Abstract
Microalgae are an effective source of bioindicators to screen any changes of the natural ecosystem in the environment. With the increase in air pollution due to different potential sources, pollution monitoring stations are deployed across the nation with sophisticated analytical methodologies. However, phytoplankton can also serve as an indicator of air pollution as they possess the ability to absorb particulate contaminants. With previous studies on indicator species based on aquatic habitats, this study was carried out to comprehend the interaction between gaseous oxides of sulphur and nitrogen, particulate matter with diameter less than 10 and 2.5 μm (PM10, PM 2.5), with the population density, abundance and frequency of terrestrial epiphytic microalgae from residential and commercial areas of Chennai District, Tamil Nadu. There was a significant correlation between the members of Chlorophyceae, Bacillariophyceae and Cyanophyceae with the abovementioned air pollutants. Cluster analysis, CCA and NMDS analysis were done to find the interaction pattern. The results suggested few indicator species from genera Chlorella, Phormidium, Nitzschia, Navicula, Spirogyra and Oscillatoria. Species of Desmodesmus, Gleocapsa, Gleocyctis and Lyngbya can be considered as an addition to Palmer’s list of tolerant species. During this study, the occurrence of filamentous Cladophora crispata is reported for the first time from Tamil Nadu, India. This study unveiled the list of microalgal species resistant to air pollutants from one of the highly polluted cities of India.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All data generated or analysed during this study are included in this published article (and its supplementary information files).
References
Aidaoui L, Triantafyllou AG, Azzi A, Garas SK, Matthaios VN (2014) Elevated stacks’ pollutants’ dispersion and its contributions to photochemical smog formation in a heavily industrialized area. Air Qual Atmos Health 8(2):213–227. https://doi.org/10.1007/S11869-014-0300-9
Altaf HG, Saltanat P (2014) Effect of physico-chemical conditions on the structure and composition of the phytoplankton community in Wular Lake at Lankrishipora, Kashmir. Int J Biodivers Conserv 6(1):71–84. https://doi.org/10.5897/ijbc2013.0597
Arguelles ED (2019) Systematic study of some epiphytic algae (non-diatoms) on the submerged parts of water hyacinth [Eichhornia crassipes (Mart.) Solms-Loubach] found in Laguna de Bay, Philippines. Trop Life Sci Res 30(1):1–21. https://doi.org/10.21315/tlsr2019.30.1.1
Armitage AR, Frankovich TA, Fourqurean JW (2006) Variable responses within epiphytic and benthic microalgal communities to nutrient enrichment. Hydrobiologia 569(1):423–435. https://doi.org/10.1007/s10750-006-0146-8
Atkinson R, Lloyd AC (2009) Evaluation of kinetic and mechanistic data for modeling of photochemical smog. J Phys Chem Ref Data 13(2):315. https://doi.org/10.1063/1.555710
Barberousse H, Lombardo RJ, Tell G, Couté A (2007) Factors involved in the colonisation of building façades by algae and cyanobacteria in France. 22(2), 69–77. https://doi.org/10.1080/08927010600564712
Barreiro A, Vasconcelos VM (2014) Interactions between allelopathic properties and growth kynetics in four freshwater phytoplankton species studied by model simulations. Aquat Ecol 48(2):191–205. https://doi.org/10.1007/S10452-014-9475-2
Bathurst RR, Zori D, Byock J (2010) Diatoms as bioindicators of site use: locating turf structures from the Viking Age. J Archaeol Sci 37(11):2920–2928. https://doi.org/10.1016/j.jas.2010.07.002
Bhanarkar AD, Goyal SK, Sivacoumar R, Chalapati Rao CV (2005) Assessment of contribution of SO2 and NO2 from different sources in Jamshedpur region, India. Atmos Environ 39(40):7745–7760. https://doi.org/10.1016/j.atmosenv.2005.07.070
Blacker JH, Brief RS (1972) Evaluation of the Jacobs-Hochheiser method for determining ambient nitrogen dioxide concentrations. Chemosphere 1(1):43–46. https://doi.org/10.1016/0045-6535(72)90011-2
Bosch-Roig P, Barca D, Crisci GM, Lalli C (2013) Lichens as bioindicators of atmospheric heavy metal deposition in Valencia, Spain. J Atmos Chem 70(4):373–388. https://doi.org/10.1007/s10874-013-9273-6
Brown TP, Rushton L, Mugglestone MA, Meechan DF (2003) Health effects of a sulphur dioxide air pollution episode. J Public Health Med 25(4):369–371. https://doi.org/10.1093/pubmed/fdg083
Cardon ZG, Gray DW, Lewis LA (2008) The green algal underground: evolutionary secrets of desert cells. Bioscience 58(2):114–122. https://doi.org/10.1641/B580206
Carey CC, Ibelings BW, Hoffmann EP, Hamilton DP, Brookes JD (2012) Eco-physiological adaptations that favour freshwater cyanobacteria in a changing climate. Water Res 46(5):1394–1407. https://doi.org/10.1016/J.WATRES.2011.12.016
Carvalho L, Poikane S, Lyche Solheim A, Phillips G, Borics G, Catalan J … Thackeray SJ (2013) Strength and uncertainty of phytoplankton metrics for assessing eutrophication impacts in lakes. Hydrobiologia 704(1):127–140. https://doi.org/10.1007/s10750-012-1344-1
Cichowicz R, Wielgosiński G, Fetter W (2017) Dispersion of atmospheric air pollution in summer and winter season. Environ Monit Assess 189(12). https://doi.org/10.1007/s10661-017-6319-2
Costa NB, Kolman MA, Giani A (2016) Cyanobacteria diversity in alkaline saline lakes in the Brazilian Pantanal wetland: a polyphasic approach. J Plankton Res 38(6):1389–1403. https://doi.org/10.1093/PLANKT/FBW066
Cox R (1970) Shoreline algae of Western Lake Erie. Ohio J Sci 70:257–276
Das D, Pathak A, Pal S (2018) Diversity of phytoplankton in some domestic wastewater-fed urban fish pond ecosystems of the Chota Nagpur Plateau in Bankura, India. Appl Water Sci 8:84. https://doi.org/10.1007/s13201-018-0726-6
Dere Ş, Karacaoğlu D, Dalkiran N (2002) A study on the epiphytic algae of the Nilüfer Stream (Bursa). Turk J Bot 26(4):219–233
Desikachary TV (1959) Cyanophyta, Indian Council of Agricultural Research, New Delhi, p 686
Dockery DW, Pope CA, Xu X, Spengler JD, Ware JH, Fay ME, … Speizer FE (1993) An association between air pollution and mortality in six U.S. cities. N Engl J Med 329(24):1753–1759. https://doi.org/10.1056/nejm199312093292401
Du W, Wang G (2020) Indoor air pollution was nonnegligible during COVID-19 lockdown. Aerosol Air Qual Res 20(9):1851–1855. https://doi.org/10.4209/AAQR.2020.06.0281
Falkowski PG, Katz ME, Knoll AH, Quigg A, Raven JA, Schofield, O., & Taylor, F. J. R. (2004, July 16). The evolution of modern eukaryotic phytoplankton. Science. American Association for the Advancement of Science. https://doi.org/10.1126/science.1095964
Gandhi, A. V. S. A. (2015). Studies on epiphytic microalgae in two freshwater lakes of Central Tamil Nadu. International Journal of Science and Research (IJSR), 4(4), 1095–1099. Retrieved from https://www.ijsr.net/archive/v4i4/SUB153144.pdf
Gaylarde CC, Gaylarde PM, Copp J, Neilan B (2004) Polyphasic detection of cyanobacteria in terrestrial biofilms. Biofouling 20(2):71–79. https://doi.org/10.1080/08927010410001681237
Geddam D, Simma T, Reddy-Vellala J (2020) Air pollution assessment during the festivals of Diwali and Bhogi in Visakhapatnam city. Poll Res 39:143–152
Gökçe D (2016) Algae as an indicator of water quality. In Algae - Organisms for Imminent Biotechnology. InTech. https://doi.org/10.5772/62916
Gunthe SS, Liu P, Panda U, Raj SS, Sharma A, Darbyshire E, … Coe H (2021) Enhanced aerosol particle growth sustained by high continental chlorine emission in India. Nat Geosci 14(2): 77–84. https://doi.org/10.1038/s41561-020-00677-x
Hao A, Haraguchi T, Kuba T, Kai H, Lin Y, Iseri Y (2021) Effect of the microorganism-adherent carrier for Nitzschia palea to control the cyanobacterial blooms. Ecol Eng 159:106127. https://doi.org/10.1016/j.ecoleng.2020.106127
Holzinger A, Karsten U (2013) Desiccation stress and tolerance in green algae: consequences for ultrastructure, physiological and molecular mechanisms. Front Plant Sci 0(AUG):327. https://doi.org/10.3389/FPLS.2013.00327
Iida T, Odate T (2014) Seasonal variability of phytoplankton biomass and composition in the major water masses of the Indian Ocean sector of the Southern Ocean. Polar Sci 8(3):283–297. https://doi.org/10.1016/J.POLAR.2014.03.003
India | Environmental Performance Index. (n.d.). Retrieved September 6, 2021, from https://epi.yale.edu/epi-results/2020/country/ind
Johnson JL, Fawley MW, Fawley KP (2007) The diversity of Scenedesmus and Desmodesmus (Chlorophyceae) in Itasca State Park, Minnesota, USA. Phycologia 46(2):214–229. https://doi.org/10.2216/05-69.1
Kadam AD, Kishore G, Mishra DK, Arunachalam K (2020) Microalgal diversity as an indicator of the state of the environment of water bodies of Doon valley in Western Himalaya, India. Ecol Indicat 112. https://doi.org/10.1016/j.ecolind.2020.106077
Karsten U, Lembcke S, Schumann R (2007) The effects of ultraviolet radiation on photosynthetic performance, growth and sunscreen compounds in aeroterrestrial biofilm algae isolated from building facades. Planta 225(4):991–1000
Kharkongor D, Ramanujam P (2014) Diversity and species composition of subaerial algal communities in forested areas of Meghalaya, India. International Journal of Biodiversity 2014:1–10. https://doi.org/10.1155/2014/456202
Kowalewska G, Konat J (1997) The role of phytoplankton in the transport and distribution of polynuclear aromatic hydrocarbons [PAHs] in the southern Baltic environment. Oceanologia 39:3
Kshirsagar A (2013) Use of algae as a bioindicator to determine water quality of River Mula from Pune City, Maharashtra (India). Univ J Environ Res Technol Www.Environmentaljournal.Org 3(1):79–85
Kularatne KIA, De Freitas CR (2013) Epiphytic lichens as biomonitors of airborne heavy metal pollution. Environ Exp Bot 88:24–32. https://doi.org/10.1016/j.envexpbot.2012.02.010
Lackey JB (1938) The manipulation and counting of river plankton and changes in some organisms due to formalin preservation. Public Health Rep (1896–1970) 53(47):2080. https://doi.org/10.2307/4582717
Lal S, Naja M, Subbaraya BH (2000) Seasonal variations in surface ozone and its precursors over an urban site in India. Atmos Environ 34(17):2713–2724. https://doi.org/10.1016/S1352-2310(99)00510-5
Leão PN, Vasconcelos MTSD, Vasconcelos VM (2009) Allelopathy in freshwater cyanobacteria allelopathy in freshwater cyanobacteria. Crit Rev Microbiol 35(4):271–282. https://doi.org/10.3109/10408410902823705
Lepoint G, Nyssen F, Gobert S, Dauby P, Bouquegneau JM (2000) Relative impact of a seagrass bed and its adjacent epilithic algal community in consumer diets. Mar Biol 136(3):513–518. https://doi.org/10.1007/s002270050711
Lewandowska AU, Śliwińska-Wilczewska S, Woźniczka D (2017) Identification of cyanobacteria and microalgae in aerosols of various sizes in the air over the Southern Baltic Sea ☆. https://doi.org/10.1016/j.marpolbul.2017.07.064
Lewitus AJ, Koepfler ET, Morris JT (1998) Seasonal variation in the regulation of phytoplankton by nitrogen and grazing in a salt-marsh estuary. Limnol Oceanogr 43(4):636–646. https://doi.org/10.4319/lo.1998.43.4.0636
Manisalidis I, Stavropoulou E, Stavropoulos A, Bezirtzoglou E (2020) Environmental and health impacts of air pollution: a review. Front Public Health 0:14. https://doi.org/10.3389/FPUBH.2020.00014
MaqboolGeelani S, Bhat SJA, HanifaGeelani HS (2012) Pollution indicators and their detection. J Pl Sci Res 28(2):55–59
Massimi L, Conti ME, Mele G, Ristorini M, Astolfi ML, Canepari S (2019) Lichen transplants as indicators of atmospheric element concentrations: a high spatial resolution comparison with PM 10 samples in a polluted area (Central Italy). Ecol Ind 101:759–769. https://doi.org/10.1016/j.ecolind.2018.12.051
Mayer AL, Vihermaa L, Nieminen N, Luomi A, Posch M (2009) Epiphytic macrolichen community correlates with modeled air pollutants and forest conditions. Ecol Ind 9(5):992–1000. https://doi.org/10.1016/j.ecolind.2008.11.010
Miller KG, Kominz MA, Browning JV, Wright JD, Mountain GS, Katz ME, … Pekar SF (2005) The phanerozoic record of global sea-level change. Science. American Association for the Advancement of Science. https://doi.org/10.1126/science.1116412
Muenscher WC, Prescott GW (1952) Algae of the Western Great Lakes area. J Wildl Manag. https://doi.org/10.2307/3797199
Narasimha Rao GM, Pragada PM (2010) Seasonal abundance of micro algae in Pandi backwaters of Godavari Estuary, Andhra Pradesh, India. Notulae Sci Biol 2(3):26–29. https://doi.org/10.15835/nsb234685
Palmer CM (1969) A composite rating of algae tolerating organic pollution. J Phycol 5(1):78–82. https://doi.org/10.1111/j.1529-8817.1969.tb02581.x
Pan M, Liu X, Ma W, Li X, Li H, Ding C, … Chen R (2021) The effect of hydrodynamics on the succession of autotrophic and heterotrophic organisms of biofilms in river ecosystems. Water Sci Technol 83(1):63–76. https://doi.org/10.2166/wst.2020.536
Phang S-M, Chu W-L, Rabiei R (2015) Phycoremediation (pp. 357–389). Springer, Dordrecht. https://doi.org/10.1007/978-94-017-7321-8_13
Qin B, Yang G, Ma J, Wu T, Li W, Liu L, … Zhou J (2018) Spatiotemporal changes of cyanobacterial bloom in large shallow eutrophic lake Taihu, China. Front Microbiol 9(MAR):451. https://doi.org/10.3389/fmicb.2018.00451
Raj S, RangarajanSagunthala TR (2021) Evaluation and forecasting of PM 10 air pollution in Chennai district using Wavelets, ARIMA, and Neural Networks algorithms. Pollution 7(1):55–72. https://doi.org/10.22059/poll.2020.300278.771
Razli SA, Abas A, Ismail A, Othman M, Mohtar AAA, Baharudin NH, … Latif MT (2020) Epiphytic microalgae as biological indicators for carbon monoxide concentrations in different areas of Peninsular Malaysia. Environ Forensics. https://doi.org/10.1080/15275922.2020.1850560
Rindi F (2011) Terrestrial green algae: systematics, biogeography and expected responses to climate change. Clim Chang Ecol Syst. https://doi.org/10.1017/CBO9780511974540.010
Salih FM (2011) Microalgae tolerance to high concentrations of carbon dioxide: a review. J Environ Prot 02(05):648–654. https://doi.org/10.4236/jep.2011.25074
Sankaran B, Thiruneelagandan E (2015) Microalgal diversity of Parthasarathy temple tank, Chennai, India. Int J Curr Microbiol App Sci 4(4):168–173
Seyyedneja SM, Niknejad M, Koochak H (2011) A review of some different effects of air pollution on plants. Res J Environ Sci 5(4):302–309. https://doi.org/10.3923/rjes.2011.302.309
Shams El-Din NG, Shaltout NA, Nassar MZ, Soliman A (2015) Ecological studies of epiphytic microalgae and epiphytic zooplankton on seaweeds of the Eastern Harbor, Alexandria, Egypt. Am J Environ Sci 11(6):450–473. https://doi.org/10.3844/ajessp.2015.450.473
Sharma NK, Rai AK, Singh S, Brown RM (2007) Airborne algae: their present status and relevance. J Phycol 43(4):615–627. https://doi.org/10.1111/j.1529-8817.2007.00373.x
Sharma H, Das D, Sarmah P, Rout J (2019) A study on freshwater algal communities of pond ecosystems from southern Assam. Vegetos 32(1):19–32. https://doi.org/10.1007/s42535-019-00003-w
Shubert LE (2003) Nonmotile coccoid and colonial green algae. In: Freshwater Algae of North America: Ecology and Classification. Elsevier Inc., pp 253–309. https://doi.org/10.1016/B978-012741550-5/50008-8
Singh SP, Singh P (2015) Effect of temperature and light on the growth of algae species: a review. Renew Sustain Energy Rev. https://doi.org/10.1016/j.rser.2015.05.024
Singh SS, Kunui K, Minj RA, Singh P (2014) Diversity and distribution pattern analysis of cyanobacteria isolated from paddy fields of Chhattisgarh, India. J Asia-Pac Biodivers 7(4):462–470. https://doi.org/10.1016/j.japb.2014.10.009
Smith GM (1891) A monograph of the algal genus Scenedesmus based upon pure culture studies. Wisconsin Academy of Sciences, Arts, and Letters, pp 422–530
Spengler JD, Ferris BG, Dockery DW, Speizer FE (1979) Sulfur dioxide and nitrogen dioxide levels inside and outside homes and the implications on health effects research. Environ Sci Technol 13(10):1276–1280. https://doi.org/10.1021/es60158a013
Stanca E, Parsons ML (2021) Examining the dynamic nature of epiphytic microalgae in the Florida Keys: what factors influence community composition? J Exp Mar Biol Ecol 538:151538. https://doi.org/10.1016/j.jembe.2021.151538
Suchéras-Marx B, Escarguel G, Ferreira J, Hammer Ø (2019) Statistical confidence intervals for relative abundances and abundance-based ratios: simple practical solutions for an old overlooked question. Mar Micropaleontol 151:101751. https://doi.org/10.1016/j.marmicro.2019.101751
Sun Y, Zhuang G, Wang Y, Han L, Guo J, Dan M, … Hao Z (2004) The air-borne particulate pollution in Beijing – concentration, composition, distribution and sources. Atmos Environ 38(35):5991–6004. https://doi.org/10.1016/j.atmosenv.2004.07.009
Sun Y, Zhuang G, Tang A, Wang Y, An Z (2006) Chemical characteristics of PM2.5 and PM10 in haze-fog episodes in Beijing. Environ Sci Technol 40(10):3148–3155. https://doi.org/10.1021/es051533g
Suresh B (2013) Dynamics of phytoplankton succession in Tungabhadra River near Harihar, Karnataka (India). J Microbiol Antimicrob 5(7):65–71. https://doi.org/10.5897/jma10.031
Taguchi YH, Oono Y (2005) Relational patterns of gene expression via non-metric multidimensional scaling analysis. Bioinformatics 21(6):730–740. https://doi.org/10.1093/bioinformatics/bti067
ter Braak CJF, Verdonschot PFM (1995) Canonical correspondence analysis and related multivariate methods in aquatic ecology. Aquat Sci 57(3):255–289. https://doi.org/10.1007/BF00877430
Tesson SVM, Skjøth CA, Šantl-Temkiv T, Löndahl J (2016) Airborne microalgae: insights, opportunities, and challenges. https://doi.org/10.1128/AEM.03333-15
Thakur RK, Jindal R, Singh UB, Ahluwalia AS (2013) Plankton diversity and water quality assessment of three freshwater lakes of Mandi (Himachal Pradesh, India) with special reference to planktonic indicators. Environ Monit Assess 185(10):8355–8373. https://doi.org/10.1007/s10661-013-3178-3
Trombetta T, Vidussi F, Mas S, Parin D, Simier M, Mostajir B (2019) Water temperature drives phytoplankton blooms in coastal waters. PLoS ONE 14(4):e0214933. https://doi.org/10.1371/JOURNAL.PONE.0214933
Wang H, Shen X, Liu J, Wu C, Gao J, Zhang Z, … Lu Z (2019) The effect of exposure time and concentration of airborne PM2.5 on lung injury in mice: a transcriptome analysis. Redox Biol 26(April):101264. https://doi.org/10.1016/j.redox.2019.101264
Weinmayr G, Romeo E, De Sario M, Weiland SK, Forastiere F (2010) Short-term effects of PM10 and NO2 on respiratory health among children with asthma or asthma-like symptoms: a systematic review and meta-analysis. Environ Health Perspect 118(4):449–457. https://doi.org/10.1289/ehp.0900844
West PW, Gaeke GC (1956) Fixation of sulfur dioxide as disuifitomercurate(II) and subsequent colorimetric estimation. Anal Chem 28(12):1816–1819. https://doi.org/10.1021/ac60120a005
WHO | WHO Global Urban Ambient Air Pollution Database (2018) WHO. http://www.who.int/airpollution/data/cities-2016/en/. Accessed 13 May 2021
Williamson CE, De Lange HJ, Leech DM (2007) Do zooplankton contribute to an ultraviolet clear-water phase in lakes? Limnol Oceanogr 52(2):662–667. https://doi.org/10.4319/lo.2007.52.2.0662
Wu LF, Chen PC, Huang AP, Lee CM (2012) The feasibility of biodiesel production by microalgae using industrial wastewater. Biores Technol 113:14–18. https://doi.org/10.1016/j.biortech.2011.12.128
XaaldiKalhor A, Movafeghi A, Mohammadi-Nassab AD, Abedi E, Bahrami A (2017) Potential of the green alga Chlorella vulgaris for biodegradation of crude oil hydrocarbons. Mar Pollut Bull 123(1–2):286–290. https://doi.org/10.1016/j.marpolbul.2017.08.045
Zhao H, Ma Y, Wang Y, Wang H, Sheng Z, Gui K, … Che H (2019) Aerosol and gaseous pollutant characteristics during the heating season (winter–spring transition) in the Harbin–Changchun megalopolis, northeastern China. J Atmos Solar-Terrestrial Phys 188:26–43. https://doi.org/10.1016/j.jastp.2019.03.001
Zhu X, Liu Y, Chen Y, Yao C, Che Z, Cao J (2015) Maternal exposure to fine particulate matter (PM2.5) and pregnancy outcomes: a meta-analysis. Environ Sci Pollut Res 22(5):3383–3396. https://doi.org/10.1007/s11356-014-3458-7
Acknowledgements
The authors thank the Ministry of Environment, Forests and Climate change, Govt. of India for financial assistance through the All India Coordinated Project on Taxonomy (AICOPTAX) of freshwater planktonic algae, No. J. 22018/20/2016-CSC (TAX). The authors would like to thank the Tamil Nadu Pollution Control Board for their support on data collection. We thank The Director, Centre for Advanced Studies in Botany, University of Madras, for providing laboratory facilities.
Funding
Ministry of Environment, Forests and Climate Change, Govt. of India for financial assistance through the All India Coordinated Project on Taxonomy (AICOPTAX) of freshwater planktonic algae, No. J. 22018/20/2016-CSC (TAX).
Author information
Authors and Affiliations
Contributions
N.S. contributed towards the experimental planning, taxonomical identification and execution of this research work. S.J.P.J. contributed towards field experiments and data collection. S.K.G. contributed towards the statistical analysis and manuscript correction. G.G. and S.K.B. contributed towards the collection of microalgal samples, enumeration and cultivation.
Corresponding author
Ethics declarations
Ethics approval and consent to participate
Not applicable.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Additional information
Responsible editor: Diane Purchase
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Joseph, S.J.P., Gopidas, S.K., Gnanam, G. et al. Epiphytic phytoplankton in response to divergent air pollutants from urban and commercial zones of Chennai District, Tamil Nadu, India: A case study towards phytoplankton based Air Quality Index. Environ Sci Pollut Res 29, 15098–15116 (2022). https://doi.org/10.1007/s11356-021-16815-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-021-16815-w