Skip to main content

Advertisement

Log in

Biodiversity analyses in freshwater meiofauna through DNA sequence data

  • MEIOFAUNA IN FRESHWATER ECOSYSTEMS
  • Review Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

Microscopic animals (also referred to as meiofauna) in freshwater habitats include several common, abundant and species-rich phyla, whose patterns of diversity are poorly known. Several approaches using DNA sequence data can be used to improve our knowledge on their biodiversity. In this review, we focus on studies using DNA data for taxonomy, and for environmental studies through metabarcoding on freshwater meiofauna. The results of the literature survey reveal that the use of DNA data is still rather limited. We screen the available literature on the topic and analyse the details of the current use and choices of the methods in freshwater meiofauna, the potential problems and limitations, and the flawed parts that still need to be improved. We conclude the review with a perspective on the still unexploited potentials in future applications to address biodiversity shortfalls in species diversity and taxonomy, and in the ecological and biogeographical patterns of species distribution.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Abad, D., A. Albaina, M. Aguirre, A. Laza-Martínez, I. Uriarte, A. Iriarte, F. Villate & A. Estonba, 2016. Is metabarcoding suitable for estuarine plankton monitoring? A comparative study with microscopy. Marine Biology 163: 739.

    Article  Google Scholar 

  • Abolafia, J. & R. Peña-Santiago, 2017. On the identity of Chiloplacus magnus Rashid & Heyns, 1990 and C. insularis Orselli & Vinciguerra, 2002 (Rhabditida: Cephalobidae), two confusable species. Nematology 19: 1017–1034.

    Article  Google Scholar 

  • Andújar, C., P. Arribas, C. Gray, C. Bruce, G. Woodward, D. W. Yu & A. P. Vogler, 2018a. Metabarcoding of freshwater invertebrates to detect the effects of a pesticide spill. Molecular Ecology 27: 146–166.

    Article  PubMed  CAS  Google Scholar 

  • Andújar, C., P. Arribas, D. W. Yu, A. P. Vogler & B. C. Emerson, 2018b. Why the COI barcode should be the community DNA metabarcode for the metazoa. Molecular Ecology 27: 3968–3975.

    Article  PubMed  Google Scholar 

  • Aránguiz-Acuña, A., P. Pérez-Portilla, A. De la Fuente & D. Fontaneto, 2018. Life-history strategies in zooplankton promote coexistence of competitors in extreme environments with high metal content. Scientific Reports 8: 11060.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Asmyhr, M. G., G. Hose, P. Graham & A. J. Stow, 2014. Fine-scale genetics of subterranean syncarids. Freshwater Biology 59: 1–11.

    Article  Google Scholar 

  • Atherton, S. & U. Jondelius, 2018. Wide distributions and cryptic diversity within a Microstomum (Platyhelminthes) species complex. Zoologica Scripta 47: 486–498.

    Article  Google Scholar 

  • Atherton, S. & U. Jondelius, 2019. A taxonomic review and revisions of Microstomidae (Platyhelminthes: Macrostomorpha). PloS ONE 14: e0212073.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baird, D. J. & M. Hajibabaei, 2012. Biomonitoring 2.0: a new paradigm in ecosystem assessment made possible by next-generation DNA sequencing. Molecular Ecology 21: 2039–2044.

    Article  PubMed  Google Scholar 

  • Banerji, A., M. Bagley, M. Elk, E. Pilgrim, J. Martinson & J. Santo Domingo, 2018. Spatial and temporal dynamics of a freshwater eukaryotic plankton community revealed via 18S rRNA gene metabarcoding. Hydrobiologia 818: 71–86.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Benson, D. A., M. Cavanaugh, K. Clark, I. Karsch-Mizrachi, D. J. Lipman, J. Ostell & E. W. Sayers, 2017. GenBank. Nucleic Acids Research 45: D37–D42.

    Article  CAS  PubMed  Google Scholar 

  • Bickford, D., D. J. Lohman, N. S. Sodhi, P. K. Ng, R. Meier, K. Winker, K. K. Ingram & I. Das, 2007. Cryptic species as a window on diversity and conservation. Trends in Ecology and Evolution 22: 148–155.

    Article  PubMed  Google Scholar 

  • Bik, H. M., D. L. Porazinska, S. Creer, J. G. Caporaso, R. Knight & W. K. Thomas, 2012. Sequencing our way towards understanding global eukaryotic biodiversity. Trends in Ecology & Evolution 27: 233–243.

    Article  Google Scholar 

  • Birky, C. W., J. Adams, M. Gemmel & J. Perry, 2010. Using population genetic theory and DNA sequences for species detection and identification in asexual organisms. PloS ONE 5: e10609.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Blaxter, M., 2016. Imagining Sisyphus happy: DNA barcoding and the unnamed majority. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 371: 2039–20044.

    Article  CAS  Google Scholar 

  • Brannock, P. M. & K. M. Halanych, 2015. Meiofaunal community analysis by high-throughput sequencing: comparison of extraction, quality filtering, and clustering methods. Marine Genomics 23: 67–75.

    Article  PubMed  Google Scholar 

  • Brown, E. A., F. J. J. Chain, T. J. Crease, H. J. Macisaac & M. E. Cristescu, 2015. Divergence thresholds and divergent biodiversity estimates: can metabarcoding reliably describe zooplankton communities? Ecology and Evolution 5: 2234–2251.

    Article  PubMed  PubMed Central  Google Scholar 

  • Brown, E. A., F. J. J. Chain, A. Zhan, H. J. Macisaac & M. E. Cristescu, 2016. Early detection of aquatic invaders using metabarcoding reveals a high number of non-indigenous species in Canadian ports. Diversity and Distributions 22: 1045–1059.

    Article  Google Scholar 

  • Callahan, B. J., P. J. McMurdie, M. J. Rosen, A. W. Han, A. J. A. Johnson & S. P. Holmes, 2016. DADA2: high-resolution sample inference from Illumina amplicon data. Nature Methods 13: 581–583.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carugati, L., C. Corinaldesi, A. Dell’Anno & R. Danovaro, 2015. Metagenetic tools for the census of marine meiofaunal biodiversity: an overview. Marine genomics 24: 11–20.

    Article  PubMed  Google Scholar 

  • Cesari, M., S. J. McInnes, R. Bertolani, L. Rebecchi & R. Guidetti, 2016. Genetic diversity and biogeography of the south polar water bear Acutuncus antarcticus (Eutardigrada: Hypsibiidae) – evidence that it is a truly pan-Antarctic species. Invertebrate Systematics 30: 635–649.

    Article  Google Scholar 

  • Chain, F. J. J., E. A. Brown, H. J. Macisaac & M. E. Cristescu, 2016. Metabarcoding reveals strong spatial structure and temporal turnover of zooplankton communities among marine and freshwater ports. Diversity and Distributions 22: 493–504.

    Article  Google Scholar 

  • Chariton, A. A., L. N. Court, D. M. Hartley, M. J. Colloff & C. M. Hardy, 2010. Ecological assessment of estuarine sediments by pyrosequencing eukaryotic ribosomal DNA. Frontiers in Ecology and the Environment 8: 233–238.

    Article  Google Scholar 

  • Chariton, A. A., K. T. Ho, D. Proestou, H. Bik, S. L. Simpson, L. M. Portis, M. G. Cantwell, J. G. Baguley, R. M. Burgess, M. M. Pelletier, M. Perron, C. Gunsch & R. A. Matthews, 2014. A molecular-based approach for examining responses of eukaryotes in microcosms to contaminant-spiked estuarine sediments. Environmental Toxicology and Chemistry 33: 359–369.

    Article  CAS  PubMed  Google Scholar 

  • Chariton, A. A., S. Stephenson, M. J. Morgan, A. D. L. Steven, M. J. Colloff, L. N. Court & C. M. Hardy, 2015. Metabarcoding of benthic eukaryote communities predicts the ecological condition of estuaries. Environmental Pollution 203: 165–174.

    Article  CAS  PubMed  Google Scholar 

  • Cieplinski, A., T. Weisse & U. Obertegger, 2017. High diversity in Keratella cochlearis (Rotifera, Monogononta): morphological and genetic evidence. Hydrobiologia 796: 145–159.

    Article  Google Scholar 

  • Cornils, A., 2014. Non-destructive DNA extraction for small pelagic copepods to perform integrative taxonomy. Journal of Plankton Research 37: 6–10.

    Article  CAS  Google Scholar 

  • Crawley, M. J., 2012. The R Book. Wiley, New York.

    Book  Google Scholar 

  • Creer, S., V. G. Fonseca, D. L. Porazinska, R. M. Giblin-Davis, W. Sung, D. M. Power, M. Packer, G. R. Carvalho, M. L. Blaxter, P. J. D. Lambshead & W. K. Thomas, 2010. Ultrasequencing of the meiofaunal biosphere: practice, pitfalls and promises. Molecular Ecology 19(Suppl 1): 4–20.

    Article  PubMed  Google Scholar 

  • Creer, S., K. Deiner, S. Frey, D. Porazinska, P. Taberlet, W. K. Thomas, C. Potter, H. M. Bik & R. Freckleton, 2016. The ecologist’s field guide to sequence-based identification of biodiversity. Methods in Ecology and Evolution 7: 1008–1018.

    Article  Google Scholar 

  • Curry, C. J., J. F. Gibson, S. Shokralla, M. Hajibabaei & D. J. Baird, 2018. Identifying North American freshwater invertebrates using DNA barcodes: are existing COI sequence libraries fit for purpose? Freshwater Science 37: 178–189.

    Article  Google Scholar 

  • Deagle, B. E., S. N. Jarman, E. Coissac, F. Pompanon & P. Taberlet, 2014. DNA metabarcoding and the cytochrome c oxidase subunit I marker: not a perfect match. Biology Letters 10: 1–4.

    Article  CAS  Google Scholar 

  • Deiner, K., E. A. Fronhofer, E. Mächler, J.-C. Walser & F. Altermatt, 2016. Environmental DNA reveals that rivers are conveyer belts of biodiversity information. Nature Communications 7: 1–9.

    Article  CAS  Google Scholar 

  • Dell’Anno, A., L. Carugati, C. Corinaldesi, G. Riccioni & R. Danovaro, 2015. Unveiling the biodiversity of deep-sea nematodes through metabarcoding: are we ready to bypass the classical taxonomy? PloS ONE 10: e0144928.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dellicour, S. & J. F. Flot, 2018. The hitchhiker’s guide to single-locus species delimitation. Molecular Ecology Resources 18: 1234–1246.

    Article  PubMed  Google Scholar 

  • Domaizon, I., A. Winegardner, E. Capo, J. Gauthier & I. Gregory-Eaves, 2017. DNA-based methods in paleolimnology: new opportunities for investigating long-term dynamics of lacustrine biodiversity. Journal of Paleolimnology 58: 1–21.

    Article  Google Scholar 

  • Epp, L. S., G. Gussarova, S. Boessenkool, J. Olsen, J. Haile, A. Schrøder-Nielsen, A. Ludikova, K. Hassel, H. K. Stenøien, S. Funder, E. Willerslev, K. Kjæer & C. Brochmann, 2015. Lake sediment multi-taxon DNA from North Greenland records early post-glacial appearance of vascular plants and accurately tracks environmental changes. Quaternary Science Reviews 117: 152–163.

    Article  Google Scholar 

  • Flot, J.-F., A. Couloux & S. Tillier, 2010. Haplowebs as a graphical tool for delimiting species: a revival of Doyle’s “field for recombination” approach and its application to the coral genus Pocillopora in Clipperton. BMC Evolutionary Biology 10: 372.

    Article  PubMed  PubMed Central  Google Scholar 

  • Flynn, J. M., E. A. Brown, F. J. J. Chain, H. J. Macisaac & M. E. Cristescu, 2015. Toward accurate molecular identification of species in complex environmental samples: testing the performance of sequence filtering and clustering methods. Ecology and Evolution 5: 2252–2266.

    Article  PubMed  PubMed Central  Google Scholar 

  • Fonseca, G., D. Fontaneto & M. Di Domenico, 2018. Addressing biodiversity shortfalls in meiofauna. Journal of Experimental Marine Biology and Ecology 502: 26–38.

    Article  Google Scholar 

  • Fontaneto, D., J. F. Flot & C. Q. Tang, 2015. Guidelines for DNA taxonomy, with a focus on the meiofauna. Marine Biodiversity 45: 433–451.

    Article  Google Scholar 

  • Fontaneto, D., E. M. Eckert, N. Anicic, E. Lara & E. A. Mitchell, 2019. We are ready for faunistic surveys of bdelloid rotifers through DNA barcoding: the example of Sphagnum bogs of the Swiss Jura Mountains. Limnetica 38: 213–225.

    Google Scholar 

  • Fraser, C. I., L. Connell, C. K. Lee & S. C. Cary, 2018. Evidence of plant and animal communities at exposed and subglacial (cave) geothermal sites in Antarctica. Polar Biology 41: 417–421.

    Article  Google Scholar 

  • Fujisawa, T. & T. G. Barraclough, 2013. Delimiting species using single-locus data and the Generalized Mixed Yule Coalescent approach: a revised method and evaluation on simulated data sets. Systematic Biology 62: 707–724.

    Article  PubMed  PubMed Central  Google Scholar 

  • Gardham, S., G. C. Hose, S. Stephenson & A. A. Chariton, 2014. DNA metabarcoding meets experimental ecotoxicology. In Woodward, G. (ed.), Big Data in Ecology. 1st ed. Advances in Ecological Research, Vol. 51. Elsevier AP, Amsterdam: 79–104.

  • Garraffoni, A. R., T. Q. Araújo, A. P. Lourenço, L. Guidi & M. Balsamo, 2017. A new genus and new species of freshwater Chaetonotidae (Gastrotricha: Chaetonotida) from Brazil with phylogenetic position inferred from nuclear and mitochondrial DNA sequences. Systematics and Biodiversity 15: 49–62.

    Article  Google Scholar 

  • Garraffoni, A. R., T. Q. Araújo, A. P. Lourenço, L. Guidi & M. Balsamo, 2019. Integrative taxonomy of a new Redudasys species (Gastrotricha: Macrodasyida) sheds light on the invasion of fresh water habitats by macrodasyids. Scientific Reports 9: 2067.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gąsiorek, P. & K. Vončina, 2019. New Echiniscidae (Heterotardigrada) from Amber Mountain (Northern Madagascar). Evolutionary Systematics 3: 29.

    Article  Google Scholar 

  • Geiger, M. F., J. J. Astrin, T. Borsch, U. Burkhardt, P. Grobe, R. Hand, A. Hausmann, K. Hohberg, L. Krogmann, M. Lutz, C. Monje, B. Misof, J. Moriniere, K. Muller, S. Pietsch, D. Quandt, B. Rulik, M. Scholler, W. Traunspurger, G. Haszprunar & W. Wagele, 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/National Research Council Canada: 1–10.

  • Gibson, J. F., S. Shokralla, C. Curry, D. J. Baird, W. A. Monk, I. King & M. Hajibabaei, 2015. Large-scale biomonitoring of remote and threatened ecosystems via high-throughput sequencing. PloS ONE 10: e0138432.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Giere, O., 2019. Perspectives in Meiobenthology: Reviews, Reflections and Conclusions. Springer, New York.

    Book  Google Scholar 

  • Guidetti, R., L. Rebecchi, M. Cesari & S. J. McInnes, 2014. Mopsechiniscus franciscae, a new species of a rare genus of Tardigrada from continental Antarctica. Polar Biology 37: 1221–1233.

    Article  Google Scholar 

  • Guidetti, R., M. Cesari, R. Bertolani, T. Altiero & L. Rebecchi, 2019. High diversity in species, reproductive modes and distribution within the Paramacrobiotus richtersi complex (Eutardigrada, Macrobiotidae). Zoological letters 5: 1.

    Article  PubMed  PubMed Central  Google Scholar 

  • Harzing, A.-W., 2007. Publish or perish. www.harzing.com/pop.htm

  • Hebert, P. D., A. Cywinska, S. L. Ball & J. R. Dewaard, 2003. Biological identifications through DNA barcodes. Proceedings of the Royal Society of London. Series B: Biological Sciences 270: 313–321.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hortal, J., F. de Bello, J. A. F. Diniz-Filho, T. M. Lewinsohn, J. M. Lobo & R. J. Ladle, 2015. Seven shortfalls that beset large-scale knowledge of biodiversity. Annual Review of Ecology, Evolution, and Systematics 46: 523–549.

    Article  Google Scholar 

  • Janssen, T., G. Karssen, V. Orlando, S. A. Subbotin & W. Bert, 2017. Molecular characterization and species delimiting of plant-parasitic nematodes of the genus Pratylenchus from the penetrans group (Nematoda: Pratylenchidae). Molecular Phylogenetics and Evolution 117: 30–48.

    Article  CAS  PubMed  Google Scholar 

  • Jaturapruek, R., D. Fontaneto, P. Meksuwan, P. Pholpunthin & S. Maiphae, 2018. Planktonic and periphytic bdelloid rotifers from Thailand reveal a species assemblage with a combination of cosmopolitan and tropical species. Systematics and Biodiversity 16: 128–141.

    Article  Google Scholar 

  • Ji, Y., L. Ashton, S. M. Pedley, D. P. Edwards, Y. Tang, A. Nakamura, R. Kitching, P. M. Dolman, P. Woodcock, F. A. Edwards & T. H. Larsen, 2013. Reliable, verifiable and efficient monitoring of biodiversity via metabarcoding. Ecology Letters 16: 1245–1257.

    Article  PubMed  Google Scholar 

  • Kaczmarek, Ł., K. Zawierucha, J. Buda, D. Stec, M. Gawlak, Ł. Michalczyk & M. Roszkowska, 2018. An integrative redescription of the nominal taxon for the Mesobiotus harmsworthi group (Tardigrada: Macrobiotidae) leads to descriptions of two new Mesobiotus species from Arctic. PloS ONE 13: e0204756.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kim, J., T. Kim & J. K. Park, 2016a. First report of Aphelenchoides bicaudatus (Nematoda: Aphelenchoididae) from South Korea. Animal Systematics, Evolution and Diversity 32: 253–257.

    Article  Google Scholar 

  • Kim, T., J. Kim, Y. J. Bae & J. K. Park, 2016b. First record of Acrobeloides nanus (Cephalobidae: Rhabditida: Nematoda) from Korea. Animal Systematics, Evolution and Diversity 32: 258–265.

    Article  Google Scholar 

  • Kim, J., T. Kim & J. K. Park, 2017a. Description of Pseudacrobeles (Pseudacrobeles) curvatus sp. n. (Cephalobidae: Rhabditida) in South Korea. Journal of Nematology 49: 162–167.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kim, T., J. Kim & J. K. Park, 2017b. Acrobeloides varius sp. n. (Rhabditida: Cephalobidae) from South Korea. Nematology 19: 489–496.

    Article  Google Scholar 

  • Kim, J., T. Kim, S. H. Ryu & J. K. Park, 2018. Prionchulus oleksandri (Nematoda: Mononchida) from Korea. Animal Systematics, Evolution and Diversity 34: 194–198.

    Google Scholar 

  • Koenders, A., I. Schön, S. Halse & K. Martens, 2016. Valve shape is not linked to genetic species in the Eucypris virens (Ostracoda, Crustacea) species complex. Zoological Journal of the Linnean Society 180: 36–46.

    Google Scholar 

  • Kolicka, M., M. Dabert, J. Dabert, T. Kånneby & J. Kisielewski, 2016. Bifidochaetus, a new Arctic genus of freshwater Chaetonotida (Gastrotricha) from Spitsbergen revealed by an integrative taxonomic approach. Invertebrate Systematics 30: 398–419.

    Article  Google Scholar 

  • Kolicka, M., P. Gadawski & M. Dabert, 2017. A new species of freshwater Chaetonotidae (Gastrotricha, Chaetonotida) from Obodska Cave (Montenegro) based on morphological and molecular characters. European Journal of Taxonomy 354: 1–30.

    Google Scholar 

  • Kordbacheh, A., G. Garbalena & E. J. Walsh, 2017. Population structure and cryptic species in the cosmopolitan rotifer Euchlanis dilatata. Zoological Journal of the Linnean Society 181: 757–777.

    Article  Google Scholar 

  • Kordbacheh, A., R. L. Wallace & E. J. Walsh, 2018. Evidence supporting cryptic species within two sessile microinvertebrates, Limnias melicerta and L. ceratophylli (Rotifera, Gnesiotrocha). PloS ONE 13: e0205203.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kordbacheh, A., A. N. Shapiro & E. J. Walsh, 2019. Reproductive isolation, morphological and ecological differentiation among cryptic species of Euchlanis dilatata, with the description of four new species. Hydrobiologia. https://doi.org/10.1007/s10750-019-3892-0.

    Article  Google Scholar 

  • Leese, F., A. Bouchez, K. Abarenkov, F. Altermatt, A. Borja, K. Bruce, T. Ekrem, F. Čiampor Jr., Z. Čiamporová-Zaovičová, F. O. Costa, S. Duarte, V. Elbrecht, D. Fontaneto, M. F. Geiger, D. Hering, M. Kahlert, B. Kalamujić Stroil, M. Kelly, E. Keskin, I. Liska, P. Mergen, K. Meissner, J. Pawlowski, L. Penev, Y. Reyjol, A. Rotter, D. Steinke, S. Vitecek, J. Zimmermann & A. M. Weigand, 2018. Why we need sustainable networks bridging countries, disciplines, cultures and generations for aquatic biomonitoring 2.0: a perspective derived from the DNAqua-Net COST Action. Advances in Ecological Research 58: 63–99.

    Article  Google Scholar 

  • Li, F., Y. Peng, W. Fang, F. Altermatt, Y. Xie, J. Yang & X. Zhang, 2018. Application of environmental DNA metabarcoding for predicting anthropogenic pollution in rivers. Environmental Science & Technology 52: 11708–11719.

    CAS  Google Scholar 

  • Lim, N. K. M., Y. C. Tay, A. Srivathsan, J. W. T. Tan, J. T. B. Kwik, B. Baloğlu, R. Meier & D. C. J. Yeo, 2016. Next-generation freshwater bioassessment: eDNA metabarcoding with a conserved metazoan primer reveals species-rich and reservoir-specific communities. Royal Society Open Science 3: 160635.

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu, L., M. Liu, D. M. Wilkinson, H. Chen, X. Yu & J. Yang, 2017. DNA metabarcoding reveals that 200-μm-size-fractionated filtering is unable to discriminate between planktonic microbial and large eukaryotes. Molecular Ecology Resources 17: 991–1002.

    Article  CAS  PubMed  Google Scholar 

  • Liu, P., L. Xu, S. L. Xu, A. Martínez, H. Chen, D. Cheng, H. J. Dumont, B. P. Han & D. Fontaneto, 2018. Species and hybrids in the genus Diaphanosoma Fischer, 1850 (Crustacea: Branchiopoda: Cladocera). Molecular Phylogenetics and Evolution 118: 369–378.

    Article  PubMed  Google Scholar 

  • Macheriotou L, Guilini K, Bezerra TN, Tytgat B, Nguyen DT, Nguyen TXP, Noppe F, Armenteros M, Boufahja F, Rigaux A, Vanreusel A, Derycke S (2019) Metabarcoding free‐living marine nematodes using curated 18S and CO1 reference sequence databases for species‐level taxonomic assignments. Ecology and Evolution 9:1211–1226

    Article  PubMed  PubMed Central  Google Scholar 

  • Machida, R. J. & N. Knowlton, 2012. PCR primers for metazoan nuclear 18S and 28S ribosomal DNA sequences. PloS ONE 7: e46180.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Machida, R. J., M. Leray, S.-L. Ho & N. Knowlton, 2017. Metazoan mitochondrial gene sequence reference datasets for taxonomic assignment of environmental samples. Scientific Data 4: 170027.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Malekzadeh-Viayeh, R., R. Pak-Tarmani, N. Rostamkhani & D. Fontaneto, 2014. Diversity of the rotifer Brachionus plicatilis species complex (Rotifera: Monogononta) in Iran through integrative taxonomy. Zoological Journal of the Linnean Society 170: 233–244.

    Article  Google Scholar 

  • Michaloudi, E., S. Mills, S. Papakostas, C. P. Stelzer, A. Triantafyllidis, I. Kappas, K. Vasileiadou, K. Proios & T. J. Abatzopoulos, 2017. Morphological and taxonomic demarcation of Brachionus asplanchnoidis Charin within the Brachionus plicatilis cryptic species complex (Rotifera, Monogononta). Hydrobiologia 796: 19–37.

    Article  Google Scholar 

  • Michaloudi, E., S. Papakostas, G. Stamou, V. Neděla, E. Tihlaříková, W. Zhang & S. A. Declerck, 2018. Reverse taxonomy applied to the Brachionus calyciflorus cryptic species complex: morphometric analysis confirms species delimitations revealed by molecular phylogenetic analysis and allows the (re) description of four species. PloS ONE 13: e0203168.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mills, S., J. A. Alcántara-Rodríguez, J. Ciros-Pérez, A. Gómez, A. Hagiwara, K. Hinson Galindo, C. D. Jersabek, R. Malekzadeh-Viayeh, F. Leasi, J.-S. Lee, D. B. M. Welch, S. Papakostas, S. Riss, H. Segers, M. Serra, R. Shiel, R. Smolak, T. W. Snell, C.-P. Stelzer, C. Q. Tang, R. L. Wallace, D. Fontaneto & E. J. Walsh, 2017. Fifteen species in one: deciphering the Brachionus plicatilis species complex (Rotifera, Monogononta) through DNA taxonomy. Hydrobiologia 796: 39–58.

    Article  CAS  Google Scholar 

  • Moreno, E., J. M. Conde-Porcuna & A. Gómez, 2017. Barcoding rotifer biodiversity in Mediterranean ponds using diapausing egg banks. Ecology and Evolution 7: 4855–4867.

    Article  PubMed  PubMed Central  Google Scholar 

  • Nguyen, T. D., T. M. L. Le, H. T. Nguyen, T. A. D. Nguyen, G. Liebanas & Q. P. Trinh, 2017. Morphological and molecular characteristics of Pratylenchus haiduongensis sp. n., a new species of root–lesion nematodes associated with carrot in Vietnam. Journal of Nematology 49: 276–285.

    PubMed  PubMed Central  Google Scholar 

  • Obertegger, U., G. Flaim & D. Fontaneto, 2014. Cryptic diversity within the rotifer Polyarthra dolichoptera along an altitudinal gradient. Freshwater Biology 59: 2413–2427.

    Article  Google Scholar 

  • Obertegger, U., A. Cieplinski, D. Fontaneto & S. Papakostas, 2018. Mitonuclear discordance as a confounding factor in the DNA taxonomy of monogonont rotifers. Zoologica Scripta 47: 122–132.

    Article  Google Scholar 

  • Olson, M., T. Harris, R. Higgins, P. Mullin, K. Powers, S. Olson & T. O. Powers, 2017. Species delimitation and description of Mesocriconema nebraskense n. sp. (Nematoda: Criconematidae), a morphologically cryptic, parthenogenetic species from North American Grasslands. Journal of Nematology 49: 42–66.

    Article  PubMed  PubMed Central  Google Scholar 

  • Papakostas, S., E. Michaloudi, K. Proios, M. Brehm, L. Verhage, J. Rota, C. Pena, G. Stamou, V. L. Pritchard, D. Fontaneto & S. A. Declerck, 2016. Integrative taxonomy recognizes evolutionary units despite widespread mitonuclear discordance: evidence from a rotifer cryptic species complex. Systematic Biology 65: 508–524.

    Article  PubMed  Google Scholar 

  • Pauls, S. U., M. Alp, M. Bálint, P. Bernabò, F. Čiampor, Z. Čiamporová-Zaťovičová, D. S. Finn, J. Kohout, F. Leese, V. Lencioni, I. Paz-Vinas & M. T. Monaghan, 2014. Integrating molecular tools into freshwater ecology: developments and opportunities. Freshwater Biology 59: 1559–1576.

    Article  Google Scholar 

  • Pawlowski, J., M. Kelly-Quinn, F. Altermatt, L. Apothéloz-Perret-Gentil, P. Beja, A. Boggero, A. Borja, A. Bouchez, T. Cordier, I. Domaizon, M. J. Feio, A. Filipa Filipe, R. Fornaroli, W. Graf, J. Herder, B. van der Hoorn, J. I. Jones, M. Sagova-Mareckova, C. Moritz, J. Barquín, J. J. Piggott, M. Pinna, F. Rimet, B. Rinkevich, C. Sousa-Santos, V. Specchia, R. Trobajo, V. Vasselon, S. Vitecek, J. Zimmerman, A. Weigand, F. Leese & M. Kahlert, 2018. The future of biotic indices in the ecogenomic era: integrating (e) DNA metabarcoding in biological assessment of aquatic ecosystems. Science of the Total Environment 637: 1295–1310.

    Article  PubMed  CAS  Google Scholar 

  • Pfenninger, M. & K. Schwenk, 2007. Cryptic animal species are homogeneously distributed among taxa and biogeographical regions. BMC Evolutionary Biology 7: 121.

    Article  PubMed  PubMed Central  Google Scholar 

  • Pires, A. C. & L. Marinoni, 2010. DNA barcoding and traditional taxonomy unified through Integrative Taxonomy: a view that challenges the debate questioning both methodologies. Biota Neotropica 10: 339–346.

    Article  Google Scholar 

  • Pompanon, F., B. E. Deagle, W. O. C. Symondson, D. S. Brown, S. N. Jarman & P. Taberlet, 2012. Who is eating what: diet assessment using next generation sequencing. Molecular Ecology 21: 1931–1950.

    Article  CAS  PubMed  Google Scholar 

  • Porazinska, D. L., R. M. Giblin-Davis, L. Faller, W. Farmerie, N. Kanzaki, K. Morris, T. O. Powers, A. E. Tucker, W. Sung & W. K. Thomas, 2009. Evaluating high-throughput sequencing as a method for metagenomic analysis of nematode diversity. Molecular Ecology Resources 9: 1439–1450.

    Article  CAS  PubMed  Google Scholar 

  • Porazinska, D. L., W. Sung, R. M. Giblin-Davis & W. K. Thomas, 2010. Reproducibility of read numbers in high-throughput sequencing analysis of nematode community composition and structure. Molecular Ecology Resources 10: 666–676.

    Article  CAS  PubMed  Google Scholar 

  • Puillandre, N., A. Lambert, S. Brouillet & G. Achaz, 2012a. ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Molecular Ecology 21: 1864–1877.

    Article  CAS  PubMed  Google Scholar 

  • Puillandre, N., M. V. Modica, Y. Zhang, L. Sirovich, M. C. Boisselier, C. Cruaud, M. Holford & S. Samadi, 2012b. Large-scale species delimitation method for hyperdiverse groups. Molecular Ecology 21: 2671–2691.

    Article  CAS  PubMed  Google Scholar 

  • Ratnasingham, S. & P. D. Hebert, 2007. BOLD: The Barcode of Life Data System (http://www.barcodinglife.org). Molecular Ecology Notes 7: 355–364.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruppert, K. M., R. J. Kline & M. S. Rahman, 2019. Past, present, and future perspectives of environmental DNA (eDNA) metabarcoding: a systematic review in methods, monitoring, and applications of global eDNA. Global Ecology and Conservation 17: e00547.

    Article  Google Scholar 

  • Schenk, J., W. Traunspurger & K. Ristau, 2016. Genetic diversity of widespread moss-dwelling nematode species in German beech forests. European Journal of Soil Biology 74: 23–31.

    Article  Google Scholar 

  • Schenk, J., K. Hohberg, J. Helder, K. Ristau & W. Traunspurger, 2017. The D3-D5 region of large subunit ribosomal DNA provides good resolution of German limnic and terrestrial nematode communities. Nematology 19: 821–837.

    Article  Google Scholar 

  • Schizas, N. V., G. T. Street, B. C. Coull, G. T. Chandler & J. M. Quattro, 1997. An efficient DNA extraction method for small metazoans. Molecular Marine Biology and Biotechnology 6: 381.

    CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Schön, I., S. Halse & K. Martens, 2017a. Cyprideis (Crustacea, Ostracoda) in Australia. Journal of Micropalaeontology 36: 31–37.

    Article  Google Scholar 

  • Schön, I., V. Pieri, D. Y. Sherbakov & K. Martens, 2017b. Cryptic diversity and speciation in endemic Cytherissa (Ostracoda, Crustacea) from Lake Baikal. Hydrobiologia 800: 61–79.

    Article  Google Scholar 

  • Schön, I., J. Higuti, T. Patel & K. Martens, 2018. Aquatic long-distance dispersal and vicariance shape the evolution of an ostracod species complex (Crustacea) in four major Brazilian floodplains. Molecular Phylogenetics and Evolution 121: 86–97.

    Article  PubMed  Google Scholar 

  • Shearn, R., I. Schön, K. Martens, S. A. Halse, J. Krawiec & A. Koenders, 2017. Patterns of genetic divergence in the Ilyodromus amplicolis lineage (Crustacea, Ostracoda), with descriptions of three new species. Zootaxa 4318: 1–46.

    Article  Google Scholar 

  • Simpson, G. G., 1961. Principles of Animal Taxonomy. Columbia University Press, New York: 247 pp.

  • Smith, D. P. & K. G. Peay, 2014. Sequence depth, not PCR replication, improves ecological inference from next generation DNA sequencing. PloS ONE 9: e90234.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Stec, D., W. Morek, P. Gąsiorek & Ł. Michalczyk, 2018. Unmasking hidden species diversity within the Ramazzottius oberhaeuseri complex, with an integrative redescription of the nominal species for the family Ramazzottiidae (Tardigrada: Eutardigrada: Parachela). Systematics and Biodiversity 16: 357–376.

    Article  Google Scholar 

  • Stefanni, S., D. Stanković, D. Borme, A. de Olazabal, T. Juretić, A. Pallavicini & V. Tirelli, 2018. Multi-marker metabarcoding approach to study mesozooplankton at basin scale. Scientific Reports 8: 12085.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Stoeckle, M. Y. & M. Stoeckle, 2003. Taxonomy, DNA, and the bar code of life. BioScience 35: 796–797.

    Article  Google Scholar 

  • Taberlet, P., E. Coissac, M. Hajibabaei & L. H. Rieseberg, 2012. Environmental DNA. Molecular Ecology 21: 1789–1793.

    Article  CAS  PubMed  Google Scholar 

  • Takemoto, S., K. Akita, N. Katayanagi, E. Urata, T. Ito, M. Saito & H. Okada, 2016. Continuous effects of winter flooding on soil fauna, as revealed by community structure of soil nematodes in a paddy field in northern Japan. Nematological Research (Japanese Journal of Nematology) 46: 45–58.

    Article  Google Scholar 

  • Tang, C. Q., F. Leasi, U. Obertegger, A. Kieneke, T. G. Barraclough & D. Fontaneto, 2012. The widely used small subunit 18S rDNA molecule greatly underestimates true diversity in biodiversity surveys of the meiofauna. Proceedings of the National Academy of Sciences of the United States of America 109: 16208–16212.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang, C. Q., U. Obertegger, D. Fontaneto & T. G. Barraclough, 2014. Sexual species are separated by larger genetic gaps than asexual species in rotifers. Evolution 68: 2901–2916.

    Article  PubMed  PubMed Central  Google Scholar 

  • Tautz, D., P. Arctander, A. Minelli, R. H. Thomas & A. P. Vogler, 2003. A plea for DNA taxonomy. Trends in Ecology and Evolution 18: 70–74.

    Article  Google Scholar 

  • Trebitz, A. S., J. C. Hoffman, G. W. Grant, T. M. Billehus & E. M. Pilgrim, 2015. Potential for DNA-based identification of Great Lakes fauna: match and mismatch between taxa inventories and DNA barcode libraries. Scientific Reports 5: 12162.

    Article  PubMed  PubMed Central  Google Scholar 

  • Trinh, Q. P., T. M. L. Le, T. D. Nguyen, H. T. Nguyen, G. Liebanas & T. A. D. Nguyen, 2018. Meloidogyne daklakensis n. sp. (Nematoda: Meloidogynidae), a new root-knot nematode associated with Robusta coffee (Coffea canephora Pierre ex A. Froehner) in the Western Highlands, Vietnam. Journal of Helminthology 93: 242–254.

    Article  PubMed  Google Scholar 

  • Vecchi, M., M. Cesari, R. Bertolani, K. I. Jönsson, L. Rebecchi & R. Guidetti, 2016. Integrative systematic studies on tardigrades from Antarctica identify new genera and new species within Macrobiotoidea and Echiniscoidea. Invertebrate Systematics 30: 303–322.

    Article  Google Scholar 

  • Velasco-Castrillón, A. & M. J. Stevens, 2014. Morphological and molecular diversity at a regional scale: a step closer to understanding Antarctic nematode biogeography. Soil Biology and Biochemistry 70: 272–284.

    Article  CAS  Google Scholar 

  • Velasco-Castrillón, A., T. J. Page, J. A. Gibson & M. I. Stevens, 2014. Surprisingly high levels of biodiversity and endemism amongst Antarctic rotifers uncovered with mitochondrial DNA. Biodiversity 15: 130–142.

    Article  Google Scholar 

  • Velasco-Castrillón, A., S. J. McInnes, M. B. Schultz, M. Arróniz-Crespo, C. A. D’Haese, J. A. E. Gibson, B. J. Adams, T. J. Page, A. D. Austin, S. J. B. Cooper & M. I. Stevens, 2015. Mitochondrial DNA analyses reveal widespread tardigrade diversity in Antarctica. Invertebrate Systematics 29: 578–590.

    Article  Google Scholar 

  • Velasco-Castrillón, A., I. Hawes & M. I. Stevens, 2018. 100 years on: a re-evaluation of the first discovery of microfauna from Ross Island, Antarctica. Antarctic Science 30: 209–219.

    Article  Google Scholar 

  • Vogler, A. P. & M. T. Monaghan, 2007. Recent advances in DNA taxonomy. Journal of Zoological Systematics and Evolutionary Research 45: 1–10.

    Article  Google Scholar 

  • Watson, N. T. N., I. C. Duggan & I. D. Hogg, 2015. Assessing the diversity of New Zealand freshwater harpacticoid copepods (Crustacea: Copepoda) using mitochondrial DNA (COI) barcodes. New Zealand Journal of Zoology 42: 57–67.

    Article  Google Scholar 

  • Wen, X., Y. Xi, G. Zhang, Y. Xue & X. Xiang, 2016. Coexistence of cryptic Brachionus calyciflorus (Rotifera) species: roles of environmental variables. Journal of Plankton Research 38: 478–489.

    Article  Google Scholar 

  • Weigand, A. M. & J.-N. Macher, 2018. A DNA metabarcoding protocol for hyporheic freshwater meiofauna: evaluating highly degenerate COI primers and replication strategy. Metabarcoding and Metagenomics 2: e26869.

    Article  Google Scholar 

  • Weigand, H., A. J. Beermann, F. Čiampor, F. O. Costa, Z. Csabai, S. Duarte, M. F. Geiger, M. Grabowski, F. Rimet, B. Rulik, M. Strand, N. Szucsich, A. M. Weigand, E. Willassen, S. A. Wyler, A. Bouchez, A. Borja, Z. Čiamporová-Zaťovičová, S. Ferreira, K.-D. B. Dijkstra, U. Eisendle, J. Freyhof, P. Gadawski, W. Graf, A. Haegerbaeumer, B. B. van der Hoorn, B. Japoshvili, L. Keresztes, E. Keskin, F. Leese, J. N. Macher, T. Mamos, G. Paz, V. Pešić, D. M. Pfannkuchen, M. A. Pfannkuchen, B. W. Price, B. Rinkevich, M. A. L. Teixeira, G. Várbíró & T. Ekrem, 2019. DNA barcode reference libraries for the monitoring of aquatic biota in Europe: gap-analysis and recommendations for future work. The Science of the total environment 678: 499–524.

    Article  CAS  PubMed  Google Scholar 

  • Willerslev, E., J. Davison, M. Moora, M. Zobel, E. Coissac, M. E. Edwards, E. D. Lorenzen, M. Vestergård, G. Gussarova, J. Haile, J. Craine, L. Gielly, S. Boessenkool, L. S. Epp, P. B. Pearman, R. Cheddadi, D. Murray, K. A. Bråthen, N. Yoccoz, H. Binney, C. Cruaud, P. Wincker, T. Goslar, I. G. Alsos, E. Bellemain, A. K. Brysting, R. Elven, J. H. Sønstebø, J. Murton, A. Sher, M. Rasmussen, R. Rønn, T. Mourier, A. Cooper, J. Austin, P. Möller, D. Froese, G. Zazula, F. Pompanon, D. Rioux, V. Niderkorn, A. Tikhonov, G. Savvinov, R. G. Roberts, R. D. E. MacPhee, M. T. P. Gilbert, K. H. Kjær, L. Orlando, C. Brochmann & P. Taberlet, 2014. Fifty thousand years of Arctic vegetation and megafaunal diet. Nature 506: 47–51.

    Article  CAS  PubMed  Google Scholar 

  • Wilson, J. J., K.-W. Sing, R. M. Floyd & P. D.N. Hebert, 2017. DNA barcodes and insect biodiversity. In Insect Biodiversity: Science and Society: 575–592.

  • Xiang, X., R. Jiang, Y. Tao, Y. Chen & Y. Xi, 2016. Differences in life history characteristics among three sympatric evolutionary species of the Rotaria rotatoria complex. Journal of Freshwater Ecology 31: 351–360.

    Article  CAS  Google Scholar 

  • Xiang, X. L., Y. L. Xi, X. L. Wen & Y. L. Ge, 2017. Molecular phylogeny and population genetic differentiation patterns in Brachionus calyciflorus Pallas (Rotifera) complex from two lakes in China. Annales de Limnologie – International Journal of Limnology 53: 401–410.

    Article  Google Scholar 

  • Yang, Z. & B. Rannala, 2014. Unguided species delimitation using DNA sequence data from multiple loci. Molecular Biology and Evolution 31: 3125–3135.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang, J., X. Zhang, Y. Xie, C. Song, Y. Zhang, H. Yu & G. A. Burton, 2017. Zooplankton community profiling in a eutrophic freshwater ecosystem-lake tai basin by DNA metabarcoding. Scientific Reports 7: 1773.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zawierucha, K., D. Stec, D. Lachowska-Cierlik, N. Takeuchi, Z. Li & Ł. Michalczyk, 2018. High mitochondrial diversity in a new water bear species (Tardigrada: Eutardigrada) from mountain glaciers in central Asia, with the erection of a new genus Cryoconicus. Annales Zoologici 68: 179–202.

    Article  Google Scholar 

  • Zhan, A., M. Hulák, F. Sylvester, X. Huang, A. A. Adebayo, C. L. Abbott, S. J. Adamowicz, D. D. Heath, M. E. Cristescu & H. J. Macisaac, 2013. High sensitivity of 454 pyrosequencing for detection of rare species in aquatic communities. Methods in Ecology and Evolution 4: 558–565.

    Article  Google Scholar 

  • Zhan, A., S. A. Bailey, D. D. Heath & H. J. Macisaac, 2014. Performance comparison of genetic markers for high-throughput sequencing-based biodiversity assessment in complex communities. Molecular Ecology Resources 14: 1049–1059.

    CAS  PubMed  Google Scholar 

  • Zhang, J., P. Kapli, P. Pavlidis & A. Stamatakis, 2013. A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29: 2869–2876.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, G. K., F. J. J. Chain, C. L. Abbott & M. E. Cristescu, 2018. Metabarcoding using multiplexed markers increases species detection in complex zooplankton communities. Evolutionary Applications 11: 1901–1914.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Janina Schenk.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Guest editors: Nabil Majdi, Jenny M. Schmid-Araya & Walter Traunspurger / Patterns and Processes of Meiofauna in Freshwater Ecosystems

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 37 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Schenk, J., Fontaneto, D. Biodiversity analyses in freshwater meiofauna through DNA sequence data. Hydrobiologia 847, 2597–2611 (2020). https://doi.org/10.1007/s10750-019-04067-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-019-04067-2

Keywords

Navigation