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Conservation Genetics Resources

, Volume 10, Issue 2, pp 259–268 | Cite as

Barcoding PCR primers detect larval lake sturgeon (Acipenser fulvescens) in diets of piscine predators

  • Justin M. Waraniak
  • Danielle M. Blumstein
  • Kim T. Scribner
Methods and Resources Article

Abstract

Population levels of recruitment are often affected by high rates of mortality during early life stages. Lake sturgeon (Acipenser fulvescens), a regionally threatened species, experiences high rates of mortality during the larval stage, partially due to predation. The objective of this study was to quantify and compare relative rates of larval sturgeon predation by piscine predators in the upper Black River (Cheboygan County, MI, USA). A molecular barcoding assay was developed using lake sturgeon-specific primers that amplify a region of mitochondrial DNA cytochrome oxidase I as an alternative to morphological analysis of gastrointestinal (GI) contents to quantify the presence or absence of larval fish collected from potential fish predators (353 specimens, 17 potential predator species). The assay was verified to be sturgeon-specific and sufficiently sensitive to amplify the low quantities of degraded DNA in GI samples. Lake sturgeon DNA was identified in 26 of 353 predator diet samples (7.34%) in 9 of 17 potential predator fish species present. There was a significant positive correlation between the numbers of predators that had consumed larval lake sturgeon and the number of samples from a predator species analyzed. No relationship between predation level and habitat type (sand or gravel substrate) was observed, though predator community composition varied between habitats. Genetic assays as described here can be used to investigate predator–prey dynamics affecting species of conservation interest during important life stages that may otherwise be under-represented in diet studies that rely solely on morphological analysis.

Keywords

Lake sturgeon Predation Larval fish Molecular diet analysis Cytochrome c oxidase mtDNA barcoding 

Notes

Acknowledgements

This project was funded by the Michigan Department of Natural Resources, the Great Lakes Fisheries Trust, and the US Fish and Wildlife Service Coastal Program. Special thanks to the 2015 field crew at the Black River Sturgeon Rearing Facility, Sturgeon For Tomorrow—Black Lake Chapter, Dr. Ed Baker, and Jeanette Kanefsky.

Supplementary material

12686_2017_790_MOESM1_ESM.pdf (79 kb)
Supplementary material 1 (PDF 79 KB)

References

  1. Auer NA, Baker EA (2002) Duration and drift of larval lake sturgeon in the Sturgeon River, Michigan. J Appl Ichthyol 18:557–564CrossRefGoogle Scholar
  2. Baker EA, Borgeson DJ. (1999) Lake sturgeon abundance and harvest in Black Lake, Michigan, 1975–1999. N Am J Fish Manage 19:1080–1088CrossRefGoogle Scholar
  3. Breck JE (2004) Compilation of databases on Michigan lakes. Department of Natural Resources, Fisheries Technical Report, 2004-2, Ann Arbor, MI, USAGoogle Scholar
  4. Caroffino DC, Sutton TM, Elliott RF, Donofrio MC (2010a) Early life stage mortality rates of lake sturgeon in the Peshtigo River, Wisconsin. N Am J Fish Manage 30:295–304CrossRefGoogle Scholar
  5. Caroffino DC, Sutton TM, Elliott RF, Donofrio MC (2010b) Predation on early life stages of lake sturgeon in the Peshtigo River, Wisconsin. Trans Am Fish Soc 139:1846–1856CrossRefGoogle Scholar
  6. Carreon-Martinez LB, Johnson TB, Ludsin SA, Heath DD (2011) Utilization of stomach content DNA to determine diet diversity in piscivorous fishes. J Fish Biol 78:1170–1182CrossRefPubMedGoogle Scholar
  7. Carreon-Martinez LB, Wellband KW, Johnson TB, Ludsin SA, Heath DD (2014) Novel molecular approach demonstrates that turbid river plumes reduce predation mortality on larval fish. Mol Ecol 23:5366–5377CrossRefPubMedGoogle Scholar
  8. Crossman JA (2008) Evaluating collection, rearing, and stocking methods for lake sturgeon (Acipenser fulvescens) restoration programs in the Great Lakes. Dissertation, Michigan State UniversityGoogle Scholar
  9. Duong TY, Scribner KT, Crossman JA, Forsythe PS, Baker EA, Kanefsky J, Homola JJ, Davis C (2011) Relative larval loss among females during dispersal of lake sturgeon (Acipenser fulvescens). Environ Biol Fish 91:459–469CrossRefGoogle Scholar
  10. Forsythe PS, Scribner KT, Crossman JA, Ragavendran A, Baker EA (2013) Experimental assessment of the magnitude and sources of lake sturgeon egg mortality in a natural stream setting. Trans Am Fish Soc 142:1005–1011CrossRefGoogle Scholar
  11. Furey NB, Hinch SG, Bass AL, Middleton CT, Minke-Martin V, Lotto AG (2016) Predator swamping reduces predation risk during nocturnal migration of juvenile salmon in a high-mortality landscape. J Anim Ecol 85:948–959CrossRefPubMedGoogle Scholar
  12. Gadomski DM, Parsley MJ (2005a) Effects of turbidity, light level, and cover on predation of white sturgeon larvae by prickly sculpins. Trans Am Fish Soc 134:369–374CrossRefGoogle Scholar
  13. Gadomski DM, Parsley MJ (2005b) Laboratory studies on the vulnerability of young white sturgeon to predation. N Am J Fish Manage 25:667–674CrossRefGoogle Scholar
  14. Gjøsæter H, Hallfredsson EH, Mikkelsen N, Bogstad B, Pedersen T (2016) Predation of early life stages is decisive for year-class strength in the Barents sea capelin (Mallotus villosus) stock. ICES J Mar Sci 73:182–195CrossRefGoogle Scholar
  15. Hallfredsson EH, Pederson T, Præbel K (2007) Estimation of digestion rates for herring Clupea harengus L. feeding on fish larvae. J Fish Biol 70:638–643CrossRefGoogle Scholar
  16. Harrell Jr FE, with contributions from Charles Dupont and many others (2015) Hmisc: Harrell Miscellaneous. R package version 3.17-1Google Scholar
  17. Harvey BC (1991) Interactions among stream fishes: Predator-induced habitat shifts and larval survival. Oecologia 87:29–36CrossRefPubMedGoogle Scholar
  18. Hjort J (1914) Fluctuations in the great fisheries of northern Europe viewed in the light of biological research. RAPS Process 20:1–228Google Scholar
  19. Houde ED (2008) Emerging from Hjort’s shadow. J Northwest Atl Fish Sci 41:53–70CrossRefGoogle Scholar
  20. Hunter E, Taylor N, Fox CJ, Maillard M, Taylor MI (2012) Effectiveness of TaqMan probes for detection of fish eggs and larvae in the stomach contents of a teleost predator. J Fish Biol 81:320–328CrossRefPubMedGoogle Scholar
  21. Hyslop E (1980) Stomach contents analysis—a review of methods and their application. J Fish Biol 17:411–429CrossRefGoogle Scholar
  22. Jane SF, Wilcox TM, McKelvey KS, Young MK, Schwartz MK, Lowe WH, Letcher BH, Whiteley AR (2015) Distance, flow, and PCR inhibition: eDNA dynamics in two headwater streams. Mol Ecol Resour 15:216–227CrossRefPubMedGoogle Scholar
  23. Jansen WA, Mackay WC (1992) Foraging in yellow perch, Perca flavescens: Biological and physical factors affecting diel periodicity in feeding, consumption, and movement. Eviron Biol Fish 34:287–303CrossRefGoogle Scholar
  24. Jerde CL, Mahon AR, Chadderton WL, Lodge DM (2011) “Sight-unseen” detection of rare aquatic species using environmental DNA. Conserv Lett 4:150–157CrossRefGoogle Scholar
  25. Johnson JH (2015) Summer diel diet and feeding periodicity of four species of cyprinids in the Salmon River, New York. Am Midl Nat 173:326–334CrossRefGoogle Scholar
  26. Kean-Howie JC, Pearre S Jr, Dickie LM (1988) Experimental predation by stickleback on larval mackerel and protection of fish larvae by zooplankton alternative prey. J Exp Mar Biol Ecol 124:239–259CrossRefGoogle Scholar
  27. Keast A, Welsh L (1968) Daily feeding periodicities, food uptake rates, and dietary changes with hour of day in some lake fishes. J Fish Res Bd Canada 25:1133–1144CrossRefGoogle Scholar
  28. Legler ND, Johnson TB, Heath DD, Lusin SA (2010) Water temperature and prey size effects on the rate of digestion of larval and early juvenile fish. Trans Am Fish Soc 139:868–875CrossRefGoogle Scholar
  29. Ley G, Saltzgiver MJ, Dowling TE, Karam AP, Kesner BR, Marsh PC (2014) Use of a molecular assay to detect predation of an endangered fish species. Trans Am Fish Soc 143:49–54CrossRefGoogle Scholar
  30. Magnan P, FitzGerald GJ (1984) Ontogenetic changes in diel activity, food habits and spatial distribution of juvenile and adult creek chub Semotilus atromaculatus. Environ Biol Fish 11:301–307CrossRefGoogle Scholar
  31. Mason DM, Brandt SB (1996) Effect of alewife predation on survival of larval yellow perch in an embayment of Lake Ontario. Can J Fish Aquat Sci 53:1609–1617CrossRefGoogle Scholar
  32. Nichols SJ, Kennedy G, Crawford E, Allen J, French J III, Black G, Blouin M, Hickey J, Chernyák S, Haas R, Thomas M (2003) Assessment of lake sturgeon (Acipenser fulvescens) spawning efforts in the lower St. Clair River, Michigan. J Great Lakes Res 29:383–391CrossRefGoogle Scholar
  33. Parsley MJ, Anders PJ, Miller AI, Beckman LG, McCabe GT Jr (2002) Recovery of white sturgeon populations through natural production: Understanding the influence of abiotic and biotic factors on spawning and subsequent recruitment. Am Fish Soc Symp 28:55–66Google Scholar
  34. Peterson DL, Vecsei P, Jennings CA (2007) Ecology and biology of the lake sturgeon: a synthesis of current knowledge of a threatened North American Acipenseridae. Rev Fish Biol Fish 17:59–76CrossRefGoogle Scholar
  35. Pine WE III, Allen MS, Dreitz VJ (2001) Population viability of the Gulf of Mexico sturgeon: Inferences from capture-recapture and age-structured models. T Am Fish Soc 122:415–438Google Scholar
  36. Pledger S, Baker E, Scribner K (2013) Breeding return times and abundance in capture-recapture models. Biometrics 69:991–1001CrossRefPubMedGoogle Scholar
  37. Pritt JJ, Roseman EF, O’Brien TP (2014) Mechanisms driving recruitment variability in fish: comparisons between the Laurentian Great Lakes and marine systems. ICES J Mar Sci 71:2252–2267CrossRefGoogle Scholar
  38. R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  39. Rosel PE, Kocher TD (2002) DNA-based identification of larval cod in stomach contents of predatory fishes. J Exp Mar Biol Ecol 267:75–88CrossRefGoogle Scholar
  40. Schooley JD, Karam AP, Kesner BR, Marsh PC, Pacey CA, and Thornbrugh, DJ (2008) Detection of larval remains after consumption by fishes. Trans Am Fish Soc 137:1044–1049CrossRefGoogle Scholar
  41. Smith KM, King DK (2005) Dynamics and extent of larval lake sturgeon Acipenser fulvescens drift in the Upper Black River, MI. J Appl Ichthyol 21:161–168CrossRefGoogle Scholar
  42. Taberlet P, Coissac E, Hajibabaei M, Rieseberg LH (2012) Environmental DNA. Mol Ecol 21:1789–1793CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2017

Authors and Affiliations

  • Justin M. Waraniak
    • 1
  • Danielle M. Blumstein
    • 2
  • Kim T. Scribner
    • 1
    • 2
  1. 1.Department of Fisheries and WildlifeMichigan State UniversityEast LansingUSA
  2. 2.Department of Integrative BiologyMichigan State UniversityEast LansingUSA

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