Abstract
Terrestrial diatom communities are dynamic, partially unknown and potential bioindicators of the soil ecological quality. Many different sampling methods for soil algae can be found in the literature. However, so far none of them have been tested for their performance with soil diatom communities and given recommendations for obtaining a representative diatom sample for bioindication purposes. The aim of this study was to develop a standardized sampling protocol for terrestrial diatoms and test the spatial variability of the communities to ensure the representativeness of the samples obtained. Sampling was performed in four different sampling sites in the Attert River basin (NW Luxembourg), using metal cylinders (Ø 5.6 cm) to extract soil cores. Our objective was to determine whether a single cylinder or a mix of several is needed to obtain a representative sample of the community of a certain site. Different statistical analyses (ANOVA, PerMANOVA and Mantel test) have been carried out to assess the reliability of the sampling method and give some recommendations for a routine sampling. Inside each site, no differences were found between single and mixed samples for their species composition or diatom-based quality index values. However, the species richness and diversity had significant differences in the only natural (forest) sampled site. The method here presented has proven to be useful for obtaining representative soil diatom samples and its use is recommended following the advices presented in this work.
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24 January 2018
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References
Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46
Antonelli M, Wetzel CE, Ector L, Teuling AJ, Pfister L (2017) On the potential for terrestrial diatom communities and diatom indices to identify anthropic disturbance in soils. Ecol Indic 75:73–81
Bate N, Newall P (2002) Techniques for the use of diatoms in water quality assessment how many valves. In: John J (ed) Proceedings of the 15th International Diatom Symposium 1998. A.R.G. Gantner Verlag K.G., Ruggell, pp 153–160
Bathurst RR, Zori D, Byock J (2010) Diatoms as bioindicators of site use: locating turf structures from the Viking Age. J Archaeol Sci 37:2920–2928
Battarbee RW (1986) Diatom analysis. In: Berglund BE (ed) Handbook of Holocene Palaeoecology and Palaeohydrology. Wiley, New York, pp 527–570
Bérard A, Dorigo U, Humbert JF, Martin-Laurent F (2005) Microalgae community structure analysis based on 18S rDNA amplification from DNA extracted directly from soil as a potential soil bioindicator. Agron Sustain Dev 25:285–291
Bertrand J, Coste C, Le Cohu R, Renon J-P, Ector L (2016) Étude préliminaire sur la présence de diatomées sur les lichens. Bot Lett 163:93–115
Blanco S, Doucet M, Fernández-Montiel I, Gabilondo R, Bécares E (2017) Changes in the soil diatom community induced by experimental CO2 leakage. Int J Greenhouse Gas Control 61:104–110
Bock W (1963) Diatomeen extrem trockener Standorte. Nova Hedwigia 5:199–254
Bock W (1970) Felsen und Mauern als Diatomeenstandorte. Beih. Nova Hedwigia 31:395–441
Brendemühl I (1949) Über die Verbreitung der Erddiatomeen. Arch Mikrobiol 14:407–449
CEMAGREF (1982) Étude des méthodes biologiques d’appréciation quantitative de la qualité des eaux. Rapport Cemagref QE Lyon-AF Bassin Rhône Méditerranée Corse, pp 218
Coles AE, Wetzel CE, Martínez-Carreras N, Ector L, McDonnell JJ, Frentress J, Klaus J, Hoffmann L, Pfister L (2016) Diatoms as a tracer of hydrological connectivity: are they supply limited? Ecohydrology 9:631–645
Corine Land Cover (2012) http://land.copernicus.eu/pan-european/corine-land-cover/clc-2012. Accessed 15 March 2017
Dorokhova MF (2007) Diatoms as indicators of soil conditions in oil production regions. Oceanol Hydrobiol Stud 36(suppl 1):129–135
Dufrêne M, Legendre P (1997) Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol Monogr 67:345–366
Elster J, Lukesová A, Svoboda J, Kopecky J (1999) Diversity and abundance of soil algae in the polar desert, Sverdrup Pass, central Ellesmere Island. Polar Rec 35:231–254
Ettl H, Gärtner G (2014) Syllabus der Boden-, Luft-, und Flechtenalgen, 2. Auflage edn. Springer Spektrum, Berlin
European Union (2000) Directive 2000/60/EC of the European Parliament and of the Council of 23 October 2000 establishing a framework for community action in the field of water policy. Off J Eur Comm L327:1–73
Falasco E, Ector L, Isaia M, Wetzel CE, Hoffmann L, Bona F (2014) Diatom flora in subterranean ecosystems: a review. Int J Speleol 43:231–251
Fazlutdinova AI, Sukhanova NV (2014) Composition of soil diatoms in zones of impact from oil production complexes. Russ J Ecol 45:188–193
Fernández MR, Martín G, Corzo J, de la Linde A, Garcia E, Lopez M, Sousa M (2017) Design and testing of a new diatom-based index for heavy metal pollution. Arch Environ Contam Toxicol. https://doi.org/10.1007/s00244-017-0409-6
Flower RJ (2005) A review of diversification trends in diatom research with special reference to taxonomy and environmental applications using examples from Lake Baikal and elsewhere. Proc Calif Acad Sci 56:107–128
Gordon R, Losic D, Tiffany MA, Nagy SS, Sterrenburg FA (2009) The Glass Menagerie: diatoms for novel applications in nanotechnology. Trends Biotechnol 27:116–127
Hammer Ø, Harper DAT, Ryan PD (2001) PAST: Paleontological statistics software package for education and data analysis. Palaeontol Electron 4:1–9
Hassan GS, Espinosa MA, Isla FI (2008) Fidelity of dead diatom assemblages in estuarine sediments: how much environmental information is preserved? PALAIOS 23:112–120
Heger TJ, Straub F, Mitchell EAD (2012) Impact of farming practices on soil diatoms and testate amoebae: a pilot study in the DOK-trial at Therwil, Switzerland. Eur J Soil Biol 49:31–36
Hofmann G, Werum M, Lange-Bertalot H (2011) Diatomeen im Susswasser-Benthos von Mitteleuropa. Bestimmungsflora Kieselalgen fur die okologische Praxis. Uber 700 der haufigsten Arten und ihre Okologie. A.R.G. Gantner Verlag K.G., Ruggell
Hunt ME, Floyd GL, Stout BB (1979) Soil algae in field and forest environments. Ecology 60:362–375
Hustedt F (1942) Aërophile Diatomeen in der nordwestdeutschen Flora. Ber Deutsch. Bot Ges 60:55–73
Ivarsson LN, Ivarsson M, Lundberg J, Sallstedt T, Rydin C (2013) Epilithic and aerophilic diatoms in the artificial environment of Kungsträdgården metro station, Stockholm, Sweden. Int J Speleol 42:289–297
Johansen JR, Javakul A, Rushforth SR (1982) Effects of burning on the algal communities of a high desert soil near Wallsburg, Utah. J Range Manag 35:598–600
Kahlert M, Rašić IS (2015) Similar small-scale variation of diatom assemblages on different substrates in a mesotrophic stream. Acta Bot Croat 74:363–376
Kale A, Levkov Z, Karthick B (2017) Typification of two species of Luticola (Bacillariophyta) from aerophilic habitats of the Western Ghats, India. Phytotaxa 298:29–42
Kelly MG, Cazaubon A, Coring E, Dell'Uomo A, Ector L, Goldsmith B, Guasch H, Hürlimann J, Jarlman A, Kawecka B, Kwandrans J, Laugaste R, Lindstrøm E-A, Leitao M, Marvan P, Padisák J, Pipp E, Prygiel J, Rott E, Sabater S, van Dam H, Vizinet J (1998) Recommendations for the routine sampling of diatoms for water quality assessments in Europe. J Appl Phycol 10:215–224
Klaus J, Wetzel CE, Martínez-Carreras N, Ector L, Pfister L (2015) A tracer to bridge the scales: on the value of diatoms for tracing fast flow path connectivity from headwaters to meso-scale catchments. Hydrol Process 29:5275–5289
Kolkwitz R, Marsson M (1909) Ökologie der tierischen Saprobien. Int Rev Ges Hydrobiol 2:126–152
Krammer K (2000) The genus Pinnularia. In: Lange-Bertalot H (ed) Diatoms of Europe, vol 1. A.R.G. Gantner Verlag K.G., Ruggell
Kulikovskiy MS, Lange-Bertalot H, Witowski A et al (2010) Diatom assemblages from Sphagnum bogs of the world. I. Nur bog in northern Mongolia. Biblioth Diatomol 55:1–326
Lakatos M, Lange-Bertalot H, Büdel B (2004) Diatoms living inside the thallus of the green algal lichen Coenogonium linkii in neotropical lowland rain forests. J Phycol 40:70–73
Lange-Bertalot H (2001) Navicula sensu stricto. 10 Genera separated from Navicula sensu lato. Frustulia. In: Lange-Bertalot H (ed) Diatoms of Europe, vol 2. A.R.G. Gantner Verlag K.G., Ruggell
Lange-Bertalot H, Cavacini P, Tagliaventi N, Alfinito S (2003) Diatoms of Sardinia. Rare and 76 new species in rock pools and other ephemeral waters. Iconogr Diatomol 12:1–438
Lange-Bertalot H, Bąk M, Witowski A, Tagliaventi N (2011) Eunotia and some related genera. In: Lange-Bertalot H (ed) Diatoms of Europe, vol 6. A.R.G. Gantner Verlag K.G., Ruggell
Lecointe C, Coste M, Prygiel J (1993) “Omnidia”: software for taxonomy, calculation of diatom indices and inventories management. Hydrobiologia 269–270:509–513
Lemes-da-Silva NM, Garey MV, Branco LHZ (2017) Floristic diversity, richness and distribution of Trentepohliales (Chlorophyta) in Neotropical ecosystems. Braz. J Bot:1–14. https://doi.org/10.1007/s40415-017-0390-3
Levkov Z, Metzeltin D, Pavlov A (2013) Luticola and Luticolopsis. In: Lange-Bertalot H (ed) Diatoms of Europe, vol 7. Koeltz Scientific Books, Köningstein, pp 1–697
Lowe R, Kociolek JP, You Q, Wang Q, Stepanek J (2017) Diversity of the diatom genus Humidophila in karst areas of Guizhou, China. Phytotaxa 305:269–284
Ludes B, Coste M (1996) Diatomées et médecine légale. Lavoisier Tec & Doc, Paris
Lukešová A (2001) Soil algae in brown coal and lignite post-mining areas in Central Europe (Czech Republic and Germany). Restor Ecol 9:341–350
Lund JWG (1945) Observations on soil algae I. The ecology, size and taxonomy of British soil diatoms. New Phytol 44:196–219
Lund JWG (1946) Observations on soil algae I. The ecology, size and taxonomy of British soil diatoms. New Phytol 45:56–110
Mann DG, Droop SJM (1996) Biodiversity, biogeography and conservation of diatoms. Hydrobiologia 336:19–32
Mann DG, Vanormelingen P (2013) An inordinate fondness? The number, distributions, and origins of diatom species. J Eukaryot Microbiol 60:414–420
Martínez-Carreras N, Wetzel CE, Frentress J, Ector L, McDonnell JJ, Hoffmann L, Pfister L (2015) Hydrological connectivity inferred from diatom transport through the riparian-stream system. Hydrol Earth Syst Sci 19:3133–3151
McCormick PV, Cairns J (1994) Algae as indicators of environmental change. J Appl Phycol 6:509–526
Medlin LK (2009) Diatoms (Bacillariophyta). In: Hedges SB, Kumar S (eds) The Timetree of life. Oxford University Press, Oxford, pp 127–130
Nychka D, Furrer R, Paige J, Sain S (2015) Fields: tools for spatial data. National Center for Atmospheric Research, Boulder, CO. https://doi.org/10.5065/D6W957CT
Oksanen J, Blanchet FG, Friendly M, et al (2017) vegan: Community Ecology Package
Pappas JL, Stoermer EF (1996) Quantitative method for determining a representative algal sample count. J Phycol 32:693–696
Petersen JB (1915) Studier over danske aërofile alger. Kongel Danske Vidensk Selsk Skr Naturvidensk Math Afd 12:269–380, 4 pls
Petersen JB (1928) The aërial algae of Iceland. In: The botany of Iceland, pp 325–447
Petersen JB (1935) Studies on the biology and taxonomy of soil algae. C.A. Reitzels Forlag, Copenhagen
Petersen JB (1946) Algae collected by Eric Hultén on the Swedish Kamtchatka Expedition, 1920–22: especially from Hot Springs. Kommission hos Munksgaard, Copenhagen
Petsch DK, Schneck F, Melo AS (2017) Substratum simplification reduces beta diversity of stream algal communities. Freshw Biol 62:205–213
Pfister L, McDonnell JJ, Wrede S, Hlúbiková D, Matgen P, Fenicia F, Ector L, Hoffmann L (2009) The rivers are alive: on the potential for diatoms as a tracer of water source and hydrological connectivity. Hydrol Process 23:2841–2845
Piette MHA, De Letter EA (2006) Drowning: still a difficult autopsy diagnosis. Forensic Sci Int 163:1–9
QGIS Development Team (2017) QGIS geographic information system. Open Source GeospatialFoundation. http://qgis.osgeo.org
R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Rao CR (1995) A review of canonical coordinates and an alternative to correspondence analysis using Hellinger distance. Qüestiió 19:23–63
Reichardt E (2008) Bemerkenswerte Diatomeenfunde aus Bayern VI. Hantzschia hyperborea (Grun.) Lange-B. Ber Bayer Bot Ges 78:17–22
Reichardt E (2012) Neue Diatomeen (Bacillariophyceae) aus dem Gebiet der Stadt Treuchtlingen. Ber Bayer Bot Ges 82:19–32
Rühland K, Priesnitz A, Smol JP (2003) Paleolimnological evidence from diatoms for recent environmental changes in 50 lakes across Canadian Arctic treeline. Arctic Antarct Alp Res 35:110–123
Schimanski H (1973) Beitrag zur Diatomeenflora von Erlangen. Nova Hedwigia 24:237–335
Schimanski H (1978) Beitrag zur Diatomeenflora des Frankenwaldes. Nova Hedwigia 30:557–633
Schlichting HE (1975) Some subaerial algae from Ireland. Br Phycol J 10:257–261
Shannon CE (1948) A mathematical theory of communication. Bell Syst Tech J 27:379–423
Smol JP, Stoermer EF (2010) The diatoms: applications for the environmental and earth sciences. Cambridge University Press, Cambridge
Soininen J (2007a) Environmental and spatial control of freshwater diatoms—a review. Diatom Res 22:473–490
Soininen J (2007b) The distance decay of similarity in ecological communities. Ecography 30:3–12
Soininen J, Könönen K (2004) Comparative study of monitoring south-Finnish rivers and streams using macroinvertebrate and benthic diatom community structure. Aquat Ecol 38:63–75
Souffreau C, Vanormelingen P, Verleyen E, Sabbe K, Vyverman W (2010) Tolerance of benthic diatoms from temperate aquatic and terrestrial habitats to experimental desiccation and temperature stress. Phycologia 49:309–324
Tauro F, Martínez-Carreras N, Barnich F, Juilleret J, Wetzel CE, Ector L, Hissler C, Pfister L (2015) Diatom percolation through soils: a proof of concept laboratory experiment. Ecohydrology 9:753–764
Utermöhl H (1958) Zur vervollkommnung der quantitativen phytoplankton methodik. Schweizerbart. Science Publishers, Stuttgart
Vacht P, Puusepp L, Koff T, Reitalu T (2014) Variability of riparian soil diatom communities and their potential as indicators of anthropogenic disturbances. Est J Ecol 63:168–184
Van Dam H, Mertens A, Sinkeldam J (1994) A coded checklist and ecological indicator values of freshwater diatoms from The Netherlands. Neth J Aquatic Ecol 28:117–133
Van de Vijver B, Beyens L (1999) Biogeography and ecology of freshwater diatoms in Subantarctica: a review. J Biogeogr 26:993–1000
Van de Vijver B, Ledeganck P, Beyens L (2002) Soil diatom communities from Ile de la Possession (Crozet, sub-Antarctica). Polar Biol 25:721–729
Venter A, Levanets A, Siebert S, Rajakaruna N (2015) A preliminary survey of the diversity of soil algae and cyanoprokaryotes on mafic and ultramafic substrates in South Africa. Aust J Bot 63:341–352
Werum M, Lange-Bertalot H (2004) Diatomeen in Quellen unter hydrogeologischen und anthropogenen Einflüssen in Mitteleuropa und anderen Regionen [Diatoms in springs from Central Europe and elsewhere under the influence of hydrogeology and anthropogenic impacts]. Iconogr Diatomol 13:1–417
Wetzel CE, Martínez-Carreras N, Hlúbiková D, Hoffmann L, Pfister L, Ector L (2013) New combinations and type analysis of Chamaepinnularia species (Bacillariophyceae) from aerial habitats. Cryptogam Algol 34:149–168
Wetzel CE, Ector L, Van de Vijver B, Compere P, Mann DG (2015) Morphology, typification and critical analysis of some ecologically important small naviculoid species (Bacillariophyta). Fottea 15:203–234
Wetzel CE, Barragán C, Ector L (2017) Sellaphora lundii nom. et stat. nov. (Bacillariophyta), a forgotten European terrestrial species. Notulae Algarum 38:1–3
Willson D, Forest HS (1957) An exploratory study on soil algae. Ecology 38:309–313
Wojtal AZ (2013) Species composition and distribution of diatom assemblages in spring waters from various geological formations in southern Poland. Biblioth Diatomol 59:1–436
Wu N, Dong X, Liu Y, Wang C, Baattrup-Pedersen A, Riis T (2017) Using river microalgae as indicators for freshwater biomonitoring: review of published research and future directions. Ecol Indic 81:124–131
Yallop ML, Kelly MG (2006) From pattern to process: understanding stream phytobenthic assemblages and implications for determining “ecological status”. Nova Hedwigia 130:357–372
Zancan S, Trevisan R, Paoletti MG (2006) Soil algae composition under different agro-ecosystems in north-eastern Italy. Agric Ecosyst Environ 112:1–12
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We are grateful to the Luxembourg Institute of Science and Technology (LIST), which provided the opportunity and the necessary funding for conducting this research.
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The original version of this article was revised: In Figs. 45-94. (foot note), “Sellaphora sp. (aff. hustedtii/sardiniensis)” had been recently described as “Sellaphora lundii”. In Table 2, the entire line with “Sellaphora lundii C.E. Wetzel, Barragán & Ector” should be moved after the taxon “Sellaphora atomoides C.E. Wetzel & Van de Vijver”. The data are now correctly shown here.
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Barragán, C., Wetzel, C.E. & Ector, L. A standard method for the routine sampling of terrestrial diatom communities for soil quality assessment. J Appl Phycol 30, 1095–1113 (2018). https://doi.org/10.1007/s10811-017-1336-7
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DOI: https://doi.org/10.1007/s10811-017-1336-7