Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-22T13:30:53.509Z Has data issue: false hasContentIssue false

Importation of psychrotolerant fungi to Antarctica associated with wooden cargo packaging

Published online by Cambridge University Press:  05 October 2018

Kevin A. Hughes*
Affiliation:
British Antarctic Survey, NERC, High Cross, Madingley Road, Cambridge CB3 0ET, UK
Marta Misiak
Affiliation:
British Antarctic Survey, NERC, High Cross, Madingley Road, Cambridge CB3 0ET, UK
Yogabaanu Ulaganathan
Affiliation:
National Antarctic Research Centre, University of Malaya, 50603 Lembah Pantai, Kuala Lumpur, Malaysia
Kevin K. Newsham
Affiliation:
British Antarctic Survey, NERC, High Cross, Madingley Road, Cambridge CB3 0ET, UK

Abstract

The harsh climatic conditions and low levels of human activity in Antarctica, relative to other regions, means few non-native species have established. However, the risk of introductions is becoming greater as human activity increases. Non-native microorganisms can be imported to Antarctica in association with fresh food, cargo and personal clothing, but the likelihood of their establishment is not well understood. In January 2015, a wooden packing crate, heavily contaminated with fungi, was imported by aircraft from Punta Arenas, Chile, to Rothera Research Station, Antarctica. Mucor racemosus Bull. and two strains of Trichoderma viridescens (A.S. Horne & H.S. Will.) Jaklitsch & Samuels were isolated from the wood. Measurements of hyphal extension rates indicated that all three strains were psychrotolerant and capable of growth at 4°C, with M. racemosus growing at 0°C. The imported fungi could grow at rates equivalent to, or faster than, species isolated from Antarctic soils, suggesting that low temperature may not be a limiting factor for establishment. It is recommended that wood heat-treatment standards, equivalent to those described in the International Standards for Phytosanitary Measures No. 15, are employed by national operators importing cargo into Antarctica, and that treated wood is adequately stored to prevent fungal contamination prior to transportation.

Type
Biological Sciences
Copyright
© Antarctic Science Ltd 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Arnold, R.J., Convey, P., Hughes, K.A. & Wynn-Williams, D.D. 2003. Seasonal periodicity of physical factors, inorganic nutrients and microalgae in Antarctic fellfields. Polar Biology, 26, 10.1007/s00300-003-0503-2.Google Scholar
Augustyniuk-Kram, A., Chwedorzewska, K.J., Korczak-Abshire, M., Olech, M. & Lityńska-Zając, M. 2013. An analysis of fungal propagules transported to the Henryk Arctowski Station. Polish Polar Research, 34, 10.2478/popore−2013−0015.Google Scholar
Błaszczyk, L., Strakowska, J., Chełkowski, J., Gąbka-Buszek, A. & Kaczmarek, J. 2016. Trichoderma species occurring on wood with decay symptoms in mountain forests in Central Europe: genetic and enzymatic characterization. Journal of Applied Genetics, 57, 10.1007/s13353-015-0326-1.Google Scholar
Bölter, M., Kandeler, E., Pietr, S.J. & Seppelt, R.D. 2002. Heterotrophic microbes, microbial and enzymatic activity in Antarctic soils. In Beyer, L. & Bölter, M., eds. Geoecology of Antarctic ice-free coastal landscapes. Berlin: Springer, 189214.Google Scholar
Bradner, J.R., Sidhu, R.K., Yee, B., Skotnicki, M.L., Selkirk, P.M. & Nevalainen, K.M.H. 2000. A new microfungal isolate, Embellisia sp., associated with the Antarctic moss Bryum argentum . Polar Biology, 23, 10.1007/s003000000161.Google Scholar
Bridge, P.D. & Hughes, K.A. 2010. Conservation issues for Antarctic fungi. Mycologia Balcanica, 7, 1114.Google Scholar
Broady, P. & Smith, R. 1994. A preliminary investigation of the diversity, survivability and dispersal of algae introduced into Antarctica by human activity. Proceedings of the NIPR Symposium on Polar Biology, 7, 185197.Google Scholar
Chown, S.L., Huiskes, A.H.L., Gremmen, N.J.M. et al. 2012. Continent-wide risk assessment for the establishment of nonindigenous species in Antarctica. Proceeds of the National Academy of Sciences USA, 109, 10.1073/pnas.1119787109.Google Scholar
Chwedorzewska, K.J., Korczak-Abshire, M., Olech, M., Lityńska-Zając, M. & Augustyniuk−Kram, A. 2013. Alien invertebrates transported accidentally to the Polish Antarctic Station in cargo and on fresh foods. Polish Polar Research, 34, 5566.Google Scholar
COMNAP & SCAR 2010. Checklists for supply chain managers of national Antarctic programmes for the reduction in risk of transfer of non-native species. Available at https://www.comnap.aq/SitePages/checklists.aspx.Google Scholar
Convey, P., Hughes, K.A. & Tin, T. 2012. Continental governance and environmental management mechanisms under the Antarctic Treaty System: sufficient for the biodiversity challenges of this century? Biodiversity, 13, 10.1080/14888386.2012.703551.Google Scholar
Corte, A. & Daglio, C.A.N. 1964. A mycological study of the Antarctic air. In Carrick, R., Holdgate, M.W. & Prevost, J., eds. Biologie Antarctique. Paris: Hermann, 115120.Google Scholar
Cowan, D. A. & Ah Tow, L. 2004. Endangered Antarctic environments. Annual Reviews in Microbiology, 58, 10.1146/annurev.micro.57.030502.090811.Google Scholar
Cowan, D.A., Chown, S.L., Convey, P., Tuffin, M., Hughes, K.A., Pointings, S. & Vincent, W.F. 2011. Non-indigenous microorganisms in the Antarctic: assessing the risks. Trends in Microbiology, 19, 10.1016/j.tim.2011.07.008.Google Scholar
Davey, M.C., Pickup, J. & Block, W. 1992. Temperature variation and its biological significance in fellfield habitats on a maritime Antarctic island. Antarctic Science, 4, 10.1017/S0954102092000567.Google Scholar
De Wever, A., Leliaert, F., Verleyen, E., Vanormelingen, P., Van Der Gucht, K., Hodgson, D.A., Sabbe, K. & Vyverman, W. 2009. Hidden levels of phylodiversity in Antarctic green algae: further evidence for the existence of glacial refugia. Proceedings of the Royal Society B – Biological Sciences, 276, 10.1098/rspb.2009.0994.Google Scholar
Eida, M.F., Nagaoka, T., Wasaki, J. & Kouno, K. 2011. Evaluation of cellulolytic and hemicellulolytic abilities of fungi isolated from coffee residue and sawdust composts. Microbes and Environments, 26, 10.1264/jsme2.ME10210.Google Scholar
Farrell, R.L., Arenz, B.E., Duncan, S.M., Held, B.W., Jurgens, J.A. & Blanchette, R.A. 2011. Introduced and indigenous fungi of the Ross Island historic huts and pristine areas of Antarctica. Polar Biology, 34, 10.1007/s00300-011-1060-8.Google Scholar
Fletcher, L.D., Kerry, E.J. & Weste, G.M. 1985. Microfungi of Mac.Robertson and Enderby Lands, Antarctica. Polar Biology, 4, 10.1007/BF00442904.Google Scholar
Frenot, Y., Chown, S.L., Whinam, J., Selkirk, P., Convey, P., Skotnicki, M. & Bergstrom, D. 2005. Biological invasions in the Antarctic: extent, impacts and implications. Biological Reviews, 80, 10.1017/S1464793104006542.Google Scholar
Gardes, M. & Bruns, T.D. 1993. ITS primers with enhanced specificity for basidiomycetes – application to the identification of mycorrhizae and rusts. Molecular Ecology, 2, 10.1111/j.1365-294X.1993.tb00005.x.Google Scholar
Held, B.W. & Blanchette, R.A. 2017. Deception Island, Antarctica, harbors a diverse assemblage of wood decay fungi. Fungal Biology, 12, 10.1016/j.funbio.2016.11.009.Google Scholar
Hughes, K.A. & Convey, P. 2010. The protection of Antarctic terrestrial ecosystems from inter- and intra-continental transfer of non-indigenous species by human activities: a review of current systems and practices. Global Environmental Change, 20, 10.1016/j.gloenvcha.2009.09.005.Google Scholar
Hughes, K.A. & Convey, P. 2012. Determining the native/non-native status of newly discovered terrestrial and freshwater species in Antarctica – current knowledge, methodology and management action. Journal of Environmental Management, 93, 10.1016/j.jenvman.2011.08.017.Google Scholar
Hughes, K.A., Bridge, P. & Clark, M.S. 2007. Tolerance of Antarctic soil fungi to hydrocarbons. Science of the Total Environment, 372, 10.1016/j.scitotenv.2006.09.016.Google Scholar
Hughes, K.A., Cowan, D.A. & Wilmotte, A. 2015a. Protection of Antarctic microbial communities – ‘out of sight, out of mind’. Frontiers in Microbiology, 10.3389/fmicb.2015.00151.Google Scholar
Hughes, K.A., Lawley, B. & Newsham, K.K. 2003. Solar UV-B radiation inhibits the growth of Antarctic terrestrial fungi. Applied and Environmental Microbiology, 69, 10.1128/AEM.69.3.1488-1491.200.Google Scholar
Hughes, K.A., Convey, P., Maslen, N.R. & Smith, R.I.L. 2010a. Accidental transfer of non-native soil organisms into Antarctica on construction vehicles. Biological Invasions, 12, 10.1007/s10530-009-9508-2.Google Scholar
Hughes, K.A., Pertierra, L.R., Molina-Montenegro, M. & Convey, P. 2015b. Biological invasions in terrestrial Antarctica: what is the current status and can we respond? Biodiversity and Conservation, 24, 10.1007/s10531-015-0896-6.Google Scholar
Hughes, K.A., Fretwell, P., Rae, J., Holmes, K. & Fleming, A. 2011a. Untouched Antarctica: mapping a finite and diminishing environmental resource. Antarctic Science, 23, 10.1017/S095410201100037X.Google Scholar
Hughes, K.A., Lee, J.E., Ware, C., Kiefer, K. & Bergstrom, D.M. 2010b. Impact of anthropogenic transportation to Antarctica on alien seed viability. Polar Biology, 33, 10.1007/s00300-010-0801-4.Google Scholar
Hughes, K.A., Lee, J.E., Tsujimoto, M. et al. 2011b. Food for thought: risks of non-native species transfer to the Antarctic region with fresh produce. Biological Conservation, 144, 10.1016/j.biocon.2011.03.001.Google Scholar
Huiskes, A.H.L., Gremmen, N.J.M., Bergstrom, D.M. et al. 2014. Aliens in Antarctica: assessing transfer of plant propagules by human visitors to reduce invasion risk. Biological Conservation, 171, 10.1016/j.biocon.2014.01.038.Google Scholar
Hurst, J.L., Pugh, G.J.F. & Walton, D.W.H. 1983. Fungal succession and substrate utilisation on the leaves of three South Georgia phanerograms. BAS Bulletin, No. 58. 89100.Google Scholar
Kerry, E. 1984. The fungal flora of Macquarie Island. Tasmanian Naturalist, 78, 1621.Google Scholar
Kerry, E. 1990a. Microorganisms colonizing plants and soil subjected to different degrees of human activity, including petroleum contamination, in the Vestfold Hills and MacRobertson Land, Antarctica. Polar Biology, 10, 10.1007/BF00233690.Google Scholar
Kerry, E. 1990b. Effects of temperature on growth rates of fungi from subantarctic Macquarie Island and Casey, Antarctica. Polar Biology, 10, 10.1007/BF00238428.Google Scholar
Kloppers, F.J. & Smith, V.R. 1998. First report of Botryotinia fuckeliana on Kerguelen cabbage on the sub-Antarctic Marion Island. Plant Disease, 82, 10.1094/PDIS.1998.82.6.710A.Google Scholar
Kochkina, G., Ivanushkina, N., Ozerskaya, S., Chigineva, N., Vasilenko, O., Firsov, S., Spirina, E. & Gilichinsky, D. 2012. Ancient fungi in Antarctic permafrost environments. FEMS Microbiology Ecology, 82, 10.1111/j.1574-6941.2012.01442.x.Google Scholar
Lawley, B., Ripley, S., Bridge, P. & Convey, P. 2004. Molecular analysis of geographic patterns of eukaryotic diversity in Antarctic soils. Applied and Environmental Microbiology, 70, 10.1128/AEM.70.10.5963-5972.2004.Google Scholar
Laws, R.M. 1984. Antarctic ecology. London: Academic Press, 858 pp.Google Scholar
Lee, J.E. & Chown, S.L. 2009. Breaching the dispersal barrier to invasion: quantification and management. Ecological Applications, 19, 10.1890/08-2157.1.Google Scholar
Line, M.A. 1988. Microbial flora of some soils of Mawson Base and the Vestfold Hills, Antarctica. Polar Biology, 8, 10.1007/BF00264718.Google Scholar
Litynska-Zając, M., Chwedorzewska, K., Olech, M., Korczak-Abshire, M. & Augustyniuk-Kram, A. 2012. Diaspores and phyto-remains accidentally transported to the Antarctic Station during three expeditions. Biodiversity and Conservation, 21, 10.1007/s10531-012-0371-6.Google Scholar
Marshall, W.A. 1998. Aerial transport of keratinaceous substrate and distribution of the fungus Geomyces pannorum in Antarctic soils. Microbial Ecology, 36, 10.1007/s002489900108.Google Scholar
McRae, C.F. & Seppelt, R.D. 1999. Filamentous fungi of the Windmill Islands, continental Antarctica: effect of water content in moss turves on fungal diversity. Polar Biology, 22, 10.1007/s003000050434.Google Scholar
Osyczka, P. 2010. Alien lichens unintentionally transported to the Arctowski Station (South Shetlands, Antarctica). Polar Biology, 33, 10.1007/s00300-010-0786-z.Google Scholar
Osyczka, P., Mleczko, P., Karasinski, D. & Chlebicki, A. 2012. Timber transported to Antarctica: a potential and undesirable carrier for alien fungi and insects. Biological Invasions, 14, 10.1007/s10530-011-9991-0.Google Scholar
Rajala, T., Peltoniemi, M., Hantula, J., Mäkipää, R. & Pennanen, T. 2011. RNA reveals a succession of active fungi during the decay of Norway spruce logs. Fungal Ecology, 4, 10.1016/j.funeco.2011.05.005.Google Scholar
Ruisi, S., Barreca, D., Selbmann, L., Zucconi, L. & Onofri, S. 2007. Fungi in Antarctica. Reviews in Environmental Science and Biotechnology, 6, 10.1007/s11157-006-9107-y.Google Scholar
Saili, N.S., Siddiquee, S., Vui Ling, C.M.W., González, M. & Vijay Kumar, S. 2014. Lignocellulolytic activities among Trichoderma isolates from Lahad Datu, Sabah and Deception Island, Antarctic. Journal of Microbial Biochemistry and Technology, 6, 10.4172/1948-5948.1000159.Google Scholar
Smith, R.I.L. 1988. Recording bryophyte microclimate in remote and severe environments. In Glime, J.M., ed. Methods in bryology. Proceedings of the bryology methods workshop, Mainz. Nichinan, Japan: Hattori Botanical Laboratory, 275284.Google Scholar
Sugiyama, J. 1970. World’s last frontier III: polar mycology in Antarctica. Polar News, 6, 1724.Google Scholar
Tin, T., Fleming, Z.L., Hughes, K.A., Ainley, D.G., Convey, P., Moreno, C.A., Pfeiffer, S., Scott, J. & Snape, I. 2009. Impacts of local human activities on the Antarctic environment. Antarctic Science, 21, 10.1017/S0954102009001722.Google Scholar
Tsujimoto, M. & Imura, S. 2012. Does a new transportation system increase the risk of importing non-native species to Antarctica? Antarctic Science, 24, 10.1017/S0954102012000272.Google Scholar
Vyverman, W., Verleyen, E., Wilmotte, A. et al. 2010. Evidence for widespread endemism among Antarctic micro-organisms. Polar Science, 4, 10.1016/j.polar.2010.03.006.Google Scholar
Whinam, J., Chilcott, N. & Bergstrom, D.M. 2005. Subantarctic hitchhikers: expeditioners as vectors for the introduction of alien organisms. Biological Conservation, 121, 10.1016/j.biocon.2004.04.020.Google Scholar
White, T.J., Bruns, T., Lee, S. & Taylor, J.W. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In Innis, M.A., Gelfand, D.H., Sninsky, J.J. & White, T.J., eds. PCR protocols: a guide to methods and applications. New York: Academic Press, 315322.Google Scholar
Wicklow, D.T. 1968. Aspergillus fumigatus Fresenius isolated from ornithogenic soil collected at Hallett Station, Antarctica. Canadian Journal of Microbiology, 14, 10.1139/m68-119.Google Scholar
Yergeau, E., Bokhorst, S., Huiskes, A.H.L., Boschker, H.T.S., Aerts, R. & Kowalchuk, G.A. 2007. Size and structure of bacterial, fungal and nematode communities along an Antarctic environmental gradient. FEMS Microbial Ecology, 59, 10.1111/j.1574-6941.2006.00200.x.Google Scholar
Yergeau, E., Bokhorst, S., Kang, S., Zhou, J.Z., Greer, C.W., Aerts, R. & Kowalchuk, G.A. 2012. Shifts in soil microorganisms in response to warming are consistent across a range of Antarctic environments. ISME Journal, 6, 10.1038/ismej.2011.124.Google Scholar