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Community Structure of Ectomycorrhizae Associated with Salix spp. Growing in Two Different Climatic Regions of Pakistan.

Byline: Sana Jabeen and Abdul Nasir Khalid

Abstract

Ectomycorrhiza is a mutualistic symbiotic relationship between the roots of higher plants and fungi. Salix is an important host genus for ectomycorrhizal symbiosis growing in a variety of environmental conditions. Eleven different types of ectomycorrhizal morphotypes were isolated from different species of Salix growing in two geologically distant zones of Pakistan with varied environmental conditions. KPK zone has moist temperate while Lahore zone falls in semi-arid climate. These morphotypes were characterized on morpho-anatomic basis. Out of these eight belonged to KPK zone and three to Lahore zone. Three morphotypes were previously undescribed and six have been found for the first time associated with Salix spp. Two are new records for Pakistan. Species richness and diversity was found higher in KPK zone as compared to Lahore zone where species richness and diversity was lower but a high number of ectomycorrhizal morphotypes were found in comparison with KPK zone. Copyright 2014 Friends Science Publishers

Keywords: Ectomycorrhizas; Salicaceae; Morphotypes; Ecological zones; Community

Introduction

Belonging to the family Salicaceae the genus Salix L. comprises about 450 species worldwide distributed mostly in the Northern Hemisphere (Argus 1997). These species are characterized by particular physiological adaptations and ecological flexibility which are predisposed to use in conservation and environmental projects in many climatic zones and adverse environmental conditions. The economic importance of Salix is currently increasing and emerging in a wide array of practical applications to restore damaged ecosystems. These tree species are widely used in wetlands and riparian situations (Yulia and Martin 2004).Among the 3 genera Salicaceae is represented by 2 in Pakistan with 32 species (Ali 2001). Being cosmopolitan in distribution it is found naturally in different climatic regions of Pakistan sometimes cultivated on arable sites. From Lahore it is represented by two species viz. Salix babylonica and S. tetrasperma. Many species are presentabundantly in Himalayan region of Pakistan besides of S.babylonica and S. tetrasperma these include S. alba S. herbacea S. iliensis S. denticulate S. persica and S. wilhelmsiana (Qureshi et al. 2007).Trappe (1962) reported that many species of the Salicaceae form ectomycorrhizae (ECM). Katenin (1964) examined members of the genus Salix in the tundra of the U.S.S.R. and found ectomycorrhizae associated with all species. Stutz (1972) reported S. arctica Pallas to be mycorrhizal and Miller et al. (1974) reported all four species of Salix present at Barrow Alaska to be

ectomycorrhizal. From Pakistan S. alba is reported as ectomycorrhizal host for Suilus cibiricus (Sarwar et al.2011).Most of the studies in Pakistan depend on the counts of fungal sporocarps rather than assessing the ectomycorrhizal symbionts actually colonizing roots of trees (Jabeen et al. 2012). On the other hand morphotyping uses macroscopic and microscopic characteristics to define individual fungal morphotype allowing for a thorough description of each morphotype so that they can be distinguished from others (Dahlberg 2001). Up till now 52ECM morphotypes published in identified and unidentified form have been reported from Pakistan (Khalid and Niazi2003; Kazmi et al. 2004; Niazi et al. 2006 2007 20092010; Sarwar et al. 2011; Hanif et al. 2012; Jabeen et al.2012; Sarwar et al. 2012; Ashraf et al. 2012). The objective of this work is to find out diversity of ECM associated with Salix spp. growing in two different climatic regions of Pakistan which differ on the basis of soil properties temperature and rain fall patterns as well as to give a comprehensive information about the below ground community structure of ECM fungi. Community diversity is mainly based upon species richness the number of species in the community and community evenness a measure of the abundance of each species in the community. In most ECM communities with a few common species and a large number of rare species greatly influence the assessment of species richness. From species accumulation curve it becomes possible to overcome this problem. The present work focuses on the comparison of richness diversity and

abundance of ECM morphotypes of two zones and judge the factors influencing the differences between the parameters of community structure.

Materials and Methods

Sampling Site Description

Lahore capital of Punjab province (Lahore zone) at 217 meters above sea level (m.a.s.l.) features a hot semi-arid climate with rainy long and extremely hot summers dry cold winters a monsoon and dust storms. The weather of Lahore is extreme at 40-48C during the months of May and June. From late June the monsoon seasons starts with heavy rainfall till August with an average 470 mm with and30% humidity. On the other hand moist temperate regions (Khyber Pakhtunkhwa/KPK zone) extended from Muree hills Ayubia Nathiagali to Miandam from1890 to 2500 m. a.s.l. between subtropical pine forests and sub alpine forest. The weather is extreme cold in December and January at3C while it reaches up to 26C during summers. Average rain fall of the area is 700 mm with 57% humidity (Ahmed et al. 2006) (Table 1).

Sampling of Morphotypes

Sampling sites were visited a number of times from October2009 to September 2010. Mature trees with a trunk diameter of 5060 cm were selected. From each zone ten trees were selected and soil blocks of 15 cm3 were excavated using shovel/spade at 15 cm to 1 m from the trunk of each tree. Two replicate samples per tree were collected and brought to the laboratory in polythene bags and catalogued.

Isolation of Roots Morphotyping and Storage of ECM

The soil blocks were soaked in tap water for overnight to loosen the adhering soil particles then shifted to 2 mm sieve and placed under shower to remove the soil. The ectomycorrhizae were carefully sorted into morphotypes according to their morphological features. Criteria for sorting included ramification colour size associated hyphae rhizomorphs cystidia etc. The attached soil particles were removed with the help of fine squirrel hair brush under Meiji Techno stereoscope. Individual root tips were dissected and stored according to their characteristics. Only mycorrhizal root tips with the same morphology from one sample were joined resulting in a given morphotypes sample. Washed roots were kept in McCartney bottles after two to three washings in two drops of Max liquid for comparative morpho-anatomic studies.

Photography of ECM

Morphotypes were placed in clean petriplate containing water with contrasting background below the petriplate in order to clearly visualize and distinguish the color of ECM

morphotypes and focused under Meji Techno Stereoscope equipped with Canon Power Shot G10 14.7 megapixel camera.

Microscopic Characterization of Morphotypes

Separations made under dissecting microscope were confirmed by examining in more detail under compound microscope. Morphotypes were anatomically characterized following Agerer's methodology. Morphological characteristics were examined under stereomicroscope. Clear view of mantle was obtained by peeling off mantle from a tip and mounting its outer and inner surface on slides in lactic acid as mounting medium and observed in detail hyphae or hyphal cells. The internal structures of rhizomorphs emanating hyphae and cystidia were also observed and measured using micro meter and drawn with the help of Camera Lucida. Characteristics of mantle emanating hyphae rhizomorphs and cystidia type were used to characterize definitely recognizable mycorrhizal types and to relate these to different species of fungal symbionts for taxonomic purpose.

Species Richness Curve

Species richness is the number of different species represented in an ecological region. Species richness of the two ecological zones was estimated by species richness curve drawn using Estimate S software.

Simpson's Diversity Index

To quantify the ectomycorrhizal diversity Simpson's Diversity Index was implied. The term 'Simpson's Diversity Index' refers to any one of 3 closely related indices. In this study Simpson's Index (D) was used. Where: D= Sn (n-1) / N (N-1) and n= total number of individuals of a particular species and N=total number of individuals of all species.The value of D ranges between 0 and 1. Index 0 represents infinite diversity and 1 no diversity. That is the bigger the value of D the lower the diversity.

Results

ECM of Salix spp. from Lahore Zone

Out of 98 root tips isolated from genus Salix 54 were found ectomycorrhizal; and 28 were found in association with S. babylonica. Among these 12 belong to Populirhiza lahorensis 9 to Quercirhiza tomentellocystidiata and 7 to Lactarious deliciosus with percent abundance of 42.8532.14 and 25 respectively.Morphotypes isolated from S. tetrasperma were 26. Out of these 19 belong to Quercirhiza tomentellocystidiata and 7 to Populirhiza lahorensis with percent abundance of82.60 and 17.39 respectively (Fig. 3).Ectomycorrhizae formed by Lactarius deliciosus L. with root system of S. babylonica have been identified (Plate 1C Plate 2R-T). Previously they have been reported with Pinus wallichana (Agerer 1987-2006). They are first time reported with S. babylonica. Ectomycorrhizal morphotypes of Populirhiza lahorensis have been found in association with S. tetrasperma (Plate 1E; Plate 2Y-a). Previously these were reported from Populus euramericana (Jabeen et al. 2012).Morphotypes of Quercirhiza tomentellocystidiata have been found with S. babylonica (Plate 1F; Plate 2b-e).Previously it has been reported on Quercus suber (Agerer1987-2002) and P. euramericana (Jabeen et al. 2012).

ECM of Salix spp. from KPK Zone

From KPK zone total 99 root tips were isolated from Salix85 have been found mycorrhizal. Among these 38 were

found associated with S. babylonica 14 belong to Dermocybe cinnamomea 8 to Picirhiza obscura 6 to Genea hispidula and 4 to Salicirhiza pakistanica with percent abundance of 43.75 25 18.75 and 12.5 respectively. Morphotypes associated with S. tetrasperma were 25. Among these 15 belong to Russula foetens 5 to S. gigantica and 5 to S. pakistanica with percent abundance of60 20 and 20 respectively. Morphotypes associated with S. herbacea were 20. Among these 15 belong to D. cinnamomea with 25% abundance and 5 to S. khanspurensis with 75% abundance. Morphotypes isolated from Salix sp. were only 4 which belong to Tuber aestivum (100% abundance) (Fig. 4).Ectomycorrhizal symbiosis of D. cinnamomea having hairy mycorrhizal system in the form of hyphal fans previously reported with Picea abies (L.) Karst. (Agerer1987-2006) (Plate 1A; Plate 2L-N). It is first time being reported with S. herbacea in this investigation.Ectomycorrhizal morphotypes of G. hispidula Berk. et. Br. isolated from S. babylonica are characterized on the basis of simple or irregularly pinnate type of ramification. Anatomically they possess pseudoparenchymatous mantle layers with angular cells throughout and emanating hyphae with wide diameter and simple septa (Plate 1B; Plate 2O-Q).

This fungus is first time reported with S. babylonica and morphotype of this fungus is a new record to the mycoflora of Pakistan.P. obscura associated with S. babylonica shows similarities with that ECM morphotypes of P. abies (Plate1D; Plate 2U-X). The fungus is previously reported with P.abies (Agerer 1987-2006) and has a wide host range. So this is first time being reported with S. babylonica.R. foetens associated with S. tetrasperma has been reported with P. alba (Agerer 1987-2002) and P. ciliata (Jabeen et al. 2012) (Plate 1G; Plate 2f-h). On the other hand morphotypes of S. gigantica isolated from S. tetrasperma has been characterized on the basis of its large dichotomous to coralloid ectomycorrhizal system and pseudoparenchymatous mantle layers with hyphae variable in size and shape. Emanating hyphae branched with clamped septa (Plate 1H; Plate 2i-k). It does not show any characteristic resemblance with any of the reported taxon and seems previously undescribed.Another ectomycorrhizal morphotype S. khanspurensis isolated from S. herbacea is previously undescribed and is characterized by its black simple smooth to grainy morphotype with infrequently formed emanating hyphae on ectomycorrhizal tips. Mantle cells are pseudoparenchymatous with angular layers to roundish cells emanating hyphae with narrow diameter and without septa. Morphotypes of these two taxa can be compared with that of P. hyphaeata (Jabeen et al. 2012). Differences between these two are the presence of abundant emanating hyphae in P. hyphaeata and infrequent in S. khanspurensis. Anatomically they differ in inner mantle hyphae which are plectenchymatous in P. hyphaeata and pseudoparenchymatous in S. khanspurensis. Emanating hyphae with septa are present in P. hyphaeata but are absent in S. khanspurensis (Plate 1I; Plate 2l-n).Morphotypes of S. pakistanica are characterized by its dark brown to black simple irregular system with somewhat beaded appearance. Inflated emanating hyphae emerging from the mantle layer distinguish it from other described taxa (Plate 1J; Plate 2o-q).Ectomycorrhizal system of T. aestivum isolated from Salix sp. has been characterized on the basis of wooly appearance due to abundance of long wooly cystidia present on the tip of mycorrhizal morphotype and pseudoparenchymatous mantle with angular cells. These morphotypes can be compared with mycorrhiza of T. aestivum associated with Corylus avellana L. (Agerer1987-2006). Wooly appearance and pseudoparenchymatous mantle layers are similarities but the main difference is the color of ectomycorrhizal morphotypes which is reddish brown in morphotypes isolated from C. avellana and dark brown to black in morphotypes associated with the root system of Salix sp. These differences might be due to maturity of ectomycorrhiza or due to difference in host species (Plate 1K; Plate 2r-t).Total eleven different types of ectomycorrhizal morphotypes were isolated and characterized. From Lahore zone 3 ectomycorrhizal fungal taxa viz. L. deliceosus P. lahorensis and Q. tomentellocystidiata were isolated. From KPK zone 8 fungal taxa were isolated. Which includes D. cinnamomea G. hispidula P. obscura R. foetens S.gigantica S. khanspurensis S. pakistanica and T. aestivum.Among these 3 morphotypes were previously undescribed and given tentative names (S. gigantica S. khanspurensis and S. pakistanica) and six have been found for the first time associated with Salix spp. (D. cinnamomea G. hispidula P. obscura S. gigantica S. khanspurensis and S. pakistanica). Two morphotypes of fungal species are new records for Pakistan (D. cinamomea and G. hispidula).

Species Accumulation Curves and Estimation of Species Richness

The number of ECM morphotypes observed from Lahore zone and KPK zone were 3 and 8 respectively. Total number of species from these zones was estimated fromcollectors curve' a graph in the form of solid line between

the number of species versus number of individuals. The smooth line of the graph can be obtained using Estimate S to get infinite number of randomizations using an algorithm developed by Mao Chang Xuan [Sobs (Mao Tau)] allowing to calculate the confidence interval.Among three lines in the graph the middle one is very close to the original Sobs (Species observed) curve. The other two lines are the confidence limits. The species accumulation curve looks as though our coverage of species is still rather incomplete (Fig. 1 and 2).

Species Richness Comparison between Lahore Zone andKPK Zone

For the comparison of two sites inferences has been made on the basis of interplotation. In Lahore zone 54 individual mycorrhizal root tips were isolated from 3 ectomycorrhizal morphotype/fungal species. The number of species expected from KPK zone can be estimated from this zone using species accumulation curves (Fig.1 and 2).With 15 samples from KPK Zone 53.4 individual ectomycorrhizal root tips would be isolated which is the nearest value to 54. The average number of species recorded would be 5.93 [Sobs (Mao Tao)]. This is more than that of the 3 species recorded from the Lahore zonewith a very similar number of individual ectomycorrhizalroot tips so it appears that KPK zone is indeed richer in ectomycorrhizal fungal species as compared to Lahore zone.

Percentage Abundance and Diversity Comparison ofEctomycorrhizae from Both Zones

In the present study diversity of ECM fungi associated with Salix spp. growing in two different ecological zones (which differ in climatic conditions e.g. temperature rainfall soil conditions humidity etc.) has been studied by using morpho-anatomical characterization. In Lahore zone Q. tomentellocystidiata showed high percentage abundance in association with S. tetrasperma (82.60%). Whereas P. lahorensis showed high abundance with S. babylonica (42.85%). Other taxa showed low abundance (Fig. 3).In KPK D. cinnamomea exhibited highest percentage abundance in association with S. herbacea and S. babylonica (75% and 43.75 respectively) while R. foetens with maximum abundance (60%) found in association with S. tetrasperma. Only T. aestivium revealed from Salix sp. There is no comparison for its abundance (Fig. 4).Simpson's diversity index measures the diversitytaken place into account the number of species present as well as relative abundance of each species from both zones. Among host tree species high ECM diversity was found in association with S. babylonica from KPK zone while lowest diversity was observed with Salix sp. from KPK zone with highest diversity index (Fig. 5). High

Table 1: Climate physiography edaphic conditions and physiognomy of two climatic regions

Site Description###Lahore (Punjab) zone###KPK zone

Climate###Climatic Region###Semi Arid###Moist Temperate

###(Sethi 2003)###(Sethi 2003)

###Temperature (Mean Annual)###26.5C###10C

###(Malik and Sukhera 2012)###(Malik and Sukhera 2012)

###Rain fall (Mean Annual)###700 mm (Ahmed et al. 2006)###1200mm (Ahmed et al. 2006)

###Humidity###30% (Ahmed et al. 2006)###57% (Ahmed et al. 2006)

Physiography Geography###Most of the area is a level plain formed by the The area ranges from lofty mountains with

###Indus and its tributaries###rugged valleys to undulating and dissected sub-

###(Khalid and Niazi 2003)###mountain plateaus and flat mountains

###(Khalid and Niazi 2003)

###Elevation (Hight Above Sea Level)###217 m###3000-4000 m

###(Government of the Punjab 2007)###(Khan 1999)

Edaphic###Soil###Silty clay loamy clayey###Rock out crop Silt loam to silty clays in valleys

characters###(Shafique et al. 2012)###non-calcareous to slightly calcarious

###(Khan 2004)

###pH###8.58 (Saline-sodic)###less than 7 (Acidic due to high organic matter)

###(Akhtar et al. 2004)###(Irshad and Khan 2012)

###Organic Matter###less than 1%###3-4%

###(Fatima et al. 2012)###(Irshad and Khan 2012)

Physiognomy Vegetation Ecological Zone###Sub-tropical thorn forest###Moist temperate pine forest

###Some dominant tree genera###Accacia Albezia Cassia Dalbergia Eucalyptus Abies Alnus Cedrus Picea Pinus Populus

###Melia Morus Populus Salix Zizyphus###Quercus Salix Taxus

###(Sheikh 1993)###(Sheikh 1993)

Table 2: Pearson correlation coefficients between morphotypes and environmental conditions

Characters###DI###Abd###pH###Temp###Ele###OM###RF

DI###Pearson Correlation###1###.831###.505###.505###-.505###-.505###-.505

###Sig. (2-tailed)###.002###.113###.113###.113###.113###.113

###N###11###11###11###11###11###11###11

Abd###Pearson Correlation###.831 1###.619###.619###-.619###-.619###-.619

###Sig. (2-tailed)###.002###.042###.042###.042###.042###.042

###N###11###11###11###11###11###11###11

pH###Pearson Correlation###.505###.619###1###1.000###-1.000###-1.000###-1.000

###Sig. (2-tailed)###.113###.042###.000###.000###.000###.000

###N###11###11###11###11###11###11###11

Temp###Pearson Correlation###.505###.619###1.000###1###-1.000###-1.000###-1.000

###Sig. (2-tailed)###.113###.042###.000###.000###.000###.000

###N###11###11###11###11###11###11###11

Ele###Pearson Correlation###-.505 -.619###-1.000###-1.000###1###1.000###1.000

###Sig. (2-tailed)###.113###.042###.000###.000###.000###.000

###N###11###11###11###11###11###11###11

OM###Pearson Correlation###-.505 -.619###-1.000###-1.000###1.000###1###1.000

###Sig. (2-tailed)###.113###.042###.000###.000###.000###.000

###N###11###11###11###11###11###11###11

RF###Pearson Correlation###-.505 -.619###-1.000###-1.000###1.000###1.000###1

###Sig. (2-tailed)###.113###.042###.000###.000###.000###.000

###N###11###11###11###11###11###11###11

ECM morphotype diversity was observed with trees found in KPK zone (0.105) while Salix spp. of Lahore zone showed low ECM diversity with their root system (0.697) (Fig. 6).

Discussion

Below ground fungal population is a critical field of study to understanding why certain ectomycorrhizal (ECM) fungi dominate in certain forests In this investigation 11 different fungal taxa were isolated from 30 root samples of

Salix spp. taken from two different geologically distant and climatically varied areas of Pakistan. Out of these eight (8) taxa belong to KPK zone and three (3) to Lahore zone. Among these four (4) morphotypes are previously undescribed and seven (7) have been found for the first time associated with Salix spp. Four (4) morphotypes of fungal species are new records for Pakistan.It appears that in Lahore zone morphotypes of ECM fungal species are abundant but as compared to KPK zone. As species richness increases diversity also increases. Diversity index shows that in KPK zone ECM diversity is greater in KPK zone while lower in Lahore zone. As far as species richness is concerned it was estimated from species richness curve drawn using Estimate S KPK zone is richer in number of ECM species as compared to Lahore zone. The probability of the species finding is higher in KPK zone in comparison with Lahore zone.Although the host genera are same but difference in their ecology is the main factor influencing the abundance diversity and richness of ECM. This difference is due to the difference in climate physiography physiognomy and edaphic conditions of these two zones (Table 1). Percentage abundance and the value of diversty index are positively correlated with pH and temperature while a negative correlation was recorded with altitude and amount of rain fall as well as organic matter content (Table 2). In KPK climate is humid with high organic content in soil provides mycobiont the acidic conditions which support the growth of fungal fruit bodies and mycorrhizae. While the semi-arid and saline soil conditions in Lahore limits the ECM diversity associated with Salix spp. Fungi that do not form obvious fruiting structures form the major mycorrhizal abundance (Gardes and Brun 1996; Jonsson et al. 1999).In conclusion the study demonstrated that ecological factors strongly influence the taxonomic diversity of ECM fungi. Altitude temperature rainfall and soil conditions greatly affect the type of ectomycorrhizae. Some fungi can tolerate high temperature and saline soil conditions as in Lahore zone where the root tip concentration is higher. The results suggest that rare species are relatively less competitive in harsh climatic conditions and increasing dominance reduces overall diversity. The ECM diversity in KPK zone with low temperature high rain fall pattern and acidic soil conditions are the parameters making the diversity two folds higher than in Lahore zone where abundance of morphotypes are found belonging to only three fungal species from equal number of root samples taken from the rhizosphere of Salix spp. of both these zones. KAlrner (2007) reported that altitude is the main factor determining ECM fungal richness. Among the environmental variables the mean annual temperature had the strongest effect on richness and was most strongly correlated with altitude which is a common phenomenon.Generally ECM fungi are important to plant when available nutrients in the soil are limiting but the diversity decrease when nutrients are readily available (Jones and Smith 2004). Despite these variables host tree species also had strong effect on ECM community composition. Dominant tree species in the area differentially modify soilproperties and nutrient availability (Tedersoo et al. 2008ab). The soil environment is one of the most complex parts of the forest ecosystem. ECM ecology is still largely focused on identifying species and describing fungal habitat parameters such as forest stand age and availability of nutrients.Although this information is rapidly accumulating as

is understating of mycorrhizal functions. Nevertheless this review reveals that many gaps in knowledge remain to be filled and mycorrhizologists should focus on little known geographic areas ecosystems host trees and fungal groups in future studies in order to face the challenges the ectomycorrhizal community possess. With more advances in these areas forest management may be improved so that it sustains a healthy below-ground environment.

Acknowledgements

We thank Dr. Abdul Rehman Khan Niazi and Dr. Muhammad Hanif for assistance in field work. We are also grateful to Ms. Sobia Ilyas Mr. Abdul Razaq and Ms. Nousheen Yousaf for their suggestions in data compilation. Thanks is to Ms. Aneela Yasmeen for technical support.

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Publication:International Journal of Agriculture and Biology
Article Type:Report
Geographic Code:9PAKI
Date:Jun 30, 2014
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