Abstract
Coastal marine fish populations are in decline due to overfishing, habitat destruction, climate change and invasive species. Seasonal monitoring is important for detecting temporal changes in the composition of fish communities, but current monitoring is often non-existent or limited to annual or semi-annual surveys. In the present study, we investigate the potential of using environmental DNA (eDNA) metabarcoding of seawater samples to detect the seasonal changes in a coastal marine fish community. Water sampling and snorkelling visual census were performed over 1 year (from 23rd of August 2013 to 11th of August 2014) at a temperate coastal habitat in Denmark (55°45′39″N, 12°35′59″E) and compared to long-term data collected over a 7-year period. We used Illumina sequencing of PCR products to demonstrate that seawater eDNA showed compositional changes in accordance with seasonal changes in the fish community. The vast majority of fish diversity observed in the study area by snorkelling was recovered from sequencing, although the overlap between methods varied widely among sampling events. In total, 24 taxa were detected by both methods, while five taxa were only detected using eDNA and three taxa were only detected by snorkelling. A limitation of the applied primers was the lack of resolution to species level in a few diverse families, and varying sequencing depth between samples represents a potential bias. However, our study demonstrates the utility of eDNA for recovering seasonal variation in marine fish communities, knowledge of which is essential for standardised long-term monitoring of marine biodiversity.
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References
Andriashev AP (1986) Zoarcidae. In: Whitehead PJP, Bauchot M-L, Hureau J-C, Nielsen J, Tortonese E (eds) Fishes of the North-Eastern Atlantic and the mediterranean. UNESCO, Geneva, pp 1130–1150
Angantyr LA, Rasmussen J, Göransson P, Jeppesen JP, Svedäng H (2007) Øresund som levested. In: Angantyr LA, Rasmussen J, Göransson P, Nerpin L (eds) Fisk i Øresund. Øresundsvandsamarbejdet, p 7. http://www.oresundsvand.dk
Azour F, van Deurs M, Behrens J, Carl H, Hüssy K, Greisen K, Ebert R, Møller PR (2015) Invasion rate and population characteristics of the invasive round goby (Neogobius melanostomus) at an established, high-density locality and a recently invaded, low-density locality. Aquat Biol 24:41–52
Bagge O (1964) Some observations on the biology of the lumpsucker (Cyclopterus lumpus). In: ICES CM 1964, Baltic-Belt Seas Commitee 150, p 7
Barnes MA, Turner CR, Jerde CL, Renshaw MA, Chadderton WL, Lodge DM (2014) Environmental conditions influence eDNA persistence in aquatic systems. Environ Sci Technol 48:1819–1827
Bergman PS, Schumer G, Blankenship S, Campbell E (2016) Detection of adult green sturgeon using environmental DNA analysis. PLoS One 11:e0153500
Boyer F, Mercier C, Bonin A, Le Bras Y, Taberlet P, Coissac E (2016) obitools: a unix-inspired software package for DNA metabarcoding. Mol Ecol Resour 16:176–182
Carl H (2012a) Brasen. In: Carl H, Møller PR (eds) Atlas over danske ferskvandsfisk. Statens Naturhistoriske Museum, Copenhagen, pp 115–126
Carl H (2012b) Suder. In: Carl H, Møller PR (eds) Atlas over danske ferskvandsfisk. Statens Naturhistoriske Museum, Copenhagen, pp 295–303
Carl H (2012c) Grundling. In: Carl H, Møller PR (eds) Atlas over danske ferskvandsfisk. Statens Naturhistoriske Museum, Copenhagen, pp 203–212
Carl H (2012d) Europæisk malle. In: Carl H, Møller PR (eds) Atlas over danske ferskvandsfisk. Statens Naturhistoriske Museum, Copenhagen, pp 339–349
Coissac E (2012) OligoTag: a program for designing sets of tags for next-generation sequencing of multiplexed samples. In: Pompanon F, Bonin A (eds) Data production and analysis of population genomics: methods and protocols. Humana Press, New York, pp 13–31
Dansk Ornitologisk Forening (2014) Ederfugl (Somateria mollissima). DOFbasen. http://dofbasen.dk/ART/art.php?art=02060. Accessed 31 Jan 2017
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 14:306–323
Dejean T, Valentini A, Duparc A, Pellier-Cuit S, Pompanon F, Taberlet P, Miaud C (2011) Persistence of environmental DNA in freshwater ecosystems. PLoS One 6:e23398
FAO (2011) Fishery and aquaculture statistics. FAO Yearbook, Rome
Ficetola GF, Miaud C, Pompanon F, Taberlet P (2008) Species detection using environmental DNA from water samples. Biol Lett 4:423–425
Ficetola GF, Coissac E, Zundel S, Riaz T, Shehzad W, Bessière J, Taberlet P, Pompanon F (2010) An in silico approach for the evaluation of DNA barcodes. BMC Genom 11:434
Foote AD, Thomsen PF, Sveegaard S, Wahlberg M, Kielgast J, Kyhn LA, Salling AB, Galatius A, Orlando L, Gilbert MTP (2012) Investigating the potential use of environmental DNA (eDNA) for genetic monitoring of marine mammals. PLoS One 7:e41781
Fossheim M, Primicerio R, Johannesen E, Ingvaldsen RB, Aschan MM, Dolgov AV (2015) Recent warming leads to a rapid borealization of fish communities in the Arctic. Nat Clim Chang 5:673–677
Goldberg CS, Turner CR, Deiner K, Klymus KE, Thomsen PF, Murphy MA, Spear SF, McKee A, Oyler-McCance SJ, Cornman RS, Laramie MB, Mahon AR, Lance RF, Pilliod DS, Strickler KM, Waits LP, Fremier AK, Takahara T, Herder JE, Taberlet P (2016) Critical considerations for the application of environmental DNA methods to detect aquatic species. Method Ecol Evol 7:1299–1307
Green SJ, Akins JL, Maljković A, Côté IM (2012) Invasive lionfish drive atlantic coral reef fish declines. PLoS One 7:e32596
Hammer Ø, Harper DAT, Ryan PD (2001) Past: Paleontological statistics software package for education and data analysis. Palaeontol Electron 4(1):4–9. http://palaeo-electronica.org/20011/past/issue1_01.htm
Heessen HJL (2015) Eelpouts (Zoarcidae). In: Heessen HJL, Daan N, Ellis JR (eds) Fish atlas of the Celtic Sea, North Sea, and Baltic Sea, Based on international research-vessel surveys. Wageningen Academic Publishers, Wageningen, pp 358–364
Holbrook SJ, Schmitt RJ, Stephens JS (1997) Changes in an assemblage of temperate reef fishes associated with a climate shift. Ecol Appl 7:1299–1310
Holmlund CM, Hammer M (1999) Ecosystem services generated by fish populations. Ecol Econ 29:253–268
Hutchings JA (2000) Collapse and recovery of marine fishes. Nature 406:882–885
ICES (2013) Fish stocks: counting the uncountable?. ICES, Copenhagen
Jackson JBC, Kirby MX, Berger WH, Bjorndal KA, Botsford LW, Bourque BJ, Bradbury RH, Cooke R, Erlandson J, Estes JA, Hughes TP, Kidwell S, Lange CB, Lenihan HS, Pandolfi JM, Peterson CH, Steneck RS, Tegner MJ, Warner RR (2001) Historical overfishing and the recent collapse of coastal ecosystems. Science 293:629–637
Jones GP, McCormick MI, Srinivasan M, Eagle JV (2004) Coral decline threatens fish biodiversity in marine reserves. Proc Natl Acad Sci USA 101:8251–8253
Jørgensen OA, Bastardie F, Eigaard OR (2014) Impact of deep-sea fishery for Greenland halibut (Reinhardtius hippoglossoides) on non-commercial fish species off West Greenland. ICES J Mar Sci J Cons 71:845–852
Jurasinski G, Retzer V (2012) Simba: a collection of functions for similarity analysis of vegetation data. R package version 0.3-5. https://CRAN.R-project.org/package=simba. Accessed 28 Mar 2017
Kenchington E, Yashayaev I, Tendal OS, Jørgensbye H (2016) Water mass characteristics and associated fauna of a recently discovered Lophelia pertusa. Polar Biol 40:321–337
MacKenzie BR, Payne MR, Boje J, Høyer JL, Siegstad H (2014) A cascade of warming impacts brings bluefin tuna to Greenland waters. Glob Change Biol 20:2484–2491
Maruyama A, Nakamura K, Yamanaka H, Kondoh M, Minamoto T (2014) The release rate of environmental DNA from juvenile and adult fish. PLoS One 9:e114639
NCBI (2017) How to submit data to GenBank. GenBank. https://www.ncbi.nlm.nih.gov/genbank/submit/. Accessed 21 Mar 2017
Nielsen JG (2012) Hork. In: Carl H, Møller PR (eds) Atlas over danske ferskvandsfisk. Statens Naturhistoriske Museum, Copenhagen, pp 561–568
Nielsen JG, Krag M (2012) Knude. In: Carl H, Møller PR (eds) Atlas over danske ferskvandsfisk. Statens Naturhistoriske Museum, Copenhagen, pp 503–513
Pauly D, Christensen V, Guénette S, Pitcher TJ, Sumaila UR, Walters CJ, Watson R, Zeller D (2002) Towards sustainability in world fisheries. Nature 418:689–695
Pedersen MI, Carl H (2012) Europæisk ål. In: Carl H, Møller PR (eds) Atlas over danske ferskvandsfisk. Statens Naturhistoriske Museum, Copenhagen, pp 97–112
Pilliod DS, Goldberg CS, Arkle RS, Waits LP (2014) Factors influencing detection of eDNA from a stream-dwelling amphibian. Mol Ecol Resour 14:109–116
Port JA, O’Donnell JL, Romero-Maraccini OC, Leary PR, Litvin SY, Nickols KJ, Yamahara KM, Kelly RP (2016) Assessing vertebrate biodiversity in a kelp forest ecosystem using environmental DNA. Mol Ecol 25:527–541
RStudio Team (2016) RStudio: integrated development for R. RStudio Inc, Boston, MA
Shelton AO, O’Donnell JL, Samhouri JF, Lowell N, Williams GD, Kelly RP (2016) A framework for inferring biological communities from environmental DNA. Ecol Appl 26:1645–1659
Sigsgaard EE, Nielsen IB, Bach SS, Lorenzen ED, Robinson DP, Knudsen SW, Pedersen MW, Jaidah MA, Orlando L, Willerslev E, Møller PR, Thomsen PF (2016) Population characteristics of a large whale shark aggregation inferred from seawater environmental DNA. Nat Ecol Evol 1:0004
Southward AJ, Langmead O, Hardman-Mountford NJ, Aiken J, Boalch GT, Dando PR, Genner MJ, Joint I, Kendall MA, Halliday NC, Harris RP, Leaper R, Mieszkowska N, Pingree RD, Richardson AJ, Sims DW, Smith T, Walne AW, Hawkins SJ (2004) Long-term oceanographic and ecological research in the Western English Channel. Adv Mar Biol 47:1–105
Spear SF, Groves JD, Williams LA, Waits LP (2015) Using environmental DNA methods to improve detectability in a hellbender (Cryptobranchus alleganiensis) monitoring program. Biol Conserv 183:38–45
Spens J, Evans AR, Halfmaerten D, Knudsen SW, Sengupta ME, Mak SST, Sigsgaard EE, Hellström M (2016) Comparison of capture and storage methods for aqueous macrobial eDNA using an optimized extraction protocol: advantage of enclosed filter. Methods Ecol Evol. doi:10.1111/2041-210X.12683
Stoeckle MY, Soboleva L, Charlop-Powers Z, Doi H (2017) Aquatic environmental DNA detects seasonal fish abundance and habitat preference in an urban estuary. PLoS One 12 (4):e0175186
Stoesser G, Baker W, Broek VDA, Camon E, Garcia-Pastor M, Kanz C, Kulikova T, Leinonen R, Lin Q, Lombard V, Lopez R, Redaschi N, Stoehr P, Tuli MA, Tzouvara K, Vaughan R (2002) The EMBL nucleotide sequence database. Nucl Acid Res 30:21–26
Støttrup JG, Sparrevohn CR, Nicolajsen H, Kristensen LD (2012) Registrering af fangster i de danske kystområder med standardredskaber. Nøglefiskerrapporten for årene 2008–2010. DTU Aqua-rapport nr. 252–2012. National Institute for Aquatic Resources, Technical University of Denmark: 94 p
Strickler KM, Fremier AK, Goldberg CS (2015) Quantifying effects of UV-B, temperature, and pH on eDNA degradation in aquatic microcosms. Biol Conserv 183:85–92
Takahara T, Minamoto T, Yamanaka H, Doi H, Kawabata Z (2012) Estimation of fish biomass using environmental DNA. PLoS One 7:e35868
Thomsen PF, Willerslev E (2015) Environmental DNA: an emerging tool in conservation for monitoring past and present biodiversity. Biol Conserv 183:4–18
Thomsen PF, Kielgast J, Iversen LL, Wiuf C, Rasmussen M, Gilbert MTP, Orlando L, Willerslev E (2012a) Monitoring endangered freshwater biodiversity using environmental DNA. Mol Ecol 21:2565–2573
Thomsen PF, Kielgast J, Iversen LL, Møller PR, Rasmussen M, Willerslev E (2012b) Detection of a diverse marine fish fauna using environmental DNA from seawater samples. PLoS One 7:e41732
Thomsen PF, Møller PR, Sigsgaard EE, Knudsen SW, Jørgensen OA, Willerslev E (2016) Environmental DNA from seawater samples correlate with trawl catches of subarctic, deepwater fishes. PLoS One 11:e0165252
Ushio M, Murakami H, Masuda R, Sado T, Miya M, Sakurai S, Yamanaka H, Minamoto T, Kondoh M (2017) Quantitative monitoring of multispecies environmental DNA using high-throughput sequencing. BioRxiv. doi:10.1101/113472
Valentini A, Taberlet P, Miaud C, Civade R, Herder J, Thomsen PF, Bellemain E, Besnard A, Coissac E, Boyer F, Gaboriaud C, Jean P, Poulet N, Roset N, Copp GH, Peroux T, Crivelli AJ, Olivier A, Acqueberge M, Brun M, Møller PR, Willerslev E, Dejean T (2016) Next-generation monitoring of aquatic biodiversity using environmental DNA metabarcoding. Mol Ecol 25:929–942
Whittaker RH (1960) Vegetation of the Siskiyou mountains, Oregon and California. Ecol Monogr 30:279–338
Willerslev E, Hansen AJ, Binladen J, Brand TB, Gilbert MTP, Shapiro B, Bunce M, Wiuf C, Gilichinsky DA, Cooper A (2003) Diverse plant and animal genetic records from Holocene and Pleistocene sediments. Science 300:791–795
Wisz MS, Broennimann O, Grønkjaer P, Møller PR, Olsen SM, Swingedouw D, Hedeholm RB, Nielsen EE, Guisan A, Pellissier L (2015) Arctic warming will promote Atlantic-Pacific fish interchange. Nat Clim Chang 5:261–265
Yamamoto S, Minami K, Fukaya K, Takahashi K, Sawada H, Murakami H, Tsuji S, Hashizume H, Kubonaga S, Horiuchi T, Hongo M, Nishida J, Okugawa Y, Fujiwara A, Fukuda M, Hidaka S, Suzuki KW, Miya M, Araki H, Yamanaka H, Maruyama A, Miyashita K, Masuda R, Minamoto T, Kondoh M (2016) Environmental DNA as a “snapshot”of fish distribution: a case study of japanese jack mackerel in Maizuru Bay, Sea of Japan. PloS One 11:e0149786
Acknowledgements
This study was funded by the Danish National Research Foundation with Grant DNRF94, which was awarded to Prof. Eske Willerslev. We thank Aage V. Jensen’s foundations, which have funded the National Fish Atlas with Grant 100307-28272. We thank Prof. Eske Willerslev for project support and providing facilities for carrying out the research. We would like to thank Lillian A. Petersen and the National High-throughput DNA Sequencing Centre for help with sequencing. Morten Rasmussen is thanked for providing a custom-made script and bioinformatic assistance during data analysis of the first test sequencing.
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Sigsgaard, E.E., Nielsen, I.B., Carl, H. et al. Seawater environmental DNA reflects seasonality of a coastal fish community. Mar Biol 164, 128 (2017). https://doi.org/10.1007/s00227-017-3147-4
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DOI: https://doi.org/10.1007/s00227-017-3147-4