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Floral Sources for Stingless Bees ( ) in NellithuraiVillage, Tamilnadu, India Tetragonula iridipennis K. Vijayakumar, R. Jeyaraaj Department of Zoology, Kongu Nadu Arts and Science College, Coimbatore, Tamil Nadu, India Key words: Bee flora, Non-floral sources, Melissopalynology, Meliponiculture. StudyArea: Nellithurai Village, Tamilnadu, India Coordinates: 11°16'59.74”N & 76°53'6.24”E RESEARCH ARTICLE Published by: National Cave Research and Protection Organization, India Vol. 3(2): 69-74 Year 2016 *Corresponding Author: [email protected] ISSN- 2348 5191 (Print) & 2348 8980 (Electronic) ambient SCIENCE Ambient Science, 2016: Vol. 03(2); 69-74 DOI:10.21276/ambi.2016.03.2.ra04 We documented 45 plant taxa belonging to 29 families and non-floral sources utilized by Tetragonula iridipennis for pollen, nectar and resin. The foragers of T. iridipennis were also found to collect non-floral resources like fruit juice, fruits kept in the market for sales and from falling and damaged mango and jasmine fruits. The mutualistic association between T. iridipennis colonies and Hemipterans was observed and documented. According to pollen analysis, all are appeared to be multifloral honeys. The families Arecaceae and Fabaceae had a significant importance amongst the samples represented by four pollen types. Coconut, Sunflower and Banana pollen types occurred most constantly among the samples. The present palynological analysis of honey samples can provide the accurate depiction of the bee flora in Nellithurai village. The present study to help the beekeepers to know the stingless bee flora and to identify the botanical origins of honey. Abstract Introduction: Stingless bees comprise a highly diverse and abundant group of eusocial bees that inhabit the tropical and subtropical parts of the world. These are the major biomass component of the nectar and pollen foraging insect community in many tropical areas. Stingless bees are effective pollinators of wild and cultivated crops. According to Kerr (2001), 30-80% of plants are pollinated by one or more species of stingless bees in their biomes. In India, Tetragonula iridipennis is widely distributed and nests invarying substrates, becoming also abundant in disturbed areas. The colonies of stingless bees make less honey, as compared to other contemporarily honey bees. In the tropical regions, there are a variety of trees, shrubs and agricultural crops that provide pollen and nectar to the bees. Apis uses large amounts of pollen to support its brood production and swarming, while the stingless bees do not often swarm and uses less pollen (Roubik, 2006 ) . is a gentle species and easily adjusts to beekeeping used to collect honey or to pollinate crops (Kumar 2012; Vijayakumar 2013). They are generalists in their habits and their eff icient pollination on the tropical flora is remarkable. Studies have been made in areas harbordifferent types et al. T. iridipennis et al. et al. of vegetation such as natural forests, grasslands, agricultural land, pasture land, or urban areas. Most of the methods for obtaining information about bee plants in an area are based on direct f ield observation of foraging bees on flowers. Absy & Kerr (1977) using pollen analysis of honey began the study of stingless bee floral visitation in the Amazon region, which comprises different forest types, namely savannas and riversides including human- disturbed landscapes and urban areas. In Brazil, Oliveira (2009) demonstrated that stingless bees are using varity of pollen resources, but they are not commonly utilized the unique plant species. The analysis of bee plant pollen loads and palynological analysis of honey samples can provide the accurate depiction of the bee flora of a particulararea/landscape (Lakshmi, 2012). The melissopalynological studies of stingless bee honey are rare, limited to and (Absy & Kerr 1977), sp. aff. sp., sp. aff. and (Vit 1994), (Carvalho , 2001) , (Alves 2006 ), (Flores & Sanchez 2010) , and (Vit 2012). In India, signif icant work et al. Melipona seminigra merrillae Melipona rufiventris paraensis Melipona compressipes, Melipona favosa, Melipona trinitatis, Frieseomelitta nigra, Frieseomelitta varia, Plebeia Scaptotrigona depilis , Scaura latitarsis T. angustula et al. Melipona scutellaris et al Melipona mandacaia et al. Tetragonisca angustula M. favosa et al.

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Floral Sources for Stingless Bees ( ) inNellithuraiVillage, Tamilnadu, India

Tetragonula iridipennis

K. Vijayakumar, R. Jeyaraaj

Department of Zoology, Kongu Nadu Arts and Science College,Coimbatore, Tamil Nadu, India

Key words: Bee flora, Non-floral sources,Melissopalynology, Meliponiculture.

StudyArea: Nellithurai Village, Tamilnadu, IndiaCoordinates: 11°16'59.74”N & 76°53'6.24”E

RESEARCH ARTICLE

Published by: National Cave Research and Protection Organization, IndiaVol. 3(2): 69-74

Year 2016

*Corresponding Author: [email protected]

ISSN- 2348 5191 (Print) & 2348 8980 (Electronic)

ambientSCIENCE

Ambient Science, 2016: Vol. 03(2); 69-74DOI:10.21276/ambi.2016.03.2.ra04

We documented 45 plant taxa belonging to 29 families andnon-floral sources utilized by Tetragonula iridipennis forpollen, nectar and resin. The foragers of T. iridipennis werealso found to collect non-floral resources like fruit juice,fruits kept in the market for sales and from falling anddamaged mango and jasmine fruits. The mutualisticassociation between T. iridipennis colonies andHemipterans was observed and documented. According topollen analysis, all are appeared to be multifloral honeys.The families Arecaceae and Fabaceae had a signif icantimportance amongst the samples represented by fourpollen types. Coconut, Sunflower and Banana pollen typesoccurred most constantly among the samples. The presentpalynological analysis of honey samples can provide theaccuratedepictionof the bee flora in Nellithurai village. Thepresent study to help the beekeepers to know the stinglessbee floraand to identify the botanical originsof honey.

Abstract

Introduction:Stingless bees comprise a highly diverse and abundantgroup of eusocial bees that inhabit the tropical andsubtropical parts of the world. These are the majorbiomass component of the nectar and pollen foraginginsect community in many tropical areas. Stingless beesare effective pollinators of wild and cultivated crops.According to Kerr (2001), 30-80% of plants arepollinated by one or more species of stingless bees in theirbiomes. In India, Tetragonula iridipennis is widelydistributed and nests in varying substrates, becoming alsoabundant indisturbed areas. Thecoloniesof stingless beesmake less honey, as compared to other contemporarilyhoney bees.

In the tropical regions, there are a variety of trees,shrubs and agricultural crops that provide pollen andnectar to the bees. Apis uses large amounts of pollen tosupport its brood production and swarming, while thestingless bees do not often swarm and uses less pollen(Roubik, 2006 ) . is a gentle species and easilyadjusts to beekeeping used to collect honey or to pollinatecrops (Kumar 2012; Vijayakumar 2013). Theyaregeneralists in their habits and their eff icient pollinationon the tropical flora is remarkable.

Studies have been made inareas harbordifferent types

et al.

T. iridipennis

et al. et al.

of vegetation such as natural forests, grasslands,agricultural land, pasture land, or urban areas. Most of themethods for obtaining information about bee plants in anarea are based on direct f ield observation of foraging beeson flowers. Absy & Kerr (1977) using pollen analysis ofhoney began the study of stingless bee floral visitation inthe Amazon region, which comprises different foresttypes, namely savannas and riversides including human-disturbed landscapes and urban areas. In Brazil, Oliveira

(2009) demonstrated that stingless bees are usingvarity of pollen resources, but they are not commonlyutilized the unique plant species. The analysis of bee plantpollen loads and palynological analysis of honey samplescan provide the accurate depiction of the bee flora of aparticulararea/landscape (Lakshmi, 2012).

The melissopalynological studies of stingless beehoney are rare, limited toand (Absy & Kerr 1977),

sp. aff.sp., sp. aff.

and (Vit 1994),(Carvalho , 2001) , (Alves2006 ), (Flores & Sanchez 2010) ,and (Vit 2012). In India, signif icant work

et al.

Melipona seminigra merrillaeMelipona rufiventris paraensis

Melipona compressipes, Melipona favosa, Meliponatrinitatis, Frieseomelitta nigra, Frieseomelitta varia,Plebeia Scaptotrigona depilis , Scaura latitarsis

T. angustula et al. Melipona scutellariset al Melipona mandacaia et al.

Tetragonisca angustulaM. favosa et al.

http://www.caves.res.in/

has beencarried out byvariousauthors (Ramanujam1992; Bhargava 2009 & Shilpa & Ratan, 2011).Melissopalynology of honey has been studiedby Suryanarayana (1966) and Bhargava (2009).Foraged pollen loads are good indicators of thesurrounding flowering plant species that provide pollenfor the bees. They also indicate availability of dominantfood resources for the different pollinators in anecosystem. The purpose of this study has been to use twodifferent methods to identify the plant species visitedmost frequently by .

The study was carried out in the Nellithuraivillage of Coimbatore district, Tamil Nadu, India. Fieldobservations were conducted between April 2013 to March2014. In situ identif ication of plants visited by stinglessbee forageswasdone bydirectobservation in the f ield. Thebee floral survey carried out during peak foraging activity(6.00 am - 6.00 pm). Plant species were consideredattractive to bees when they were observed tovisit by morethan f ive bees during a particular time interval (10 min).The identif ication of pollen, nectar and resin foragersvisually based on either pollen or resin load on corbiculaeand honey stomach. The forager bees were caught withsweep netsand preserved for furtherstudies.

Present melissopalyno-logical investigation was carried out in 15 different honeysamples collected from different hived colonies ofTetragonula iridipennis located at Nellithurai village,Tamil Nadu, India. Pollen slides of honey samples wereprepared using the method of Loureaux et al. (1978) andacetolysis (Erdtman, 1960). The pollen grains obtainedfrom honey samples were identif ied and compared withthe reference slides made from identif ied plants and fromstandard works of Erdthman (1960) and Lakshmi (2012).The absolute pollen count and percentages of pollen typesin each sample were calculated (Lakshmi, 2012) on thebasis of total number of pollen grains counted in eachsample. Samples were observed using light and polarizedlight microscopy.

The pollen spectra were constructed on the basisof these percentages. Honey samples having 45% or moregrains of a single pollen type were termed as “unifloralhoney” and those having several pollen types inconsiderable percentage were termed as “multifloralhoney”. Frequencies and frequency classes of the pollentypes were determined in accordance with Louveaux etal.(1978) and the pollen types were placed under fourpollen frequency classes (Predominant pollen D (Above45%), Secondary pollen S (16% to 45%), Important minorpollen - IM (3% to 15%), Minor pollen m (Less than 3%))recommended by the International Commission for BeeBotany (ICBB) (Moore & Webb, 1978).

et al.,et al.,

Syzygiumet al.

T. iridipennis

Study Area:

Melissopalynological study:

Materialsand methods:

ResultsBeefloral survey

Extra-floral nectarines and non- floral resources:

Melissopalynological study:

Predominant families of flowering plants in the studyarea: A total of 45 plant species belonging to 28 familieswere recorded. The important flowering families wereArecaceae and Fabaceae representing the highestfrequency of 4 (8.89% N=45), Cucurbitaceae,Euphorbiaceae, Poaceae and Solanaceae with frequencyof 3 (6.67% N=67), Lamiaceae and Rutaceae withfrequency of 2 (4.44% N=45) and remaining 20 families( A m a r a n t h a ce a e , A n a c a r d i a ce a e , A p i a ce a e ,Ap o c yn a ceae , C a l e n d u l eae , Co m m e l i n a ceae ,Convolvulaceae, Lythraceae, Malvaceae, Meliaceae,Moringaceae, Musaceae, Myrtaceae, Nyctaginaceae,Phyllanthaceae, Portulacaceae, Rubiaceae, Verbenaceae,Vitaceae and Zygophyllaceae) with frequency of 1 (2.22%N=45) (Figure: 1).

honeydew produced by sap-sucking Homoptera is animportant resource for a variety of organisms. Theforagers of were also found to collect non-floral resources like fruit juice, fruits kept in the marketfor sales and from falling and damaged mango andjasmine fruits. Foragersof were also found tocollect sugar sap from leaf nectaries (Plate 1a), sugar canesap from crushed sugarcane stems (Plate 1b), watermelonjuiceand coconut neera. The foragerscollected honeydewactively from papaya mealy bug ( )(Plate 1c). The forager of collects fresh resinfrom falling flowers (Plate 1d) and tree wounds. Theforager of were observed landing onmealybug assemblages and ingesting excess honeydewand bees were found to collect the honeydew from themealy bug in the morning and late afternoon duringobservation times.

melissopalynologicalinvestigations carried out on 15 honey samples collectedfrom hived T. iridipennis colonies and indicated that thebees were found to forage on 45 pollen types belonging to29 families for pollen, nectar and resin. The pollenmicrograph was showed in plate 2. During this study, thepollen samples are taken from 15 hived T. iridipennis

T. iridipennis

T. iridipennis

Paracoccus marginatusT. iridipennis

T. iridipennis

Ambient Science (2016) Vol.-03(2): p. 70

Figure 1. Important families of floral resources utilizedby T. iridipennis

RESEARCH ARTICLE

Ambient Science, 2016: Vol. 03(2); 69-74DOI:10.21276/ambi.2016.03.2.ra04

colonies on April 2013 to March 2014 and were subjected tomicroscopicanalysis.

Results from the palynological studies show thatstingless bees collect pollen from a wide range of plantspecies. Pollen grains of Cocus nucifera, Helianthusannuls and Musa paradisiaca were identif ied as asecondary pollen group. The important minor pollengroups (IM) and minor pollen groups (m) tabulated intable 3. Other plants were also visited by are

sp.,

and . The lowest pollenfrequency of 11 to 20 was noted in

and

the present study site located near the NilgiriBiosphere Reserve located within the Western Ghatsand isa region having high ecological and sociologicalimportance (Prabhakar, 1994). Recently, Sasidharan &Kunhikannan (2010) recorded 113 plant species belongingto 93 genera and 42 families which associated with bees inthe Nilgiri Biosphere Reserve. During the study, a total of45 plant species of 12 families was recorded at the source ofPollen/nectar/resin for stingless bees ( ). Theplant species found in agricultural f ields are of greateconomic importance. Results showed that the stingless

T. iridipennisAlternanthera sessilis, Tamarindus indica, Helianthusannuls, Cajanus cajan, Citrus medica.Calotropisgigantean, Parthenium hysterophorus, Pongamia pinnata,Azadirachta indica, Aerva tomentosa, Digera muricata,Evolvulus alsinoides, Mimosa pudica, Jatropha curcas,Phyllanthus emblica, Capsicum frutescens, EucalyptusSoalnum melongena, Mangifera indica, Benincasa hispida,Prisopis julifera Sorghum halepense

Vitex negundo,Coriandrum sativum, Tribulus terrestris Pennisetumamericanum.

T. iridipennis

Floral sources and non flora sources for stinglessbees:

Discussion:

bee-flora consists of mostly timber, medicinal, fruits,vegetables, ornamentals and other commerciallyimportant plants like pulses, cereals, oil yielding, f iber,fodder etc. Multivarious of the economic importance ofthe beeplants must beprotected.

Honeydew produced by sap-sucking Homopterais an important resource for a variety of organisms. In thepresent study, the mutualistic association between T.iridipennis colonies and Hemipterans was observed anddocumented. The forager bees found to collect thehoneydew from the mealy bug. Similarly, the associationbetween Hemipterans and stingless bees were discussedby Camargo & Pedro (2002) and found only the genusSchwarzula had mutualist ic association withHemipterans. Roubik (1989) observed the mutualisticassociation between stingless bees and Hemipterans. Inaddition, some species of stingless bees with obligatenacrophagic habits, three species (Trigona necrophaga,T.hypogea and T.crassipes) were found to collect flesh ofdead animals is their only protein source and sugarsobtained from ripe or rotting fruit, extra floral nectaries,fallen flowerson theground (Roubik, 1982).

: the results of the pollenanalysesreveals that the foragesof are mostlypreferred the 12 plants species belonging to four familes(Asteraceae, Musaceae, Fabaceae and Poaceae). Thehighest frequency (71 to 100%) was noted in pollen of

. The presence of the abovepollen types were noted annually, which conf irmed theattractivenessof theirpollenand nectartostingless bees.

Similarly, Singh & Kar (2011) recorded a diversespectrum of 27 pollen types belonging to 19 families from12 Sunderbans honey samples (Bangaldesh) andAndaman (India). Jhansi (1994) recorded 51 pollentypes referable to 36 families in the samples studies fromAndhra Pradesh, India. Atwal (1970) studieddifferent bee flora for four species of forLucknow region based on the pollen analysis. Recently,Padmavathy & Rehel (2014) recorded 12 species belonging

Melissopalynological studyT. iridipennis

Cocus nucifera, Zea myze, Musa paradisiaca andCommelina benghalensis

et al.

et al.Apis mellifera

http://www.caves.res.in/Ambient Science (2016) Vol.-03(2): p. 71

aa bb

ddccPlate 1: collecting - nector from leaf, from

crushed sugercane, excretes from animal waste,resin from falling flowers

T. iridipennis a) b)c) d)

Acacia torta

Parthenium sp.

Alternanthera Cocus nucifera Cocus nuciferasp.

Tamarindus indica Mimosa pudica Mimosa pudica

Plate 2: Pollen micrographs

RESEARCH ARTICLE

Ambient Science, 2016: Vol. 03(2); 69-74DOI:10.21276/ambi.2016.03.2.ra04

to 11 families were identif ied as floral sources forin Conoor, Nilgiri hills, Tamil Nadu. Theyrecorded

the pollen grains of and spp.frequently from the honeysamplesof .

Apollenspectrumreveled that thepollengrainsofas a major source of pollen and it was found

throughout the year in the present study area. Similarly,Bhargava (2009) reported that as thepollen source available throughout the year in Karnataka,India. In addition, Sekhar (2000) revealed that thedominant pollen sources for bees in Bangaluru region arealso and . ManyAsteraceae species produce nectar (Terrab 2001) andaccording to our results the taxa of this family are of greatimportance both as nectar and pollen source in the studyarea. In addition, Suryanarayana (1991) in their studyat Muzaffarpur (Bihar), India, reported that members ofAsteraceaeprovided forage fora majorpartof theyear.

The present study conf irmed the availability ofhigh diversity vegetation around Nellithurai village. Inaddition, melissopalynology of stingless bee honey helpsto characterize vegetation surrounding the collection siteand provide detailed information on stingless beeflowering plants. The present study helps the beekeepersand farmers to know the flowering plants utilized bystingless bees. Thus they can take appropriates steps todevelop meliponiculture.

Apisdorsata

Syzygium cumini AcaciaA.dorsata

Cocus nucifera

et al. Cocus nucifera

Cocus nucifera Eucalyptus tereticorniset al.,

et al.

We are grateful to Dr. Cleofas R.Cervancia, for her guidance during the study. We are especiallyindebted to Dr. Deborah Smith (University of Kansas, USA) foridentifying stingless bee species and providing relevant literature.I extend my sincere thank to Dr. M. Muthuraman, for hisencouragement and motivation to pursue the research work. Iwould also like to thank to beekeeper Mr. G.K. Thangavelu forsamplecollectionand documentation.

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,

Table-1: Stingless bee floral sources in Nellithurai village

No Scientif ic name Common name /Tamil name Family Habitat1 Adhatoda zeylanica Malabarnut/ Adathoda Acanthaceae Herb2 Alternanthera sessilis Dwarf copperleaf Ponnanganni Keerai Amaranthaceae Herb3 Azadirachta india Neem/Vambu Meliacae Tree4 Benincasa hispida Pumpkin / Poosanikai Cucurbitaceae Vegetable5 Boerhavia diffusa Red spiderling/ Mukkarattai keerai Nyctaginaceae Herb6 Calotropis gigantean Yerukku Apocynaceae Shrub7 Calendula off icinalis Mary gold Calenduleae Herb8 Capsicum frutescens Chilly Solanaceae Vegetable9 Caryota urens Jaggery Palm Arecaceaee Herb10 Ceiba pentandra Java kapok/ Ilavam Malvaceaee Tree11 Cissus quadrangularis Devil's Backbone/ Pirandai Vitaceae Climber12 Citrus medica Lemon Rutaceae Shrup13 Coccinia grandis Little gourd/ Kovai Cucurbitaceae Climber14 Cocus nucifera Coconut Palm Arecaceaee Tree15 Commelina benghalensis Benghal dayflower/ Kanan Keerai Commelinaceae Herb16 Coriandrum sativum Coriander/ Kothamalli Apiaceae Herb17 Croton bonplandianum Croton/ Rail Poondu Euphorbiaceae Herb18 Evolvulus alsinoides Vishnukiranthi Convolvulaceae Herb19 Eucalyptus sp. Thailamaram Myrtaceae Tree20 Helianthus annuls Sunflower Asteraceae Oil seed21 Ixora coxinia Jungle flame/ Itlly Poo Rubiaceae Shrub22 Jatropha curcas Physic nut Euphorbiaceae Shrub23 Jatropha gossypifoli - Euphorbiaceae Shrub24 Lantana camara Wild Sage/ Unni Verbenaceae Shrub25 Lawsonia inermis Henna/ Maruthani Lythraceae Shrub26 Mangifera indica Mango/ Maa Anacardiaceae Tree27 Momordica charantia Bitter Guard/ Paval Cucurbitaceae Climber28 Moringa pterygosperma Drum Stick/ Murungai Moringaceae Tree29 Murraya koenigii Curry tree/ Karuvapplli Rutaceae Shrub30 Musa paradisiaca Banana Musaceae Tree31 Ocimum canum Holy Basil/ Nai thulasi Lamiaceae Herb32 Parthenium hysterophorus Parthenium weed/ Visha Poondu Asteraceae Herb33 Pennisetum americanum Pearl millet/ Kambu Poaceae Pulses34 Phyllanthus emblica Amla/ Nelli Phyllanthaceae Tree35 Portulaca oleracea . Pigweed/ Paruppu Keerai Portulacaceae Herb36 Prisopis julifera Mesquite Fabaceae Shrub37 Pithecellobium dulce Manila tamarind/ Kodukkapuli Fabaceae Tree38 Soalnum melongena Brinjal Solanaceae Vegetable39 Solanum nigrum Black nightshade/ Manathakali Solanaceae Herb40 Sorghum halepense Johnson grass/ Solam Poaceae Pulses41 Tamarindus indica Tamarind/ Poliyamaram Fabaceae Tree42 Tribulus terrestris Tackweed/ Nerinji Zygophyllaceae Herb43 Vigna radiate Green Gram/ Pasi Payaru Fabaceae Pulses44 Vitex negundo Nochi Lamiaceae Shrub45 Zea myze Myze Poaceae Pulses

RESEARCH ARTICLE

Ambient Science, 2016: Vol. 03(2); 69-74DOI:10.21276/ambi.2016.03.2.ra04

Ambient Science (2016) Vol.-03(2): p. 74http://www.caves.res.in/

Table-2: Important pollen groups in the study area and their frequency

S.No Family Pollen type S IM M FO*

*Frequency observation

1 Acanthaceae Aerva tomentosa 5 33.302 Alternanthera sessilis 10 66.703 Digera muricata 6 40.004 Anacardiaceae Mangifera indica 1 3 26.605 Apiaceae Coriandrum sativum 2 1 20.006 Apocynaceae Calotropis gigantean 6 1 46.677 Asteraceae Cocus nucifera 12 2 1 100.008 Helianthus annuls 6 3 60.009 Parthenium hysterophorus 3 2 2 46.6710 Tridax procumbens 1 5 40.0011 Commelinaceae Commelina benghalensis 11 73.3312 Convolvulaceae Evolvulus alsinoides 5 33.3013 Euphorbiaceae Croton bonplandianum 3 20.0014 Jatropha curcas 4 2 40.0015 Fabaceae Cajanus cajan 5 3 53.3316 Pongamia pinnata 4 3 46.6717 Mimosa pudica 4 26.6018 Tamarindus indica 2 5 3 66.7019 Lamiaceae Vitex negundo 1 1 13.3320 Meliaceae Azadirachta indica 6 1 46.6721 Myrtaceae Eucalyptus sp. 2 2 26.6022 Musaceae Musa paradisiaca 7 4 73.3323 Phyllanthaceae Phyllanthus emblica 1 4 33.3324 Poaceae Pennisetum americanum 3 20.0025 Sorghum halepense 4 26.6026 Zea myze 7 3 2 80.0027 Rutaceae Citrus medica 3 1 4 53.3328 Solanaceae Capsicum frutescens 1 5 40.0029 Soalnum melongena 6 40.0030 Zygophyllaceae Tribulus terrestris 3 20.00

RESEARCH ARTICLE

Ambient Science, 2016: Vol. 03(2); 69-74DOI:10.21276/ambi.2016.03.2.ra04