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Influence of heavy metals on the occurrence of Antarctic soil microalgae

Published online by Cambridge University Press:  13 September 2021

Nguk-Ling Dang Open the ORCID record for Nguk-Ling Dang [Opens in a new window] ,
Wan-Loy Chu ,
Kok-Seng Ivan Yap ,
Yih-Yih Kok ,
Siew-Moi Phang ,
Kok-Keong Chan  and
Peter Convey Open the ORCID record for Peter Convey [Opens in a new window]
Nguk-Ling Dang*
Affiliation:
School of Postgraduate Studies, Institute for Research, Development and Innovation (IRDI), International Medical University, Bukit Jalil, 57000 Kuala Lumpur, Malaysia
Wan-Loy Chu
Affiliation:
School of Postgraduate Studies, Institute for Research, Development and Innovation (IRDI), International Medical University, Bukit Jalil, 57000 Kuala Lumpur, Malaysia National Antarctic Research Centre, University of Malaya, 50603 Kuala Lumpur, Malaysia
Kok-Seng Ivan Yap
Affiliation:
Sarawak Research and Development Council, 11th Floor LCDA Tower, The Isthmus, Off Jalan Bako, 93050 Kuching, Sarawak, Malaysia
Yih-Yih Kok
Affiliation:
Division of Applied Biomedical Sciences and Biotechnology, International Medical University, Bukit Jalil, 57000 Kuala Lumpur, Malaysia
Siew-Moi Phang
Affiliation:
Institute of Ocean and Earth Sciences, University of Malaya, 50603 Kuala Lumpur, Malaysia Faculty of Applied Sciences, UCSI University, Cheras, 56000 Kuala Lumpur, Malaysia
Kok-Keong Chan
Affiliation:
Division of Human Biology, International Medical University, Bukit Jalil, 57000 Kuala Lumpur, Malaysia
Peter Convey
Affiliation:
British Antarctic Survey, NERC, High Cross, Madingley Road, Cambridge CB3 0ET, UK Department of Zoology, University of Johannesburg, PO Box 524, Auckland Park 2006, South Africa
*
[email protected]
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Abstract

Human- and animal-impacted sites in Antarctica can be contaminated with heavy metals, as well as areas influenced by underlying geology and naturally occurring minerals. The present study examined the relationship between heavy metal presence and soil microalgal occurrence across a range of human-impacted and undisturbed locations on Signy Island. Microalgae were identified based on cultures that developed after inoculation into an enriched medium. Twenty-nine microalgae representing Cyanobacteria, Bacillariophyta, Chlorophyta and Tribophyta were identified. High levels of As, Ca, Cd, Cu and Zn were detected in Gourlay Peninsula and North Point, both locations hosting dense penguin rookeries. Samples from Berntsen Point, the location of most intense human activity both today and historically, contained high levels of Pb. The contamination factor and pollution load index confirmed that the former locations were polluted by Cd, Cu and Zn, with these being of marine biogenic origin. Variation in the microalgal community was significantly correlated with concentrations of Mn, Ca, Mg, Fe, Zn, Cd, Co, Cr and Cu. However, the overall proportion of the total variation contributed by all metals was low (16.11%). Other factors not measured in this study are likely to underlie the majority of the observed variation in microalgal community composition between sampling locations.

Keywords

animal impactscontaminationhuman impactsICP-MSpollutantsterrestrial environment
Type
Earth Sciences
Information
Antarctic Science , Volume 33 , Issue 6 , December 2021 , pp. 645 - 659
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Copyright
Copyright © Antarctic Science Ltd 2021

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References

Afkar, E., Ababna, H. & Fathi, A. 2010. Toxicological response of the green alga Chlorella vulgaris, to some heavy metals. American Journal of Environmental Sciences, 6, 230.CrossRefGoogle Scholar
Anderson, M.J., Gorley, R.N. & Clarke, K.S. 2008. PERMANOVA+ for PRIMER: guide to software and statistical methods. Plymouth: PRIMER-e, 214 pp.Google Scholar
Andrade, S., Poblet, A., Scagliola, M., Vodopivez, C., Curtosi, A., Pucci, A. & Marcovecchio, J. 2001. Distribution of heavy metals in surface sediments from an Antarctic marine ecosystem. Environmental Monitoring and Assessment, 66, 147–158.CrossRefGoogle ScholarPubMed
Arnold, R., Convey, P., Hughes, K. & Wynn-Williams, D. 2003. Seasonal periodicity of physical factors, inorganic nutrients and microalgae in Antarctic fellfields. Polar Biology, 26, 396–403.CrossRefGoogle Scholar
Beattie, R.E., Henke, W., Campa, M.F., Hazen, T.C., McAliley, L.R. & Campbell, J.H. 2018. Variation in microbial community structure correlates with heavy-metal contamination in soils decades after mining ceased. Soil Biology and Biochemistry, 126, 57–63.CrossRefGoogle Scholar
Bhuiyan, M.A., Parvez, L., Islam, M., Dampare, S.B. & Suzuki, S. 2010. Heavy metal pollution of coal mine-affected agricultural soils in the northern part of Bangladesh. Journal of Hazardous Materials, 173, 384–392.CrossRefGoogle ScholarPubMed
Bockheim, J.G. 2015. The soils of Antarctica. New York: Springer International Publishing, 322 pp.CrossRefGoogle Scholar
Broady, P.A. 1976. Six new species of terrestrial algae from Signy Island, South Orkney Islands, Antarctica. British Phycological Journal, 11, 387–405.CrossRefGoogle Scholar
Broady, P.A. 1979. The terrestrial algae of Signy Island, South Orkney Islands. BAS Scientific Reports, 98, 1–117.Google Scholar
Broady, P.A. 1996. Diversity, distribution and dispersal of Antarctic terrestrial algae. Biodiversity & Conservation, 5, 1307–1335.CrossRefGoogle Scholar
Broady, P.A. 2005. The distribution of terrestrial and hydro-terrestrial algal associations at three contrasting locations in southern Victoria Land, Antarctica. Algological Studies, 118, 95–112.Google Scholar
Broady, P.A. & Ingerfeld, M. 1993. Three new species and a new record of Chaetophoracean (Chlorophyta) algae from terrestrial habitats in Antarctica. European Journal of Phycology, 28, 25–31.CrossRefGoogle Scholar
Broady, P., Garrick, R. & Anderson, G. 1984. Culture studies on the morphology of ten strains of Antarctic Oscillatoriaceae (Cyanobacteria). Polar Biology, 2, 233–244.CrossRefGoogle Scholar
Brooks, S.T., Jabour, J., Van Den Hoff, J. & Bergstrom, D.M. 2019. Our footprint on Antarctica competes with nature for rare ice-free land. Nature Sustainability, 2, 185–190.CrossRefGoogle Scholar
Cabrita, M.T., Padeiro, A., Amaro, E., dos Santos, M.C., Leppe, M., Verkulich, S., et al. 2017. Evaluating trace element bioavailability and potential transfer into marine food chains using immobilised diatom model species Phaeodactylum tricornutum, on King George Island, Antarctica. Marine Pollution Bulletin, 121, 192–200.CrossRefGoogle Scholar
Cavet, J.S., Borrelly, G.P. & Robinson, N.J. 2003. Zn, Cu and Co in cyanobacteria: selective control of metal availability. FEMS Microbiology Reviews, 27, 165–181.CrossRefGoogle Scholar
Chen, J., He, F., Zhang, X., Sun, X., Zheng, J. & Zheng, J. 2014. Heavy metal pollution decreases microbial abundance, diversity and activity within particle-size fractions of a paddy soil. FEMS Microbiology Ecology, 87, 164–181.CrossRefGoogle ScholarPubMed
Chong, C.W., Dunn, M.J., Convey, P., Tan, G.A., Wong, R.C. & Tan, I.K. 2009. Environmental influences on bacterial diversity of soils on Signy Island, Maritime Antarctic. Polar Biology, 32, 1571–1582.CrossRefGoogle Scholar
Chong, C.W., Pearce, D.A., Convey, P., Tan, G.A., Wong, R.C. & Tan, I.K. 2010. High levels of spatial heterogeneity in the biodiversity of soil prokaryotes on Signy Island, Antarctica. Soil Biology and Biochemistry, 42, 601–610.CrossRefGoogle Scholar
Chu, W.-L., Dang, N.-L., Kok, Y.-Y., Yap, K.-S.I., Phang, S.-M. & Convey, P. 2019a. Heavy metal pollution in Antarctica and its potential impacts on algae. Polar Science, 20, 75–83.CrossRefGoogle Scholar
Chu, Z., Yang, Z., Wang, Y., Sun, L., Yang, W., Yang, L. & Gao, Y. 2019b. Assessment of heavy metal contamination from penguins and anthropogenic activities on Fildes Peninsula and Ardley Island, Antarctic. Science of the Total Environment, 646, 951–957.CrossRefGoogle Scholar
Claridge, G.G.C., Campbell, I.B., Powell, H.K.J., Amin, Z.H. & Balks, M.R. 1995. Heavy metal contamination in some soils of the McMurdo Sound region, Antarctica. Antarctic Science, 7, 9–14.CrossRefGoogle Scholar
Clarke, K. & Gorley, R. 2015. Getting started with PRIMER v7. Plymouth: PRIMER-e, 20 pp.Google Scholar
Clarke, K.R. & Warwick, R.M. 2001. Change in marine communities: an approach to statistical analysis and interpretation. Plymouth: PRIMER-e, 176 pp.Google Scholar
Clemens, S. 2006. Evolution and function of phytochelatin synthases. Journal of Plant Physiology, 163, 319–332.CrossRefGoogle ScholarPubMed
Convey, P. 2020. The price of cumulative human activities in the Antarctic. Antarctic Science, 32, 425.CrossRefGoogle Scholar
Convey, P. & Lebouvier, M. 2009. Environmental change and human impacts on terrestrial ecosystems of the sub-Antarctic islands between their discovery and the mid-twentieth century. Papers and Proceedings of the Royal Society of Tasmania, 143, 33–44.CrossRefGoogle Scholar
Convey, P., Coulson, S., Worland, M. & Sjöblom, A. 2018. The importance of understanding annual and shorter-term temperature patterns and variation in the surface levels of polar soils for terrestrial biota. Polar Biology, 41, 1587–1605.CrossRefGoogle Scholar
Convey, P., Chown, S.L., Clarke, A., Barnes, D.K., Bokhorst, S., Cummings, V., et al. 2014. The spatial structure of Antarctic biodiversity. Ecological Monographs, 84, 203–244.CrossRefGoogle Scholar
Davey, M.C. 1991. The seasonal periodicity of algae on Antarctic fellfield soils. Ecography, 14, 112–120.CrossRefGoogle Scholar
Davey, M. & Clarke, K. 1991. The spatial distribution of microalgae on Antarctic fellfield soils. Antarctic Science, 3, 257–263.CrossRefGoogle Scholar
Davey, M.C. & Rothery, P. 1993. Primary colonization by microalgae in relation to spatial variation in edaphic factors on Antarctic fellfield soils. Journal of Ecology, 8, 335–343.CrossRefGoogle Scholar
de Lima Neto, E., Guerra, M.B.B., Thomazini, A., Daher, M., de Andrade, A.M. & Schaefer, C.E.G.R. 2017. Soil contamination by toxic metals near an Antarctic refuge in Robert Island, Maritime Antarctica: a monitoring strategy. Water, Air, & Soil Pollution, 228, 66.CrossRefGoogle Scholar
Espejo, W., Celis, J.E., González-Acuña, D., Jara, S. & Barra, R. 2014. Concentration of trace metals in excrements of two species of penguins from different locations of the Antarctic Peninsula. Polar Biology, 37, 675–683.CrossRefGoogle Scholar
Gillan, D.C., Danis, B., Pernet, P., Joly, G. & Dubois, P. 2005. Structure of sediment-associated microbial communities along a heavy-metal contamination gradient in the marine environment. Applied and Environmental Microbiology, 71, 679–690.CrossRefGoogle ScholarPubMed
Gilpin, L.C., Davidson, K. & Roberts, E. 2004. The influence of changes in nitrogen: silicon ratios on diatom growth dynamics. Journal of Sea Research, 51, 21–35.CrossRefGoogle Scholar
Gourmelon, V., Maggia, L., Powell, J.R., Gigante, S., Hortal, S., Gueunier, C., et al. 2016. Environmental and geographical factors structure soil microbial diversity in New Caledonian ultramafic substrates: a metagenomic approach. PLoS One, 11, e0167405.CrossRefGoogle ScholarPubMed
Harikumar, P. & Jisha, T. 2010. Distribution pattern of trace metal pollutants in the sediments of an urban wetland in the southwest coast of India. International Journal of Engineering Science and Technology 2, 840–850.Google Scholar
Hawes, I. 1983. Nutrients and their effects on phytoplankton populations in lakes on Signy Island, Antarctica. Polar Biology, 2, 115–126.CrossRefGoogle Scholar
Holdgate, M., Allen, S. & Chambers, M. 1967. A preliminary investigation of the soils of Signy Island, South Orkney Islands. BAS Bulletin, No. 12, 53–71.Google Scholar
Hughes, K.A. & Convey, P. 2020. Implications of the COVID-19 pandemic for Antarctica. Antarctic Science, 32, 426–439.CrossRefGoogle Scholar
Johansson, P. & Thor, G. 2008. Lichen species density and abundance over ten years in permanent plots in inland Dronning Maud Land, Antarctica. Antarctic Science, 20, 115–121.CrossRefGoogle Scholar
Kennedy, A.D. 1993. Water as a limiting factor in the Antarctic terrestrial environment: a biogeographical synthesis. Arctic and Alpine Research, 25, 308–315.CrossRefGoogle Scholar
Laundon, J.R. 1985. Desmococcus olivaceus – the name of the common subaerial green alga. Taxon, 34, 671–672.CrossRefGoogle Scholar
Li, F., Huang, J., Zeng, G., Yuan, X., Li, X., Liang, J., et al. 2013. Spatial risk assessment and sources identification of heavy metals in surface sediments from the Dongting Lake, Middle China. Journal of Geochemical Exploration, 132, 75–83.CrossRefGoogle Scholar
Lone, S.A., Hamid, A. & Bhat, S.U. 2021. Algal community dynamics and underlying driving factors in some crenic habitats of Kashmir Himalaya. Water, Air, & Soil Pollution, 232, 104.CrossRefGoogle Scholar
Mataloni, G., Tell, G. & Wynn-Williams, D. 2000. Structure and diversity of soil algal communities from Cierva Point (Antarctic Peninsula). Polar Biology, 23, 205–211.CrossRefGoogle Scholar
Naveen, R. 1996. Human activity and disturbance: building an Antarctic site inventory. Foundations for Ecological Research West of the Antarctic Peninsula, 70, 389–400.CrossRefGoogle Scholar
Ohtani, S., Suyama, K., Yamamoto, H., Aridomi, Y., Itohm, R. & Fukuoka, Y. 2000. Distribution of soil algae at the monitoring sites in the vicinity of Syowa Station between austral summers of 1992/1993 and 1997/1998. Polar Bioscience, 13, 113–132.Google Scholar
Rahmonov, O., Cabala, J., Bednarek, R., Rozek, D. & Florkiewicz, A. 2015. Role of soil algae on the initial stages of soil formation in sandy polluted areas. Ecological Chemistry and Engineering S, 22, 675–690.CrossRefGoogle Scholar
Renuka, N., Sood, A., Prasanna, R. & Ahluwalia, A.S. 2014. Influence of seasonal variation in water quality on the microalgal diversity of sewage wastewater. South African Journal of Botany, 90, 137–145.CrossRefGoogle Scholar
de la Rocha, Ródenas, Sánchez-Muniz, S., Gómez-Juaristi, F.J., & Marín, M., M.T.L. 2009. Trace elements determination in edible seaweeds by an optimized and validated ICP-MS method. Journal of Food Composition and Analysis, 22, 330–336.CrossRefGoogle Scholar
Sabbe, K., Verleyen, E., Hodgson, D., Vanhoutte, K. & Vyverman, W. 2003. Benthic diatom flora of freshwater and saline lakes in the Larsemann Hills and Rauer Islands, East Antarctica. Antarctic Science, 15, 227–248.CrossRefGoogle Scholar
Santamans, A.C., Boluda, R., Picazo, A., Gil, C., Ramos-Miras, J., Tejedo, P., et al. 2017. Soil features in rookeries of Antarctic penguins reveal sea to land biotransport of chemical pollutants. PLoS One, 12, e0181901.CrossRefGoogle ScholarPubMed
Santos, I.R., Silva-Filho, E.V., Schaefer, C.E., Albuquerque-Filho, M.R. & Campos, L.S. 2005. Heavy metal contamination in coastal sediments and soils near the Brazilian Antarctic Station, King George Island. Marine Pollution Bulletin, 50, 185–194.CrossRefGoogle ScholarPubMed
Snape, I., Scouller, R., Stark, S., Stark, J., Riddle, M. & Gore, D. 2004. Characterisation of the dilute HCl extraction method for the identification of metal contamination in Antarctic marine sediments. Chemosphere, 57, 491–504.CrossRefGoogle ScholarPubMed
Stark, J.S., Riddle, M.J., Snape, I. & Scouller, R.C. 2003. Human impacts in Antartic marine soft-sediment assemblages: correlations between multivariate biological patterns and environmental variables at Casey Station. Estuarine, Coastal and Shelf Science, 56, 717–734.CrossRefGoogle Scholar
Sun, W., Skidmore, A.K., Wang, T. & Zhang, X. 2019. Heavy metal pollution at mine sites estimated from reflectance spectroscopy following correction for skewed data. Environmental Pollution, 252, 1117–1124.CrossRefGoogle ScholarPubMed
Tin, T., Fleming, Z.L., Hughes, K.A., Ainley, D., Convey, P., Moreno, C., et al. 2009. Impacts of local human activities on the Antarctic environment. Antarctic Science, 21, 3–33.CrossRefGoogle Scholar
Tomlinson, D., Wilson, J., Harris, C. & Jeffrey, D. 1980. Problems in the assessment of heavy-metal levels in estuaries and the formation of a pollution index. Helgoländer Meeresuntersuchungen, 33, 566–575.CrossRefGoogle Scholar
Van de Vijver, B. 2008. Pinnularia obaesa sp. nov. and P. australorabenhorstii sp. nov., two new large Pinnularia (sect. Distantes) from the Antarctic King George Island (South Shetland Islands). Diatom Research, 23, 221–232.CrossRefGoogle Scholar
Velichko, N., Smirnova, S., Averina, S. & Pinevich, A. 2021. A survey of Antarctic cyanobacteria. Hydrobiologia, 848, 2627–2652.CrossRefGoogle Scholar
Vodopivez, C., Curtosi, A., Villaamil, E., Smichowski, P., Pelletier, E. & Mac Cormack, W.P. 2015. Heavy metals in sediments and soft tissues of the Antarctic clam Laternula elliptica: more evidence as a possible biomonitor of coastal marine pollution at high latitudes? Science of the Total Environment, 502, 375–384.CrossRefGoogle ScholarPubMed
Wuana, R.A. & Okieimen, F.E. 2011. Heavy metals in contaminated soils: a review of sources, chemistry, risks and best available strategies for remediation. ISRN Ecology, 2011, 1–20.CrossRefGoogle Scholar
Wynn-Williams, D. 1996. Antarctic microbial diversity: the basis of polar ecosystem processes. Biodiversity & Conservation, 5, 1271–1293.CrossRefGoogle Scholar
Wynn-Williams, D.D. 1990. Microbial colonization processes in Antarctic fellfield soils - an experimental overview. Proceedings of the NIPR Symposium on Polar Biology, 3, 164–178.Google Scholar
Zhao, Y. & Xu, C. 2000. Human impacts on the terrestrial ecosystem of Fildes Peninsula of King George Island, Antarctica. Journal of Environmental Sciences, 12, 12–17.Google Scholar
Zidarova, R., Kopalová, K. & Van de Vijver, B. 2016. Ten new Bacillariophyta species from James Ross Island and the South Shetland Islands (Maritime Antarctic Region). Phytotaxa, 272, 37–62.CrossRefGoogle Scholar
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