Skip to main content

RETRACTED ARTICLE: Molecular taxonomic tools provide more accurate estimates of species richness at less cost than traditional morphology-based taxonomic practices in a vegetation survey

Biodiversity and Conservation volume 23, pages 1411–1424 (2014)Cite this article

This article was retracted on 27 October 2021

This article has been updated

Abstract

Vegetation surveys are conducted to obtain a catalogue of the plant species that occupy an area of interest, and are used to inform the decisions of policymakers about conservation, development, and remediation efforts. Currently, vegetation surveys rely on traditional morphology-based taxonomic practices to identify collected specimens. By implementing recent advances in molecular taxonomy, it may be possible to improve upon these methods and reduce the associated costs. In this study, we used both morphological and molecular taxonomic methods to sample 337 forest vegetation plots in northeastern Ontario, Canada. DNA barcoding—a molecular taxonomic tool—was used to identify specimens collected in the molecular taxonomic survey. The molecular taxonomic survey identified a mean of 12.4 species per plot and 202 species in total, whereas the morphological taxonomic survey identified a mean of 9.8 species per plot and 142 species in total; both surveys provided identical estimates of community similarity. The morphological taxonomic survey was 37 % more expensive than molecular taxonomic survey, owing largely to the increased time required in the field to collect specimens that flowered at different times. Our results indicate that molecular taxonomic tools are more cost-effective than traditional morphology-based taxonomic practices for species identification in vegetation surveys. Taxonomy underpins all conservation, and the implementation of molecular taxonomic tools for vegetation surveys has promise to lessen the consequences of the taxonomic impediment and increase the effectiveness of conservation efforts.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

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

Fig. 1
Fig. 2

Change history

  • 08 September 2021

    Editor’s Note: Readers are alerted that the reliability of data presented in this manuscript is currently in question. Appropriate editorial action will be taken once this matter is resolved.

  • 27 October 2021

    This article has been retracted. Please see the Retraction Notice for more detail: https://doi.org/10.1007/s10531-021-02316-2

References

  • Archaux F (2009) Could we obtain better estimates of plot species richness from multiple-observer plant censuses? J Veg Sci 20:603–611

    Google Scholar 

  • Austin MP, Heyligers PC (1989) Vegetation survey design for conservation: gradsect sampling of forests in North-eastern New South Wales. Biol Conserv 50:13–32

    Google Scholar 

  • Balmford A, Gaston KJ, Rodrigues ASL, James A (2000) Integrating costs of conservation into international priority setting. Conserv Biol 14:597–605

    Google Scholar 

  • Beanlands GE, Duinker PN (1983) An ecological framework for environmental impact assessment in Canada. Institute for Resource and Environmental Studies, Dalhousie

    Google Scholar 

  • Begerow D, Nilsson H, Unterseher M, Maier W (2010) Current state and perspectives of fungal DNA barcoding and rapid identification procedures. Appl Microbiol Biotechnol 87:99–108

    CAS  PubMed  Google Scholar 

  • Bell F, Parton J, Stocker N, Joyce D (2008) Developing a silvicultural framework and definitions for use in forest management planning and practice. Forest Chron 84:678–693

    Google Scholar 

  • Campbell JB (1959) Flowering sequence of a local flora. J Range Manag 12:127–132

    Google Scholar 

  • CBOL Plant Working Group (2009) A DNA barcode for land plants. Proc Natl Acad Sci USA 106:12794–12797

    PubMed Central  Google Scholar 

  • Chase M, Fay M, Devey D et al (2006) Multigene analyses of monocot relationships: a summary. Aliso 22:62–74

    Google Scholar 

  • Chen S, Yao H, Han J et al (2010) Validation of the ITS2 region as a novel DNA barcode for identifying medicinal plant species. PLoS ONE 5:e8613

    PubMed  PubMed Central  Google Scholar 

  • Claridge MF, Dawah HA, Wilson MR (1997) Species: The units of biodiversity. Chapman & Hall, London

    Google Scholar 

  • Core Team R (2013) R: a language and environment for statistical computing. Austria, Vienna

    Google Scholar 

  • Costa GC, Nogueira C, Machado RB, Colli GR (2010) Sampling bias and the use of ecological niche modeling in conservation planning: a field evaluation in a biodiversity hotspot. Biodivers Conserv 19:883–899

    Google Scholar 

  • Curtis JT (1959) The vegetation of Wisconsin: an ordination of plant communities. University of Wisconsin Press, Madison

    Google Scholar 

  • de Boer HJ, Ouarghidi A, Martin G et al (2014) DNA barcoding reveals limited accuracy of identifications based on folk taxonomy. PLoS ONE 9:e84291

    PubMed  PubMed Central  Google Scholar 

  • de Carvalho MR, Bockmann FA, Amorim DS et al (2005) Revisiting the taxonomic impediment. Science 307:353

    PubMed  Google Scholar 

  • de Mattia F, Gentili R, Bruni I et al (2012) A multi-marker DNA barcoding approach to save time and resources in vegetation surveys. Bot J Linn Soc 169:518–529

    Google Scholar 

  • Dubois A (2003) The relationships between taxonomy and conservation biology in the century of extinctions. C R Biol 326:9–21

    Google Scholar 

  • Ensing DJ, Moffat CE, Pither J (2012) Taxonomic identification errors generate misleading ecological niche model predictions of an invasive hawkweed. Botany 91:137–147

    Google Scholar 

  • Fazekas AJ, Burgess KS, Kesanakurti PR et al (2008) Multiple multilocus DNA barcodes from the plastid genome discriminate plant species equally well. PLoS ONE 3:e2802

    PubMed  PubMed Central  Google Scholar 

  • Fazekas AJ, Kuzmina ML, Newmaster SG, Hollingsworth PM (2012) DNA barcoding methods for land plants. In: Kress WJ, Erickson (ed) DNA barcodes: methods and protocols. Methods Mol Bol 853:223–252

  • Frézal L, Leblois R (2008) Four years of DNA barcoding: current advances and prospects. Infect Genet Evol 8:727–736

    PubMed  Google Scholar 

  • García-Robledo C, Erickson DL, Staines CL et al (2013) Tropical plant-herbivore networks: reconstructing species interactions using DNA barcodes. PLoS ONE 8:e52967

    PubMed  PubMed Central  Google Scholar 

  • Ghahramanzadeh R, Esselink G, Kodde LP et al (2013) Efficient distinction of invasive aquatic plant species from non-invasive related species using DNA barcoding. Mol Ecol Resour 13:21–31

    CAS  PubMed  Google Scholar 

  • Gonzalez MA, Baraloto C, Engel J et al (2009) Identification of Amazonian trees with DNA barcodes. PLoS ONE 4:e7483

    PubMed  PubMed Central  Google Scholar 

  • Gotelli NJ, Colwell RK (2001) Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol Lett 4:379–391

    Google Scholar 

  • Gurevitch J, Padilla DK (2004) Are invasive species a major cause of extinctions? Trends Ecol Evol 19:470–474

    PubMed  Google Scholar 

  • Hajibabaei M, Shokralla S, Zhou X et al (2011) Environmental barcoding: a next-generation sequencing approach for biomonitoring applications using river benthos. PLoS ONE 6:e17497

    CAS  PubMed  PubMed Central  Google Scholar 

  • Harrell Jr FE, Dupont MC (2012) Hmisc: Harrell miscellaneous. R package version 3.10-1. [http://CRAN.R-project.org/package=Hmisc]

  • Hebert PDN, Gregory TR (2005) The promise of DNA barcoding for taxonomy. Syst Biol 54:852–859

    PubMed  Google Scholar 

  • Hebert PDN, Cywinska A, Ball SL (2003) Biological identifications through DNA barcodes. Proc R Soc London Series B Biol Sci 270:313–321

    CAS  Google Scholar 

  • Hill SR (2003) Conservation assessment for Barren strawberry (Waldsteinia fragarioides ssp. fragarioides). United States Forest Service, Washington, DC

    Google Scholar 

  • Hill MO, Gauch HG (1980) Detrended correspondence analysis: an improved ordination technique. Vegetatio 42:47–58

    Google Scholar 

  • Ivanova NV, Grainger C (2006) Pre-made frozen PCR and sequencing plates. [www.dnabarcoding.ca/CCDB_DOCS/CCDB_Advances_Methods_Release_No4_Dec1st_2006.pdf]

  • Ivanova NV, DeWaard JR, Hajibabaei M, Hebert PDN (2005) Protocols for high volume DNA barcoding; [http://www.dnabarcoding.ca/]

  • Ivanova NV, Fazekas AJ, Hebert PDN (2008) Semi-automated, membrane-based protocol for DNA isolation from plants. Plant Mol Biol Rep 26:186–198

    CAS  Google Scholar 

  • Ivanova NV, Kuzmina ML, Fazekas AJ (2011) CCDB Protocols. Manual protocol employing centrifugation: Glass fiber plate DNA extraction protocol for plants, fungi, echinoderms, and mollusks. [http://www.ccdb.ca/CCDB_DOCS/CCDB_DNA_Extraction-Plants.pdf]

  • Jongman RHG, ter Braak CJF, Van Tongeren OFR (1995) Data analysis in community and landscape ecology. Cambridge University Press, Cambridge

    Google Scholar 

  • Kesanakurti PR, Fazekas AJ, Burgess KS et al (2011) Spatial patterns of plant diversity below-ground as revealed by DNA barcoding. Mol Ecol 20:1289–1302

    PubMed  Google Scholar 

  • Kool A, de Boer HJ, Krüger Å et al (2012) Molecular identification of commercialized medicinal plants in southern Morocco. PLoS ONE 7:e39459

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kress WJ, Erickson DL (2007) A two-locus global DNA barcode for land plants: the coding rbcL gene complements the non-coding trnH-psbA spacer region. PLoS ONE 2:e508

    PubMed  PubMed Central  Google Scholar 

  • Kress WJ, Wurdack KJ, Zimmer EA et al (2005) Use of DNA barcodes to identify flowering plants. Proc Natl Acad Sci USA 102:8369–8374

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kress WJ, Erickson DL, Jones FA et al (2009) Plant DNA barcodes and a community phylogeny of a tropical forest dynamics plot in Panama. Proc Natl Acad Sci USA 106:18621–18626

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kress WJ, Erickson DL, Swenson NG et al (2010) Advances in the use of DNA barcodes to build a community phylogeny for tropical trees in a Puerto Rican forest dynamics plot. PLoS ONE 5:e15409

    PubMed  PubMed Central  Google Scholar 

  • Kuzmina ML, Ivanova NV (2011a) PCR amplification for plants and fungi. [http://www.ccdb.ca/CCDB_DOCS/CCDB_Amplification-Plants.pdf]

  • Kuzmina ML, Ivanova NV (2011b) CCDB Protocols. [http://www.ccdb.ca/CCDB_DOCS/CCDB_PrimerSets-Plants.pdf]

  • Kuzmina ML, Johnson KL, Barron HR, Hebert PDN (2012) Identification of the vascular plants of Churchill, Manitoba, using a DNA barcode library. BMC Ecol 12:25

    CAS  PubMed  PubMed Central  Google Scholar 

  • Laiou A, Mandolini LA, Piredda R et al (2013) DNA barcoding as a complementary tool for conservation and valorisation of forest resources. Zookeys 213:197–213

    Google Scholar 

  • Lawrence DP (2003) Environmental impact assessment. Wiley & Sons, Hoboken

    Google Scholar 

  • Lepš J, Hadincová V (1992) How reliable are our vegetation analyses? J Veg Sci 3:119–124

    Google Scholar 

  • Levin RA, Wagner WL, Hoch PC et al (2003) Family-level relationships of Onagraceae based on chloroplast rbcL and ndhF data. Am J Bot 90:107–115

    CAS  PubMed  Google Scholar 

  • Li D-Z, Gao L-M, Li H-T et al (2011) Comparative analysis of a large dataset indicates that internal transcribed spacer (ITS) should be incorporated into the core barcode for seed plants. Proc Natl Acad Sci 108:19641–19646

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li CP, Yu ZG, Han GS, Chu KH (2012a) Analyzing multi-locus plant barcoding datasets with a composition vector method based on adjustable weighted distance. PLoS ONE 7:e42154

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li H-Q, Chen J-Y, Wang S, Xiong S-Z (2012b) Evaluation of six candidate DNA barcoding loci in Ficus (Moraceae) of China. Mol Ecol Resour 12:783–790

    CAS  PubMed  Google Scholar 

  • Liu Z, Zeng X, Yang D et al (2012) Identification of medicinal vines by ITS2 using complementary discrimination methods. J Ethnopharmacol 141:242–249

    PubMed  Google Scholar 

  • Mace GM (2004) The role of taxonomy in species conservation. Philos Trans R Soc Lond B Biol Sci 359:711–719

    PubMed  PubMed Central  Google Scholar 

  • Margules CR, Austin MP, Mollison D, Smith F (1994) Biological models for monitoring species decline: the construction and use of data bases [and discussion]. Philos Trans R Soc London Series B Biol Sci 344:69–75

    Google Scholar 

  • McCune B, Dey JP, Peck JE et al (1997) Repeatability of community data: species richness versus gradient scores in large-scale lichen studies. Bryologist 100:40–46

    Google Scholar 

  • Murdoch W, Polasky S, Wilson KA et al (2007) Maximizing return on investment in conservation. Biol Conserv 139:375–388

    Google Scholar 

  • Newmaster SG, Ragupathy S (2013) Flora Ontario Integrated Botanical Information System (FOIBIS). BIO/OAC Herbarium, Biodiversity Institute of Ontario, Guelph. [http://www.uoguelph.ca/foibis]

  • Newmaster SG, Fazekas AJ, Ragupathy S (2006) DNA barcoding in land plants: evaluation of rbcL in a multigene tiered approach. Botany 341:335–341

    Google Scholar 

  • Newmaster SG, Fazekas AJ, Steeves RAD, Janovec J (2008) Testing candidate plant barcode regions in the Myristicaceae. Mol Ecol Resour 8:480–490

    CAS  PubMed  Google Scholar 

  • Newmaster SG, Ragupathy S, Dhivya S et al (2013a) Genomic valorization of the fine scale classification of small millet landraces in southern India. Genome 56:123–127

    CAS  PubMed  Google Scholar 

  • Newmaster SG, Grguric M, Shanmughanandhan D et al (2013b) DNA barcoding detects contamination and substitution in North American herbal products. BMC Med 11:222

    PubMed  PubMed Central  Google Scholar 

  • Prendergast JR, Quinn RM, Lawton JH et al (1993) Rare species, the coincidence of diversity hotspots and conservation strategies. Nature 365:335–337

    Google Scholar 

  • Ratnasingham S, Hebert PDN (2007) BOLD: The barcode of life data system. Mol Ecol Notes 7:355–364. http://www.boldsystems.org

    CAS  PubMed  PubMed Central  Google Scholar 

  • Resh V, Unzicker J (1975) Water quality monitoring and aquatic organisms: the importance of species identification. Water Pollut Control Fed 47:9–19

    CAS  Google Scholar 

  • Sandionigi A, Galimberti A, Labra M et al (2012) Analytical approaches for DNA barcoding data-how to find a way for plants? Plant Biosyst 146:803–813

    Google Scholar 

  • Schemske DW, Husband BC, Ruckelshaus MH et al (1994) Evaluating approaches to the conservation of rare and endangered plants. Ecology 75:584–606

    Google Scholar 

  • Schuster SC (2008) Next-generation sequencing transforms today’s biology. Nat Methods 5:16–18

    CAS  PubMed  Google Scholar 

  • Scott WA, Hallam CJ (2003) Assessing species misidentification rates through quality assurance of vegetation monitoring. Plant Ecol 165:101–115

    Google Scholar 

  • Su JC, Debinski DM, Jakubauskas ME, Kindscher K (2004) Beyond species richness: community similarity as a measure of cross-taxon congruence for coarse-filter conservation. Conserv Biol 18:167–173

    Google Scholar 

  • Tautz D, Arctander P, Minelli A et al (2003) A plea for DNA taxonomy. Trends Ecol Evol 18:70–74

    Google Scholar 

  • ter Braak CJF (1986) Canonical correspondence analysis: a new eigenvector technique for multivariate direct gradient analysis. Ecology 67:1167–1179

    Google Scholar 

  • Ter Braak, CJF, Smilauer P (2012) CANOCO reference manual and CanoDraw for Windows user’s guide: software for canonical community ordination (version 5.0). Microcomputer Power, Ithaca

  • Thomas CD, Cameron A, Green RE et al (2004) Extinction risk from climate change. Nature 427:145–148

    CAS  PubMed  Google Scholar 

  • Vences M, Thomas M, van der Meijden A et al (2005) Comparative performance of the 16S rRNA gene in DNA barcoding of amphibians. Front Zool 2:5

    PubMed  PubMed Central  Google Scholar 

  • von Cräutlein M, Korpelainen H, Pietiläinen M, Rikkinen J (2011) DNA barcoding: a tool for improved taxon identification and detection of species diversity. Biodivers Conserv 20:373–389

    Google Scholar 

  • Yao H, Song J, Liu C et al (2010) Use of ITS2 region as the universal DNA barcode for plants and animals. PLoS ONE 5:e13102

    PubMed  PubMed Central  Google Scholar 

  • Zhang C-Y, Wang F-Y, Yan H-F et al (2012) Testing DNA barcoding in closely related groups of Lysimachia L. (Myrsinaceae). Mol Ecol Resour 12:98–108

    PubMed  Google Scholar 

Download references

Acknowledgments

The authors thank W. Bell and the Ontario Forest Research Institute for assistance with fieldwork, N. Webster for assistance with morphology-based specimen identification, and S. Ragupathy for assistance with DNA barcoding. SGN was supported with Grants from NSERC CRD, OMNR, Forest Ecosystem Co-op, and the Forest Research Partnership.

Author information

Authors and Affiliations

  1. Department of Integrative Biology, University of Guelph, Guelph, ON, N1G 2W1, Canada

    Ken A. Thompson & Steven G. Newmaster

Authors
  1. Ken A. Thompson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Steven G. Newmaster
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ken A. Thompson.

Additional information

Communicated by Dirk Sven Schmeller.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Thompson, K.A., Newmaster, S.G. RETRACTED ARTICLE: Molecular taxonomic tools provide more accurate estimates of species richness at less cost than traditional morphology-based taxonomic practices in a vegetation survey. Biodivers Conserv 23, 1411–1424 (2014). https://doi.org/10.1007/s10531-014-0672-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10531-014-0672-z

Keywords

  • Community inventory
  • DNA barcoding
  • DNA taxonomy
  • Ecological survey
  • Environmental impact assessment
  • Plant identification