Skip to main content

Advertisement

SpringerLink
Log in

Applications of environmental DNA (eDNA) in ecology and conservation: opportunities, challenges and prospects

  • Review Paper
  • Published:
Biodiversity and Conservation Aims and scope Submit manuscript

Abstract

Conserving biodiversity in the face of ever-increasing human pressure is hampered by our lack of basic information on species occurrence, distribution, abundance, habitat requirements, and threats. Obtaining this information requires efficient and sensitive methods capable of detecting and quantifying true occurrence and diversity, including rare, cryptic and elusive species. Environmental DNA (eDNA) is an emerging technique that can increase our ability to detect and quantify biodiversity, by overcoming some of the challenges of labor-intensive traditional surveys. The application of eDNA in ecology and conservation has grown enormously in recent years, but without a concurrent growth in appreciation of its strengths and limitations. In many situations, eDNA may either not work, or it may work but not provide the information needed. Problems with (1) imperfect detection, (2) abundance quantification, (3) taxonomic assignment, (4) eDNA spatial and temporal dynamics, (5) data analysis and interpretation, and (6) assessing ecological status have all been significant. The technique has often been used without a careful evaluation of the technical challenges and complexities involved, and a determination made that eDNA is the appropriate method for the species or environment of interest. It is therefore important to evaluate the scope and relevance of eDNA-based studies, and to identify critical considerations that need to be taken into account before using the approach. We review and synthesize eDNA studies published to date to highlight the opportunities and limitations of utilizing eDNA in ecology and conservation. We identify potential ways of reducing limitations in eDNA analysis, and demonstrate how eDNA and traditional surveys can complement each other.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Aas AB, Davey ML, Kauserud H (2017) ITS all right mama: investigating the formation of chimeric sequences in the ITS2 region by DNA metabarcoding analyses of fungal mock communities of different complexities. Mol Ecol Resour 17:730–741

    Google Scholar 

  • Akamatsu Y, Kume G, Gotou M, Kono T, Fujii T, Inui R et al (2020) Using environmental DNA analyses to assess the occurrence and abundance of the endangered amphidromous fish Plecoglossus altivelis ryukyuensis. Biodivers Data J 8:e39679

    PubMed  PubMed Central  Google Scholar 

  • Akre TS, Parker LD, Ruther E, Maldonado JE, Lemmon L, Mclnerney NR (2019) Concurrent visual encounter sampling validates eDNA selectivity and sensitivity for the endangered wood turtle (Glyptemys insculpta). PLoS ONE 14:e0215586

    CAS  PubMed  PubMed Central  Google Scholar 

  • Alberdi A, Aizpurua O, Gilbert MTP, Bohmann K (2018) Scrutinizing key steps for reliable metabarcoding of environmental samples. Methods Ecol Evol 9:134–147

    Google Scholar 

  • Alexander JB, Bunce M, White N, Wilkinson SP, Adam AAS, Berry T et al (2020) Development of a multi-assay approach for monitoring coral diversity using eDNA metabarcoding. Coral Reefs 39:159–171

    Google Scholar 

  • Amberg JJ, Merkes CM, Stott W, Rees CB, Erickson RA (2019) Environmental DNA as a tool to help inform zebra mussel, Dreissena polymorpha, management in inland lakes. Manag Biol Invasion 10:96–110

    Google Scholar 

  • Amend AS, Seifert KA, Bruns TD (2010) Quantifying microbial communities with 454 pyrosequencing: does read abundance count? Mol Ecol 19:5555–5565

    CAS  PubMed  Google Scholar 

  • Andersen K, Bird KL, Rasmussen M, Haile J, Breuning-Madsen H, Kjaer KH et al (2012) Meta-barcoding of 'dirt' DNA from soil reflects vertebrate biodiversity. Mol Ecol 21:1966–1979

    CAS  PubMed  Google Scholar 

  • Andruszkiewicz EA, Starks HA, Chavez FP, Sassoubre LM, Block BA, Boehm AB (2017) Biomonitoring of marine vertebrates in Monterey Bay using eDNA metabarcoding. PLoS ONE 12:e0176343–e0176343

    PubMed  PubMed Central  Google Scholar 

  • Anglès d’Auriac MB, Strand DA, Mjelde M, Demars BOL, Thaulow J (2019) Detection of an invasive aquatic plant in natural water bodies using environmental DNA. PLoS ONE 14:e0219700

    PubMed  PubMed Central  Google Scholar 

  • Antognazza CM, Britton JR, Potter C, Franklin E, Hardouin EA, Gutmann Roberts C et al (2019) Environmental DNA as a non-invasive sampling tool to detect the spawning distribution of European anadromous shads (Alosa spp.). Aquat Conserv Mar Freshw Ecosys 29:148–152

    Google Scholar 

  • Ardura A (2019) Species-specific markers for early detection of marine invertebrate invaders through eDNA methods: Gaps and priorities in GenBank as database example. J Nat Conserv 47:51–57

    Google Scholar 

  • Bailey LL, Jones P, Thompson KG, Foutz HP, Logan JM, Wright FB et al (2019) Determining presence of rare amphibian species: testing and combining novel survey methods. J Herpetol 53:115–124

    Google Scholar 

  • Bakker J, Wangensteen OS, Baillie C, Buddo D, Chapman DD, Gallagher AJ et al (2019) Biodiversity assessment of tropical shelf eukaryotic communities via pelagic eDNA metabarcoding. Ecol Evol 9:14341–14355

    PubMed  PubMed Central  Google Scholar 

  • Balasingham KD, Walter RP, Heath DD (2017) Residual eDNA detection sensitivity assessed by quantitative real-time PCR in a river ecosystem. Mol Ecol Resour 17:523–532

    CAS  PubMed  Google Scholar 

  • Baldigo BP, Sporn LA, George SD, Ball JA (2017) Efficacy of environmental DNA to detect and quantify Brook Trout populations in headwater streams of the Adirondack Mountains, New York. T Am Fish Soc 146:99–111

    CAS  Google Scholar 

  • Barnes MA, Turner CR (2016) The ecology of environmental DNA and implications for conservation genetics. Conserv Genet 17:1–17

    CAS  Google Scholar 

  • Barnes MA, Turner CR, Jerde CL, Renshaw MA, Chadderton WL, Lodge DM (2014) Environmental conditions influence eDNA persistence in aquatic systems. Environ Sci Technol 48:1819–1827

    CAS  PubMed  Google Scholar 

  • Basset Y, Cizek L, Cuénoud P, Didham RK, Guilhaumon F, Missa O et al (2012) Arthropod diversity in a tropical forest. Science 338:1481–1484

    CAS  PubMed  Google Scholar 

  • Beauclerc K, Wozney K, Smith C, Wilson C (2019) Development of quantitative PCR primers and probes for environmental DNA detection of amphibians in Ontario. Conserv Genet Resour 11:43–46

    Google Scholar 

  • Bedwell ME, Goldberg CS (2020) Spatial and temporal patterns of environmental DNA detection to inform sampling protocols in lentic and lotic systems. Ecol Evol 10(3):1602–1612

    PubMed  PubMed Central  Google Scholar 

  • Bienert F, De Danieli S, Miquel C, Coissac E, Poillot C, Brun JJ et al (2012) Tracking earthworm communities from soil DNA. Mol Ecol 21:2017–2030

    CAS  PubMed  Google Scholar 

  • Biggs J, Ewald N, Valentini A, Gaboriaud C, Dejean T, Griffiths RA et al (2015) Using eDNA to develop a national citizen science-based monitoring programme for the great crested newt (Triturus cristatus). Biol Conserv 183:19–28

    Google Scholar 

  • Bista I, Carvalho GR, Tang M, Walsh K, Zhou X, Hajibabaei M et al (2018) Performance of amplicon and shotgun sequencing for accurate biomass estimation in invertebrate community samples. Mol Ecol Resour 18:1020–1034

    CAS  Google Scholar 

  • Bista I, Carvalho GR, Walsh K, Seymour M, Hajibabaei M, Lallias D et al (2017) Annual time-series analysis of aqueous eDNA reveals ecologically relevant dynamics of lake ecosystem biodiversity. Nat Commun 8:14087

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bracken FSA, Rooney SM, Kelly-Quinn M, King JJ, Carlsson J (2019) Identifying spawning sites and other critical habitat in lotic systems using eDNA "snapshots": a case study using the sea lamprey Petromyzon marinus L. Ecol Evol 9:553–567

    PubMed  Google Scholar 

  • Brannock PM, Halanych KM (2015) Meiofaunal community analysis by high-throughput sequencing: comparison of extraction, quality filtering, and clustering methods. Mar Genom 23:67–75

    Google Scholar 

  • Burivalova Z, Game ET, Butler RA (2019) The sound of a tropical forest. Science 363:28–29

    CAS  PubMed  Google Scholar 

  • Buxton AS, Groombridge JJ, Zakaria NB, Griffiths RA (2017) Seasonal variation in environmental DNA in relation to population size and environmental factors. Sci Rep 7:1–9

    Google Scholar 

  • Bylemans J, Furlan EM, Gleeson DM, Hardy CM, Duncan RP (2018) Does size matter? an experimental evaluation of the relative abundance and decay rates of aquatic environmental DNA. Environ Sci Technol 52:6408–6416

    CAS  PubMed  Google Scholar 

  • Bylemans J, Furlan EM, Hardy CM, McGuffie P, Lintermans M, Gleeson DM (2017) An environmental DNA-based method for monitoring spawning activity: a case study, using the endangered Macquarie perch (Macquaria australasica). Methods Ecol Evol 8:646–655

    Google Scholar 

  • Cannon MV, Hester J, Shalkhauser A, Chan ER, Logue K, Small ST et al (2016) In silico assessment of primers for eDNA studies using PrimerTree and application to characterize the biodiversity surrounding the Cuyahoga River. Sci Rep 6:22908

    CAS  PubMed  PubMed Central  Google Scholar 

  • Carraro L, Hartikainen H, Jokela J, Bertuzzo E, Rinaldo A (2018) Estimating species distribution and abundance in river networks using environmental DNA. Proc Natl Acad Sci 115:11724–11729

    CAS  PubMed  PubMed Central  Google Scholar 

  • Carvalho S, Aylagas E, Villalobos R, Kattan Y, Berumen M, Pearman JK (2019) Beyond the visual: using metabarcoding to characterize the hidden reef cryptobiome. P Roy Soc B-Biol Sci 286:20182697

    CAS  Google Scholar 

  • Champlot S, Berthelot C, Pruvost M, Bennett EA, Grange T, Geigl EM (2010) An efficient multistrategy DNA decontamination procedure of PCR reagents for hypersensitive PCR applications. PLoS ONE 5:e1342

    Google Scholar 

  • Chen WT, Ficetola GF (2019) Conditionally autoregressive models improve occupancy analyses of autocorrelated data: an example with environmental DNA. Mol Ecol Resour 19:163–175

    PubMed  Google Scholar 

  • Cilleros K, Valentini A, Allard L, Dejean T, Etienne R, Grenouillet G et al (2019) Unlocking biodiversity and conservation studies in high-diversity environments using environmental DNA (eDNA): a test with Guianese freshwater fishes. Mol Ecol Resour 19:27–46

    CAS  PubMed  Google Scholar 

  • Civade R, Dejean T, Valentini A, Roset N, Raymond J-C, Bonin A et al (2016) Spatial representativeness of environmental DNA metabarcoding signal for fish biodiversity assessment in a natural freshwater system. PLoS ONE 11:e0157366–e0157366

    PubMed  PubMed Central  Google Scholar 

  • Clare EL, Symondson WOC, Broders H, Fabianek F, Fraser EE, MacKenzie A et al (2014) The diet of Myotis lucifugus across Canada: assessing foraging quality and diet variability. Mol Ecol 23:3618–3632

    PubMed  Google Scholar 

  • Clarke A, Fraser KPP (2004) Why does metabolism scale with temperature? Funct Ecol 18:243–251

    Google Scholar 

  • Coissac E, Riaz T, Puillandre N (2012) Bioinformatic challenges for DNA metabarcoding of plants and animals. Mol Ecol 21:1834–1847

    CAS  PubMed  Google Scholar 

  • Collins RA, Bakker J, Wangensteen OS, Soto AZ, Corrigan L, Sims DW et al (2019) Non-specific amplification compromises environmental DNA metabarcoding with COI. Methods Ecol Evol 10(11):1985–2001

    Google Scholar 

  • Collins RA, Wangensteen OS, O’Gorman EJ, Mariani S, Sims DW, Genner MJ (2018) Persistence of environmental DNA in marine systems. Commun Biol 1:185

    PubMed  PubMed Central  Google Scholar 

  • Cordier T, Frontalini F, Cermakova K, Apothéloz-Perret-Gentil L, Treglia M, Scantamburlo E et al (2019) Multi-marker eDNA metabarcoding survey to assess the environmental impact of three offshore gas platforms in the North Adriatic Sea (Italy). Mar Environ Res 146:24–34

    CAS  PubMed  Google Scholar 

  • Corlett RT (2017) A bigger toolbox: biotechnology in biodiversity conservation. Trends Biotechnol 35:55–65

    CAS  PubMed  Google Scholar 

  • Cowart DA, Matabos M, Brandt MI, Marticorena J, Sarrazin J (2020) Exploring environmental DNA (eDNA) to assess biodiversity of hard substratum faunal communities on the lucky strike vent field (Mid-Atlantic Ridge) and investigate recolonization dynamics after an induced disturbance. Front Mar Sci 6:783

    Google Scholar 

  • Davy CM, Kidd AG, Wilson CC (2015) Development and validation of environmental DNA (eDNA) markers for detection of freshwater turtles. PLoS ONE 10:e0130965–e0130965

    PubMed  PubMed Central  Google Scholar 

  • de Souza LS, Godwin JC, Renshaw MA, Larson E (2016) Environmental DNA (eDNA) detection probability is influenced by seasonal activity of organisms. PLoS ONE 11:e0165273

    PubMed  PubMed Central  Google Scholar 

  • Deagle BE, Eveson JP, Jarman SN (2006) Quantification of damage in DNA recovered from highly degraded samples–a case study on DNA in faeces. Front Zool 3:11

    PubMed  PubMed Central  Google Scholar 

  • Deagle BE, Jarman SN, Coissac E, Pompanon F, Taberlet P (2014) DNA metabarcoding and the cytochrome c oxidase subunit I marker: not a perfect match. Biol Let 10:20140562

    Google Scholar 

  • Deagle BE, Kirkwood R, Jarman SN (2009) Analysis of Australian fur seal diet by pyrosequencing prey DNA in faeces. Mol Ecol 18:2022–2038

    CAS  PubMed  Google Scholar 

  • Deagle BE, Thomas AC, Shaffer AK, Trites AW, Jarman SN (2013) Quantifying sequence proportions in a DNA-based diet study using Ion Torrent amplicon sequencing: which counts count? Mol Ecol Resour 13:620–633

    CAS  PubMed  Google Scholar 

  • Deiner K, Altermatt F (2014) Transport Distance of invertebrate environmental DNA in a natural river. PLoS ONE 9:e88786

    PubMed  PubMed Central  Google Scholar 

  • Deiner K, Bik HM, Machler E, Seymour M, Lacoursiere-Roussel A, Altermatt F et al (2017) Environmental DNA metabarcoding: Transforming how we survey animal and plant communities. Mol Ecol 26:5872–5895

    PubMed  Google Scholar 

  • Deiner K, Fronhofer EA, Mächler E, Walser J-C, Altermatt F (2016) Environmental DNA reveals that rivers are conveyer belts of biodiversity information. Nat Commun 7:12544

    CAS  PubMed  PubMed Central  Google Scholar 

  • Deiner K, Walser J-C, Mächler E, Altermatt F (2015) Choice of capture and extraction methods affect detection of freshwater biodiversity from environmental DNA. Biol Cons 183:53–63

    Google Scholar 

  • Dejean T, Valentini A, Duparc A, Pellier-Cuit S, Pompanon F, Taberlet P et al (2011) Persistence of environmental DNA in freshwater ecosystems. PLoS ONE 6:e23398

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dejean T, Valentini A, Miquel C, Taberlet P, Bellemain E, Miaud C (2012) Improved detection of an alien invasive species through environmental DNA barcoding: the example of the American bullfrog Lithobates catesbeianus. J Appl Ecol 49:953–959

    Google Scholar 

  • Deutschmann B, Mueller A-K, Hollert H, Brinkmann M (2019) Assessing the fate of brown trout (Salmo trutta) environmental DNA in a natural stream using a sensitive and specific dual-labelled probe. Sci Total Environ 655:321–327

    CAS  PubMed  Google Scholar 

  • DiBattista JD, Reimer JD, Stat M, Masucci GD, Biondi P, De Brauwer M et al (2019) Digging for DNA at depth: rapid universal metabarcoding surveys (RUMS) as a tool to detect coral reef biodiversity across a depth gradient. Peerj 7:36379

    Google Scholar 

  • Divoll TJ, Brown VA, Kinne J, McCracken GF, O'Keefe JM (2018) Disparities in second-generation DNA metabarcoding results exposed with accessible and repeatable workflows. Mol Ecol Resour 18:590–601

    CAS  PubMed  Google Scholar 

  • Djurhuus A, Closek CJ, Kelly RP, Pitz KJ, Michisaki RP, Starks HA et al (2020) Environmental DNA reveals seasonal shifts and potential interactions in a marine community. Nature Communications 11:254

    CAS  PubMed  PubMed Central  Google Scholar 

  • Djurhuus A, Port J, Closek CJ, Yamahara KM, Romero-Maraccini O, Walz KR et al (2017) Evaluation of filtration and DNA extraction methods for environmental DNA biodiversity assessments across multiple trophic levels. Front Mar Sci 4:314

    Google Scholar 

  • Doi H, Akamatsu Y, Watanabe Y, Goto M, Inui R, Katano I et al (2017) Water sampling for environmental DNA surveys by using an unmanned aerial vehicle. Limnol Oceanogr-Meth 15:939–944

    CAS  Google Scholar 

  • Doi H, Fukaya K, Oka S, Sato K, Kondoh M, Miya M (2019) Evaluation of detection probabilities at the water-filtering and initial PCR steps in environmental DNA metabarcoding using a multispecies site occupancy model. Sci Rep 9:1–8

    Google Scholar 

  • Doi H, Uchii K, Takahara T, Matsuhashi S, Yamanaka H, Minamoto T (2015) Use of droplet digital PCR for estimation of fish abundance and biomass in environmental DNA surveys. PLoS ONE 10:e0122763

    PubMed  PubMed Central  Google Scholar 

  • Dunn N, Priestley V, Herraiz A, Arnold R, Savolainen V (2017) Behavior and season affect crayfish detection and density inference using environmental DNA. Ecol Evol 7:7777–7785

    PubMed  PubMed Central  Google Scholar 

  • Edgar RC (2016) UCHIME2: improved chimera prediction for amplicon sequencing. BioRxiv. https://doi.org/10.1101/074252

    Article  Google Scholar 

  • Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200

    CAS  PubMed  PubMed Central  Google Scholar 

  • Edwards ME, Alsos IG, Yoccoz N, Coissac E, Goslar T, Gielly L et al (2018) Metabarcoding of modern soil DNA gives a highly local vegetation signal in Svalbard tundra. Holocene 28:2006–2016

    Google Scholar 

  • Eichmiller JJ, Miller LM, Sorensen PW (2016) Optimizing techniques to capture and extract environmental DNA for detection and quantification of fish. Mol Ecol Resour 16:56–68

    CAS  PubMed  Google Scholar 

  • Eiler A, Löfgren A, Hjerne O, Nordén S, Saetre P (2018) Environmental DNA (eDNA) detects the pool frog (Pelophylax lessonae) at times when traditional monitoring methods are insensitive. Sci Rep 8:5452

    PubMed  PubMed Central  Google Scholar 

  • Elbrecht V, Leese F (2015) Can DNA-based ecosystem assessments quantify species abundance? testing primer bias and biomass—sequence relationships with an innovative metabarcoding protocol. PLoS ONE 10:e0130324

    PubMed  PubMed Central  Google Scholar 

  • Epp LS, Boessenkool S, Bellemain EP, Haile J, Esposito A, Riaz T et al (2012) New environmental metabarcodes for analysing soil DNA: potential for studying past and present ecosystems. Mol Ecol 21:1821–1833

    CAS  PubMed  Google Scholar 

  • Erickson RA, Rees CB, Coulter AA, Merkes CM, Mccalla SG, Touzinsky KF et al (2016) Detecting the movement and spawning activity of bigheaded carps with environmental DNA. Mol Ecol Resour 16:957–965

    CAS  PubMed  PubMed Central  Google Scholar 

  • Evans NT, Li YY, Renshaw MA, Olds BP, Deiner K, Turner CR et al (2017a) Fish community assessment with eDNA metabarcoding: effects of sampling design and bioinformatic filtering. Can J Fish Aquat Sci 74:1362–1374

    CAS  Google Scholar 

  • Evans NT, Olds BP, Renshaw MA, Turner CR, Li Y, Jerde CL et al (2016) Quantification of mesocosm fish and amphibian species diversity via environmental DNA metabarcoding. Mol Ecol Resour 16:29–41

    CAS  PubMed  Google Scholar 

  • Evans NT, Shirey PD, Wieringa JG, Mahon AR, Lamberti GA (2017b) Comparative cost and effort of fish distribution detection via environmental DNA analysis and electrofishing. Fisheries 42:90–99

    Google Scholar 

  • Evrard O, Laceby JP, Ficetola GF, Gielly L, Huon S, Lefèvre I et al (2019) Environmental DNA provides information on sediment sources: a study in catchments affected by Fukushima radioactive fallout. Sci Total Environ 665:873–881

    CAS  PubMed  Google Scholar 

  • Fernanda Nardi C, Alfredo Fernandez D, Alberto Vanella F, Chalde T (2019) The expansion of exotic Chinook salmon (Oncorhynchus tshawytscha) in the extreme south of Patagonia: an environmental DNA approach. Biol Invasions 21:1415–1425

    Google Scholar 

  • Ficetola GF, Manenti R, Taberlet P (2019) Environmental DNA and metabarcoding for the study of amphibians and reptiles: species distribution, the microbiome, and much more. Amphibia-Reptilia 40:129–148

    Google Scholar 

  • Ficetola GF, Miaud C, Pompanon F, Taberlet P (2008) Species detection using environmental DNA from water samples. Biol Letters 4:423–425

    Google Scholar 

  • Ficetola GF, Pansu J, Bonin A, Coissac E, Giguet-Covex C, De Barba M et al (2015) Replication levels, false presences and the estimation of the presence/absence from eDNA metabarcoding data. Mol Ecol Resour 15:543–556

    CAS  PubMed  Google Scholar 

  • Ficetola GF, Taberlet P, Coissac E (2016) How to limit false positives in environmental DNA and metabarcoding? Mol Ecol Resour 16:604–607

    CAS  PubMed  Google Scholar 

  • Fonseca VG (2018) Pitfalls in relative abundance estimation using eDNA metabarcoding. Mol Ecol Resour 18:923–926

    CAS  Google Scholar 

  • Franklin TW, McKelvey KS, Golding JD, Mason DH, Dysthe JC, Pilgrim KL et al (2019) Using environmental DNA methods to improve winter surveys for rare carnivores: DNA from snow and improved noninvasive techniques. Biol Cons 229:50–58

    Google Scholar 

  • Fraser CI, Connell L, Lee CK, Cary SC (2018) Evidence of plant and animal communities at exposed and subglacial (cave) geothermal sites in Antarctica. Polar Biol 41:417–421

    Google Scholar 

  • Fritts AK, Knights BC, Larson JH, Amberg JJ, Merkes CM, Tajjioui T et al (2019) Development of a quantitative PCR method for screening ichthyoplankton samples for bigheaded carps. Biol Invasions 21:1143–1153

    Google Scholar 

  • Fujii K, Doi H, Matsuoka S, Nagano M, Sato H, Yamanaka H (2019) Environmental DNA metabarcoding for fish community analysis in backwater lakes: A comparison of capture methods. PLoS ONE 14:e0210357–e0210357

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fukumoto S, Ushimaru A, Minamoto T (2015) A basin-scale application of environmental DNA assessment for rare endemic species and closely related exotic species in rivers: a case study of giant salamanders in Japan. J Appl Ecol 52:358–365

    CAS  Google Scholar 

  • Galan M, Pages M, Cosson JF (2012) Next-Generation sequencing for rodent barcoding: species identification from fresh. Degraded and Environmental Samples, Plos One, p 7

    Google Scholar 

  • Galan M, Pons J-B, Tournayre O, Pierre E, Leuchtmann M, Pontier D et al (2018) Metabarcoding for the parallel identification of several hundred predators and their prey: Application to bat species diet analysis. Mol Ecol Resour 18:474–489

    CAS  PubMed  Google Scholar 

  • Gillet B, Cottet M, Destanque T, Kue K, Descloux S, Chanudet V et al (2018) Direct fishing and eDNA metabarcoding for biomonitoring during a 3-year survey significantly improves number of fish detected around a South East Asian reservoir. PLoS ONE 13:e0208592–e0208592

    PubMed  PubMed Central  Google Scholar 

  • Goldberg CS, Pilliod DS, Arkle RS, Waits LP (2011) Molecular detection of vertebrates in stream water: a demonstration using Rocky Mountain tailed frogs and idaho giant salamanders. PLoS ONE 6:e22746

    CAS  PubMed  PubMed Central  Google Scholar 

  • Goldberg CS, Sepulveda A, Ray A, Baumgardt J, Waits LP (2013) Environmental DNA as a new method for early detection of New Zealand mudsnails (Potamopyrgus antipodarum). Freshw Sci 32:792–800

    Google Scholar 

  • Goldberg CS, Strickler KM, Fremier AK (2018) Degradation and dispersion limit environmental DNA detection of rare amphibians in wetlands: Increasing efficacy of sampling designs. Sci Total Environ 633:695–703

    CAS  PubMed  Google Scholar 

  • Goldberg CS, Turner CR, Deiner K, Klymus KE, Thomsen PF, Murphy MA et al (2016) Critical considerations for the application of environmental DNA methods to detect aquatic species. Methods Ecol Evol 7:1299–1307

    Google Scholar 

  • Gomes GB, Hutson KS, Domingos JA, Villamil SI, Huerlimann R, Miller TL et al (2019) Parasitic protozoan interactions with bacterial microbiome in a tropical fish farm. Aquaculture 502:196–201

    Google Scholar 

  • Gómez-Zurita J, Cardoso A, Coronado I, De la Cadena G, Jurado-Rivera JA, Maes J-M et al (2016) High-throughput biodiversity analysis: rapid assessment of species richness and ecological interactions of Chrysomelidae (Coleoptera) in the tropics. Zookeys 597:3–26

    Google Scholar 

  • Graham SE, Chariton AA, Landis WG (2019) Using Bayesian networks to predict risk to estuary water quality and patterns of benthic environmental DNA in Queensland. Integr Environ Assess Manag 15:93–111

    CAS  PubMed  Google Scholar 

  • Guillera-Arroita G, Lahoz-Monfort JJ, van Rooyen AR, Weeks AR, Tingley R (2017) Dealing with false-positive and false-negative errors about species occurrence at multiple levels. Methods Ecol Evol 8:1081–1091

    Google Scholar 

  • Günther B, Knebelsberger T, Neumann H, Laakmann S, Martínez Arbizu P (2018) Metabarcoding of marine environmental DNA based on mitochondrial and nuclear genes. Sci Rep 8:14822

    PubMed  PubMed Central  Google Scholar 

  • Hanfling B, Handley LL, Read DS, Hahn C, Li JL, Nichols P et al (2016) Environmental DNA metabarcoding of lake fish communities reflects long-term data from established survey methods. Mol Ecol 25:3101–3119

    PubMed  Google Scholar 

  • Harper KJ, Goodwin KD, Harper LR, LaCasella EL, Frey A, Dutton PH (2020) Finding Crush: environmental DNA analysis as a tool for tracking the Green Sea Turtle Chelonia mydas in a Marine Estuary. Front Mar Sci 6:810

    Google Scholar 

  • Harper LR, Griffiths NP, Handley LL, Sayer CD, Read DS, Harper KJ et al (2019) Development and application of environmental DNA surveillance for the threatened crucian carp (Carassius carassius). Freshw Biol 64:93–107

    CAS  Google Scholar 

  • Harper LR, Lawson Handley L, Hahn C, Boonham N, Rees HC, Gough KC et al (2018) Needle in a haystack? A comparison of eDNA metabarcoding and targeted qPCR for detection of the great crested newt (Triturus cristatus). Ecol Evol 8:6330–6341

    PubMed  PubMed Central  Google Scholar 

  • Harrer LEF, Levi T (2018) The primacy of bears as seed dispersers in salmon-bearing ecosystems. Ecosphere 9:e02076

    Google Scholar 

  • Harrison JB, Sunday JM, Rogers SM (2019) Predicting the fate of eDNA in the environment and implications for studying biodiversity. Proc Royal Soc B Biol Sci 286:20191409

    Google Scholar 

  • Hemery LG, Politano KK, Henkel SK (2017) Assessing differences in macrofaunal assemblages as a factor of sieve mesh size, distance between samples, and time of sampling. Environ Monit Assess 189:413

    PubMed  Google Scholar 

  • Hering D, Borja A, Jones JI, Pont D, Boets P, Bouchez A et al (2018) Implementation options for DNA-based identification into ecological status assessment under the European water framework directive. Water Res 138:192–205

    CAS  PubMed  Google Scholar 

  • Hinlo R, Furlan E, Suitor L, Gleeson D (2017) Environmental DNA monitoring and management of invasive fish: comparison of eDNA and fyke netting. Manag Biol Invasion 8:89–100

    Google Scholar 

  • Hobbs J, Round JM, Allison MJ, Helbing CC (2019) Expansion of the known distribution of the coastal tailed frog, Ascaphus truei, in British Columbia, Canada, using robust eDNA detection methods. PLoS ONE 14:e0213849

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hopken MW, Orning EK, Young JK, Piaggio AJ (2016) Molecular forensics in avian conservation: a DNA-based approach for identifying mammalian predators of ground-nesting birds and eggs. BMC Res Notes 9:14

    PubMed  PubMed Central  Google Scholar 

  • Hunter ME, Ferrante JA, Meigs-Friend G, Ulmer A (2019) Improving eDNA yield and inhibitor reduction through increased water volumes and multi-filter isolation techniques. Sci Rep-Uk 9:1–9

    CAS  Google Scholar 

  • Huver JR, Koprivnikar J, Johnson PTJ, Whyard S (2015) Development and application of an eDNA method to detect and quantify a pathogenic parasite in aquatic ecosystems. Ecol Appl 25:991–1002

    CAS  PubMed  PubMed Central  Google Scholar 

  • Itakura H, Wakiya R, Yamamoto S, Kaifu K, Sato T, Minamoto T (2019) Environmental DNA analysis reveals the spatial distribution, abundance, and biomass of Japanese eels at the river-basin scale. Aquat Conserv 29:361–373

    Google Scholar 

  • Jane SF, Wilcox TM, McKelvey KS, Young MK, Schwartz MK, Lowe WH et al (2015) Distance, flow and PCR inhibition: eDNA dynamics in two headwater streams. Mol Ecol Resour 15:216–227

    CAS  PubMed  Google Scholar 

  • Jerde CL, Chadderton WL, Mahon AR, Renshaw MA, Corush J, Budny ML et al (2013) Detection of Asian carp DNA as part of a Great Lakes basin-wide surveillance program. Can J Fish Aquat Sci 70:522–526

    CAS  Google Scholar 

  • Jerde CL, Mahon AR, Chadderton WL, Lodge DM (2011) “Sight-unseen” detection of rare aquatic species using environmental DNA. Conserv Lett 4:150–157

    Google Scholar 

  • Jerde CL, Olds BP, Shogren AJ, Andruszkiewicz EA, Mahon AR, Bolster D et al (2016) Influence of stream bottom substrate on retention and transport of vertebrate environmental DNA. Environ Sci Technol 50:8770–8779

    CAS  PubMed  Google Scholar 

  • Jeunen GJ, Knapp M, Spencer HG, Lamare MD, Taylor HR, Stat M et al (2019) Environmental DNA (eDNA) metabarcoding reveals strong discrimination among diverse marine habitats connected by water movement. Mol Ecol Resour 19:426–438

    CAS  PubMed  Google Scholar 

  • Ji Y, Baker CC, Li Y, Popescu VD, Wang Z, Wang J et al (2020) Large-scale quantification of vertebrate biodiversity in ailaoshan nature reserve from leech iDNA. BioRxiv. https://doi.org/10.1101/2020.02.10.941336

    Article  PubMed  PubMed Central  Google Scholar 

  • Ji Y, Huotari T, Roslin T, Martin-Schmidt N, Wang J, Yu D et al (2019) SPIKEPIPE: A metagenomic pipeline for the accurate quantification of eukaryotic species occurrences and abundances using DNA barcodes or mitogenomes. BioRxiv. https://doi.org/10.1101/533737

    Article  Google Scholar 

  • Jia Q, Wang X, Zhang Y, Cao L, Fox AD (2018) Drivers of waterbird communities and their declines on Yangtze River floodplain lakes. Biol Conserv 218:240–246

    Google Scholar 

  • Jo T, Murakami H, Masuda R, Sakata MK, Yamamoto S, Minamoto T (2017) Rapid degradation of longer DNA fragments enables the improved estimation of distribution and biomass using environmental DNA. Mol Ecol Resour 17:e25–e33

    CAS  PubMed  Google Scholar 

  • Judo MS, Wedel AB, Wilson C (1998) Stimulation and suppression of PCR-mediated recombination. Nucleic Acids Res 26:1819–1825

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jusino MA, Banik MT, Palmer JM, Wray AK, Xiao L, Pelton E et al (2019) An improved method for utilizing high-throughput amplicon sequencing to determine the diets of insectivorous animals. Mol Ecol Resour 19:176–190

    CAS  PubMed  Google Scholar 

  • Kebschull JM, Zador AM (2015) Sources of PCR-induced distortions in high-throughput sequencing data sets. Nucleic Acids Res 43:e143

    PubMed  PubMed Central  Google Scholar 

  • Kemp BM, Smith DG (2005) Use of bleach to eliminate contaminating DNA from the surface of bones and teeth. Forensic Sci Int 154:53–61

    CAS  PubMed  Google Scholar 

  • Kessler EJ, Ash KT, Barratt SN, Larson ER, Davis MA (2020) Radiotelemetry reveals effects of upstream biomass and UV exposure on environmental DNA occupancy and detection for a large freshwater turtle. Environ DNA 2:13–23

    Google Scholar 

  • Khelifa R (2019) Sensitivity of biodiversity indices to life history stage, habitat type and landscape in Odonata community. Biol Conserv 237:63–69

    Google Scholar 

  • Klein CJ, Beher J, Chaloupka M, Hamann M, Limpus C, Possingham HP (2017) Prioritization of marine turtle management projects: a protocol that accounts for threats to different life history stages. Conserv Lett 10:547–554

    Google Scholar 

  • Klymus KE, Richter CA, Chapman DC, Paukert C (2015) Quantification of eDNA shedding rates from invasive bighead carp Hypophthalmichthys nobilis and silver carp Hypophthalmichthys molitrix. Biol Conserv 183:77–84

    Google Scholar 

  • Knudsen SW, Ebert RB, Hesselsoe M, Kuntke F, Hassingboe J, Mortensen PB et al (2019) Species-specific detection and quantification of environmental DNA from marine fishes in the Baltic Sea. J Exp Mar Biol Ecol 510:31–45

    CAS  Google Scholar 

  • Koziol A, Stat M, Simpson T, Jarman S, DiBattista JD, Harvey ES et al (2019) Environmental DNA metabarcoding studies are critically affected by substrate selection. Mol Ecol Resour 19:366–376

    CAS  PubMed  Google Scholar 

  • Kraaijeveld K, De Weger LA, Garcia MV, Buermans H, Frank J, Hiemstra PS et al (2015) Efficient and sensitive identification and quantification of airborne pollen using next-generation DNA sequencing. Mol Ecol Resour 15:8–16

    CAS  PubMed  Google Scholar 

  • Kuzmina ML, Braukmann TWA, Zakharov EV (2018) Finding the pond through the weeds: eDNA reveals underestimated diversity of pondweeds. Appl Plant Sci 6:e01155

    PubMed  PubMed Central  Google Scholar 

  • Lacoursière-Roussel A, Howland K, Normandeau E, Grey EK, Archambault P, Deiner K et al (2018) eDNA metabarcoding as a new surveillance approach for coastal Arctic biodiversity. Ecol Evol 8:7763–7777

    PubMed  PubMed Central  Google Scholar 

  • Lacoursière-Roussel A, Rosabal M, Bernatchez L (2016) Estimating fish abundance and biomass from eDNA concentrations: variability among capture methods and environmental conditions. Mol Ecol Resour 16:1401–1414

    PubMed  Google Scholar 

  • Lahoz-Monfort JJ, Guillera-Arroita G, Tingley R (2016) Statistical approaches to account for false-positive errors in environmental DNA samples. Mol Ecol Resour 16:673–685

    CAS  PubMed  Google Scholar 

  • Laramie MB, Pilliod DS, Goldberg CS (2015) Characterizing the distribution of an endangered salmonid using environmental DNA analysis. Biol Conserv 183:29–37

    Google Scholar 

  • Laroche O, Wood SA, Tremblay LA, Lear G, Ellis JI, Pochon X (2017) Metabarcoding monitoring analysis: the pros and cons of using co-extracted environmental DNA and RNA data to assess offshore oil production impacts on benthic communities. Peerj 5:e3347

    PubMed  PubMed Central  Google Scholar 

  • Lecaudey LA, Schletterer M, Kuzovlev VV, Hahn C, Weiss SJ (2019) Fish diversity assessment in the headwaters of the Volga River using environmental DNA metabarcoding. Aquat Conserv 29(10):1785–1800

    Google Scholar 

  • Leempoel K, Hebert T, Hadly EA (2020) A comparison of eDNA to camera trapping for assessment of terrestrial mammal diversity. Proc Royal Soc B Biol Sci 287:20192353

    Google Scholar 

  • Leray M, Knowlton N (2017) Random sampling causes the low reproducibility of rare eukaryotic OTUs in Illumina COI metabarcoding. Peerj 5:e3006

    PubMed  PubMed Central  Google Scholar 

  • Leray M, Yang JY, Meyer CP, Mills SC, Agudelo N, Ranwez V et al (2013) A new versatile primer set targeting a short fragment of the mitochondrial COI region for metabarcoding metazoan diversity: application for characterizing coral reef fish gut contents. Front Zool 10:34

    PubMed  PubMed Central  Google Scholar 

  • Levy-Booth DJ, Campbell RG, Gulden RH, Hart MM, Powell JR, Klironomos JN et al (2007) Cycling of extracellular DNA in the soil environment. Soil Biol Biochem 39:2977–2991

    CAS  Google Scholar 

  • Levi T, Allen JM, Bell D, Joyce J, Russell JR, Tallmon DA et al (2019) Environmental DNA for the enumeration and management of Pacific salmon. Mol Ecol Resour 19:597–608

    PubMed  Google Scholar 

  • Liang Z, Keeley A (2013) Filtration Recovery of Extracellular DNA from Environmental Water Samples. Environ Sci Technol 47:9324–9331

    CAS  PubMed  Google Scholar 

  • Lim NKM, Tay YC, Srivathsan A, Tan JWT, Kwik JTB, Baloglu B et al (2016) Next-generation freshwater bioassessment: eDNA metabarcoding with a conserved metazoan primer reveals species-rich and reservoir-specific communities. Roy Soc Open Sci 3:160635

    Google Scholar 

  • Lin MX, Zhang S, Yao M (2019) Effective detection of environmental DNA from the invasive American bullfrog. Biol Invasions 21:2255–2268

    Google Scholar 

  • Lindahl T (1993) Instability and decay of the primary structure of DNA. Nature 362:709–715

    CAS  PubMed  Google Scholar 

  • Liu S, Zhou X, Zhou C, Yang C (2017) Filling reference gaps via assembling DNA barcodes using high-throughput sequencing—moving toward barcoding the world. Gigascience 6:gix104

    Google Scholar 

  • Lugg WH, Griffiths J, van Rooyen AR, Weeks AR, Tingley R (2018) Optimal survey designs for environmental DNA sampling. Methods Ecol Evol 9:1049–1059

    Google Scholar 

  • Ma HJ, Stewart K, Lougheed S, Zheng JS, Wang YX, Zhao JF (2016) Characterization, optimization, and validation of environmental DNA (eDNA) markers to detect an endangered aquatic mammal. Conserv Genet Resour 8:561–568

    Google Scholar 

  • Machida RJ, Leray M, Ho SL, Knowlton N (2017) Metazoan mitochondrial gene sequence reference datasets for taxonomic assignment of environmental samples. Sci Data 4:170027

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mahe F, Rognes T, Quince C, de Vargas C, Dunthorn M (2014) Swarm: robust and fast clustering method for amplicon-based studies. Peerj 2:e593

    PubMed  PubMed Central  Google Scholar 

  • Mahe F, Rognes T, Quince C, de Vargas C, Dunthorn M (2015) Swarm v2: highly-scalable and high-resolution amplicon clustering. Peerj 3:e1420

    PubMed  PubMed Central  Google Scholar 

  • Mahon AR, Jerde CL, Galaska M, Bergner JL, Chadderton WL, Lodge DM et al (2013) Validation of eDNA surveillance sensitivity for detection of asian carps in controlled and field experiments. PLoS ONE 8:e58316

    CAS  PubMed  PubMed Central  Google Scholar 

  • Majaneva M, Diserud OH, Eagle SHC, Boström E, Hajibabaei M, Ekrem T (2018) Environmental DNA filtration techniques affect recovered biodiversity. Scientific Reports 8:4682

    PubMed  PubMed Central  Google Scholar 

  • Manfrin C, Souty-Grosset C, Anastacio PM, Reynolds J, Giulianini PG (2019) Detection and Control of Invasive Freshwater Crayfish: From Traditional to Innovative Methods. Diversity-Basel 11:5

    Google Scholar 

  • Marshall NT, Stepien CA (2019) Invasion genetics from eDNA and thousands of larvae: a targeted metabarcoding assay that distinguishes species and population variation of zebra and quagga mussels. Ecol Evol 9:3515–3538

    PubMed  PubMed Central  Google Scholar 

  • Maruyama A, Nakamura K, Yamanaka H, Kondoh M, Minamoto T (2014) The release rate of environmental DNA from Juvenile and adult fish. PLoS ONE 9:e114639

    PubMed  PubMed Central  Google Scholar 

  • Maruyama A, Nakamura K, Yamanaka H, Kondoh M, Minamoto T (2019) The release rate of environmental DNA from Juvenile and Adult Fish (2014). PLoS ONE 14:e114639

    Google Scholar 

  • Maruyama A, Sugatani K, Watanabe K, Yamanaka H, Imamura A (2018) Environmental DNA analysis as a non-invasive quantitative tool for reproductive migration of a threatened endemic fish in rivers. Ecol Evol 8:11964–11974

    PubMed  PubMed Central  Google Scholar 

  • Mata VA, Amorim F, Corley MFV, McCracken GF, Rebelo H, Beja P (2016) Female dietary bias towards large migratory moths in the European free-tailed bat (Tadarida teniotis). Biol Lett 12:20150988

    PubMed  PubMed Central  Google Scholar 

  • Mata VA, Rebelo H, Amorim F, McCracken GF, Jarman S, Beja P (2019) How much is enough? Effects of technical and biological replication on metabarcoding dietary analysis. Mol Ecol 28:165–175

    CAS  PubMed  Google Scholar 

  • Matter AN, Falke JA, Lopez JA, Savereide JW (2018) A rapid-assessment method to estimate the distribution of Juvenile Chinook Salmon in Tributary habitats using eDNA and occupancy estimation. N Am J Fish Manage 38:223–236

    Google Scholar 

  • Minamoto T, Uchii K, Takahara T, Kitayoshi T, Tsuji S, Yamanaka H et al (2017) Nuclear internal transcribed spacer-1 as a sensitive genetic marker for environmental DNA studies in common carp Cyprinus carpio. Mol Ecol Resour 17:324–333

    CAS  PubMed  Google Scholar 

  • Minamoto T, Yamanaka H, Takahara T, Honjo MN, Kawabata Z (2012) Surveillance of fish species composition using environmental DNA. Limnology 13:193–197

    CAS  Google Scholar 

  • Montagna M, Berruti A, Bianciotto V, Cremonesi P, Giannico R, Gusmeroli F et al (2018) Differential biodiversity responses between kingdoms (plants, fungi, bacteria and metazoa) along an Alpine succession gradient. Mol Ecol 27:3671–3685

    PubMed  Google Scholar 

  • Mora AJ, Prosse SWJ, Mora JA (2019) DNA metabarcoding allows non-invasive identification of arthropod prey provisioned to nestling Rufous hummingbirds (Selasphorus rufus). Peerj 7:e6596

    Google Scholar 

  • Moraes CT (2001) What regulates mitochondrial DNA copy number in animal cells? Trends Genet 17:199–205

    CAS  PubMed  Google Scholar 

  • Morin PA, Chambers KE, Boesch C, Vigilant L (2001) Quantitative polymerase chain reaction analysis of DNA from noninvasive samples for accurate microsatellite genotyping of wild chimpanzees (Pan troglodytes verus). Mol Ecol 10:1835–1844

    CAS  PubMed  Google Scholar 

  • Morley SA, Nielsen BL (2016) Chloroplast DNA copy number changes during plant development in organelle DNA polymerase mutants. Front Plant Sci 7:57

    PubMed  PubMed Central  Google Scholar 

  • Moushomi R, Wilgar G, Carvalho G, Creer S, Seymour M (2019) Environmental DNA size sorting and degradation experiment indicates the state of Daphnia magna mitochondrial and nuclear eDNA is subcellular. Sci Rep 9:12500

    PubMed  PubMed Central  Google Scholar 

  • Moyer GR, Diaz-Ferguson E, Hill JE, Shea C (2014) Assessing environmental DNA detection in controlled lentic systems. PLoS ONE 9:e103767

    PubMed  PubMed Central  Google Scholar 

  • Muha TP, Robinson CV, Garcia de Leaniz C, Consuegra S (2019) An optimised eDNA protocol for detecting fish in lentic and lotic freshwaters using a small water volume. PLoS ONE 14:e0219218

    CAS  PubMed  PubMed Central  Google Scholar 

  • Murakami H, Yoon S, Kasai A, Minamoto T, Yamamoto S, Sakata MK et al (2019) Dispersion and degradation of environmental DNA from caged fish in a marine environment. Fisheries Sci 85:327–337

    CAS  Google Scholar 

  • Nardi CF, Fernandez DA, Vanella FA, Chalde T (2019) The expansion of exotic Chinook salmon (Oncorhynchus tshawytscha) in the extreme south of Patagonia: an environmental DNA approach. Biol Invasions 21:1415–1425

    Google Scholar 

  • Nichols RV, Vollmers C, Newsom LA, Wang Y, Heintzman PD, Leighton M et al (2018) Minimizing polymerase biases in metabarcoding. Mol Ecol Resour 18:927–939

    CAS  Google Scholar 

  • O’Donnell JL, Kelly RP, Lowell NC, Port JA (2016) Indexed PCR primers induce template-specific bias in large-scale DNA sequencing studies. PLoS ONE 11:e0148698

    PubMed  PubMed Central  Google Scholar 

  • O’Donnell JL, Kelly RP, Shelton AO, Samhouri JF, Lowell NC, Williams GD (2017) Spatial distribution of environmental DNA in a nearshore marine habitat. Peerj 5:e3044

    PubMed  PubMed Central  Google Scholar 

  • Olds BP, Jerde CL, Renshaw MA, Li YY, Evans NT, Turner CR et al (2016) Estimating species richness using environmental DNA. Ecol Evol 6:4214–4226

    PubMed  PubMed Central  Google Scholar 

  • Olson ZH, Briggler JT, Williams RN (2012) An eDNA approach to detect eastern hellbenders (Cryptobranchus A. alleganiensis) using samples of water. Wildlife Res 39:629–636

    CAS  Google Scholar 

  • Orzechowski SCM, Frederick PC, Dorazio RM, Hunter ME (2019) Environmental DNA sampling reveals high occupancy rates of invasive Burmese pythons at wading bird breeding aggregations in the central Everglades. PLoS ONE. https://doi.org/10.1371/journal.pone.0213943

    Article  PubMed  PubMed Central  Google Scholar 

  • Outhwaite CL, Gregory RD, Chandler RE, Collen B, Isaac NJB (2020) Complex long-term biodiversity change among invertebrates, bryophytes and lichens. Nat Ecol Evol 4:384–392

    PubMed  Google Scholar 

  • Ovaskainen O, Moliterno de Camargo U, Somervuo P (2018) Animal sound identifier (ASI): software for automated identification of vocal animals. Ecol Lett 21:1244–1254

    PubMed  Google Scholar 

  • Piaggio AJ, Engeman RM, Hopken MW, Humphrey JS, Keacher KL, Bruce WE et al (2014) Detecting an elusive invasive species: a diagnostic PCR to detect Burmese python in Florida waters and an assessment of persistence of environmental DNA. Mol Ecol Resour 14:374–380

    CAS  PubMed  Google Scholar 

  • Piggott MP (2016) Evaluating the effects of laboratory protocols on eDNA detection probability for an endangered freshwater fish. Ecol Evol 6:2739–2750

    PubMed  PubMed Central  Google Scholar 

  • Pilliod DS, Goldberg CS, Arkle RS, Waits LP (2013) Estimating occupancy and abundance of stream amphibians using environmental DNA from filtered water samples. Can J Fish Aquat Sci 70:1123–1130

    CAS  Google Scholar 

  • Pilliod DS, Goldberg CS, Arkle RS, Waits LP (2014) Factors influencing detection of eDNA from a stream-dwelling amphibian. Mol Ecol Resour 14:109–116

    CAS  PubMed  Google Scholar 

  • Piñol J, Senar MA, Symondson WOC (2019) The choice of universal primers and the characteristics of the species mixture determine when DNA metabarcoding can be quantitative. Mol Ecol 28:407–419

    PubMed  Google Scholar 

  • Pompanon F, Deagle BE, Symondson WOC, Brown DS, Jarman SN, Taberlet P (2012) Who is eating what: diet assessment using next generation sequencing. Mol Ecol 21:1931–1950

    CAS  PubMed  Google Scholar 

  • Porter TM, Hajibabaei M (2018) Over 2.5 million COI sequences in GenBank and growing. PLoS ONE 13:e0200177

    PubMed  PubMed Central  Google Scholar 

  • Preissler K, Watzal AD, Vences M, Steinfartz S (2019) Detection of elusive fire salamander larvae (Salamandra salamandra) in streams via environmental DNA. Amphibia-Reptilia 40:55–64

    Google Scholar 

  • Prince AM, Andrus L (1992) Pcr - How to Kill Unwanted DNA. Biotechniques 12:358–360

    CAS  PubMed  Google Scholar 

  • Qu C, Stewart KA (2019) Evaluating monitoring options for conservation: comparing traditional and environmental DNA tools for a critically endangered mammal. Sci Nat 106:9

    Google Scholar 

  • Radstrom P, Knutsson R, Wolffs P, Lovenklev M, Lofstrom C (2004) Pre-PCR processing—strategies to generate PCR-compatible samples. Mol Biotechnol 26:133–146

    PubMed  Google Scholar 

  • Rajan SC, Athira K, Jaishanker R, Sooraj NP, Sarojkumar V (2019) Rapid assessment of biodiversity using acoustic indices. Biodivers Conserv 28:2371–2383

    Google Scholar 

  • Ratnasingham, S. & Hebert, P.D. (2007). bold: The barcode of life data system (https://www.barcodinglife.org). Mol Ecol Notes, 7, 355–364.

  • Rees HC, Baker CA, Gardner DS, Maddison BC, Gough KC (2017) The detection of great crested newts year round via environmental DNA analysis. BMC Res Notes 10:327

    PubMed  PubMed Central  Google Scholar 

  • Reinhardt T, van Schingen M, Windisch HS, Nguyen TQ, Ziegler T, Fink P (2019) Monitoring a loss: Detection of the semi-aquatic crocodile lizard (Shinisaurus crocodilurus) in inaccessible habitats via environmental DNA. Aquat Conserv 29:353–360

    Google Scholar 

  • Renshaw MA, Olds BP, Jerde CL, McVeigh MM, Lodge DM (2015) The room temperature preservation of filtered environmental DNA samples and assimilation into a phenol–chloroform–isoamyl alcohol DNA extraction. Molecular Ecology Resources 15:168–176

    CAS  PubMed  Google Scholar 

  • Rice CJ, Larson ER, Taylor CA (2018) Environmental DNA detects a rare large river crayfish but with little relation to local abundance. Freshwater Biol 63:443–455

    CAS  Google Scholar 

  • Riggio J, Kija H, Masenga E, Mbwilo F, Van de Perre F, Caro T (2018) Sensitivity of Africa's larger mammals to humans. J Nat Conserv 43:136–145

    Google Scholar 

  • Rivera SF, Vasselon V, Bouchez A, Rimet F (2020) Diatom metabarcoding applied to large scale monitoring networks: optimization of bioinformatics strategies using Mothur software. Ecol Indic 109:105775

    CAS  Google Scholar 

  • Rodriguez-Estrella R, Estrada CG, Alvarez-Castaneda ST, Ferrer-Sanchez Y (2019) Comparing individual raptor species and coarse taxonomic groups as biodiversity surrogates in desert ecosystems. Biodivers Conserv 28:1225–1244

    Google Scholar 

  • Rose JP, Wademan C, Weir S, Wood JS, Todd BD (2019) Traditional trapping methods outperform eDNA sampling for introduced semi-aquatic snakes. PLoS ONE 14(7):e0219244

    CAS  PubMed  PubMed Central  Google Scholar 

  • Roussel J-M, Paillisson J-M, Tréguier A, Petit E (2015) The downside of eDNA as a survey tool in water bodies. J Appl Ecol 52:823–826

    CAS  Google Scholar 

  • Rudko SP, Turnbull A, Reimink RL, Froelich K, Hanington PC (2019) Species-specific qPCR assays allow for high-resolution population assessment of four species avian schistosome that cause swimmer's itch in recreational lakes. International journal for parasitology. Parasit Wildlife 9:122–129

    Google Scholar 

  • Rytkonen S, Vesterinen EJ, Westerduin C, Leviakangas T, Vatka E, Mutanen M et al (2019) From feces to data: A metabarcoding method for analyzing consumed and available prey in a bird-insect food web. Ecol Evol 9:631–639

    PubMed  Google Scholar 

  • Saha A, McRae L, Dodd CK, Gadsden H, Hare KM, Lukoschek V et al (2018) Tracking global population trends: population time-series data and a living planet index for reptiles. J Herpetol 52:259–268

    Google Scholar 

  • Sales NG, Wangensteen OS, Carvalho DC, Deiner K, Præbel K, Coscia I et al (2020) Space-time dynamics in monitoring neotropical fish communities using eDNA metabarcoding. BioRxiv. https://doi.org/10.1101/2020.02.04.933366

    Article  Google Scholar 

  • Sansom BJ, Sassoubre LM (2017) Environmental DNA (eDNA) shedding and decay rates to model freshwater mussel eDNA transport in a river. Environ Sci Technol 51:14244–14253

    CAS  PubMed  Google Scholar 

  • Sassoubre LM, Yamahara KM, Gardner LD, Block BA, Boehm AB (2016) Quantification of environmental DNA (eDNA) shedding and decay rates for three marine fish. Environ Sci Technol 50:10456–10464

    CAS  PubMed  Google Scholar 

  • Sawaya NA, Djurhuus A, Closek CJ, Hepner M, Olesin E, Visser L et al (2019) Assessing eukaryotic biodiversity in the Florida Keys National Marine Sanctuary through environmental DNA metabarcoding. Ecol Evol 9:1029–1040

    PubMed  PubMed Central  Google Scholar 

  • Schmidt BR, Kery M, Ursenbacher S, Hyman OJ, Collins JP (2013) Site occupancy models in the analysis of environmental DNA presence/absence surveys: a case study of an emerging amphibian pathogen. Methods Ecol Evol 4:646–653

    Google Scholar 

  • Schrader C, Schielke A, Ellerbroek L, Johne R (2012) PCR inhibitors—occurrence, properties and removal. J Appl Microbiol 113:1014–1026

    CAS  PubMed  Google Scholar 

  • Schumer G, Crowley K, Maltz E, Johnston M, Anders P, Blankenship S (2019) Utilizing environmental DNA for fish eradication effectiveness monitoring in streams. Biol Invasions 21:3415–3426

    Google Scholar 

  • Sekercioglu CH, Mendenhall CD, Oviedo-Brenes F, Horns JJ, Ehrlich PR, Daily GC (2019) Long-term declines in bird populations in tropical agricultural countryside. P Natl Acad Sci USA 116:9903–9912

    CAS  Google Scholar 

  • Sengupta ME, Hellstrom M, Kariuki HC, Olsen A, Thomsen PF, Mejer H et al (2019) Environmental DNA for improved detection and environmental surveillance of schistosomiasis. P Natl Acad Sci USA 116:8931–8940

    CAS  Google Scholar 

  • Seymour M (2019) Rapid progression and future of environmental DNA research. Commun Biol 2:80

    PubMed  PubMed Central  Google Scholar 

  • Seymour M, Durance I, Cosby BJ, Ransom-Jones E, Deiner K, Ormerod SJ et al (2018) Acidity promotes degradation of multi-species environmental DNA in lotic mesocosms. Commun Biol 1:4

    PubMed  PubMed Central  Google Scholar 

  • Shelton AO, Kelly RP, O'Donnell JL, Park L, Schwenke P, Greene C et al (2019) Environmental DNA provides quantitative estimates of a threatened salmon species. Biol Conserv 237:383–391

    Google Scholar 

  • Sigsgaard EE, Carl H, Møller PR, Thomsen PF (2015) Monitoring the near-extinct European weather loach in Denmark based on environmental DNA from water samples. Biol Cons 183:46–52

    Google Scholar 

  • Singer D, Kosakyan A, Seppey CVW, Pillonel A, Fernández LD, Fontaneto D et al (2018) Environmental filtering and phylogenetic clustering correlate with the distribution patterns of cryptic protist species. Ecology 99:904–914

    PubMed  Google Scholar 

  • Singer GAC, Fahner NA, Barnes JG, McCarthy A, Hajibabaei M (2019) Comprehensive biodiversity analysis via ultra-deep patterned flow cell technology: a case study of eDNA metabarcoding seawater. Sci Rep 9:5991

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sirois SH, Buckley DH (2019) Factors governing extracellular DNA degradation dynamics in soil. Environ Microbiol Rep 11:173–184

    CAS  PubMed  Google Scholar 

  • Smart AS, Weeks AR, van Rooyen AR, Moore A, McCarthy MA, Tingley R (2016) Assessing the cost-efficiency of environmental DNA sampling. Methods Ecol Evol 7:1291–1298

    Google Scholar 

  • Song JW, Small MJ, Casman EA (2017) Making sense of the noise: The effect of hydrology on silver carp eDNA detection in the Chicago area waterway system. Sci Total Environ 605:713–720

    PubMed  Google Scholar 

  • Spear SF, Groves JD, Williams LA, Waits LP (2015) Using environmental DNA methods to improve detectability in a hellbender (Cryptobranchus alleganiensis) monitoring program. Biol Conserv 183:38–45

    Google Scholar 

  • Spens J, Evans AR, Halfmaerten D, Knudsen SW, Sengupta ME, Mak SST et al (2017) Comparison of capture and storage methods for aqueous macrobial eDNA using an optimized extraction protocol: advantage of enclosed filter. Methods Ecol Evol 8:635–645

    Google Scholar 

  • Srinivasan U (2019) Morphological and behavioral correlates of long-term bird survival in selectively logged forest. Front Ecol Evol 7:17

    Google Scholar 

  • Stadhouders R, Pas SD, Anber J, Voermans J, Mes THM, Schutten M (2010) The effect of primer-template mismatches on the detection and quantification of nucleic acids using the 5' nuclease assay. J Mol Diagn 12:109–117

    CAS  PubMed  PubMed Central  Google Scholar 

  • Steenweg R, Hebblewhite M, Kays R, Ahumada J, Fisher JT, Burton C et al (2017) Scaling-up camera traps: monitoring the planet's biodiversity with networks of remote sensors. Front Ecol Environ 15:26–34

    Google Scholar 

  • Stewart K, Ma HJ, Zheng JS, Zhao JF (2017) Using environmental DNA to assess population-wide spatiotemporal reserve use. Conserv Biol 31:1173–1182

    PubMed  Google Scholar 

  • Stewart KA (2019) Understanding the effects of biotic and abiotic factors on sources of aquatic environmental DNA. Biodivers Conserv 28:983–1001

    Google Scholar 

  • Stoeckle BC, Kuehn R, Geist J (2016) Environmental DNA as a monitoring tool for the endangered freshwater pearl mussel (Margaritifera margaritifera L.): a substitute for classical monitoring approaches? Aquat Conserv 26:1120–1129

    Google Scholar 

  • Stoeckle MY, Soboleva L, Charlop-Powers Z (2017) Aquatic environmental DNA detects seasonal fish abundance and habitat preference in an urban estuary. PLoS ONE 12:e0175186

    PubMed  PubMed Central  Google Scholar 

  • Strickland GJ, Roberts JH (2019) Utility of eDNA and occupancy models for monitoring an endangered fish across diverse riverine habitats. Hydrobiologia 826:129–144

    CAS  Google Scholar 

  • Strickler KM, Fremier AK, Goldberg CS (2015) Quantifying effects of UV-B, temperature, and pH on eDNA degradation in aquatic microcosms. Biol Cons 183:85–92

    Google Scholar 

  • Sutter M, Kinziger AP (2019) Rangewide tidewater goby occupancy survey using environmental DNA. Conserv Genet 20:597–613

    Google Scholar 

  • Taberlet P, Coissac E, Hajibabaei M, Rieseberg LH (2012a) Environmental DNA. Mol Ecol 21:1789–1793

    CAS  PubMed  Google Scholar 

  • Taberlet P, Prud'homme SM, Campione E, Roy J, Miquel C, Shehzad W et al (2012b) Soil sampling and isolation of extracellular DNA from large amount of starting material suitable for metabarcoding studies. Mol Ecol 21:1816–1820

    CAS  PubMed  Google Scholar 

  • Takahara T, Iwai N, Yasumiba K, Igawa T (2020) Comparison of the detection of 3 endangered frog species by eDNA and acoustic surveys across 3 seasons. Freshw Sci 39:18–27

    Google Scholar 

  • Takahara T, Minamoto T, Yamanaka H, Doi H, Kawabata Z (2012) Estimation of fish biomass using environmental DNA. PLoS ONE 7:e35868

    CAS  PubMed  PubMed Central  Google Scholar 

  • Takeuchi A, Iijima T, Kakuzen W, Watanabe S, Yamada Y, Okamura A et al (2019a) Release of eDNA by different life history stages and during spawning activities of laboratory-reared Japanese eels for interpretation of oceanic survey data. Sci Rep 9:6074

    PubMed  PubMed Central  Google Scholar 

  • Takeuchi A, Watanabe S, Yamamoto S, Miller MJ, Fukuba T, Miwa T et al (2019b) First use of oceanic environmental DNA to study the spawning ecology of the Japanese eel Anguilla japonica. Mar Ecol Prog Ser 609:187–196

    CAS  Google Scholar 

  • Thomas AC, Howard J, Nguyen PL, Seimon TA, Goldberg CS (2018) ANDe (TM): a fully integrated environmental DNA sampling system. Methods Ecol Evol 9:1379–1385

    Google Scholar 

  • Thomas AC, Nguyen PL, Howard J, Goldberg CS (2019) A self-preserving, partially biodegradable eDNA filter. Methods Ecol Evol 10:1136–1141

    Google Scholar 

  • Thomsen PF, Kielgast J, Iversen LL, Møller PR, Rasmussen M, Willerslev E (2012a) Detection of a diverse marine fish fauna using environmental DNA from seawater samples. PLoS ONE 7:e41732

    CAS  PubMed  PubMed Central  Google Scholar 

  • Thomsen PF, Kielgast J, Iversen LL, Wiuf C, Rasmussen M, Gilbert MTP et al (2012b) Monitoring endangered freshwater biodiversity using environmental DNA. Mol Ecol 21:2565–2573

    CAS  PubMed  Google Scholar 

  • Thomsen PF, Sigsgaard EE (2019) Environmental DNA metabarcoding of wild flowers reveals diverse communities of terrestrial arthropods. Ecol Evol 9:1665–1679

    PubMed  PubMed Central  Google Scholar 

  • Thomsen PF, Willerslev E (2015) Environmental DNA—an emerging tool in conservation for monitoring past and present biodiversity. Biol Conserv 183:4–18

    Google Scholar 

  • Tillotson MD, Kelly RP, Duda JJ, Hoy M, Kralj J, Quinn TP (2018) Concentrations of environmental DNA (eDNA) reflect spawning salmon abundance at fine spatial and temporal scales. Biol Conserv 220:1–11

    Google Scholar 

  • Tingley R, Greenlees M, Oertel S, van Rooyen AR, Weeks AR (2019) Environmental DNA sampling as a surveillance tool for cane toad Rhinella marina introductions on offshore islands. Biol Invasions 21:1–6

    Google Scholar 

  • Togaki D, Doi H, Katano I (2020) Detection of freshwater mussels (Sinanodonta spp.) in artificial ponds through environmental DNA: a comparison with traditional hand collection methods. Limnology 21:59–65

    CAS  Google Scholar 

  • Trebitz AS, Hoffman JC, Darling JA, Pilgrim EM, Kelly JR, Brown EA et al (2017) Early detection monitoring for aquatic non-indigenous species: optimizing surveillance, incorporating advanced technologies, and identifying research needs. J Environ Manage 202:299–310

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tsuji S, Ushio M, Sakurai S, Minamoto T, Yamanaka H (2017) Water temperature-dependent degradation of environmental DNA and its relation to bacterial abundance. PLoS ONE 12:e0176608

    PubMed  PubMed Central  Google Scholar 

  • Tsukamoto K, Chow S, Otake T, Kurogi H, Mochioka N, Miller MJ et al (2011) Oceanic spawning ecology of freshwater eels in the western North Pacific. Nat Commun 2:179

    PubMed  Google Scholar 

  • Turner CR, Barnes MA, Xu CCY, Jones SE, Jerde CL, Lodge DM (2014a) Particle size distribution and optimal capture of aqueous macrobial eDNA. Methods Ecol Evol 5:676–684

    Google Scholar 

  • Turner CR, Miller DJ, Coyne KJ, Corush J (2014b) Improved methods for capture, extraction, and quantitative assay of environmental DNA from asian bigheaded carp (Hypophthalmichthys spp.). PLoS ONE 9:e114329

    PubMed  PubMed Central  Google Scholar 

  • Turner CR, Uy KL, Everhart RC (2015) Fish environmental DNA is more concentrated in aquatic sediments than surface water. Biol Conserv 183:93–102

    Google Scholar 

  • Ulibarri RM, Bonar SA, Rees C, Amberg J, Ladell B, Jackson C (2017) Comparing efficiency of American Fisheries Society standard snorkeling techniques to environmental DNA sampling techniques. N Am J Fish Manage 37:644–651

    Google Scholar 

  • Unnithan VV, Unc A, Joe V, Smith GB (2014) Short RNA indicator sequences are not completely degraded by autoclaving. Sci Rep 4:4070–4070

    PubMed  PubMed Central  Google Scholar 

  • Valentini A, Taberlet P, Miaud C, Civade R, Herder J, Thomsen PF et al (2016) Next-generation monitoring of aquatic biodiversity using environmental DNA metabarcoding. Mol Ecol 25:929–942

    CAS  PubMed  Google Scholar 

  • van der Heyde M, Bunce M, Wardell-Johnson G, Fernandes K, White NE, Nevill P (2020) Testing multiple substrates for terrestrial biodiversity monitoring using environmental DNA metabarcoding. Mol Ecol Resour 00:1–14. https://doi.org/10.1111/1755-0998.13148

    Article  Google Scholar 

  • Vimercati G, Labadesse M, Dejean T, Secondi J (2020) Assessing the effect of landscape features on pond colonisation by an elusive amphibian invader using environmental DNA. Freshw Biol 65:502–513

    CAS  Google Scholar 

  • Voros J, Marton O, Schmidt BR, Gal JT, Jelic D (2017) Surveying Europe’s only cave-dwelling chordate species (Proteus anguinus) Using Environmental DNA. PLoS ONE 12:e0170945

    PubMed  PubMed Central  Google Scholar 

  • Walsh JR, Spear MJ, Shannon TP, Krysan PJ, Vander Zanden MJ (2019) Using eDNA, sediment subfossils, and zooplankton nets to detect invasive spiny water flea (Bythotrephes longimanus). Biol Invasions 21:377–389

    Google Scholar 

  • Watson RJ, Blackwell B (2000) Purification and characterization of a common soil component which inhibits the polymerase chain reaction. Can J Microbiol 46:633–642

    CAS  PubMed  Google Scholar 

  • Wei N, Nakajima F, Tobino T (2018) Effects of treated sample weight and DNA marker length on sediment eDNA based detection of a benthic invertebrate. Ecol Indic 93:267–273

    CAS  Google Scholar 

  • Weltz K, Lyle JM, Ovenden J, Morgan JAT, Moreno DA, Semmens JM (2017) Application of environmental DNA to detect an endangered marine skate species in the wild. PLoS ONE 12:e0178124

    PubMed  PubMed Central  Google Scholar 

  • Wilcox TM, McKelvey KS, Young MK, Jane SF, Lowe WH, Whiteley AR et al (2013) Robust detection of rare species using environmental DNA: the importance of primer specificity. PLoS ONE 8:e59520–e59520

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wilcox TM, McKelvey KS, Young MK, Sepulveda AJ, Shepard BB, Jane SF et al (2016) Understanding environmental DNA detection probabilities: a case study using a stream-dwelling char Salvelinus fontinalis. Biol Conserv 194:209–216

    Google Scholar 

  • Wilcox TM, Zarn KE, Piggott MP, Young MK, McKelvey KS, Schwartz MK (2018) Capture enrichment of aquatic environmental DNA: a first proof of concept. Mol Ecol Resour 18:1392–1401

    CAS  PubMed  Google Scholar 

  • Williams KE, Huyvaert KP, Piaggio AJ (2016) No filters, no fridges: a method for preservation of water samples for eDNA analysis. BMC Res Notes 9:298

    PubMed  PubMed Central  Google Scholar 

  • Willoughby JR, Wijayawardena BK, Sundaram M, Swihart RK, Dewoody JA (2016) The importance of including imperfect detection models in eDNA experimental design. Mol Ecol Resour 16:837–844

    CAS  PubMed  Google Scholar 

  • Wilson CC, Wozney KM, Smith CM (2016) Recognizing false positives: synthetic oligonucleotide controls for environmental DNA surveillance. Methods Ecol Evol 7:23–29

    Google Scholar 

  • Wineland SM, Welch SM, Pauley TK, Apodaca JJ, Olszack M, Mosher JJ et al (2019) Using environmental DNA and occupancy modelling to identify drivers of eastern hellbender (Cryptobranchus alleganiensis alleganiensis) extirpation. Freshw Biol 64:208–221

    CAS  Google Scholar 

  • Wood SA, Pochon X, Ming W, von Ammon U, Woods C, Carter M et al (2019) Considerations for incorporating real-time PCR assays into routine marine biosecurity surveillance programmes: a case study targeting the Mediterranean fanworm (Sabella spallanzanii) and club tunicate (Styela clava). Genome 62:137–146

    CAS  PubMed  Google Scholar 

  • Wu QQ, Kawano K, Uehara Y, Okuda N, Hongo M, Tsuji S et al (2018) Environmental DNA reveals nonmigratory individuals of Palaemon paucidens overwintering in Lake Biwa shallow waters. Freshw Sci 37:307–314

    Google Scholar 

  • Xia ZQ, Zhan AB, Gao YC, Zhang L, Haffner GD, MacIsaac HJ (2018) Early detection of a highly invasive bivalve based on environmental DNA (eDNA). Biol Invasions 20:437–447

    Google Scholar 

  • Xiong W, Zhan AB (2018) Testing clustering strategies for metabarcoding-based investigation of community-environment interactions. Mol Ecol Resour 18:1326–1338

    CAS  PubMed  Google Scholar 

  • Yamahara KM, Preston CM, Birch J, Walz K, Marin R, Jensen S et al (2019) In situ autonomous acquisition and preservation of marine environmental DNA using an autonomous underwater vehicle. Front Mar Sci 6:373

    Google Scholar 

  • Yamamoto S, Masuda R, Sato Y, Sado T, Araki H, Kondoh M et al (2017) Environmental DNA metabarcoding reveals local fish communities in a species-rich coastal sea. Sci Rep 7:1–12

    Google Scholar 

  • Yamanaka H, Minamoto T, Matsuura J, Sakurai S, Tsuji S, Motozawa H et al (2017) A simple method for preserving environmental DNA in water samples at ambient temperature by addition of cationic surfactant. Limnology 18:233–241

    CAS  Google Scholar 

  • Yang J, Zhang X (2020) eDNA metabarcoding in zooplankton improves the ecological status assessment of aquatic ecosystems. Environ Int 134:105230

    CAS  PubMed  Google Scholar 

  • Yoccoz NG, Brathen KA, Gielly L, Haile J, Edwards ME, Goslar T et al (2012) DNA from soil mirrors plant taxonomic and growth form diversity. Mol Ecol 21:3647–3655

    CAS  PubMed  Google Scholar 

  • Young MR, Proctor HC, deWaard JR, Hebert PDN (2019) DNA barcodes expose unexpected diversity in Canadian mites. Mol Ecol 2019(28):5347–5359

    Google Scholar 

  • Zeale MRK, Butlin RK, Barker GLA, Lees DC, Jones G (2011) Taxon-specific PCR for DNA barcoding arthropod prey in bat faeces. Mol Ecol Resour 11:236–244

    CAS  PubMed  Google Scholar 

  • Zhang S, Lu Q, Wang Y, Wang X, Zhao J, Yao M (2020a) Assessment of fish communities using environmental DNA: effect of spatial sampling design in lentic systems of different sizes. Mol Ecol Resour 20:242–255

    CAS  PubMed  Google Scholar 

  • Zhang Y, Pavlovska M, Stoica E, Prekrasna I, Yang J, Slobodnik J et al (2020b) Holistic pelagic biodiversity monitoring of the Black Sea via eDNA metabarcoding approach: From bacteria to marine mammals. Environ Int 135:105307

    PubMed  Google Scholar 

  • Zhou X, Li Y, Liu S, Yang Q, Su X, Zhou L et al (2013) Ultra-deep sequencing enables high-fidelity recovery of biodiversity for bulk arthropod samples without PCR amplification. Gigascience 2:4

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zinger L, Taberlet P, Schimann H, Bonin A, Boyer F, De Barba M et al (2019) Body size determines soil community assembly in a tropical forest. Mol Ecol 28:528–543

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This study was financially supported by the Yunnan Oriented Fund for Postdoctoral Researchers (Grant No. Y7YN021B09) and the Chinese Academy Science (CAS) 135 Program (Grant No. 2017XTBG-T03). Neither funding bodies played any role in the design of the study, data collection and analysis, interpretation of results, or writing the manuscript. We are grateful to Zhang Xiaowei for his insightful comments and suggestions that improved the manuscript quality.

Author information

Authors and Affiliations

  1. Center for Integrative Conservation, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Menglun, 666303, Mengla, Yunnan, China

    Kingsly C. Beng & Richard T. Corlett

  2. Center of Conservation Biology, Core Botanical Gardens, Chinese Academy of Sciences, Menglun, 666303, Mengla, Yunnan, China

    Kingsly C. Beng & Richard T. Corlett

  3. Department of Ecosystem Research, Leibniz-Institute of Freshwater Ecology and Inland Fisheries, Müggelseedamm 310, Berlin, 12587, Germany

    Kingsly C. Beng

Authors
  1. Kingsly C. Beng
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Richard T. Corlett
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Kingsly C. Beng or Richard T. Corlett.

Additional information

Communicated by David Hawksworth.

Publisher's Note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Beng, K.C., Corlett, R.T. Applications of environmental DNA (eDNA) in ecology and conservation: opportunities, challenges and prospects. Biodivers Conserv 29, 2089–2121 (2020). https://doi.org/10.1007/s10531-020-01980-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10531-020-01980-0

Keywords

Search

Navigation