Improved detection of an alien invasive species through environmental DNA barcoding: the example of the American bullfrog Lithobates catesbeianus

Summary 1. Alien invasive species (AIS) are one of the major causes of biodiversity loss and global homogenization. Once an AIS becomes established, costs of control can be extremely high and complete eradication is not always achieved. The ability to detect a species at a low density greatly improves the success of eradication and decreases both the costs of control and the impact on ecosystems. 2. In this study, we compare the sensitivity of traditional field methods, based on auditory and visual encounter surveys, with an environmental DNA (eDNA) survey for the detection of the American bullfrog Rana catesbeiana = Lithobates catesbeianus, which is invasive in south-western France. 3. We demonstrate that the eDNA method is valuable for species detection and surpasses traditional amphibian survey methods in terms of sensitivity and sampling effort. The bullfrog was detected in 38 sites using the molecular method, compared with seven sites using the diurnal and nocturnal surveys, suggesting that traditional field surveys have strongly underestimated the distribution of the American bullfrog. 4. Synthesis and applications. The environmental DNA approach permits the early detection of alien invasive species (AIS), at very low densities and at any life stage, which is particularly important for the detection of rare and ⁄ or secretive aquatic species. This method can also be used to confirm the sensitivity of control operations and to better identify the distributions of vulnerable species, making this a very relevant tool for species inventory and management.

[1]  G. Ficetola,et al.  Pattern of distribution of the American bullfrog Rana catesbeiana in Europe , 2007, Biological Invasions.

[2]  P. Taberlet,et al.  DNA barcoding for ecologists. , 2009, Trends in ecology & evolution.

[3]  E. Gilder,et al.  The Authors , 1977 .

[4]  C. Lever Naturalized Reptiles and Amphibians of the World , 2003 .

[5]  B. Schmidt,et al.  Monitoring distributions using call surveys: estimating site occupancy, detection probabilities and inferring absence. , 2005 .

[6]  Gregg Howald,et al.  Invasive Rodent Eradication on Islands , 2007, Conservation biology : the journal of the Society for Conservation Biology.

[7]  P Taberlet,et al.  Reliable genotyping of samples with very low DNA quantities using PCR. , 1996, Nucleic acids research.

[8]  P. Hulme Beyond control : wider implications for the management of biological invasions , 2006 .

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

[10]  S. Lowe,et al.  100 of the world's worst invasive alien species. A selection from the global invasive species database , 2004 .

[11]  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.

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

[13]  P. M. Galetti,et al.  Chromosome Studies of Serrasalmus spilopleura (Characidae, Serrasalminae) from the Parana-Paraguay Rivers: Evolutionary and Cytotaxonomic Considerations , 1992 .

[14]  B. Schmidt,et al.  Quantifying abundance: Counts, detection probabilities and estimates , 2009 .

[15]  Thierry Vermat,et al.  Power and limitations of the chloroplast trnL (UAA) intron for plant DNA barcoding , 2006, Nucleic acids research.

[16]  D. Simberloff,et al.  Eradication revisited: dealing with exotic species. , 2000, Trends in ecology & evolution.

[17]  David R. Anderson,et al.  Model selection and multimodel inference : a practical information-theoretic approach , 2003 .

[18]  D. MacKenzie Occupancy Estimation and Modeling: Inferring Patterns and Dynamics of Species Occurrence , 2005 .

[19]  H. Poinar,et al.  Ancient DNA: Do It Right or Not at All , 2000, Science.

[20]  C. Kenneth Dodd,et al.  Amphibian Ecology and Conservation: A Handbook of Techniques , 2009 .

[21]  Peter W. C. Paton,et al.  Assessing the Use of Call Surveys to Monitor Breeding Anurans in Rhode Island , 2002 .

[22]  J. Ehrenfeld Ecosystem Consequences of Biological Invasions , 2010 .

[23]  Kristen S. Genet,et al.  Evaluation of methods and data quality from a volunteer-based amphibian call survey , 2003 .

[24]  W. Ingram,et al.  Additional Studies on the Movement of Tagged Bullfrogs, Rana catesbeiana Shaw , 1943 .

[25]  Wilfried Thuiller,et al.  Prediction and validation of the potential global distribution of a problematic alien invasive species — the American bullfrog , 2007 .

[26]  Issg 100 of the World’s Worst Invasive Alien Species: A Selection From The Global Invasive Species Database , 2000 .

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

[28]  J. Andrew Royle,et al.  Modeling Anuran Detection and Site Occupancy on North American Amphibian Monitoring Program (NAAMP) Routes in Maryland , 2009 .

[29]  N. Baeshen,et al.  Biological Identifications Through DNA Barcodes , 2012 .

[30]  T. S. Baskett,et al.  Emergence, Breeding, Hibernation, Movements and Transformation of the Bullfrog, Rana catesbeiana, in Missouri , 1956 .

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

[32]  H. Shaffer,et al.  Annual review of ecology, evolution, and systematics , 2003 .

[33]  A. Solow,et al.  Measuring biological diversity , 2006, Environmental and Ecological Statistics.

[34]  Petr Pyšek,et al.  Invasive Species, Environmental Change and Management, and Health , 2010 .

[35]  M. Ryan The Reproductive Behavior of the Bullfrog (Rana catesbeiana) , 1980 .

[36]  K. Fernie,et al.  Effect of sampling effort and species detectability on volunteer based anuran monitoring programs , 2005 .

[37]  Chad T. Harvey,et al.  Detection of a colonizing, aquatic, non‐indigenous species , 2009 .

[38]  P. Vitousek,et al.  INTRODUCED SPECIES: A SIGNIFICANT COMPONENT OF HUMAN-CAUSED GLOBAL CHANGE , 1997 .

[39]  B. Schmidt,et al.  Population Size Influences Amphibian Detection Probability: Implications for Biodiversity Monitoring Programs , 2011, PloS one.

[40]  Shefali V. Mehta,et al.  Optimal detection and control strategies for invasive species management , 2007 .