INTERNATIONAL JOURNAL OF ENVIRONMENT Volume-5, Issue-2, Mar-May 2016 Received:3 September 2015 ISSN 2091-2854 Revised:13 September 2015 Accepted:21 May 2016 LICHEN AS BIOINDICATOR FOR MONITORING ENVIRONMENTAL STATUS IN WESTERN HIMALAYA, INDIA Sugam Gupta1 *, Roshni Khare2, Omesh Bajpai3, Himanshu Rai4, Dalip Kumar Upreti5 , Rajan Kumar Gupta6 and Pradeep Kumar Sharma7 1,7 Department of Environmental Science, Graphic Era University, Dehradun, Uttarakhand, India 2 Biodiversity-Palaeobiology Lab, Agharkar Research Institute, Pune, Maharashtra, India 3 G.B. Pant Institute of Himalayan Environment & Development, Kosi-Katarmal, Almora, Uttarakhand, India 4,5 Lichenology laboratory, Plant Diversity, Systematics and Herbarium Division; CSIRNational Botanical research Institute, Lucknow, Uttar Pradesh, India 6 Department of Botany, Dr. P.D.B.H. Government Post Graduate College, Kotdwar (Pauri Garhwal), Uttarakhand, India *Corresponding author: sugam_gupta2001@yahoo.com Abstract The use of bioindicator communities (lichen) to assess the environmental status of an area is a well-proved strategy to monitor any habitat without any logistic and instrumental facilities. In the present study, 13 bioindicator communities of lichen have been used to assess the environmental status of holy pilgrimage (Badrinath), western Himalaya, India. Three sites (i.e. Badrinath, Mana & pilgrimage route from Bhimpul to Vasudhara) have been comparatively assessed. The results of the study reveals that Badrinath site is less polluted and experiences low degree of anthropogenic disturbances compared to Mana, and pilgrimage route (Bhimpul to Vasudhara). Human settlements, construction of civil works, vehicular emission, and trampling and trekking by tourists are the major threats on these habitats, which ultimately decrease the quality of vegetation and adjacent environment. Controlled vehicular use, promotion of modern way of cooking and managed trekking in these pilgrimage routes could be helpful to combat the decreasing vegetation and environmental quality therein. Keywords: Bioindicator, Lichen, Vehicular pollution, Anthropogenic disturbances, Badrinath International Journal of Environment ISSN 2091-2854 1|Page Introduction Lichens are slow growing organism and most successful symbiotic association between autotrophic alga and heterotrophic fungus (Farrar, 1976; Galloway, 1992). They are adopted to grow on several kinds of substrates and are reported from all the possible climatic conditions (Ahti, 1959; Sheard, 1968; Pirintsos et al., 1995; Rai et al., 2012). These unique organisms are very sensitive and able to accumulate a range of atmospheric pollutants (Shukla and Upreti, 2008; Shukla and Upreti, 2012; Bajpai et al., 2014). These qualities of the organism attract the environment monitoring workers to use it as a bioindicator to determine the degree and intensity of atmospheric pollution (Sloof et al., 1988; Nimis et al., 1993; Bajpai et al., 2010; Khare et al., 2010; Rai et al., 2012; Van der Wat and Forbes, 2015). Lichen species are highly habitat and climate specific and form the specific communities in different macroclimates (Eldridge and Rosentreter, 1999; Will-wolf et al., 2002; Zedda et al., 2011; Rai et al., 2012). A wide distribution range, adoptability to grow on different substrates and ability to survival in extreme environmental conditions makes them ideal monitors for the assessment of environmental status of a particular area. The poikilohydric nature and unique physiology makes lichens susceptible to climatic variations, pollution, and other environmental factors (Blum, 1973; Lange et al., 1986; Rai et al., 2013). The responses against these variables are reliable at genetic, species, population and community levels (Rosentreter et al., 2014). Natural and/or anthropogenic induced changes in a small area can be easily identified through the occurrence of lichen communities growing in that area (Scutari et al., 2004; Lalley et al., 2006). The monitoring of environmental status of different regions has also been conducted with the help of predictive ability of lichen communities (Srivastava, 2005; Satya and Upreti, 2011; Logesh et al., 2014). Since the last ten decades, a considerable changes/decline in the lichens diversity all around the world has been observed (Hauck, 2009). In context of Indian scenario, Himalayan region is the reserve bank of the lichen diversity (Negi and Gadgil, 1996; Upreti, 1998). At present, the Himalayan region is facing extensive deterioration of air quality owing to increase of anthropogenic disturbances (Rai et al., 2010; Shukla and Upreti, 2011; Rai et al., 2012); which resulted in the rapid decline of lichen diversity (Upreti, 1998; Upreti and Nayaka, 2008). The western Himalaya of Uttarakhand state of India is encountering higher anthropogenic disturbances, bears the higher human as well as animal population and higher magnitude of local tourists due to the presence of holy pilgrimages and sacred shrines in this state, in comparison with the other west Himalayan states of the country. Badrinath is one of the important pilgrimages of the state as well as the country. Although, the floristic diversity of lichen from Badrinath area was studied earlier (Shukla and Upreti, 2007); no biomonitoring study using lichen communities has been executed in the area so far. Thus, International Journal of Environment ISSN 2091-2854 2|Page the present study was carried out in and around Badrinath holy pilgrimage area. The present study was aimed to compare the level of pollution and anthropogenic disturbances using distribution pattern of bioindicator lichen communities. Material and Methods Study Area: Badrinath is a holy pilgrimage, situated in extreme north-west of Chamoli district in the Uttarakhand state of India. It is situated between N 30°44'1.43 to N 30°46'33.74 and E 79°29'32.8 to E 79°29'37.4 with an elevation ranged from 2950 to 3670m on the bank of Alaknanda River (Gupta et al., 2014). The area comprises of typical alpine habitat characterized by alpine grasslands, devoid of big tress with small shrubs of Junipers, Berberis and other herbs scattered onto the open grasslands. Three sites (i.e. Badrinath, Mana & pilgrimage route from Bhimpul to Vasudhara) were selected to conduct the present study (Figure 1). Figure 1. Map showing distribution of lichen communities Lichen Sampling and Identification: During the field trips (2013), more than 500 lichen samples were randomly collected by employing opportunistic survey representing their population size from Badrinath, Mana and pilgrimage route from Bhimpul to Vasudhara (Table 1). The random samplings were carried out according to the availability of the lichens. The geographical co-ordinates of sampling sites were also recorded. The lichens samples were examined morphologically, taxonomically, anatomically and chemically for their identification with the help of previous works (Awasthi, 1988, 1991, 2000, 2007; Gupta et al., 2014; Gupta et al., 2016). The morphological features were studied with Leica EZ4 International Journal of Environment ISSN 2091-2854 3|Page bionocular (40X) and anatomical structures were studied by Nikon Eclipse E400 compound Microscope. The chemistry of all the specimens were performed by colour spot tests (K,C,P) followed by thin layer chromatography (TLC) methods for detection of lichen substances in solvent A (180 toluene: 60 dioxane: 8 acidic acid) (Culberson, 1972). The identification of lichen substances was made on the basis of the position and colour of the spots by charts and data published in reverent references of Elix and Ernst-Russel (1993) and Orange et al. (2001). Voucher specimens of identified species have been deposited in the herbarium of National Botanical Research Institute (LWG), Lucknow. Table 1: Topographical features of Study sites S.No. Sites Elevation Vegetation 1. Badrinath (B) 2950 – 3000 m Devoid of trees, scare growth of shrubs, open rocks, boulders 2. Mana (M) 3000 – 3100 m Devoid of tree, shrubs (except cultivated trees and shrubs) 3. Enroute from Bhimpul 3100 – 3500 m Open grasslands with big boulders and to Vasudhara (B-V) rocks and scattered branches of Berberis, Junipers shrubs. Assessment of pollution and anthropogenic disturbance level: To assess the level of pollution and anthropogenic disturbances, the passive way of biomonitoring (El-Shenaway et al., 2010) was done using well-defined bioindicator lichen communities following Upreti (2014). The randomly collected lichen samples were grouped (three groups) viz. Badrinath (B), Mana (M) and pilgrimage route from Bhimpul to Vasudhara (B-V) according to their localities. Samples were further grouped according to their indicator communities in each locality. Finally, based on the number of lichen samples of an indicator community, the percentage of population was calculated for all three study sites. On the basis of distribution and population percentage of lichen communities, the level of pollution and anthropogenic disturbances have been assessed for these three study sites. Result and Discussion In total, 85 lichen species from three localities (Badrinath, Mana and enroute from Bhimpul to Vasudhara) have been identified and congregated into 13 bioindicator communities (Table 2). The indications of these communities have already been described by several workers in past (Will-Wolf et al., 2002; Pinho et al., 2004; Srivastava, 2005; Khare et al., 2010; Satya and Upreti, 2011; Zedda et al., 2011; Shukla et al., 2014; Upreti, 2014). International Journal of Environment ISSN 2091-2854 4|Page Table 2: List of bioindicator lichen communities with representing species, indication and population percentage in three sites of Badrinath pilgrimage S.No. Community Name of Species Indication 1. Aspicilioid Exposed illuminated less or moderately polluted areas 2. Dimorphic 3. Lecanoriod 4. Lecideoid Acarospora smaragdula (Wahlenb.) A. Massal Acarospora fusca B. de Lesd. Aspicilia maculate (H. Magn.) Aspicilia calcarea (L.) Korb. Candelariella aurella (Hoffm.) Zahlbar Dimelaena oreina (Ach.) Norm Diploschistes scruposus (Schreb.) Norman Diploschistes muscorum (Scop.) R. Sant. Lobothallina praeradiosa (Nyl.) Hafellner Lobothallina alphoplaca (Wahlenb.) Hafellner. Rhizocarpon geographicum (L.) DC Rhizocarpon disporum (Naeg. ex. Hepp) Mull Arg. Cladonia fimbriata (L.) Fr. Cladonia pyxidata (L.) Hoffm. Cladonia subsquamosa Kremp. Cladonia coniocraea (Florke) Spreng. Cladonia ochrochlora Florke. Stereocaulon foliolosum Nyl. Stereocaulon alpinum Laurer in Funck. Stereocaulon myriocarpum Th. Fr. Lecanora muralis (Schreb.) Rabenh Lecanora frustulosa (Dicks.) Ach. Lecanora muralis var. dubyi (MÜll. Arg) Poelt Lecanora garovaglioi (Körb.) Zahlbr Mycobilimbia hunana (Zahlbr.) D.D Awasthi Sarcogyne privigna (Ach.) A Massal. 5. Leprarioid Lepraria lobificans Nyl. 6. Lobarian 7. Parmelioid Lobaria kurokawaeYoshim Peltigera horizontalis (Huds.) Baumg. Peltigera collina (Ach.) Schrad Petigera rufescens (Weiss) Humb Peltigera praetextata (FlÖrke ex Sommerf.) Zopf. Cetraria nigricans Nyl. Cetrelia cetrarioides (Delise) W.L. Club & C.F. Club. Everniastrum cirrhatum (Fr.) Hale ex Sipman Melanohalea infumata (Nyl.) O. Blanco A. Crespo Divakar, Essl., D. Hawksw & Lambush Melanohalea exasperatula (Nyl.) O. Blanco, A. Crespo, International Journal of Environment B 44.0% Study Sites M B-V 35.0% 21.0% High tourist pressure, trampling 52.0% 18.0% 30.0% Open and disturbed vegetation 30.0% 27.0% 43.0% Open and disturbed vegetation Construction disturbances Air pollution 25.0% 30.0% 45.0% 0.0% 100.0% 0.0% 60.0% 0.0% 40.0% Anthropogenic disturbances 18.0% 24.0% 58.0% ISSN 2091-2854 5|Page Divakar, Essl., D. Hawksw & Lambush Melanelia disjuncta (Erichsen) Essl. Flavoparmelia caperata (L.) Hale Hypotrachyna awasthii Hale & Patw. Hypotrachyna incognita (Kurok.) Hale Hypotrachyna flexilis (Kurok) Hale. Parmotrema praesorediosum (Nyl.) Hale Parmelia saxalitis (L.) Ach. Parmelia sulcata Taylor in Mackay Parmelia squarrosa Hale Puntelia subrudecta (Nyl.) Krog. Peltula patellata (Bagl.) Swincow & Krog. 8. Peltuloid 9. Physcioid 10. Teloschistacean 11. Umbilicarioid Heterodermia microphylla (Kurok.) Skorepa Heterodermia japonica (M. SatÖ) Swins & krog Heterodermia boryi (Fee) Kr. P. Singh & S.R Singh Heterodermia pseudospeciosa (Kurok.) W.L. Culb. Heterodermia hypocaesia (Yasuda ex Rasänen) D.D. Awasthi. Physcia albinea (Ach.) Nyl. Physcia gomukhensis D.D. awasthi & S.R. Singh Phaeophyscia constipate Nyl. Moberg. Phaeophyscia hispidula (Ach.) Essl. Phaeophyscia primaria (Peolt) Trass. Pheaophyscia pyrrhophora (Poelt) D. D awasthi & M Josh Physconia detersa (Nyl.) Poelt. Shorepa Physconia muscigena (Ach.) Peolt. Candelaria concolor (Dicks.) Arnold Caloplaca lithophila H. Magn. Xanthoria elegans (Link) Th. Fr. Xanthoria candelaria (L.) Th. Fr. Xanthoria ulophyllodes Räsänen. Normandina pulchella (Borrer) Nyl. Dermatocarpon vellereum Zschacke Dermatocarpon miniatum (L.) W. Mann. Endocarpon rosettum Ajay Singh &Upreti. Endocarpon subrosettum Ajay Singh &Upreti Lasallia pustulata (L.) Merat. Lasallia pertusa (Rassad) Llano. Rhizoplaca chrysoleuca (Sm.) Zopf. Umbilicaria indica Frey. International Journal of Environment Stable rocks 100.0% 0.0% 0.0% Vehicular pollution 31.0% 57.0% 12.0% Higher ultraviolet radiation 13.0% 40.0% 47.0% Higher ultraviolet radiation 15.0% 46.0% 39.0% ISSN 2091-2854 6|Page 12. Usnioid Ramalina sinensis Jatta Usnea subfloridana Stirton. Usnea orientalis Motyka Usnea pseudosinensis Asahina Usnea subflorida (Zahlbr.) Mof. Usnea perplexans Stirt. 13. Xanthoparmelioid Xanthoparmelia bellatula (Kurok. & Filson) Elix & J. Johnst. Xanthoparmelia congensis (B. Stein) Hale. Xanthoparmelia mexicane (Gyeln.) Hale. Xanthoparmelia terricola Hale. T.H. Nash & Elix. Note: B, Badrinath; M, Mana; B-V, Enroute from Bhimpul to Vasudhara. Healthy vegetation and air quality 64.0% 0.0% 36.0% High tourist pressure, trekking 57.0% 31.0% 12.0% Aspicilioid community represented by the species of Acarospora, Aspicilia, Candelariella, Dimelaena, Diploschistes, Lobothallina and Rhizocarpon genera indicates the exposed illuminated area with moderate pollution level. Out of the total samples, Badrinath (B) was represented by 44.0%, Mana (M) by 35.0% and Bhimpul to Vasudhara (B-V) with only 21.0% population (Figure 2A). Dimorphic community representing the species of Cladonia and Stereocaulon genera indicates the trampling and other tourist pressures. Out of the total samples, B represented 52.0%, B-V 30.0% and M only 18.0% population (Figure 2B). Lecanoriod community represented by the species of genus Lecanora indicates the open and disturbed vegetation. Among them, B-V represented 43.0%, B 30.0% and M 27.0% population (Figure 3A). Lecideoid community represented by the species of Mycobilimbia and Sarcogyne genera also indicates the open and disturbed vegetation. B-V represented 45.0%, M 30.0% and B 25.0% population (Figure 3B). Leprarioid community represented by a single species (Lepraria lobificans Nyl.) of Lepraria genus indicates the presence of anthropogenic disturbances caused by the civil construction woks. The species was encountered and sighted only from the Mana (M) village. Lobarian community represented by the species of Lobaria and Peltigera genera indicates the level of air pollution. B represented 60.0% and B-V 40.0% population; while the community was found absent in Mana (M) village (Figure 4A). Parmelioid community represented by the species of Cetraria, Everniastrum, Melanohalea, Melanelia, Flavoparmelia, Hypotrachyna, Parmotrema and Parmelia genera indicates the status of anthropogenic disturbances. B-V represented 58.0%, B 22.0% and M 20.0% population (Figure 4B). Peltuloid community was represented by a single species (Peltula patellata (Bagl.) Swincow & Krog.) of Peltula genus indicates the presence of stable rocks i.e. lower risk of landslides. The species was encountered from the Badrinath (B) area only. Physcioid community represented by the species of Heterodermia, Physcia, Phaeophyscia and Physconia genera indicates the level of vehicular pollution. M represented 57.0%, B 31.0% and B-Vonly 12.0% population (Figure 5A). Teloschistacean community represented by the species of Candelaria, Caloplaca and International Journal of Environment ISSN 2091-2854 7|Page Xanthoria genera indicates the higher level of ultraviolet radiation. B-V represented 47.0%, M 40.0% and B only 13.0% population (Figure 5B). Umbilicarioid community represented by the species of Normandina, Dermatocarpon, Endocarpon, Lasallia, Rhizoplaca and Umbilicaria genera also indicates the higher level of ultraviolet radiation. M represented 46.0%, B-V 39.0% and B only 15.0% population (Figure 6A). Usnioid community represented by the species of Ramalina and Usnea genera also indicates the healthy vegetation and good air quality. B represented 64.0%, and B-V 36.0% population; while no Usnioid community was encountered from Mana (M) village (Figure 6B). Xanthoparmelioid community represented by the species of Xanthoparmelia genus indicates the trekking and tourist pressure. B represented 57.0%, M 31.0% and B-V only 12.0% population (Figure 6C). Figure 2. Contribution by different sites in lichen community of: A- Aspicilioid; BDimorphic Figure 3. Contribution by different sites in lichen community of: A- Lecanoriod; BLecideoid International Journal of Environment ISSN 2091-2854 8|Page Figure 4. Contribution by different sites in lichen community of: A- Lobarian; BParmelioid Figure 5. Contribution by different sites in lichen community of: A- Physcioid; BTeloschistacean Figure 6. Contribution by different sites in lichen community of: A- Umbilicarioid; BUsnioid; C- Xenthoparmelioid International Journal of Environment ISSN 2091-2854 9|Page The presence of Aspicilioid community members in Badrinath (B) and Mana (M) area with higher population percentage clearly indicates that both the areas are facing less to moderate anthropogenic disturbances. As the Lobarian, Physcioid and Usnioid communities indicates the air quality, it is very clear that the Badrinath (B) area has the good air quality, less pollution and less vehicular pollution in comparison with the Mana (M) area. The absence of Lobarian and Usnioid communities in Mana indicated the worst condition of air quality in this area. Such kind of indications is also observed by other workers in different areas (Sloof et al., 1988; Pinho et al., 2004; Shukla et al., 2014). The presence of Physcioid community in very few localities of enroute from Bhimpul to Vasudhara (B-V) indicates very less vehicular pollution in this area. Teloschistacean and Umbilicarioid communities comprise the ultraviolet tolerant lichen species. The presence of lichen species of Teloschistacean & Umbilicarioid communities from Mana (40.0% & 46.0%) and B-V (47.0% & 39.0%) respectively indicates the presence of higher ultraviolet radiation in these two sites in comparison to Badrinath area with 13% & 15% population respectively. Upreti et al. (2014) also utilizes these species as indicator of ultraviolet radiation. Lecanoriod & Lecideoid communities comprise the lichen species which can tolerate higher anthropogenic disturbances. B-V site represent the maximum (43.0% & 45.0%) population of Lecanoriod & Lecideoid communities respectively and clearly indicates the presence of higher anthropogenic pressure, which is reflected by the disturbed vegetation present in the pilgrimage route. The status of anthropogenic disturbances has also been accessed by the distribution of these indicator lichen communities by Shukla and Upreti (2011) and Rai et al. (2012). The species of Dimorphic & Xanthoparmelioid communities are very sensitive to any kind of disturbances caused by trampling & trekking of tourists and demolished from the area suffering from such type of pressure. Presence of good population of these indicator species from Badrinath area (52.0% & 57.0% respectively) reveals the low pressure trampling & trekking pressures; while the lower population of these communities from Mana and B-V area designates these areas with higher tourist pressure. The similar observation has also been observed in other area of Garhwal Himalaya (Khare et al., 2010). The Leprarioid community is the pioneer ones, which appears very first after any civil construction in an area. The presence of this community only from the Mana site reveals that several kinds of civil constructions (roads, houses etc.) are going on in this area, which ultimately caused the adverse effects on the lichen as well as entire vegetation (Satya and Upreti, 2011; Upreti, 2014). The members of Peltuloid community always found to grow on the older rocks and boulders and thus they are the good indicators of the landslides area. The presence of this community only from Badrinath site reveals that the landslides occurred very rarely in this area; while it occurred frequently in Mana and B-V sites as no indicator species has been collected from these two areas. The Parmelioid members have the higher International Journal of Environment ISSN 2091-2854 10 | P a g e tolerance capacity against different anthropogenic activities and environmental pollution (Shukla and Upreti, 2012; Bajpai et al., 2014). The presence of luxurious population of the species (58.0%) belonging to this community at B-V site reveals the higher anthropogenic activities in this site in comparison with the other two sites, Mana (24.0%) and Badrinath (18.0%) population. Over all the Parmelioid, Peltuloid, Leprarioid, Dimorphic, Xanthoparmelioid, Lecanoriod, Lecideoid, Teloschistacean and Umbilicarioid bioindicator communities cumulatively indicates that the Badrinath site is comparatively bears healthy vegetation, less polluted, ultraviolet radiation and also facing the lower level of anthropogenic disturbances; on the other hand Mana & enroute from Bhimpul to Vasudhara (B-V) sites bears disturbed vegetation, more polluted, ultraviolet radiationand facing higher level of anthropogenic disturbances. When we talk about the air quality, it has been exposed by good population of Lobarian, Physcioid and Usnioid communities that Badrinath site is again represents the good air quality; while in Mana site the air quality is in bad condition as it very less and/or no population of these communities. This is may be due to the heavy vehicular and household pollution as the site has a good human settlement. Conclusion The study reveals that the Badrinath site of Badrinath holy pilgrimage of Western Himalaya is still comparatively less polluted and disturbed. The Mana site has been found as highly polluted and disturbed due to human settlement, different construction of civil works and vehicular emittion. The pilgrimage route from Bhimpul to Vasudhara (B-V) has also been found highly disturbed but here trampling and trekking caused by tourists was the major source of disturbances. Some suggestions to overcome the increasing level of pollution & anthropogenic disturbances and to conserve not only the lichen as well as other vegetation are, governmental control on the use of vehicles in higher elevation areas, promotion of lesser pollution emitting way of cooking (LPG, biogas, modern stove etc.) and managed trekking in the pilgrimage routes. 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