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The effect of bivalve filtration on eDNA-based detection of aquatic organisms


Autoři: Ryan Friebertshauser aff001;  Kurtis Shollenberger aff001;  Alexis Janosik aff002;  Jeffrey T. Garner aff003;  Carol Johnston aff001
Působiště autorů: Department of Fisheries, Aquaculture, and Aquatic Sciences, Auburn University, Auburn, AL, United States of America aff001;  Department of Biology, University of West Florida, Pensacola, FL, United States of America aff002;  Division of Wildlife and Freshwater Fisheries, Alabama Department of Conservation and Natural Resources, Florence, AL, United States of America aff003
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0222830

Souhrn

As the use of environmental-DNA (eDNA) expands as a method to detect the presence and quantity of aquatic taxa, factors potentially impacting the efficacy of this technique must be investigated. Many studies have examined the effects of abiotic parameters on the degradation of environmental-DNA (e.g. UV radiation, pH, temperature, etc.), however, few have focused on biotic effectors. Through high-filtering rates coupled with dense colonization, Asian clams (Corbicula fluminea) are able to drastically alter the quantity of particulate matter through translocation into the sediment, potentially including sources of eDNA in lotic and lentic systems. Using a longitudinal, laboratory experiment, we tested the effect of varying densities of Asian clams on the translocation rate of common goldfish (Carassius auratus) DNA. Target DNA in testing tanks was quantified through quantitative PCR (qPCR) at regular intervals and compared. Tanks housing the highest density of Asian clams produced significantly lower DNA concentrations over time compared to tanks of lower densities. These results show, for the first time, a density-dependent reduction of local eDNA sources by bivalve filtration that may lead to the obstructed detection of target species through the sampling of eDNA. Based on these findings, we recommend highly concentrated bivalve populations be taken into consideration when choosing the time and locality of eDNA sampling efforts.

Klíčová slova:

Bivalves – DNA extraction – DNA replication – Invasive species – Polymerase chain reaction – Sediment – Water columns – Goldfish


Zdroje

1. Magurran AE. Measuring Biological Diversity. John Wiley & Sons; 2013.

2. MacKenzie DI, Nichols JD, Sutton N, Kawanishi K, Bailey LL. Improving Inferences in Population Studies of Rare Species That Are Detected Imperfectly. Ecology. 2005;86: 1101–1113. doi: 10.1890/04-1060

3. Taberlet P, Coissac E, Hajibabaei M, Rieseberg LH. Environmental DNA. Mol Ecol. 2012;21: 1789–1793. doi: 10.1111/j.1365-294X.2012.05542.x 22486819

4. Pfleger MO, Rider SJ, Johnston CE, Janosik AM. Saving the doomed: Using eDNA to aid in detection of rare sturgeon for conservation (Acipenseridae). Glob Ecol Conserv. 2016;8: 99–107. doi: 10.1016/j.gecco.2016.08.008

5. Janosik AM, Johnston CE. Environmental DNA as an effective tool for detection of imperiled fishes. Environ Biol Fishes. 2015;98: 1889–1893. doi: 10.1007/s10641-015-0405-5

6. Harper LR, Handley LL, Hahn C, Boonham N, Rees HC, Gough KC, et al. Needle in a haystack? A comparison of eDNA metabarcoding and targeted qPCR for detection of the great crested newt (Triturus cristatus). Ecol Evol. 2018;8: 6330–6341. doi: 10.1002/ece3.4013 29988445

7. Jerde CL, Mahon AR, Chadderton WL, Lodge DM. “Sight-unseen” detection of rare aquatic species using environmental DNA. Conserv Lett. 4: 150–157. doi: 10.1111/j.1755-263X.2010.00158.x

8. Lance RF, Klymus KE, Richter CA, Guan X, Farrington HL, Carr MR, et al. Experimental observations on the decay of environmental DNA from bighead and silver carps. Manag Biol Invasions. 2017;8: 343359. doi: 10.3391/mbi.2017.8.3.08

9. Thomsen PF, Kielgast J, Iversen LL, Møller PR, Rasmussen M, Willerslev E. Detection of a Diverse Marine Fish Fauna Using Environmental DNA from Seawater Samples. PLOS ONE. 2012;7: e41732. doi: 10.1371/journal.pone.0041732 22952584

10. Dejean T, Valentini A, Duparc A, Pellier-Cuit S, Pompanon F, Taberlet P, et al. Persistence of Environmental DNA in Freshwater Ecosystems. PLOS ONE. 2011;6: e23398. doi: 10.1371/journal.pone.0023398 21858099

11. Goldberg CS, Sepulveda A, Ray A, Baumgardt J, Waits LP. Environmental DNA as a new method for early detection of New Zealand mudsnails (Potamopyrgus antipodarum). Freshw Sci. 2013;32: 792–800. doi: 10.1899/13-046.1

12. Barnes MA, Turner CR, Jerde CL, Renshaw MA, Chadderton WL, Lodge DM. Environmental Conditions Influence eDNA Persistence in Aquatic Systems. Environ Sci Technol. 2014;48: 1819–1827. doi: 10.1021/es404734p 24422450

13. Tsuji S, Ushio M, Sakurai S, Minamoto T, Yamanaka H. Water temperature-dependent degradation of environmental DNA and its relation to bacterial abundance. PLOS ONE. 2017;12: e0176608. doi: 10.1371/journal.pone.0176608 28448613

14. Strickler KM, Fremier AK, Goldberg CS. Quantifying effects of UV-B, temperature, and pH on eDNA degradation in aquatic microcosms. Biol Conserv. 2015;183: 85–92. doi: 10.1016/j.biocon.2014.11.038

15. McMAHON RF. 12—Ecology of an Invasive Pest Bivalve, Corbicula. In: Russell-hunter WD, editor. Ecology. Academic Press; 1983. pp. 505–561. doi: 10.1016/B978-0-12-751406-2.50019–2

16. Dame R, Zingmark R, Stevenson H, Nelson D. FILTER FEEDER COUPLING BETWEEN THE ESTUARINE WATER COLUMN AND BENTHIC SUBSYSTEMS. In: Kennedy VS, editor. Estuarine Perspectives. Academic Press; 1980. pp. 521–526. doi: 10.1016/B978-0-12-404060-1.50048–4

17. Wilcox TM, McKelvey KS, Young MK, Lowe WH, Schwartz MK. Environmental DNA particle size distribution from Brook Trout (Salvelinus fontinalis). Conserv Genet Resour. 2015;7: 639–641. doi: 10.1007/s12686-015-0465-z

18. Turner CR, Barnes MA, Xu CCY, Jones SE, Jerde CL, Lodge DM. Particle size distribution and optimal capture of aqueous macrobial eDNA. Methods Ecol Evol. 5: 676–684. doi: 10.1111/2041-210X.12206

19. Mächler E, Osathanunkul M, Altermatt F. Shedding light on eDNA: neither natural levels of UV radiation nor the presence of a filter feeder affect eDNA-based detection of aquatic organisms. PLOS ONE. 2018;13: e0195529. doi: 10.1371/journal.pone.0195529 29624607

20. Seymour M, Durance I, Cosby BJ, Ransom-Jones E, Deiner K, Ormerod SJ, et al. Acidity promotes degradation of multi-species environmental DNA in lotic mesocosms. Commun Biol. 2018;1: 4. doi: 10.1038/s42003-017-0005-3 30271891

21. Pilliod DS, Goldberg CS, Arkle RS, Waits LP. Factors influencing detection of eDNA from a stream‐dwelling amphibian. In: Molecular Ecology Resources [Internet]. 1 Jan 2014 [cited 18 Aug 2019]. doi: 10.1111/1755-0998.12281

22. Klymus KE, Richter CA, Chapman DC, Paukert C. Quantification of eDNA shedding rates from invasive bighead carp Hypophthalmichthys nobilis and silver carp Hypophthalmichthys molitrix. Biol Conserv. 2015;183: 77–84. doi: 10.1016/j.biocon.2014.11.020

23. Ficetola Gentile Francesco, Miaud Claude, Pompanon François, Taberlet Pierre. Species detection using environmental DNA from water samples. Biol Lett. 2008;4: 423–425. doi: 10.1098/rsbl.2008.0118 18400683

24. Sugiura S. Rapid estimation of species-specific DNA digestibility based on differential qPCR. Fish Sci. 2014;80: 795–801. doi: 10.1007/s12562-014-0757-3

25. Jo T, Murakami H, Masuda R, Sakata MK, Yamamoto S, Minamoto T. Rapid degradation of longer DNA fragments enables the improved estimation of distribution and biomass using environmental DNA. Mol Ecol Resour. 2017;17: e25–e33. doi: 10.1111/1755-0998.12685 28449215

26. Biggs J, Ewald N, Valentini A, Gaboriaud C, Dejean T, Griffiths RA, et al. Using eDNA to develop a national citizen science-based monitoring programme for the great crested newt (Triturus cristatus). Biol Conserv. 2015;183: 19–28. doi: 10.1016/j.biocon.2014.11.029

27. Rees HC, Maddison BC, Middleditch DJ, Patmore JRM, Gough KC. REVIEW: The detection of aquatic animal species using environmental DNA–a review of eDNA as a survey tool in ecology. J Appl Ecol. 2014;51: 1450–1459. doi: 10.1111/1365-2664.12306

28. Silverman H, Achberger EC, Lynn JW, Dietz TH. Filtration and Utilization of Laboratory-Cultured Bacteria by Dreissena polymorpha, Corbicula fluminea, and Carunculina texasensis. Biol Bull. 1995;189: 308–319. doi: 10.2307/1542148 29244572

29. Furlan EM, Gleeson D, Hardy CM, Duncan RP. A framework for estimating the sensitivity of eDNA surveys. Mol Ecol Resour. 2016;16: 641–654. doi: 10.1111/1755-0998.12483 26536842

30. Tenore KR, Dunstan WM. Comparison of feeding and biodeposition of three bivalves at different food levels. Mar Biol. 1973;21: 190–195. doi: 10.1007/BF00355249

31. Basen T, Gergs R, Rothhaupt K-O, Martin-Creuzburg D. Phytoplankton food quality effects on gammarids: benthic–pelagic coupling mediated by an invasive freshwater clam. Can J Fish Aquat Sci. 2012;70: 198–207. doi: 10.1139/cjfas-2012-0188

32. Turek KA, Hoellein TJ. The invasive Asian clam (Corbicula fluminea) increases sediment denitrification and ammonium flux in 2 streams in the midwestern USA. Freshw Sci. 2015;34: 472–484. doi: 10.1086/680400

33. Levy-Booth DJ, Campbell RG, Gulden RH, Hart MM, Powell JR, Klironomos JN, et al. Cycling of extracellular DNA in the soil environment. Soil Biol Biochem. 2007;39: 2977–2991. doi: 10.1016/j.soilbio.2007.06.020

34. Chen I, Dubnau D. DNA uptake during bacterial transformation. Nat Rev Microbiol. 2004;2: 241–249. doi: 10.1038/nrmicro844 15083159

35. Lucy F, Karatayev A, Burlakova L. Predictions for the spread, population density and impacts of Corbicula fluminea in Ireland. 2012; Available: https://research.thea.ie/handle/20.500.12065/715

36. Werner S, Rothhaupt K-O. Effects of the invasive Asian clam <I>Corbicula fluminea</I> on benthic macroinvertebrate taxa in laboratory experiments. Fundam Appl Limnol Arch Für Hydrobiol. 2008;173: 145–152. doi: 10.1127/1863-9135/2008/0173-0145

37. Marescaux J, Falisse E, Lorquet J, Van Doninck K, Beisel J-N, Descy J-P. Assessing filtration rates of exotic bivalves: dependence on algae concentration and seasonal factors. Hydrobiologia. 2016;777: 67–78. doi: 10.1007/s10750-016-2764-0


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