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2.Gingera Et Al. 2016 Edna for Lampreys in Great Lakes Streams.Pdf Journal of Great Lakes Research 42 (2016) 649–659 Contents lists available at ScienceDirect Journal of Great Lakes Research journal homepage: www.elsevier.com/locate/jglr Detection and identification of lampreys in Great Lakes streams using environmental DNA Timothy D. Gingera a, Todd B. Steeves b, David A. Boguski a, Steven Whyard a, Weiming Li c, Margaret F. Docker a,⁎ a University of Manitoba, Department of Biological, Sciences, 50 Sifton Road, Winnipeg, MB R3T 2N2, Canada b Sea Lamprey Control Centre, 1219 Queen Street East, Sault Ste. Marie, ON P6A 2E5, Canada c Michigan State University, Department of Fisheries and Wildlife, 13 Natural Resources Building, East Lansing, MI 48824, USA article info abstract Article history: Control of sea lamprey Petromyzon marinus in the Great Lakes requires accurate assessment of the instream Received 16 July 2015 distribution of this pest species and the ability to distinguish it from the four lamprey species that are native to Accepted 17 February 2016 the Great Lakes (American brook lamprey Lethenteron appendix, chestnut lamprey Ichthyomyzon castaneus, Available online 19 March 2016 northern brook lamprey Ichthyomyzon fossor, and silver lamprey Ichthyomyzon unicuspis). We developed PCR- based environmental DNA (eDNA) assays to distinguish among the four “genetic species” of Great Lakes lampreys Communicated by Stephen Charles Riley (silver and northern brook lampreys were genetically indistinguishable), tested them under laboratory fi Keywords: conditions, and demonstrated in the eld that both spawning and larval sea lamprey can be detected using eDNA eDNA. In the laboratory, mean detection frequency decreased with increasing flow rate, but was not significantly Invasive species related to larval density or temperature over the range of relatively high densities tested. Proof-of-concept Sea lamprey control was demonstrated in the field when sea lamprey eDNA was detected during the spawning season (when Native lampreys large-bodied adults, their gametes, and later their carcasses were present); sampling effort involved collection Cryptic organisms of three 1–2 L water samples at each of four transects (0.4–1.0 km apart). Mean detection frequency remained Spawning high (81–97%) until spawning ceased at the end of June, but decreased thereafter, falling to 6% by mid-August. We also demonstrated that eDNA of smaller, burrowing larvae (in water collected after mid-August) was detectable in two of four streams with medium to high larval density (1–2larvae/m2), but not at low densities (b0.1 larvae/m2), potentially due to the exacerbating effect of high flow rates. © 2016 International Association for Great Lakes Research. Published by Elsevier B.V. All rights reserved. Introduction 3–7 years) in the sediment of rivers and streams (Dawson et al., 2015); the second stage, the parasitic juvenile, feeds on the blood and body The presence of an invasive species can have profound negative fluids of actinopterygian fishes for one growing season in the Great impacts on an ecosystem, including loss of native diversity, species Lakes (Bergstedt and Swink, 1995); and during the third stage, the sex- extinction, and shifts in community structure, as well as devastating ually maturing adult migrates upstream to a stream system with suit- socio-economic effects (Nienhuis et al., 2014; Pimentel et al., 2005; able larval habitat and spawns. Sea lamprey, like all lamprey species, Reaser et al., 2007; Simberloff, 1981). The sea lamprey Petromyzon are semelparous and die after spawning. marinus is an aquatic invasive species of jawless fish which was first The Sea Lamprey Control program, initiated over 50 years ago by the recorded in Lake Ontario in the mid-1800s and which subsequently Great Lakes Fishery Commission, represents one of the largest and most spread into the other Laurentian Great Lakes by the late 1930s intensive efforts to control a vertebrate pest (Siefkes et al., 2012). To (Eshenroder, 2014; Smith and Tibbles, 1980). Sea lamprey aggressively effectively reduce the impact of the parasitic stage on fish stocks, stream parasitize commercially-important fish species such as lake trout and river systems that contain filter-feeding sea lamprey larvae are Salvelinus namaycush,lakewhitefish Coregonus clupeaformis, and cisco identified and treated with the selective lampricide 3-trifluoromethyl- Coregonus artedi. This has resulted in the decimation of commercial 4-nitrophenol (TFM) to kill sea lamprey before they metamorphose fisheries and severe population imbalances within the Great Lakes into the parasitic juvenile phase (Siefkes et al., 2012). Effective TFM (Smith and Tibbles, 1980). Sea lamprey have three distinct life stages: treatment therefore requires accurate assessment of larval distribution the first is a filter-feeding larval stage which resides (for approximately and the ability to distinguish this pest species from the four lamprey species that are native to the Great Lakes (American brook lamprey ⁎ Corresponding author. Tel.: +1 204 474 8831. Lethenteron appendix,chestnutlampreyIchthyomyzon castaneus,north- E-mail address: [email protected] (M.F. Docker). ern brook lamprey Ichthyomyzon fossor, and silver lamprey Ichthyomyzon http://dx.doi.org/10.1016/j.jglr.2016.02.017 0380-1330/© 2016 International Association for Great Lakes Research. Published by Elsevier B.V. All rights reserved. 650 T.D. Gingera et al. / Journal of Great Lakes Research 42 (2016) 649–659 unicuspis). Silver and northern brook lampreys, in particular, are of con- lakes Superior and Huron basins with a range of larval sea lamprey den- servation concern in some jurisdictions surrounding the Great Lakes sities to test the ability of the developed sea lamprey assay to detect the (Maitland et al., 2015). Because TFM is also lethal to other lampreys smaller, burrowing lamprey larvae under natural conditions. (Hubert, 2003), effects on non-target species can be achieved only through the targeted treatment of stream reaches containing sea lam- Methods prey and avoidance of those where the other lamprey species occur. Sea lamprey distribution and density is currently assessed using Marker design traditional sampling tools such as electrofishing (Slade et al., 2003). Traditional sampling methods, however, can be labor-intensive and Species-specific eDNA genetic markers were designed to diag- time-consuming, or are sometimes not feasible due to inaccessible nostically identify sea lamprey, American brook lamprey, chestnut terrain, dense vegetation, turbid water, or if the targeted species has a lamprey, and silver and northern brook lampreys (Table 1). The low population density or elusive life stages (Bayley and Peterson, silver and northern brook lampreys were treated as one species 2001; Darling and Mahon, 2011; MacKenzie et al., 2005). As an alterna- because they cannot be distinguished by any known genetic methods tive to these traditional surveillance methods, new highly-sensitive (Docker et al., 2012; Ren et al., 2014). The mitochondrial cytochrome molecular surveillance techniques are being developed in an attempt oxidase c subunit I gene (COI) was targeted because sequence data to collect more accurate species distribution data (e.g., Jerde et al., for the “DNA barcode” region of COI were available on GenBank for 2013; Laramie et al., 2015; Stewart and Baker, 2012; Xi et al., 2011). 13 sea lamprey (EU524270–273, JN028182–190), 24 American brook Currently, environmental DNA (eDNA) is the most common of these lamprey (EU524109–118, HQ579133–136, JN027063–072), 16 chest- molecular surveillance techniques (Jerde et al., 2011; Lodge et al., 2012). nut lamprey (EU524087–089, JN026863–875), 16 silver lamprey Mucus and feces excreted by the organism, the sloughing off of cells (EU524097–105, JN026903–909), and 12 northern brook lamprey from the gut lining, and decomposition of dead organisms introduce (EU524090–096, JN026876–880) specimens from across a broad geo- DNA into the environment (Klymus et al., 2015; Valentini et al., 2008). graphic range (April et al., 2011; Hubert et al., 2008). To increase sensi- Polymerase chain reaction (PCR) can then be used in combination tivity, primers were designed (using Primer3 software, bioinfo.ut.ee/ fi with species-speci c genetic markers to amplify, from water samples, primer3–0.4.0/) to amplify short fragments of the COI gene (119– fragments of DNA from the species of interest. This technique is 227 bp). BLAST (Basic Local Alignment Search Tool; GenBank, www. now being used for the detection of both endangered and invasive ncbi.nlm.nih.gov/blast) searches compared the primer sequences to all fi aquatic species, including freshwater shes (Jerde et al., 2011, 2013; available sequence data to test whether they were likely to result in Minamoto et al., 2012; Takahara et al., 2012, 2013; Thomsen et al., non-target amplification from other organisms. Each candidate marker 2012a), amphibians (Dejean et al., 2012; Ficetola et al., 2008; was tested against tissue-derived DNA from 44–60 specimens of Goldberg et al., 2011; Pilliod et al., 2013; Spear et al., 2015), and inver- the target species from across a broad geographic range (Table 2) tebrates (Deiner et al., 2015; Goldberg et al., 2013), as well as many and against each of the other (non-target) lamprey species (see PCR species of marine vertebrates (Foote et al., 2012; Thomsen et al., amplification and evaluation). PCR products were visualized on a 1.5% 2012b). Monitoring protocols which involve the use of eDNA tech- agarose gel stained with
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