Environmental DNA (eDNA) detects the invasive rusty crayfish Orconectes rusticus at low abundances

Journal of Applied Ecology

Volumn 53, Issue 3, 2016, Pages 722-732

  Dougherty, Matthew M ^a,b   Larson, Eric R ^a,c,d   Renshaw, Mark A ^a   Gantz, Crysta A ^a   Egan, Scott P ^e   Erickson, Daniel M ^a   Lodge, David M ^a  

^a UNIVERSITY OF NOTRE DAME   (United States)

^b Catholic Theological Union   (United States)

^c Shedd Aquarium Daniel P Haerther Center for Conservation and Research   (United States)

^d UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^e RICE UNIVERSITY   (United States)

Author keywords

crayfish; detection probability; early detection; early warning; exotic species; invasive species; lake; non indigenous; occupancy estimation; quantitative PCR (qPCR)

Indexed keywords

BIOLOGICAL INVASION; CRAYFISH; DETECTION METHOD; DNA; EARLY WARNING SYSTEM; INVASIVE SPECIES; LAKE WATER; POLYMERASE CHAIN REACTION; PROBABILITY; QUANTITATIVE ANALYSIS; RELATIVE ABUNDANCE; SPECIES OCCURRENCE; TRAPPING;

DETECTION; LAKES; NUCLEIC ACIDS; PATTERNS; PROBABILITY; PROCESSES; SAMPLING; WATER;

MIDWEST; UNITED STATES;

ARTHROPODA; ASTACOIDEA; ORCONECTES RUSTICUS;

EID: 84959419499     PISSN: 00218901     EISSN: 13652664     Source Type: Journal    
DOI: 10.1111/1365-2664.12621     Document Type: Article

References (49)

1. Beisner, B.E., Dent, C.L. & Carpenter, S.R. (2003) Variability of lakes on the landscape: roles of phosphorus, food webs, and dissolved organic carbon. Ecology, 84, 1563–1575.
2. Bobeldyk, A.M. & Lamberti, G.A. (2008) A decade after invasion: evaluating the continuing effects of rusty crayfish on a Michigan river. Journal of Great Lakes Research, 34, 265–275.
3. Burnham, K.P. & Anderson, D.R. (2002) Model Selection and Multi-Model Inference: A Practical Information-Theoretic Approach, 2nd edn. Springer, New York.
4. Capelli, G.M. & Magnuson, J.J. (1983) Morphoedaphic and biogeographic analysis of crayfish distribution in northern Wisconsin. Journal of Crustacean Biology, 3, 548–564.
5. Deiner, K. & Altermatt, F. (2014) Transport distance of invertebrate environmental DNA in a natural river. PLoS ONE, 9, e88786.
6. 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. Journal of Applied Ecology, 49, 953–959.
7. Dextrase, A.J. & Mandrak, N.E. (2006) Impacts of alien invasive species on freshwater fauna at risk in Canada. Biological Invasions, 18, 13–24.
8. Dougherty, M.M., Larson, E.R., Renshaw, M.A., Gantz, C.A., Egan, S.P., Erickson, D.M. & Lodge, D.M. (2016) Data from: Environmental DNA (eDNA) detects the invasive rusty crayfish Orconectes rusticus at low abundances. Dryad Digital Repository, http://dx.doi.org/10.5061/dryad.3hp15.
9. Duitama, J., Kumar, D.M., Hemphill, E., Khan, M., Mandoiu, I.I. & Nelson, C.E. (2009) PrimerHunter: a primer design tool for PCR-based virus subtype identification. Nucleic Acids Research, 37, 2483–2492.
10. Egan, S.P., Olds, B., Grey, E., Feder, J.L. & Lodge, D.L. (2015) Molecular detection of invasive species in ballast water using environmental DNA and Laser Transmission Spectroscopy. Environmental Science & Technology, 49, 4113–4121.
11. Ficetola, G.F., Miaud, C., Pompanon, F. & Taberlet, P. (2008) Species detection using environmental DNA from water samples. Biology Letters, 4, 423–425.
12. Foote, A.D., Thomsen, P.F., Sveegaard, S., Wahlberg, M., Kielgast, J. & Kyhn, L.A. (2012) Investigating the potential use of environmental DNA (eDNA) for genetic monitoring of marine mammals. PLoS ONE, 7, e41781.
13. Frings, R.M., Vaeβen, S.C.K., Groβ, H., Roger, S., Schüttrumpf, H. & Hollert, H. (2013) A fish-passable barrier to stop the invasion of non-indigenous crayfish. Biological Conservation, 159, 521–529.
14. Gherardi, F., Aquiloni, L., Diéguez-Uribeondo, J. & Tricarico, E. (2011) Managing invasive crayfish: is there a hope? Aquatic Science, 73, 185–200.
15. Goldberg, C.S., Pilliod, D.S., Arkle, R.S. & Waits, L.P. (2011) Molecular detection of vertebrates in stream water: a demonstration using rocky mountain tailed frogs and Idaho giant salamanders. PLoS ONE, 6, e22746.
16. Goldberg, C.S., Sepulveda, A., Ray, A., Baumgardt, J. & Waits, L.P. (2013) Environmental DNA as a new method for early detection of New Zealand mudsnails (Potamopyrgus antipodarum). Freshwater Science, 32, 792–800.
17. Gunawardana, M., Chang, S., Jimenez, A., Holland-Moritz, D., Holland-Moritz, H., La Val, T.P. et al. (2014) Isolation of PCR quality microbial community DNA from heavily contaminated environments. Journal of Microbiological Methods, 102, 1–7.
18. Gurevitch, J. & Padilla, D.K. (2004) Are invasive species a major cause of extinctions? Trends in Ecology & Evolution, 19, 470–474.
19. Higgins, S.N. & Vander Zanden, M.J. (2010) What a difference a species makes: a meta-analysis of dreissenid mussel impacts on freshwater ecosystems. Ecological Monographs, 80, 179–196.
20. Jane, S.F., Wilcox, T.M., McKelvey, K.S., Young, M.K., Schwartz, M.K., Lowe, W.H., Letcher, B.H. & Whiteley, A.R. (2015) Distance, flow and PCR inhibition: eDNA dynamics in two headwater streams. Molecular Ecology Resources, 15, 216–227.
21. Jerde, C.L., Mahon, A.R., Chadderton, W.L. & Lodge, D.M. (2011) Sight-unseen: detection of rare aquatic species using environmental DNA. Conservation Letters, 4, 150–157.
22. Keller, R.P., Lodge, D.M., Lewis, M.A. & Shogren, J.F. (2009) Bioeconomics of Invasive Species. Oxford University Press, New York.
23. Larson, E.R. & Olden, J.D. (2016) Field sampling techniques for crayfish. Biology and Ecology of Crayfish (eds M. Longshaw & P. Stebbing), pp. 287–323. CRC Press, Boca Raton.
24. Lodge, D.M., Williams, S.L., MacIsaac, H., Hayes, K., Leung, B., Reichard, S. et al. (2006) Biological invasions: recommendations for U.S. policy and management. Ecological Applications, 16, 2035–2054.
25. Lodge, D.M., Deines, A., Gherardi, F., Yeo, D.C.J., Arcella, T., Baldridge, A.K. et al. (2012a) Global introductions of crayfishes: evaluating impact of species invasions on ecosystem services. Annual Review of Ecology, Evolution, and Systematics, 43, 449–472.
26. Lodge, D.M., Turner, C.R., Jerde, C.L., Barnes, M.A., Chadderton, L., Egan, S.P., Feder, J.L., Mahon, A.R. & Pfrender, M.E. (2012b) Conservation in a cup of water: estimating biodiversity and population abundance from environmental DNA. Molecular Ecology, 21, 2555–2558.
27. Longmire, J.L., Maltbie, M. & Baker, R.J. (1997) Use of “lysis buffer” in DNA isolation and its implication for museum collections. Museum of Texas Tech University, 163.
28. MacKenzie, D.I., Nichols, J.D., Lachman, G.B., Droege, S., Royle, J.A. & Langtimm, C.A. (2002) Estimating site occupancy rates when detection probabilities are less than one. Ecology, 83, 2248–2255.
29. McArdle, B.H. (1990) When are rare species not there? Oikos, 57, 276–277.
30. Olden, J.D., Adams, J.W. & Larson, E.R. (2009) First record of Orconectes rusticus (Girard, 1852) (Decapoda, Cambaridae) west of the Great Continental Divide in North America. Crustaceana, 82, 1347–1351.
31. Olden, J.D., McCarthy, J.M., Maxted, J.T., Fetzer, W.W. & Vander Zanden, M.J. (2006) The rapid spread of rusty crayfish (Orconectes rusticus) with observations on native crayfish declines in Wisconsin (U.S.A.) over the past 130 years. Biological Invasions, 8, 1621–1628.
32. Olsen, T.M., Lodge, D.M., Capelli, G.M. & Houlihan, R.J. (1991) Mechanisms of impact of an introduced crayfish (Orconectes rusticus) on littoral congeners, snails, and macrophytes. Canadian Journal of Fisheries and Aquatic Sciences, 48, 1853–1861.
33. Perry, W.L., Feder, J.L., Dwyer, G. & Lodge, D.M. (2001) Hybrid zone dynamics and species replacement between Orconectes crayfishes in a northern Wisconsin lake. Evolution, 55, 1153–1166.
34. Peters, J.A., Cooper, M.J., Creque, S.M., Kornis, M.S., Maxted, J.T., Perry, W.L. & Schueler, F.W. (2014) Historical changes and current status of crayfish diversity and distribution in the Laurentian Great Lakes. Journal of Great Lakes Research, 40, 35–46.
35. Piaggio, A.J., Engeman, R.M., Hopken, M.W., Humphrey, J.S., Keacher, K.L., Bruce, W.E. & Avery, M.L. (2013) Detecting an elusive invasive species: a diagnostic PCR to detect Burmese python in Florida waters and an assessment of persistence of environmental DNA. Molecular Ecology Resources, 14, 374–380.
36. Pilliod, D.S., Goldberg, C.S., Arkle, R.S. & Waits, L.P. (2013) Estimating occupancy and abundance of stream amphibians using environmental DNA from filtered water samples. Canadian Journal of Fisheries and Aquatic Sciences, 70, 1123–1130.
37. R Development Core Team (2009) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org
38. Rees, H.C., Maddison, B.C., Middleditch, D.J., Patmore, J.R.M. & Grough, K.C. (2014) The detection of aquatic animal species using environmental DNA- a review of eDNA as a survey tool in ecology. Journal of Applied Ecology, 51, 1450–1459.
39. Renshaw, M.A., Olds, B.P., Jerde, C.L., McVeigh, M.M. & Lodge, D.M. (2014) 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.
40. Richman, N.I., Bohm, M., Adams, S.B., Alvarez, F., Bergey, E.A., Bunn, J.J.S. et al. (2013) Multiple drivers of decline in the global status of freshwater crayfish (Decapoda: Astacidea). Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 370, 20140060.
41. Schmidt, B.R., Kery, M., Ursenbacher, S., Hyman, O.J. & Collins, J.P. (2013) Site occupancy models in the analysis of environmental DNA presence/absence surveys: a case study of an emerging amphibian pathogen. Methods in Ecology and Evolution, 4, 646–653.
42. Svec, D., Tichopad, A., Novosadova, V., Pfaffl, M.W. & Kubista, M. (2015) How good is a PCR efficiency estimate: Recommendations for precise and robust qPCR efficiency assessments. Biomolecular Detection and Quantification, 3, 9–16.
43. Thomsen, P.F., Kielgast, J., Iversen, L.L., Moller, P.R., Rasmussen, M. & Willerslev, E. (2012a) Detection of a diverse marine fish fauna using environmental DNA from seawater samples. PLoS ONE, 7, e41732.
44. Thomsen, P.F., Kielgast, J., Iversen, L.L., Wiuf, C., Rasmussen, M., Gilbert, M.T.P., Orlando, L. & Willerslev, E. (2012b) Monitoring endangered freshwater biodiversity using environmental DNA. Molecular Ecology, 21, 2565–2573.
45. Tréguier, A., Paillisson, J.M., Dejean, T., Valentini, A., Schlaepfer, M.A. & Roussel, J.M. (2014) Environmental DNA surveillance for invertebrate species: advantages and technical limitations to detect invasive crayfish Procambarus clarkia in freshwater ponds. Journal of Applied Ecology, 51, 871–879.
46. Turner, C.R., Uy, K.L. & Everhart, R.C. (2015) Fish environmental DNA is more concentrated in aquatic sediments than surface water. Biological Conservation, 183, 93–102.
47. Twardochleb, L.A., Olden, J.D. & Larson, E.R. (2013) A global meta-analysis of the ecological impacts of non-native crayfish. Freshwater Science, 32, 1367–1382.
48. Vander Zanden, M.J., Hansen, G.J.A., Higgins, S.N. & Kornis, M.S. (2010) A pound of prevention, plus a pound of cure: early detection and eradication of invasive species in the Laurentian Great Lakes. Journal of Great Lakes Research, 36, 199–205.
49. Wilson, K.A., Magnuson, J.J., Lodge, D.M., Hill, A.M., Kratz, T.K., Perry, W.L. & Willis, T.V. (2004) A long-term rusty crayfish (Orconectes rusticus) invasion: dispersal patterns and community change in a north temperate lake. Canadian Journal of Fisheries and Aquatic Sciences, 61, 2004.