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Journal Article•DOI•

“Sight‐unseen” detection of rare aquatic species using environmental DNA

Christopher L. Jerde1, Andrew R. Mahon1, W. Lindsay Chadderton2, David M. Lodge1•
University of Notre Dame1, The Nature Conservancy2
01 Apr 2011-Conservation Letters (Blackwell Publishing Inc)-Vol. 4, Iss: 2, pp 150-157
TL;DR: Quantitative comparisons with traditional fisheries surveillance tools illustrate the greater sensitivity of eDNA and reveal that the risk of invasion to the Laurentian Great Lakes is imminent.
Abstract: Effective management of rare species, including endangered native species and recently introduced nonindigenous species, requires the detection of populations at low density. For endangered species, detecting the localized distribution makes it possible to identify and protect critical habitat to enhance survival or reproductive success. Similarly, early detection of an incipient invasion by a harmful species increases the feasibility of rapid responses to eradicate the species or contain its spread. Here we demonstrate the efficacy of environmental DNA (eDNA) as a detection tool in freshwater environments. Specifically, we delimit the invasion fronts of two species of Asian carps in Chicago, Illinois, USA area canals and waterways. Quantitative comparisons with traditional fisheries surveillance tools illustrate the greater sensitivity of eDNA and reveal that the risk of invasion to the Laurentian Great Lakes is imminent.

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Citations
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Journal Article•DOI•
Environmental DNA - An emerging tool in conservation for monitoring past and present biodiversity

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Philip Francis Thomsen1, Eske Willerslev1•
University of Copenhagen1
01 Mar 2015-Biological Conservation
TL;DR: The achievements gained through analyses of eDNA from macro-organisms in a conservation context are reviewed, its potential advantages and limitations are discussed, and it is expected the eDNA-based approaches to move from single-marker analyses of species or communities to meta-genomic surveys of entire ecosystems to predict spatial and temporal biodiversity patterns.

1,278 citations

Cites background or result from "“Sight‐unseen” detection of rare aq..."

  • ...Nevertheless, several studies report shorter handling time and lower cost using eDNA compared to traditional monitoring techniques (Jerde et al., 2011; Biggs et al., 2015; Sigsgaard et al., 2015)....

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  • ...Jerde et al. (2011) studied two species of Asian carps in river systems, which demonstrated that the forefronts of the species were closer to invasion of upstream lake systems than initially seen by traditional surveillance methods....

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Journal Article•DOI•
Environmental DNA metabarcoding: transforming how we survey animal and plant communities

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Kristy Deiner1, Holly M. Bik2, Elvira Mächler3, Elvira Mächler4, Mathew Seymour5, Anaïs Lacoursière-Roussel6, Florian Altermatt4, Florian Altermatt3, Simon Creer5, Iliana Bista7, Iliana Bista5, David M. Lodge1, Natasha de Vere8, Michael E. Pfrender9, Louis Bernatchez6 •
Cornell University1, University of California, Riverside2, Swiss Federal Institute of Aquatic Science and Technology3, University of Zurich4, Bangor University5, Laval University6, Wellcome Trust Sanger Institute7, Aberystwyth University8, University of Notre Dame9
01 Nov 2017-Molecular Ecology
TL;DR: The use of eDNA metabarcoding for surveying animal and plant richness, and the challenges in using eDNA approaches to estimate relative abundance are reviewed, which distill what is known about the ability of different eDNA sample types to approximate richness in space and across time.
Abstract: The genomic revolution has fundamentally changed how we survey biodiversity on earth. High-throughput sequencing ("HTS") platforms now enable the rapid sequencing of DNA from diverse kinds of environmental samples (termed "environmental DNA" or "eDNA"). Coupling HTS with our ability to associate sequences from eDNA with a taxonomic name is called "eDNA metabarcoding" and offers a powerful molecular tool capable of noninvasively surveying species richness from many ecosystems. Here, we review the use of eDNA metabarcoding for surveying animal and plant richness, and the challenges in using eDNA approaches to estimate relative abundance. We highlight eDNA applications in freshwater, marine and terrestrial environments, and in this broad context, we distill what is known about the ability of different eDNA sample types to approximate richness in space and across time. We provide guiding questions for study design and discuss the eDNA metabarcoding workflow with a focus on primers and library preparation methods. We additionally discuss important criteria for consideration of bioinformatic filtering of data sets, with recommendations for increasing transparency. Finally, looking to the future, we discuss emerging applications of eDNA metabarcoding in ecology, conservation, invasion biology, biomonitoring, and how eDNA metabarcoding can empower citizen science and biodiversity education.

1,038 citations

Journal Article•DOI•
Monitoring endangered freshwater biodiversity using environmental DNA

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Philip Francis Thomsen1, Jos Kielgast1, Lars Iversen1, Carsten Wiuf2, Morten Rasmussen1, M. Thomas P. Gilbert1, Ludovic Orlando1, Eske Willerslev1 •
University of Copenhagen1, Aarhus University2
01 Jun 2012-Molecular Ecology
TL;DR: It is demonstrated that entire faunas of amphibians and fish can be detected by high-throughput sequencing of DNA extracted from pond water, underpin the ubiquitous nature of DNA traces in the environment and establish environmental DNA as a tool for monitoring rare and threatened species across a wide range of taxonomic groups.
Abstract: Freshwater ecosystems are among the most endangered habitats on Earth, with thousands of animal species known to be threatened or already extinct. Reliable monitoring of threatened organisms is crucial for data-driven conservation actions but remains a challenge owing to nonstandardized methods that depend on practical and taxonomic expertise, which is rapidly declining. Here, we show that a diversity of rare and threatened freshwater animals—representing amphibians, fish, mammals, insects and crustaceans—can be detected and quantified based on DNA obtained directly from small water samples of lakes, ponds and streams. We successfully validate our findings in a controlled mesocosm experiment and show that DNA becomes undetectable within 2 weeks after removal of animals, indicating that DNA traces are near contemporary with presence of the species. We further demonstrate that entire faunas of amphibians and fish can be detected by high-throughput sequencing of DNA extracted from pond water. Our findings underpin the ubiquitous nature of DNA traces in the environment and establish environmental DNA as a tool for monitoring rare and threatened species across a wide range of taxonomic groups.

951 citations

Cites background or methods from "“Sight‐unseen” detection of rare aq..."

  • ...Although of great potential for contemporary biodiversity monitoring, environmental DNA detection in wild populations has so far only been applied to a few common or invasive species of amphibians and fish (Ficetola et al. 2008; Goldberg et al. 2011; Jerde et al. 2011)....

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  • ...Precipitation, as used in this study, recovers DNA independent of state but is limited to small sample volumes compared to filtering methods (e.g. Jerde et al. 2011), which accommodate larger samples but may fail to recover free DNA....

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  • ...sity monitoring, environmental DNA detection in wild populations has so far only been applied to a few common or invasive species of amphibians and fish (Ficetola et al. 2008; Goldberg et al. 2011; Jerde et al. 2011)....

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  • ...used on several different modern and ancient environmental samples including terrestrial sediments, lake and ice cores, and freshwater lakes and rivers (Hofreiter et al. 2003; Haile et al. 2007, 2009; Willerslev et al. 2007; Ficetola et al. 2008; Matisoo-Smith et al. 2008; Jerde et al. 2011)....

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  • ...…used on several different modern and ancient environmental samples including terrestrial sediments, lake and ice cores, and freshwater lakes and rivers (Hofreiter et al. 2003; Haile et al. 2007, 2009; Willerslev et al. 2007; Ficetola et al. 2008; Matisoo-Smith et al. 2008; Jerde et al. 2011)....

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Journal Article•DOI•
Environmental DNA for wildlife biology and biodiversity monitoring

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Kristine Bohmann1, Kristine Bohmann2, Alice Evans3, M. Thomas P. Gilbert1, M. Thomas P. Gilbert4, Gary R. Carvalho3, Simon Creer3, Michael Knapp3, Douglas W. Yu5, Douglas W. Yu6, Mark de Bruyn3 •
University of Copenhagen1, University of Bristol2, Bangor University3, Curtin University4, Kunming Institute of Zoology5, University of East Anglia6
01 Jun 2014-Trends in Ecology and Evolution
TL;DR: In this paper, the authors examine the current frontiers of eDNA, outline key aspects requiring improvement, and suggest future developments and innovations for research, including improved ability to explore ecosystem-level processes, the generation of quantitative indices for analyses of species, community diversity, and dynamics, and novel opportunities through the use of time-serial samples and unprecedented sensitivity for detecting rare or difficult-to-sample taxa.
Abstract: Extraction and identification of DNA from an environmental sample has proven noteworthy recently in detecting and monitoring not only common species, but also those that are endangered, invasive, or elusive. Particular attributes of so-called environmental DNA (eDNA) analysis render it a potent tool for elucidating mechanistic insights in ecological and evolutionary processes. Foremost among these is an improved ability to explore ecosystem-level processes, the generation of quantitative indices for analyses of species, community diversity, and dynamics, and novel opportunities through the use of time-serial samples and unprecedented sensitivity for detecting rare or difficult-to-sample taxa. Although technical challenges remain, here we examine the current frontiers of eDNA, outline key aspects requiring improvement, and suggest future developments and innovations for research.

849 citations

Environmental DNA for wildlife biology and biodiversity monitoring (vol 29, pg 358, 2014)

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Kristine Bohmann, Evans A, Gilbert Mtp, Gary R. Carvalho, Simon Creer, Knapp M, Yu Dw, de Bruyn M 
01 Jan 2014
TL;DR: The current frontiers of eDNA are examined, key aspects requiring improvement are outlined, and future developments and innovations for research are suggested.

752 citations

References
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Journal Article•DOI•
MEGA: A biologist-centric software for evolutionary analysis of DNA and protein sequences

[...]

Sudhir Kumar1, Masatoshi Nei2, Joel T. Dudley3, Koichiro Tamura4•
Arizona State University1, Pennsylvania State University2, Stanford University3, Tokyo Metropolitan University4
01 Jul 2008-Briefings in Bioinformatics
TL;DR: The motivation, design principles and priorities that have shaped the development of MEGA are discussed and how MEGA might evolve in the future to assist researchers in their growing need to analyze large data set using new computational methods are discussed.
Abstract: The Molecular Evolutionary Genetics Analysis (MEGA) software is a desktop application designed for comparative analysis of homologous gene sequences either from multigene families or from different species with a special emphasis on inferring evolutionary relationships and patterns of DNA and protein evolution. In addition to the tools for statistical analysis of data, MEGA provides many convenient facilities for the assembly of sequence data sets from files or web-based repositories, and it includes tools for visual presentation of the results obtained in the form of interactive phylogenetic trees and evolutionary distance matrices. Here we discuss the motivation, design principles and priorities that have shaped the development of MEGA. We also discuss how MEGA might evolve in the future to assist researchers in their growing need to analyze large data set using new computational methods.

3,290 citations

"“Sight‐unseen” detection of rare aq..." refers background or methods in this paper

  • ...S. et al. (2010) A mark-recapture population estimate for invasive silver carp (Hypophthalmichthys molitrix) in the La Grange Reach, Illinois River. Biol Invasions 12, 433–436. Sampson, S.J., Chick J.H., Pegg M.A. (2009) Diet overlap among two Asian carp and three native fishes in backwater lakes on the Illinois and Mississippi Rivers. Biol Invasions 11, 483–496. Taberlet, P. (1996) The use of mitochondrial DNA control region sequencing in conservation genetics. Pages 125–142 in T. Bates-Smith , R.K. Wayne, editors. Molecular genetic approaches in conservation. Oxford University Press, New York. Thompson, W.L. (2004) Introduction to sampling rare or elusive species. Pages 1–7 in W.L. Thompson, editor. Sampling rare or elusive species. Island Press, New York. USACE. (2010) Dispersal Barrier Efficacy Study: interim 1 – Dispersal Barrier Bypass Risk Reduction Study & Integrated Environmental Assessment....

    [...]

  • ...S. et al. (2010) A mark-recapture population estimate for invasive silver carp (Hypophthalmichthys molitrix) in the La Grange Reach, Illinois River. Biol Invasions 12, 433–436. Sampson, S.J., Chick J.H., Pegg M.A. (2009) Diet overlap among two Asian carp and three native fishes in backwater lakes on the Illinois and Mississippi Rivers. Biol Invasions 11, 483–496. Taberlet, P. (1996) The use of mitochondrial DNA control region sequencing in conservation genetics. Pages 125–142 in T. Bates-Smith , R.K. Wayne, editors. Molecular genetic approaches in conservation. Oxford University Press, New York. Thompson, W.L. (2004) Introduction to sampling rare or elusive species....

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  • ...S. et al. (2010) A mark-recapture population estimate for invasive silver carp (Hypophthalmichthys molitrix) in the La Grange Reach, Illinois River. Biol Invasions 12, 433–436. Sampson, S.J., Chick J.H., Pegg M.A. (2009) Diet overlap among two Asian carp and three native fishes in backwater lakes on the Illinois and Mississippi Rivers. Biol Invasions 11, 483–496. Taberlet, P. (1996) The use of mitochondrial DNA control region sequencing in conservation genetics....

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  • ...S. et al. (2010) A mark-recapture population estimate for invasive silver carp (Hypophthalmichthys molitrix) in the La Grange Reach, Illinois River. Biol Invasions 12, 433–436. Sampson, S.J., Chick J.H., Pegg M.A. (2009) Diet overlap among two Asian carp and three native fishes in backwater lakes on the Illinois and Mississippi Rivers. Biol Invasions 11, 483–496. Taberlet, P. (1996) The use of mitochondrial DNA control region sequencing in conservation genetics. Pages 125–142 in T. Bates-Smith , R.K. Wayne, editors. Molecular genetic approaches in conservation. Oxford University Press, New York. Thompson, W.L. (2004) Introduction to sampling rare or elusive species. Pages 1–7 in W.L. Thompson, editor. Sampling rare or elusive species. Island Press, New York. USACE. (2010) Dispersal Barrier Efficacy Study: interim 1 – Dispersal Barrier Bypass Risk Reduction Study & Integrated Environmental Assessment. United States Army Corps of Engineers, Chicago District. Final Report. Williamson, C.J., Garvey J.E. (2005) Growth, fecundity, and diets of newly established silver carp in the middle Mississippi River....

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  • ...The genetic distance (as uncorrected p genetic distance calculated using MEGA 4.0; Kumar et al. 2008) between this fragment of DNA for bighead carp and other species is: silver carp, 13.7%; and common carp, 25.2%....

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Journal Article•DOI•
The role of propagule pressure in explaining species invasions.

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Julie L. Lockwood1, Phillip Cassey2, Tim M. Blackburn2•
Rutgers University1, University of Birmingham2
01 May 2005-Trends in Ecology and Evolution
TL;DR: Propagule pressure is proposed as a key element to understanding why some introduced populations fail to establish whereas others succeed and how the study of propagule pressure can provide an opportunity to tie together disparate research agendas within invasion ecology.
Abstract: Human-mediated species invasions are a significant component of current global environmental change. There is every indication that the rate at which locations are accumulating non-native species is accelerating as free trade and globalization advance. Thus, the need to incorporate predictive models in the assessment of invasion risk has become acute. However, finding elements of the invasion process that provide consistent explanatory power has proved elusive. Here, we propose propagule pressure as a key element to understanding why some introduced populations fail to establish whereas others succeed. In the process, we illustrate how the study of propagule pressure can provide an opportunity to tie together disparate research agendas within invasion ecology.

2,288 citations

"“Sight‐unseen” detection of rare aq..." refers background in this paper

  • ...It is not therefore inevitable that either bighead or silver carps will establish populations in Lake Michigan, especially if the numbers of individuals with access to Lake Michigan can be reduced (Lockwood et al. 2005)....

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Journal Article•DOI•
Species detection using environmental DNA from water samples.

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Gentile Francesco Ficetola1, Claude Miaud2, François Pompanon3, Pierre Taberlet3•
Joseph Fourier University1, University of Savoy2, Centre national de la recherche scientifique3
23 Aug 2008-Biology Letters
TL;DR: A novel approach, based on the limited persistence of DNA in the environment, to detect the presence of a species in fresh water, using specific primers that amplify short mitochondrial DNA sequences to track the existence of a frog in controlled environments and natural wetlands.
Abstract: The assessment of species distribution is a first critical phase of biodiversity studies and is necessary to many disciplines such as biogeography, conservation biology and ecology. However, several species are difficult to detect, especially during particular time periods or developmental stages, potentially biasing study outcomes. Here we present a novel approach, based on the limited persistence of DNA in the environment, to detect the presence of a species in fresh water. We used specific primers that amplify short mitochondrial DNA sequences to track the presence of a frog (Rana catesbeiana) in controlled environments and natural wetlands. A multi-sampling approach allowed for species detection in all environments where it was present, even at low densities. The reliability of the results was demonstrated by the identification of amplified DNA fragments, using traditional sequencing and parallel pyrosequencing techniques. As the environment can retain the molecular imprint of inhabiting species, our approach allows the reliable detection of secretive organisms in wetlands without direct observation. Combined with massive sequencing and the development of DNA barcodes that enable species identification, this approach opens new perspectives for the assessment of current biodiversity from environmental samples.

1,226 citations

"“Sight‐unseen” detection of rare aq..." refers background in this paper

  • ...This conservation application of the eDNA method was inspired by previous identification of whales (Megaptera novaeangliae, 150 Conservation Letters 4 (2011) 150–157 Copyright and Photocopying: c©2011 Wiley Periodicals, Inc. Physeter macrocephalus, and Eubalaena glacialis) using DNA in the backwash and feces of diving individuals (Amos et al. 1992), and the use of DNA to detect bullfrogs (Rana catesbeiana) in ponds in France (Ficetola et al. 2008)....

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  • ...…150–157 Copyright and Photocopying: c©2011 Wiley Periodicals, Inc. Physeter macrocephalus, and Eubalaena glacialis) using DNA in the backwash and feces of diving individuals (Amos et al. 1992), and the use of DNA to detect bullfrogs (Rana catesbeiana) in ponds in France (Ficetola et al. 2008)....

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Journal Article•DOI•
Biological invasions: recommendations for U.S. policy and management.

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David M. Lodge1, Susan L. Williams2, Hugh J. MacIsaac3, Keith R. Hayes4, Brian Leung1, Sarah H. Reichard5, Richard N. Mack6, Peter B. Moyle2, Maggie Smith7, David A. Andow8, James T. Carlton9, Anthony J. McMichael10 •
University of Notre Dame1, University of California, Davis2, University of Windsor3, CSIRO Marine and Atmospheric Research4, University of Washington5, Washington State University6, Ecological Society of America7, University of Minnesota8, Williams College9, Australian National University10
01 Dec 2006-Ecological Applications
TL;DR: The Ecological Society of America recommends that the federal government take the following six actions: use new information and practices to better manage commercial and other pathways to reduce the transport and release of potentially harmful species, and establish a National Center for Invasive Species Management.
Abstract: The Ecological Society of America has evaluated current U.S. national policies and practices on biological invasions in light of current scientific knowledge. Invasions by harmful nonnative species are increasing in number and area affected; the damages to ecosystems, economic activity, and human welfare are accumulating. Without improved strategies based on recent scientific advances and increased investments to counter invasions, harm from invasive species is likely to accelerate. Federal leadership, with the cooperation of state and local governments, is required to increase the effectiveness of prevention of invasions, detect and respond quickly to new potentially harmful invasions, control and slow the spread of existing invasions, and provide a national center to ensure that these efforts are coordinated and cost effective. Specifically, the Ecological Society of America recommends that the federal government take the following six actions: (1) Use new information and practices to better manage commercial and other pathways to reduce the transport and release of potentially harmful species; (2) Adopt more quantitative procedures for risk analysis and apply them to every species proposed for importation into the country; (3) Use new cost-effective diagnostic technologies to increase active surveillance and sharing of information about invasive species so that responses to new invasions can be more rapid and effective; (4) Create new legal authority and provide emergency funding to support rapid responses to emerging invasions; (5) Provide funding and incentives for cost-effective programs to slow the spread of existing invasive species in order to protect still uninvaded ecosystems, social and industrial infrastructure, and human welfare; and (6) Establish a National Center for Invasive Species Management (under the existing National Invasive Species Council) to coordinate and lead improvements in federal, state, and international policies on invasive species. Recent scientific and technical advances provide a sound basis for more cost-effective national responses to invasive species. Greater investments in improved technology and management practices would be more than repaid by reduced damages from current and future invasive species. The Ecological Society of America is committed to assist all levels of government and provide scientific advice to improve all aspects of invasive-species management.

908 citations

"“Sight‐unseen” detection of rare aq..." refers background in this paper

  • ...In the absence of tools to detect rare species, uncertainty about when, where, and for how long a management action should be implemented often results in inaction or ineffective use of management resources (Thompson 2004; Lodge et al. 2006)....

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Journal Article•DOI•
An ounce of prevention or a pound of cure: bioeconomic risk analysis of invasive species

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Brian Leung1, David M. Lodge1, David Finnoff2, Jason F. Shogren3, Mark A. Lewis4, Gary A. Lamberti1 •
University of Notre Dame1, University of Central Florida2, University of Wyoming3, University of Alberta4
07 Dec 2002-Proceedings of The Royal Society B: Biological Sciences
TL;DR: A quantitative bioeconomic modelling framework is presented to analyse risks from non–indigenous species to economic activity and the environment, and it is shown that society could benefit by spending up to US$324 000 year−1 to prevent invasions into a single lake with a power plant.
Abstract: Numbers of non-indigenous species--species introduced from elsewhere - are increasing rapidly worldwide, causing both environmental and economic damage. Rigorous quantitative risk-analysis frameworks, however, for invasive species are lacking. We need to evaluate the risks posed by invasive species and quantify the relative merits of different management strategies (e.g. allocation of resources between prevention and control). We present a quantitative bioeconomic modelling framework to analyse risks from non-indigenous species to economic activity and the environment. The model identifies the optimal allocation of resources to prevention versus control, acceptable invasion risks and consequences of invasion to optimal investments (e.g. labour and capital). We apply the model to zebra mussels (Dreissena polymorpha), and show that society could benefit by spending up to US$324 000 year(-1) to prevent invasions into a single lake with a power plant. By contrast, the US Fish and Wildlife Service spent US$825 000 in 2001 to manage all aquatic invaders in all US lakes. Thus, greater investment in prevention is warranted.

845 citations

"“Sight‐unseen” detection of rare aq..." refers background in this paper

  • ...Targeting management earlier and in more appropriate locations will also improve the cost effectiveness of management (Leung et al. 2002)....

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Related Papers (5)
Species detection using environmental DNA from water samples.

[...]

23 Aug 2008-Biology Letters
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Monitoring endangered freshwater biodiversity using environmental DNA

[...]

01 Jun 2012-Molecular Ecology
Philip Francis Thomsen, Jos Kielgast, Lars Iversen, Carsten Wiuf, Morten Rasmussen, M. Thomas P. Gilbert, Ludovic Orlando, Eske Willerslev 
Estimation of fish biomass using environmental DNA.

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26 Apr 2012-PLOS ONE
Teruhiko Takahara, Toshifumi Minamoto, Hiroki Yamanaka, Hideyuki Doi, Zen'ichiro Kawabata 
Detection of a diverse marine fish fauna using environmental DNA from seawater samples.

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29 Aug 2012-PLOS ONE
Philip Francis Thomsen, Jos Kielgast, Lars Iversen, Peter Rask Møller, Morten Rasmussen, Eske Willerslev 
Persistence of environmental DNA in freshwater ecosystems.

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08 Aug 2011-PLOS ONE
Tony Dejean, Alice Valentini, Antoine Duparc, Stéphanie Pellier-Cuit, François Pompanon, Pierre Taberlet, Claude Miaud