Environmental DNA reveals quantitative patterns of fish biodiversity in large rivers despite its downstream transportation

Despite the ecological and societal importance of large rivers, fish sampling remains costly and limited to specific habitats (e.g., river banks). Using an eDNA metabarcoding approach, we regularly sampled 500 km of a large river (Rhône River). Comparisons with long-term electrofishing surveys demonstrated the ability of eDNA metabarcoding to qualitatively and quantitatively reveal fish assemblage structures (relative species abundance) but eDNA integrated a larger space than the classical sampling location. Combination of a literature review and field data showed that eDNA behaves in the water column like fine particulate organic matter. Its detection distance varied from a few km in a small stream to more than 100 km in a large river. To our knowledge, our results are the first demonstration of the capacity of eDNA metabarcoding to describe longitudinal fish assemblage patterns in a large river, and metabarcoding appears to be a reliable, cost-effective method for future monitoring.

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

[2]  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.

[3]  Carol A. Stepien,et al.  Environmental DNA (eDNA) metabarcoding assays to detect invasive invertebrate species in the Great Lakes , 2017, PloS one.

[4]  L. Handley How will the ‘molecular revolution’ contribute to biological recording? , 2015 .

[5]  Jean Thioulouse,et al.  CO‐INERTIA ANALYSIS AND THE LINKING OF ECOLOGICAL DATA TABLES , 2003 .

[6]  Emanuel A. Fronhofer,et al.  Environmental DNA reveals that rivers are conveyer belts of biodiversity information , 2016, Nature Communications.

[7]  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 .

[8]  N. Pettorelli,et al.  Essential Biodiversity Variables , 2013, Science.

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

[10]  William N. Venables,et al.  Modern Applied Statistics with S , 2010 .

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

[12]  P. Legendre,et al.  vegan : Community Ecology Package. R package version 1.8-5 , 2007 .

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

[14]  D. Gleeson,et al.  Environmental DNA monitoring and management of invasive fish: comparison of eDNA and fyke netting , 2017 .

[15]  P. Taberlet,et al.  Towards next‐generation biodiversity assessment using DNA metabarcoding , 2012, Molecular ecology.

[16]  R. A. A. Noble,et al.  Manual for the application of the new European Fish Index - EFI+. A fish-based method to assess the ecological status of European running waters in support of the Water Framework Directive. , 2005 .

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

[18]  C. Wiuf,et al.  Monitoring endangered freshwater biodiversity using environmental DNA. , 2012, Molecular ecology.

[19]  Paul Nichols,et al.  Environmental DNA metabarcoding of lake fish communities reflects long‐term data from established survey methods , 2016, Molecular ecology.

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

[21]  Brian D. Ripley,et al.  Modern Applied Statistics with S Fourth edition , 2002 .

[22]  J. Nichols,et al.  IMPROVING INFERENCES IN POPULATION STUDIES OF RARE SPECIES THAT ARE DETECTED IMPERFECTLY , 2005 .

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

[24]  H. Doi,et al.  Environmental DNA analysis for estimating the abundance and biomass of stream fish , 2017 .

[25]  M. Miya,et al.  Comparing local‐ and regional‐scale estimations of the diversity of stream fish using eDNA metabarcoding and conventional observation methods , 2018 .

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

[27]  Gregory D. Williams,et al.  A framework for inferring biological communities from environmental DNA. , 2016, Ecological applications : a publication of the Ecological Society of America.

[28]  D. Lodge,et al.  Estimating species richness using environmental DNA , 2016, Ecology and evolution.

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

[30]  Douglas W. Yu,et al.  Environmental DNA for wildlife biology and biodiversity monitoring. , 2014, Trends in ecology & evolution.

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

[32]  Carsten Wiuf,et al.  Diverse Plant and Animal Genetic Records from Holocene and Pleistocene Sediments , 2003, Science.

[33]  W. L. Chadderton,et al.  “Sight‐unseen” detection of rare aquatic species using environmental DNA , 2011 .

[34]  D. Pont,et al.  Using γ-emitting artificial radionuclides, released by nuclear plants, as markers of restricted movements by chub,Leuciscus cephalus, in a large river, the Lower Rhône , 1994, Environmental Biology of Fishes.

[35]  J. Newbold,et al.  The influence of particle size on seston deposition in streams , 2001 .

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

[37]  R. Meier,et al.  Next-generation freshwater bioassessment: eDNA metabarcoding with a conserved metazoan primer reveals species-rich and reservoir-specific communities , 2016, Royal Society Open Science.

[38]  John A Darling,et al.  From molecules to management: adopting DNA-based methods for monitoring biological invasions in aquatic environments. , 2011, Environmental research.

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

[40]  C. Wolter,et al.  The gain of additional sampling methods for the fish-based assessment of large rivers , 2018 .

[41]  J. Newbold,et al.  Physical factors influencing fine organic particle transport and deposition in streams , 2000, Journal of the North American Benthological Society.

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

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

[44]  B. Baldigo,et al.  Efficacy of Environmental DNA to Detect and Quantify Brook Trout Populations in Headwater Streams of the Adirondack Mountains, New York , 2017 .

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

[46]  Stéphane Dray,et al.  The ade4 Package-II: Two-table and K-table Methods , 2007 .

[47]  P. Taberlet,et al.  Spatial Representativeness of Environmental DNA Metabarcoding Signal for Fish Biodiversity Assessment in a Natural Freshwater System , 2016, PloS one.

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

[49]  Adam J. Sepulveda,et al.  Understanding environmental DNA detection probabilities: A case study using a stream-dwelling char Salvelinus fontinalis , 2015 .

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

[51]  P. Taberlet,et al.  Next‐generation monitoring of aquatic biodiversity using environmental DNA metabarcoding , 2016, Molecular ecology.

[52]  T. Erős,et al.  Typology of a Great River Using Fish Assemblages: Implications for the Bioassessment of the Danube River , 2017 .

[53]  Kristy Deiner,et al.  Environmental DNA metabarcoding: Transforming how we survey animal and plant communities , 2017, Molecular ecology.