Skip to main content

Advertisement

Log in

Early detection monitoring for non-indigenous fishes; comparison of survey approaches during two species introductions in a Great Lakes port

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

A Correction to this article was published on 13 December 2021

This article has been updated

Abstract

Assessing relative performance of different sampling methods used for early detection monitoring (EDM) is a critical step in understanding the likelihood of detecting new non-indigenous species (NIS) in an environment of interest. EDM performance metrics are typically based on the probability of detecting established NIS or rare indigenous species; however, detection probability estimates for these proxies may not accurately reflect survey effectiveness for newly introduced NIS. We used data from three different EDM survey approaches that varied by targeted life-stage (adult–juvenile versus ichthyoplankton), media (physical fish versus environmental DNA), and taxonomic method (morphology-based versus DNA-based taxonomy) to explore relative detection sensitivity for recently introduced white bass (Morone chrysops) and gizzard shad (Dorosoma cepedianum) in the Port of Duluth-Superior, a NIS introduction hot spot within the Laurentian Great Lakes. Detection efficiency, measured by the effort (number of samples) required to achieve 95% probability of detection, differed by EDM approach and species. Also, the relative sensitivity (detection rate) of each survey approach differed by species. For both species, detection in surveys using DNA-based taxonomy was generally as good or better than the adult–juvenile survey using morphology-based taxonomy. While both species appear to have been detected at early stages of invasion, white bass were likely present up to 5 years prior to initial detection, whereas gizzard shad may have been detected in the first year of introduction. We conclude that using complimentary sampling methods can help to balance the strengths and weaknesses of each approach and provide more reliable early detection of new invaders.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

Availability of data and material

Data underlying this manuscript will be made publicly available via EPA’s Environmental Dataset Gateway at https://edg.epa.gov/.

Change history

References

  • Bailey SA, Deneau MG, Jean L, Wiley CJ, Leung B, MacIsaac HJ (2013) Evaluating efficacy of an environmental policy to prevent biological invasions. Environ Sci Technol 45:2554–2561

    Google Scholar 

  • Becker GC (1983) Fishes of Wisconsin. University of Wisconsin Press, Madison Wisconsin

    Google Scholar 

  • Bishop MJ, Hutchings PA (2011) How useful are port surveys focused on target pest identification for exotic species management? Mar Poll Bull 62:36–42

    CAS  Google Scholar 

  • Bodola A (1966) Life history of the gizzard shad, Dorosoma cepedianum (LeSeuer), in western Lake Erie. US Fish Bull 65:391–425

    Google Scholar 

  • Brown JE, Stepien CA (2009) Invasion genetics of the Eurasian round goby in North America: tracing sources and spread patterns. Mol Ecol 18:64–79

    CAS  PubMed  Google Scholar 

  • Colautti RI, MacIsaac HJ (2004) A neutral terminology to define ‘invasive’ species. Diversity Distrib 10:135–141

    Google Scholar 

  • Crooks JA (2005) Lag times and exotic species: the ecology and management of biological invasions in slow-motion. Ecoscience 12:316–329

    Google Scholar 

  • DeVries JM, Stein RA (1990) Manipulating shad to enhance sport fisheries in North America: an assessment. N Am J Fish Manage 10:209–223

    Google Scholar 

  • Eckmayer WJ, Margraf FJ (2004) The influence of diet, consumption and lipid use on recruitment of white bass. Lake Res Manage 9:133–141

    Google Scholar 

  • Edgar JC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461. https://doi.org/10.1093/bioinformatics/btq461

    Article  CAS  PubMed  Google Scholar 

  • Elbrecht V, Leese F (2015) Can DNA-based ecosystem assessments quantify species abundance? Testing primer bias and biomass-sequence relationships with an innovative metabarcoding protocol. PLoS ONE 10(7):e0130324

  • Evans NT, Olds BP, Renshaw MA, Turner CR, Li Y, Jerde CL, Mahon AR, Pfrender ME, Lamberti GA, Lodge DM (2016) Quantification of mesocosm fish and amphibian species diversity via environmental DNA metabarcoding. Mol Ecol Resour 16:29–41

    CAS  PubMed  Google Scholar 

  • Evans NT, Li Y, Renshaw MA, Olds BP, Deiner K, Turner CR, Jerde CL, Lodge DM, Lamberti GA, Pfrender ME (2017a) Fish community assessment with eDNA metabarcoding: effects of sampling design and bioinformatic filtering. Can J Fish Aquat Sci 74:1362–1374

    CAS  Google Scholar 

  • Evans NT, Shirey PD, Wieringa JG, Mahon AR, Lamberti GA (2017b) Comparative cost and effort of fish distribution detection via environmental DNA analysis and electrofishing. Fisheries 42(2):90–99

    Google Scholar 

  • Feiner ZS, Rice JA, Bunch AJ, Aday DD (2013) Trophic niche and diet overlap between invasive white perch and resident white bass in a southeastern reservoir. Trans Am Fish Soc 142(4):912–919

    Google Scholar 

  • Fincel MJ, Dembkowski DJ, Chipps SR (2014) Influence of variable rainbow smelt and gizzard shad abundance on walleye diets and growth. Lake Res Manage 30:258–267

    CAS  Google Scholar 

  • Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotech 3:294–297

  • Fuller P, Neilson ME, Hopper K (2020) Dorosoma cepedianum (Lesueur, 1818): U.S. Geological Survey, Nonindigenous Aquatic Species Database, Gainesville, FL, https://nas.er.usgs.gov/queries/factsheet.aspx?SpeciesID=492. Accessed 16 April 2020

  • Goldberg CS, Turner CR, Deiner K, Klymus KE, Thomsen PF, Murphy MA, Spear SF, McKee A, Oyler-McCance S, Cornman RS, Laramie MB, Mahon AR, Lance RF, Pilliod DS, Strickler KM, Waits LP, Fremier AK, Takahara T, Herde JE, Taberlet MB (2016) Critical considerations for the application of environmental DNA methods to detect aquatic species. Meth Ecol Evol 7:1299–1307

    Google Scholar 

  • Gopalan G, Culver DA, Wu L, Trauven BK (1998) Effects of recent ecosystem changes on the recruitment of young-of-year fish in western Lake Erie. Can J Fish Aquat Sci 55:2572–2579

    Google Scholar 

  • Gotelli NJ, Colwell RK (2001) Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol Lett 4:379–391

    Google Scholar 

  • Grigorovich IA, Colautti RI, Mills EL, Holeck K, Ballert AG, MacIsaac HJ (2003) Ballast-mediated animal introductions in the Laurentian Great Lakes: retrospective and prospective analyses. Can J Fish Aquat Sci 60:740–756

    Google Scholar 

  • Guy CS, Schultz RD, Colvin MA (2002) Ecology and management of white bass. N Amer J Fish Manage 22:606–608

    Google Scholar 

  • Harris J (2006) Impacts of the invasive White Perch on the fish assemblage of Kerr Reservoir, Virginia. Master’s thesis. Virginia Tech University, Blacksburg.

  • Harvey CT, Qureshi SA, MacIsaac HJ (2009) Detection of a colonizing, aquatic, non-indigenous species. Divers Distrib 15(3):429–437

    Google Scholar 

  • Hatzenbuhler CI, Kelly JR, Martinson J, Okum S, Pilgrim E (2017) Sensitivity and accuracy of high-throughput metabarcoding methods for early detection of invasive fish species. Sci Rep 7:46393

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hoffman JC, Kelly JR, Trebitz AS, Peterson GS, West CW (2011) Effort and potential efficiencies for aquatic non-native species early detection. Can J Fish Aquat Sci 68:2064–2079

    Google Scholar 

  • Hoffman J, Schloesser J, Trebitz A, Peterson G, Gutsch M, Quinlan H, Kelly JR (2016) Sampling design for early detection of aquatic invasive species in Great lakes ports. Fisheries 41:26–37

    Google Scholar 

  • Hoffman J, Meredith C, Pilgrim E, Trebitz A, Hatzenbuhler C, Kelly J, Peterson G, Lietz J, Okum S, Martinson J (2020), High Throughput Sequence-Based Identification of Fish Larvae Assemblages From a High Risk Port: Benchmarking Performance for Invasive Species Early Detection. Can J Fish Aquat Sci (in review).

  • Hubbs CL, Lagler KF (1958) Fishes of the Great Lakes Region. University of Michigan Press, Ann Arbor

    Google Scholar 

  • Ivanova NV, Zemlak TS, Hanner RH, Hebert PD (2007) Universal primer cocktails for fish DNA barcoding. Mol Ecol Notes 7(4):544–548

  • Kelly RP, Closek CJ, O’Donnell JL, Kralj JE, Ao S, Samhouri JF (2017) Genetic and manual survey methods yield different and complementary views of an ecosystem. Front Mar Sci 3:283

    Google Scholar 

  • Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD (2013) Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol 79:5112–5120

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li Y, Evans NT, Renshaw MA, Jerde CL, Olds BP, Shogren AJ, Deiner K, Lodge DM, Lamberti GA, Pfrender ME (2018) Estimating fish alpha- and beta-diversity along a small stream with environmental DNA metabarcoding. Metabarcoding Metagenomics 2:1–11

    Google Scholar 

  • Longmire JL, Maltbie M, Baker RJ (1997) Use of “lysis buffer” in DNA isolation and its implications for museum collections. Museum Texas Tech Univ 163:1–3

    Google Scholar 

  • Madenjian CP, Knight RL, Bur MT, Forney JL (2000) Reduction in recruitment of white bass in Lake Erie after invasion of white perch. Trans Am Fish Soc 129:1340–1353

    Google Scholar 

  • Mao CX, Colwell RK (2005) Estimation of species richness: mixture models, the role of rare species, and inferential challenges. Ecology 86:1143–1153

    Google Scholar 

  • Miller RR (1957) Origin and dispersal of the alewife, Alosa pseudoharengus, and the gizzard shad, Dorosoma cepedianum, in the Great Lakes. Trans Am Fish Soc 86:97–111

    Google Scholar 

  • Mills EL, Leach JH, Carlton JT, Secor CL (1993) Exotic species in the Great Lakes: a history of biotic crises and anthropogenic introductions. J Great Lakes Res 19(1):1–54

    Google Scholar 

  • Mundahl ND, Wissing TE (1987) Nutritional importance of detritivory in the growth and condition of gizzard shad in an Ohio reservoir. Environ Biol Fish 20(2):129–142

    Google Scholar 

  • O’Malia EM, Johnson LB, Hoffman JC (2018a) Pathways and places associated with nonindigenous aquatic introductions in the Laurentian Great Lakes. Hydrobiologia 817:23–40

    PubMed  PubMed Central  Google Scholar 

  • O’Malia EM, Johnson LB, Hoffman JC (2018b) Pathways and places associated with nonindigenous aquatic species introductions in the Laurentian Great Lakes. Hydrobiologia 817:23–40

    PubMed  PubMed Central  Google Scholar 

  • Ogle DH, Isermann DA (2017) Estimating age at a specified length from the von Bertalanffy growth function. N Am J Fish Manage 37(5):1176–1180

    Google Scholar 

  • Olds BP, Jerde CL, Renshaw MA, Li Y, Evans NT, Turner CR, Deiner K, Mahon AR, Brueseke MA, Shirey PD, Pfrender ME, Lodge DM, Lamberti GA (2016) Estimating species richness using environmental DNA. Ecol Evolut 6:4214–4226

    Google Scholar 

  • Peterson GS, Lietz JE (2017) Identification of ruffe larvae (Gymnocephalus cernua) in the St. Louis River, Lake Superior: Clarification and guidance regarding morphological descriptions. J Great Lakes Res 43:205–210

    PubMed  PubMed Central  Google Scholar 

  • Peterson GS, Hoffman JC, Trebitz AS, West CW, Kelly JR (2011) Establishment patterns of non-native fishes: lessons from the Duluth-Superior harbor and lower St Louis River, an invasion-prone Great Lakes coastal ecosystem. J Great Lakes Res 37:349–358

    Google Scholar 

  • Porath MT (2006) Climate and habitat factors related to a localized extirpation of gizzard shad (Dorosoma cepedianum). Great Plains Res 16:127–135

    Google Scholar 

  • Pothoven SA, Höök TO (2015) Feeding ecology of invasive age-0 white perch and native white bass after two decades of co-existence in Saginaw Bay, Lake Huron. Aquat Invasions 10:347–357

    Google Scholar 

  • Priegel GR (1971) Age and rate of growth of the white bass in Lake Winnebago, Wisconsin. Trans Am Fish Soc 3:567–569

    Google Scholar 

  • Renshaw MA, Olds BP, Jerde CL, McVeigh MM, Lodge DM (2015) The room temperature preservation of filtered environmental DNA samples and assimilation into a phenol-chloroform-isoamyl alcohol DNA extraction. Molec Ecol Resources 15:168–176

    CAS  Google Scholar 

  • Ricciardi A (2006) Patterns of invasion in the Laurentian Great Lakes in relation to changes in vector activity. Diversity Distributions 12:423–433

    Google Scholar 

  • Sard NM, Herbst SJ, Nathan L, Uhrig G, Kanefsky J, Robinson JD, Scribner KT (2019) Comparison of fish detections, community diversity, and relative abundance using environmental DNA metabarcoding and traditional gears. Environ DNA 1:368–394

    Google Scholar 

  • Schnell IB, Bohmann K, Gilbert MTP (2015) Tag jumps illuminated reducing sequence to sample misidentifications in metabarcoding studies. Molec Ecol Resources 15:1289–1303

    CAS  Google Scholar 

  • Shaw JLA, Clarke LJ, Wedderburn SD, Barnes TC, Weyrich LS, Cooper A (2016) Comparison of environmental DNA metabarcoding and conventional fish survey methods in a river system. Biol Conserv 197:131–138

    Google Scholar 

  • Staggs MD, Otis KJ (1996) Factors affecting first year growth of fishes in Lake Winnebago, Wisconsin. N Am J Fish Manage 16:608–618

    Google Scholar 

  • Stevens DL Jr, Olsen AR (2004) Spatially-balanced sampling of natural resources in the presence of frame imperfections. J Am Stat Assoc 99(465):262–278. https://doi.org/10.1198/016214504000000250

    Article  Google Scholar 

  • Sturtevant RA, Mason DM, Rutherford ES, Elgin A, Lower E, Martinez F (2019) Recent history of nonindigenous species in the Laurentian Great Lakes; An update to Mills et al., 1993 (25 years later). J Great Lakes Res 45:1011–1035

    Google Scholar 

  • Sullivan CL, Schoenebeck CW, Koupal KD, Hoback WW, Peterson BC (2011) Patterns of age-0 gizzard shad abundance and food habits in a Nebraska irrigation reservoir. Prairie Nat 43:110–116

    Google Scholar 

  • Transportation Research Board (2008) Great Lakes shipping, trade, and aquatic invasive species. Special Report 291. The National Academies Press, Washington DC. https://doi.org/10.17226/12439.

  • 1854 Treaty Authority (2017) 2016 St. Louis River Estuary bottom trawling survey summary report. 1854 Treaty Authority—Resource Management Division, tech. rep. no 17–02

  • Trebitz AS, Kelly JR, Hoffman JC, Peterson GS, West CW (2009) Exploiting habitat and gear patterns for efficient detection of rare and non-native benthos and fish in Great Lakes coastal ecosystems. Aquat Invasions 4:651–667

    Google Scholar 

  • Trebitz AS, Hoffman JC, Grant GW, Billehus TM, Pilgrim EM (2015) Potential for DNA-based identification of Great Lakes fauna: match and mismatch between taxa inventories and DNA barcode libraries. Sci Rep 5:12162. https://doi.org/10.1038/srep12162

    Article  PubMed  PubMed Central  Google Scholar 

  • Trebitz A, Hoffman J, Darling J, Pilgrim E, Kelly J, Brown E, Chadderton W, Egan S, Grey S, Hashsham K, Klymus K, Mahon A, Ram J, Schultz M, Stepien C, Schardt J (2017) Early detection monitoring for aquatic non-indigenous species: optimizing surveillance, incorporating advanced technologies, and identifying research needs. J Environ Manage 202:299–310

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tucker AJ, Chadderton WL, Annis G, Davidson AD, Hoffman J, Bossenbroek J, Hensler S, Hoff M, Jensen E, Kashian D, LeSage S, Strakosh T (2020) A framework for aquatic invasive species surveillance site selection and prioritization in the US waters of the Laurentian Great Lakes. Manage Biol Invasions 11(3):607–632

    Google Scholar 

  • VanDeHey JA, Willis DW, Blackwell BG (2012) Survival, reproduction, and recruitment of gizzard shad (Dorosoma cepedianum) at the northwestern edge of its native range. J Fresh Ecol 27(1):41–53

    Google Scholar 

  • Vander Zanden MJ, Hansen GJA, Higgins SN, Kornis MS (2010) A pound of prevention, plus a pound of cure: early detection and eradication of invasive species in the Great Lakes. J Great Lakes Res 36:199–205

    Google Scholar 

  • Vatland S, Budy P (2007) Predicting the invasion success of an introduced omnivore in a large, heterogenous reservoir. Can J Aquat Sci 64:1329–1345

    Google Scholar 

  • Ward MJ, Willis DW, Galinat GF (2006) Gizzard shad recruitment patterns in a western South Dakota irrigation reservoir. J Fresh Ecol 21(2):201–207. https://doi.org/10.1080/02705060.2006.9664988

    Article  Google Scholar 

  • Willis DW, Paukert CP, Blackwell BG (2002) Biology of white bass in eastern South Dakota glacial lakes. N Amer J Fish Manage 22:627–636

    Google Scholar 

  • Wuellner MR, Graeb BD, Ward MJ, Willis DW (2008a) Review of gizzard shad population dynamics at the northwestern edge of its range. Am Fish Soc Symp 62:637–653

    Google Scholar 

  • Wuellner MR, Graeb BDS, Ward MJ, Willis DW (2008b) Review of gizzard shad dynamics at the northwestern edge of its range. In: Allen MS, Sammons S, Maceina MJ (eds) Balancing fisheries management and water uses for impounded river systems. American Fisheries Society, Bethesda MD, pp 637–653

    Google Scholar 

  • Xiong W, Li H, Zahn A (2016) Early detection of invasive species in marine ecosystem using high-throughput sequencing: technical challenges and possible solutions. Mar Biol 163:139

    Google Scholar 

Download references

Acknowledgements

We thank the many people who were involved with field sampling and with laboratory fish ID/ageing and DNA sample processing. We thank Andrew Tucker from The Nature Conservancy, and David Gillett with the Southern California Coastal Water Research Project for their helpful and insightful suggestions. The views expressed in this article are those of the authors and do not necessarily reflect the views or policies of the US Environmental Protection Agency or the US Fish and Wildlife Service.

Funding

The positions of co-authors Chelsea Hatzenbuhler and Sara Okum were supported by funds from the Great Lakes Restoration Initiative administered by the US EPA Great Lakes National Program Office.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Greg S. Peterson.

Ethics declarations

Consent for publication

This manuscript has been cleared for publication per the internal review process of the US EPA.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

The original online version of this article was revised: In the original publication of the article, the table 4 was published with misalignment and it has been corrected.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Peterson, G.S., Hoffman, J.C., Trebitz, A.S. et al. Early detection monitoring for non-indigenous fishes; comparison of survey approaches during two species introductions in a Great Lakes port. Biol Invasions 24, 463–478 (2022). https://doi.org/10.1007/s10530-021-02655-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-021-02655-9

Keywords

Navigation