The sceptical optimist: challenges and perspectives for the application of environmental DNA in marine fisheries

Application of environmental DNA (eDNA) analysis has attracted the attention of researchers, advisors and managers of living marine resources and biodiversity. The apparent simplicity and cost‐effectiveness of eDNA analysis make it highly attractive as species distributions can be revealed from water samples. Further, species‐specific analyses indicate that eDNA concentrations correlate with biomass and abundance, suggesting the possibility for quantitative applications estimating abundance and biomass of specific organisms in marine ecosystems, such as for stock assessment. However, the path from detecting occurrence of an organism to quantitative estimates is long and indirect, not least as eDNA concentration depends on several physical, chemical and biological factors which influence its production, persistence and transport in marine ecosystems. Here, we provide an overview of basic principles in relation to eDNA analysis with potential for marine fisheries application. We describe fundamental processes governing eDNA generation, breakdown and transport and summarize current uncertainties about these processes. We describe five major challenges in relation to application in fisheries assessment, where there is immediate need for knowledge building in marine systems, and point to apparent weaknesses of eDNA compared to established marine fisheries monitoring methods. We provide an overview of emerging applications of interest to fisheries management and point to recent technological advances, which could improve analysis efficiency. We advise precaution against exaggerating the present scope for application of eDNA analysis in fisheries monitoring, but also argue that with informed insights into strengths and limitations, eDNA analysis can become an integrated tool in fisheries assessment and management.

[1]  Yaniv Erlich,et al.  Rapid re-identification of human samples using portable DNA sequencing , 2017, eLife.

[2]  Dawn B. Goldsmith,et al.  Evaluation of Filtration and DNA Extraction Methods for Environmental DNA Biodiversity Assessments across Multiple Trophic Levels , 2017, Front. Mar. Sci..

[3]  Michael Bunce,et al.  Ecosystem biomonitoring with eDNA: metabarcoding across the tree of life in a tropical marine environment , 2017, Scientific Reports.

[4]  E. Garcia-Vazquez,et al.  DNA in a bottle—Rapid metabarcoding survey for early alerts of invasive species in ports , 2017, PloS one.

[5]  P. L. Chang,et al.  The complete mitochondrial genome of the grooved carpet shell, Ruditapes decussatus (Bivalvia, Veneridae) , 2017, PeerJ.

[6]  E. Garcia-Vazquez,et al.  On the way for detecting and quantifying elusive species in the sea: The Octopus vulgaris case study , 2017 .

[7]  J. Semmens,et al.  Application of environmental DNA to detect an endangered marine skate species in the wild , 2017, PloS one.

[8]  S. Knudsen,et al.  Seawater environmental DNA reflects seasonality of a coastal fish community , 2017 .

[9]  E. Sampayo,et al.  Using eDNA to determine the source of organic carbon in seagrass meadows , 2017 .

[10]  Masayuki Ushio,et al.  Water temperature-dependent degradation of environmental DNA and its relation to bacterial abundance , 2017, PloS one.

[11]  Lauren M. Sassoubre,et al.  Biomonitoring of marine vertebrates in Monterey Bay using eDNA metabarcoding , 2017, PloS one.

[12]  T. Morato,et al.  Development of a sensitive detection method to survey pelagic biodiversity using eDNA and quantitative PCR: a case study of devil ray at seamounts , 2017 .

[13]  M. Stoeckle,et al.  Aquatic environmental DNA detects seasonal fish abundance and habitat preference in an urban estuary , 2017, PloS one.

[14]  Andrew S. Buxton,et al.  Seasonal variation in environmental DNA in relation to population size and environmental factors , 2017, Scientific Reports.

[15]  B. Rinkevich,et al.  Employing DNA barcoding as taxonomy and conservation tools for fish species censuses at the southeastern Mediterranean, a hot-spot area for biological invasion , 2017 .

[16]  Marius N. Müller,et al.  Effects of CO2 concentration on a late summer surface sea ice community , 2017 .

[17]  S. Planes,et al.  Rapid assessment of non-indigenous species in the era of the eDNA barcoding: A Mediterranean case study , 2017 .

[18]  Satoshi Yamamoto,et al.  Environmental DNA reflects spatial and temporal jellyfish distribution , 2017, PloS one.

[19]  M. Miya,et al.  Environmental DNA metabarcoding reveals local fish communities in a species-rich coastal sea , 2017, Scientific Reports.

[20]  Andrew O. Shelton,et al.  Genetic and Manual Survey Methods Yield Different and Complementary Views of an Ecosystem , 2017 .

[21]  G. Carvalho,et al.  Fish, genes and genomes: contributions to ecology, evolution and management. , 2016, Journal of fish biology.

[22]  Eske Willerslev,et al.  Environmental DNA from Seawater Samples Correlate with Trawl Catches of Subarctic, Deepwater Fishes , 2016, PloS one.

[23]  L. Bernatchez,et al.  Estimating fish abundance and biomass from eDNA concentrations: variability among capture methods and environmental conditions , 2016, Molecular ecology resources.

[24]  Lauren M. Sassoubre,et al.  Quantification of Environmental DNA (eDNA) Shedding and Decay Rates for Three Marine Fish. , 2016, Environmental science & technology.

[25]  A. Vasemägi,et al.  Can environmental DNA (eDNA) be used for detection and monitoring of introduced crab species in the Baltic Sea? , 2016, Marine pollution bulletin.

[26]  P. Croot,et al.  Identifying the Sources and Sinks of CDOM/FDOM across the Mauritanian Shelf and Their Potential Role in the Decomposition of Superoxide (O2-) , 2016, Front. Mar. Sci..

[27]  A. Kinziger,et al.  Using occupancy modelling to compare environmental DNA to traditional field methods for regional‐scale monitoring of an endangered aquatic species , 2016, Molecular ecology resources.

[28]  R. Yamamoto,et al.  Collective motion of cells crawling on a substrate: roles of cell shape and contact inhibition , 2016, Scientific Reports.

[29]  Elizabeth A. Ottesen.  Probing the living ocean with ecogenomic sensors. , 2016, Current opinion in microbiology.

[30]  J. McPherson,et al.  Coming of age: ten years of next-generation sequencing technologies , 2016, Nature Reviews Genetics.

[31]  M. Miya,et al.  Environmental DNA as a ‘Snapshot’ of Fish Distribution: A Case Study of Japanese Jack Mackerel in Maizuru Bay, Sea of Japan , 2016, PloS one.

[32]  D. Dolgikh,et al.  Human Secreted Ly-6/uPAR Related Protein-1 (SLURP-1) Is a Selective Allosteric Antagonist of α7 Nicotinic Acetylcholine Receptor , 2016, PloS one.

[33]  Matthew A. Barnes,et al.  The ecology of environmental DNA and implications for conservation genetics , 2016, Conservation Genetics.

[34]  P. Sorensen,et al.  Effects of Temperature and Trophic State on Degradation of Environmental DNA in Lake Water. , 2016, Environmental science & technology.

[35]  Jesse A. Port,et al.  Assessing vertebrate biodiversity in a kelp forest ecosystem using environmental DNA , 2015, Molecular ecology.

[36]  K. Sand‐Jensen,et al.  Monitoring of animal abundance by environmental DNA — An increasingly obscure perspective: A reply to Klymus et al., 2015 , 2015 .

[37]  Anastasija Zaiko,et al.  eDNA and specific primers for early detection of invasive species--A case study on the bivalve Rangia cuneata, currently spreading in Europe. , 2015, Marine environmental research.

[38]  M. Kennard,et al.  Measuring benefits of protected area management: trends across realms and research gaps for freshwater systems , 2015, Philosophical Transactions of the Royal Society B: Biological Sciences.

[39]  E. Garcia-Vazquez,et al.  Environmental DNA evidence of transfer of North Sea molluscs across tropical waters through ballast water , 2015 .

[40]  J. Hemmer-Hansen,et al.  Archived DNA reveals fisheries and climate induced collapse of a major fishery , 2015, Scientific Reports.

[41]  M. Johnson,et al.  Circulating microRNAs in Sera Correlate with Soluble Biomarkers of Immune Activation but Do Not Predict Mortality in ART Treated Individuals with HIV-1 Infection: A Case Control Study , 2015, PloS one.

[42]  John P. Ryan,et al.  Development of a mobile ecogenomic sensor , 2015, OCEANS 2015 - MTS/IEEE Washington.

[43]  L. Clausen,et al.  Gene-associated markers can assign origin in a weakly structured fish, Atlantic herring , 2015 .

[44]  E. Petit,et al.  The downside of eDNA as a survey tool in water bodies , 2015 .

[45]  C. Davy,et al.  Development and Validation of Environmental DNA (eDNA) Markers for Detection of Freshwater Turtles , 2015, PloS one.

[46]  M. Kondoh,et al.  MiFish, a set of universal PCR primers for metabarcoding environmental DNA from fishes: detection of more than 230 subtropical marine species , 2015, Royal Society Open Science.

[47]  Yiyuan Li,et al.  Quantification of mesocosm fish and amphibian species diversity via environmental DNA metabarcoding , 2015, Molecular ecology resources.

[48]  S. Whyard,et al.  Development and application of an eDNA method to detect and quantify a pathogenic parasite in aquatic ecosystems. , 2015, Ecological applications : a publication of the Ecological Society of America.

[49]  H. Doi,et al.  Use of Droplet Digital PCR for Estimation of Fish Abundance and Biomass in Environmental DNA Surveys , 2015, PloS one.

[50]  E. E. Sigsgaard,et al.  Monitoring the near-extinct European weather loach in Denmark based on environmental DNA from water samples , 2015 .

[51]  D. Chapman,et al.  Quantification of eDNA shedding rates from invasive bighead carp Hypophthalmichthys nobilis and silver carp Hypophthalmichthys molitrix. , 2015 .

[52]  C. Dichmont,et al.  Ocean's eleven: a critical evaluation of the role of population, evolutionary and molecular genetics in the management of wild fisheries , 2015 .

[53]  L. Waits,et al.  Using environmental DNA methods to improve detectability in a hellbender (Cryptobranchus alleganiensis) monitoring program , 2015 .

[54]  C. Turner,et al.  Fish environmental DNA is more concentrated in aquatic sediments than surface water , 2015 .

[55]  C. Goldberg,et al.  Quantifying effects of UV-B, temperature, and pH on eDNA degradation in aquatic microcosms , 2015 .

[56]  Pengjuan Xu,et al.  MKL1 inhibits cell cycle progression through p21 in podocytes , 2015, BMC Molecular Biology.

[57]  B. Letcher,et al.  Distance, flow and PCR inhibition: eDNA dynamics in two headwater streams , 2015, Molecular ecology resources.

[58]  M. Kondoh,et al.  The Release Rate of Environmental DNA from Juvenile and Adult Fish , 2014, PloS one.

[59]  K. Coyne,et al.  Improved Methods for Capture, Extraction, and Quantitative Assay of Environmental DNA from Asian Bigheaded Carp (Hypophthalmichthys spp.) , 2014, PloS one.

[60]  G. Moyer,et al.  History, applications, methodological issues and perspectives for the use of environmental DNA (eDNA) in marine and freshwater environments. , 2014, Revista de biologia tropical.

[61]  J. Amberg,et al.  Persistence of DNA in Carcasses, Slime and Avian Feces May Affect Interpretation of Environmental DNA Data , 2014, PloS one.

[62]  Andrew R Mahon,et al.  Quantifying environmental DNA signals for aquatic invasive species across multiple detection platforms. , 2014, Environmental science & technology.

[63]  Helen C. Rees,et al.  REVIEW: The detection of aquatic animal species using environmental DNA – a review of eDNA as a survey tool in ecology , 2014 .

[64]  P. Bajer,et al.  The Relationship between the Distribution of Common Carp and Their Environmental DNA in a Small Lake , 2014, PloS one.

[65]  F. Altermatt,et al.  Utility of Environmental DNA for Monitoring Rare and Indicator Macroinvertebrate Species , 2014, Freshwater Science.

[66]  P. Lambin,et al.  Decoding tumour phenotype by noninvasive imaging using a quantitative radiomics approach , 2014, Nature Communications.

[67]  M. Schlaepfer,et al.  Environmental DNA surveillance for invertebrate species: advantages and technical limitations to detect invasive crayfish Procambarus clarkii in freshwater ponds. , 2014 .

[68]  Jeffrey E. Hill,et al.  Assessing Environmental DNA Detection in Controlled Lentic Systems , 2014, PloS one.

[69]  Roman Marin,et al.  Multispecies diel transcriptional oscillations in open ocean heterotrophic bacterial assemblages , 2014, Science.

[70]  Margaret R. Caldwell,et al.  Harnessing DNA to improve environmental management , 2014, Science.

[71]  L. Fändriks,et al.  Surface area of the digestive tract – revisited , 2014, Scandinavian journal of gastroenterology.

[72]  A. Piaggio,et al.  Detecting an elusive invasive species: a diagnostic PCR to detect Burmese python in Florida waters and an assessment of persistence of environmental DNA , 2014, Molecular ecology resources.

[73]  F. Altermatt,et al.  Transport Distance of Invertebrate Environmental DNA in a Natural River , 2014, PloS one.

[74]  Roman Marin,et al.  Ecogenomic sensor reveals controls on N2-fixing microorganisms in the North Pacific Ocean , 2014, The ISME Journal.

[75]  D. Lodge,et al.  Particle size distribution and optimal capture of aqueous macrobial eDNA , 2014, bioRxiv.

[76]  Jesse A. Port,et al.  Using Environmental DNA to Census Marine Fishes in a Large Mesocosm , 2014, PloS one.

[77]  M. Otagiri,et al.  Cys34-Cysteinylated Human Serum Albumin Is a Sensitive Plasma Marker in Oxidative Stress-Related Chronic Diseases , 2014, PloS one.

[78]  Robert S. Arkle,et al.  Factors influencing detection of eDNA from a stream‐dwelling amphibian , 2014, Molecular ecology resources.

[79]  Naiara Rodríguez-Ezpeleta,et al.  Genomics in marine monitoring: new opportunities for assessing marine health status. , 2013, Marine pollution bulletin.

[80]  W. L. Chadderton,et al.  Environmental conditions influence eDNA persistence in aquatic systems. , 2014, Environmental science & technology.

[81]  P. Girguis,et al.  Autonomous application of quantitative PCR in the deep sea: in situ surveys of aerobic methanotrophs using the deep-sea environmental sample processor. , 2013, Environmental science & technology.

[82]  Adam J. Sepulveda,et al.  Environmental DNA as a new method for early detection of New Zealand mudsnails (Potamopyrgus antipodarum) , 2013, Freshwater Science.

[83]  Robert S. Arkle,et al.  Estimating occupancy and abundance of stream amphibians using environmental DNA from filtered water samples , 2013 .

[84]  E. Willerslev,et al.  Detection of a Diverse Marine Fish Fauna Using Environmental DNA from Seawater Samples , 2012, PloS one.

[85]  M. Thomas P. Gilbert,et al.  Investigating the Potential Use of Environmental DNA (eDNA) for Genetic Monitoring of Marine Mammals , 2012, PloS one.

[86]  S. Foote,et al.  A Novel ENU-Mutation in Ankyrin-1 Disrupts Malaria Parasite Maturation in Red Blood Cells of Mice , 2012, PloS one.

[87]  Z. Kawabata,et al.  Estimation of Fish Biomass Using Environmental DNA , 2012, PloS one.

[88]  P. Taberlet,et al.  Who is eating what: diet assessment using next generation sequencing , 2012, Molecular ecology.

[89]  P. Taberlet,et al.  Tracking earthworm communities from soil DNA , 2012, Molecular ecology.

[90]  P. Taberlet,et al.  Environmental DNA , 2012, Molecular ecology.

[91]  J. Ryan,et al.  Robotic sampling, in situ monitoring and molecular detection of marine zooplankton , 2012 .

[92]  Rob Ogden,et al.  Gene-associated markers provide tools for tackling illegal fishing and false eco-certification , 2012, Nature Communications.

[93]  L. Torrance,et al.  Unusual Features of Pomoviral RNA Movement , 2011, Front. Microbio..

[94]  V. V. Bulygin,et al.  Examination of Microbial Proteome Preservation Techniques Applicable to Autonomous Environmental Sample Collection , 2011, Front. Microbio..

[95]  P. Bustos,et al.  Genomic lineages of Rhizobium etli revealed by the extent of nucleotide polymorphisms and low recombination , 2011, BMC Evolutionary Biology.

[96]  B. Neville,et al.  Implication of RNA-Binding Protein La in Proliferation, Migration and Invasion of Lymph Node-Metastasized Hypopharyngeal SCC Cells , 2011, PloS one.

[97]  François Pompanon,et al.  Persistence of Environmental DNA in Freshwater Ecosystems , 2011, PloS one.

[98]  Robert S. Arkle,et al.  Molecular Detection of Vertebrates in Stream Water: A Demonstration Using Rocky Mountain Tailed Frogs and Idaho Giant Salamanders , 2011, PloS one.

[99]  T. Johnson,et al.  Utilization of stomach content DNA to determine diet diversity in piscivorous fishes. , 2011, Journal of fish biology.

[100]  T. Singer,et al.  Short-Term Compassion Training Increases Prosocial Behavior in a Newly Developed Prosocial Game , 2011, PloS one.

[101]  A. Kasarskis,et al.  A window into third-generation sequencing. , 2010, Human molecular genetics.

[102]  Eric Biber.  The Problem of Environmental Monitoring , 2010 .

[103]  J. Ascher,et al.  Extracellular DNA in soil and sediment: fate and ecological relevance , 2009, Biology and Fertility of Soils.

[104]  A. Dell'Anno,et al.  Damage and degradation rates of extracellular DNA in marine sediments: implications for the preservation of gene sequences , 2008, Molecular ecology.

[105]  P. Taberlet,et al.  Species detection using environmental DNA from water samples , 2008, Biology Letters.

[106]  P. Lumbiganon,et al.  Use of Evidence-Based Practices in Pregnancy and Childbirth: South East Asia Optimising Reproductive and Child Health in Developing Countries Project , 2008, PloS one.

[107]  E. Matisoo-Smith,et al.  Recovery of DNA and pollen from New Zealand lake sediments , 2008 .

[108]  Dirk Steinke,et al.  DNA barcoding for the identification of smoked fish products , 2008 .

[109]  M. Oetterer,et al.  Use of fish waste as silage: a review , 2007 .

[110]  Natalia Ivanova,et al.  Universal primer cocktails for fish DNA barcoding , 2007 .

[111]  Jae S. Choi,et al.  Reconciling differences in trophic control in mid-latitude marine ecosystems. , 2006, Ecology letters.

[112]  Julian Lewis,et al.  Organizing cell renewal in the intestine: stem cells, signals and combinatorial control , 2006, Nature Reviews Genetics.

[113]  F. Panara,et al.  A nondestructive, rapid, reliable and inexpensive method to sample, store and extract high‐quality DNA from fish body mucus and buccal cells , 2006 .

[114]  John F. Steffensen,et al.  The response of Atlantic cod, Gadus morhua, to progressive hypoxia: fish swimming speed and physiological stress , 2005 .

[115]  P. C. Reid,et al.  Plankton effect on cod recruitment in the North Sea , 2003, Nature.

[116]  Martin I. Taylor,et al.  Species‐specific TaqMan probes for simultaneous identification of (Gadus morhua L.), haddock (Melanogrammus aeglefinus L.) and whiting (Merlangius merlangus L.). , 2002 .

[117]  A. Clarke,et al.  Scaling of metabolic rate with body mass and temperature in teleost fish , 1999 .

[118]  R. Waples.  Separating the wheat from the chaff: patterns of genetic differentiation in high gene flow species , 1998 .

[119]  J. Steffensen,et al.  Effects of temperature, hypoxia and activity on the metabolism of juvenile Atlantic cod , 1997 .

[120]  J. Lee,et al.  Metabolic ontogeny of teleost fishes , 1996 .

[121]  M. G. Lorenz,et al.  Bacterial gene transfer by natural genetic transformation in the environment. , 1994, Microbiological reviews.

[122]  D. Skibinski,et al.  A comparison of genetic diversity levels in marine, freshwater, and anadromous fishes , 1994 .

[123]  J. B. Jones.  Environmental impact of trawling on the seabed: A review , 1992 .

[124]  R. Thresher,et al.  Phytoplankton production pulses and episodic settlement of a temperate marine fish , 1989, Nature.

[125]  J. Paul,et al.  Dynamics of extracellular DNA in the marine environment , 1987, Applied and environmental microbiology.

[126]  E. Nielsen.  Population or Point-of-Origin Identification , 2016 .

[127]  David R. Smith,et al.  Environmental DNA calibration study. Interim technical review report , 2014 .

[128]  Mogens Schou,et al.  Dansk fiskeris udnyttelse af discardforbuddet: En udredning , 2013 .

[129]  S. Alasaad,et al.  Efficient identification of Microtus cabrerae excrements using noninvasive molecular analysis , 2010, Conservation Genetics Resources.

[130]  James H. Brown,et al.  UNM Digital Repository UNM Digital Repository Effects of size and temperature on metabolic rate Effects of size and temperature on metabolic rate , 2022 .