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Biomonitoring of Non-Native Species Through eDNA Metabarcoding Method and Risk Screening for Ballast Water in Northwest Türkiye

Year 2025, Volume: 31 Issue: 2, 470 - 495, 25.03.2025

Abstract

The exponential development of maritime transport has made ballast water a primary vector for the spread of invasive organisms across the aquatic realm. This research aims to present a comprehensive overview of methodological and bioinformatic considerations for eDNA metabarcoding applied to ballast water from ships in İzmit Gulf, northwest Türkiye, with an emphasis on non-native species. The data related to DNA sequences for COI, 18Sv8, 18Sv4, 16S, and 12S presented a broad diverse taxonomic group for both microbial and macroscopic species, even for rare ones, with numbers of 93, 191, 241, 19, and 44, respectively. Additionally, the research unveiled the presence of highly invasive species such as Rhopilema nomadica and identified their invasiveness risk for İzmit Gulf, primarily due to elevated water temperatures in relation to climate change. The outlined results indicate that metabarcoding offers a potential tool for early detection of non-indigenous species and implementing management plans in view of current global warming interactions.

Supporting Institution

ANKARA Üniversitesi BAP

Project Number

18L0447013

References

  • Alberdi A, Aizpurua O, Gilbert M T P & Bohmann K (2018). Scrutinizing key steps for reliable metabarcoding of environmental samples. Methods in Ecology and Evolution 9: 134–147. https://doi.org/doi:10.1111/2041-210X.12849.
  • Ammon U V, Wood S A, Laroche O, Zaiko A, Tait L, Lavery S, Inglis G J & Pochon X (2018). Combining morpho-taxonomy and metabarcoding enhances the detection of non-indigenous marine pests in biofouling communities. Scientific Reports, 8(1): 1-11. https://doi.org/10.1038/s41598-018-34541-1.
  • Andrews S (2010). FastQC: A quality control tool for high throughput sequence data. http://www.bioinformatics.babraham.ac.uk/projects/fastqc/.
  • Antich A, Palacín C, Cebrian E, Golo R, Wangensteen O S & Turon X. (2021). Marine biomonitoring with eDNA: Can metabarcoding of water samples cut it as a tool for surveying benthic communities? Molecular Ecology, 30: 3175–3188. https://doi.org/10.1111/mec.15641.
  • Aylagas E, Borja Á, Muxika I & Rodríguez-Ezpeleta N (2018). Adapting metabarcoding-based benthic biomonitoring into routine marine ecological status assessment networks. Ecological Indicators, 95: 194–202. https://doi.org/10.1016/j.ecolind.2018.07.044.
  • Bautista J A, Manubag J J, Sumaya N H, Martinez J G & Tabugo S R (2023). Environmental DNA (eDNA) metabarcoding and fish visual census reveals the first record of Doboatherina magnidentata in the Philippines. Biodiversitas, 24(5): 3063-3072. https://doi.org/10.13057/biodiv/d240562.
  • Blackman R C, Constable D, Hahn C, Sheard A M, Durkota J, Hänfling B & Lawson Handley L (2017). Detection of a new non-native freshwater species by DNA metabarcoding of environmental samples-first record of Gammarus fossarum in the UK. Aquatic Invasions, 2(2): 177-189. https://doi.org/10.3391/ai.2017.12.2.06.
  • Bradie J (2016). METEOR Voyage M116/2: Report on performance of ballast water collection and analysis devices. Prepared for BSH (German Federal Maritime and Hydrographic Agency): 130 pages.
  • Bradley I M, Pinto A J & Guest J S (2016). Design and evaluation of Illumina MiSeq-compatible, 18S rRNA gene-specific primers for improved characterization of mixed phototrophic communities. Applied and Environmental Microbiology, 82(19): 5878-5891. https://doi.org/10.1128/AEM.01630-16.
  • Borrell Y J, Miralles L, Do Huu H, Mohammed-Geba K & Garcia-Vazquez E (2017). DNA in a bottle—rapid metabarcoding survey for early alerts of invasive species in ports. PloS One, 12(9): 1-17. https://doi.org/10.1371/journal.pone.0183347.
  • Bourlat S J, Haenel Q, Finnman J & Leray M (2016). Preparation of amplicon libraries for metabarcoding of marine eukaryotes using Illumina MiSeq: the dual-PCR method. Methods in molecular biology, 1452: 197-207. https://doi.org/10.1007/978-1-4939-3774-5_13.
  • Boyer F, Mercier C, Bonin A, Le Bras Y, Taberlet P, Coissac E (2016). Obitools: a unix-inspired software package for DNA metabarcoding. Molecular Ecology Resources, 16(1): 176–182. https://doi.org/10.1111/1755-0998.12428.
  • Carraro L, Mächler E, Wüthrich R & Altermatt F (2020). Environmental DNA allows upscaling spatial patterns of biodiversity in freshwater ecosystems. Nature Communications, 11(1): 1–12. https://doi.org/10.1038/s41467-020-17337-8.
  • Chambert T, Pilliod D S, Goldberg C S, Doi H & Takahara T (2018). An analytical framework for estimating aquatic species density from environmental DNA. Ecology and Evolution; 8: 3468–3477.https://doi.org/10.1002/ece3.3764.
  • Comtet T, Sandionigi A, Viard F & Casiraghi M (2015). DNA (meta) barcoding of biological invasions: a powerful tool to elucidate invasion processes and help managing aliens. Biological invasions, 17(3): 905-922. https://doi.org/10.1007/s10530-015-0854-y.
  • Copp G H, Vilizzi L, Tidbury H, Stebbing P D, Tarkan A S, Moissec L & Goulletquer P (2016). Development of a generic decision-support tool for identifying potentially invasive aquatic taxa: AS-ISK. Management of biological invasions, 7(4): 343–350. https://doi.org/10.3391/mbi.2016.7.4.04.
  • Deiner K, Bik H M, Mächler E, Seymour M, Lacoursière-Roussel A, Altermatt F, Creer S, Bista I, Lodge D M, de Vere N, Pfrender M E & Bernatchez L (2017). Environmental DNA metabarcoding: Transforming how we survey animal and plant communities. Molecular ecology, 26: 5872-5895. https://doi.org/10.1111/mec.14350.
  • Doi H, Fukaya K, Oka S, Sato K, Kondoh M & Miya M (2019). Evaluation of detection probabilities at the waterfiltering and initial PCR steps in environmental DNA metabarcoding using a multispecies site occupancy model. Scientific Reports, 9: 3581. https://doi.org/10.1038/s41598-019-40233-1.
  • Dugal L, Thomas L, Meenakshisundaram A,·Simpson T, Lines R, Colquhoun J, Jarman S & Meekan M (2023). Distinct coral reef habitat communities characterized by environmental DNA metabarcoding. Coral Reefs, 42: 17-30. https://doi.org/10.1007/s00338-022-02301-3.
  • Elton C S (1942). Voles, mice and lemmings: problems in populations dynamics. Clarendon press, Oxford. Fonseca V G, Davison P I, Creach V, Stone D, Bass D & Tidbury H J (2023). The Application of eDNA for Monitoring Aquatic Non- Indigenous Species: Practical and Policy Considerations. Diversity, 15: 631. https://doi.org/10.3390/d15050631
  • Freeland J R (2017). The importance of molecular markers and primer design when characterizing biodiversity from environmental DNA. Genome, 60: 358–374. https://doi.org/10.1139/gen-2016-0100.
  • Furlan E M & Gleeson D (2016). Improving reliability in environmental DNA detection surveys through enhanced quality control. Marine and Freshwater Research, 68(2), 388–395. https://doi.org/10.1071/MF15349.
  • Galil B S, Spanier E & Ferguson W W (1990). The Scyphomedusae of theMediterranean coast of Israel, including two lessepsian migrants new to theMediterranean. Zoologische Mededelingen, Leiden 64: 95-105.
  • Gehri R R, Larson W A, Gruenthal K, Sard N M & Shi Y (2021). eDNA metabarcoding outperforms traditional fisheries sampling and reveals fine-scale heterogeneity in a temperate freshwater lake. Environmental DNA, 3(5): 912–929. https://doi.org/10.1002/edn3.197.
  • Ghabooli S, Zhan A, Paolucci E, Hernandez M R, Briski E. Cristescu M E & MacIsaac H J (2016). Population attenuation in zooplankton communities during transoceanic transfer in balast water. Ecology and Evolution, 6: 6170–6177. https://doi.org/10.1002/ece3.2349.
  • Gibb C, Pratt N & Sessa R (2013). The Youth Guide to Biodiversity. http://www.fao.org/3/i3157e/i3157e02.pdf. Access: 07.11.2023.
  • Giroux M S, Reichman J R, Langknecht T, Burgess R M & Ho K T (2022). Environmental RNA as a Tool for Marine Community Biodiversity Assessments. Scientific Reports, 12: 17782. https://doi.org/10.1038/s41598-022-22198-w.
  • Gold Z, Sprague J, Kushner D J, Zerecero Marin E & Barber P H (2021). eDNA metabarcoding as a biomonitoring tool for marine protected areas. PloS one, 16(2): e0238557. https://doi.org/10.1371/journal.pone.0238557.
  • Goldberg C S, Sepulveda A, Ray A, Baumgardt J & Waits L P (2013). Environmental DNA as a new method for early detection of New Zealand mudsnails (Potamopyrgus antipodarum). Freshwater Science, 32(3): 792-800. https://doi.org/10.1899/13-046.1.
  • Goldberg C S, Turner C R, Deiner K, Klymus K E, Thomsen P F, Murphy M A, Spear S F, McKee A, Oyler–McCance S J & Cornman R S (2016). Critical considerations for the application of environmental DNA methods to detect aquatic species. Methods in Ecology and Evolution, 7(11): 1299–1307. https://doi.org/10.1111/2041-210X.12595.
  • Grey E K, Bernatchez L, Cassey P, Deiner K, Deveney M, Howland K L, Lacoursière-Roussel A, Leong S C Y, Li Y, Olds B, Pfrender M E, Prowse T A A, Renshaw M A & Lodge D M (2018). Effects of sampling effort on biodiversity patterns estimated from environmental DNA metabarcoding surveys. Scientific Reports, 8(1): 1-10. https://doi.org/10.1038/s41598-018-27048-2.
  • Gülşahin N (2017). A Freshwater Jellyfish in Pond Ula, Muğla: Craspedacusta sowerbii Lankester, 1880. Journal of Aquaculture Engineering and Fisheries Research, 3(2): 82-86.
  • He X, Jeffery N W, Stanley R R E, Hamilton L C, Rubidge E M & Abbott C L (2023). eDNA metabarcoding enriches traditional trawl survey data for monitoring biodiversity in the marine environment. ICES Journal of Marine Science, 80: 1529–1538. https://doi.org/10.1093/icesjms/fsad083.
  • Hellmann J J, Byers J E, Bierwagen B G & Dukes J S (2008). Five potential consequences of climate change for invasive species. Conservation Biology, 22(3): 534-543. https://doi.org/10.1111/j.1523-1739.2008.00951.x
  • Huerlimann R, Cooper M, Edmunds R, Villacorta–Rath C, Le Port A, Robson H, Strugnell J, Burrows D & Jerry D (2020). Enhancing tropical conservation and ecology research with aquatic environmental DNA methods: an introduction for non-environmental DNA specialists. Animal Conservation, 23(6): 632–645. https://doi.org/10.1111/acv.12583.
  • IMO (2004). International Convention for the Control and Management of Ships' Ballast Water and Sediments. IMO 2023. Access: 07.11.2023. https://wwwcdn.imo.org/localresources/en/About/Conventions/StatusOfConventions/StatusOfTreatiesByCountry%20(2).pdf
  • IPCC (2005). Carbon Dioxide Capture and Storage. Metz B, Davidson O, de Coninck H, Loos M & Meyer L (Eds.) Cambridge University Press, UK. pp 431.
  • Jeunen G J, Knapp M, Spencer H G, Taylor H R, Lamare M D, Stat M, Bunce M & Gemmell N J (2019). Species‐level biodiversity assessment using marine environmental DNA metabarcoding requires protocol optimization and standardization. Ecology and Evolution, 9(3): 1323- 1335. https://doi.org/10.1002/ece3.4843.
  • Keskin E & Atar H H (2013). DNA Barcoding: Molecular Identification Using Mitochondrial COI Gene. Türk Bilimsel Derlemeler Dergisi, 6(2): 01-08.
  • Kıdeys A E & Gücü A C (1995). Rhopilema nomadica: A Lessepsian scyphomedusan new to the Mediterranean coast of Turkey. Israel Journal of Zoology, 41: 615–617. https://doi.org/10.1080/00212210.1995.10688827.
  • Killi N, Tarkan A S, Kozic S, Copp G H, Davison P I & Vilizzi L (2020). Risk screening of the potential invasiveness of non-native jellyfishes in the Mediterranean Sea. Marine Pollution Bulletin, 150: 110728. https://doi.org/10.1016/j.marpolbul.2019.110728.
  • Lacoursière-Roussel A, Howland K, Normandeau E, Grey E K, Archambault P, Deiner K, Lodge D M, Hernandez C, Leduc N & Bernatchez L (2018). eDNA metabarcoding as a new surveillance approach for coastal Arctic biodiversity. Ecology and Evolution, 8(16): 7763-7777. https://doi.org/10.1002/ece3.4213.
  • Li R, Gao Y, Hou Y, Ye S, Wang L, Sun J & Li Q (2018). Mitochondrial genome sequencing and analysis of scuticociliates (Uronema marinum) isolated from Takifugu rubripes. Mitochondrial DNA Part B, 3(2): 736-737. https://doi.org/10.1080/23802359.2018.1483757.
  • McClenaghan B, Fahner N, Cote D, Chawarski J, McCarthy A, Rajabi H, Singer G & Hajibabaei M (2020). Harnessing the power of eDNA metabarcoding for the detection of deep–sea fishes. PLoS One, 15(11): e0236540. https://doi.org/10.1371/journal.pone.0236540.
  • Miya M, Sato Y, Fukunaga T, Sado T, Poulsen J Y, Sato K, Minamoto T, Yamamoto S, Yamanaka H, Araki H, Kondoh M & Iwasaki W (2015). MiFish, a set of universal PCR primers for metabarcoding environmental DNA from fishes: detection of more than 230 subtropical marine species. Royal Society Open Science, 2(7): 150088. https://doi.org/10.1098/rsos.150088.
  • Oka S I, Doi H, Miyamoto K, Hanahara N, Sado T & Miya M (2021). Environmental DNA metabarcoding for biodiversity monitoring of a highly diverse tropical fish community in a coral reef lagoon: Estimation of species richness and detection of habitat segregation. Environmental DNA, 3: 55–69. https://doi.org/10.1002/edn3.132.
  • Ojaveer H, Galil B S, Carlton J T, Alleway H, Goulletquer P, Lehtiniemi M, Marchini A, Miller W, Occhipinti-Ambrogi A, Peharda M, Ruiz G M, Williams S L & Zaiko A (2018). Historical baselines in marine bioinvasions: Implications for policy and management. PLoS One, 13: e0202383. https://doi.org/10.1371/journal.pone.0202383.
  • Öztürk B & İşinibilir M (2010). An alien jellyfish Rhopilema nomadica and its impacts to the Eastern Mediterranean part of Turkey. J. Black Sea/Mediterranean Environment, 16(2): 149-156.
  • Pascher K, Švara V & Jungmeier M (2022). Environmental DNA-Based Methods in Biodiversity Monitoring of Protected Areas: Application Range, Limitations, and Needs. Diversity, 14: 463. https://doi.org/10.3390/d14060463.
  • Pawluczyk M, Weiss J, Links M G, Aranguren M E, Wilkinson M D & Egea-Cortines M (2015). Quantitative evaluation of bias in PCR amplification and next-generation sequencing derived from metabarcoding samples. Analytical and Bioanalytical Chemistry, 407: 1841– 1848. https://doi.org/10.1007/s00216-014-8435-y.
  • Pochon X, Bott N J, Smith K F & Wood S A (2013). Evaluating detection limits of next- generation sequencing for the surveillance and monitoring of international marine pests. PLoS One, 8: e73935. https://doi.org/10.1371/journal.pone.0073935.
  • Polanco Fernández A, Marques V, Fopp F, Juhel J B, Borrero-Pérez G H, Cheutin M C, Dejean T, Corredor J D G, Acosta-Chaparro A, Hocdé R, Eme D, Maire E, Spescha M, Valentini A, Manel S, Mouillot D, Albouy C & Pellissier L (2021). Comparing environmental DNA metabarcoding and underwater visual census to monitor tropical reef fishes. Environmental DNA, 3 (4): 142–156. https://doi.org/10.1002/edn3.140.
  • Rahel F J & Olden J D (2008). Assessing the effects of climate change on aquatic invasive species. Conservation Biology, 22(3): 521-533. https://doi.org/10.1111/j.1523-1739.2008.00950.x
  • Rey A (2019). From port to ballast water: application of ADN metabarcoding of shipborne biodiversity. Thesis, 207 p. http://hdl.handle.net/10651/52628.
  • Rishan S T, Kline R J & Rahman S (2023). Applications of environmental DNA (eDNA) to detect subterranean and aquatic invasive species: A critical review on the challenges and limitations of eDNA metabarcoding. Environmental Advances, 12: 100370. https://doi.org/10.1016/j.envadv.2023.100370.
  • Roy H E, Rabitsch W, Scalera R, Stewart A, Gallardo B, Genovesi P, Essl F, Adriaens T, Bacher S, Booy O, Branquart E, Brunel S, Copp G H, Dean H, D’hondt B, Josefsson M, Kenis M, Kettunen M, Linnamagi M, Lucy F, Martinou A, Moore N, Nentwig W, Perg A J, Peyton
  • J, Roques A, Schindler S, Schönrogge K, Solarz W, Stebbing P D, Trichkova T, Vanderhoeven S, van Valkenburg J & Zenetos A (2018). Developing a framework of minimum standards for the risk assessment of alien species. Journal of Applied Ecology, 55 (2): 526–538. https://doi.org/10.1111/1365-2664.13025.
  • Sanchez L, Boulanger E, Arnal V, Boissery P, Dalongeville A, Dejeand T, Deterf J, Guellatia N, Holonf F, Juhela J B, Lenfantg P, Leprieura F, Valentinid A, Manela S & Mouillota D (2022). Ecological indicators based on quantitative eDNA metabarcoding: the case of marine reserves. Ecological Indicators, 140: 108966. https://doi.org/10.1016/j.ecolind.2022.108966.
  • Sassoubre L M, Yamahara K M, Gardner L D, Block B A & Boehm A B (2016). Quantification of Environmental DNA (eDNA) Shedding and Decay Rates for Three Marine Fish. Environmental Science & Technology, 50: 10456–10464. https://doi.org/10.1021/acs.est.6b03114.
  • Shaw J L A, Weyrich L & Cooper A (2017). Using environmental (e)DNA sequencing for aquatic biodiversity surveys: a beginner’s guide. Marine and Freshwater Research, 68(1): 20–33. https://doi.org/10.1071/MF15361.
  • Spens J, Evans A R, Halfmaerten D, Knudsen S W, Sengupta M E, Mak S S T, Sigsgaard E E & Hellström M (2017). Comparison of capture and storage methods for aqueous macrobial eDNA using an optimized extraction protocol: advantage of enclosed filter. Methods in Ecology and Evolution, 8: 635–645. https://doi.org/10.1111/2041- 210X.12683.
  • Stat M, John J, Di Battista J D, Newman S J, Bunce M & Harvey E S (2019). Combined use of eDNA metabarcoding and video surveillance for the assessment of fish biodiversity. Conservation Biology, 33:196–205. https://doi.org/10.1111/cobi.13183.
  • Tarkan A S, Vilizzi L, Top N, Ekmekçi G, Stebbing P D & Copp G H (2017). Identification of potentially invasive freshwater fishes, including translocated species, in Turkey using the Aquatic Species Invasiveness Screening Kit (AS-ISK). International Review of Hydrobiology, 102: 47-56. https://doi.org/10.1002/iroh.201601877
  • Tarkan A S, Emiroğlu Ö, Aksu S, Başkurt S, Aksu I, Vilizzi L & Yoğurtçuoğlu B (2022). Coupling molecular and risk analysis to investigate the origin, distribution and potential impact of non-native species: an application to ruffe Gymnocephalus cernua in Turkey. The European Zoological Journal, 89(1): 109-121. https://doi.org/10.1080/24750263.2021.2022222.
  • Thomsen P F, Kielgast J, Iversen L L, Møller P R, Rasmussen M & Willerslev E (2012). Detection of a Diverse Marine Fish Fauna Using Environmental DNA from Seawater Samples. PLoS ONE, 7: e41732. https://doi.org/10.1371/journal.pone.0041732.
  • Turan C, Gürlek M, Özbalcılar B, Yağlıoğlu D, Ergüden D, Öztürk B & Güngör M (2011). Jellyfish bycatch data by puse seine, trawl and net fisheries during March–April 2011 in the Mediterranean coasts of Turkey. In First National Workshop on Jellyfish and Other Gelatinous Species in Turkish Marine Waters, Bodrum, 20–21 May 2011. Turkish Marine Research Foundation, (In: Turan, C., Öztürk, B. eds.) (Istanbul, Turkey).
  • Türe M (2021). Molecular identification of Uronema marinum (Protozoa, Ciliophora, Scuticociliatia) in cultured turbot (Psetta maxima) larvae. Veterinary Research Forum, 12(1): 121-124. https://doi.org/10.30466/vrf.2020.110220.2614.
  • Valdivia–Carrillo T, Rocha–Olivares A, Reyes–Bonilla H, Domínguez–Contreras J F & Munguia–Vega A (2021). Integrating eDNA metabarcoding and simultaneous underwater visual surveys to describe complex fish communities in a marine biodiversity hotspot. Molecular Ecology Resources, 21(5): 1558–1574. https://doi.org/10.1111/1755-0998.13375.
  • Van Driessche C, Everts T, Neyrinck S & Brys R (2023). Experimental assessment of downstream environmental DNA patterns under variable fish biomass and river discharge rates. Environmental DNA, 5(1): 102-116. https://doi.org/10.1002/edn3.361.
  • Vences M, Lyra M, Bina Perl R G, Bletz M C, Stanković D, Lopes C, Jarek M, Bhuju S, Geffers R, Haddad C & Steinfartz S (2016). Freshwater vertebrate metabarcoding on Illumina platforms using double-indexed primers of the mitochondrial 16S rRNA gene. Conservation Genetics Resources, 8(3): 2–6. https://doi.org/10.1007/s12686-016-0550-y.
  • Verling E, Ruiz G M, Smith L D, Galil B, Miller A W & Murphy K R (2005). Supply-side invasion ecology: characterizing propagule pressure in coastal ecosystems. Proceedings of the Royal Society B: Biological Sciences, 272(1569): 1249–1257. https://doi.org/10.1098/rspb.2005.3090.
  • Vilizzi L, Copp, G H, Hill J E, Adamovich B, Aislabie L, Akin D, Al-Faisal A J, Almeida D, Azmai M N A, Bakiu R,
  • Bellati A, Bernier R, Bies J M, Bilge G, Branco P, Bui T D, Canning-Clode J, Cardoso Ramos H A, Castellanos-
  • Galindo G A, Castro N, Chaichana R, Chainho P, Chan J, Cunico A M, Curd A, Dangchana P, Dashinov D,
  • Davison P I, de Camargo M P, Dodd J A, Durland Donahou A L, Edsman L, Ekmekçi F G, Elphinstone-Davis J,
  • Erős T, Evangelista C, Fenwick G, Ferincz Á, Ferreira T, Feunteun E, Filiz H, Forneck S C, Gajduchenko H S,
  • Gama Monteiro J, Gestoso I, Giannetto D, Gilles A S Jr, Gizzi F, Glamuzina B, Glamuzina L, Goldsmit J,
  • Gollasch S, Goulletquer P, Grabowska J, Harmer R, Haubrock P J, He D, Hean J W, Herczeg G, Howland KL,
  • İlhan A, Interesova E, Jakubčinová K, Jelmert A, Johnsen S I, Kakareko T, Kanongdate K, Killi N, Kim J E,
  • Kırankaya Ş G, Kňazovická D, Kopecký O, Kostov V, KoutsikosN, Kozic S, Kuljanishvili T, Kumar B, Kumar L,
  • Kurita Y, Kurtul I, Lazzaro L, Lee L, Lehtiniemi M, Leonardi G, Leuven R.S E W, Li S, Lipinskaya T, Liu F, Lloyd L,
  • Lorenzoni M, Luna S A, Lyons T J, Magellan K, Malmstrøm M, Marchini A, Marr S M, Masson G, Masson L,
  • McKenzie, C H, Memedemin D, Mendoza R, Minchin D, Miossec L, Moghaddas S D, Moshobane M C,
  • Mumladze L, Naddafi R,
  • Najafi-Majd E, Năstase A, Năvodaru I, Neal J W, Nienhuis S, Nimtim M, Nolan E T,Occhipinti-Ambrogi A, Ojaveer H, Olenin S, Olsson
Year 2025, Volume: 31 Issue: 2, 470 - 495, 25.03.2025

Abstract

Project Number

18L0447013

References

  • Alberdi A, Aizpurua O, Gilbert M T P & Bohmann K (2018). Scrutinizing key steps for reliable metabarcoding of environmental samples. Methods in Ecology and Evolution 9: 134–147. https://doi.org/doi:10.1111/2041-210X.12849.
  • Ammon U V, Wood S A, Laroche O, Zaiko A, Tait L, Lavery S, Inglis G J & Pochon X (2018). Combining morpho-taxonomy and metabarcoding enhances the detection of non-indigenous marine pests in biofouling communities. Scientific Reports, 8(1): 1-11. https://doi.org/10.1038/s41598-018-34541-1.
  • Andrews S (2010). FastQC: A quality control tool for high throughput sequence data. http://www.bioinformatics.babraham.ac.uk/projects/fastqc/.
  • Antich A, Palacín C, Cebrian E, Golo R, Wangensteen O S & Turon X. (2021). Marine biomonitoring with eDNA: Can metabarcoding of water samples cut it as a tool for surveying benthic communities? Molecular Ecology, 30: 3175–3188. https://doi.org/10.1111/mec.15641.
  • Aylagas E, Borja Á, Muxika I & Rodríguez-Ezpeleta N (2018). Adapting metabarcoding-based benthic biomonitoring into routine marine ecological status assessment networks. Ecological Indicators, 95: 194–202. https://doi.org/10.1016/j.ecolind.2018.07.044.
  • Bautista J A, Manubag J J, Sumaya N H, Martinez J G & Tabugo S R (2023). Environmental DNA (eDNA) metabarcoding and fish visual census reveals the first record of Doboatherina magnidentata in the Philippines. Biodiversitas, 24(5): 3063-3072. https://doi.org/10.13057/biodiv/d240562.
  • Blackman R C, Constable D, Hahn C, Sheard A M, Durkota J, Hänfling B & Lawson Handley L (2017). Detection of a new non-native freshwater species by DNA metabarcoding of environmental samples-first record of Gammarus fossarum in the UK. Aquatic Invasions, 2(2): 177-189. https://doi.org/10.3391/ai.2017.12.2.06.
  • Bradie J (2016). METEOR Voyage M116/2: Report on performance of ballast water collection and analysis devices. Prepared for BSH (German Federal Maritime and Hydrographic Agency): 130 pages.
  • Bradley I M, Pinto A J & Guest J S (2016). Design and evaluation of Illumina MiSeq-compatible, 18S rRNA gene-specific primers for improved characterization of mixed phototrophic communities. Applied and Environmental Microbiology, 82(19): 5878-5891. https://doi.org/10.1128/AEM.01630-16.
  • Borrell Y J, Miralles L, Do Huu H, Mohammed-Geba K & Garcia-Vazquez E (2017). DNA in a bottle—rapid metabarcoding survey for early alerts of invasive species in ports. PloS One, 12(9): 1-17. https://doi.org/10.1371/journal.pone.0183347.
  • Bourlat S J, Haenel Q, Finnman J & Leray M (2016). Preparation of amplicon libraries for metabarcoding of marine eukaryotes using Illumina MiSeq: the dual-PCR method. Methods in molecular biology, 1452: 197-207. https://doi.org/10.1007/978-1-4939-3774-5_13.
  • Boyer F, Mercier C, Bonin A, Le Bras Y, Taberlet P, Coissac E (2016). Obitools: a unix-inspired software package for DNA metabarcoding. Molecular Ecology Resources, 16(1): 176–182. https://doi.org/10.1111/1755-0998.12428.
  • Carraro L, Mächler E, Wüthrich R & Altermatt F (2020). Environmental DNA allows upscaling spatial patterns of biodiversity in freshwater ecosystems. Nature Communications, 11(1): 1–12. https://doi.org/10.1038/s41467-020-17337-8.
  • Chambert T, Pilliod D S, Goldberg C S, Doi H & Takahara T (2018). An analytical framework for estimating aquatic species density from environmental DNA. Ecology and Evolution; 8: 3468–3477.https://doi.org/10.1002/ece3.3764.
  • Comtet T, Sandionigi A, Viard F & Casiraghi M (2015). DNA (meta) barcoding of biological invasions: a powerful tool to elucidate invasion processes and help managing aliens. Biological invasions, 17(3): 905-922. https://doi.org/10.1007/s10530-015-0854-y.
  • Copp G H, Vilizzi L, Tidbury H, Stebbing P D, Tarkan A S, Moissec L & Goulletquer P (2016). Development of a generic decision-support tool for identifying potentially invasive aquatic taxa: AS-ISK. Management of biological invasions, 7(4): 343–350. https://doi.org/10.3391/mbi.2016.7.4.04.
  • Deiner K, Bik H M, Mächler E, Seymour M, Lacoursière-Roussel A, Altermatt F, Creer S, Bista I, Lodge D M, de Vere N, Pfrender M E & Bernatchez L (2017). Environmental DNA metabarcoding: Transforming how we survey animal and plant communities. Molecular ecology, 26: 5872-5895. https://doi.org/10.1111/mec.14350.
  • Doi H, Fukaya K, Oka S, Sato K, Kondoh M & Miya M (2019). Evaluation of detection probabilities at the waterfiltering and initial PCR steps in environmental DNA metabarcoding using a multispecies site occupancy model. Scientific Reports, 9: 3581. https://doi.org/10.1038/s41598-019-40233-1.
  • Dugal L, Thomas L, Meenakshisundaram A,·Simpson T, Lines R, Colquhoun J, Jarman S & Meekan M (2023). Distinct coral reef habitat communities characterized by environmental DNA metabarcoding. Coral Reefs, 42: 17-30. https://doi.org/10.1007/s00338-022-02301-3.
  • Elton C S (1942). Voles, mice and lemmings: problems in populations dynamics. Clarendon press, Oxford. Fonseca V G, Davison P I, Creach V, Stone D, Bass D & Tidbury H J (2023). The Application of eDNA for Monitoring Aquatic Non- Indigenous Species: Practical and Policy Considerations. Diversity, 15: 631. https://doi.org/10.3390/d15050631
  • Freeland J R (2017). The importance of molecular markers and primer design when characterizing biodiversity from environmental DNA. Genome, 60: 358–374. https://doi.org/10.1139/gen-2016-0100.
  • Furlan E M & Gleeson D (2016). Improving reliability in environmental DNA detection surveys through enhanced quality control. Marine and Freshwater Research, 68(2), 388–395. https://doi.org/10.1071/MF15349.
  • Galil B S, Spanier E & Ferguson W W (1990). The Scyphomedusae of theMediterranean coast of Israel, including two lessepsian migrants new to theMediterranean. Zoologische Mededelingen, Leiden 64: 95-105.
  • Gehri R R, Larson W A, Gruenthal K, Sard N M & Shi Y (2021). eDNA metabarcoding outperforms traditional fisheries sampling and reveals fine-scale heterogeneity in a temperate freshwater lake. Environmental DNA, 3(5): 912–929. https://doi.org/10.1002/edn3.197.
  • Ghabooli S, Zhan A, Paolucci E, Hernandez M R, Briski E. Cristescu M E & MacIsaac H J (2016). Population attenuation in zooplankton communities during transoceanic transfer in balast water. Ecology and Evolution, 6: 6170–6177. https://doi.org/10.1002/ece3.2349.
  • Gibb C, Pratt N & Sessa R (2013). The Youth Guide to Biodiversity. http://www.fao.org/3/i3157e/i3157e02.pdf. Access: 07.11.2023.
  • Giroux M S, Reichman J R, Langknecht T, Burgess R M & Ho K T (2022). Environmental RNA as a Tool for Marine Community Biodiversity Assessments. Scientific Reports, 12: 17782. https://doi.org/10.1038/s41598-022-22198-w.
  • Gold Z, Sprague J, Kushner D J, Zerecero Marin E & Barber P H (2021). eDNA metabarcoding as a biomonitoring tool for marine protected areas. PloS one, 16(2): e0238557. https://doi.org/10.1371/journal.pone.0238557.
  • Goldberg C S, Sepulveda A, Ray A, Baumgardt J & Waits L P (2013). Environmental DNA as a new method for early detection of New Zealand mudsnails (Potamopyrgus antipodarum). Freshwater Science, 32(3): 792-800. https://doi.org/10.1899/13-046.1.
  • Goldberg C S, Turner C R, Deiner K, Klymus K E, Thomsen P F, Murphy M A, Spear S F, McKee A, Oyler–McCance S J & Cornman R S (2016). Critical considerations for the application of environmental DNA methods to detect aquatic species. Methods in Ecology and Evolution, 7(11): 1299–1307. https://doi.org/10.1111/2041-210X.12595.
  • Grey E K, Bernatchez L, Cassey P, Deiner K, Deveney M, Howland K L, Lacoursière-Roussel A, Leong S C Y, Li Y, Olds B, Pfrender M E, Prowse T A A, Renshaw M A & Lodge D M (2018). Effects of sampling effort on biodiversity patterns estimated from environmental DNA metabarcoding surveys. Scientific Reports, 8(1): 1-10. https://doi.org/10.1038/s41598-018-27048-2.
  • Gülşahin N (2017). A Freshwater Jellyfish in Pond Ula, Muğla: Craspedacusta sowerbii Lankester, 1880. Journal of Aquaculture Engineering and Fisheries Research, 3(2): 82-86.
  • He X, Jeffery N W, Stanley R R E, Hamilton L C, Rubidge E M & Abbott C L (2023). eDNA metabarcoding enriches traditional trawl survey data for monitoring biodiversity in the marine environment. ICES Journal of Marine Science, 80: 1529–1538. https://doi.org/10.1093/icesjms/fsad083.
  • Hellmann J J, Byers J E, Bierwagen B G & Dukes J S (2008). Five potential consequences of climate change for invasive species. Conservation Biology, 22(3): 534-543. https://doi.org/10.1111/j.1523-1739.2008.00951.x
  • Huerlimann R, Cooper M, Edmunds R, Villacorta–Rath C, Le Port A, Robson H, Strugnell J, Burrows D & Jerry D (2020). Enhancing tropical conservation and ecology research with aquatic environmental DNA methods: an introduction for non-environmental DNA specialists. Animal Conservation, 23(6): 632–645. https://doi.org/10.1111/acv.12583.
  • IMO (2004). International Convention for the Control and Management of Ships' Ballast Water and Sediments. IMO 2023. Access: 07.11.2023. https://wwwcdn.imo.org/localresources/en/About/Conventions/StatusOfConventions/StatusOfTreatiesByCountry%20(2).pdf
  • IPCC (2005). Carbon Dioxide Capture and Storage. Metz B, Davidson O, de Coninck H, Loos M & Meyer L (Eds.) Cambridge University Press, UK. pp 431.
  • Jeunen G J, Knapp M, Spencer H G, Taylor H R, Lamare M D, Stat M, Bunce M & Gemmell N J (2019). Species‐level biodiversity assessment using marine environmental DNA metabarcoding requires protocol optimization and standardization. Ecology and Evolution, 9(3): 1323- 1335. https://doi.org/10.1002/ece3.4843.
  • Keskin E & Atar H H (2013). DNA Barcoding: Molecular Identification Using Mitochondrial COI Gene. Türk Bilimsel Derlemeler Dergisi, 6(2): 01-08.
  • Kıdeys A E & Gücü A C (1995). Rhopilema nomadica: A Lessepsian scyphomedusan new to the Mediterranean coast of Turkey. Israel Journal of Zoology, 41: 615–617. https://doi.org/10.1080/00212210.1995.10688827.
  • Killi N, Tarkan A S, Kozic S, Copp G H, Davison P I & Vilizzi L (2020). Risk screening of the potential invasiveness of non-native jellyfishes in the Mediterranean Sea. Marine Pollution Bulletin, 150: 110728. https://doi.org/10.1016/j.marpolbul.2019.110728.
  • Lacoursière-Roussel A, Howland K, Normandeau E, Grey E K, Archambault P, Deiner K, Lodge D M, Hernandez C, Leduc N & Bernatchez L (2018). eDNA metabarcoding as a new surveillance approach for coastal Arctic biodiversity. Ecology and Evolution, 8(16): 7763-7777. https://doi.org/10.1002/ece3.4213.
  • Li R, Gao Y, Hou Y, Ye S, Wang L, Sun J & Li Q (2018). Mitochondrial genome sequencing and analysis of scuticociliates (Uronema marinum) isolated from Takifugu rubripes. Mitochondrial DNA Part B, 3(2): 736-737. https://doi.org/10.1080/23802359.2018.1483757.
  • McClenaghan B, Fahner N, Cote D, Chawarski J, McCarthy A, Rajabi H, Singer G & Hajibabaei M (2020). Harnessing the power of eDNA metabarcoding for the detection of deep–sea fishes. PLoS One, 15(11): e0236540. https://doi.org/10.1371/journal.pone.0236540.
  • Miya M, Sato Y, Fukunaga T, Sado T, Poulsen J Y, Sato K, Minamoto T, Yamamoto S, Yamanaka H, Araki H, Kondoh M & Iwasaki W (2015). MiFish, a set of universal PCR primers for metabarcoding environmental DNA from fishes: detection of more than 230 subtropical marine species. Royal Society Open Science, 2(7): 150088. https://doi.org/10.1098/rsos.150088.
  • Oka S I, Doi H, Miyamoto K, Hanahara N, Sado T & Miya M (2021). Environmental DNA metabarcoding for biodiversity monitoring of a highly diverse tropical fish community in a coral reef lagoon: Estimation of species richness and detection of habitat segregation. Environmental DNA, 3: 55–69. https://doi.org/10.1002/edn3.132.
  • Ojaveer H, Galil B S, Carlton J T, Alleway H, Goulletquer P, Lehtiniemi M, Marchini A, Miller W, Occhipinti-Ambrogi A, Peharda M, Ruiz G M, Williams S L & Zaiko A (2018). Historical baselines in marine bioinvasions: Implications for policy and management. PLoS One, 13: e0202383. https://doi.org/10.1371/journal.pone.0202383.
  • Öztürk B & İşinibilir M (2010). An alien jellyfish Rhopilema nomadica and its impacts to the Eastern Mediterranean part of Turkey. J. Black Sea/Mediterranean Environment, 16(2): 149-156.
  • Pascher K, Švara V & Jungmeier M (2022). Environmental DNA-Based Methods in Biodiversity Monitoring of Protected Areas: Application Range, Limitations, and Needs. Diversity, 14: 463. https://doi.org/10.3390/d14060463.
  • Pawluczyk M, Weiss J, Links M G, Aranguren M E, Wilkinson M D & Egea-Cortines M (2015). Quantitative evaluation of bias in PCR amplification and next-generation sequencing derived from metabarcoding samples. Analytical and Bioanalytical Chemistry, 407: 1841– 1848. https://doi.org/10.1007/s00216-014-8435-y.
  • Pochon X, Bott N J, Smith K F & Wood S A (2013). Evaluating detection limits of next- generation sequencing for the surveillance and monitoring of international marine pests. PLoS One, 8: e73935. https://doi.org/10.1371/journal.pone.0073935.
  • Polanco Fernández A, Marques V, Fopp F, Juhel J B, Borrero-Pérez G H, Cheutin M C, Dejean T, Corredor J D G, Acosta-Chaparro A, Hocdé R, Eme D, Maire E, Spescha M, Valentini A, Manel S, Mouillot D, Albouy C & Pellissier L (2021). Comparing environmental DNA metabarcoding and underwater visual census to monitor tropical reef fishes. Environmental DNA, 3 (4): 142–156. https://doi.org/10.1002/edn3.140.
  • Rahel F J & Olden J D (2008). Assessing the effects of climate change on aquatic invasive species. Conservation Biology, 22(3): 521-533. https://doi.org/10.1111/j.1523-1739.2008.00950.x
  • Rey A (2019). From port to ballast water: application of ADN metabarcoding of shipborne biodiversity. Thesis, 207 p. http://hdl.handle.net/10651/52628.
  • Rishan S T, Kline R J & Rahman S (2023). Applications of environmental DNA (eDNA) to detect subterranean and aquatic invasive species: A critical review on the challenges and limitations of eDNA metabarcoding. Environmental Advances, 12: 100370. https://doi.org/10.1016/j.envadv.2023.100370.
  • Roy H E, Rabitsch W, Scalera R, Stewart A, Gallardo B, Genovesi P, Essl F, Adriaens T, Bacher S, Booy O, Branquart E, Brunel S, Copp G H, Dean H, D’hondt B, Josefsson M, Kenis M, Kettunen M, Linnamagi M, Lucy F, Martinou A, Moore N, Nentwig W, Perg A J, Peyton
  • J, Roques A, Schindler S, Schönrogge K, Solarz W, Stebbing P D, Trichkova T, Vanderhoeven S, van Valkenburg J & Zenetos A (2018). Developing a framework of minimum standards for the risk assessment of alien species. Journal of Applied Ecology, 55 (2): 526–538. https://doi.org/10.1111/1365-2664.13025.
  • Sanchez L, Boulanger E, Arnal V, Boissery P, Dalongeville A, Dejeand T, Deterf J, Guellatia N, Holonf F, Juhela J B, Lenfantg P, Leprieura F, Valentinid A, Manela S & Mouillota D (2022). Ecological indicators based on quantitative eDNA metabarcoding: the case of marine reserves. Ecological Indicators, 140: 108966. https://doi.org/10.1016/j.ecolind.2022.108966.
  • Sassoubre L M, Yamahara K M, Gardner L D, Block B A & Boehm A B (2016). Quantification of Environmental DNA (eDNA) Shedding and Decay Rates for Three Marine Fish. Environmental Science & Technology, 50: 10456–10464. https://doi.org/10.1021/acs.est.6b03114.
  • Shaw J L A, Weyrich L & Cooper A (2017). Using environmental (e)DNA sequencing for aquatic biodiversity surveys: a beginner’s guide. Marine and Freshwater Research, 68(1): 20–33. https://doi.org/10.1071/MF15361.
  • Spens J, Evans A R, Halfmaerten D, Knudsen S W, Sengupta M E, Mak S S T, Sigsgaard E E & Hellström M (2017). Comparison of capture and storage methods for aqueous macrobial eDNA using an optimized extraction protocol: advantage of enclosed filter. Methods in Ecology and Evolution, 8: 635–645. https://doi.org/10.1111/2041- 210X.12683.
  • Stat M, John J, Di Battista J D, Newman S J, Bunce M & Harvey E S (2019). Combined use of eDNA metabarcoding and video surveillance for the assessment of fish biodiversity. Conservation Biology, 33:196–205. https://doi.org/10.1111/cobi.13183.
  • Tarkan A S, Vilizzi L, Top N, Ekmekçi G, Stebbing P D & Copp G H (2017). Identification of potentially invasive freshwater fishes, including translocated species, in Turkey using the Aquatic Species Invasiveness Screening Kit (AS-ISK). International Review of Hydrobiology, 102: 47-56. https://doi.org/10.1002/iroh.201601877
  • Tarkan A S, Emiroğlu Ö, Aksu S, Başkurt S, Aksu I, Vilizzi L & Yoğurtçuoğlu B (2022). Coupling molecular and risk analysis to investigate the origin, distribution and potential impact of non-native species: an application to ruffe Gymnocephalus cernua in Turkey. The European Zoological Journal, 89(1): 109-121. https://doi.org/10.1080/24750263.2021.2022222.
  • Thomsen P F, Kielgast J, Iversen L L, Møller P R, Rasmussen M & Willerslev E (2012). Detection of a Diverse Marine Fish Fauna Using Environmental DNA from Seawater Samples. PLoS ONE, 7: e41732. https://doi.org/10.1371/journal.pone.0041732.
  • Turan C, Gürlek M, Özbalcılar B, Yağlıoğlu D, Ergüden D, Öztürk B & Güngör M (2011). Jellyfish bycatch data by puse seine, trawl and net fisheries during March–April 2011 in the Mediterranean coasts of Turkey. In First National Workshop on Jellyfish and Other Gelatinous Species in Turkish Marine Waters, Bodrum, 20–21 May 2011. Turkish Marine Research Foundation, (In: Turan, C., Öztürk, B. eds.) (Istanbul, Turkey).
  • Türe M (2021). Molecular identification of Uronema marinum (Protozoa, Ciliophora, Scuticociliatia) in cultured turbot (Psetta maxima) larvae. Veterinary Research Forum, 12(1): 121-124. https://doi.org/10.30466/vrf.2020.110220.2614.
  • Valdivia–Carrillo T, Rocha–Olivares A, Reyes–Bonilla H, Domínguez–Contreras J F & Munguia–Vega A (2021). Integrating eDNA metabarcoding and simultaneous underwater visual surveys to describe complex fish communities in a marine biodiversity hotspot. Molecular Ecology Resources, 21(5): 1558–1574. https://doi.org/10.1111/1755-0998.13375.
  • Van Driessche C, Everts T, Neyrinck S & Brys R (2023). Experimental assessment of downstream environmental DNA patterns under variable fish biomass and river discharge rates. Environmental DNA, 5(1): 102-116. https://doi.org/10.1002/edn3.361.
  • Vences M, Lyra M, Bina Perl R G, Bletz M C, Stanković D, Lopes C, Jarek M, Bhuju S, Geffers R, Haddad C & Steinfartz S (2016). Freshwater vertebrate metabarcoding on Illumina platforms using double-indexed primers of the mitochondrial 16S rRNA gene. Conservation Genetics Resources, 8(3): 2–6. https://doi.org/10.1007/s12686-016-0550-y.
  • Verling E, Ruiz G M, Smith L D, Galil B, Miller A W & Murphy K R (2005). Supply-side invasion ecology: characterizing propagule pressure in coastal ecosystems. Proceedings of the Royal Society B: Biological Sciences, 272(1569): 1249–1257. https://doi.org/10.1098/rspb.2005.3090.
  • Vilizzi L, Copp, G H, Hill J E, Adamovich B, Aislabie L, Akin D, Al-Faisal A J, Almeida D, Azmai M N A, Bakiu R,
  • Bellati A, Bernier R, Bies J M, Bilge G, Branco P, Bui T D, Canning-Clode J, Cardoso Ramos H A, Castellanos-
  • Galindo G A, Castro N, Chaichana R, Chainho P, Chan J, Cunico A M, Curd A, Dangchana P, Dashinov D,
  • Davison P I, de Camargo M P, Dodd J A, Durland Donahou A L, Edsman L, Ekmekçi F G, Elphinstone-Davis J,
  • Erős T, Evangelista C, Fenwick G, Ferincz Á, Ferreira T, Feunteun E, Filiz H, Forneck S C, Gajduchenko H S,
  • Gama Monteiro J, Gestoso I, Giannetto D, Gilles A S Jr, Gizzi F, Glamuzina B, Glamuzina L, Goldsmit J,
  • Gollasch S, Goulletquer P, Grabowska J, Harmer R, Haubrock P J, He D, Hean J W, Herczeg G, Howland KL,
  • İlhan A, Interesova E, Jakubčinová K, Jelmert A, Johnsen S I, Kakareko T, Kanongdate K, Killi N, Kim J E,
  • Kırankaya Ş G, Kňazovická D, Kopecký O, Kostov V, KoutsikosN, Kozic S, Kuljanishvili T, Kumar B, Kumar L,
  • Kurita Y, Kurtul I, Lazzaro L, Lee L, Lehtiniemi M, Leonardi G, Leuven R.S E W, Li S, Lipinskaya T, Liu F, Lloyd L,
  • Lorenzoni M, Luna S A, Lyons T J, Magellan K, Malmstrøm M, Marchini A, Marr S M, Masson G, Masson L,
  • McKenzie, C H, Memedemin D, Mendoza R, Minchin D, Miossec L, Moghaddas S D, Moshobane M C,
  • Mumladze L, Naddafi R,
  • Najafi-Majd E, Năstase A, Năvodaru I, Neal J W, Nienhuis S, Nimtim M, Nolan E T,Occhipinti-Ambrogi A, Ojaveer H, Olenin S, Olsson
There are 85 citations in total.

Details

Primary Language English
Subjects Water Quality and Water Pollution
Journal Section Makaleler
Authors

Yusuf Koray Küçük This is me 0000-0001-8013-9747

Akasya Topçu 0000-0002-5229-4181

Esra Mine Ünal This is me 0000-0003-3324-4493

Emre Keskin 0000-0002-7279-313X

Ali Serhan Tarkan 0000-0001-8628-0514

İlknur Meriç Turgut 0000-0001-7404-5680

Project Number 18L0447013
Publication Date March 25, 2025
Submission Date August 19, 2024
Acceptance Date December 5, 2024
Published in Issue Year 2025 Volume: 31 Issue: 2

Cite

APA Küçük, Y. K., Topçu, A., Ünal, E. M., Keskin, E., et al. (2025). Biomonitoring of Non-Native Species Through eDNA Metabarcoding Method and Risk Screening for Ballast Water in Northwest Türkiye. Journal of Agricultural Sciences, 31(2), 470-495.
AMA Küçük YK, Topçu A, Ünal EM, Keskin E, Tarkan AS, Meriç Turgut İ. Biomonitoring of Non-Native Species Through eDNA Metabarcoding Method and Risk Screening for Ballast Water in Northwest Türkiye. J Agr Sci-Tarim Bili. March 2025;31(2):470-495.
Chicago Küçük, Yusuf Koray, Akasya Topçu, Esra Mine Ünal, Emre Keskin, Ali Serhan Tarkan, and İlknur Meriç Turgut. “Biomonitoring of Non-Native Species Through EDNA Metabarcoding Method and Risk Screening for Ballast Water in Northwest Türkiye”. Journal of Agricultural Sciences 31, no. 2 (March 2025): 470-95.
EndNote Küçük YK, Topçu A, Ünal EM, Keskin E, Tarkan AS, Meriç Turgut İ (March 1, 2025) Biomonitoring of Non-Native Species Through eDNA Metabarcoding Method and Risk Screening for Ballast Water in Northwest Türkiye. Journal of Agricultural Sciences 31 2 470–495.
IEEE Y. K. Küçük, A. Topçu, E. M. Ünal, E. Keskin, A. S. Tarkan, and İ. Meriç Turgut, “Biomonitoring of Non-Native Species Through eDNA Metabarcoding Method and Risk Screening for Ballast Water in Northwest Türkiye”, J Agr Sci-Tarim Bili, vol. 31, no. 2, pp. 470–495, 2025.
ISNAD Küçük, Yusuf Koray et al. “Biomonitoring of Non-Native Species Through EDNA Metabarcoding Method and Risk Screening for Ballast Water in Northwest Türkiye”. Journal of Agricultural Sciences 31/2 (March 2025), 470-495.
JAMA Küçük YK, Topçu A, Ünal EM, Keskin E, Tarkan AS, Meriç Turgut İ. Biomonitoring of Non-Native Species Through eDNA Metabarcoding Method and Risk Screening for Ballast Water in Northwest Türkiye. J Agr Sci-Tarim Bili. 2025;31:470–495.
MLA Küçük, Yusuf Koray et al. “Biomonitoring of Non-Native Species Through EDNA Metabarcoding Method and Risk Screening for Ballast Water in Northwest Türkiye”. Journal of Agricultural Sciences, vol. 31, no. 2, 2025, pp. 470-95.
Vancouver Küçük YK, Topçu A, Ünal EM, Keskin E, Tarkan AS, Meriç Turgut İ. Biomonitoring of Non-Native Species Through eDNA Metabarcoding Method and Risk Screening for Ballast Water in Northwest Türkiye. J Agr Sci-Tarim Bili. 2025;31(2):470-95.

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