Environmental DNA for assessing impact and recovery of aquatic communities in an invaded mountain lake

References

• Albert JS, Destouni G, Duke-Sylvester SM, Magurran AE, Oberdorff T, Reis RE, Winemiller KO, Ripple WJ. 2021. Scientists’ warning to humanity on the freshwater biodiversity crisis. Ambio. 50(1):85–94. doi: 10.1007/s13280-020-01318-8.
   PubMed Web of Science ®Google Scholar
• Anderson RS. 1970. Effects of rotenone on zooplankton communities and a study of their recovery patterns in two mountain lakes in Alberta. J Fish Res Bd Can. 27(8):1335–1356. doi: 10.1139/f70-159.
   Google Scholar
• Antich A, Palacin C, Wangensteen OS, Turon X. 2021. To denoise or to cluster, that is not the question: optimizing pipelines for COI metabarcoding and metaphylogeography. BMC Bioinform. 22(1):1–24.
   PubMed Web of Science ®Google Scholar
• Antos-Krzeminska N, Jarmuszkiewicz W. 2019. Alternative type II NAD(P)H dehydrogenases in the mitochondria of protists and fungi. Protist 170(1):21–37. doi: 10.1016/j.protis.2018.11.001.
   PubMed Web of Science ®Google Scholar
• Armstrong GD. 1985. Colonies as defence in the freshwater phytoplankton genus Dinobryon (Chrysophyceae). Vancouver (Canada): University of British Columbia.
   Google Scholar
• Atkinson CL, Capps KA, Rugenski AT, Vanni MJ. 2017. Consumer-driven nutrient dynamics in freshwater ecosystems: from individuals to ecosystems. Biol Rev Camb Philos Soc. 92(4):2003–2023. doi: 10.1111/brv.12318.
   PubMed Web of Science ®Google Scholar
• Aylagas E, Borja Á, Irigoien X, Rodríguez-Ezpeleta N. 2016. Benchmarking DNA metabarcoding for biodiversity-based monitoring and assessment. Front Mar Sci. 3(JUN):1–12. doi: 10.3389/fmars.2016.00096.
   Google Scholar
• Beal DL, Anderson RV. 1993. Response of zooplankton to rotenone in a small pond. Bull Environ Contam Toxicol. 51(4):551–556. doi: 10.1007/BF00192171.
   PubMed Web of Science ®Google Scholar
• Beaulieu J, Trépanier-Leroux D, Fischer JM, Olson MH, Thibodeau S, Humphries S, Fraser DJ, Derry AM. 2021. Rotenone for exotic trout eradication: nontarget impacts on aquatic communities in a mountain lake. Lake Reserv Manag. 37(3):323–338. doi: 10.1080/10402381.2021.1912864.
   Web of Science ®Google Scholar
• Buchner D, Leese F. 2020. BOLDigger—a Python package to identify and organise sequences with the Barcode of Life Data systems. MBMG. 4:19–21. doi: 10.3897/mbmg.4.53535.
   Google Scholar
• Bucklin A, Lindeque PK, Rodriguez-Ezpeleta N, Albaina A, Lehtiniemi M. 2016. Metabarcoding of marine zooplankton: prospects, progress and pitfalls. J Plankton Res. 38(3):393–400. doi: 10.1093/plankt/fbw023.
   Web of Science ®Google Scholar
• Callahan BJ, McMurdie PJ, Holmes SP. 2017a. Exact sequence variants should replace operational taxonomic units in marker-gene data analysis. ISME J. 11(12):2639–2643. doi: 10.1038/ismej.2017.119.
   PubMed Web of Science ®Google Scholar
• Callahan BJ, McMurdie PJ, Holmes SP. 2017b. DADA2 Pipeline Tutorial (1.16). R tutorial; [cited Jun 2022]. Available from https://benjjneb.github.io/dada2/tutorial.html.
   Google Scholar
• Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. 2016. DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods. 13(7):581–583. doi: 10.1038/nmeth.3869.
   PubMed Web of Science ®Google Scholar
• Carim KJ, Bean NJ, Connor JM, Baker WP, Jaeger M, Ruggles MP, McKelvey KS, Franklin TW, Young MK, Schwartz MK. 2020. Environmental DNA sampling informs fish eradication efforts: case studies and lessons learned. N Am J Fish Manag. 40(2):488–508. doi: 10.1002/nafm.10428.
   Web of Science ®Google Scholar
• Clarke LJ, Beard JM, Swadling KM, Deagle BE. 2017. Effect of marker choice and thermal cycling protocol on zooplankton DNA metabarcoding studies. Ecol Evol. 7(3):873–883. doi: 10.1002/ece3.2667.
   PubMed Web of Science ®Google Scholar
• Collins RA, Judith B, Wangensteen OS, Soto AZ, Corrigan L, Sims DW, Genner MJ, Mariani S. 2018. Non-specific amplification compromises environmental DNA metabarcoding with COI. Methods Ecol Evol. 10(11):1985–2001. doi: 10.1111/2041-210X.13276.
   Web of Science ®Google Scholar
• Cucherousset J, Olden JD. 2011. Ecological impacts of non-native freshwater fishes. Fisheries. 36(5):215–230. doi: 10.1080/03632415.2011.574578.
   Web of Science ®Google Scholar
• Dalu T, Wasserman RJ, Jordaan M, Froneman WP, Weyl OLF. 2015. An assessment of the effect of rotenone on selected non-target aquatic fauna. PLoS One. 10(11):e0142140. doi: 10.1371/journal.pone.0142140.
   PubMed Web of Science ®Google Scholar
• Davis NM, Proctor DM, Holmes SP, Relman DA, Callahan BJ. 2018. Simple statistical identification and removal of contaminant sequences in marker-gene and metagenomics data. Microbiome. 6(1):226. doi: 10.1186/s40168-018-0605-2.
   PubMedGoogle Scholar
• Davison PI, Copp GH, Créach V, Vilizzi L, Britton JR. 2017. Application of environmental DNA analysis to inform invasive fish eradication operations. Sci Nat. 104(3-4):1–7. doi: 10.1007/s00114-017-1453-9.
   PubMed Web of Science ®Google Scholar
• de Barba M, Miquel C, Boyer F, Mercier C, Rioux D, Coissac E, Taberlet P. 2014. DNA metabarcoding multiplexing and validation of data accuracy for diet assessment: application to omnivorous diet. Mol Ecol Resour. 14(2):306–323. doi: 10.1111/1755-0998.12188.
   PubMed Web of Science ®Google Scholar
• Duggan IC, Wood SA, West DW. 2015. Brown trout (Salmo trutta) removal by rotenone alters zooplankton and phytoplankton community composition in a shallow mesotrophic reservoir. N Z J Mar Freshwater Res. 49(3):356–365. doi: 10.1080/00288330.2015.1018279.
   Web of Science ®Google Scholar
• Dunker KJ, Sepulveda AJ, Massengill RL, Olsen JB, Russ OL, Wenburg JK, Antonovich A. 2016. Potential of environmental DNA to evaluate northern pike (Esox lucius) eradication efforts: an experimental test and case study. PLoS One. 11(9):e0162277. doi: 10.1371/journal.pone.0162277.
   PubMed Web of Science ®Google Scholar
• Eloranta AP, Kjærstad G, Power M, Lakka H-K, Arnekleiv JV, Finstad AG. 2022. Impacts of piscicide-induced fish removal on resource use and trophic diversity of lake invertebrates. Sci Total Environ. 835(May):155364. doi: 10.1016/j.scitotenv.2022.155364.
   PubMedGoogle Scholar
• El-Sayed WMM, Van Ginkel SW, Igou T, Ibrahim HA, Abdul-Raouf UM, Chen Y. 2018. Environmental influence on rotenone performance as an algal crop protective agent to prevent pond crashes for biofuel production. Algal Res. 33(January):277–283. doi: 10.1016/j.algal.2018.05.015.
   Google Scholar
• Gast RJ, Dennett MR, Caron DA. 2004. Characterization of protistan assemblages in the Ross Sea, Antarctica, by denaturing gradient gel electrophoresis. Appl Environ Microbiol. 70(4):2028–2037. doi: 10.1128/AEM.70.4.2028-2037.2004.
   PubMed Web of Science ®Google Scholar
• Gołdyn R, Kowalczewska-Madura K. 2007. Interactions between phytoplankton and zooplankton in the hypertrophic Swarzȩdzkie Lake in western Poland. J Plankton Res. 30(1):33–42. doi: 10.1093/plankt/fbm086.
   Web of Science ®Google Scholar
• Hajibabaei M, Porter TM, Robinson CV, Baird DJ, Shokralla S, Wright MTG. 2019. Watered-down biodiversity? A comparison of metabarcoding results from DNA extracted from matched water and bulk tissue biomonitoring samples. PLoS One. 14(12):e0225409. doi: 10.1371/journal.pone.0225409.
   PubMed Web of Science ®Google Scholar
• Ivankovic M, Ptacnik R, Bengtsson MM. 2022. Top-down structuring of freshwater bacterial communities by mixotrophic and heterotrophic protists. bioRxiv. 1–33.
   Google Scholar
• Jeppesen E, Meerhoff M, Jacobsen BA, Hansen RS, Søndergaard M, Jensen JP, Lauridsen TL, Mazzeo N, Branco CWC. 2007. Restoration of shallow lakes by nutrient control and biomanipulation—the successful strategy varies with lake size and climate. Hydrobiologia. 581(1):269–285. doi: 10.1007/s10750-006-0507-3.
   Google Scholar
• Jones MDM, Forn I, Gadelha C, Egan MJ, Bass D, Massana R, Richards TA. 2011. Discovery of novel intermediate forms redefines the fungal tree of life. Nature. 474(7350):200–203. doi: 10.1038/nature09984.
   PubMed Web of Science ®Google Scholar
• Josephson DC, Youngs WD. 1996. Association between emigration and age structure in populations of brook trout (Salvelinus fontinalis) in Adirondack lakes. Can J Fish Aquat Sci. 53(3):534–541. doi: 10.1139/f95-223.
   Web of Science ®Google Scholar
• Leese F, Sander M, Buchner D, Elbrecht V, Haase P, Zizka VMA. 2021. Improved freshwater macroinvertebrate detection from environmental DNA through minimized nontarget amplification. Environ DNA. 3(1):261–276. doi: 10.1002/edn3.177.
   Google Scholar
• Lepère C, Domaizon I, Humbert JF, Jardillier L, Hugoni M, Debroas D. 2019. Diversity, spatial distribution and activity of fungi in freshwater ecosystems. PeerJ. 7(2):e6247. doi: 10.7717/peerj.6247.
   PubMedGoogle Scholar
• Leray M, Yang JY, Meyer CP, Mills SC, Agudelo N, Ranwez V, Boehm JT, Machida RJ. 2013. A new versatile primer set targeting a short fragment of the mitochondrial COI region for metabarcoding metazoan diversity: application for characterizing coral reef fish gut contents. Front Zool. 10(1):34. doi: 10.1186/1742-9994-10-34.
   PubMedGoogle Scholar
• Martin M. 2011. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. 17(1):10. doi: 10.14806/ej.17.1.200.
   Google Scholar
• McGann BN, Strecker AL. 2022. Zooplankton recovery from a whole-lake disturbance: examining roles of abiotic factors, biotic interactions, and traits. Ecosphere. 13(4):1–26. doi: 10.1002/ecs2.3983.
   Web of Science ®Google Scholar
• McNaught AS, Schindler DW, Parker BR, Paul AJ, Anderson RS, Donald DB, Agbeti M. 1999. Restoration of the food web of an alpine lake following fish stocking. Limnol Oceanogr. 44(1):127–136. doi: 10.4319/lo.1999.44.1.0127.
   Web of Science ®Google Scholar
• Medina-Sánchez JM, Villar-Argaiz M, Carrillo P. 2004. Neither with nor without you: a complex algal control on bacterioplankton in a high mountain lake. Limnol Oceanogr. 49(5):1722–1733. doi: 10.4319/lo.2004.49.5.1722.
   Web of Science ®Google Scholar
• Meredith C, Hoffman J, Trebitz A, Pilgrim E, Okum S, Martinson J, Cameron ES. 2021. Evaluating the performance of DNA metabarcoding for assessment of zooplankton communities in Western Lake Superior using multiple markers. Metabarcoding Metagenom. 50:83–97. doi: 10.3897/mbmg.5.64735.
   PubMedGoogle Scholar
• Messner JS, Maclennan MM, Vinebrooke RD. 2013. Higher temperatures enhance the effects of invasive sportfish on mountain zooplankton communities. Freshw Biol. 58(2):354–364. doi: 10.1111/fwb.12062.
   Web of Science ®Google Scholar
• Murali A, Bhargava A, Wright ES. 2018. IDTAXA: a novel approach for accurate taxonomic classification of microbiome sequences. Microbiome. 6(1):140. doi: 10.1186/s40168-018-0521-5.
   PubMedGoogle Scholar
• Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, Mcglinn D, Minchin PR, Hara RBO, Simpson GL, Solymos P. 2020. vegan: community ecology package. R Package Version 2.5-6; p. 2395–2396.
   Google Scholar
• Palmer G, Horgan DJ, Tisdale H, Singer TP, Beinert H. 1968. Studies on the respiratory chain-linked reduced nicotinamide adenine dinucleotide dehydrogenase. J Biol Chem. 243(4):844–847. doi: 10.1016/S0021-9258(19)81742-8.
   PubMed Web of Science ®Google Scholar
• Parks Canada. 2020. Summary report for the chemical removal of brook trout from Hidden Lake, Upper Corral Creek and tributaries. Radium Hot-Springs (BC): Internal Report.
   Google Scholar
• Pinheiro J, Bates D, R Core Team. 2023. nlme: linear and nonlinear mixed effects models. R Package Version 3.1-163.
   Google Scholar
• Porter KG. 1973. Selective grazing and differential digestion of algae by zooplankton. Nature. 244(5412):179–180. doi: 10.1038/244179a0.
   Web of Science ®Google Scholar
• Pukk L, Kanefsky J, Heathman AL, Weise EM, Nathan LR, Herbst SJ, Sard NM, Scribner KT, Robinson JD. 2021. eDNA metabarcoding in lakes to quantify influences of landscape features and human activity on aquatic invasive species prevalence and fish community diversity. Divers Distrib. 27(10):2016–2031. doi: 10.1111/ddi.13370.
   Web of Science ®Google Scholar
• R Core Team. 2020. R: a language and environment for statistical computing. https://www.r-project.org.
   Google Scholar
• Ratnasingham S, Hebert PDN. 2007. BOLD: the Barcode of Life Data system: barcoding. Mol Ecol Notes. 7(3):355–364. doi: 10.1111/j.1471-8286.2007.01678.x.
   PubMed Web of Science ®Google Scholar
• Robinson CV, Garcia de Leaniz C, Rolla M, Consuegra S. 2019. Monitoring the eradication of the highly invasive topmouth gudgeon (Pseudorasbora parva) using a novel eDNA assay. Environ DNA. 1(1):74–85. doi: 10.1002/edn3.12.
   Google Scholar
• Rudko SP, Ruecker NJ, Ashbolt NJ, Neumann NF, Hanington PC. 2017. Enterobius vermicularis as a novel surrogate for the presence of helminth ova in tertiary wastewater treatment plants. Appl Environ Microbiol. 83(11):1–13. doi: 10.1128/AEM.00547-17.
   Web of Science ®Google Scholar
• Ruppert KM, Kline RJ, Rahman MS. 2019. Past, present, and future perspectives of environmental DNA (eDNA) metabarcoding: a systematic review in methods, monitoring, and applications of global eDNA. Glob Ecol Conserv. 17:e00547. doi: 10.1016/j.gecco.2019.e00547.
   Web of Science ®Google Scholar
• Rytwinski T, Taylor JJ, Donaldson LA, Britton JR, Browne DR, Gresswell RE, Lintermans M, Prior KA, Pellatt MG, Vis C, et al. 2019. The effectiveness of non-native fish removal techniques in freshwater ecosystems: a systematic review. Environ Rev. 27(1):71–94. doi: 10.1139/er-2018-0049.
   Google Scholar
• Sanni S, Wærvågen SB. 1990. Oligotrophication as a result of planktivorous fish removal with rotenone in the small, eutrophic, Lake Mosvatn, Norway. Hydrobiologia. 200–201(1):263–274.
   Google Scholar
• Sarnelle O, Knapp RA. 2005. Nutrient recycling by fish versus zooplankton grazing as drivers of the trophic cascade in alpine lakes. Limnol Oceanogr. 50(6):2032–2042. doi: 10.4319/lo.2005.50.6.2032.
   Web of Science ®Google Scholar
• Schindler DE, Knapp RA, Leavitt PR. 2001. Alteration of nutrient cycles and algal production resulting from fish introductions into Mountain Lakes. Ecosystems. 4(4):308–321. doi: 10.1007/s10021-001-0013-4.
   Web of Science ®Google Scholar
• Schnee ME, Clancy NG, Boyer MC, Bourret SL. 2021. Recovery of freshwater invertebrates in alpine lakes and streams following eradication of nonnative trout with rotenone. J Fish Wildl Manag. 12(2):475–484. doi: 10.3996/JFWM-20-040.
   Web of Science ®Google Scholar
• Simberloff D. 2021. Maintenance management and eradication of established aquatic invaders. Hydrobiologia. 848(9):2399–2420. doi: 10.1007/s10750-020-04352-5.
   Web of Science ®Google Scholar
• Søndergaard M, Liboriussen L, Pedersen AR, Jeppesen E. 2008. Lake restoration by fish removal: short- and long-term effects in 36 Danish lakes. Ecosystems. 11(8):1291–1305. doi: 10.1007/s10021-008-9193-5.
   Web of Science ®Google Scholar
• Suter L, Polanowski AM, Clarke LJ, Kitchener JA, Deagle BE. 2021. Capturing open ocean biodiversity: comparing environmental DNA metabarcoding to the continuous plankton recorder. Mol Ecol. 30(13):3140–3157. doi: 10.1111/mec.15587.
   PubMed Web of Science ®Google Scholar
• Taipale S, Strandberg U, Peltomaa E, Galloway AWE, Ojala A, Brett MT. 2013. Fatty acid composition as biomarkers of freshwater microalgae: analysis of 37 strains of microalgae in 22 genera and in seven classes. Aquat Microb Ecol. 71(2):165–178. doi: 10.3354/ame01671.
   Web of Science ®Google Scholar
• Taylor WD. 1988. Ecology of the Cryptophyceae in a north temperate hardwater lake. East Lansing (MI): Michigan State University.
   Google Scholar
• Thomas AC, Nguyen PL, Howard J, Goldberg CS. 2019. A self-preserving, partially biodegradable eDNA filter. Methods Ecol Evol. 10(8):1136–1141. doi: 10.1111/2041-210X.13212.
   Web of Science ®Google Scholar
• Tiberti R, Brighenti S, Canedoli C, Iacobuzio R, Pasquini G, Rolla M. 2016. The diet of introduced brook trout (Salvelinus fontinalis; Mitchill, 1814) in an alpine area and a literature review on its feeding ecology. J Limnol. 75(3):488–507. doi: 10.4081/jlimnol.2016.1366.
   Web of Science ®Google Scholar
• Trépanier-Leroux D, Yates MC, Astorg L, Fraser DJ, Humphries S, Cristescu ME, Derry AM. 2023. Density-dependent effects of exotic brook trout on aquatic communities in mountain lakes revealed by environmental DNA and morphological taxonomy. Hydrobiologia.1-24. doi: 10.1007/s10750-023-05398-x.
   Web of Science ®Google Scholar
• Turner CR, Barnes MA, Xu CCY, Jones SE, Jerde CL, Lodge DM. 2014. Particle size distribution and optimal capture of aqueous macrobial eDNA. Methods Ecol. 5(7):676–684. doi: 10.1111/2041-210X.12206.
   Web of Science ®Google Scholar
• Turner CR, Uy KL, Everhart RC. 2015. Fish environmental DNA is more concentrated in aquatic sediments than surface water. Biol Conserv. 183:93–102. doi: 10.1016/j.biocon.2014.11.017.
   Web of Science ®Google Scholar
• Van de Peer Y, Baldauf SL, Doolittle WF, Meyer A. 2000. An updated and comprehensive rRNA phylogeny of (crown) eukaryotes based on rate-calibrated evolutionary distances. J Mol Evol. 51(6):565–576. doi: 10.1007/s002390010120.
   PubMed Web of Science ®Google Scholar
• Van Ginkel SW, Igou T, Hu Z, Narode A, Cheruvu S, Doi S, Johnston R, Snell T, Chen Y. 2015. Taking advantage of rotifer sensitivity to rotenone to prevent pond crashes for algal-biofuel production. Algal Res. 10(December 2017):100–103. doi: 10.1016/j.algal.2015.03.013.
   Google Scholar
• Vanni MJ. 2002. Nutrient cycling by animals in freshwater ecosystems. Annu Rev Ecol Syst. 33(1):341–370. doi: 10.1146/annurev.ecolsys.33.010802.150519.
   Google Scholar
• Vaulot D, Schoenle A, Sandin M, Morard R, Mahé F, Fiore-Donno AM, del Campo J, EurkRef Team. 2021. PR2 Version 4.14.0. R package; [cited Jun 2022]. Available from https://github.com/pr2database/pr2database/releases.
   Google Scholar
• Vinson MR, Dinger EC, Vinson DK. 2010. Piscicides and invertebrates: after 70 years, does anyone really know? Fisheries. 35(2):61–71. doi: 10.1577/1548-8446-35.2.61.
   Web of Science ®Google Scholar
• Wickham H. 2016. ggplot2: elegant graphics for data analysis. New York (NY): Springer-Verlag.
   Google Scholar
• Wilcox TM, McKelvey KS, Young MK, Jane SF, Lowe WH, Whiteley AR, Schwartz MK. 2013. Robust detection of rare species using environmental DNA: the importance of primer specificity. PLoS One. 8(3):e59520. doi: 10.1371/journal.pone.0059520.
   PubMed Web of Science ®Google Scholar
• Witzel LD, Maccrimmon HR. 1983. Redd-site selection by brook trout and brown trout in southwestern Ontario streams. Trans Am Fish Soc. 112(6):760–771. doi: 10.1577/1548-8659(1983)112<760:RSBBTA>2.0.CO;2.
   Web of Science ®Google Scholar
• Wurzbacher CM, Bärlocher F, Grossart HP. 2010. Fungi in lake ecosystems. Aquat Microb Ecol. 59(2):125–149. doi: 10.3354/ame01385.
   Web of Science ®Google Scholar
• Yates MC, Cristescu ME, Derry AM. 2021. Integrating physiology and environmental dynamics to operationalize environmental DNA (eDNA) as a means to monitor freshwater macro-organism abundance Mol Ecol. 30(24):6531–6550.
   Google Scholar
• Yates MC, Glaser DM, Post JR, Cristescu ME, Fraser DJ, Derry AM. 2020. The relationship between eDNA particle concentration and organism abundance in nature is strengthened by allometric scaling. Mol Ecol. 30(13)3068-3082.
   PubMed Web of Science ®Google Scholar
• Yates MC, Wilcox T, Stoeckle M, Heath D. 2022. Interspecific allometric scaling in eDNA production in fishes reflects physiological and surface area allometry. eDNA. 3(3):553-560
   Google Scholar
• Yin C, He W, Guo L, Gong L, Yang Y, Yang J, Ni L, Chen Y, Jeppesen E. 2022. Can top-down effects of planktivorous fish removal be used to mitigate cyanobacterial blooms in large subtropical highland lakes? Water Res. 218(January):118483. doi: 10.1016/j.watres.2022.118483.
   PubMedGoogle Scholar
• Zhan A, MacIsaac HJ. 2015. Rare biosphere exploration using high-throughput sequencing: research progress and perspectives. Conserv Genet. 16(3):513–522. doi: 10.1007/s10592-014-0678-9.
   Web of Science ®Google Scholar
• Zhang GK, Chain FJJ, Abbott CL, Cristescu ME. 2018. Metabarcoding using multiplexed markers increases species detection in complex zooplankton communities. Evol Appl. 11(10):1901–1914. doi: 10.1111/eva.12694.
   PubMed Web of Science ®Google Scholar