Assessing DNA barcode sequences for Collembola species discrimination
DOI:
https://doi.org/10.25674/496Keywords:
Springtails, mtCOI, barcoding, specimen identification, GermanyAbstract
When dealing with small soil organisms such as Collembola, which occur in large numbers in soil, studies on e.g., population genetics or monitoring of soil conditions can significantly be accelerated by molecular-based high-throughput DNA barcoding methods. However, a prerequisite for the success of such approaches is a sufficient completeness of the reference databases. We used Collembola as an example to examine the current status of completeness of the two most important public repositories for DNA barcode sequences, the Barcode of Life DataSystems (BOLD) and GenBank, and the current accuracy of Collembola sequence identification. As part of the surveys for the Biological Monitoring Network of the federal state of Baden-Württemberg, we analysed how many of the Collembola species found in Baden-Württemberg so far have DNA barcodes. Additional sequence data were generated from currently obtained Collembola samples in order to close identified gaps in the barcode reference libraries. We then used these new sequences to determine how accurately they are assigned to a respective taxon by the identification systems of the reference databases, from species level to higher taxonomic ranks, or whether there are discrepancies. The results showed that the probability of correct identification in the reference databases is related to the number of individuals stored and identified to species level, but in most cases the accuracy of matches seemed to be less related to the sheer number of sequence data of the respective taxon already deposited but rather to the accuracy of morphological determination of the respective top matches. We give recommendations for users of such databases to avoid ambiguous entries when uploading their own sequences and to improve the quality of their sequence data through curation and annotation.
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Ahmed, S., M. Ibrahim, C. Nantasenamat, M. F. Nisar, A. A. Malik, R. Waheed, M. Z. Ahmed, S. C. Ojha, M. K. Alam & S. Khan (2022): Pragmatic Applications and Universality of DNA Barcoding for Substantial Organisms at Species Level. A Review to Explore a Way Forward. – BioMed Research International 2022 (2): 1–19.
Altschul, S. F., W. Gish, W. Miller, E. W. Myers & D. J. Lipman (1990): Basic local alignment search tool. – Journal of Molecular Biology 215 (3): 403–410.
Anthony, M. A., S. F. Bender & M. G. A. van der Heijden (2023): Enumerating soil biodiversity. – Proceedings of the National Academy of Sciences 120 (33).
Antil, S., J. S. Abraham, S. Sripoorna, S. Maurya, J. Dagar, S. Makhija, P. Bhagat, R. Gupta, U. Sood, R. Lal & R. Toteja (2023): DNA barcoding, an effective tool for species identification. A review. – Molecular Biology Reports 50 (1): 761–775.
Arribas, P., C. Andújar, K. Hopkins, M. Shepherd, A. P. Vogler & D. Yu (2016): Metabarcoding and mitochondrial metagenomics of endogean arthropods to unveil the mesofauna of the soil. – Methods in Ecology and Evolution 7 (9): 1071–1081.
Astrin, J. J., H. Höfer, J. Spelda, J. Holstein, S. Bayer, L. Hendrich, B. A. Huber, K.-H. Kielhorn, H.-J. Krammer, M. Lemke, J. C. Monje, J. Morinière, B. Rulik, M. Petersen, H. Janssen, C. Muster & M. Kuntner (2016): Towards a DNA Barcode Reference Database for Spiders and Harvestmen of Germany. – PLOS ONE 11 (9): e0162624.
Bardgett, R. D. & W. H. van der Putten (2014): Belowground biodiversity and ecosystem functioning. – Nature 515: 505–511.
Bellinger, P. F., K. Christiansen & F. Janssens (1996-2024): Checklist of the Collembola of the World [https://www.collembola.org/].
Bispo, A., D. Cluzeau, R. Creamer, M. Dombos, U. Graefe, P. Krogh, J. Sousa, G. Peres, M. Rutgers, A. Winding & J. Römbke (2009): Indicators for monitoring soil biodiversity. – Integrated environmental assessment and management 5 (4): 717–719.
Borisenko, A. V., J. E. Sones & P. D. N. Hebert (2009): The front-end logistics of DNA barcoding. Challenges and prospects. – Molecular Ecology Resources 9 Suppl s1: 27–34.
Bortolus, A. (2008): Error Cascades in the Biological Sciences. The Unwanted Consequences of Using Bad Taxonomy in Ecology. – AMBIO: A Journal of the Human Environment 37 (2): 114–118.
Bretfeld, G. (1999): Synopses on Palaearctic Collembola Part II: Symphypleona. – Abhandlungen und Berichte des Naturkundemuseums Görlitz 71 (1): 1–318.
Brussaard, L., P. C. de Ruiter & G. G. Brown (2007): Soil biodiversity for agricultural sustainability. – Agriculture, Ecosystems & Environment 121 (3): 233–244.
Buckner, J. C., R. C. Sanders, B. C. Faircloth & P. Chakrabarty (2021): The critical importance of vouchers in genomics. – eLife 10.
Buhay, J. E. (2009): "COI-like" Sequences Are Becoming Problematic in Molecular Systematic and DNA Barcoding Studies. – Journal of Crustacean Biology 29 (1): 96–110.
Burkhardt, U., D. J. Russell, P. Decker, M. Döhler, H. Höfer, S. Lesch, S. Rick, J. Römbke, C. Trog, J. Vorwald, E. Wurst & W. E. R. Xylander (2014): The Edaphobase Project of GBIF-Germany - A new online soil-zoological data warehouse. – Applied Soil Ecology 83: 3–12.
Carapelli, A., F. Frati, P. P. Fanciulli & R. Dallai (2001): Taxonomic revision of 14 south-western European species of Isotomurus (Collembola, Isotomidae), with description of four new species and the designation of the neotype for I.palustris. – Zoologica Scripta 30 (2): 115–143.
Ceríaco, L. M. P., E. E. Gutiérrez & A. Dubois (2016): Photography-based taxonomy is inadequate, unnecessary, and potentially harmful for biological sciences. – Zootaxa 4196 (3): zootaxa.4196.3.9.
Chorlton, S. D. (2024): Ten common issues with reference sequence databases and how to mitigate them. – Frontiers in bioinformatics 4 (1278228).
Coca-de-la-Iglesia, M., A. Gallego-Narbón, A. Alonso & V. Valcárcel (2024): High rate of species misidentification reduces the taxonomic certainty of European biodiversity databases of ivies (Hedera L.). – Scientific Reports 14 (1): 4876.
Collins, G., C. Schneider, L. L. Boštjančić, U. Burkhardt, A. Christian, P. Decker, I. Ebersberger, K. Hohberg, O. Lecompte, D. Merges, H. Muelbaier, J. Romahn, J. Römbke, C. Rutz, R. Schmelz, A. Schmidt, K. Theissinger, R. Veres, R. Lehmitz, M. Pfenninger & M. Bálint (2023): The MetaInvert soil invertebrate genome resource provides insights into below-ground biodiversity and evolution. – Communications Biology 6 (1): 1241.
Deharveng, L. (1982): Clé de détermination des genres de Neanurinae (Collemboles) d'Europe et de la région méditerranéenne, avec description de deux nouveaux genres. – Travaux du Laboratoire d'Ecobiologie des Arthropododes édaphiques, Toulouse 3: 7–13.
Dejaco, T., T. Arthofer, H. D. Sheets, K. Moder, B. Thaler-Knoflach, E. Christian, L. F. Mendes, B. C. Schlick-Steiner & F. M. Steiner (2012): A toolbox for integrative species delimitation in Machilis jumping bristletails (Microcoryphia: Machilidae). – Zoologischer Anzeiger 251 (4): 307–316.
Dunger, W. (1994): Synopses on Palaearctic Collembola: Introduction. – Abhandlungen und Berichte des Naturkundemuseums Görlitz 68 (3): 1–4.
Dunger, W. & B. Schlitt (2011): Synopses on Palaearctic Collembola Part VI-1: Tullbergiidae. – Soil Organisms 83 (1): 1–168.
Edaphobase (2025): Edaphobase data warehouse for soil organisms. Accessed via the Edaphobase Data-Query Portal [https://portal.edaphobase.org].
Engel, M., L. Ceríaco, G. Daniel, P. Dellapé, I. Löbl, M. Marinov, R. Reis, M. Young, A. Dubois, I. Agarwal, P. Lehmann A., M. Alvarado, N. Alvarez, F. Andreone, K. Araujo-Vieira, J. Ascher, D. Baêta, D. Baldo, S. Bandeira & C. Kusamba (2021): The taxonomic impediment. A shortage of taxonomists, not the lack of technical approaches. – Zoological Journal of the Linnean Society 193: 381–387.
Fjellberg, A. (1998): The Collembola of Fennoscandia and Denmark. Part 1. Poduromorpha. – Fauna Entomologica Scandinavica 35: 1–184.
Fjellberg, A. (2007): The Collembola of Fennoscandia and Denmark. Part 2. Entomobryomorpha and Symphypleona. – Fauna Entomologica Scandinavica 42: 1–266.
Folmer, O., M. Black, W. Hoeh, R. Lutz & R. Vrijenhoek (1994): DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. – Molecular Marine Biology and Biotechnology 3 (5): 294–299.
Geiger, M. F., J. J. Astrin, T. Borsch, U. Burkhardt, P. Grobe, R. Hand, A. Hausmann, K. Hohberg, L. Krogmann, M. Lutz, J. C. Monje, B. Misof, J. Moriniere, K. F. Müller, S. Pietsch, D. Quandt, B. Rulik, M. Scholler, W. Traunspurger, G. Haszprunar & W. Wägele (2016): How to tackle the molecular species inventory for an industrialized nation - lessons from the first phase of the German Barcode of Life initiative GBOL (2012-2015). – Genome 59 (9): 661–670.
Gisin, H. (1960): Collembolenfauna Europas. – Museum D'Histoire Naturelle, Genève: 1-311.
Gonzalez, A., P. Vihervaara, P. Balvanera, A. E. Bates, E. Bayraktarov, P. J. Bellingham, A. Bruder, J. Campbell, M. D. Catchen, J. Cavender-Bares, J. Chase, N. Coops, M. J. Costello, B. Czúcz, A. Delavaud, M. Dornelas, G. Dubois, E. J. Duffy, H. Eggermont, M. Fernandez, N. Fernandez, S. Ferrier, G. N. Geller, M. Gill, D. Gravel, C. A. Guerra, R. Guralnick, M. Harfoot, T. Hirsch, S. Hoban, A. C. Hughes, W. Hugo, M. E. Hunter, F. Isbell, W. Jetz, N. Juergens, W. D. Kissling, C. B. Krug, P. Kullberg, Y. Le Bras, B. Leung, M. C. Londoño-Murcia, J.-M. Lord, M. Loreau, A. Luers, K. Ma, A. J. MacDonald, J. Maes, M. McGeoch, J. B. Mihoub, K. L. Millette, Z. Molnar, E. Montes, A. S. Mori, F. E. Muller-Karger, H. Muraoka, M. Nakaoka, L. Navarro, T. Newbold, A. Niamir, D. Obura, M. O’Connor, M. Paganini, D. Pelletier, H. Pereira, T. Poisot, L. J. Pollock, A. Purvis, A. Radulovici, D. Rocchini, C. Roeoesli, M. Schaepman, G. Schaepman-Strub, D. S. Schmeller, U. Schmiedel, F. D. Schneider, M. M. Shakya, A. Skidmore, A. L. Skowno, Y. Takeuchi, M.-N. Tuanmu, E. Turak, W. Turner, M. C. Urban, N. Urbina-Cardona, R. Valbuena, A. van de Putte, B. van Havre, V. R. Wingate, E. Wright & C. Z. Torrelio (2023): A global biodiversity observing system to unite monitoring and guide action. – Nature Ecology & Evolution 7 (12): 1947–1952.
Gostel, M. R. & W. J. Kress (2022): The Expanding Role of DNA Barcodes. Indispensable Tools for Ecology, Evolution, and Conservation. – Diversity 14 (3): 213.
Gotelli, N. J., D. B. Booher, M. C. Urban, W. Ulrich, A. V. Suarez, D. K. Skelly, D. J. Russell, R. J. Rowe, M. Rothendler, N. Rios, S. M. Rehan, G. Ni, C. S. Moreau, A. E. Magurran, F. A. M. Jones, G. R. Graves, C. Fiera, U. Burkhardt & R. B. Primack (2021): Estimating species relative abundances from museum records. – Methods in Ecology and Evolution 14 (2): 431–443.
Griffiths, B. S., J. Römbke, R. M. Schmelz, A. Scheffczyk, J. H. Faber, J. Bloem, G. Pérès, D. Cluzeau, A. Chabbi, M. Suhadolc, J. P. Sousa, P. Martins da Silva, F. Carvalho, S. Mendes, P. Morais, R. Francisco, C. Pereira, M. Bonkowski, S. Geisen, R. D. Bardgett, F. T. de Vries, T. Bolger, T. Dirilgen, O. Schmidt, A. Winding, N. B. Hendriksen, A. Johansen, L. Philippot, P. Plassart, D. Bru, B. Thomson, R. I. Griffiths, M. J. Bailey, A. Keith, M. Rutgers, C. Mulder, S. E. Hannula, R. Creamer & D. Stone (2016): Selecting cost effective and policy-relevant biological indicators for European monitoring of soil biodiversity and ecosystem function. – Ecological Indicators 69: 213–223.
Hamilton, H. C., M. S. Strickland, K. Wickings, M. A. Bradford & N. Fierer (2009): Surveying soil faunal communities using a direct molecular approach. – Zoologischer Anzeiger 41 (6): 1311–1314.
Hardulak, L. A., J. Morinière, A. Hausmann, L. Hendrich, S. Schmidt, D. Doczkal, J. Müller, P. D. N. Hebert & G. Haszprunar (2020): DNA metabarcoding for biodiversity monitoring in a national park. Screening for invasive and pest species. – Molecular Ecology Resources.
Hendrich, L., J. Moriniere, G. Haszprunar, P. D. N. Hebert, A. Hausmann, F. Köhler & M. Balke (2014): A comprehensive DNA barcode database for Central European beetles with a focus on Germany: adding more than 3500 identified species to BOLD. – Molecular Ecology Resources.
Hogg, I. D. & P. D. N. Hebert (2004): Biological identification of springtails (Hexapoda: Collembola) from the Canadian Arctic, using mitochondrial DNA barcodes. – Canadian Journal of Zoology 82 (5): 749–754.
Hopkin, S. P. (2007): A Key to the Collembola (springtails) of Britain and Ireland. – Field Studies Council, Totnes / Devon: 252 pp.
Hüther, W. (1993): Sammel- und Präparationsmethoden für Bodenarthropoden. – Abhandlungen und Berichte des Naturkundemuseums Görlitz 66 (6): 1–11.
Jänsch, S., A. Scheffczyk, J. Römbke, V. Rojo, J. Vierna, A. Vizcaino, T. Natal da Luz, D. Alves, P. Martins, S. Mendes, L. Scopel, J. P. Sousa, P. H. Krogh, R. Sapkota & R. Schmelz (2023): Bewertung der Biologischen Vielfalt mittels DNA-Extraktion aus Bodenproben von Dauerbeobachtungsflächen (BDF). – UBA-Texte 142/2023 [https://www.umweltbundesamt.de/publikationen/bewertung-der-biologischen-vielfalt-mittels-dna].
Jordana, R. (2012): Synopses on Palaearctic Collembola 7/1: Capbryinae and Entomobryini. – Soil Organisms 84 (1): 1–390.
Kovac, L. & J. G. Palacios-Vargas (2008): Redescription of Isotomiella alulu and I. delamarei (Collembola: Isotomidae) with notes on the systematics of the genus and new records from the Neotropics. – Zootaxa 1825: 1–17.
Lavelle, P., T. Decaens, M. Aubert, S. Barot, M. Blouin, F. Bureau, P. Margerie, P. Mora & J. P. Rossi (2006): Soil invertebrates and ecosystem services. – European Journal of Soil Biology 42 (Supplement1): S3-S15.
Le Cadre, J., F. L. Klemp, M. Bálint, S. Scheu & I. Schaefer (2024): Applicability and perspectives for DNA barcoding of soil invertebrates. – PeerJ 12: e17709.
Lorenz, J. G., W. E. Jackson, J. C. Beck & R. Hanner (2005): The problems and promise of DNA barcodes for species diagnosis of primate biomaterials. – Philosophical Transactions of the Royal Society of London Series B-Biological Sciences 360: 1869–1878.
LUBW (2025): Baden-Wuerttemberg State Institute for the Environment, dept. 23 (LUBW) - Medienübergreifende Umweltbeobachtung [https://www.lubw.baden-wuerttemberg.de/medienuebergreifende-umweltbeobachtung].
Macfadyen, A. (1961): Improved funnel-type extractors for soil arthropods. – Journal of Animal Ecology 30 (1): 171–184.
Mari Mutt, J. A. (1980): A revision of Heteromurus s. str. (Insecta: Collembola: Entomobryidae). – Transactions of the Illinois State Academy of Sciences 72 (3): 29–50.
Mateos, E. (2008): The European Lepidocyrtus Bourlet, 1839 (Collembola: Entomobryidae). – Zootaxa 1769: 35–59.
Mateos, E. (2011): New Lepidocyrtus Bourlet, 1839 taxa from Greece (Collembola: Entomobryidae). – Zootaxa 3108: 25–40.
Mateos, E. (2012): The European Lepidocyrtus lanuginosus group (Collembola: Entomobryidae), definition and description of a new species from Spain. – Zootaxa 3570: 69–81.
Mateos, E. & M. Álvarez-Presas (2022): Integrative taxonomy reveals three new species of European Lepidocyrtus lignorum-group (Collembola, Entomobryidae). – Zootaxa 5100 (4): 451–481.
Mateos, E., P. Escuer, G. Buşmachiu, M. Riutort & M. Álvarez-Presas (2018): Untangling Lepidocyrtus (Collembola, Entomobryidae). New molecular data shed light on the relationships of the European groups. – Invertebrate Systematics.
Mateos, E. & H. Petersen (2012): Definition of the European Lepidocyrtus curvicollis group (Collembola: Entomobryidae) with description of a new species from Sardinia (Italy). – Zootaxa 3237: 51–62.
Mateos, E. & D. Winkler (2018): New data clarifying the taxonomy of European members of the Lepidocyrtus pallidus–serbicus group (Collembola, Entomobryidae). – Zootaxa 4429 (3).
Mebes, K. H. & J. Filser (1998): Does the species composition of Collembola affect nitrogen turnover? – Applied Soil Ecology 9 (1-3): 241–247.
Meier, R. (2017): Citation of taxonomic publications. The why, when, what and what not. – Systematic Entomology 42 (2): 301–304.
Meiklejohn, K. A., N. Damaso & J. M. Robertson (2019): Assessment of BOLD and GenBank - Their accuracy and reliability for the identification of biological materials. – PLOS ONE 14 (6): e0217084.
Orgiazzi, A., R. Bardgett, E. Barrios, V. Behan-Pelletier, M. Briones, J.-L. Chotte, G. B. Deyn, P. Eggleton, N. Fierer, T. D. Fraser, K. Hedlund, S. Jeffery, N. Johnson, A. Jones, E. Kandeler, N. Kaneko, P. Lavelle, P. Lemanceau, L. Miko & D. Wall (eds) (2016): Global Soil Biodiversity Atlas. – Luxembourg: 176 pp.
Packer, L., J. Gibbs, C. Sheffield & R. Hanner (2009): DNA barcoding and the mediocrity of morphology. – Molecular Ecology Resources 9: 42–50.
Palissa, A. (1964): Collembola. – In: Brohmer, P., P. Ehrmann & G. Ulmer (eds): Die Tierwelt Mitteleuropas, Band 4 Insekten 1. Teil, 1. Abschnitt. – Verlag von Quelle & Meyer, Leipzig: 2–299.
Parimuchova, A. & Ľ. Kovac (2016): A new cave species of the genus Protaphorura Absolon, 1901 (Collembola, Onychiuridae) from the Western Carpathians (Slovakia) with critical comments to the Palaearctic representatives of the genus. – Zootaxa 4098 (2): 254–272.
Pasnik, G. & W. M. Weiner (2017): First phylogenetic analysis of the tribe Oligaphorurini (Collembola. Onychiuridae) inferred from morphological data, with implications for generic classification. – Organisms Diversity & Evolution 17 (3): 619–631.
Pasquetto, I. V., B. M. Randles & C. L. Borgman (2017): On the Reuse of Scientific Data. – Data Science Journal 16: 8.
Pedersen, M. W., S. Overballe-Petersen, L. Ermini, C. D. Sarkissian, J. Haile, M. Hellstrom, J. Spens, P. F. Thomsen, K. Bohmann, E. Cappellini, I. B. Schnell, N. A. Wales, C. Carøe, P. F. Campos, A. M. Z. Schmidt, M. T. P. Gilbert, A. J. Hansen, L. Orlando & E. Willerslev (2015): Ancient and modern environmental DNA. – Philosophical transactions of the Royal Society of London. Series B, Biological sciences 370 (1660): 20130383.
Pentinsaari, M., S. Ratnasingham, S. E. Miller & P. D. N. Hebert (2020): BOLD and GenBank revisited - Do identification errors arise in the lab or in the sequence libraries? – PLOS ONE 15 (4): e0231814.
Phillips, J. D., D. J. Gillis & R. H. Hanner (2022): Lack of Statistical Rigor in DNA Barcoding Likely Invalidates the Presence of a True Species' Barcode Gap. – Frontiers in Ecology and Evolution 10: 44.
Pomorski, R. J. (1990): Morphological-systematic studies on the variability of pseudocelli and some morphological characters in Onychiurus of the "armatus-group" (Collembola, Onychiuridae) Part II. On synonyms within the ''armatus-group'', with special reference to diagnostic characters. – Annales Zoologici 43: 535–575.
Pomorski, R. J. (1998): Onychiurinae of Poland (Collembola: Onychiuridae), Genus - International Journal of Invertebrate Taxonomy (Supplement). – Polish Taxonomical Society, Wroclaw: 1-201.
Pomorski, R. J. (2001): Review of the genus Hymenaphorura Bagnall, 1948 with description of eleven new species from North America and Siberia (Collembola: Onychiuridae). – Insect Systematics and Evolution 32 (4): 439–474.
Porco, D., A. Bedos, P. Greenslade, C. Janion, D. Skarzynski, M. I. Stevens, B. J. van Vuuren & L. Deharveng (2012): Challenging species delimitation in Collembola: cryptic diversity among common springtails unveiled by DNA barcoding. – Invertebrate Systematics 26: 470–477.
Porco, D., L. Deharveng, T. Decaens, S. James, P. Stoev, D. Walter & P. D. N. Hebert (2012): DNA barcoding soil invertebrates: lighting up the underground. – Book of Abstracts XVI ICSZ: 60.
Potapov, M. B. (2001): Synopses on Palaearctic Collembola Part III: Isotomidae. – Abhandlungen und Berichte des Naturkundemuseums Görlitz 73 (2): 1–603.
Ratnasingham, S. & P. D. N. Hebert (2007): BOLD: The Barcode of Life Data System (www.barcodinglife.org). – Molecular Ecology Notes 7 (3): 355–364.
Recuero, E., F. E. Etzler & M. S. Caterino (2024): Most soil and litter arthropods are unidentifiable based on current DNA barcode reference libraries. – Current Zoology 70 (5): 637–646.
Resch, M. C., J. Shrubovych, D. Bartel, N. U. Szucsich, G. Timelthaler, Y. Bu, M. Walzl & G. Pass (2014): Where Taxonomy Based on Subtle Morphological Differences Is Perfectly Mirrored by Huge Genetic Distances: DNA Barcoding in Protura (Hexapoda). – PLOS ONE 9 (3): e90653.
Ristok, C., D. Babin, B. Bertkowski, B. Burkhard, J. Filser, K. Hohberg, J. Kleemann, S. Kolb, R. Lehmitz, M. C. Rillig, J. Römbke, L. Ruess, S. Scheu, N. Scheunemann, A. Schmidt, B. Steinhoff-Knopp, N. Eisenhauer, C. C. Tebbe & W. E. R. Xylander (2025): Towards a comprehensive assessment of soil biodiversity in Germany: status quo, challenges, and policy implications. – Soil Organisms 97 (2).
Roithmeier, O., U. Burkhardt, E. Daghighi & J. Filser (2018): Desoria trispinata (MacGillivray, 1896), a promising model Collembola species to study biological invasions in soil communities. – Pedobiologia 67: 45–56.
Rougerie, R., T. Decaens, L. Deharveng, D. Porco, S. W. James, C. H. Chang, B. Richard, M. Potapov, Y. Suhardjono & P. D. N. Hebert (2009): DNA barcodes for soil animal taxonomy. – Pesquisa Agropecuaria Brasileira 44 (8): 789–802.
Rubinoff, D. (2006): Utility of mitochondrial DNA barcodes in species conservation. – Conservation Biology 20 (4): 1026–1033.
Russell, D. J., E. Naudts, N. A. Soudzilovskaia, M.J.I. Briones, M. Çakır, E. Conti, J. Cortet, C. Fiera, D. H. Kutuzovic, M. Hedde, K. Hohberg, D. Indjic, P. H. Krogh, R. Lehmitz, S. Lesch, Z. Marjanovic, C. Mulder, L. Mumladze, M. Murvanidze, S. Rick, M. Roß-Nickoll, J. Schlaghamerský, O. Schmidt, O. Shelef, M. Suhadolc, M. Tsiafouli, A. Winding, A. Zaytsev & A. Potapov (2024): Edaphobase 2.0. Advanced international data warehouse for collating and using soil biodiversity datasets. – Applied Soil Ecology 204 (3): 105710.
Saltzwedel, H. von, S. Scheu & I. Schaefer (2016): Founder events and pre-glacial divergences shape the genetic structure of European Collembola species. – BMC Evolutionary Biology 16 (1): 69.
Schenekar, T., M. Schletterer, L. A. Lecaudey & S. J. Weiss (2020): Reference databases, primer choice, and assay sensitivity for environmental metabarcoding. Lessons learnt from a re‐evaluation of an eDNA fish assessment in the Volga headwaters. – River Research and Applications 36 (7): 1004–1013.
Schlick-Steiner, B. C., F. M. Steiner, B. Seifert, C. Stauffer, E. Christian & R. H. Crozier (2010): Integrative Taxonomy: A Multisource Approach to Exploring Biodiversity. – Annual Review of Entomology 55: 421–438.
Schneider, C. & C. A. D'Haese (2013): Morphological and molecular insights on Megalothorax: the largest Neelipleona genus revisited (Collembola). – Invertebrate Systematics 27: 317–364.
Simon Benito, J. C. & J. G. Palacios-Vargas (2007): New species of Pseudosinella (Collembola: Entomobryidae) from Iberian Peninsula. – Zootaxa 1479: 9–19.
Simon Benito, J. C. & J. G. Palacios-Vargas (2008): Four new Pseudosinella (Collembola: Entomobryidae) from La Rioja, Spain. – Zootaxa 1728: 59–68.
Smolis, A. & L. Deharveng (2017): Neanura judithae n. sp. from Polish Carpathians, with an updated and illustrated key to all species of the genus Neanura MacGillivray, 1893 (Collembola, Neanuridae). – Zoosystema 39 (1): 37–47.
Stach, J. (1960): Materialien zur Kenntnis der Collembolenfauna Afghanistans [Contribution à l'étude de la faune d'Afghanistan]. – Acta Zoologica Cracoviensia 5 (12): 507–582.
Sunnucks, P. & D. F. Hales (1996): Numerous transposed sequences of mitochondrial cytochrome oxidase I-II in aphids of the Genus Sitobion (Hemiptera: Aphididae). – Molecular Biology and Evolution 13 (3): 510–524.
Tenopir, C., N. M. Rice, S. Allard, L. Baird, J. Borycz, L. Christian, B. Grant, R. Olendorf & R. J. Sandusky (2020): Data sharing, management, use, and reuse. Practices and perceptions of scientists worldwide. – PLOS ONE 15 (3): e0229003.
Thibaud, J.-M., H. J. Schulz, M. M. da Gama & W. Dunger (2004): Synopses on Palaearctic Collembola Part IV: Hypogastruridae. – Abhandlungen und Berichte des Naturkundemuseums Görlitz 75 (2): 1–287.
Thomsen, P. F. & E. Willerslev (2015): Environmental DNA. An emerging tool in conservation for monitoring past and present biodiversity. – Biological Conservation 183: 4–18.
van Bezouw, R., J. McCulloch, F. Janssens & M. Berg (2022): An emended description of Sminthurinus lawrencei Gisin 1963, with notes on the identification of black Sminthurinus species. – Soil Organisms 94 (3): 127–138.
Wagg, C., F. Bender, F. Widmer & M. G.-A. van der Heijden (2014): Soil biodiversity and soil community composition determine ecosystem multifunctionality. – Proceedings of the National Academy of Sciences of the United States of America 111: 5266–5270.
Wall, D. H. (ed) (2012): Soil ecology and ecosystem services. – Oxford University Press, Oxford: 406 pp.
Weiner, W. M. & C. Fiera (2020): Two new species of Hymenaphorura Bagnall, 1948 (Collembola, Onychiuridae) from Romania and an updated key to the genus. – ZooKeys 960: 17–38.
Whitworth, T. L., R. D. Dawson, H. Magalon & E. Baudry (2007): DNA barcoding cannot reliably identify species of the blowfly genus Protocalliphora (Diptera. Calliphoridae). – Proceedings of the Royal Society B-Biological Sciences 274 (1619): 1731–1739.
Winkler, D., M. T. Németh & C. Fiera (2021): A new species of Pseudosinella Schäffer, 1897 (Collembola, Entomobryidae) from Hungary and Romania, with redescription of the related species Pseudosinella huetheri Stomp, 1971. – ZooKeys 1063: 121–137.
Young, M. R., J. R. deWaard & P. D. N. Hebert (2021): DNA barcodes enable higher taxonomic assignments in the Acari. – Scientific Reports 11 (1): 2963.
Young, M. R. & P. D. N. Hebert (2022): Unearthing soil arthropod diversity through DNA metabarcoding. – PeerJ 10 (6822): e12845.
Young, M. R., M. L. Moraza, E. Ueckermann, D. Heylen, L. F. Baardsen, J. F. Lima-Barbero, S. Gal, E. Gavish-Regev, Y. Gottlieb, L. Roy, E. Recht, M. El Adouzi & E. Palevsky (2019): Linking morphological and molecular taxonomy for the identification of poultry house, soil, and nest dwelling mites in the Western Palearctic. – Scientific Reports 9 (1): 5784.
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