast (Apulia) Ital Bot 2009 41 263ndash2793 Shah M Farrukh HSyed NMSImran AHumaira W Life Form And Floristic Characteristics Along Altitudinal Gradient Of

Humid Temperate Forests Located In Remote Area Of Pakistan Glob J Biodivers Sci Manag 2013 3 276ndash2814 Rafaqat M An Annotated Checklist of Amphibians and Reptiles of Margalla Hills National Park Pakistan Pak J Zool 2011 43

1041ndash10485 Shimwell DW Festuco-Brometea Br-Bl amp R Tx 1943 in the British isles The Phytogeography and Phytosociology of Limestone

Grasslands Part I (A) General Introduction(B) Xerobromion in England Vegetatio 1971 23 1ndash276 Raunkiaer C The Life Forms of Plants and Statistical Plant Geography Being the Collected Papers of C Raunkiaer In The Life

Forms of Plants and Statistical Plant Geography Being the Collected Papers of C Raunkiaer Clarendon Press Oxford UK 19347 Oosting HJ Hess DW Microclimate and a relic stand of Tsuga canadensis in the lower piedmont of North Carolina Ecology

1956 37 28ndash39 [CrossRef]8 Bailey IW Sinnott EW A botanical index of Cretaceous and Tertiary climates Science 1915 41 831ndash834 [CrossRef]9 Cain SA De Oliveira Castro GM Manual of Vegetation Analysis Haper and Row New York NY USA 195910 Augusto L Dupouey JL Ranger J Effects of tree species on understory vegetation and environmental conditions in temperate

forests Ann For Sci 2003 60 823ndash831 [CrossRef]11 Gracia M Montaneacute F Piqueacute J Retana J Overstory structure and topographic gradients determining diversity and abundance

of understory shrub species in temperate forests in central Pyrenees (NE Spain) For Ecol Manag 2007 242 391ndash397 [CrossRef]12 Gilliam FS The ecological significance of the herbaceous layer in temperate forest ecosystems Bioscience 2007 57 845ndash858

[CrossRef]13 Messier C Parent S Bergeron Y Effects of overstory and understory vegetation on the understory light environment in mixed

boreal forests J Veg Sci 1998 9 511ndash520 [CrossRef]14 Nilsson MC Wardle DA Understory vegetation as a forest ecosystem driver Evidence from the northern Swedish boreal

forest Front Ecol Environ 2005 3 421ndash428 [CrossRef]15 Bartels SF Chen HYH Is understory plant species diversity driven by resource quantity or resource heterogeneity Ecology

2010 91 1931ndash1938 [CrossRef] [PubMed]16 Dauber J Hirsch M Simmering D Waldhardt R Otte A Wolters V Landscape structure as an indicator of biodiversity

Matrix effects on species richness Agric Ecosyst Environ 2003 98 321ndash329 [CrossRef]17 Duguid MC Frey BR Ellum DS Kelty M Ashton MS The influence of ground disturbance and gap position on understory

plant diversity in upland forests of southern New England For Ecol Manag 2013 303 148ndash159 [CrossRef]

Appl Sci 2021 11 11372 6 of 17

Table 1 Cont

Taxon Family Habit Chorotype Life-Form Leaf Size

Myrsine africana L Primulaceae Shrub Bireg NPh LOriganum vulgare L Lamiaceae Herb Unireg Th N

Otostegia limbata (Benth) Boiss Lamiaceae Herb Unireg NPh LOxytropis mollis Royle ex Benth Fabaceae Herb Unireg H L

Plantago lanceolata L Plantiganaceae Herb Plurireg H MiPlantago major L Plantaginaceae Herb Plurireg H Mi

Polygonatum verticillatum (L) All Asparagaceae Herb Plurireg Th NPteris cretica L Pteridaceae Herb Plurireg G Mi

Ranunculus laetus Salisb Ranunculaceae Herb Unireg H MeRosa webbiana Wall ex Royle Rosaceae Herb Plurireg NPh NRumex denticulatus K Koch Polygonaceae Herb Bireg H Me

Rumex nepalensis Spreng Polygonaceae Herb Bireg H MeSarcococca saligna (DDon) MuumlllArg Buxaceae Shrub Bireg NPh Mi

Smilax lanceolata L Smilacaceae Herb Bireg L MiSolidago virgaurea L Asteraceae Herb Unireg H Mi

Tagetes minuta L Asteraceae Herb Bireg Th MiTaraxacum officinale (L) Weber ex

FHWigg Asteraceae Herb Cosm H Mi

Trifolium repens L Fabaceae Herb Cosm G NViburnum grandiflorum Wall ex DC Viburnaceae Shrub Unireg NPh Ma

Viola serpens Wall ex Ging Violaceae Shrub Plurireg G MiYoungia japonica (L) DC Asteraceae Herb Cosm Th Mi

Zanthoxylum armatum DC Rutaceae Tree Cosm MPh Mi

Plurireg (Pluriregional) Unireg (Uniregional) Cosm (Cosmopolitan) Bireg (Biregional) Th (Therophyte) G (Geophytes) NPh (Nano-phanerophyte) H (Hemicryptophyt) MPh (Microphanerophytes) Ch (Chamaephyte) Mi (Microphyllous) Ma (Megaphyllous) N(Nanophyllous) L (Leptophyllous) Acronyms were assigned by following Shehata [45] except Raunkiaer life-form

The present study identified seven different life-form classes in the study area (Figure 2)The most dominant life-form was hemicryptophytes with 19 species (33) followedby nanophanerophytes with 15 species (26) therophytes with 13 species (22) andgeophytes with 7 species (12) Two species of chamaephytes (3) and one species (2)of nanophanerophytes and liana were also recorded (Table 1)

Appl Sci 2021 11 x FOR PEER REVIEW 7 of 18

Figure 2 Life-form classes of the plant species recorded in the understory vegetation of oak-domi-

nated forests of Swat Pakistan

32 Leaf Size Spectra

Results of leaf size spectra trait revealed that species with microphyllous leaves dom-

inated the area with 24 species (41) followed by nanophyll 17 species (29) leptophyll

11 species (19) and mesophyll 5 species (9) (Figure 3) Single species (2) with meg-

aphyllous leaf size was also recorded A high rate of microphylls may be identified within

the cool environment of the sub-elevated and snowcapped areas Here the top layer was

less settled it contained a slim sheet that may deny them the entrance of roots The micro-

phyllous and nanophyllous leaves species were inexhaustible because of the biological

variety for this dry condition

Figure 3 Leaf size classes of the plant species recorded in the understory vegetation of oak-domi-

nated forests of Swat Pakistan

The chorotype of the species varies from uniregional to cosmopolitan ie 22 were

cosmopolitan 26 pluriregional 23 bioregional and 29 were uniregional

26

33

22

12

3 2 2

Life forms

Nanophanerophytes

Hemicryptophytes

Therophytes

Geophytes

Chamaephytes

Microphanerophytes

Lianas

19

2941

9

2

Leaf size class

Leptophylls

Nanophylls

Microphylls

Mesophylls

Megaphylls

Figure 2 Life-form classes of the plant species recorded in the understory vegetation of oak-dominated forests of Swat Pakistan

Appl Sci 2021 11 11372 7 of 17

32 Leaf Size Spectra

Results of leaf size spectra trait revealed that species with microphyllous leaves domi-nated the area with 24 species (41) followed by nanophyll 17 species (29) leptophyll11 species (19) and mesophyll 5 species (9) (Figure 3) Single species (2) with mega-phyllous leaf size was also recorded A high rate of microphylls may be identified withinthe cool environment of the sub-elevated and snowcapped areas Here the top layer wasless settled it contained a slim sheet that may deny them the entrance of roots The mi-crophyllous and nanophyllous leaves species were inexhaustible because of the biologicalvariety for this dry condition

Appl Sci 2021 11 x FOR PEER REVIEW 7 of 18

Figure 2 Life-form classes of the plant species recorded in the understory vegetation of oak-domi-

nated forests of Swat Pakistan

32 Leaf Size Spectra

Results of leaf size spectra trait revealed that species with microphyllous leaves dom-

inated the area with 24 species (41) followed by nanophyll 17 species (29) leptophyll

11 species (19) and mesophyll 5 species (9) (Figure 3) Single species (2) with meg-

aphyllous leaf size was also recorded A high rate of microphylls may be identified within

the cool environment of the sub-elevated and snowcapped areas Here the top layer was

less settled it contained a slim sheet that may deny them the entrance of roots The micro-

phyllous and nanophyllous leaves species were inexhaustible because of the biological

variety for this dry condition

Figure 3 Leaf size classes of the plant species recorded in the understory vegetation of oak-domi-

nated forests of Swat Pakistan

The chorotype of the species varies from uniregional to cosmopolitan ie 22 were

cosmopolitan 26 pluriregional 23 bioregional and 29 were uniregional

26

33

22

12

3 2 2

Life forms

Nanophanerophytes

Hemicryptophytes

Therophytes

Geophytes

Chamaephytes

Microphanerophytes

Lianas

19

2941

9

2

Leaf size class

Leptophylls

Nanophylls

Microphylls

Mesophylls

Megaphylls

Figure 3 Leaf size classes of the plant species recorded in the understory vegetation of oak-dominatedforests of Swat Pakistan

The chorotype of the species varies from uniregional to cosmopolitan ie 22 werecosmopolitan 26 pluriregional 23 bioregional and 29 were uniregional

33 Understory Classification

A total of 58 plant species were recorded as associates in the understory vegeta-tion and clustered into three major groups by applying Wardrsquos agglomerative clustering(Figure 4 and Table 2) Among 58 species 43 plant species were found in association withgroup III clearly indicating the speciesrsquo wide sociability in the studied oak-dominatedforests Moreover the analysis reveals that IVI of Berberis lycium Royle (782) Convolvulusarvensis L (687) and Asplenium trichomanes L (66) were the most abundant species ingroup III Group II was recorded intermediately diverse in understory species having25 plant species with Calamintha vulgaris (L) H Karst Dryopteris stewartii Fraser-Jenkand Plantago lanceolata L as the dominant associates having IVI of 115 934 and 986respectively The results revealed group I as the less diverse in terms of species (18 species)and B lycium having IVI of 986 A trichomanes (914) and Indigofera heterantha Wall exBrandis (893) were the most abundant species

Appl Sci 2021 11 11372 8 of 17

Appl Sci 2021 11 x FOR PEER REVIEW 8 of 18

33 Understory Classification

A total of 58 plant species were recorded as associates in the understory vegetation

and clustered into three major groups by applying Wardrsquos agglomerative clustering (Fig-

ure 4 and Table 2) Among 58 species 43 plant species were found in association with

group III clearly indicating the speciesrsquo wide sociability in the studied oak-dominated

forests Moreover the analysis reveals that IVI of Berberis lycium Royle (782) Convolvulus

arvensis L (687) and Asplenium trichomanes L (66) were the most abundant species in

group III Group II was recorded intermediately diverse in understory species having 25

plant species with Calamintha vulgaris (L) H Karst Dryopteris stewartii Fraser-Jenk and

Plantago lanceolata L as the dominant associates having IVI of 115 934 and 986 respec-

tively The results revealed group I as the less diverse in terms of species (18 species) and

B lycium having IVI of 986 A trichomanes (914) and Indigofera heterantha Wall ex Brandis

(893) were the most abundant species

Figure 4 Cluster dendrogram classifying understory vegetation into three distinct groups Note G

(Group) St (Stand)

Table 2 Understory flora associated with oak-dominated forest recorded in the three clusters separated by Wardrsquos ag-

glomerative clustering procedure

Species Name Code Cluster I Cluster II Cluster III

M plusmn SE M plusmn SE M plusmn SE

Achyranthes aspera L As 241 plusmn 241 - -

Adiantum venustum D Don Av - - 077 plusmn 077

Ajuga bracteosa Wall ex Benth Ab 387 plusmn 265 - -

Amaranthus viridis L Am 510 plusmn 323 - 241 plusmn 144

Arabidopsis thaliana (L) Heynh At - - 116 plusmn 079

Arenaria serpyllifolia L Am - - 053 plusmn 053

Artimisia vulgaris L Av 72 plusmn 471 - -

Figure 4 Cluster dendrogram classifying understory vegetation into three distinct groups NoteG (Group) St (Stand)

Table 2 Understory flora associated with oak-dominated forest recorded in the three clusters separated by Wardrsquosagglomerative clustering procedure

Species Name CodeCluster I Cluster II Cluster III

M plusmn SE M plusmn SE M plusmn SE

Achyranthes aspera L As 241 plusmn 241 - -Adiantum venustum D Don Av - - 077 plusmn 077

Ajuga bracteosa Wall ex Benth Ab 387 plusmn 265 - -Amaranthus viridis L Am 510 plusmn 323 - 241 plusmn 144

Arabidopsis thaliana (L) Heynh At - - 116 plusmn 079Arenaria serpyllifolia L Am - - 053 plusmn 053

Artimisia vulgaris L Av 72 plusmn 471 - -Asplenium trichomanes L As 914 plusmn 471 423 plusmn 423 66 plusmn 26

Astragalus grahamianus Benth Ag - - 053 plusmn 053Atropa acuminata Royle ex Lindl Aa 34 plusmn 346 - 242 plusmn 243

Berberis lycium Royle B 986 plusmn 549 766 plusmn 491 782 plusmn 354Bidens cernua L Bc - 171 plusmn 171 -

Buddleja asiatica Lour Ba 093 plusmn 093 - 169 plusmn 117Calamintha vulgaris (L) H Karst Cv - 115 plusmn 411 346 plusmn 166

Chenopodium album L Ca - 44 plusmn 442 -Convolvulus arvensis L Ca 25 plusmn 252 42 plusmn 274 687 plusmn 176Erigeron canadensis L Co 085 plusmn 085 - -

Cynodon dactylon (L) Pers Cd 7 plusmn 5 617 plusmn 617 488 plusmn 332Daphne mucronata Royle Dm 383 plusmn 383 - 194 plusmn 134

Dioscorea deltoidea Wall ex Griseb Dd 183 plusmn 183 - -Dodonaea viscosa Jacq Do 142 plusmn 142 - -

Dryopteris stewartii Fraser-Jenk Ds - 986 plusmn 986 -Elaeagnus angustifolia L Ea 23 plusmn 23 - -Festuca gigantea (L) Vill Fg - - 046 plusmn 046

Appl Sci 2021 11 11372 9 of 17

Table 2 Cont

Species Name CodeCluster I Cluster II Cluster III

M plusmn SE M plusmn SE M plusmn SE

Fragaria indica Andrews Fi - 271 plusmn 271 553 plusmn 222Galium asperifolium Wall Ga 436 plusmn 436 - 134 plusmn 134

Hibiscus syriacus L Hs - - 06 plusmn 062Indigofera gerardiana Graham ex Baker Ig - - 365 plusmn 286Indigofera heterantha Wall ex Brandis Ih 893 plusmn 893 - -Isodon rugosus (Wall ex Benth) Codd Ir - 82 plusmn 82 -

justica adathoda L Ja - - 196 plusmn 145Lamium album L La - - 053 plusmn 053

Lespedeza juncea (L f) Pers Lj 502 plusmn 502 - 291 plusmn 291Lotus corniculatus L Lc 25 plusmn 25 - 252 plusmn 157Malva neglecta Wallr Mn - - 106 plusmn 106Medicago lupulina L Ml - - 121 plusmn 121Myrsine africana L Ma 45 plusmn 37 185 plusmn 185 596 plusmn 253

Origanum vulgare L Ov - 26 plusmn 268 -Otostegia limbata (Benth) Boiss Ol - - 160 plusmn 113Oxytropis mollis Royle ex Benth Om 363 plusmn 363 171 plusmn 171 336 plusmn 197

Plantago lanceolata L Pl 23 plusmn 23 934 plusmn 615 605 plusmn 329Plantago major L Pm - 59 plusmn 4 046 plusmn 046

Polygonatum verticillatum (L) All Pv - 171 plusmn 171 -Pteris cretica L Pc - - 167 plusmn 118

Ranunculus laetus Salisb Rl - - 093 plusmn 093Rosa webbiana Wall ex Royle Rw - - -Rumex denticulatus K Koch Ru - - 449 plusmn 257

Rumex nepalensis Spreng Rn - 357 plusmn 357 053 plusmn 053Sarcococca saligna (DDon) MuumlllArg Ss - - 053 plusmn 053

Smilax lanceolata L Sl 1 plusmn 12 - 308 plusmn 179Solidago virgaurea L Sv - - 053 plusmn 053

Tagetes minuta L Tg 502 plusmn 502 - 121 plusmn 121Taraxacum officinale (L) Weber ex

FHWigg To - - 06 plusmn 061

Trifolium repens L Tr - - 136 plusmn 095Viburnum grandiflorum Wall ex DC Vg - - 228 plusmn 228

Viola serpens Wall ex Ging Vs - - 135 plusmn 094Youngia japonica (L) DC Yj - 27 plusmn 272 -

Zanthoxylum armatum DC Za - - 106 plusmn 106

Note - Represent absence of specie in particular group

34 Understory Species Diversity and Richness

Significant differences in species richness (p lt 0015) ShannonndashWiener Margalef(p lt 000076) Simpson (p lt 0040) and Beta indexes were detected among three majorgroups of the understory layer of oak-dominated forests (Table 3) Nonetheless Pielousevenness was found non-significantly different (p gt 005) among the three major groups ofunderstory vegetation Group III had the highest species richness (103) α-diversity (274)and β-diversity (985) and the highest value of Margalef index (395) On the contrary thegroup I had the highest Pielous and Simpson index values with 097 and 713 respectively(Table 3)

Appl Sci 2021 11 11372 10 of 17

Table 3 Species richness and diversity indexes of oak-dominated forests of Swat Pakistan

IndexesGroup I Group II Group III

F pMean plusmn SE Mean plusmn SE Mean plusmn SE

Total number of Species (S) 587 plusmn 066 b 4 plusmn 037 a 1032 plusmn 15 b 485 0015ShannonndashWiener Index (H) 184 plusmn 019 a 13 plusmn 011 a 274 plusmn 020 b 1393 697 times 10minus5

Pielous Index (J) 097 plusmn 001 095 plusmn 001 093 plusmn 001 209 014Margalef Index (M) 29 plusmn 033 a 14 plusmn 021 a 395 plusmn 042 b 948 000076

Simpson Index (1D) 713 plusmn 110 a 368 plusmn 042 b 6 plusmn 061 a 361 004Beta diversity (B = Sa) 641 plusmn 127 a 368 plusmn 043 a 985 plusmn 054 b 1645 213 times 10minus5

Note Different superscript letters mean significant variation at p lt 05 tested by post hoc Tukey HSD insignificant variations haveno superscript

35 Influence of Physiographic and Edaphic Variables on the Understory Species Composition

In the ordination analysis the permutation test revealed that the eigenvalues for thefirst axis and those for all canonical axes were significant (p lt 001) and indicated thatunderstory species composition was influenced by physiographic and edaphic variables(Figure 5) All three axes explained 65 of the cumulative variance and 308 of thevariance in the relationship among understory species composition (Table 4) Forwardselection of the RDA ordination revealed that seven variables (ie latitude elevationclay wilting point bulk density saturation and electric conductivity) were the significantinfluential among all 23 variables in relation to the understory vegetation of oak-dominatedforests (Table 5) Group I (Quercus balootndashPinus roxburghii community) which lies at anintermediate elevation among the three communities has lower quantities of organic matterLime Nitrogen and Potassium In contrast group II (Quercus semecarpifoliandashQuercus rubur)which lies at a higher elevation has higher quantities of these nutrients Moreover in theordination axes summery the first axis was significantly associated with total importancevalue index (r = 0639) potassium (r = 0363) and elevation (r = 0239) The second axiswas found in close relation with QIVI (r = minus0414) wilting point (r = minus0374) and clay(r = minus0369) While the third axis was found in close correlation with silt (r = 0381) lime(r = 0395) and available water (r = minus0377) (Table 6)

Table 4 Ordination analysis of the understory vegetation concerning physiographic andedaphic variables

Axis Axis 1 Axis 2 Axis 3

Eigenvalue 3327 2512 2396

Variance in species data

of variance explained 1242 941 9Cumulative explained 1241 2181 3082

Pearson Correlation Response-Pred 100 098 1Kendall Correlation Response-Pred 096 081 099

Symbol of steric show signidicant of the data

Table 5 Average values (Mean plusmn stand error) of the environmental variables ie topographic edaphic and soil in thethree community types (vegetation groups) separated by Wardrsquos agglomerative cluster analysis The three groups wereGroup I (Quercus balootndashPinus roxburghii) Group II (Quercus semecarpifoliandashQuercus robur) and Group III (QuercuslanatandashOlea ferruginea)

Environmental Variables CodeGroup I Group II Group III

F-Value p-ValueMean plusmn SE Mean plusmn SE Mean plusmn SE

Latitude () Lat 350 plusmn 012 a 349694 plusmn 019 b 3458 plusmn 0050 b 557 0009Longitude () Long 7228 plusmn 003 7229 plusmn 0023 7225 plusmn 0016 172 019Elevation (m) Elev 201775 plusmn 20523 a 22895 plusmn 24022 b 16594 plusmn 6448 a 487 0015

Slope () Slope 418 plusmn 181 4114 plusmn 255 3866 plusmn 114 115 033Clay () CLY 1637 plusmn 117 a 175 plusmn 22 a 1211 plusmn 102 b 465 001

Appl Sci 2021 11 11372 11 of 17

Table 5 Cont

Environmental Variables CodeGroup I Group II Group III

F-Value p-ValueMean plusmn SE Mean plusmn SE Mean plusmn SE

Silt () SLT 2444 plusmn 220 26 plusmn 36 2903 plusmn 274 066 052Sand () SND 5918 plusmn 266 5638 plusmn 342 5885 plusmn 308 017 084pH (15) pH 64 plusmn 012 66 plusmn 017 626 plusmn 013 125 030

Organic matter () OM 221 plusmn 078 462 plusmn 076 261 plusmn 054 292 007Lime () L 316 plusmn 052 406 plusmn 061 361 plusmn 038 066 052

Nitrogen (mgKg) N 012 plusmn 004 018 plusmn 003 016 plusmn 003 0503 060Phosphorus (mgKg) P 824 plusmn 063 744 plusmn 112 1294 plusmn 446 061 054Potassium (mgKg) K 14625 plusmn 2707 23342 plusmn 3752 18633 plusmn 2633 155 022

Wilting point (mLgm) WP 0114 plusmn 042 011 plusmn 009 009 plusmn 0004 436 002Field capacity (mLgm) FC 022 plusmn 061 023 plusmn 009 021 plusmn 007 131 028

Bulk density (gcm3) BD 14 plusmn 011 a 146 plusmn 002 a 152 plusmn 001 ab 343 004Saturation Point (0 kPa) SP 044 plusmn 052 a 044 plusmn 0008 a 042 plusmn 006 ab 341 004

Electrical Conductivity (mSm) EC 1241 plusmn 163 a 128 plusmn 003 a 2346 plusmn 280 b 544 001Available water () AW 010 plusmn 038 011 plusmn 0005 011 plusmn 004 046 063

Temperature minimum (C) Tpmi 1430 plusmn 192 1188 plusmn 037 1189 plusmn 017 213 014Temperature maximum (F) Tpma 2898 plusmn 875 2789 plusmn 533 3646 plusmn 575 211 014

Precipitation (mm) Preci 4984 plusmn 121 4916 plusmn 186 5184 plusmn 097 132 028Relative humidity () RH 4984 plusmn 122 4916 plusmn 187 5184 plusmn 098 132 028

Water Holding capacity () WHC 5212 plusmn 182 5482 plusmn 198 5347 plusmn 289 018 083

Note Different superscript letters mean significant variation at p lt 05 tested by post hoc Tukey HSD insignificant variations haveno superscript

Table 6 Results of the RDA showed correlation coefficients between the physiographic and edaphicvariables and the RDA axes and biplot scores of each variable on all the three axes

S No VariablesCorrelation Biplot Scores

Axis 1 Axis 2 Axis 3 Axis 1 Axis 2 Axis 3

1 Lat minus006 minus049 minus002 minus055 minus394 minus01552 Long minus019 018 minus022 minus181 148 minus1743 E 023 minus039 006 218 minus309 05184 ASP 008 minus009 016 074 minus074 1255 CLY 019 minus036 minus019 177 minus292 minus1486 SLT minus020 029 038 minus183 228 2957 SND 009 minus009 minus026 085 minus072 minus2038 pH 022 minus022 minus021 197 minus172 minus1639 OM 009 016 minus0003 088 126 minus002

10 L 021 017 minus039 196 132 minus30511 N 022 009 minus002 182 075 minus01812 P 0007 minus013 020 007 minus106 15613 K 036 minus004 minus012 331 minus031 minus09614 WP 018 minus037 minus018 166 minus296 minus13915 FC 003 minus013 009 027 minus105 07216 BD minus010 030 005 minus093 237 04217 SP 0104 minus031 minus005 095 minus238 minus03718 EC minus0121 043 013 minus111 341 100419 AW minus0176 025 038 minus160 197 29220 TIVI minus063 minus047 002 minus583 minus379 01721 QIVI 0162 minus041 013 148 minus328 09722 BA minus0025 minus011 022 minus023 minus088 15523 Dha 0112 minus022 minus017 102 minus178 minus12824 TpMi minus0246 minus009 minus004 minus224 minus077 minus03425 TpMa minus0185 001 032 minus168 011 24826 Preci 0259 minus009 003 236 minus071 02427 RH 0102 minus005 minus004 0935 minus037 minus03528 WHC minus0273 0005 0079 minus249 004 061

Note (p lt 005) (p lt 001)

Appl Sci 2021 11 11372 12 of 17Appl Sci 2021 11 x FOR PEER REVIEW 12 of 18

Figure 5 RDA ordination of physiographic and edaphic variables concerning stands and the understory vegetation Note

Blue square represent the species point in the ordination biplot St (Stand number)

Table 6 Results of the RDA showed correlation coefficients between the physiographic and edaphic

variables and the RDA axes and biplot scores of each variable on all the three axes

S No Variables Correlation Biplot Scores

Axis 1 Axis 2 Axis 3 Axis 1 Axis 2 Axis 3

1 Lat minus006 minus049 minus002 minus055 minus394 minus0155

2 Long minus019 018 minus022 minus181 148 minus174

3 E 023 minus039 006 218 minus309 0518

4 ASP 008 minus009 016 074 minus074 125

5 CLY 019 minus036 minus019 177 minus292 minus148

6 SLT minus020 029 038 minus183 228 295

7 SND 009 minus009 minus026 085 minus072 minus203

8 pH 022 minus022 minus021 197 minus172 minus163

9 OM 009 016 minus0003 088 126 minus002

10 L 021 017 minus039 196 132 minus305

11 N 022 009 minus002 182 075 minus018

12 P 0007 minus013 020 007 minus106 156

13 K 036 minus004 minus012 331 minus031 minus096

Figure 5 RDA ordination of physiographic and edaphic variables concerning stands and the understory vegetation NoteBlue square represent the species point in the ordination biplot St (Stand number)

4 Discussion

Vegetation is a group of plants growing together in a particular locality [43] and it mayalso be defined as a unit that retains its unique structure and physiognomic characteristicsin an adequately great and sufficient way to permit their distinction from other units [46]The understory plant species in the oak-dominated forests consist of 58 species belongingto 32 families at 30 different locations in the Hindukush ranges of Swat The physiognomyof the studied area was dominated by herbaceous growth form with 47 plant species (81)followed by shrubs with 10 plant species (17) and trees with individual plant species(2) Herbaceous dominancy and less tree percentage might be due to altitudinal andgeographical variations which indicates that the climatic factors favor the herbaceous floraOur findings are associated with researchers in allied neighboring and national regions inwhich the species reported were mostly herbaceous [4748] Among all families Fabaceaewas recorded as the leading family with eight plant species followed by Asteraceae andLamiaceae with seven species each For instance several researchers [532ndash343846] forinstance [31] have documented Asteraceae and Fabaceae as the two most important fami-lies While other researchers [38] cited Lamiaceae and Rosaceae and [48] cited LamiaceaeMoraceae and Asteraceae as dominant plant families from Darra Adam Khel KP Pakistan

Appl Sci 2021 11 11372 13 of 17

Plant life-forms and vegetation are indicators of the climate [6] According to Meher-Homji [49] life-forms are reflective of the bioclimates of an area Raunkiaer [6] designedthree major phytoclimates based on life-form spectra on the earth It includes phanerophyticclimate for the tropics therophytic for the xeric environments and hemicryptophytic forthe cold temperate region The present study identified seven different life-form classes inthe study area The most dominant life-form was hemicryptophytes with 19 species (33)followed by nanophanerophytes with 15 species (26) and therophytes with 13 species(22) Hemicryptophytes usually prevail in open physiognomies while phanerophytesare mainly in closed ones [5051] Biological spectra are important in comparing geographyand habitats and might change due to biotic influences viz grazing human activities andclimatic changes [52ndash54] Hemicryptophytes lose their aboveground parts during mostsummer and winter months while therophytes remain seeded to avoid summer droughtand cold winter stresses

Furthermore the flora of the study area is under anthropogenic pressure in the formof overgrazing and deforestation by nomadic and native people Nasir and Sultan [55]reported a similar finding from District Chakwal where therophytes were the dominantbiological spectra A community that therophytes dominate can be a characteristic fea-ture of a highly disturbed area under anthropogenic pressure [4854] In addition [56]reported therophytes as the dominant plant species of the rangeland district Tank Pak-istan and [57] assessed that therophytes is the leading life-form of Lahor District SwabiPakistan showing that the results of the current study are in compliance with the findingsof several other studies

Results of leaf size spectra trait revealed that species with microphyllous leaves domi-nated the area (with 24 species 41) followed by nanophylls (17 species 29) leptophylls(11 species 19) and mesophyll (5 species 9) Nonetheless 2 with megaphyllousleaf size was also recorded Microphyllous leaf size class is normally the characteristicfeature of meadow plant species while leptophylls and nanophylls are illustrative of hotdeserts [754] Comparable outcomes where microphylls and nanophylls overwhelmedthe vegetation and were reported in the work of researchers [7] and [45] where the authorslinked these two leaf size classes with the physiognomies of mild ranges A high rate ofmicrophylls may be identified with cool atmospheres of the sub-elevated and snowcappedareas Here as well the top layer was less settled containing a slim sheet that is notconclusive about the entrance of roots Microphyllous and nanophyllous leaves specieswere inexhaustible because of the biological variety for this dry condition The presentresults concur with [58] who detailed that microphylls and nanophylls predominance inthe dry mild atmosphere of District Quetta Our inferences additionally uncovered that thehigh extent in leaf size class changes with increasing altitude and the rate of microphyllswas emphatically connected with this as well [5960]

Among the 58 species documented 43 plant species were found in association withgroup III clustered by applying Wardrsquos agglomerative clustering which indicates widesociability of the species in the studied oak-dominated forests Moreover the analysisreveals that B lycium (782) C arvensis (687) and A trichomanes (66) were the mostabundant species in group III Group II was less diverse in terms of understory speciesnumbering in total of 25 plant species In this group Calamintha vulgaris (L) H KarstDryopteris stewartii Fraser-Jenk and Plantago lanceolata L were dominant (115 934 and986 respectively) Plant species in the understory with varying degrees of resistance tothese factors prefer a specific forest type Since certain plant species are limited to a specificforest type the extinction of that forest could result in the extinction of certain understoryplants [2761]

According to a recent analysis the richness and diversity of understory species inoak forests differed greatly depending on canopy dominants Herbaceous species abun-dance and α-diversity were highest in the oaks forest but there was less heterogeneity(β-diversity) across sites and major groups These findings highlight the importance of oakforests in protecting habitat and plant composition in the understory vegetation An herb

Appl Sci 2021 11 11372 14 of 17

layer with higher species abundance and diversity in oak forests may be due to highersolar radiation on south-facing slopes which is better for herbaceous species [62ndash64]

Environmental variables such as geographic parameters and physiochemical soilcharacteristics are important in determining the community structure and composition [65]In particular latitude and altitude were found to vary significantly in the understory groupsClay particles in soil texture and bulk density saturation point and electrical conductivityvaried significantly in the understory vegetation Similarly in the same region [66] thesoil parameters in understory vegetation of Pinus wallichiana AB Jacks dominated foresthave been studied revealing that elevation slope and phosphorus are vital factors indetermining the understory vegetation An oak species Q rubur L was also reported asa major associated species Furthermore many other researchers from other parts of theworld have reported that edaphic factors can significantly affect the species compositionand species diversity in plant communities [1066ndash68]

Forward selection of the RDA ordination revealed that latitude elevation clay wiltingpoint bulk density saturation and electric conductivity were significantly influential indetermining the understory vegetation of oak-dominated forests These results followthe findings of many other previous studies [12596970] Ali and Begum [62] also in-vestigated the vegetation of Swat and determined congruent results by stating a strongrelationship between vegetation and edaphic factors Many other researchers worldwidehave recorded that soil characteristics matter more than canopy organisms in decidingunderstory vegetation [62ndash6470] The study of species composition analysis in the oak-dominated forest revealed a general pattern of variation in the community diversity andspecies composition A similar pattern of species composition was also reported by [65] inP wallachiana understory from the same region The species diversity was found to increasewith time as Beg and Mirza [29] reported only 36 understory species due to the increase inanthropogenic activities

5 Conclusions

The current study reveals that Swat oak forests have rich floristic diversity with domi-nance of the therophytic life-form and microphyllous leaf size class indicating sub-tropicaland moist temperate type climates The species diversity was observed to increase duringthe spring and summer seasons and decreased later in the autumn As the winter seasonapproaches the decline in diversity was observed associated with dry environmentalconditions slow growth rate and other climatic factors Nonetheless critical impactsof seasonal variation on life-forms and overall species diversity were evident Among58 species 43 plant species were associated with group III clustered by applying Wardrsquosagglomerative clustering indicating the wide sociability of the species in the studied oak-dominated forests The understory vegetation of these forests plays an important role inthe forest ecology of the region

Moreover the environmental and soil variables ie latitude elevation clay percent-age wilting point electrical conductivity and potassium (mgKg) affect the understoryvegetation In addition important overstory variables like Quercus IVI and Total IVI ofoverstory were also found to affect the understory vegetation in oak-dominated forestsFurther it is concluded that the area is vulnerable due to the pressure from the localinhabitants in the form of overgrazing and deforestation which may significantly affectthe understory vegetation This information is particularly important for the success ofefforts intended to prevent the loss of genetic diversity of species within these forestsby destroying their natural habitats Moreover it is imperative to conserve the arearsquosbiodiversity and provide alternative means of livelihood for the local communities thatmay allow sustainable utilization and conservation of the invaluable biodiversity of thisarea for future generations

Appl Sci 2021 11 11372 15 of 17

Author Contributions The research work was designed and supervised by NK AR carried outthe field and laboratory work data analysis and manuscript writing RU also contributed tomanuscript writing and data collection KA DAJ and MEHK provided valuable informationand comments on the initial draft and refine the text in addition to language editing and data analysisIUR provided valuable suggestions during the write-up process and data analysis All authorshave read and agreed to the published version of the manuscript

Funding The research was conducted as a PhD project and did not receive support from anyfunding agency

Institutional Review Board Statement Not applicable

Informed Consent Statement Not applicable

Data Availability Statement All the data analyzedgenerated are included and available inthis manuscript

Acknowledgments We express our gratitude towards the Master students enrolled in the Depart-ment of Botany and the people of Malakand Division who helped with the fieldwork for this projectWe thank Achim Braumluning (Institute of Geography Department of Geography and GeosciencesFriedrich-Alexander-University (FAU) Erlangen-Nuremberg Erlangen Germany) for insightfulcomments that substantially improved the early version We also acknowledged the anonymous re-viewers and editors of the Applied Sciences journal for their valuable comment and language editing

Conflicts of Interest We hereby declare that all the authors have participated in this study and thedevelopment of the manuscript All the authors have read the final version and consent for the articleto be published in the Applied Sciences

References1 Musarella CM Mendoza-Fernaacutendez AJ Mota JF Alessandrini JFMA Bacchetta G Brullo GBS Caldarella O

Ciaschetti OCG Conti F Di Martino FCL et al Checklist of gypsophilous vascular flora in Italy Phyto Keys 2018 103 61ndash82[CrossRef] [PubMed]

2 Perrino EV Signorile G Checklist of the vascular flora from the Monopoli coast (Apulia) Ital Bot 2009 41 263ndash2793 Shah M Farrukh HSyed NMSImran AHumaira W Life Form And Floristic Characteristics Along Altitudinal Gradient Of

Humid Temperate Forests Located In Remote Area Of Pakistan Glob J Biodivers Sci Manag 2013 3 276ndash2814 Rafaqat M An Annotated Checklist of Amphibians and Reptiles of Margalla Hills National Park Pakistan Pak J Zool 2011 43

1041ndash10485 Shimwell DW Festuco-Brometea Br-Bl amp R Tx 1943 in the British isles The Phytogeography and Phytosociology of Limestone

Grasslands Part I (A) General Introduction(B) Xerobromion in England Vegetatio 1971 23 1ndash276 Raunkiaer C The Life Forms of Plants and Statistical Plant Geography Being the Collected Papers of C Raunkiaer In The Life

Forms of Plants and Statistical Plant Geography Being the Collected Papers of C Raunkiaer Clarendon Press Oxford UK 19347 Oosting HJ Hess DW Microclimate and a relic stand of Tsuga canadensis in the lower piedmont of North Carolina Ecology

1956 37 28ndash39 [CrossRef]8 Bailey IW Sinnott EW A botanical index of Cretaceous and Tertiary climates Science 1915 41 831ndash834 [CrossRef]9 Cain SA De Oliveira Castro GM Manual of Vegetation Analysis Haper and Row New York NY USA 195910 Augusto L Dupouey JL Ranger J Effects of tree species on understory vegetation and environmental conditions in temperate

forests Ann For Sci 2003 60 823ndash831 [CrossRef]11 Gracia M Montaneacute F Piqueacute J Retana J Overstory structure and topographic gradients determining diversity and abundance

of understory shrub species in temperate forests in central Pyrenees (NE Spain) For Ecol Manag 2007 242 391ndash397 [CrossRef]12 Gilliam FS The ecological significance of the herbaceous layer in temperate forest ecosystems Bioscience 2007 57 845ndash858

[CrossRef]13 Messier C Parent S Bergeron Y Effects of overstory and understory vegetation on the understory light environment in mixed

boreal forests J Veg Sci 1998 9 511ndash520 [CrossRef]14 Nilsson MC Wardle DA Understory vegetation as a forest ecosystem driver Evidence from the northern Swedish boreal

forest Front Ecol Environ 2005 3 421ndash428 [CrossRef]15 Bartels SF Chen HYH Is understory plant species diversity driven by resource quantity or resource heterogeneity Ecology

2010 91 1931ndash1938 [CrossRef] [PubMed]16 Dauber J Hirsch M Simmering D Waldhardt R Otte A Wolters V Landscape structure as an indicator of biodiversity

Matrix effects on species richness Agric Ecosyst Environ 2003 98 321ndash329 [CrossRef]17 Duguid MC Frey BR Ellum DS Kelty M Ashton MS The influence of ground disturbance and gap position on understory

plant diversity in upland forests of southern New England For Ecol Manag 2013 303 148ndash159 [CrossRef]

Appl Sci 2021 11 11372 7 of 17

32 Leaf Size Spectra

Results of leaf size spectra trait revealed that species with microphyllous leaves domi-nated the area with 24 species (41) followed by nanophyll 17 species (29) leptophyll11 species (19) and mesophyll 5 species (9) (Figure 3) Single species (2) with mega-phyllous leaf size was also recorded A high rate of microphylls may be identified withinthe cool environment of the sub-elevated and snowcapped areas Here the top layer wasless settled it contained a slim sheet that may deny them the entrance of roots The mi-crophyllous and nanophyllous leaves species were inexhaustible because of the biologicalvariety for this dry condition

Appl Sci 2021 11 x FOR PEER REVIEW 7 of 18

Figure 2 Life-form classes of the plant species recorded in the understory vegetation of oak-domi-

nated forests of Swat Pakistan

32 Leaf Size Spectra

Results of leaf size spectra trait revealed that species with microphyllous leaves dom-

inated the area with 24 species (41) followed by nanophyll 17 species (29) leptophyll

11 species (19) and mesophyll 5 species (9) (Figure 3) Single species (2) with meg-

aphyllous leaf size was also recorded A high rate of microphylls may be identified within

the cool environment of the sub-elevated and snowcapped areas Here the top layer was

less settled it contained a slim sheet that may deny them the entrance of roots The micro-

phyllous and nanophyllous leaves species were inexhaustible because of the biological

variety for this dry condition

Figure 3 Leaf size classes of the plant species recorded in the understory vegetation of oak-domi-

nated forests of Swat Pakistan

The chorotype of the species varies from uniregional to cosmopolitan ie 22 were

cosmopolitan 26 pluriregional 23 bioregional and 29 were uniregional

26

33

22

12

3 2 2

Life forms

Nanophanerophytes

Hemicryptophytes

Therophytes

Geophytes

Chamaephytes

Microphanerophytes

Lianas

19

2941

9

2

Leaf size class

Leptophylls

Nanophylls

Microphylls

Mesophylls

Megaphylls

Figure 3 Leaf size classes of the plant species recorded in the understory vegetation of oak-dominatedforests of Swat Pakistan

The chorotype of the species varies from uniregional to cosmopolitan ie 22 werecosmopolitan 26 pluriregional 23 bioregional and 29 were uniregional

33 Understory Classification

A total of 58 plant species were recorded as associates in the understory vegeta-tion and clustered into three major groups by applying Wardrsquos agglomerative clustering(Figure 4 and Table 2) Among 58 species 43 plant species were found in association withgroup III clearly indicating the speciesrsquo wide sociability in the studied oak-dominatedforests Moreover the analysis reveals that IVI of Berberis lycium Royle (782) Convolvulusarvensis L (687) and Asplenium trichomanes L (66) were the most abundant species ingroup III Group II was recorded intermediately diverse in understory species having25 plant species with Calamintha vulgaris (L) H Karst Dryopteris stewartii Fraser-Jenkand Plantago lanceolata L as the dominant associates having IVI of 115 934 and 986respectively The results revealed group I as the less diverse in terms of species (18 species)and B lycium having IVI of 986 A trichomanes (914) and Indigofera heterantha Wall exBrandis (893) were the most abundant species

Appl Sci 2021 11 11372 8 of 17

Appl Sci 2021 11 x FOR PEER REVIEW 8 of 18

33 Understory Classification

A total of 58 plant species were recorded as associates in the understory vegetation

and clustered into three major groups by applying Wardrsquos agglomerative clustering (Fig-

ure 4 and Table 2) Among 58 species 43 plant species were found in association with

group III clearly indicating the speciesrsquo wide sociability in the studied oak-dominated

forests Moreover the analysis reveals that IVI of Berberis lycium Royle (782) Convolvulus

arvensis L (687) and Asplenium trichomanes L (66) were the most abundant species in

group III Group II was recorded intermediately diverse in understory species having 25

plant species with Calamintha vulgaris (L) H Karst Dryopteris stewartii Fraser-Jenk and

Plantago lanceolata L as the dominant associates having IVI of 115 934 and 986 respec-

tively The results revealed group I as the less diverse in terms of species (18 species) and

B lycium having IVI of 986 A trichomanes (914) and Indigofera heterantha Wall ex Brandis

(893) were the most abundant species

Figure 4 Cluster dendrogram classifying understory vegetation into three distinct groups Note G

(Group) St (Stand)

Table 2 Understory flora associated with oak-dominated forest recorded in the three clusters separated by Wardrsquos ag-

glomerative clustering procedure

Species Name Code Cluster I Cluster II Cluster III

M plusmn SE M plusmn SE M plusmn SE

Achyranthes aspera L As 241 plusmn 241 - -

Adiantum venustum D Don Av - - 077 plusmn 077

Ajuga bracteosa Wall ex Benth Ab 387 plusmn 265 - -

Amaranthus viridis L Am 510 plusmn 323 - 241 plusmn 144

Arabidopsis thaliana (L) Heynh At - - 116 plusmn 079

Arenaria serpyllifolia L Am - - 053 plusmn 053

Artimisia vulgaris L Av 72 plusmn 471 - -

Figure 4 Cluster dendrogram classifying understory vegetation into three distinct groups NoteG (Group) St (Stand)

Table 2 Understory flora associated with oak-dominated forest recorded in the three clusters separated by Wardrsquosagglomerative clustering procedure

Species Name CodeCluster I Cluster II Cluster III

M plusmn SE M plusmn SE M plusmn SE

Achyranthes aspera L As 241 plusmn 241 - -Adiantum venustum D Don Av - - 077 plusmn 077

Ajuga bracteosa Wall ex Benth Ab 387 plusmn 265 - -Amaranthus viridis L Am 510 plusmn 323 - 241 plusmn 144

Arabidopsis thaliana (L) Heynh At - - 116 plusmn 079Arenaria serpyllifolia L Am - - 053 plusmn 053

Artimisia vulgaris L Av 72 plusmn 471 - -Asplenium trichomanes L As 914 plusmn 471 423 plusmn 423 66 plusmn 26

Astragalus grahamianus Benth Ag - - 053 plusmn 053Atropa acuminata Royle ex Lindl Aa 34 plusmn 346 - 242 plusmn 243

Berberis lycium Royle B 986 plusmn 549 766 plusmn 491 782 plusmn 354Bidens cernua L Bc - 171 plusmn 171 -

Buddleja asiatica Lour Ba 093 plusmn 093 - 169 plusmn 117Calamintha vulgaris (L) H Karst Cv - 115 plusmn 411 346 plusmn 166

Chenopodium album L Ca - 44 plusmn 442 -Convolvulus arvensis L Ca 25 plusmn 252 42 plusmn 274 687 plusmn 176Erigeron canadensis L Co 085 plusmn 085 - -

Cynodon dactylon (L) Pers Cd 7 plusmn 5 617 plusmn 617 488 plusmn 332Daphne mucronata Royle Dm 383 plusmn 383 - 194 plusmn 134

Dioscorea deltoidea Wall ex Griseb Dd 183 plusmn 183 - -Dodonaea viscosa Jacq Do 142 plusmn 142 - -

Dryopteris stewartii Fraser-Jenk Ds - 986 plusmn 986 -Elaeagnus angustifolia L Ea 23 plusmn 23 - -Festuca gigantea (L) Vill Fg - - 046 plusmn 046

Appl Sci 2021 11 11372 9 of 17

Table 2 Cont

Species Name CodeCluster I Cluster II Cluster III

M plusmn SE M plusmn SE M plusmn SE

Fragaria indica Andrews Fi - 271 plusmn 271 553 plusmn 222Galium asperifolium Wall Ga 436 plusmn 436 - 134 plusmn 134

Hibiscus syriacus L Hs - - 06 plusmn 062Indigofera gerardiana Graham ex Baker Ig - - 365 plusmn 286Indigofera heterantha Wall ex Brandis Ih 893 plusmn 893 - -Isodon rugosus (Wall ex Benth) Codd Ir - 82 plusmn 82 -

justica adathoda L Ja - - 196 plusmn 145Lamium album L La - - 053 plusmn 053

Lespedeza juncea (L f) Pers Lj 502 plusmn 502 - 291 plusmn 291Lotus corniculatus L Lc 25 plusmn 25 - 252 plusmn 157Malva neglecta Wallr Mn - - 106 plusmn 106Medicago lupulina L Ml - - 121 plusmn 121Myrsine africana L Ma 45 plusmn 37 185 plusmn 185 596 plusmn 253

Origanum vulgare L Ov - 26 plusmn 268 -Otostegia limbata (Benth) Boiss Ol - - 160 plusmn 113Oxytropis mollis Royle ex Benth Om 363 plusmn 363 171 plusmn 171 336 plusmn 197

Plantago lanceolata L Pl 23 plusmn 23 934 plusmn 615 605 plusmn 329Plantago major L Pm - 59 plusmn 4 046 plusmn 046

Polygonatum verticillatum (L) All Pv - 171 plusmn 171 -Pteris cretica L Pc - - 167 plusmn 118

Ranunculus laetus Salisb Rl - - 093 plusmn 093Rosa webbiana Wall ex Royle Rw - - -Rumex denticulatus K Koch Ru - - 449 plusmn 257

Rumex nepalensis Spreng Rn - 357 plusmn 357 053 plusmn 053Sarcococca saligna (DDon) MuumlllArg Ss - - 053 plusmn 053

Smilax lanceolata L Sl 1 plusmn 12 - 308 plusmn 179Solidago virgaurea L Sv - - 053 plusmn 053

Tagetes minuta L Tg 502 plusmn 502 - 121 plusmn 121Taraxacum officinale (L) Weber ex

FHWigg To - - 06 plusmn 061

Trifolium repens L Tr - - 136 plusmn 095Viburnum grandiflorum Wall ex DC Vg - - 228 plusmn 228

Viola serpens Wall ex Ging Vs - - 135 plusmn 094Youngia japonica (L) DC Yj - 27 plusmn 272 -

Zanthoxylum armatum DC Za - - 106 plusmn 106

Note - Represent absence of specie in particular group

34 Understory Species Diversity and Richness

Significant differences in species richness (p lt 0015) ShannonndashWiener Margalef(p lt 000076) Simpson (p lt 0040) and Beta indexes were detected among three majorgroups of the understory layer of oak-dominated forests (Table 3) Nonetheless Pielousevenness was found non-significantly different (p gt 005) among the three major groups ofunderstory vegetation Group III had the highest species richness (103) α-diversity (274)and β-diversity (985) and the highest value of Margalef index (395) On the contrary thegroup I had the highest Pielous and Simpson index values with 097 and 713 respectively(Table 3)

Appl Sci 2021 11 11372 10 of 17

Table 3 Species richness and diversity indexes of oak-dominated forests of Swat Pakistan

IndexesGroup I Group II Group III

F pMean plusmn SE Mean plusmn SE Mean plusmn SE

Total number of Species (S) 587 plusmn 066 b 4 plusmn 037 a 1032 plusmn 15 b 485 0015ShannonndashWiener Index (H) 184 plusmn 019 a 13 plusmn 011 a 274 plusmn 020 b 1393 697 times 10minus5

Pielous Index (J) 097 plusmn 001 095 plusmn 001 093 plusmn 001 209 014Margalef Index (M) 29 plusmn 033 a 14 plusmn 021 a 395 plusmn 042 b 948 000076

Simpson Index (1D) 713 plusmn 110 a 368 plusmn 042 b 6 plusmn 061 a 361 004Beta diversity (B = Sa) 641 plusmn 127 a 368 plusmn 043 a 985 plusmn 054 b 1645 213 times 10minus5

Note Different superscript letters mean significant variation at p lt 05 tested by post hoc Tukey HSD insignificant variations haveno superscript

35 Influence of Physiographic and Edaphic Variables on the Understory Species Composition

In the ordination analysis the permutation test revealed that the eigenvalues for thefirst axis and those for all canonical axes were significant (p lt 001) and indicated thatunderstory species composition was influenced by physiographic and edaphic variables(Figure 5) All three axes explained 65 of the cumulative variance and 308 of thevariance in the relationship among understory species composition (Table 4) Forwardselection of the RDA ordination revealed that seven variables (ie latitude elevationclay wilting point bulk density saturation and electric conductivity) were the significantinfluential among all 23 variables in relation to the understory vegetation of oak-dominatedforests (Table 5) Group I (Quercus balootndashPinus roxburghii community) which lies at anintermediate elevation among the three communities has lower quantities of organic matterLime Nitrogen and Potassium In contrast group II (Quercus semecarpifoliandashQuercus rubur)which lies at a higher elevation has higher quantities of these nutrients Moreover in theordination axes summery the first axis was significantly associated with total importancevalue index (r = 0639) potassium (r = 0363) and elevation (r = 0239) The second axiswas found in close relation with QIVI (r = minus0414) wilting point (r = minus0374) and clay(r = minus0369) While the third axis was found in close correlation with silt (r = 0381) lime(r = 0395) and available water (r = minus0377) (Table 6)

Table 4 Ordination analysis of the understory vegetation concerning physiographic andedaphic variables

Axis Axis 1 Axis 2 Axis 3

Eigenvalue 3327 2512 2396

Variance in species data

of variance explained 1242 941 9Cumulative explained 1241 2181 3082

Pearson Correlation Response-Pred 100 098 1Kendall Correlation Response-Pred 096 081 099

Symbol of steric show signidicant of the data

Table 5 Average values (Mean plusmn stand error) of the environmental variables ie topographic edaphic and soil in thethree community types (vegetation groups) separated by Wardrsquos agglomerative cluster analysis The three groups wereGroup I (Quercus balootndashPinus roxburghii) Group II (Quercus semecarpifoliandashQuercus robur) and Group III (QuercuslanatandashOlea ferruginea)

Environmental Variables CodeGroup I Group II Group III

F-Value p-ValueMean plusmn SE Mean plusmn SE Mean plusmn SE

Latitude () Lat 350 plusmn 012 a 349694 plusmn 019 b 3458 plusmn 0050 b 557 0009Longitude () Long 7228 plusmn 003 7229 plusmn 0023 7225 plusmn 0016 172 019Elevation (m) Elev 201775 plusmn 20523 a 22895 plusmn 24022 b 16594 plusmn 6448 a 487 0015

Slope () Slope 418 plusmn 181 4114 plusmn 255 3866 plusmn 114 115 033Clay () CLY 1637 plusmn 117 a 175 plusmn 22 a 1211 plusmn 102 b 465 001

Appl Sci 2021 11 11372 11 of 17

Table 5 Cont

Environmental Variables CodeGroup I Group II Group III

F-Value p-ValueMean plusmn SE Mean plusmn SE Mean plusmn SE

Silt () SLT 2444 plusmn 220 26 plusmn 36 2903 plusmn 274 066 052Sand () SND 5918 plusmn 266 5638 plusmn 342 5885 plusmn 308 017 084pH (15) pH 64 plusmn 012 66 plusmn 017 626 plusmn 013 125 030

Organic matter () OM 221 plusmn 078 462 plusmn 076 261 plusmn 054 292 007Lime () L 316 plusmn 052 406 plusmn 061 361 plusmn 038 066 052

Nitrogen (mgKg) N 012 plusmn 004 018 plusmn 003 016 plusmn 003 0503 060Phosphorus (mgKg) P 824 plusmn 063 744 plusmn 112 1294 plusmn 446 061 054Potassium (mgKg) K 14625 plusmn 2707 23342 plusmn 3752 18633 plusmn 2633 155 022

Wilting point (mLgm) WP 0114 plusmn 042 011 plusmn 009 009 plusmn 0004 436 002Field capacity (mLgm) FC 022 plusmn 061 023 plusmn 009 021 plusmn 007 131 028

Bulk density (gcm3) BD 14 plusmn 011 a 146 plusmn 002 a 152 plusmn 001 ab 343 004Saturation Point (0 kPa) SP 044 plusmn 052 a 044 plusmn 0008 a 042 plusmn 006 ab 341 004

Electrical Conductivity (mSm) EC 1241 plusmn 163 a 128 plusmn 003 a 2346 plusmn 280 b 544 001Available water () AW 010 plusmn 038 011 plusmn 0005 011 plusmn 004 046 063

Temperature minimum (C) Tpmi 1430 plusmn 192 1188 plusmn 037 1189 plusmn 017 213 014Temperature maximum (F) Tpma 2898 plusmn 875 2789 plusmn 533 3646 plusmn 575 211 014

Precipitation (mm) Preci 4984 plusmn 121 4916 plusmn 186 5184 plusmn 097 132 028Relative humidity () RH 4984 plusmn 122 4916 plusmn 187 5184 plusmn 098 132 028

Water Holding capacity () WHC 5212 plusmn 182 5482 plusmn 198 5347 plusmn 289 018 083

Note Different superscript letters mean significant variation at p lt 05 tested by post hoc Tukey HSD insignificant variations haveno superscript

Table 6 Results of the RDA showed correlation coefficients between the physiographic and edaphicvariables and the RDA axes and biplot scores of each variable on all the three axes

S No VariablesCorrelation Biplot Scores

Axis 1 Axis 2 Axis 3 Axis 1 Axis 2 Axis 3

1 Lat minus006 minus049 minus002 minus055 minus394 minus01552 Long minus019 018 minus022 minus181 148 minus1743 E 023 minus039 006 218 minus309 05184 ASP 008 minus009 016 074 minus074 1255 CLY 019 minus036 minus019 177 minus292 minus1486 SLT minus020 029 038 minus183 228 2957 SND 009 minus009 minus026 085 minus072 minus2038 pH 022 minus022 minus021 197 minus172 minus1639 OM 009 016 minus0003 088 126 minus002

10 L 021 017 minus039 196 132 minus30511 N 022 009 minus002 182 075 minus01812 P 0007 minus013 020 007 minus106 15613 K 036 minus004 minus012 331 minus031 minus09614 WP 018 minus037 minus018 166 minus296 minus13915 FC 003 minus013 009 027 minus105 07216 BD minus010 030 005 minus093 237 04217 SP 0104 minus031 minus005 095 minus238 minus03718 EC minus0121 043 013 minus111 341 100419 AW minus0176 025 038 minus160 197 29220 TIVI minus063 minus047 002 minus583 minus379 01721 QIVI 0162 minus041 013 148 minus328 09722 BA minus0025 minus011 022 minus023 minus088 15523 Dha 0112 minus022 minus017 102 minus178 minus12824 TpMi minus0246 minus009 minus004 minus224 minus077 minus03425 TpMa minus0185 001 032 minus168 011 24826 Preci 0259 minus009 003 236 minus071 02427 RH 0102 minus005 minus004 0935 minus037 minus03528 WHC minus0273 0005 0079 minus249 004 061

Note (p lt 005) (p lt 001)

Appl Sci 2021 11 11372 12 of 17Appl Sci 2021 11 x FOR PEER REVIEW 12 of 18

Figure 5 RDA ordination of physiographic and edaphic variables concerning stands and the understory vegetation Note

Blue square represent the species point in the ordination biplot St (Stand number)

Table 6 Results of the RDA showed correlation coefficients between the physiographic and edaphic

variables and the RDA axes and biplot scores of each variable on all the three axes

S No Variables Correlation Biplot Scores

Axis 1 Axis 2 Axis 3 Axis 1 Axis 2 Axis 3

1 Lat minus006 minus049 minus002 minus055 minus394 minus0155

2 Long minus019 018 minus022 minus181 148 minus174

3 E 023 minus039 006 218 minus309 0518

4 ASP 008 minus009 016 074 minus074 125

5 CLY 019 minus036 minus019 177 minus292 minus148

6 SLT minus020 029 038 minus183 228 295

7 SND 009 minus009 minus026 085 minus072 minus203

8 pH 022 minus022 minus021 197 minus172 minus163

9 OM 009 016 minus0003 088 126 minus002

10 L 021 017 minus039 196 132 minus305

11 N 022 009 minus002 182 075 minus018

12 P 0007 minus013 020 007 minus106 156

13 K 036 minus004 minus012 331 minus031 minus096

Figure 5 RDA ordination of physiographic and edaphic variables concerning stands and the understory vegetation NoteBlue square represent the species point in the ordination biplot St (Stand number)

4 Discussion

Vegetation is a group of plants growing together in a particular locality [43] and it mayalso be defined as a unit that retains its unique structure and physiognomic characteristicsin an adequately great and sufficient way to permit their distinction from other units [46]The understory plant species in the oak-dominated forests consist of 58 species belongingto 32 families at 30 different locations in the Hindukush ranges of Swat The physiognomyof the studied area was dominated by herbaceous growth form with 47 plant species (81)followed by shrubs with 10 plant species (17) and trees with individual plant species(2) Herbaceous dominancy and less tree percentage might be due to altitudinal andgeographical variations which indicates that the climatic factors favor the herbaceous floraOur findings are associated with researchers in allied neighboring and national regions inwhich the species reported were mostly herbaceous [4748] Among all families Fabaceaewas recorded as the leading family with eight plant species followed by Asteraceae andLamiaceae with seven species each For instance several researchers [532ndash343846] forinstance [31] have documented Asteraceae and Fabaceae as the two most important fami-lies While other researchers [38] cited Lamiaceae and Rosaceae and [48] cited LamiaceaeMoraceae and Asteraceae as dominant plant families from Darra Adam Khel KP Pakistan

Appl Sci 2021 11 11372 13 of 17

Plant life-forms and vegetation are indicators of the climate [6] According to Meher-Homji [49] life-forms are reflective of the bioclimates of an area Raunkiaer [6] designedthree major phytoclimates based on life-form spectra on the earth It includes phanerophyticclimate for the tropics therophytic for the xeric environments and hemicryptophytic forthe cold temperate region The present study identified seven different life-form classes inthe study area The most dominant life-form was hemicryptophytes with 19 species (33)followed by nanophanerophytes with 15 species (26) and therophytes with 13 species(22) Hemicryptophytes usually prevail in open physiognomies while phanerophytesare mainly in closed ones [5051] Biological spectra are important in comparing geographyand habitats and might change due to biotic influences viz grazing human activities andclimatic changes [52ndash54] Hemicryptophytes lose their aboveground parts during mostsummer and winter months while therophytes remain seeded to avoid summer droughtand cold winter stresses

Furthermore the flora of the study area is under anthropogenic pressure in the formof overgrazing and deforestation by nomadic and native people Nasir and Sultan [55]reported a similar finding from District Chakwal where therophytes were the dominantbiological spectra A community that therophytes dominate can be a characteristic fea-ture of a highly disturbed area under anthropogenic pressure [4854] In addition [56]reported therophytes as the dominant plant species of the rangeland district Tank Pak-istan and [57] assessed that therophytes is the leading life-form of Lahor District SwabiPakistan showing that the results of the current study are in compliance with the findingsof several other studies

Results of leaf size spectra trait revealed that species with microphyllous leaves domi-nated the area (with 24 species 41) followed by nanophylls (17 species 29) leptophylls(11 species 19) and mesophyll (5 species 9) Nonetheless 2 with megaphyllousleaf size was also recorded Microphyllous leaf size class is normally the characteristicfeature of meadow plant species while leptophylls and nanophylls are illustrative of hotdeserts [754] Comparable outcomes where microphylls and nanophylls overwhelmedthe vegetation and were reported in the work of researchers [7] and [45] where the authorslinked these two leaf size classes with the physiognomies of mild ranges A high rate ofmicrophylls may be identified with cool atmospheres of the sub-elevated and snowcappedareas Here as well the top layer was less settled containing a slim sheet that is notconclusive about the entrance of roots Microphyllous and nanophyllous leaves specieswere inexhaustible because of the biological variety for this dry condition The presentresults concur with [58] who detailed that microphylls and nanophylls predominance inthe dry mild atmosphere of District Quetta Our inferences additionally uncovered that thehigh extent in leaf size class changes with increasing altitude and the rate of microphyllswas emphatically connected with this as well [5960]

Among the 58 species documented 43 plant species were found in association withgroup III clustered by applying Wardrsquos agglomerative clustering which indicates widesociability of the species in the studied oak-dominated forests Moreover the analysisreveals that B lycium (782) C arvensis (687) and A trichomanes (66) were the mostabundant species in group III Group II was less diverse in terms of understory speciesnumbering in total of 25 plant species In this group Calamintha vulgaris (L) H KarstDryopteris stewartii Fraser-Jenk and Plantago lanceolata L were dominant (115 934 and986 respectively) Plant species in the understory with varying degrees of resistance tothese factors prefer a specific forest type Since certain plant species are limited to a specificforest type the extinction of that forest could result in the extinction of certain understoryplants [2761]

According to a recent analysis the richness and diversity of understory species inoak forests differed greatly depending on canopy dominants Herbaceous species abun-dance and α-diversity were highest in the oaks forest but there was less heterogeneity(β-diversity) across sites and major groups These findings highlight the importance of oakforests in protecting habitat and plant composition in the understory vegetation An herb

Appl Sci 2021 11 11372 14 of 17

layer with higher species abundance and diversity in oak forests may be due to highersolar radiation on south-facing slopes which is better for herbaceous species [62ndash64]

Environmental variables such as geographic parameters and physiochemical soilcharacteristics are important in determining the community structure and composition [65]In particular latitude and altitude were found to vary significantly in the understory groupsClay particles in soil texture and bulk density saturation point and electrical conductivityvaried significantly in the understory vegetation Similarly in the same region [66] thesoil parameters in understory vegetation of Pinus wallichiana AB Jacks dominated foresthave been studied revealing that elevation slope and phosphorus are vital factors indetermining the understory vegetation An oak species Q rubur L was also reported asa major associated species Furthermore many other researchers from other parts of theworld have reported that edaphic factors can significantly affect the species compositionand species diversity in plant communities [1066ndash68]

Forward selection of the RDA ordination revealed that latitude elevation clay wiltingpoint bulk density saturation and electric conductivity were significantly influential indetermining the understory vegetation of oak-dominated forests These results followthe findings of many other previous studies [12596970] Ali and Begum [62] also in-vestigated the vegetation of Swat and determined congruent results by stating a strongrelationship between vegetation and edaphic factors Many other researchers worldwidehave recorded that soil characteristics matter more than canopy organisms in decidingunderstory vegetation [62ndash6470] The study of species composition analysis in the oak-dominated forest revealed a general pattern of variation in the community diversity andspecies composition A similar pattern of species composition was also reported by [65] inP wallachiana understory from the same region The species diversity was found to increasewith time as Beg and Mirza [29] reported only 36 understory species due to the increase inanthropogenic activities

5 Conclusions

The current study reveals that Swat oak forests have rich floristic diversity with domi-nance of the therophytic life-form and microphyllous leaf size class indicating sub-tropicaland moist temperate type climates The species diversity was observed to increase duringthe spring and summer seasons and decreased later in the autumn As the winter seasonapproaches the decline in diversity was observed associated with dry environmentalconditions slow growth rate and other climatic factors Nonetheless critical impactsof seasonal variation on life-forms and overall species diversity were evident Among58 species 43 plant species were associated with group III clustered by applying Wardrsquosagglomerative clustering indicating the wide sociability of the species in the studied oak-dominated forests The understory vegetation of these forests plays an important role inthe forest ecology of the region

Moreover the environmental and soil variables ie latitude elevation clay percent-age wilting point electrical conductivity and potassium (mgKg) affect the understoryvegetation In addition important overstory variables like Quercus IVI and Total IVI ofoverstory were also found to affect the understory vegetation in oak-dominated forestsFurther it is concluded that the area is vulnerable due to the pressure from the localinhabitants in the form of overgrazing and deforestation which may significantly affectthe understory vegetation This information is particularly important for the success ofefforts intended to prevent the loss of genetic diversity of species within these forestsby destroying their natural habitats Moreover it is imperative to conserve the arearsquosbiodiversity and provide alternative means of livelihood for the local communities thatmay allow sustainable utilization and conservation of the invaluable biodiversity of thisarea for future generations

Appl Sci 2021 11 11372 15 of 17

Author Contributions The research work was designed and supervised by NK AR carried outthe field and laboratory work data analysis and manuscript writing RU also contributed tomanuscript writing and data collection KA DAJ and MEHK provided valuable informationand comments on the initial draft and refine the text in addition to language editing and data analysisIUR provided valuable suggestions during the write-up process and data analysis All authorshave read and agreed to the published version of the manuscript

Funding The research was conducted as a PhD project and did not receive support from anyfunding agency

Institutional Review Board Statement Not applicable

Informed Consent Statement Not applicable

Data Availability Statement All the data analyzedgenerated are included and available inthis manuscript

Acknowledgments We express our gratitude towards the Master students enrolled in the Depart-ment of Botany and the people of Malakand Division who helped with the fieldwork for this projectWe thank Achim Braumluning (Institute of Geography Department of Geography and GeosciencesFriedrich-Alexander-University (FAU) Erlangen-Nuremberg Erlangen Germany) for insightfulcomments that substantially improved the early version We also acknowledged the anonymous re-viewers and editors of the Applied Sciences journal for their valuable comment and language editing

Conflicts of Interest We hereby declare that all the authors have participated in this study and thedevelopment of the manuscript All the authors have read the final version and consent for the articleto be published in the Applied Sciences

References1 Musarella CM Mendoza-Fernaacutendez AJ Mota JF Alessandrini JFMA Bacchetta G Brullo GBS Caldarella O

Ciaschetti OCG Conti F Di Martino FCL et al Checklist of gypsophilous vascular flora in Italy Phyto Keys 2018 103 61ndash82[CrossRef] [PubMed]

2 Perrino EV Signorile G Checklist of the vascular flora from the Monopoli coast (Apulia) Ital Bot 2009 41 263ndash2793 Shah M Farrukh HSyed NMSImran AHumaira W Life Form And Floristic Characteristics Along Altitudinal Gradient Of

Humid Temperate Forests Located In Remote Area Of Pakistan Glob J Biodivers Sci Manag 2013 3 276ndash2814 Rafaqat M An Annotated Checklist of Amphibians and Reptiles of Margalla Hills National Park Pakistan Pak J Zool 2011 43

1041ndash10485 Shimwell DW Festuco-Brometea Br-Bl amp R Tx 1943 in the British isles The Phytogeography and Phytosociology of Limestone

Grasslands Part I (A) General Introduction(B) Xerobromion in England Vegetatio 1971 23 1ndash276 Raunkiaer C The Life Forms of Plants and Statistical Plant Geography Being the Collected Papers of C Raunkiaer In The Life

Forms of Plants and Statistical Plant Geography Being the Collected Papers of C Raunkiaer Clarendon Press Oxford UK 19347 Oosting HJ Hess DW Microclimate and a relic stand of Tsuga canadensis in the lower piedmont of North Carolina Ecology

1956 37 28ndash39 [CrossRef]8 Bailey IW Sinnott EW A botanical index of Cretaceous and Tertiary climates Science 1915 41 831ndash834 [CrossRef]9 Cain SA De Oliveira Castro GM Manual of Vegetation Analysis Haper and Row New York NY USA 195910 Augusto L Dupouey JL Ranger J Effects of tree species on understory vegetation and environmental conditions in temperate

forests Ann For Sci 2003 60 823ndash831 [CrossRef]11 Gracia M Montaneacute F Piqueacute J Retana J Overstory structure and topographic gradients determining diversity and abundance

of understory shrub species in temperate forests in central Pyrenees (NE Spain) For Ecol Manag 2007 242 391ndash397 [CrossRef]12 Gilliam FS The ecological significance of the herbaceous layer in temperate forest ecosystems Bioscience 2007 57 845ndash858

[CrossRef]13 Messier C Parent S Bergeron Y Effects of overstory and understory vegetation on the understory light environment in mixed

boreal forests J Veg Sci 1998 9 511ndash520 [CrossRef]14 Nilsson MC Wardle DA Understory vegetation as a forest ecosystem driver Evidence from the northern Swedish boreal

forest Front Ecol Environ 2005 3 421ndash428 [CrossRef]15 Bartels SF Chen HYH Is understory plant species diversity driven by resource quantity or resource heterogeneity Ecology

2010 91 1931ndash1938 [CrossRef] [PubMed]16 Dauber J Hirsch M Simmering D Waldhardt R Otte A Wolters V Landscape structure as an indicator of biodiversity

Matrix effects on species richness Agric Ecosyst Environ 2003 98 321ndash329 [CrossRef]17 Duguid MC Frey BR Ellum DS Kelty M Ashton MS The influence of ground disturbance and gap position on understory

plant diversity in upland forests of southern New England For Ecol Manag 2013 303 148ndash159 [CrossRef]

Appl Sci 2021 11 11372 8 of 17

Appl Sci 2021 11 x FOR PEER REVIEW 8 of 18

33 Understory Classification

A total of 58 plant species were recorded as associates in the understory vegetation

and clustered into three major groups by applying Wardrsquos agglomerative clustering (Fig-

ure 4 and Table 2) Among 58 species 43 plant species were found in association with

group III clearly indicating the speciesrsquo wide sociability in the studied oak-dominated

forests Moreover the analysis reveals that IVI of Berberis lycium Royle (782) Convolvulus

arvensis L (687) and Asplenium trichomanes L (66) were the most abundant species in

group III Group II was recorded intermediately diverse in understory species having 25

plant species with Calamintha vulgaris (L) H Karst Dryopteris stewartii Fraser-Jenk and

Plantago lanceolata L as the dominant associates having IVI of 115 934 and 986 respec-

tively The results revealed group I as the less diverse in terms of species (18 species) and

B lycium having IVI of 986 A trichomanes (914) and Indigofera heterantha Wall ex Brandis

(893) were the most abundant species

Figure 4 Cluster dendrogram classifying understory vegetation into three distinct groups Note G

(Group) St (Stand)

Table 2 Understory flora associated with oak-dominated forest recorded in the three clusters separated by Wardrsquos ag-

glomerative clustering procedure

Species Name Code Cluster I Cluster II Cluster III

M plusmn SE M plusmn SE M plusmn SE

Achyranthes aspera L As 241 plusmn 241 - -

Adiantum venustum D Don Av - - 077 plusmn 077

Ajuga bracteosa Wall ex Benth Ab 387 plusmn 265 - -

Amaranthus viridis L Am 510 plusmn 323 - 241 plusmn 144

Arabidopsis thaliana (L) Heynh At - - 116 plusmn 079

Arenaria serpyllifolia L Am - - 053 plusmn 053

Artimisia vulgaris L Av 72 plusmn 471 - -

Figure 4 Cluster dendrogram classifying understory vegetation into three distinct groups NoteG (Group) St (Stand)

Table 2 Understory flora associated with oak-dominated forest recorded in the three clusters separated by Wardrsquosagglomerative clustering procedure

Species Name CodeCluster I Cluster II Cluster III

M plusmn SE M plusmn SE M plusmn SE

Achyranthes aspera L As 241 plusmn 241 - -Adiantum venustum D Don Av - - 077 plusmn 077

Ajuga bracteosa Wall ex Benth Ab 387 plusmn 265 - -Amaranthus viridis L Am 510 plusmn 323 - 241 plusmn 144

Arabidopsis thaliana (L) Heynh At - - 116 plusmn 079Arenaria serpyllifolia L Am - - 053 plusmn 053

Artimisia vulgaris L Av 72 plusmn 471 - -Asplenium trichomanes L As 914 plusmn 471 423 plusmn 423 66 plusmn 26

Astragalus grahamianus Benth Ag - - 053 plusmn 053Atropa acuminata Royle ex Lindl Aa 34 plusmn 346 - 242 plusmn 243

Berberis lycium Royle B 986 plusmn 549 766 plusmn 491 782 plusmn 354Bidens cernua L Bc - 171 plusmn 171 -

Buddleja asiatica Lour Ba 093 plusmn 093 - 169 plusmn 117Calamintha vulgaris (L) H Karst Cv - 115 plusmn 411 346 plusmn 166

Chenopodium album L Ca - 44 plusmn 442 -Convolvulus arvensis L Ca 25 plusmn 252 42 plusmn 274 687 plusmn 176Erigeron canadensis L Co 085 plusmn 085 - -

Cynodon dactylon (L) Pers Cd 7 plusmn 5 617 plusmn 617 488 plusmn 332Daphne mucronata Royle Dm 383 plusmn 383 - 194 plusmn 134

Dioscorea deltoidea Wall ex Griseb Dd 183 plusmn 183 - -Dodonaea viscosa Jacq Do 142 plusmn 142 - -

Dryopteris stewartii Fraser-Jenk Ds - 986 plusmn 986 -Elaeagnus angustifolia L Ea 23 plusmn 23 - -Festuca gigantea (L) Vill Fg - - 046 plusmn 046

Appl Sci 2021 11 11372 9 of 17

Table 2 Cont

Species Name CodeCluster I Cluster II Cluster III

M plusmn SE M plusmn SE M plusmn SE

Fragaria indica Andrews Fi - 271 plusmn 271 553 plusmn 222Galium asperifolium Wall Ga 436 plusmn 436 - 134 plusmn 134

Hibiscus syriacus L Hs - - 06 plusmn 062Indigofera gerardiana Graham ex Baker Ig - - 365 plusmn 286Indigofera heterantha Wall ex Brandis Ih 893 plusmn 893 - -Isodon rugosus (Wall ex Benth) Codd Ir - 82 plusmn 82 -

justica adathoda L Ja - - 196 plusmn 145Lamium album L La - - 053 plusmn 053

Lespedeza juncea (L f) Pers Lj 502 plusmn 502 - 291 plusmn 291Lotus corniculatus L Lc 25 plusmn 25 - 252 plusmn 157Malva neglecta Wallr Mn - - 106 plusmn 106Medicago lupulina L Ml - - 121 plusmn 121Myrsine africana L Ma 45 plusmn 37 185 plusmn 185 596 plusmn 253

Origanum vulgare L Ov - 26 plusmn 268 -Otostegia limbata (Benth) Boiss Ol - - 160 plusmn 113Oxytropis mollis Royle ex Benth Om 363 plusmn 363 171 plusmn 171 336 plusmn 197

Plantago lanceolata L Pl 23 plusmn 23 934 plusmn 615 605 plusmn 329Plantago major L Pm - 59 plusmn 4 046 plusmn 046

Polygonatum verticillatum (L) All Pv - 171 plusmn 171 -Pteris cretica L Pc - - 167 plusmn 118

Ranunculus laetus Salisb Rl - - 093 plusmn 093Rosa webbiana Wall ex Royle Rw - - -Rumex denticulatus K Koch Ru - - 449 plusmn 257

Rumex nepalensis Spreng Rn - 357 plusmn 357 053 plusmn 053Sarcococca saligna (DDon) MuumlllArg Ss - - 053 plusmn 053

Smilax lanceolata L Sl 1 plusmn 12 - 308 plusmn 179Solidago virgaurea L Sv - - 053 plusmn 053

Tagetes minuta L Tg 502 plusmn 502 - 121 plusmn 121Taraxacum officinale (L) Weber ex

FHWigg To - - 06 plusmn 061

Trifolium repens L Tr - - 136 plusmn 095Viburnum grandiflorum Wall ex DC Vg - - 228 plusmn 228

Viola serpens Wall ex Ging Vs - - 135 plusmn 094Youngia japonica (L) DC Yj - 27 plusmn 272 -

Zanthoxylum armatum DC Za - - 106 plusmn 106

Note - Represent absence of specie in particular group

34 Understory Species Diversity and Richness

Significant differences in species richness (p lt 0015) ShannonndashWiener Margalef(p lt 000076) Simpson (p lt 0040) and Beta indexes were detected among three majorgroups of the understory layer of oak-dominated forests (Table 3) Nonetheless Pielousevenness was found non-significantly different (p gt 005) among the three major groups ofunderstory vegetation Group III had the highest species richness (103) α-diversity (274)and β-diversity (985) and the highest value of Margalef index (395) On the contrary thegroup I had the highest Pielous and Simpson index values with 097 and 713 respectively(Table 3)

Appl Sci 2021 11 11372 10 of 17

Table 3 Species richness and diversity indexes of oak-dominated forests of Swat Pakistan

IndexesGroup I Group II Group III

F pMean plusmn SE Mean plusmn SE Mean plusmn SE

Total number of Species (S) 587 plusmn 066 b 4 plusmn 037 a 1032 plusmn 15 b 485 0015ShannonndashWiener Index (H) 184 plusmn 019 a 13 plusmn 011 a 274 plusmn 020 b 1393 697 times 10minus5

Pielous Index (J) 097 plusmn 001 095 plusmn 001 093 plusmn 001 209 014Margalef Index (M) 29 plusmn 033 a 14 plusmn 021 a 395 plusmn 042 b 948 000076

Simpson Index (1D) 713 plusmn 110 a 368 plusmn 042 b 6 plusmn 061 a 361 004Beta diversity (B = Sa) 641 plusmn 127 a 368 plusmn 043 a 985 plusmn 054 b 1645 213 times 10minus5

Note Different superscript letters mean significant variation at p lt 05 tested by post hoc Tukey HSD insignificant variations haveno superscript

35 Influence of Physiographic and Edaphic Variables on the Understory Species Composition

In the ordination analysis the permutation test revealed that the eigenvalues for thefirst axis and those for all canonical axes were significant (p lt 001) and indicated thatunderstory species composition was influenced by physiographic and edaphic variables(Figure 5) All three axes explained 65 of the cumulative variance and 308 of thevariance in the relationship among understory species composition (Table 4) Forwardselection of the RDA ordination revealed that seven variables (ie latitude elevationclay wilting point bulk density saturation and electric conductivity) were the significantinfluential among all 23 variables in relation to the understory vegetation of oak-dominatedforests (Table 5) Group I (Quercus balootndashPinus roxburghii community) which lies at anintermediate elevation among the three communities has lower quantities of organic matterLime Nitrogen and Potassium In contrast group II (Quercus semecarpifoliandashQuercus rubur)which lies at a higher elevation has higher quantities of these nutrients Moreover in theordination axes summery the first axis was significantly associated with total importancevalue index (r = 0639) potassium (r = 0363) and elevation (r = 0239) The second axiswas found in close relation with QIVI (r = minus0414) wilting point (r = minus0374) and clay(r = minus0369) While the third axis was found in close correlation with silt (r = 0381) lime(r = 0395) and available water (r = minus0377) (Table 6)

Table 4 Ordination analysis of the understory vegetation concerning physiographic andedaphic variables

Axis Axis 1 Axis 2 Axis 3

Eigenvalue 3327 2512 2396

Variance in species data

of variance explained 1242 941 9Cumulative explained 1241 2181 3082

Pearson Correlation Response-Pred 100 098 1Kendall Correlation Response-Pred 096 081 099

Symbol of steric show signidicant of the data

Table 5 Average values (Mean plusmn stand error) of the environmental variables ie topographic edaphic and soil in thethree community types (vegetation groups) separated by Wardrsquos agglomerative cluster analysis The three groups wereGroup I (Quercus balootndashPinus roxburghii) Group II (Quercus semecarpifoliandashQuercus robur) and Group III (QuercuslanatandashOlea ferruginea)

Environmental Variables CodeGroup I Group II Group III

F-Value p-ValueMean plusmn SE Mean plusmn SE Mean plusmn SE

Latitude () Lat 350 plusmn 012 a 349694 plusmn 019 b 3458 plusmn 0050 b 557 0009Longitude () Long 7228 plusmn 003 7229 plusmn 0023 7225 plusmn 0016 172 019Elevation (m) Elev 201775 plusmn 20523 a 22895 plusmn 24022 b 16594 plusmn 6448 a 487 0015

Slope () Slope 418 plusmn 181 4114 plusmn 255 3866 plusmn 114 115 033Clay () CLY 1637 plusmn 117 a 175 plusmn 22 a 1211 plusmn 102 b 465 001

Appl Sci 2021 11 11372 11 of 17

Table 5 Cont

Environmental Variables CodeGroup I Group II Group III

F-Value p-ValueMean plusmn SE Mean plusmn SE Mean plusmn SE

Silt () SLT 2444 plusmn 220 26 plusmn 36 2903 plusmn 274 066 052Sand () SND 5918 plusmn 266 5638 plusmn 342 5885 plusmn 308 017 084pH (15) pH 64 plusmn 012 66 plusmn 017 626 plusmn 013 125 030

Organic matter () OM 221 plusmn 078 462 plusmn 076 261 plusmn 054 292 007Lime () L 316 plusmn 052 406 plusmn 061 361 plusmn 038 066 052

Nitrogen (mgKg) N 012 plusmn 004 018 plusmn 003 016 plusmn 003 0503 060Phosphorus (mgKg) P 824 plusmn 063 744 plusmn 112 1294 plusmn 446 061 054Potassium (mgKg) K 14625 plusmn 2707 23342 plusmn 3752 18633 plusmn 2633 155 022

Wilting point (mLgm) WP 0114 plusmn 042 011 plusmn 009 009 plusmn 0004 436 002Field capacity (mLgm) FC 022 plusmn 061 023 plusmn 009 021 plusmn 007 131 028

Bulk density (gcm3) BD 14 plusmn 011 a 146 plusmn 002 a 152 plusmn 001 ab 343 004Saturation Point (0 kPa) SP 044 plusmn 052 a 044 plusmn 0008 a 042 plusmn 006 ab 341 004

Electrical Conductivity (mSm) EC 1241 plusmn 163 a 128 plusmn 003 a 2346 plusmn 280 b 544 001Available water () AW 010 plusmn 038 011 plusmn 0005 011 plusmn 004 046 063

Temperature minimum (C) Tpmi 1430 plusmn 192 1188 plusmn 037 1189 plusmn 017 213 014Temperature maximum (F) Tpma 2898 plusmn 875 2789 plusmn 533 3646 plusmn 575 211 014

Precipitation (mm) Preci 4984 plusmn 121 4916 plusmn 186 5184 plusmn 097 132 028Relative humidity () RH 4984 plusmn 122 4916 plusmn 187 5184 plusmn 098 132 028

Water Holding capacity () WHC 5212 plusmn 182 5482 plusmn 198 5347 plusmn 289 018 083

Note Different superscript letters mean significant variation at p lt 05 tested by post hoc Tukey HSD insignificant variations haveno superscript

Table 6 Results of the RDA showed correlation coefficients between the physiographic and edaphicvariables and the RDA axes and biplot scores of each variable on all the three axes

S No VariablesCorrelation Biplot Scores

Axis 1 Axis 2 Axis 3 Axis 1 Axis 2 Axis 3

1 Lat minus006 minus049 minus002 minus055 minus394 minus01552 Long minus019 018 minus022 minus181 148 minus1743 E 023 minus039 006 218 minus309 05184 ASP 008 minus009 016 074 minus074 1255 CLY 019 minus036 minus019 177 minus292 minus1486 SLT minus020 029 038 minus183 228 2957 SND 009 minus009 minus026 085 minus072 minus2038 pH 022 minus022 minus021 197 minus172 minus1639 OM 009 016 minus0003 088 126 minus002

10 L 021 017 minus039 196 132 minus30511 N 022 009 minus002 182 075 minus01812 P 0007 minus013 020 007 minus106 15613 K 036 minus004 minus012 331 minus031 minus09614 WP 018 minus037 minus018 166 minus296 minus13915 FC 003 minus013 009 027 minus105 07216 BD minus010 030 005 minus093 237 04217 SP 0104 minus031 minus005 095 minus238 minus03718 EC minus0121 043 013 minus111 341 100419 AW minus0176 025 038 minus160 197 29220 TIVI minus063 minus047 002 minus583 minus379 01721 QIVI 0162 minus041 013 148 minus328 09722 BA minus0025 minus011 022 minus023 minus088 15523 Dha 0112 minus022 minus017 102 minus178 minus12824 TpMi minus0246 minus009 minus004 minus224 minus077 minus03425 TpMa minus0185 001 032 minus168 011 24826 Preci 0259 minus009 003 236 minus071 02427 RH 0102 minus005 minus004 0935 minus037 minus03528 WHC minus0273 0005 0079 minus249 004 061

Note (p lt 005) (p lt 001)

Appl Sci 2021 11 11372 12 of 17Appl Sci 2021 11 x FOR PEER REVIEW 12 of 18

Figure 5 RDA ordination of physiographic and edaphic variables concerning stands and the understory vegetation Note

Blue square represent the species point in the ordination biplot St (Stand number)

Table 6 Results of the RDA showed correlation coefficients between the physiographic and edaphic

variables and the RDA axes and biplot scores of each variable on all the three axes

S No Variables Correlation Biplot Scores

Axis 1 Axis 2 Axis 3 Axis 1 Axis 2 Axis 3

1 Lat minus006 minus049 minus002 minus055 minus394 minus0155

2 Long minus019 018 minus022 minus181 148 minus174

3 E 023 minus039 006 218 minus309 0518

4 ASP 008 minus009 016 074 minus074 125

5 CLY 019 minus036 minus019 177 minus292 minus148

6 SLT minus020 029 038 minus183 228 295

7 SND 009 minus009 minus026 085 minus072 minus203

8 pH 022 minus022 minus021 197 minus172 minus163

9 OM 009 016 minus0003 088 126 minus002

10 L 021 017 minus039 196 132 minus305

11 N 022 009 minus002 182 075 minus018

12 P 0007 minus013 020 007 minus106 156

13 K 036 minus004 minus012 331 minus031 minus096

Figure 5 RDA ordination of physiographic and edaphic variables concerning stands and the understory vegetation NoteBlue square represent the species point in the ordination biplot St (Stand number)

4 Discussion

Vegetation is a group of plants growing together in a particular locality [43] and it mayalso be defined as a unit that retains its unique structure and physiognomic characteristicsin an adequately great and sufficient way to permit their distinction from other units [46]The understory plant species in the oak-dominated forests consist of 58 species belongingto 32 families at 30 different locations in the Hindukush ranges of Swat The physiognomyof the studied area was dominated by herbaceous growth form with 47 plant species (81)followed by shrubs with 10 plant species (17) and trees with individual plant species(2) Herbaceous dominancy and less tree percentage might be due to altitudinal andgeographical variations which indicates that the climatic factors favor the herbaceous floraOur findings are associated with researchers in allied neighboring and national regions inwhich the species reported were mostly herbaceous [4748] Among all families Fabaceaewas recorded as the leading family with eight plant species followed by Asteraceae andLamiaceae with seven species each For instance several researchers [532ndash343846] forinstance [31] have documented Asteraceae and Fabaceae as the two most important fami-lies While other researchers [38] cited Lamiaceae and Rosaceae and [48] cited LamiaceaeMoraceae and Asteraceae as dominant plant families from Darra Adam Khel KP Pakistan

Appl Sci 2021 11 11372 13 of 17

Plant life-forms and vegetation are indicators of the climate [6] According to Meher-Homji [49] life-forms are reflective of the bioclimates of an area Raunkiaer [6] designedthree major phytoclimates based on life-form spectra on the earth It includes phanerophyticclimate for the tropics therophytic for the xeric environments and hemicryptophytic forthe cold temperate region The present study identified seven different life-form classes inthe study area The most dominant life-form was hemicryptophytes with 19 species (33)followed by nanophanerophytes with 15 species (26) and therophytes with 13 species(22) Hemicryptophytes usually prevail in open physiognomies while phanerophytesare mainly in closed ones [5051] Biological spectra are important in comparing geographyand habitats and might change due to biotic influences viz grazing human activities andclimatic changes [52ndash54] Hemicryptophytes lose their aboveground parts during mostsummer and winter months while therophytes remain seeded to avoid summer droughtand cold winter stresses

Furthermore the flora of the study area is under anthropogenic pressure in the formof overgrazing and deforestation by nomadic and native people Nasir and Sultan [55]reported a similar finding from District Chakwal where therophytes were the dominantbiological spectra A community that therophytes dominate can be a characteristic fea-ture of a highly disturbed area under anthropogenic pressure [4854] In addition [56]reported therophytes as the dominant plant species of the rangeland district Tank Pak-istan and [57] assessed that therophytes is the leading life-form of Lahor District SwabiPakistan showing that the results of the current study are in compliance with the findingsof several other studies

Results of leaf size spectra trait revealed that species with microphyllous leaves domi-nated the area (with 24 species 41) followed by nanophylls (17 species 29) leptophylls(11 species 19) and mesophyll (5 species 9) Nonetheless 2 with megaphyllousleaf size was also recorded Microphyllous leaf size class is normally the characteristicfeature of meadow plant species while leptophylls and nanophylls are illustrative of hotdeserts [754] Comparable outcomes where microphylls and nanophylls overwhelmedthe vegetation and were reported in the work of researchers [7] and [45] where the authorslinked these two leaf size classes with the physiognomies of mild ranges A high rate ofmicrophylls may be identified with cool atmospheres of the sub-elevated and snowcappedareas Here as well the top layer was less settled containing a slim sheet that is notconclusive about the entrance of roots Microphyllous and nanophyllous leaves specieswere inexhaustible because of the biological variety for this dry condition The presentresults concur with [58] who detailed that microphylls and nanophylls predominance inthe dry mild atmosphere of District Quetta Our inferences additionally uncovered that thehigh extent in leaf size class changes with increasing altitude and the rate of microphyllswas emphatically connected with this as well [5960]

Among the 58 species documented 43 plant species were found in association withgroup III clustered by applying Wardrsquos agglomerative clustering which indicates widesociability of the species in the studied oak-dominated forests Moreover the analysisreveals that B lycium (782) C arvensis (687) and A trichomanes (66) were the mostabundant species in group III Group II was less diverse in terms of understory speciesnumbering in total of 25 plant species In this group Calamintha vulgaris (L) H KarstDryopteris stewartii Fraser-Jenk and Plantago lanceolata L were dominant (115 934 and986 respectively) Plant species in the understory with varying degrees of resistance tothese factors prefer a specific forest type Since certain plant species are limited to a specificforest type the extinction of that forest could result in the extinction of certain understoryplants [2761]

According to a recent analysis the richness and diversity of understory species inoak forests differed greatly depending on canopy dominants Herbaceous species abun-dance and α-diversity were highest in the oaks forest but there was less heterogeneity(β-diversity) across sites and major groups These findings highlight the importance of oakforests in protecting habitat and plant composition in the understory vegetation An herb

Appl Sci 2021 11 11372 14 of 17

layer with higher species abundance and diversity in oak forests may be due to highersolar radiation on south-facing slopes which is better for herbaceous species [62ndash64]

Environmental variables such as geographic parameters and physiochemical soilcharacteristics are important in determining the community structure and composition [65]In particular latitude and altitude were found to vary significantly in the understory groupsClay particles in soil texture and bulk density saturation point and electrical conductivityvaried significantly in the understory vegetation Similarly in the same region [66] thesoil parameters in understory vegetation of Pinus wallichiana AB Jacks dominated foresthave been studied revealing that elevation slope and phosphorus are vital factors indetermining the understory vegetation An oak species Q rubur L was also reported asa major associated species Furthermore many other researchers from other parts of theworld have reported that edaphic factors can significantly affect the species compositionand species diversity in plant communities [1066ndash68]

Forward selection of the RDA ordination revealed that latitude elevation clay wiltingpoint bulk density saturation and electric conductivity were significantly influential indetermining the understory vegetation of oak-dominated forests These results followthe findings of many other previous studies [12596970] Ali and Begum [62] also in-vestigated the vegetation of Swat and determined congruent results by stating a strongrelationship between vegetation and edaphic factors Many other researchers worldwidehave recorded that soil characteristics matter more than canopy organisms in decidingunderstory vegetation [62ndash6470] The study of species composition analysis in the oak-dominated forest revealed a general pattern of variation in the community diversity andspecies composition A similar pattern of species composition was also reported by [65] inP wallachiana understory from the same region The species diversity was found to increasewith time as Beg and Mirza [29] reported only 36 understory species due to the increase inanthropogenic activities

5 Conclusions

The current study reveals that Swat oak forests have rich floristic diversity with domi-nance of the therophytic life-form and microphyllous leaf size class indicating sub-tropicaland moist temperate type climates The species diversity was observed to increase duringthe spring and summer seasons and decreased later in the autumn As the winter seasonapproaches the decline in diversity was observed associated with dry environmentalconditions slow growth rate and other climatic factors Nonetheless critical impactsof seasonal variation on life-forms and overall species diversity were evident Among58 species 43 plant species were associated with group III clustered by applying Wardrsquosagglomerative clustering indicating the wide sociability of the species in the studied oak-dominated forests The understory vegetation of these forests plays an important role inthe forest ecology of the region

Moreover the environmental and soil variables ie latitude elevation clay percent-age wilting point electrical conductivity and potassium (mgKg) affect the understoryvegetation In addition important overstory variables like Quercus IVI and Total IVI ofoverstory were also found to affect the understory vegetation in oak-dominated forestsFurther it is concluded that the area is vulnerable due to the pressure from the localinhabitants in the form of overgrazing and deforestation which may significantly affectthe understory vegetation This information is particularly important for the success ofefforts intended to prevent the loss of genetic diversity of species within these forestsby destroying their natural habitats Moreover it is imperative to conserve the arearsquosbiodiversity and provide alternative means of livelihood for the local communities thatmay allow sustainable utilization and conservation of the invaluable biodiversity of thisarea for future generations

Appl Sci 2021 11 11372 15 of 17

Author Contributions The research work was designed and supervised by NK AR carried outthe field and laboratory work data analysis and manuscript writing RU also contributed tomanuscript writing and data collection KA DAJ and MEHK provided valuable informationand comments on the initial draft and refine the text in addition to language editing and data analysisIUR provided valuable suggestions during the write-up process and data analysis All authorshave read and agreed to the published version of the manuscript

Funding The research was conducted as a PhD project and did not receive support from anyfunding agency

Institutional Review Board Statement Not applicable

Informed Consent Statement Not applicable

Data Availability Statement All the data analyzedgenerated are included and available inthis manuscript

Acknowledgments We express our gratitude towards the Master students enrolled in the Depart-ment of Botany and the people of Malakand Division who helped with the fieldwork for this projectWe thank Achim Braumluning (Institute of Geography Department of Geography and GeosciencesFriedrich-Alexander-University (FAU) Erlangen-Nuremberg Erlangen Germany) for insightfulcomments that substantially improved the early version We also acknowledged the anonymous re-viewers and editors of the Applied Sciences journal for their valuable comment and language editing

Conflicts of Interest We hereby declare that all the authors have participated in this study and thedevelopment of the manuscript All the authors have read the final version and consent for the articleto be published in the Applied Sciences

References1 Musarella CM Mendoza-Fernaacutendez AJ Mota JF Alessandrini JFMA Bacchetta G Brullo GBS Caldarella O

Ciaschetti OCG Conti F Di Martino FCL et al Checklist of gypsophilous vascular flora in Italy Phyto Keys 2018 103 61ndash82[CrossRef] [PubMed]

2 Perrino EV Signorile G Checklist of the vascular flora from the Monopoli coast (Apulia) Ital Bot 2009 41 263ndash2793 Shah M Farrukh HSyed NMSImran AHumaira W Life Form And Floristic Characteristics Along Altitudinal Gradient Of

Humid Temperate Forests Located In Remote Area Of Pakistan Glob J Biodivers Sci Manag 2013 3 276ndash2814 Rafaqat M An Annotated Checklist of Amphibians and Reptiles of Margalla Hills National Park Pakistan Pak J Zool 2011 43

1041ndash10485 Shimwell DW Festuco-Brometea Br-Bl amp R Tx 1943 in the British isles The Phytogeography and Phytosociology of Limestone

Grasslands Part I (A) General Introduction(B) Xerobromion in England Vegetatio 1971 23 1ndash276 Raunkiaer C The Life Forms of Plants and Statistical Plant Geography Being the Collected Papers of C Raunkiaer In The Life

Forms of Plants and Statistical Plant Geography Being the Collected Papers of C Raunkiaer Clarendon Press Oxford UK 19347 Oosting HJ Hess DW Microclimate and a relic stand of Tsuga canadensis in the lower piedmont of North Carolina Ecology

1956 37 28ndash39 [CrossRef]8 Bailey IW Sinnott EW A botanical index of Cretaceous and Tertiary climates Science 1915 41 831ndash834 [CrossRef]9 Cain SA De Oliveira Castro GM Manual of Vegetation Analysis Haper and Row New York NY USA 195910 Augusto L Dupouey JL Ranger J Effects of tree species on understory vegetation and environmental conditions in temperate

forests Ann For Sci 2003 60 823ndash831 [CrossRef]11 Gracia M Montaneacute F Piqueacute J Retana J Overstory structure and topographic gradients determining diversity and abundance

of understory shrub species in temperate forests in central Pyrenees (NE Spain) For Ecol Manag 2007 242 391ndash397 [CrossRef]12 Gilliam FS The ecological significance of the herbaceous layer in temperate forest ecosystems Bioscience 2007 57 845ndash858

[CrossRef]13 Messier C Parent S Bergeron Y Effects of overstory and understory vegetation on the understory light environment in mixed

boreal forests J Veg Sci 1998 9 511ndash520 [CrossRef]14 Nilsson MC Wardle DA Understory vegetation as a forest ecosystem driver Evidence from the northern Swedish boreal

forest Front Ecol Environ 2005 3 421ndash428 [CrossRef]15 Bartels SF Chen HYH Is understory plant species diversity driven by resource quantity or resource heterogeneity Ecology

2010 91 1931ndash1938 [CrossRef] [PubMed]16 Dauber J Hirsch M Simmering D Waldhardt R Otte A Wolters V Landscape structure as an indicator of biodiversity

Matrix effects on species richness Agric Ecosyst Environ 2003 98 321ndash329 [CrossRef]17 Duguid MC Frey BR Ellum DS Kelty M Ashton MS The influence of ground disturbance and gap position on understory

plant diversity in upland forests of southern New England For Ecol Manag 2013 303 148ndash159 [CrossRef]

Appl Sci 2021 11 11372 9 of 17

Table 2 Cont

Species Name CodeCluster I Cluster II Cluster III

M plusmn SE M plusmn SE M plusmn SE

Fragaria indica Andrews Fi - 271 plusmn 271 553 plusmn 222Galium asperifolium Wall Ga 436 plusmn 436 - 134 plusmn 134

Hibiscus syriacus L Hs - - 06 plusmn 062Indigofera gerardiana Graham ex Baker Ig - - 365 plusmn 286Indigofera heterantha Wall ex Brandis Ih 893 plusmn 893 - -Isodon rugosus (Wall ex Benth) Codd Ir - 82 plusmn 82 -

justica adathoda L Ja - - 196 plusmn 145Lamium album L La - - 053 plusmn 053

Lespedeza juncea (L f) Pers Lj 502 plusmn 502 - 291 plusmn 291Lotus corniculatus L Lc 25 plusmn 25 - 252 plusmn 157Malva neglecta Wallr Mn - - 106 plusmn 106Medicago lupulina L Ml - - 121 plusmn 121Myrsine africana L Ma 45 plusmn 37 185 plusmn 185 596 plusmn 253

Origanum vulgare L Ov - 26 plusmn 268 -Otostegia limbata (Benth) Boiss Ol - - 160 plusmn 113Oxytropis mollis Royle ex Benth Om 363 plusmn 363 171 plusmn 171 336 plusmn 197

Plantago lanceolata L Pl 23 plusmn 23 934 plusmn 615 605 plusmn 329Plantago major L Pm - 59 plusmn 4 046 plusmn 046

Polygonatum verticillatum (L) All Pv - 171 plusmn 171 -Pteris cretica L Pc - - 167 plusmn 118

Ranunculus laetus Salisb Rl - - 093 plusmn 093Rosa webbiana Wall ex Royle Rw - - -Rumex denticulatus K Koch Ru - - 449 plusmn 257

Rumex nepalensis Spreng Rn - 357 plusmn 357 053 plusmn 053Sarcococca saligna (DDon) MuumlllArg Ss - - 053 plusmn 053

Smilax lanceolata L Sl 1 plusmn 12 - 308 plusmn 179Solidago virgaurea L Sv - - 053 plusmn 053

Tagetes minuta L Tg 502 plusmn 502 - 121 plusmn 121Taraxacum officinale (L) Weber ex

FHWigg To - - 06 plusmn 061

Trifolium repens L Tr - - 136 plusmn 095Viburnum grandiflorum Wall ex DC Vg - - 228 plusmn 228

Viola serpens Wall ex Ging Vs - - 135 plusmn 094Youngia japonica (L) DC Yj - 27 plusmn 272 -

Zanthoxylum armatum DC Za - - 106 plusmn 106

Note - Represent absence of specie in particular group

34 Understory Species Diversity and Richness

Significant differences in species richness (p lt 0015) ShannonndashWiener Margalef(p lt 000076) Simpson (p lt 0040) and Beta indexes were detected among three majorgroups of the understory layer of oak-dominated forests (Table 3) Nonetheless Pielousevenness was found non-significantly different (p gt 005) among the three major groups ofunderstory vegetation Group III had the highest species richness (103) α-diversity (274)and β-diversity (985) and the highest value of Margalef index (395) On the contrary thegroup I had the highest Pielous and Simpson index values with 097 and 713 respectively(Table 3)

Appl Sci 2021 11 11372 10 of 17

Table 3 Species richness and diversity indexes of oak-dominated forests of Swat Pakistan

IndexesGroup I Group II Group III

F pMean plusmn SE Mean plusmn SE Mean plusmn SE

Total number of Species (S) 587 plusmn 066 b 4 plusmn 037 a 1032 plusmn 15 b 485 0015ShannonndashWiener Index (H) 184 plusmn 019 a 13 plusmn 011 a 274 plusmn 020 b 1393 697 times 10minus5

Pielous Index (J) 097 plusmn 001 095 plusmn 001 093 plusmn 001 209 014Margalef Index (M) 29 plusmn 033 a 14 plusmn 021 a 395 plusmn 042 b 948 000076

Simpson Index (1D) 713 plusmn 110 a 368 plusmn 042 b 6 plusmn 061 a 361 004Beta diversity (B = Sa) 641 plusmn 127 a 368 plusmn 043 a 985 plusmn 054 b 1645 213 times 10minus5

Note Different superscript letters mean significant variation at p lt 05 tested by post hoc Tukey HSD insignificant variations haveno superscript

35 Influence of Physiographic and Edaphic Variables on the Understory Species Composition

In the ordination analysis the permutation test revealed that the eigenvalues for thefirst axis and those for all canonical axes were significant (p lt 001) and indicated thatunderstory species composition was influenced by physiographic and edaphic variables(Figure 5) All three axes explained 65 of the cumulative variance and 308 of thevariance in the relationship among understory species composition (Table 4) Forwardselection of the RDA ordination revealed that seven variables (ie latitude elevationclay wilting point bulk density saturation and electric conductivity) were the significantinfluential among all 23 variables in relation to the understory vegetation of oak-dominatedforests (Table 5) Group I (Quercus balootndashPinus roxburghii community) which lies at anintermediate elevation among the three communities has lower quantities of organic matterLime Nitrogen and Potassium In contrast group II (Quercus semecarpifoliandashQuercus rubur)which lies at a higher elevation has higher quantities of these nutrients Moreover in theordination axes summery the first axis was significantly associated with total importancevalue index (r = 0639) potassium (r = 0363) and elevation (r = 0239) The second axiswas found in close relation with QIVI (r = minus0414) wilting point (r = minus0374) and clay(r = minus0369) While the third axis was found in close correlation with silt (r = 0381) lime(r = 0395) and available water (r = minus0377) (Table 6)

Table 4 Ordination analysis of the understory vegetation concerning physiographic andedaphic variables

Axis Axis 1 Axis 2 Axis 3

Eigenvalue 3327 2512 2396

Variance in species data

of variance explained 1242 941 9Cumulative explained 1241 2181 3082

Pearson Correlation Response-Pred 100 098 1Kendall Correlation Response-Pred 096 081 099

Symbol of steric show signidicant of the data

Table 5 Average values (Mean plusmn stand error) of the environmental variables ie topographic edaphic and soil in thethree community types (vegetation groups) separated by Wardrsquos agglomerative cluster analysis The three groups wereGroup I (Quercus balootndashPinus roxburghii) Group II (Quercus semecarpifoliandashQuercus robur) and Group III (QuercuslanatandashOlea ferruginea)

Environmental Variables CodeGroup I Group II Group III

F-Value p-ValueMean plusmn SE Mean plusmn SE Mean plusmn SE

Latitude () Lat 350 plusmn 012 a 349694 plusmn 019 b 3458 plusmn 0050 b 557 0009Longitude () Long 7228 plusmn 003 7229 plusmn 0023 7225 plusmn 0016 172 019Elevation (m) Elev 201775 plusmn 20523 a 22895 plusmn 24022 b 16594 plusmn 6448 a 487 0015

Slope () Slope 418 plusmn 181 4114 plusmn 255 3866 plusmn 114 115 033Clay () CLY 1637 plusmn 117 a 175 plusmn 22 a 1211 plusmn 102 b 465 001

Appl Sci 2021 11 11372 11 of 17

Table 5 Cont

Environmental Variables CodeGroup I Group II Group III

F-Value p-ValueMean plusmn SE Mean plusmn SE Mean plusmn SE

Silt () SLT 2444 plusmn 220 26 plusmn 36 2903 plusmn 274 066 052Sand () SND 5918 plusmn 266 5638 plusmn 342 5885 plusmn 308 017 084pH (15) pH 64 plusmn 012 66 plusmn 017 626 plusmn 013 125 030

Organic matter () OM 221 plusmn 078 462 plusmn 076 261 plusmn 054 292 007Lime () L 316 plusmn 052 406 plusmn 061 361 plusmn 038 066 052

Nitrogen (mgKg) N 012 plusmn 004 018 plusmn 003 016 plusmn 003 0503 060Phosphorus (mgKg) P 824 plusmn 063 744 plusmn 112 1294 plusmn 446 061 054Potassium (mgKg) K 14625 plusmn 2707 23342 plusmn 3752 18633 plusmn 2633 155 022

Wilting point (mLgm) WP 0114 plusmn 042 011 plusmn 009 009 plusmn 0004 436 002Field capacity (mLgm) FC 022 plusmn 061 023 plusmn 009 021 plusmn 007 131 028

Bulk density (gcm3) BD 14 plusmn 011 a 146 plusmn 002 a 152 plusmn 001 ab 343 004Saturation Point (0 kPa) SP 044 plusmn 052 a 044 plusmn 0008 a 042 plusmn 006 ab 341 004

Electrical Conductivity (mSm) EC 1241 plusmn 163 a 128 plusmn 003 a 2346 plusmn 280 b 544 001Available water () AW 010 plusmn 038 011 plusmn 0005 011 plusmn 004 046 063

Temperature minimum (C) Tpmi 1430 plusmn 192 1188 plusmn 037 1189 plusmn 017 213 014Temperature maximum (F) Tpma 2898 plusmn 875 2789 plusmn 533 3646 plusmn 575 211 014

Precipitation (mm) Preci 4984 plusmn 121 4916 plusmn 186 5184 plusmn 097 132 028Relative humidity () RH 4984 plusmn 122 4916 plusmn 187 5184 plusmn 098 132 028

Water Holding capacity () WHC 5212 plusmn 182 5482 plusmn 198 5347 plusmn 289 018 083

Note Different superscript letters mean significant variation at p lt 05 tested by post hoc Tukey HSD insignificant variations haveno superscript

Table 6 Results of the RDA showed correlation coefficients between the physiographic and edaphicvariables and the RDA axes and biplot scores of each variable on all the three axes

S No VariablesCorrelation Biplot Scores

Axis 1 Axis 2 Axis 3 Axis 1 Axis 2 Axis 3

1 Lat minus006 minus049 minus002 minus055 minus394 minus01552 Long minus019 018 minus022 minus181 148 minus1743 E 023 minus039 006 218 minus309 05184 ASP 008 minus009 016 074 minus074 1255 CLY 019 minus036 minus019 177 minus292 minus1486 SLT minus020 029 038 minus183 228 2957 SND 009 minus009 minus026 085 minus072 minus2038 pH 022 minus022 minus021 197 minus172 minus1639 OM 009 016 minus0003 088 126 minus002

10 L 021 017 minus039 196 132 minus30511 N 022 009 minus002 182 075 minus01812 P 0007 minus013 020 007 minus106 15613 K 036 minus004 minus012 331 minus031 minus09614 WP 018 minus037 minus018 166 minus296 minus13915 FC 003 minus013 009 027 minus105 07216 BD minus010 030 005 minus093 237 04217 SP 0104 minus031 minus005 095 minus238 minus03718 EC minus0121 043 013 minus111 341 100419 AW minus0176 025 038 minus160 197 29220 TIVI minus063 minus047 002 minus583 minus379 01721 QIVI 0162 minus041 013 148 minus328 09722 BA minus0025 minus011 022 minus023 minus088 15523 Dha 0112 minus022 minus017 102 minus178 minus12824 TpMi minus0246 minus009 minus004 minus224 minus077 minus03425 TpMa minus0185 001 032 minus168 011 24826 Preci 0259 minus009 003 236 minus071 02427 RH 0102 minus005 minus004 0935 minus037 minus03528 WHC minus0273 0005 0079 minus249 004 061

Note (p lt 005) (p lt 001)

Appl Sci 2021 11 11372 12 of 17Appl Sci 2021 11 x FOR PEER REVIEW 12 of 18

Figure 5 RDA ordination of physiographic and edaphic variables concerning stands and the understory vegetation Note

Blue square represent the species point in the ordination biplot St (Stand number)

Table 6 Results of the RDA showed correlation coefficients between the physiographic and edaphic

variables and the RDA axes and biplot scores of each variable on all the three axes

S No Variables Correlation Biplot Scores

Axis 1 Axis 2 Axis 3 Axis 1 Axis 2 Axis 3

1 Lat minus006 minus049 minus002 minus055 minus394 minus0155

2 Long minus019 018 minus022 minus181 148 minus174

3 E 023 minus039 006 218 minus309 0518

4 ASP 008 minus009 016 074 minus074 125

5 CLY 019 minus036 minus019 177 minus292 minus148

6 SLT minus020 029 038 minus183 228 295

7 SND 009 minus009 minus026 085 minus072 minus203

8 pH 022 minus022 minus021 197 minus172 minus163

9 OM 009 016 minus0003 088 126 minus002

10 L 021 017 minus039 196 132 minus305

11 N 022 009 minus002 182 075 minus018

12 P 0007 minus013 020 007 minus106 156

13 K 036 minus004 minus012 331 minus031 minus096

Figure 5 RDA ordination of physiographic and edaphic variables concerning stands and the understory vegetation NoteBlue square represent the species point in the ordination biplot St (Stand number)

4 Discussion

Vegetation is a group of plants growing together in a particular locality [43] and it mayalso be defined as a unit that retains its unique structure and physiognomic characteristicsin an adequately great and sufficient way to permit their distinction from other units [46]The understory plant species in the oak-dominated forests consist of 58 species belongingto 32 families at 30 different locations in the Hindukush ranges of Swat The physiognomyof the studied area was dominated by herbaceous growth form with 47 plant species (81)followed by shrubs with 10 plant species (17) and trees with individual plant species(2) Herbaceous dominancy and less tree percentage might be due to altitudinal andgeographical variations which indicates that the climatic factors favor the herbaceous floraOur findings are associated with researchers in allied neighboring and national regions inwhich the species reported were mostly herbaceous [4748] Among all families Fabaceaewas recorded as the leading family with eight plant species followed by Asteraceae andLamiaceae with seven species each For instance several researchers [532ndash343846] forinstance [31] have documented Asteraceae and Fabaceae as the two most important fami-lies While other researchers [38] cited Lamiaceae and Rosaceae and [48] cited LamiaceaeMoraceae and Asteraceae as dominant plant families from Darra Adam Khel KP Pakistan

Appl Sci 2021 11 11372 13 of 17

Plant life-forms and vegetation are indicators of the climate [6] According to Meher-Homji [49] life-forms are reflective of the bioclimates of an area Raunkiaer [6] designedthree major phytoclimates based on life-form spectra on the earth It includes phanerophyticclimate for the tropics therophytic for the xeric environments and hemicryptophytic forthe cold temperate region The present study identified seven different life-form classes inthe study area The most dominant life-form was hemicryptophytes with 19 species (33)followed by nanophanerophytes with 15 species (26) and therophytes with 13 species(22) Hemicryptophytes usually prevail in open physiognomies while phanerophytesare mainly in closed ones [5051] Biological spectra are important in comparing geographyand habitats and might change due to biotic influences viz grazing human activities andclimatic changes [52ndash54] Hemicryptophytes lose their aboveground parts during mostsummer and winter months while therophytes remain seeded to avoid summer droughtand cold winter stresses

Furthermore the flora of the study area is under anthropogenic pressure in the formof overgrazing and deforestation by nomadic and native people Nasir and Sultan [55]reported a similar finding from District Chakwal where therophytes were the dominantbiological spectra A community that therophytes dominate can be a characteristic fea-ture of a highly disturbed area under anthropogenic pressure [4854] In addition [56]reported therophytes as the dominant plant species of the rangeland district Tank Pak-istan and [57] assessed that therophytes is the leading life-form of Lahor District SwabiPakistan showing that the results of the current study are in compliance with the findingsof several other studies

Results of leaf size spectra trait revealed that species with microphyllous leaves domi-nated the area (with 24 species 41) followed by nanophylls (17 species 29) leptophylls(11 species 19) and mesophyll (5 species 9) Nonetheless 2 with megaphyllousleaf size was also recorded Microphyllous leaf size class is normally the characteristicfeature of meadow plant species while leptophylls and nanophylls are illustrative of hotdeserts [754] Comparable outcomes where microphylls and nanophylls overwhelmedthe vegetation and were reported in the work of researchers [7] and [45] where the authorslinked these two leaf size classes with the physiognomies of mild ranges A high rate ofmicrophylls may be identified with cool atmospheres of the sub-elevated and snowcappedareas Here as well the top layer was less settled containing a slim sheet that is notconclusive about the entrance of roots Microphyllous and nanophyllous leaves specieswere inexhaustible because of the biological variety for this dry condition The presentresults concur with [58] who detailed that microphylls and nanophylls predominance inthe dry mild atmosphere of District Quetta Our inferences additionally uncovered that thehigh extent in leaf size class changes with increasing altitude and the rate of microphyllswas emphatically connected with this as well [5960]

Among the 58 species documented 43 plant species were found in association withgroup III clustered by applying Wardrsquos agglomerative clustering which indicates widesociability of the species in the studied oak-dominated forests Moreover the analysisreveals that B lycium (782) C arvensis (687) and A trichomanes (66) were the mostabundant species in group III Group II was less diverse in terms of understory speciesnumbering in total of 25 plant species In this group Calamintha vulgaris (L) H KarstDryopteris stewartii Fraser-Jenk and Plantago lanceolata L were dominant (115 934 and986 respectively) Plant species in the understory with varying degrees of resistance tothese factors prefer a specific forest type Since certain plant species are limited to a specificforest type the extinction of that forest could result in the extinction of certain understoryplants [2761]

According to a recent analysis the richness and diversity of understory species inoak forests differed greatly depending on canopy dominants Herbaceous species abun-dance and α-diversity were highest in the oaks forest but there was less heterogeneity(β-diversity) across sites and major groups These findings highlight the importance of oakforests in protecting habitat and plant composition in the understory vegetation An herb

Appl Sci 2021 11 11372 14 of 17

layer with higher species abundance and diversity in oak forests may be due to highersolar radiation on south-facing slopes which is better for herbaceous species [62ndash64]

Environmental variables such as geographic parameters and physiochemical soilcharacteristics are important in determining the community structure and composition [65]In particular latitude and altitude were found to vary significantly in the understory groupsClay particles in soil texture and bulk density saturation point and electrical conductivityvaried significantly in the understory vegetation Similarly in the same region [66] thesoil parameters in understory vegetation of Pinus wallichiana AB Jacks dominated foresthave been studied revealing that elevation slope and phosphorus are vital factors indetermining the understory vegetation An oak species Q rubur L was also reported asa major associated species Furthermore many other researchers from other parts of theworld have reported that edaphic factors can significantly affect the species compositionand species diversity in plant communities [1066ndash68]

Forward selection of the RDA ordination revealed that latitude elevation clay wiltingpoint bulk density saturation and electric conductivity were significantly influential indetermining the understory vegetation of oak-dominated forests These results followthe findings of many other previous studies [12596970] Ali and Begum [62] also in-vestigated the vegetation of Swat and determined congruent results by stating a strongrelationship between vegetation and edaphic factors Many other researchers worldwidehave recorded that soil characteristics matter more than canopy organisms in decidingunderstory vegetation [62ndash6470] The study of species composition analysis in the oak-dominated forest revealed a general pattern of variation in the community diversity andspecies composition A similar pattern of species composition was also reported by [65] inP wallachiana understory from the same region The species diversity was found to increasewith time as Beg and Mirza [29] reported only 36 understory species due to the increase inanthropogenic activities

5 Conclusions

The current study reveals that Swat oak forests have rich floristic diversity with domi-nance of the therophytic life-form and microphyllous leaf size class indicating sub-tropicaland moist temperate type climates The species diversity was observed to increase duringthe spring and summer seasons and decreased later in the autumn As the winter seasonapproaches the decline in diversity was observed associated with dry environmentalconditions slow growth rate and other climatic factors Nonetheless critical impactsof seasonal variation on life-forms and overall species diversity were evident Among58 species 43 plant species were associated with group III clustered by applying Wardrsquosagglomerative clustering indicating the wide sociability of the species in the studied oak-dominated forests The understory vegetation of these forests plays an important role inthe forest ecology of the region

Moreover the environmental and soil variables ie latitude elevation clay percent-age wilting point electrical conductivity and potassium (mgKg) affect the understoryvegetation In addition important overstory variables like Quercus IVI and Total IVI ofoverstory were also found to affect the understory vegetation in oak-dominated forestsFurther it is concluded that the area is vulnerable due to the pressure from the localinhabitants in the form of overgrazing and deforestation which may significantly affectthe understory vegetation This information is particularly important for the success ofefforts intended to prevent the loss of genetic diversity of species within these forestsby destroying their natural habitats Moreover it is imperative to conserve the arearsquosbiodiversity and provide alternative means of livelihood for the local communities thatmay allow sustainable utilization and conservation of the invaluable biodiversity of thisarea for future generations

Appl Sci 2021 11 11372 15 of 17

Author Contributions The research work was designed and supervised by NK AR carried outthe field and laboratory work data analysis and manuscript writing RU also contributed tomanuscript writing and data collection KA DAJ and MEHK provided valuable informationand comments on the initial draft and refine the text in addition to language editing and data analysisIUR provided valuable suggestions during the write-up process and data analysis All authorshave read and agreed to the published version of the manuscript

Funding The research was conducted as a PhD project and did not receive support from anyfunding agency

Institutional Review Board Statement Not applicable

Informed Consent Statement Not applicable

Data Availability Statement All the data analyzedgenerated are included and available inthis manuscript

Acknowledgments We express our gratitude towards the Master students enrolled in the Depart-ment of Botany and the people of Malakand Division who helped with the fieldwork for this projectWe thank Achim Braumluning (Institute of Geography Department of Geography and GeosciencesFriedrich-Alexander-University (FAU) Erlangen-Nuremberg Erlangen Germany) for insightfulcomments that substantially improved the early version We also acknowledged the anonymous re-viewers and editors of the Applied Sciences journal for their valuable comment and language editing

Conflicts of Interest We hereby declare that all the authors have participated in this study and thedevelopment of the manuscript All the authors have read the final version and consent for the articleto be published in the Applied Sciences

References1 Musarella CM Mendoza-Fernaacutendez AJ Mota JF Alessandrini JFMA Bacchetta G Brullo GBS Caldarella O

Ciaschetti OCG Conti F Di Martino FCL et al Checklist of gypsophilous vascular flora in Italy Phyto Keys 2018 103 61ndash82[CrossRef] [PubMed]

2 Perrino EV Signorile G Checklist of the vascular flora from the Monopoli coast (Apulia) Ital Bot 2009 41 263ndash2793 Shah M Farrukh HSyed NMSImran AHumaira W Life Form And Floristic Characteristics Along Altitudinal Gradient Of

Humid Temperate Forests Located In Remote Area Of Pakistan Glob J Biodivers Sci Manag 2013 3 276ndash2814 Rafaqat M An Annotated Checklist of Amphibians and Reptiles of Margalla Hills National Park Pakistan Pak J Zool 2011 43

1041ndash10485 Shimwell DW Festuco-Brometea Br-Bl amp R Tx 1943 in the British isles The Phytogeography and Phytosociology of Limestone

Grasslands Part I (A) General Introduction(B) Xerobromion in England Vegetatio 1971 23 1ndash276 Raunkiaer C The Life Forms of Plants and Statistical Plant Geography Being the Collected Papers of C Raunkiaer In The Life

Forms of Plants and Statistical Plant Geography Being the Collected Papers of C Raunkiaer Clarendon Press Oxford UK 19347 Oosting HJ Hess DW Microclimate and a relic stand of Tsuga canadensis in the lower piedmont of North Carolina Ecology

1956 37 28ndash39 [CrossRef]8 Bailey IW Sinnott EW A botanical index of Cretaceous and Tertiary climates Science 1915 41 831ndash834 [CrossRef]9 Cain SA De Oliveira Castro GM Manual of Vegetation Analysis Haper and Row New York NY USA 195910 Augusto L Dupouey JL Ranger J Effects of tree species on understory vegetation and environmental conditions in temperate

forests Ann For Sci 2003 60 823ndash831 [CrossRef]11 Gracia M Montaneacute F Piqueacute J Retana J Overstory structure and topographic gradients determining diversity and abundance

of understory shrub species in temperate forests in central Pyrenees (NE Spain) For Ecol Manag 2007 242 391ndash397 [CrossRef]12 Gilliam FS The ecological significance of the herbaceous layer in temperate forest ecosystems Bioscience 2007 57 845ndash858

[CrossRef]13 Messier C Parent S Bergeron Y Effects of overstory and understory vegetation on the understory light environment in mixed

boreal forests J Veg Sci 1998 9 511ndash520 [CrossRef]14 Nilsson MC Wardle DA Understory vegetation as a forest ecosystem driver Evidence from the northern Swedish boreal

forest Front Ecol Environ 2005 3 421ndash428 [CrossRef]15 Bartels SF Chen HYH Is understory plant species diversity driven by resource quantity or resource heterogeneity Ecology

2010 91 1931ndash1938 [CrossRef] [PubMed]16 Dauber J Hirsch M Simmering D Waldhardt R Otte A Wolters V Landscape structure as an indicator of biodiversity

Matrix effects on species richness Agric Ecosyst Environ 2003 98 321ndash329 [CrossRef]17 Duguid MC Frey BR Ellum DS Kelty M Ashton MS The influence of ground disturbance and gap position on understory

plant diversity in upland forests of southern New England For Ecol Manag 2013 303 148ndash159 [CrossRef]

Appl Sci 2021 11 11372 10 of 17

Table 3 Species richness and diversity indexes of oak-dominated forests of Swat Pakistan

IndexesGroup I Group II Group III

F pMean plusmn SE Mean plusmn SE Mean plusmn SE

Total number of Species (S) 587 plusmn 066 b 4 plusmn 037 a 1032 plusmn 15 b 485 0015ShannonndashWiener Index (H) 184 plusmn 019 a 13 plusmn 011 a 274 plusmn 020 b 1393 697 times 10minus5

Pielous Index (J) 097 plusmn 001 095 plusmn 001 093 plusmn 001 209 014Margalef Index (M) 29 plusmn 033 a 14 plusmn 021 a 395 plusmn 042 b 948 000076

Simpson Index (1D) 713 plusmn 110 a 368 plusmn 042 b 6 plusmn 061 a 361 004Beta diversity (B = Sa) 641 plusmn 127 a 368 plusmn 043 a 985 plusmn 054 b 1645 213 times 10minus5

Note Different superscript letters mean significant variation at p lt 05 tested by post hoc Tukey HSD insignificant variations haveno superscript

35 Influence of Physiographic and Edaphic Variables on the Understory Species Composition

In the ordination analysis the permutation test revealed that the eigenvalues for thefirst axis and those for all canonical axes were significant (p lt 001) and indicated thatunderstory species composition was influenced by physiographic and edaphic variables(Figure 5) All three axes explained 65 of the cumulative variance and 308 of thevariance in the relationship among understory species composition (Table 4) Forwardselection of the RDA ordination revealed that seven variables (ie latitude elevationclay wilting point bulk density saturation and electric conductivity) were the significantinfluential among all 23 variables in relation to the understory vegetation of oak-dominatedforests (Table 5) Group I (Quercus balootndashPinus roxburghii community) which lies at anintermediate elevation among the three communities has lower quantities of organic matterLime Nitrogen and Potassium In contrast group II (Quercus semecarpifoliandashQuercus rubur)which lies at a higher elevation has higher quantities of these nutrients Moreover in theordination axes summery the first axis was significantly associated with total importancevalue index (r = 0639) potassium (r = 0363) and elevation (r = 0239) The second axiswas found in close relation with QIVI (r = minus0414) wilting point (r = minus0374) and clay(r = minus0369) While the third axis was found in close correlation with silt (r = 0381) lime(r = 0395) and available water (r = minus0377) (Table 6)

Table 4 Ordination analysis of the understory vegetation concerning physiographic andedaphic variables

Axis Axis 1 Axis 2 Axis 3

Eigenvalue 3327 2512 2396

Variance in species data

of variance explained 1242 941 9Cumulative explained 1241 2181 3082

Pearson Correlation Response-Pred 100 098 1Kendall Correlation Response-Pred 096 081 099

Symbol of steric show signidicant of the data

Table 5 Average values (Mean plusmn stand error) of the environmental variables ie topographic edaphic and soil in thethree community types (vegetation groups) separated by Wardrsquos agglomerative cluster analysis The three groups wereGroup I (Quercus balootndashPinus roxburghii) Group II (Quercus semecarpifoliandashQuercus robur) and Group III (QuercuslanatandashOlea ferruginea)

Environmental Variables CodeGroup I Group II Group III

F-Value p-ValueMean plusmn SE Mean plusmn SE Mean plusmn SE

Latitude () Lat 350 plusmn 012 a 349694 plusmn 019 b 3458 plusmn 0050 b 557 0009Longitude () Long 7228 plusmn 003 7229 plusmn 0023 7225 plusmn 0016 172 019Elevation (m) Elev 201775 plusmn 20523 a 22895 plusmn 24022 b 16594 plusmn 6448 a 487 0015

Slope () Slope 418 plusmn 181 4114 plusmn 255 3866 plusmn 114 115 033Clay () CLY 1637 plusmn 117 a 175 plusmn 22 a 1211 plusmn 102 b 465 001

Appl Sci 2021 11 11372 11 of 17

Table 5 Cont

Environmental Variables CodeGroup I Group II Group III

F-Value p-ValueMean plusmn SE Mean plusmn SE Mean plusmn SE

Silt () SLT 2444 plusmn 220 26 plusmn 36 2903 plusmn 274 066 052Sand () SND 5918 plusmn 266 5638 plusmn 342 5885 plusmn 308 017 084pH (15) pH 64 plusmn 012 66 plusmn 017 626 plusmn 013 125 030

Organic matter () OM 221 plusmn 078 462 plusmn 076 261 plusmn 054 292 007Lime () L 316 plusmn 052 406 plusmn 061 361 plusmn 038 066 052

Nitrogen (mgKg) N 012 plusmn 004 018 plusmn 003 016 plusmn 003 0503 060Phosphorus (mgKg) P 824 plusmn 063 744 plusmn 112 1294 plusmn 446 061 054Potassium (mgKg) K 14625 plusmn 2707 23342 plusmn 3752 18633 plusmn 2633 155 022

Wilting point (mLgm) WP 0114 plusmn 042 011 plusmn 009 009 plusmn 0004 436 002Field capacity (mLgm) FC 022 plusmn 061 023 plusmn 009 021 plusmn 007 131 028

Bulk density (gcm3) BD 14 plusmn 011 a 146 plusmn 002 a 152 plusmn 001 ab 343 004Saturation Point (0 kPa) SP 044 plusmn 052 a 044 plusmn 0008 a 042 plusmn 006 ab 341 004

Electrical Conductivity (mSm) EC 1241 plusmn 163 a 128 plusmn 003 a 2346 plusmn 280 b 544 001Available water () AW 010 plusmn 038 011 plusmn 0005 011 plusmn 004 046 063

Temperature minimum (C) Tpmi 1430 plusmn 192 1188 plusmn 037 1189 plusmn 017 213 014Temperature maximum (F) Tpma 2898 plusmn 875 2789 plusmn 533 3646 plusmn 575 211 014

Precipitation (mm) Preci 4984 plusmn 121 4916 plusmn 186 5184 plusmn 097 132 028Relative humidity () RH 4984 plusmn 122 4916 plusmn 187 5184 plusmn 098 132 028

Water Holding capacity () WHC 5212 plusmn 182 5482 plusmn 198 5347 plusmn 289 018 083

Note Different superscript letters mean significant variation at p lt 05 tested by post hoc Tukey HSD insignificant variations haveno superscript

Table 6 Results of the RDA showed correlation coefficients between the physiographic and edaphicvariables and the RDA axes and biplot scores of each variable on all the three axes

S No VariablesCorrelation Biplot Scores

Axis 1 Axis 2 Axis 3 Axis 1 Axis 2 Axis 3

1 Lat minus006 minus049 minus002 minus055 minus394 minus01552 Long minus019 018 minus022 minus181 148 minus1743 E 023 minus039 006 218 minus309 05184 ASP 008 minus009 016 074 minus074 1255 CLY 019 minus036 minus019 177 minus292 minus1486 SLT minus020 029 038 minus183 228 2957 SND 009 minus009 minus026 085 minus072 minus2038 pH 022 minus022 minus021 197 minus172 minus1639 OM 009 016 minus0003 088 126 minus002

10 L 021 017 minus039 196 132 minus30511 N 022 009 minus002 182 075 minus01812 P 0007 minus013 020 007 minus106 15613 K 036 minus004 minus012 331 minus031 minus09614 WP 018 minus037 minus018 166 minus296 minus13915 FC 003 minus013 009 027 minus105 07216 BD minus010 030 005 minus093 237 04217 SP 0104 minus031 minus005 095 minus238 minus03718 EC minus0121 043 013 minus111 341 100419 AW minus0176 025 038 minus160 197 29220 TIVI minus063 minus047 002 minus583 minus379 01721 QIVI 0162 minus041 013 148 minus328 09722 BA minus0025 minus011 022 minus023 minus088 15523 Dha 0112 minus022 minus017 102 minus178 minus12824 TpMi minus0246 minus009 minus004 minus224 minus077 minus03425 TpMa minus0185 001 032 minus168 011 24826 Preci 0259 minus009 003 236 minus071 02427 RH 0102 minus005 minus004 0935 minus037 minus03528 WHC minus0273 0005 0079 minus249 004 061

Note (p lt 005) (p lt 001)

Appl Sci 2021 11 11372 12 of 17Appl Sci 2021 11 x FOR PEER REVIEW 12 of 18

Figure 5 RDA ordination of physiographic and edaphic variables concerning stands and the understory vegetation Note

Blue square represent the species point in the ordination biplot St (Stand number)

Table 6 Results of the RDA showed correlation coefficients between the physiographic and edaphic

variables and the RDA axes and biplot scores of each variable on all the three axes

S No Variables Correlation Biplot Scores

Axis 1 Axis 2 Axis 3 Axis 1 Axis 2 Axis 3

1 Lat minus006 minus049 minus002 minus055 minus394 minus0155

2 Long minus019 018 minus022 minus181 148 minus174

3 E 023 minus039 006 218 minus309 0518

4 ASP 008 minus009 016 074 minus074 125

5 CLY 019 minus036 minus019 177 minus292 minus148

6 SLT minus020 029 038 minus183 228 295

7 SND 009 minus009 minus026 085 minus072 minus203

8 pH 022 minus022 minus021 197 minus172 minus163

9 OM 009 016 minus0003 088 126 minus002

10 L 021 017 minus039 196 132 minus305

11 N 022 009 minus002 182 075 minus018

12 P 0007 minus013 020 007 minus106 156

13 K 036 minus004 minus012 331 minus031 minus096

Figure 5 RDA ordination of physiographic and edaphic variables concerning stands and the understory vegetation NoteBlue square represent the species point in the ordination biplot St (Stand number)

4 Discussion

Vegetation is a group of plants growing together in a particular locality [43] and it mayalso be defined as a unit that retains its unique structure and physiognomic characteristicsin an adequately great and sufficient way to permit their distinction from other units [46]The understory plant species in the oak-dominated forests consist of 58 species belongingto 32 families at 30 different locations in the Hindukush ranges of Swat The physiognomyof the studied area was dominated by herbaceous growth form with 47 plant species (81)followed by shrubs with 10 plant species (17) and trees with individual plant species(2) Herbaceous dominancy and less tree percentage might be due to altitudinal andgeographical variations which indicates that the climatic factors favor the herbaceous floraOur findings are associated with researchers in allied neighboring and national regions inwhich the species reported were mostly herbaceous [4748] Among all families Fabaceaewas recorded as the leading family with eight plant species followed by Asteraceae andLamiaceae with seven species each For instance several researchers [532ndash343846] forinstance [31] have documented Asteraceae and Fabaceae as the two most important fami-lies While other researchers [38] cited Lamiaceae and Rosaceae and [48] cited LamiaceaeMoraceae and Asteraceae as dominant plant families from Darra Adam Khel KP Pakistan

Appl Sci 2021 11 11372 13 of 17

Plant life-forms and vegetation are indicators of the climate [6] According to Meher-Homji [49] life-forms are reflective of the bioclimates of an area Raunkiaer [6] designedthree major phytoclimates based on life-form spectra on the earth It includes phanerophyticclimate for the tropics therophytic for the xeric environments and hemicryptophytic forthe cold temperate region The present study identified seven different life-form classes inthe study area The most dominant life-form was hemicryptophytes with 19 species (33)followed by nanophanerophytes with 15 species (26) and therophytes with 13 species(22) Hemicryptophytes usually prevail in open physiognomies while phanerophytesare mainly in closed ones [5051] Biological spectra are important in comparing geographyand habitats and might change due to biotic influences viz grazing human activities andclimatic changes [52ndash54] Hemicryptophytes lose their aboveground parts during mostsummer and winter months while therophytes remain seeded to avoid summer droughtand cold winter stresses

Furthermore the flora of the study area is under anthropogenic pressure in the formof overgrazing and deforestation by nomadic and native people Nasir and Sultan [55]reported a similar finding from District Chakwal where therophytes were the dominantbiological spectra A community that therophytes dominate can be a characteristic fea-ture of a highly disturbed area under anthropogenic pressure [4854] In addition [56]reported therophytes as the dominant plant species of the rangeland district Tank Pak-istan and [57] assessed that therophytes is the leading life-form of Lahor District SwabiPakistan showing that the results of the current study are in compliance with the findingsof several other studies

Results of leaf size spectra trait revealed that species with microphyllous leaves domi-nated the area (with 24 species 41) followed by nanophylls (17 species 29) leptophylls(11 species 19) and mesophyll (5 species 9) Nonetheless 2 with megaphyllousleaf size was also recorded Microphyllous leaf size class is normally the characteristicfeature of meadow plant species while leptophylls and nanophylls are illustrative of hotdeserts [754] Comparable outcomes where microphylls and nanophylls overwhelmedthe vegetation and were reported in the work of researchers [7] and [45] where the authorslinked these two leaf size classes with the physiognomies of mild ranges A high rate ofmicrophylls may be identified with cool atmospheres of the sub-elevated and snowcappedareas Here as well the top layer was less settled containing a slim sheet that is notconclusive about the entrance of roots Microphyllous and nanophyllous leaves specieswere inexhaustible because of the biological variety for this dry condition The presentresults concur with [58] who detailed that microphylls and nanophylls predominance inthe dry mild atmosphere of District Quetta Our inferences additionally uncovered that thehigh extent in leaf size class changes with increasing altitude and the rate of microphyllswas emphatically connected with this as well [5960]

Among the 58 species documented 43 plant species were found in association withgroup III clustered by applying Wardrsquos agglomerative clustering which indicates widesociability of the species in the studied oak-dominated forests Moreover the analysisreveals that B lycium (782) C arvensis (687) and A trichomanes (66) were the mostabundant species in group III Group II was less diverse in terms of understory speciesnumbering in total of 25 plant species In this group Calamintha vulgaris (L) H KarstDryopteris stewartii Fraser-Jenk and Plantago lanceolata L were dominant (115 934 and986 respectively) Plant species in the understory with varying degrees of resistance tothese factors prefer a specific forest type Since certain plant species are limited to a specificforest type the extinction of that forest could result in the extinction of certain understoryplants [2761]

According to a recent analysis the richness and diversity of understory species inoak forests differed greatly depending on canopy dominants Herbaceous species abun-dance and α-diversity were highest in the oaks forest but there was less heterogeneity(β-diversity) across sites and major groups These findings highlight the importance of oakforests in protecting habitat and plant composition in the understory vegetation An herb

Appl Sci 2021 11 11372 14 of 17

layer with higher species abundance and diversity in oak forests may be due to highersolar radiation on south-facing slopes which is better for herbaceous species [62ndash64]

Environmental variables such as geographic parameters and physiochemical soilcharacteristics are important in determining the community structure and composition [65]In particular latitude and altitude were found to vary significantly in the understory groupsClay particles in soil texture and bulk density saturation point and electrical conductivityvaried significantly in the understory vegetation Similarly in the same region [66] thesoil parameters in understory vegetation of Pinus wallichiana AB Jacks dominated foresthave been studied revealing that elevation slope and phosphorus are vital factors indetermining the understory vegetation An oak species Q rubur L was also reported asa major associated species Furthermore many other researchers from other parts of theworld have reported that edaphic factors can significantly affect the species compositionand species diversity in plant communities [1066ndash68]

Forward selection of the RDA ordination revealed that latitude elevation clay wiltingpoint bulk density saturation and electric conductivity were significantly influential indetermining the understory vegetation of oak-dominated forests These results followthe findings of many other previous studies [12596970] Ali and Begum [62] also in-vestigated the vegetation of Swat and determined congruent results by stating a strongrelationship between vegetation and edaphic factors Many other researchers worldwidehave recorded that soil characteristics matter more than canopy organisms in decidingunderstory vegetation [62ndash6470] The study of species composition analysis in the oak-dominated forest revealed a general pattern of variation in the community diversity andspecies composition A similar pattern of species composition was also reported by [65] inP wallachiana understory from the same region The species diversity was found to increasewith time as Beg and Mirza [29] reported only 36 understory species due to the increase inanthropogenic activities

5 Conclusions

The current study reveals that Swat oak forests have rich floristic diversity with domi-nance of the therophytic life-form and microphyllous leaf size class indicating sub-tropicaland moist temperate type climates The species diversity was observed to increase duringthe spring and summer seasons and decreased later in the autumn As the winter seasonapproaches the decline in diversity was observed associated with dry environmentalconditions slow growth rate and other climatic factors Nonetheless critical impactsof seasonal variation on life-forms and overall species diversity were evident Among58 species 43 plant species were associated with group III clustered by applying Wardrsquosagglomerative clustering indicating the wide sociability of the species in the studied oak-dominated forests The understory vegetation of these forests plays an important role inthe forest ecology of the region

Moreover the environmental and soil variables ie latitude elevation clay percent-age wilting point electrical conductivity and potassium (mgKg) affect the understoryvegetation In addition important overstory variables like Quercus IVI and Total IVI ofoverstory were also found to affect the understory vegetation in oak-dominated forestsFurther it is concluded that the area is vulnerable due to the pressure from the localinhabitants in the form of overgrazing and deforestation which may significantly affectthe understory vegetation This information is particularly important for the success ofefforts intended to prevent the loss of genetic diversity of species within these forestsby destroying their natural habitats Moreover it is imperative to conserve the arearsquosbiodiversity and provide alternative means of livelihood for the local communities thatmay allow sustainable utilization and conservation of the invaluable biodiversity of thisarea for future generations

Appl Sci 2021 11 11372 15 of 17

Author Contributions The research work was designed and supervised by NK AR carried outthe field and laboratory work data analysis and manuscript writing RU also contributed tomanuscript writing and data collection KA DAJ and MEHK provided valuable informationand comments on the initial draft and refine the text in addition to language editing and data analysisIUR provided valuable suggestions during the write-up process and data analysis All authorshave read and agreed to the published version of the manuscript

Funding The research was conducted as a PhD project and did not receive support from anyfunding agency

Institutional Review Board Statement Not applicable

Informed Consent Statement Not applicable

Data Availability Statement All the data analyzedgenerated are included and available inthis manuscript

Acknowledgments We express our gratitude towards the Master students enrolled in the Depart-ment of Botany and the people of Malakand Division who helped with the fieldwork for this projectWe thank Achim Braumluning (Institute of Geography Department of Geography and GeosciencesFriedrich-Alexander-University (FAU) Erlangen-Nuremberg Erlangen Germany) for insightfulcomments that substantially improved the early version We also acknowledged the anonymous re-viewers and editors of the Applied Sciences journal for their valuable comment and language editing

Conflicts of Interest We hereby declare that all the authors have participated in this study and thedevelopment of the manuscript All the authors have read the final version and consent for the articleto be published in the Applied Sciences

References1 Musarella CM Mendoza-Fernaacutendez AJ Mota JF Alessandrini JFMA Bacchetta G Brullo GBS Caldarella O

Ciaschetti OCG Conti F Di Martino FCL et al Checklist of gypsophilous vascular flora in Italy Phyto Keys 2018 103 61ndash82[CrossRef] [PubMed]

2 Perrino EV Signorile G Checklist of the vascular flora from the Monopoli coast (Apulia) Ital Bot 2009 41 263ndash2793 Shah M Farrukh HSyed NMSImran AHumaira W Life Form And Floristic Characteristics Along Altitudinal Gradient Of

Humid Temperate Forests Located In Remote Area Of Pakistan Glob J Biodivers Sci Manag 2013 3 276ndash2814 Rafaqat M An Annotated Checklist of Amphibians and Reptiles of Margalla Hills National Park Pakistan Pak J Zool 2011 43

1041ndash10485 Shimwell DW Festuco-Brometea Br-Bl amp R Tx 1943 in the British isles The Phytogeography and Phytosociology of Limestone

Grasslands Part I (A) General Introduction(B) Xerobromion in England Vegetatio 1971 23 1ndash276 Raunkiaer C The Life Forms of Plants and Statistical Plant Geography Being the Collected Papers of C Raunkiaer In The Life

Forms of Plants and Statistical Plant Geography Being the Collected Papers of C Raunkiaer Clarendon Press Oxford UK 19347 Oosting HJ Hess DW Microclimate and a relic stand of Tsuga canadensis in the lower piedmont of North Carolina Ecology

1956 37 28ndash39 [CrossRef]8 Bailey IW Sinnott EW A botanical index of Cretaceous and Tertiary climates Science 1915 41 831ndash834 [CrossRef]9 Cain SA De Oliveira Castro GM Manual of Vegetation Analysis Haper and Row New York NY USA 195910 Augusto L Dupouey JL Ranger J Effects of tree species on understory vegetation and environmental conditions in temperate

forests Ann For Sci 2003 60 823ndash831 [CrossRef]11 Gracia M Montaneacute F Piqueacute J Retana J Overstory structure and topographic gradients determining diversity and abundance

of understory shrub species in temperate forests in central Pyrenees (NE Spain) For Ecol Manag 2007 242 391ndash397 [CrossRef]12 Gilliam FS The ecological significance of the herbaceous layer in temperate forest ecosystems Bioscience 2007 57 845ndash858

[CrossRef]13 Messier C Parent S Bergeron Y Effects of overstory and understory vegetation on the understory light environment in mixed

boreal forests J Veg Sci 1998 9 511ndash520 [CrossRef]14 Nilsson MC Wardle DA Understory vegetation as a forest ecosystem driver Evidence from the northern Swedish boreal

forest Front Ecol Environ 2005 3 421ndash428 [CrossRef]15 Bartels SF Chen HYH Is understory plant species diversity driven by resource quantity or resource heterogeneity Ecology

2010 91 1931ndash1938 [CrossRef] [PubMed]16 Dauber J Hirsch M Simmering D Waldhardt R Otte A Wolters V Landscape structure as an indicator of biodiversity

Matrix effects on species richness Agric Ecosyst Environ 2003 98 321ndash329 [CrossRef]17 Duguid MC Frey BR Ellum DS Kelty M Ashton MS The influence of ground disturbance and gap position on understory

plant diversity in upland forests of southern New England For Ecol Manag 2013 303 148ndash159 [CrossRef]

Appl Sci 2021 11 11372 11 of 17

Table 5 Cont

Environmental Variables CodeGroup I Group II Group III

F-Value p-ValueMean plusmn SE Mean plusmn SE Mean plusmn SE

Silt () SLT 2444 plusmn 220 26 plusmn 36 2903 plusmn 274 066 052Sand () SND 5918 plusmn 266 5638 plusmn 342 5885 plusmn 308 017 084pH (15) pH 64 plusmn 012 66 plusmn 017 626 plusmn 013 125 030

Organic matter () OM 221 plusmn 078 462 plusmn 076 261 plusmn 054 292 007Lime () L 316 plusmn 052 406 plusmn 061 361 plusmn 038 066 052

Nitrogen (mgKg) N 012 plusmn 004 018 plusmn 003 016 plusmn 003 0503 060Phosphorus (mgKg) P 824 plusmn 063 744 plusmn 112 1294 plusmn 446 061 054Potassium (mgKg) K 14625 plusmn 2707 23342 plusmn 3752 18633 plusmn 2633 155 022

Wilting point (mLgm) WP 0114 plusmn 042 011 plusmn 009 009 plusmn 0004 436 002Field capacity (mLgm) FC 022 plusmn 061 023 plusmn 009 021 plusmn 007 131 028

Bulk density (gcm3) BD 14 plusmn 011 a 146 plusmn 002 a 152 plusmn 001 ab 343 004Saturation Point (0 kPa) SP 044 plusmn 052 a 044 plusmn 0008 a 042 plusmn 006 ab 341 004

Electrical Conductivity (mSm) EC 1241 plusmn 163 a 128 plusmn 003 a 2346 plusmn 280 b 544 001Available water () AW 010 plusmn 038 011 plusmn 0005 011 plusmn 004 046 063

Temperature minimum (C) Tpmi 1430 plusmn 192 1188 plusmn 037 1189 plusmn 017 213 014Temperature maximum (F) Tpma 2898 plusmn 875 2789 plusmn 533 3646 plusmn 575 211 014

Precipitation (mm) Preci 4984 plusmn 121 4916 plusmn 186 5184 plusmn 097 132 028Relative humidity () RH 4984 plusmn 122 4916 plusmn 187 5184 plusmn 098 132 028

Water Holding capacity () WHC 5212 plusmn 182 5482 plusmn 198 5347 plusmn 289 018 083

Note Different superscript letters mean significant variation at p lt 05 tested by post hoc Tukey HSD insignificant variations haveno superscript

Table 6 Results of the RDA showed correlation coefficients between the physiographic and edaphicvariables and the RDA axes and biplot scores of each variable on all the three axes

S No VariablesCorrelation Biplot Scores

Axis 1 Axis 2 Axis 3 Axis 1 Axis 2 Axis 3

1 Lat minus006 minus049 minus002 minus055 minus394 minus01552 Long minus019 018 minus022 minus181 148 minus1743 E 023 minus039 006 218 minus309 05184 ASP 008 minus009 016 074 minus074 1255 CLY 019 minus036 minus019 177 minus292 minus1486 SLT minus020 029 038 minus183 228 2957 SND 009 minus009 minus026 085 minus072 minus2038 pH 022 minus022 minus021 197 minus172 minus1639 OM 009 016 minus0003 088 126 minus002

10 L 021 017 minus039 196 132 minus30511 N 022 009 minus002 182 075 minus01812 P 0007 minus013 020 007 minus106 15613 K 036 minus004 minus012 331 minus031 minus09614 WP 018 minus037 minus018 166 minus296 minus13915 FC 003 minus013 009 027 minus105 07216 BD minus010 030 005 minus093 237 04217 SP 0104 minus031 minus005 095 minus238 minus03718 EC minus0121 043 013 minus111 341 100419 AW minus0176 025 038 minus160 197 29220 TIVI minus063 minus047 002 minus583 minus379 01721 QIVI 0162 minus041 013 148 minus328 09722 BA minus0025 minus011 022 minus023 minus088 15523 Dha 0112 minus022 minus017 102 minus178 minus12824 TpMi minus0246 minus009 minus004 minus224 minus077 minus03425 TpMa minus0185 001 032 minus168 011 24826 Preci 0259 minus009 003 236 minus071 02427 RH 0102 minus005 minus004 0935 minus037 minus03528 WHC minus0273 0005 0079 minus249 004 061

Note (p lt 005) (p lt 001)

Appl Sci 2021 11 11372 12 of 17Appl Sci 2021 11 x FOR PEER REVIEW 12 of 18

Figure 5 RDA ordination of physiographic and edaphic variables concerning stands and the understory vegetation Note

Blue square represent the species point in the ordination biplot St (Stand number)

Table 6 Results of the RDA showed correlation coefficients between the physiographic and edaphic

variables and the RDA axes and biplot scores of each variable on all the three axes

S No Variables Correlation Biplot Scores

Axis 1 Axis 2 Axis 3 Axis 1 Axis 2 Axis 3

1 Lat minus006 minus049 minus002 minus055 minus394 minus0155

2 Long minus019 018 minus022 minus181 148 minus174

3 E 023 minus039 006 218 minus309 0518

4 ASP 008 minus009 016 074 minus074 125

5 CLY 019 minus036 minus019 177 minus292 minus148

6 SLT minus020 029 038 minus183 228 295

7 SND 009 minus009 minus026 085 minus072 minus203

8 pH 022 minus022 minus021 197 minus172 minus163

9 OM 009 016 minus0003 088 126 minus002

10 L 021 017 minus039 196 132 minus305

11 N 022 009 minus002 182 075 minus018

12 P 0007 minus013 020 007 minus106 156

13 K 036 minus004 minus012 331 minus031 minus096

Figure 5 RDA ordination of physiographic and edaphic variables concerning stands and the understory vegetation NoteBlue square represent the species point in the ordination biplot St (Stand number)

4 Discussion

Vegetation is a group of plants growing together in a particular locality [43] and it mayalso be defined as a unit that retains its unique structure and physiognomic characteristicsin an adequately great and sufficient way to permit their distinction from other units [46]The understory plant species in the oak-dominated forests consist of 58 species belongingto 32 families at 30 different locations in the Hindukush ranges of Swat The physiognomyof the studied area was dominated by herbaceous growth form with 47 plant species (81)followed by shrubs with 10 plant species (17) and trees with individual plant species(2) Herbaceous dominancy and less tree percentage might be due to altitudinal andgeographical variations which indicates that the climatic factors favor the herbaceous floraOur findings are associated with researchers in allied neighboring and national regions inwhich the species reported were mostly herbaceous [4748] Among all families Fabaceaewas recorded as the leading family with eight plant species followed by Asteraceae andLamiaceae with seven species each For instance several researchers [532ndash343846] forinstance [31] have documented Asteraceae and Fabaceae as the two most important fami-lies While other researchers [38] cited Lamiaceae and Rosaceae and [48] cited LamiaceaeMoraceae and Asteraceae as dominant plant families from Darra Adam Khel KP Pakistan

Appl Sci 2021 11 11372 13 of 17

Plant life-forms and vegetation are indicators of the climate [6] According to Meher-Homji [49] life-forms are reflective of the bioclimates of an area Raunkiaer [6] designedthree major phytoclimates based on life-form spectra on the earth It includes phanerophyticclimate for the tropics therophytic for the xeric environments and hemicryptophytic forthe cold temperate region The present study identified seven different life-form classes inthe study area The most dominant life-form was hemicryptophytes with 19 species (33)followed by nanophanerophytes with 15 species (26) and therophytes with 13 species(22) Hemicryptophytes usually prevail in open physiognomies while phanerophytesare mainly in closed ones [5051] Biological spectra are important in comparing geographyand habitats and might change due to biotic influences viz grazing human activities andclimatic changes [52ndash54] Hemicryptophytes lose their aboveground parts during mostsummer and winter months while therophytes remain seeded to avoid summer droughtand cold winter stresses

Furthermore the flora of the study area is under anthropogenic pressure in the formof overgrazing and deforestation by nomadic and native people Nasir and Sultan [55]reported a similar finding from District Chakwal where therophytes were the dominantbiological spectra A community that therophytes dominate can be a characteristic fea-ture of a highly disturbed area under anthropogenic pressure [4854] In addition [56]reported therophytes as the dominant plant species of the rangeland district Tank Pak-istan and [57] assessed that therophytes is the leading life-form of Lahor District SwabiPakistan showing that the results of the current study are in compliance with the findingsof several other studies

Results of leaf size spectra trait revealed that species with microphyllous leaves domi-nated the area (with 24 species 41) followed by nanophylls (17 species 29) leptophylls(11 species 19) and mesophyll (5 species 9) Nonetheless 2 with megaphyllousleaf size was also recorded Microphyllous leaf size class is normally the characteristicfeature of meadow plant species while leptophylls and nanophylls are illustrative of hotdeserts [754] Comparable outcomes where microphylls and nanophylls overwhelmedthe vegetation and were reported in the work of researchers [7] and [45] where the authorslinked these two leaf size classes with the physiognomies of mild ranges A high rate ofmicrophylls may be identified with cool atmospheres of the sub-elevated and snowcappedareas Here as well the top layer was less settled containing a slim sheet that is notconclusive about the entrance of roots Microphyllous and nanophyllous leaves specieswere inexhaustible because of the biological variety for this dry condition The presentresults concur with [58] who detailed that microphylls and nanophylls predominance inthe dry mild atmosphere of District Quetta Our inferences additionally uncovered that thehigh extent in leaf size class changes with increasing altitude and the rate of microphyllswas emphatically connected with this as well [5960]

Among the 58 species documented 43 plant species were found in association withgroup III clustered by applying Wardrsquos agglomerative clustering which indicates widesociability of the species in the studied oak-dominated forests Moreover the analysisreveals that B lycium (782) C arvensis (687) and A trichomanes (66) were the mostabundant species in group III Group II was less diverse in terms of understory speciesnumbering in total of 25 plant species In this group Calamintha vulgaris (L) H KarstDryopteris stewartii Fraser-Jenk and Plantago lanceolata L were dominant (115 934 and986 respectively) Plant species in the understory with varying degrees of resistance tothese factors prefer a specific forest type Since certain plant species are limited to a specificforest type the extinction of that forest could result in the extinction of certain understoryplants [2761]

According to a recent analysis the richness and diversity of understory species inoak forests differed greatly depending on canopy dominants Herbaceous species abun-dance and α-diversity were highest in the oaks forest but there was less heterogeneity(β-diversity) across sites and major groups These findings highlight the importance of oakforests in protecting habitat and plant composition in the understory vegetation An herb

Appl Sci 2021 11 11372 14 of 17

layer with higher species abundance and diversity in oak forests may be due to highersolar radiation on south-facing slopes which is better for herbaceous species [62ndash64]

Environmental variables such as geographic parameters and physiochemical soilcharacteristics are important in determining the community structure and composition [65]In particular latitude and altitude were found to vary significantly in the understory groupsClay particles in soil texture and bulk density saturation point and electrical conductivityvaried significantly in the understory vegetation Similarly in the same region [66] thesoil parameters in understory vegetation of Pinus wallichiana AB Jacks dominated foresthave been studied revealing that elevation slope and phosphorus are vital factors indetermining the understory vegetation An oak species Q rubur L was also reported asa major associated species Furthermore many other researchers from other parts of theworld have reported that edaphic factors can significantly affect the species compositionand species diversity in plant communities [1066ndash68]

Forward selection of the RDA ordination revealed that latitude elevation clay wiltingpoint bulk density saturation and electric conductivity were significantly influential indetermining the understory vegetation of oak-dominated forests These results followthe findings of many other previous studies [12596970] Ali and Begum [62] also in-vestigated the vegetation of Swat and determined congruent results by stating a strongrelationship between vegetation and edaphic factors Many other researchers worldwidehave recorded that soil characteristics matter more than canopy organisms in decidingunderstory vegetation [62ndash6470] The study of species composition analysis in the oak-dominated forest revealed a general pattern of variation in the community diversity andspecies composition A similar pattern of species composition was also reported by [65] inP wallachiana understory from the same region The species diversity was found to increasewith time as Beg and Mirza [29] reported only 36 understory species due to the increase inanthropogenic activities

5 Conclusions

The current study reveals that Swat oak forests have rich floristic diversity with domi-nance of the therophytic life-form and microphyllous leaf size class indicating sub-tropicaland moist temperate type climates The species diversity was observed to increase duringthe spring and summer seasons and decreased later in the autumn As the winter seasonapproaches the decline in diversity was observed associated with dry environmentalconditions slow growth rate and other climatic factors Nonetheless critical impactsof seasonal variation on life-forms and overall species diversity were evident Among58 species 43 plant species were associated with group III clustered by applying Wardrsquosagglomerative clustering indicating the wide sociability of the species in the studied oak-dominated forests The understory vegetation of these forests plays an important role inthe forest ecology of the region

Moreover the environmental and soil variables ie latitude elevation clay percent-age wilting point electrical conductivity and potassium (mgKg) affect the understoryvegetation In addition important overstory variables like Quercus IVI and Total IVI ofoverstory were also found to affect the understory vegetation in oak-dominated forestsFurther it is concluded that the area is vulnerable due to the pressure from the localinhabitants in the form of overgrazing and deforestation which may significantly affectthe understory vegetation This information is particularly important for the success ofefforts intended to prevent the loss of genetic diversity of species within these forestsby destroying their natural habitats Moreover it is imperative to conserve the arearsquosbiodiversity and provide alternative means of livelihood for the local communities thatmay allow sustainable utilization and conservation of the invaluable biodiversity of thisarea for future generations

Appl Sci 2021 11 11372 15 of 17

Author Contributions The research work was designed and supervised by NK AR carried outthe field and laboratory work data analysis and manuscript writing RU also contributed tomanuscript writing and data collection KA DAJ and MEHK provided valuable informationand comments on the initial draft and refine the text in addition to language editing and data analysisIUR provided valuable suggestions during the write-up process and data analysis All authorshave read and agreed to the published version of the manuscript

Funding The research was conducted as a PhD project and did not receive support from anyfunding agency

Institutional Review Board Statement Not applicable

Informed Consent Statement Not applicable

Data Availability Statement All the data analyzedgenerated are included and available inthis manuscript

Acknowledgments We express our gratitude towards the Master students enrolled in the Depart-ment of Botany and the people of Malakand Division who helped with the fieldwork for this projectWe thank Achim Braumluning (Institute of Geography Department of Geography and GeosciencesFriedrich-Alexander-University (FAU) Erlangen-Nuremberg Erlangen Germany) for insightfulcomments that substantially improved the early version We also acknowledged the anonymous re-viewers and editors of the Applied Sciences journal for their valuable comment and language editing

Conflicts of Interest We hereby declare that all the authors have participated in this study and thedevelopment of the manuscript All the authors have read the final version and consent for the articleto be published in the Applied Sciences

References1 Musarella CM Mendoza-Fernaacutendez AJ Mota JF Alessandrini JFMA Bacchetta G Brullo GBS Caldarella O

Ciaschetti OCG Conti F Di Martino FCL et al Checklist of gypsophilous vascular flora in Italy Phyto Keys 2018 103 61ndash82[CrossRef] [PubMed]

2 Perrino EV Signorile G Checklist of the vascular flora from the Monopoli coast (Apulia) Ital Bot 2009 41 263ndash2793 Shah M Farrukh HSyed NMSImran AHumaira W Life Form And Floristic Characteristics Along Altitudinal Gradient Of

Humid Temperate Forests Located In Remote Area Of Pakistan Glob J Biodivers Sci Manag 2013 3 276ndash2814 Rafaqat M An Annotated Checklist of Amphibians and Reptiles of Margalla Hills National Park Pakistan Pak J Zool 2011 43

1041ndash10485 Shimwell DW Festuco-Brometea Br-Bl amp R Tx 1943 in the British isles The Phytogeography and Phytosociology of Limestone

Grasslands Part I (A) General Introduction(B) Xerobromion in England Vegetatio 1971 23 1ndash276 Raunkiaer C The Life Forms of Plants and Statistical Plant Geography Being the Collected Papers of C Raunkiaer In The Life

Forms of Plants and Statistical Plant Geography Being the Collected Papers of C Raunkiaer Clarendon Press Oxford UK 19347 Oosting HJ Hess DW Microclimate and a relic stand of Tsuga canadensis in the lower piedmont of North Carolina Ecology

1956 37 28ndash39 [CrossRef]8 Bailey IW Sinnott EW A botanical index of Cretaceous and Tertiary climates Science 1915 41 831ndash834 [CrossRef]9 Cain SA De Oliveira Castro GM Manual of Vegetation Analysis Haper and Row New York NY USA 195910 Augusto L Dupouey JL Ranger J Effects of tree species on understory vegetation and environmental conditions in temperate

forests Ann For Sci 2003 60 823ndash831 [CrossRef]11 Gracia M Montaneacute F Piqueacute J Retana J Overstory structure and topographic gradients determining diversity and abundance

of understory shrub species in temperate forests in central Pyrenees (NE Spain) For Ecol Manag 2007 242 391ndash397 [CrossRef]12 Gilliam FS The ecological significance of the herbaceous layer in temperate forest ecosystems Bioscience 2007 57 845ndash858

[CrossRef]13 Messier C Parent S Bergeron Y Effects of overstory and understory vegetation on the understory light environment in mixed

boreal forests J Veg Sci 1998 9 511ndash520 [CrossRef]14 Nilsson MC Wardle DA Understory vegetation as a forest ecosystem driver Evidence from the northern Swedish boreal

forest Front Ecol Environ 2005 3 421ndash428 [CrossRef]15 Bartels SF Chen HYH Is understory plant species diversity driven by resource quantity or resource heterogeneity Ecology

2010 91 1931ndash1938 [CrossRef] [PubMed]16 Dauber J Hirsch M Simmering D Waldhardt R Otte A Wolters V Landscape structure as an indicator of biodiversity

Matrix effects on species richness Agric Ecosyst Environ 2003 98 321ndash329 [CrossRef]17 Duguid MC Frey BR Ellum DS Kelty M Ashton MS The influence of ground disturbance and gap position on understory

plant diversity in upland forests of southern New England For Ecol Manag 2013 303 148ndash159 [CrossRef]

Appl Sci 2021 11 11372 12 of 17Appl Sci 2021 11 x FOR PEER REVIEW 12 of 18

Figure 5 RDA ordination of physiographic and edaphic variables concerning stands and the understory vegetation Note

Blue square represent the species point in the ordination biplot St (Stand number)

Table 6 Results of the RDA showed correlation coefficients between the physiographic and edaphic

variables and the RDA axes and biplot scores of each variable on all the three axes

S No Variables Correlation Biplot Scores

Axis 1 Axis 2 Axis 3 Axis 1 Axis 2 Axis 3

1 Lat minus006 minus049 minus002 minus055 minus394 minus0155

2 Long minus019 018 minus022 minus181 148 minus174

3 E 023 minus039 006 218 minus309 0518

4 ASP 008 minus009 016 074 minus074 125

5 CLY 019 minus036 minus019 177 minus292 minus148

6 SLT minus020 029 038 minus183 228 295

7 SND 009 minus009 minus026 085 minus072 minus203

8 pH 022 minus022 minus021 197 minus172 minus163

9 OM 009 016 minus0003 088 126 minus002

10 L 021 017 minus039 196 132 minus305

11 N 022 009 minus002 182 075 minus018

12 P 0007 minus013 020 007 minus106 156

13 K 036 minus004 minus012 331 minus031 minus096

Figure 5 RDA ordination of physiographic and edaphic variables concerning stands and the understory vegetation NoteBlue square represent the species point in the ordination biplot St (Stand number)

4 Discussion

Vegetation is a group of plants growing together in a particular locality [43] and it mayalso be defined as a unit that retains its unique structure and physiognomic characteristicsin an adequately great and sufficient way to permit their distinction from other units [46]The understory plant species in the oak-dominated forests consist of 58 species belongingto 32 families at 30 different locations in the Hindukush ranges of Swat The physiognomyof the studied area was dominated by herbaceous growth form with 47 plant species (81)followed by shrubs with 10 plant species (17) and trees with individual plant species(2) Herbaceous dominancy and less tree percentage might be due to altitudinal andgeographical variations which indicates that the climatic factors favor the herbaceous floraOur findings are associated with researchers in allied neighboring and national regions inwhich the species reported were mostly herbaceous [4748] Among all families Fabaceaewas recorded as the leading family with eight plant species followed by Asteraceae andLamiaceae with seven species each For instance several researchers [532ndash343846] forinstance [31] have documented Asteraceae and Fabaceae as the two most important fami-lies While other researchers [38] cited Lamiaceae and Rosaceae and [48] cited LamiaceaeMoraceae and Asteraceae as dominant plant families from Darra Adam Khel KP Pakistan

Appl Sci 2021 11 11372 13 of 17

Plant life-forms and vegetation are indicators of the climate [6] According to Meher-Homji [49] life-forms are reflective of the bioclimates of an area Raunkiaer [6] designedthree major phytoclimates based on life-form spectra on the earth It includes phanerophyticclimate for the tropics therophytic for the xeric environments and hemicryptophytic forthe cold temperate region The present study identified seven different life-form classes inthe study area The most dominant life-form was hemicryptophytes with 19 species (33)followed by nanophanerophytes with 15 species (26) and therophytes with 13 species(22) Hemicryptophytes usually prevail in open physiognomies while phanerophytesare mainly in closed ones [5051] Biological spectra are important in comparing geographyand habitats and might change due to biotic influences viz grazing human activities andclimatic changes [52ndash54] Hemicryptophytes lose their aboveground parts during mostsummer and winter months while therophytes remain seeded to avoid summer droughtand cold winter stresses

Furthermore the flora of the study area is under anthropogenic pressure in the formof overgrazing and deforestation by nomadic and native people Nasir and Sultan [55]reported a similar finding from District Chakwal where therophytes were the dominantbiological spectra A community that therophytes dominate can be a characteristic fea-ture of a highly disturbed area under anthropogenic pressure [4854] In addition [56]reported therophytes as the dominant plant species of the rangeland district Tank Pak-istan and [57] assessed that therophytes is the leading life-form of Lahor District SwabiPakistan showing that the results of the current study are in compliance with the findingsof several other studies

Results of leaf size spectra trait revealed that species with microphyllous leaves domi-nated the area (with 24 species 41) followed by nanophylls (17 species 29) leptophylls(11 species 19) and mesophyll (5 species 9) Nonetheless 2 with megaphyllousleaf size was also recorded Microphyllous leaf size class is normally the characteristicfeature of meadow plant species while leptophylls and nanophylls are illustrative of hotdeserts [754] Comparable outcomes where microphylls and nanophylls overwhelmedthe vegetation and were reported in the work of researchers [7] and [45] where the authorslinked these two leaf size classes with the physiognomies of mild ranges A high rate ofmicrophylls may be identified with cool atmospheres of the sub-elevated and snowcappedareas Here as well the top layer was less settled containing a slim sheet that is notconclusive about the entrance of roots Microphyllous and nanophyllous leaves specieswere inexhaustible because of the biological variety for this dry condition The presentresults concur with [58] who detailed that microphylls and nanophylls predominance inthe dry mild atmosphere of District Quetta Our inferences additionally uncovered that thehigh extent in leaf size class changes with increasing altitude and the rate of microphyllswas emphatically connected with this as well [5960]

Among the 58 species documented 43 plant species were found in association withgroup III clustered by applying Wardrsquos agglomerative clustering which indicates widesociability of the species in the studied oak-dominated forests Moreover the analysisreveals that B lycium (782) C arvensis (687) and A trichomanes (66) were the mostabundant species in group III Group II was less diverse in terms of understory speciesnumbering in total of 25 plant species In this group Calamintha vulgaris (L) H KarstDryopteris stewartii Fraser-Jenk and Plantago lanceolata L were dominant (115 934 and986 respectively) Plant species in the understory with varying degrees of resistance tothese factors prefer a specific forest type Since certain plant species are limited to a specificforest type the extinction of that forest could result in the extinction of certain understoryplants [2761]

According to a recent analysis the richness and diversity of understory species inoak forests differed greatly depending on canopy dominants Herbaceous species abun-dance and α-diversity were highest in the oaks forest but there was less heterogeneity(β-diversity) across sites and major groups These findings highlight the importance of oakforests in protecting habitat and plant composition in the understory vegetation An herb

Appl Sci 2021 11 11372 14 of 17

layer with higher species abundance and diversity in oak forests may be due to highersolar radiation on south-facing slopes which is better for herbaceous species [62ndash64]

Environmental variables such as geographic parameters and physiochemical soilcharacteristics are important in determining the community structure and composition [65]In particular latitude and altitude were found to vary significantly in the understory groupsClay particles in soil texture and bulk density saturation point and electrical conductivityvaried significantly in the understory vegetation Similarly in the same region [66] thesoil parameters in understory vegetation of Pinus wallichiana AB Jacks dominated foresthave been studied revealing that elevation slope and phosphorus are vital factors indetermining the understory vegetation An oak species Q rubur L was also reported asa major associated species Furthermore many other researchers from other parts of theworld have reported that edaphic factors can significantly affect the species compositionand species diversity in plant communities [1066ndash68]

Forward selection of the RDA ordination revealed that latitude elevation clay wiltingpoint bulk density saturation and electric conductivity were significantly influential indetermining the understory vegetation of oak-dominated forests These results followthe findings of many other previous studies [12596970] Ali and Begum [62] also in-vestigated the vegetation of Swat and determined congruent results by stating a strongrelationship between vegetation and edaphic factors Many other researchers worldwidehave recorded that soil characteristics matter more than canopy organisms in decidingunderstory vegetation [62ndash6470] The study of species composition analysis in the oak-dominated forest revealed a general pattern of variation in the community diversity andspecies composition A similar pattern of species composition was also reported by [65] inP wallachiana understory from the same region The species diversity was found to increasewith time as Beg and Mirza [29] reported only 36 understory species due to the increase inanthropogenic activities

5 Conclusions

The current study reveals that Swat oak forests have rich floristic diversity with domi-nance of the therophytic life-form and microphyllous leaf size class indicating sub-tropicaland moist temperate type climates The species diversity was observed to increase duringthe spring and summer seasons and decreased later in the autumn As the winter seasonapproaches the decline in diversity was observed associated with dry environmentalconditions slow growth rate and other climatic factors Nonetheless critical impactsof seasonal variation on life-forms and overall species diversity were evident Among58 species 43 plant species were associated with group III clustered by applying Wardrsquosagglomerative clustering indicating the wide sociability of the species in the studied oak-dominated forests The understory vegetation of these forests plays an important role inthe forest ecology of the region

Moreover the environmental and soil variables ie latitude elevation clay percent-age wilting point electrical conductivity and potassium (mgKg) affect the understoryvegetation In addition important overstory variables like Quercus IVI and Total IVI ofoverstory were also found to affect the understory vegetation in oak-dominated forestsFurther it is concluded that the area is vulnerable due to the pressure from the localinhabitants in the form of overgrazing and deforestation which may significantly affectthe understory vegetation This information is particularly important for the success ofefforts intended to prevent the loss of genetic diversity of species within these forestsby destroying their natural habitats Moreover it is imperative to conserve the arearsquosbiodiversity and provide alternative means of livelihood for the local communities thatmay allow sustainable utilization and conservation of the invaluable biodiversity of thisarea for future generations

Appl Sci 2021 11 11372 15 of 17

Author Contributions The research work was designed and supervised by NK AR carried outthe field and laboratory work data analysis and manuscript writing RU also contributed tomanuscript writing and data collection KA DAJ and MEHK provided valuable informationand comments on the initial draft and refine the text in addition to language editing and data analysisIUR provided valuable suggestions during the write-up process and data analysis All authorshave read and agreed to the published version of the manuscript

Funding The research was conducted as a PhD project and did not receive support from anyfunding agency

Institutional Review Board Statement Not applicable

Informed Consent Statement Not applicable

Data Availability Statement All the data analyzedgenerated are included and available inthis manuscript

Acknowledgments We express our gratitude towards the Master students enrolled in the Depart-ment of Botany and the people of Malakand Division who helped with the fieldwork for this projectWe thank Achim Braumluning (Institute of Geography Department of Geography and GeosciencesFriedrich-Alexander-University (FAU) Erlangen-Nuremberg Erlangen Germany) for insightfulcomments that substantially improved the early version We also acknowledged the anonymous re-viewers and editors of the Applied Sciences journal for their valuable comment and language editing

Conflicts of Interest We hereby declare that all the authors have participated in this study and thedevelopment of the manuscript All the authors have read the final version and consent for the articleto be published in the Applied Sciences

References1 Musarella CM Mendoza-Fernaacutendez AJ Mota JF Alessandrini JFMA Bacchetta G Brullo GBS Caldarella O

Ciaschetti OCG Conti F Di Martino FCL et al Checklist of gypsophilous vascular flora in Italy Phyto Keys 2018 103 61ndash82[CrossRef] [PubMed]

2 Perrino EV Signorile G Checklist of the vascular flora from the Monopoli coast (Apulia) Ital Bot 2009 41 263ndash2793 Shah M Farrukh HSyed NMSImran AHumaira W Life Form And Floristic Characteristics Along Altitudinal Gradient Of

Humid Temperate Forests Located In Remote Area Of Pakistan Glob J Biodivers Sci Manag 2013 3 276ndash2814 Rafaqat M An Annotated Checklist of Amphibians and Reptiles of Margalla Hills National Park Pakistan Pak J Zool 2011 43

1041ndash10485 Shimwell DW Festuco-Brometea Br-Bl amp R Tx 1943 in the British isles The Phytogeography and Phytosociology of Limestone

Grasslands Part I (A) General Introduction(B) Xerobromion in England Vegetatio 1971 23 1ndash276 Raunkiaer C The Life Forms of Plants and Statistical Plant Geography Being the Collected Papers of C Raunkiaer In The Life

Forms of Plants and Statistical Plant Geography Being the Collected Papers of C Raunkiaer Clarendon Press Oxford UK 19347 Oosting HJ Hess DW Microclimate and a relic stand of Tsuga canadensis in the lower piedmont of North Carolina Ecology

1956 37 28ndash39 [CrossRef]8 Bailey IW Sinnott EW A botanical index of Cretaceous and Tertiary climates Science 1915 41 831ndash834 [CrossRef]9 Cain SA De Oliveira Castro GM Manual of Vegetation Analysis Haper and Row New York NY USA 195910 Augusto L Dupouey JL Ranger J Effects of tree species on understory vegetation and environmental conditions in temperate

forests Ann For Sci 2003 60 823ndash831 [CrossRef]11 Gracia M Montaneacute F Piqueacute J Retana J Overstory structure and topographic gradients determining diversity and abundance

of understory shrub species in temperate forests in central Pyrenees (NE Spain) For Ecol Manag 2007 242 391ndash397 [CrossRef]12 Gilliam FS The ecological significance of the herbaceous layer in temperate forest ecosystems Bioscience 2007 57 845ndash858

[CrossRef]13 Messier C Parent S Bergeron Y Effects of overstory and understory vegetation on the understory light environment in mixed

boreal forests J Veg Sci 1998 9 511ndash520 [CrossRef]14 Nilsson MC Wardle DA Understory vegetation as a forest ecosystem driver Evidence from the northern Swedish boreal

forest Front Ecol Environ 2005 3 421ndash428 [CrossRef]15 Bartels SF Chen HYH Is understory plant species diversity driven by resource quantity or resource heterogeneity Ecology

2010 91 1931ndash1938 [CrossRef] [PubMed]16 Dauber J Hirsch M Simmering D Waldhardt R Otte A Wolters V Landscape structure as an indicator of biodiversity

Matrix effects on species richness Agric Ecosyst Environ 2003 98 321ndash329 [CrossRef]17 Duguid MC Frey BR Ellum DS Kelty M Ashton MS The influence of ground disturbance and gap position on understory

plant diversity in upland forests of southern New England For Ecol Manag 2013 303 148ndash159 [CrossRef]

Appl Sci 2021 11 11372 13 of 17

Plant life-forms and vegetation are indicators of the climate [6] According to Meher-Homji [49] life-forms are reflective of the bioclimates of an area Raunkiaer [6] designedthree major phytoclimates based on life-form spectra on the earth It includes phanerophyticclimate for the tropics therophytic for the xeric environments and hemicryptophytic forthe cold temperate region The present study identified seven different life-form classes inthe study area The most dominant life-form was hemicryptophytes with 19 species (33)followed by nanophanerophytes with 15 species (26) and therophytes with 13 species(22) Hemicryptophytes usually prevail in open physiognomies while phanerophytesare mainly in closed ones [5051] Biological spectra are important in comparing geographyand habitats and might change due to biotic influences viz grazing human activities andclimatic changes [52ndash54] Hemicryptophytes lose their aboveground parts during mostsummer and winter months while therophytes remain seeded to avoid summer droughtand cold winter stresses

Furthermore the flora of the study area is under anthropogenic pressure in the formof overgrazing and deforestation by nomadic and native people Nasir and Sultan [55]reported a similar finding from District Chakwal where therophytes were the dominantbiological spectra A community that therophytes dominate can be a characteristic fea-ture of a highly disturbed area under anthropogenic pressure [4854] In addition [56]reported therophytes as the dominant plant species of the rangeland district Tank Pak-istan and [57] assessed that therophytes is the leading life-form of Lahor District SwabiPakistan showing that the results of the current study are in compliance with the findingsof several other studies

Results of leaf size spectra trait revealed that species with microphyllous leaves domi-nated the area (with 24 species 41) followed by nanophylls (17 species 29) leptophylls(11 species 19) and mesophyll (5 species 9) Nonetheless 2 with megaphyllousleaf size was also recorded Microphyllous leaf size class is normally the characteristicfeature of meadow plant species while leptophylls and nanophylls are illustrative of hotdeserts [754] Comparable outcomes where microphylls and nanophylls overwhelmedthe vegetation and were reported in the work of researchers [7] and [45] where the authorslinked these two leaf size classes with the physiognomies of mild ranges A high rate ofmicrophylls may be identified with cool atmospheres of the sub-elevated and snowcappedareas Here as well the top layer was less settled containing a slim sheet that is notconclusive about the entrance of roots Microphyllous and nanophyllous leaves specieswere inexhaustible because of the biological variety for this dry condition The presentresults concur with [58] who detailed that microphylls and nanophylls predominance inthe dry mild atmosphere of District Quetta Our inferences additionally uncovered that thehigh extent in leaf size class changes with increasing altitude and the rate of microphyllswas emphatically connected with this as well [5960]

Among the 58 species documented 43 plant species were found in association withgroup III clustered by applying Wardrsquos agglomerative clustering which indicates widesociability of the species in the studied oak-dominated forests Moreover the analysisreveals that B lycium (782) C arvensis (687) and A trichomanes (66) were the mostabundant species in group III Group II was less diverse in terms of understory speciesnumbering in total of 25 plant species In this group Calamintha vulgaris (L) H KarstDryopteris stewartii Fraser-Jenk and Plantago lanceolata L were dominant (115 934 and986 respectively) Plant species in the understory with varying degrees of resistance tothese factors prefer a specific forest type Since certain plant species are limited to a specificforest type the extinction of that forest could result in the extinction of certain understoryplants [2761]

According to a recent analysis the richness and diversity of understory species inoak forests differed greatly depending on canopy dominants Herbaceous species abun-dance and α-diversity were highest in the oaks forest but there was less heterogeneity(β-diversity) across sites and major groups These findings highlight the importance of oakforests in protecting habitat and plant composition in the understory vegetation An herb

Appl Sci 2021 11 11372 14 of 17

layer with higher species abundance and diversity in oak forests may be due to highersolar radiation on south-facing slopes which is better for herbaceous species [62ndash64]

Environmental variables such as geographic parameters and physiochemical soilcharacteristics are important in determining the community structure and composition [65]In particular latitude and altitude were found to vary significantly in the understory groupsClay particles in soil texture and bulk density saturation point and electrical conductivityvaried significantly in the understory vegetation Similarly in the same region [66] thesoil parameters in understory vegetation of Pinus wallichiana AB Jacks dominated foresthave been studied revealing that elevation slope and phosphorus are vital factors indetermining the understory vegetation An oak species Q rubur L was also reported asa major associated species Furthermore many other researchers from other parts of theworld have reported that edaphic factors can significantly affect the species compositionand species diversity in plant communities [1066ndash68]

Forward selection of the RDA ordination revealed that latitude elevation clay wiltingpoint bulk density saturation and electric conductivity were significantly influential indetermining the understory vegetation of oak-dominated forests These results followthe findings of many other previous studies [12596970] Ali and Begum [62] also in-vestigated the vegetation of Swat and determined congruent results by stating a strongrelationship between vegetation and edaphic factors Many other researchers worldwidehave recorded that soil characteristics matter more than canopy organisms in decidingunderstory vegetation [62ndash6470] The study of species composition analysis in the oak-dominated forest revealed a general pattern of variation in the community diversity andspecies composition A similar pattern of species composition was also reported by [65] inP wallachiana understory from the same region The species diversity was found to increasewith time as Beg and Mirza [29] reported only 36 understory species due to the increase inanthropogenic activities

5 Conclusions

The current study reveals that Swat oak forests have rich floristic diversity with domi-nance of the therophytic life-form and microphyllous leaf size class indicating sub-tropicaland moist temperate type climates The species diversity was observed to increase duringthe spring and summer seasons and decreased later in the autumn As the winter seasonapproaches the decline in diversity was observed associated with dry environmentalconditions slow growth rate and other climatic factors Nonetheless critical impactsof seasonal variation on life-forms and overall species diversity were evident Among58 species 43 plant species were associated with group III clustered by applying Wardrsquosagglomerative clustering indicating the wide sociability of the species in the studied oak-dominated forests The understory vegetation of these forests plays an important role inthe forest ecology of the region

Moreover the environmental and soil variables ie latitude elevation clay percent-age wilting point electrical conductivity and potassium (mgKg) affect the understoryvegetation In addition important overstory variables like Quercus IVI and Total IVI ofoverstory were also found to affect the understory vegetation in oak-dominated forestsFurther it is concluded that the area is vulnerable due to the pressure from the localinhabitants in the form of overgrazing and deforestation which may significantly affectthe understory vegetation This information is particularly important for the success ofefforts intended to prevent the loss of genetic diversity of species within these forestsby destroying their natural habitats Moreover it is imperative to conserve the arearsquosbiodiversity and provide alternative means of livelihood for the local communities thatmay allow sustainable utilization and conservation of the invaluable biodiversity of thisarea for future generations

Appl Sci 2021 11 11372 15 of 17

Author Contributions The research work was designed and supervised by NK AR carried outthe field and laboratory work data analysis and manuscript writing RU also contributed tomanuscript writing and data collection KA DAJ and MEHK provided valuable informationand comments on the initial draft and refine the text in addition to language editing and data analysisIUR provided valuable suggestions during the write-up process and data analysis All authorshave read and agreed to the published version of the manuscript

Funding The research was conducted as a PhD project and did not receive support from anyfunding agency

Institutional Review Board Statement Not applicable

Informed Consent Statement Not applicable

Data Availability Statement All the data analyzedgenerated are included and available inthis manuscript

Acknowledgments We express our gratitude towards the Master students enrolled in the Depart-ment of Botany and the people of Malakand Division who helped with the fieldwork for this projectWe thank Achim Braumluning (Institute of Geography Department of Geography and GeosciencesFriedrich-Alexander-University (FAU) Erlangen-Nuremberg Erlangen Germany) for insightfulcomments that substantially improved the early version We also acknowledged the anonymous re-viewers and editors of the Applied Sciences journal for their valuable comment and language editing

Conflicts of Interest We hereby declare that all the authors have participated in this study and thedevelopment of the manuscript All the authors have read the final version and consent for the articleto be published in the Applied Sciences

References1 Musarella CM Mendoza-Fernaacutendez AJ Mota JF Alessandrini JFMA Bacchetta G Brullo GBS Caldarella O

Ciaschetti OCG Conti F Di Martino FCL et al Checklist of gypsophilous vascular flora in Italy Phyto Keys 2018 103 61ndash82[CrossRef] [PubMed]

2 Perrino EV Signorile G Checklist of the vascular flora from the Monopoli coast (Apulia) Ital Bot 2009 41 263ndash2793 Shah M Farrukh HSyed NMSImran AHumaira W Life Form And Floristic Characteristics Along Altitudinal Gradient Of

Humid Temperate Forests Located In Remote Area Of Pakistan Glob J Biodivers Sci Manag 2013 3 276ndash2814 Rafaqat M An Annotated Checklist of Amphibians and Reptiles of Margalla Hills National Park Pakistan Pak J Zool 2011 43

1041ndash10485 Shimwell DW Festuco-Brometea Br-Bl amp R Tx 1943 in the British isles The Phytogeography and Phytosociology of Limestone

Grasslands Part I (A) General Introduction(B) Xerobromion in England Vegetatio 1971 23 1ndash276 Raunkiaer C The Life Forms of Plants and Statistical Plant Geography Being the Collected Papers of C Raunkiaer In The Life

Forms of Plants and Statistical Plant Geography Being the Collected Papers of C Raunkiaer Clarendon Press Oxford UK 19347 Oosting HJ Hess DW Microclimate and a relic stand of Tsuga canadensis in the lower piedmont of North Carolina Ecology

1956 37 28ndash39 [CrossRef]8 Bailey IW Sinnott EW A botanical index of Cretaceous and Tertiary climates Science 1915 41 831ndash834 [CrossRef]9 Cain SA De Oliveira Castro GM Manual of Vegetation Analysis Haper and Row New York NY USA 195910 Augusto L Dupouey JL Ranger J Effects of tree species on understory vegetation and environmental conditions in temperate

forests Ann For Sci 2003 60 823ndash831 [CrossRef]11 Gracia M Montaneacute F Piqueacute J Retana J Overstory structure and topographic gradients determining diversity and abundance

of understory shrub species in temperate forests in central Pyrenees (NE Spain) For Ecol Manag 2007 242 391ndash397 [CrossRef]12 Gilliam FS The ecological significance of the herbaceous layer in temperate forest ecosystems Bioscience 2007 57 845ndash858

[CrossRef]13 Messier C Parent S Bergeron Y Effects of overstory and understory vegetation on the understory light environment in mixed

boreal forests J Veg Sci 1998 9 511ndash520 [CrossRef]14 Nilsson MC Wardle DA Understory vegetation as a forest ecosystem driver Evidence from the northern Swedish boreal

forest Front Ecol Environ 2005 3 421ndash428 [CrossRef]15 Bartels SF Chen HYH Is understory plant species diversity driven by resource quantity or resource heterogeneity Ecology

2010 91 1931ndash1938 [CrossRef] [PubMed]16 Dauber J Hirsch M Simmering D Waldhardt R Otte A Wolters V Landscape structure as an indicator of biodiversity

Matrix effects on species richness Agric Ecosyst Environ 2003 98 321ndash329 [CrossRef]17 Duguid MC Frey BR Ellum DS Kelty M Ashton MS The influence of ground disturbance and gap position on understory

plant diversity in upland forests of southern New England For Ecol Manag 2013 303 148ndash159 [CrossRef]

Appl Sci 2021 11 11372 14 of 17

layer with higher species abundance and diversity in oak forests may be due to highersolar radiation on south-facing slopes which is better for herbaceous species [62ndash64]

Environmental variables such as geographic parameters and physiochemical soilcharacteristics are important in determining the community structure and composition [65]In particular latitude and altitude were found to vary significantly in the understory groupsClay particles in soil texture and bulk density saturation point and electrical conductivityvaried significantly in the understory vegetation Similarly in the same region [66] thesoil parameters in understory vegetation of Pinus wallichiana AB Jacks dominated foresthave been studied revealing that elevation slope and phosphorus are vital factors indetermining the understory vegetation An oak species Q rubur L was also reported asa major associated species Furthermore many other researchers from other parts of theworld have reported that edaphic factors can significantly affect the species compositionand species diversity in plant communities [1066ndash68]

Forward selection of the RDA ordination revealed that latitude elevation clay wiltingpoint bulk density saturation and electric conductivity were significantly influential indetermining the understory vegetation of oak-dominated forests These results followthe findings of many other previous studies [12596970] Ali and Begum [62] also in-vestigated the vegetation of Swat and determined congruent results by stating a strongrelationship between vegetation and edaphic factors Many other researchers worldwidehave recorded that soil characteristics matter more than canopy organisms in decidingunderstory vegetation [62ndash6470] The study of species composition analysis in the oak-dominated forest revealed a general pattern of variation in the community diversity andspecies composition A similar pattern of species composition was also reported by [65] inP wallachiana understory from the same region The species diversity was found to increasewith time as Beg and Mirza [29] reported only 36 understory species due to the increase inanthropogenic activities

5 Conclusions

The current study reveals that Swat oak forests have rich floristic diversity with domi-nance of the therophytic life-form and microphyllous leaf size class indicating sub-tropicaland moist temperate type climates The species diversity was observed to increase duringthe spring and summer seasons and decreased later in the autumn As the winter seasonapproaches the decline in diversity was observed associated with dry environmentalconditions slow growth rate and other climatic factors Nonetheless critical impactsof seasonal variation on life-forms and overall species diversity were evident Among58 species 43 plant species were associated with group III clustered by applying Wardrsquosagglomerative clustering indicating the wide sociability of the species in the studied oak-dominated forests The understory vegetation of these forests plays an important role inthe forest ecology of the region

Moreover the environmental and soil variables ie latitude elevation clay percent-age wilting point electrical conductivity and potassium (mgKg) affect the understoryvegetation In addition important overstory variables like Quercus IVI and Total IVI ofoverstory were also found to affect the understory vegetation in oak-dominated forestsFurther it is concluded that the area is vulnerable due to the pressure from the localinhabitants in the form of overgrazing and deforestation which may significantly affectthe understory vegetation This information is particularly important for the success ofefforts intended to prevent the loss of genetic diversity of species within these forestsby destroying their natural habitats Moreover it is imperative to conserve the arearsquosbiodiversity and provide alternative means of livelihood for the local communities thatmay allow sustainable utilization and conservation of the invaluable biodiversity of thisarea for future generations

Appl Sci 2021 11 11372 15 of 17

Author Contributions The research work was designed and supervised by NK AR carried outthe field and laboratory work data analysis and manuscript writing RU also contributed tomanuscript writing and data collection KA DAJ and MEHK provided valuable informationand comments on the initial draft and refine the text in addition to language editing and data analysisIUR provided valuable suggestions during the write-up process and data analysis All authorshave read and agreed to the published version of the manuscript

Funding The research was conducted as a PhD project and did not receive support from anyfunding agency

Institutional Review Board Statement Not applicable

Informed Consent Statement Not applicable

Data Availability Statement All the data analyzedgenerated are included and available inthis manuscript

Acknowledgments We express our gratitude towards the Master students enrolled in the Depart-ment of Botany and the people of Malakand Division who helped with the fieldwork for this projectWe thank Achim Braumluning (Institute of Geography Department of Geography and GeosciencesFriedrich-Alexander-University (FAU) Erlangen-Nuremberg Erlangen Germany) for insightfulcomments that substantially improved the early version We also acknowledged the anonymous re-viewers and editors of the Applied Sciences journal for their valuable comment and language editing

Conflicts of Interest We hereby declare that all the authors have participated in this study and thedevelopment of the manuscript All the authors have read the final version and consent for the articleto be published in the Applied Sciences

References1 Musarella CM Mendoza-Fernaacutendez AJ Mota JF Alessandrini JFMA Bacchetta G Brullo GBS Caldarella O

Ciaschetti OCG Conti F Di Martino FCL et al Checklist of gypsophilous vascular flora in Italy Phyto Keys 2018 103 61ndash82[CrossRef] [PubMed]

2 Perrino EV Signorile G Checklist of the vascular flora from the Monopoli coast (Apulia) Ital Bot 2009 41 263ndash2793 Shah M Farrukh HSyed NMSImran AHumaira W Life Form And Floristic Characteristics Along Altitudinal Gradient Of

Humid Temperate Forests Located In Remote Area Of Pakistan Glob J Biodivers Sci Manag 2013 3 276ndash2814 Rafaqat M An Annotated Checklist of Amphibians and Reptiles of Margalla Hills National Park Pakistan Pak J Zool 2011 43

1041ndash10485 Shimwell DW Festuco-Brometea Br-Bl amp R Tx 1943 in the British isles The Phytogeography and Phytosociology of Limestone

Grasslands Part I (A) General Introduction(B) Xerobromion in England Vegetatio 1971 23 1ndash276 Raunkiaer C The Life Forms of Plants and Statistical Plant Geography Being the Collected Papers of C Raunkiaer In The Life

Forms of Plants and Statistical Plant Geography Being the Collected Papers of C Raunkiaer Clarendon Press Oxford UK 19347 Oosting HJ Hess DW Microclimate and a relic stand of Tsuga canadensis in the lower piedmont of North Carolina Ecology

1956 37 28ndash39 [CrossRef]8 Bailey IW Sinnott EW A botanical index of Cretaceous and Tertiary climates Science 1915 41 831ndash834 [CrossRef]9 Cain SA De Oliveira Castro GM Manual of Vegetation Analysis Haper and Row New York NY USA 195910 Augusto L Dupouey JL Ranger J Effects of tree species on understory vegetation and environmental conditions in temperate

forests Ann For Sci 2003 60 823ndash831 [CrossRef]11 Gracia M Montaneacute F Piqueacute J Retana J Overstory structure and topographic gradients determining diversity and abundance

of understory shrub species in temperate forests in central Pyrenees (NE Spain) For Ecol Manag 2007 242 391ndash397 [CrossRef]12 Gilliam FS The ecological significance of the herbaceous layer in temperate forest ecosystems Bioscience 2007 57 845ndash858

[CrossRef]13 Messier C Parent S Bergeron Y Effects of overstory and understory vegetation on the understory light environment in mixed

boreal forests J Veg Sci 1998 9 511ndash520 [CrossRef]14 Nilsson MC Wardle DA Understory vegetation as a forest ecosystem driver Evidence from the northern Swedish boreal

forest Front Ecol Environ 2005 3 421ndash428 [CrossRef]15 Bartels SF Chen HYH Is understory plant species diversity driven by resource quantity or resource heterogeneity Ecology

2010 91 1931ndash1938 [CrossRef] [PubMed]16 Dauber J Hirsch M Simmering D Waldhardt R Otte A Wolters V Landscape structure as an indicator of biodiversity

Matrix effects on species richness Agric Ecosyst Environ 2003 98 321ndash329 [CrossRef]17 Duguid MC Frey BR Ellum DS Kelty M Ashton MS The influence of ground disturbance and gap position on understory

plant diversity in upland forests of southern New England For Ecol Manag 2013 303 148ndash159 [CrossRef]

Appl Sci 2021 11 11372 15 of 17

Author Contributions The research work was designed and supervised by NK AR carried outthe field and laboratory work data analysis and manuscript writing RU also contributed tomanuscript writing and data collection KA DAJ and MEHK provided valuable informationand comments on the initial draft and refine the text in addition to language editing and data analysisIUR provided valuable suggestions during the write-up process and data analysis All authorshave read and agreed to the published version of the manuscript

Funding The research was conducted as a PhD project and did not receive support from anyfunding agency

Institutional Review Board Statement Not applicable

Informed Consent Statement Not applicable

Data Availability Statement All the data analyzedgenerated are included and available inthis manuscript

Acknowledgments We express our gratitude towards the Master students enrolled in the Depart-ment of Botany and the people of Malakand Division who helped with the fieldwork for this projectWe thank Achim Braumluning (Institute of Geography Department of Geography and GeosciencesFriedrich-Alexander-University (FAU) Erlangen-Nuremberg Erlangen Germany) for insightfulcomments that substantially improved the early version We also acknowledged the anonymous re-viewers and editors of the Applied Sciences journal for their valuable comment and language editing

Conflicts of Interest We hereby declare that all the authors have participated in this study and thedevelopment of the manuscript All the authors have read the final version and consent for the articleto be published in the Applied Sciences

References1 Musarella CM Mendoza-Fernaacutendez AJ Mota JF Alessandrini JFMA Bacchetta G Brullo GBS Caldarella O

Ciaschetti OCG Conti F Di Martino FCL et al Checklist of gypsophilous vascular flora in Italy Phyto Keys 2018 103 61ndash82[CrossRef] [PubMed]

2 Perrino EV Signorile G Checklist of the vascular flora from the Monopoli coast (Apulia) Ital Bot 2009 41 263ndash2793 Shah M Farrukh HSyed NMSImran AHumaira W Life Form And Floristic Characteristics Along Altitudinal Gradient Of

Humid Temperate Forests Located In Remote Area Of Pakistan Glob J Biodivers Sci Manag 2013 3 276ndash2814 Rafaqat M An Annotated Checklist of Amphibians and Reptiles of Margalla Hills National Park Pakistan Pak J Zool 2011 43

1041ndash10485 Shimwell DW Festuco-Brometea Br-Bl amp R Tx 1943 in the British isles The Phytogeography and Phytosociology of Limestone

Grasslands Part I (A) General Introduction(B) Xerobromion in England Vegetatio 1971 23 1ndash276 Raunkiaer C The Life Forms of Plants and Statistical Plant Geography Being the Collected Papers of C Raunkiaer In The Life

Forms of Plants and Statistical Plant Geography Being the Collected Papers of C Raunkiaer Clarendon Press Oxford UK 19347 Oosting HJ Hess DW Microclimate and a relic stand of Tsuga canadensis in the lower piedmont of North Carolina Ecology

1956 37 28ndash39 [CrossRef]8 Bailey IW Sinnott EW A botanical index of Cretaceous and Tertiary climates Science 1915 41 831ndash834 [CrossRef]9 Cain SA De Oliveira Castro GM Manual of Vegetation Analysis Haper and Row New York NY USA 195910 Augusto L Dupouey JL Ranger J Effects of tree species on understory vegetation and environmental conditions in temperate

forests Ann For Sci 2003 60 823ndash831 [CrossRef]11 Gracia M Montaneacute F Piqueacute J Retana J Overstory structure and topographic gradients determining diversity and abundance

of understory shrub species in temperate forests in central Pyrenees (NE Spain) For Ecol Manag 2007 242 391ndash397 [CrossRef]12 Gilliam FS The ecological significance of the herbaceous layer in temperate forest ecosystems Bioscience 2007 57 845ndash858

[CrossRef]13 Messier C Parent S Bergeron Y Effects of overstory and understory vegetation on the understory light environment in mixed

boreal forests J Veg Sci 1998 9 511ndash520 [CrossRef]14 Nilsson MC Wardle DA Understory vegetation as a forest ecosystem driver Evidence from the northern Swedish boreal

forest Front Ecol Environ 2005 3 421ndash428 [CrossRef]15 Bartels SF Chen HYH Is understory plant species diversity driven by resource quantity or resource heterogeneity Ecology

2010 91 1931ndash1938 [CrossRef] [PubMed]16 Dauber J Hirsch M Simmering D Waldhardt R Otte A Wolters V Landscape structure as an indicator of biodiversity

Matrix effects on species richness Agric Ecosyst Environ 2003 98 321ndash329 [CrossRef]17 Duguid MC Frey BR Ellum DS Kelty M Ashton MS The influence of ground disturbance and gap position on understory

plant diversity in upland forests of southern New England For Ecol Manag 2013 303 148ndash159 [CrossRef]

Appl Sci 2021 11 11372 16 of 17

18 Koncz G Papp M Toumlroumlk P Kotroczoacute Z Krakomperger Z Matus G Toacutethmeacutereacutesz B The role of seed bank in the dynamicsof understorey in an oak forest in Hungary Acta Biol Hung 2010 61 109ndash119 [CrossRef] [PubMed]

19 Barbier S Gosselin F Balandier P Influence of tree species on understory vegetation diversity and mechanisms involvedmdashAcritical review for temperate and boreal forests For Ecol Manag 2008 254 1ndash15 [CrossRef]

20 Yu M Sun OJ Effects of forest patch type and site on herb-layer vegetation in a temperate forest ecosystem For Ecol Manag2013 300 14ndash20 [CrossRef]

21 Roberts MR Zhu L Early response of the herbaceous layer to harvesting in a mixed coniferousndashdeciduous forest in NewBrunswick Canada For Ecol Manag 2002 155 17ndash31 [CrossRef]

22 Hart SA Chen HYH Fire logging and overstory affect understory abundance diversity and composition in boreal forestEcol Monogr 2008 78 123ndash140 [CrossRef]

23 Ellsworth JW Harrington RA Fownes JH Seedling emergence growth and allocation of Oriental bittersweet Effects ofseed input seed bank and forest floor litter For Ecol Manag 2004 190 255ndash264 [CrossRef]

24 Chaacutevez V Macdonald SE The influence of canopy patch mosaics on understory plant community composition in borealmixedwood forest For Ecol Manag 2010 259 1067ndash1075 [CrossRef]

25 Koorem K Moora M Positive association between understory species richness and a dominant shrub species (Corylus avellana)in a boreonemoral spruce forest For Ecol Manag 2010 260 1407ndash1413 [CrossRef]

26 Warren RJ Mechanisms driving understory evergreen herb distributions across slope aspects As derived from landscapeposition Plant Ecol 2008 198 297ndash308 [CrossRef]

27 Ali SI Qaiser M A phytogeographical analysis of the phanerogams of Pakistan and Kashmir Proceedings of the Royal Societyof Edinburgh Sect B Biol Sci 1986 89 89ndash101 [CrossRef]

28 Ilahi I Suleman M Species composition and relative abundance of mosquitoes in Swat Pakistan Int J Innov Appl Stud 20132 454ndash463

29 Beg AR Mirza HK Some more plant communities and the future of dry oak forest zone in Swat valley Pak J For 1984 3425ndash35

30 Rahman IU Ijaz F Iqbal Z Afzal A Ali N Afzal M Khan MA Muhammad S Qadir G Asif M A novel survey of theethno medicinal knowledge of dental problems in Manoor Valley (Northern Himalaya) Pakistan J Ethnopharmacol 2016 194877ndash894 [CrossRef]

31 Qian H Klinka K Oslashkland RH Krestov P Kayahara GJ Understorey vegetation in boreal Picea mariana and Populustremuloides stands in British Columbia J Veg Sci 2003 14 173ndash184 [CrossRef]

32 Wulf M Naaf T Herb layer response to broadleaf tree species with different leaf litter quality and canopy structure in temperateforests J Veg Sci 2009 20 517ndash526 [CrossRef]

33 Nasir E Ali SI Flora of West Pakistan Department of Botany University of Karachi Karachi Pakistan 2007 Volume1971 pp 112ndash115

34 Ali SI Significance of flora with special reference to Pakistan Pak J Bot 2008 40 967ndash97135 Nelson DW Sommers LE Total Carbon Organic Carbon and Organic Matter In Methods of Soil Analysis Part 3 Chemical

Method Sparks DL Page AL Helmke PA Loeppert RH Soltanpour PN Tabatabai MA Johnston CT Summer MEEds Soil Science Society of America and American Society of Agronomy Madison WI USA 1996 pp 961ndash1010 [CrossRef]

36 Yeomans JC Bremner JM Carbon and nitrogen analysis of soils by automated combustion techniques Commun Soil Sci PlantAnal 1991 22 843ndash850 [CrossRef]

37 Zhang Z Hu G Ni J Effects of topographical and edaphic factors on the distribution of plant communities in two subtropicalkarst forests southwestern China J Mt Sci 2013 10 95ndash104 [CrossRef]

38 Agriculture Chemistry Council Soil Science Society of China General Analysis Methods of Soil Agriculture Chemistry Science PressBeijing China 1983 (In Chinese)

39 Day PR Particle Fractionation and Particle-Size Analysis No methods of soil analysis American Society of Agronomy MadisonSoil Science Society of America Madison WI USA 1965 pp 545ndash567

40 Orloacuteci L An agglomerative method for classification of plant communities J Ecol 1967 55 193ndash206 [CrossRef]41 Jongman E Jongman SRR Data Analysis in Community and Landscape Ecology Cambridge University Press Cambridge

UK 199542 Braak CJFT The analysis of vegetation-environment relationships by canonical correspondence analysis Vegetation 1987 69

69ndash77 [CrossRef]43 Skinner WR Jefferies RL Carleton TJ Abraham RRDK Prediction of reproductive success and failure in lesser snow geese

based on early season climatic variables Glob Chang Biol 1998 4 3ndash16 [CrossRef]44 Lepš J Šmilauer P Multivariate Analysis of Ecological Data Using CANOCO Cambridge University Press Cambridge UK 200345 Shehata HFS Ecology and nutritive status of Sisymbrium irio L in the Nile delta Egypt J Exp Biol 2014 10 127ndash14246 Khattak NS Nouroz F Rahman IU Noreen S Ethno veterinary uses of medicinal plants of district Karak Pak J

Ethnopharmacol 2015 171 273ndash279 [CrossRef]47 Shah GM Khan MA Common medicinal folk recipes of siran valley Mansehra Pakistan Ethnobot Leafl 2006 10 49ndash6248 Ullah R Iqbal ZHZ Hussain J Khan FU Khan N Muhammad Z Ayaz S Ahmad S Rehman NU Hussain I

Traditional uses of medicinal plants in Darra Adam Khel NWFP Pakistan J Med Plants Res 2010 4 1815ndash1821

Appl Sci 2021 11 11372 17 of 17

49 Meher-Homji VM Life-Forms and Biological Spectra as Epharmonic Criteria of Aridity and Humidity in the Tropics The BangalorePress Mysore India 1964

50 Amjad MS Qaeem MF Ahmad I Khan SU Chaudhari SK Zahid Malik N Shaheen H Khan AM Descriptive studyof plant resources in the context of the ethnomedicinal relevance of indigenous flora A case study from Toli Peer National ParkAzad Jammu and Kashmir Pakistan PLoS ONE 2017 12 e0171896 [CrossRef]

51 Haq F Ahmad H Iqbal Z Vegetation description and phytoclimatic gradients of subtropical forests of Nandiar Khuwarcatchment District Battagram Pak J Bot 2015 47 1399ndash1405

52 Khan M Hussain F Musharaf S Floristic composition and biological characteristics of the vegetation of Sheikh Maltoon TownDistrict Mardan Pakistan Annu Res Rev Biol 2013 3 31ndash41

53 Shimwell DW The Description and Classification of Vegetation Sedgwick and Jackson Sidgwick amp Jackson London UK 1971 p 32254 Nasir ZA Sultan S Floristic biological and leaf size spectra of weeds in gram lentil mustard and wheat fields of district

Chakwal Pakistan Pak J Biol Sci 2002 5 758ndash76255 Barik KL Misra BN Biological spectrum of grassland ecosystem of South Orissa Ecoprint 1998 5 73ndash7756 Badshah L Hussain F Sher Z Floristic inventory ecological characteristics and biological spectrum of rangeland District Tank

Pakistan Pak J Bot 2013 45 1159ndash116857 Sher Z Hussain F Badshah L Biodiversity and ecological characterization of the flora of Gadoon rangeland district Swabi

Khyber Pukhtunkhwa Pakistan Iran J Bot 2014 20 96ndash10858 Tareen RB Qadir SA Phytosociology of the hills of Quetta district Pak J Bot 1991 23 90ndash11459 Batalha MA Martins FR Floristic frequency and vegetation life-form spectra of a cerrado site Braz J Biol 2004 64 201ndash209

[CrossRef]60 Tareen RB Qadir S Harnai Sinjawi to Duki regions of Pakistan Pak Bot Soc 1993 25 83ndash9261 Thomsen RP Svenning J Balslev H Overstorey control of understorey species composition in a near-natural temperate

broadleaved forest in Denmark Plant Ecol 2005 181 113ndash126 [CrossRef]62 Ali K Begum HA A comparative assessment of climate change effect on some of the important tree species of Hindu-Kush

Himalayas using predictive modelling techniques Int J Adv Res 2015 3 1230ndash124063 Qian H Klinka K Sivak B Diversity of the understory vascular vegetation in 40 year-old and old-growth forest stands on

Vancouver Island British Columbia J Veg Sci 1997 8 773ndash780 [CrossRef]64 Triantafyllidis V Zotos A Kosma C Kokkotos E Effect of land-use types on edaphic properties and plant species diversity in

Mediterranean agroecosystem Saudi J Biol Sci 2020 27 3676ndash3690 [CrossRef]65 Rahman IU Khan N Ali K Classification and ordination of understory vegetation using multivariate techniques in the Pinus

wallichiana forests of Swat Valley northern Pakistan Sci Nat 2017 104 24 [CrossRef] [PubMed]66 Nazaryuk VM Klenova MI Kalimullina FR Ecoagrochemical approaches to the problem of nitrate pollution in agroecosys-

tems Russ J Ecol 2002 33 392ndash397 [CrossRef]67 Colombo C Palumbo G Sellitto VM Di Iorio E Castrignanograve A Stelluti M The effects of land use and landscape on soil

nitrate availability in Southern Italy (Molise region) Geoderma 2015 239 1ndash12 [CrossRef]68 Saxena RS Gupta B Saxena KK Singh RC Prasad DN Study of anti-inflammatory activity in the leaves of Nyctanthes

arbor tristis Linn An Indian Medicinal Plant J Ethnopharmacol 1987 11 319ndash330 [CrossRef]69 Macdonald SE Fenniak TE Understory plant communities of boreal mixedwood forests in western Canada Natural patterns

and response to variable-retention harvesting For Ecol Manag 2007 242 34ndash48 [CrossRef]70 Small CJ McCarthy BC Spatial and temporal variability of herbaceous vegetation in an eastern deciduous forest Plant Ecol

2003 164 37ndash48 [CrossRef]