First application of environmental eDNA for detecting the presence of the European eel [Anguilla anguilla, (Linnaeus, 1758)] in the Adriatic, as a basis for conservation remarks
Published:
Jun 29, 2023
Keywords:
eel Anguilla Environmental monitoring Mediterranean region environmental dna conservation genetics
Abstract
Anguilla anguilla, the European eel, is an important species for aquaculture and fisheries. Its population has dropped dramatically in recent decades, reaching an all-time low. As a result, it has been listed as critically endangered on the IUCN Red List of Endangered Species since 2007. Therefore, constant population monitoring is essential to ensure the survival of this iconic species. Glass eel recruitment is declining worldwide, including the populations in the Mediterranean region. Despite the negative impact of man-made activities in Mediterranean coastal waters over the past few decades, data on spawning biomass escaping from the Mediterranean highlights the region’s importance for the global eel supply. Eel research and monitoring is done using conventional techniques, which have certain drawbacks. Therefore, the use of molecular-based detection as a credible choice for monitoring species in aquatic ecosystems was recently shown to be an effective management plan alternative. We present the first use of environmental DNA for monitoring eel populations in the Adriatic Sea and in the complex Dinaric karst freshwater ecosystem. The method has been demonstrated to be accurate and useful for detecting the presence of A. anguilla eDNA and identifying conservation areas. This is also the first study investigating the range and presence of the European eel in the Adriatic and in the Mediterranean Sea, as well as in underground karst systems, springs, and in the karst poljes of the Eastern Adriatic coast.
Article Details
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VUCIĆ, M., JELIĆ, D., KLOBUČAR, G., PAVLINEC, ŽELJKO, GHRIB, F. L., JARAK, M., BAUDRY, T., & GALOV, A. (2023). First application of environmental eDNA for detecting the presence of the European eel [Anguilla anguilla, (Linnaeus, 1758)] in the Adriatic, as a basis for conservation remarks. Mediterranean Marine Science, 24(2), 364–376. https://doi.org/10.12681/mms.31829
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References
Aalto, E., Capoccioni, F., Terradez Mas, J., Schiavina, M., et al., 2016. Quantifying 60 years of declining European eel (Anguilla anguilla L., 1758) fishery yields in Mediterranean coastal lagoons. ICES Journal of Marine Science, 73, 101-110.
Agersnap, S., Larsen, W.B., Knudsen, S.W., Strand, D., Thomsen, P.F. et al., 2017. Monitoring of noble, signal and narrow- clawed crayfish using environmental DNA from freshwater samples. PloS One, 12(6), e0179261.
Amilhat, E., Fazio, G., Simon, G., Manetti, M., Paris, S., et al., 2014. Silver European eels health in Mediterranean habitats. Ecology of Freshwater Fish, 23, 49-64.
Anonymous, 2007. Council Regulation (EC) No 1100/2007 of 18 September 2007 establishing measures for the recovery of the stock of European eel. Official Journal of the European Union L 248/17. https://eur-lex.europa.eu/legal-content/ EN/TXT/?uri=celex%3A32007R1100 (Accessed 8 December 2021).
Badamasi, I., Odong, R., Masembe, C., 2020. Threats posed by xenoestrogenic chemicals to the aquatic ecosystem, fish reproduction and humans: a review. African Journal of Aquatic Science, 45 (3), 243-258.
Barry, J., Newton, M., Dodd, J. A., Lucas, M.C., Boylan, P. et al., 2016. Freshwater and coastal migration patterns in the silver‐stage eel Anguilla anguilla. Journal of Fish Biology, 88, 676-689.
Baudry, T., Mauvisseau, Q., Goût, J.P., Arqué, A., Delaunay, C. et al., 2021. Mapping a super-invader in a biodiversity hotspot, an eDNA-based success story. Ecological Indicators, 126, 107637.
Bedwell, M.E., Goldberg, C.S., 2020. Spatial and temporal patterns of environmental DNA detection to inform sampling protocols in lentic and lotic systems. Ecology and Evolution, 10, 1602-1612.
Belpaire, C., Hodson, P., Pierron, F., Freese, M., 2019. Impact of chemical pollution on Atlantic eels: Facts, research needs, and implications for management. Current Opinion in Environmental Science & Health, 11, 26-36.
Bevacqua, D., Melià, P., Crivelli, A. J., Gatto, M., De Leo, G.A., 2009. Assessing management plans for the recovery of the European eel: a need for multi-objective analyses. American Fisheries Society Symposium, 69, 637-647.
Bonacci, O., 1999. Water circulation in karst and determination of catchment areas: example of the River Zrmanja. Hydrological Sciences Journal, 44, 373-386.
Bonacci, O., 2015. Surface waters and groundwater in karst. p. 149-169. In: Karst aquifers-characterization and engineering. Stevanović, Z. (Ed.). Springer International Publishing, Switzerland.
Bonacci, O., Andrić, I., 2008. Karst rivers hydrology: case of the Lika and Gacka (Croatia). Acta carsologica, 37 (2-3), 185-196.
Bonacci, O., Željković, I., Galić, A., 2013. Karst rivers’ particularity: an example from Dinaric karst (Croatia/Bosnia and Herzegovina). Environmental earth sciences, 70, 963-974.
Bustin, S.A., Vandesompele, J., Pfaffl, M., 2009. Standardization of qPCR and RT-qPCR. Gen Eng Biotechnol News 2009b, 29.
Burgoa Cardás, J.B., Deconinck, D., Márquez, I., Torre, P.P., Garcia-Vazquez, E. et al., 2020. New eDNA based tool applied to the specific detection and monitoring of the endangered European eel. Biological Conservation, 250, 108750.
Castadelli, G., Aschonitis, V., Lanzoni, M., Gelli, F., Rossi, R. et al., 2014. An update of the length-weight and length-age relationships of the European eel (Anguilla anguilla, Linnaeus 1758) in the Comacchio Lagoon, northeast Adriatic Sea, Italy. Journal of Applied Ichthyology, 30 (3), 558-559.
Cataudella, S., Crosetti, D., Ciccotti, E., Massa, F., 2014. Sustainable management in Mediterranean coastal lagoons: Interactions among capture fisheries, aquaculture and environment. p. 7-49. In: Mediterranean coastal lagoons: sustainable management and interactions among aquaculture, capture fisheries and environment. S. Cataudella, D. Crosetti, F. Massa (Eds.). General Fisheries Commission for the Mediterranean. Studies and reviews, N. 95. FAO, Rome.
Capoccioni, F., Leone, C., Belpaire, C., Malarvannan, G., Poma, G. et al., 2020. Quality assessment of escaping silver eel (Anguilla anguilla L.) to support management and conservation strategies in Mediterranean coastal lagoons. Environmental Monitoring and Assessment, 192, 1-22.
Core Team R Development, 2019. R: a language and environment for statistical computing. Cresci, A., 2020. A comprehensive hypothesis on the migration of European glass eels (Anguilla anguilla). Biological Reviews, 95, 1273-1286.
Ćurčić, V., 1916. Narodno ribarstvo u Bosni i Hercegovini: II. Hercegovina. (in Croatian) [Folk fishing in Bosnia and Herzegovina: II. Herzegovina]. Zemaljska Štamparija, Sarajevo, Bosnia and Hercegovina, 208 pp.
de Graaf, M., van der Heul, J.W., van Willigen, J. A., Leijzer, T.B., 2010. The use of light traps in monitoring abundance of glass eel. No. C167/10, IMARES, 16 pp.
Deiner K., Altermatt F., 2014. Transport Distance of Invertebrate Environmental DNA in a Natural River. PLoS ONE, 9, 2, e88786.
Dekker, W., 2000. The fractal geometry of the European eel stock. ICES Journal of Marine Science, 57, 109-121.
Dekker, W., 2003. On the distribution of the European eel and its fisheries. Canadian Journal of Fisheries and Aquatic Sciences, 60, 787-799.
Dekker, W., 2016. Management of the eel is slipping through our hands! Distribute control and orchestrate national protection. ICES Journal of Marine Science, 73, 2442-2452.
Dekker, W., Beaulaton, L., 2016. Climbing back up what slippery slope? Dynamics of the European eel stock ad its management in historical perspective. ICES Journal of Marine Science, 73, 5-13.
Dezfuli, B.S., Giari, L., Castaldelli, G., Lanzoni, M., Rossi, R. et al., 2014. Temporal and spatial changes in the composition and structure of helminth component communities in European eels Anguilla anguilla in an Adriatic coastal lagoon and some freshwaters in Italy. Parasitology Research, 113, 113-120.
Di Cave, D., Berrilli, F., De Liberato, C., Orecchia, P., Kennedy, C.R., 2001. Helminth communities in eels Anguilla anguilla from Adriatic coastal lagoons in Italy. Journal of Helminthology, 75, 7-13.
Dojmi, L., 1939. Podzemne migracije jegulja. (in Croatian) [Underground migrations of eel]. Priroda: popularni časopis Hrvatskog prirodoslovnog društva, 9, 263-269.
Dubreuil, T., Baudry, T., Mauvisseau, Q., Arqué, A.. Courty, C. et al., 2022. The development of early monitoring tools to detect aquatic invasive species: eDNA assay development and the case of the armored catfish Hypostomus robinii. Environmental DNA, 1-14.
Dulčić, J., Glamuzina, B., 2006. Length–weight relationships for selected fish species from three eastern Adriatic estuarine systems (Croatia). Journal of Applied Ichthyology, 22 (4), 254-256.
Dedibegović, J., Larssen, T., Skrbo, A., Marjanović, A., Sober, M., 2012. Contents of cadmium, copper, mercury and lead in fish from the Neretva river (Bosnia and Herzegovina) determined by inductively coupled plasma mass spectrometry (ICP-MS). Food Chemistry, 131, 469-476.
Ficetola, G. F., Miaud, C., Pompanon, F., Taberlet, P., 2008. Species detection using environmental DNA from water samples. Biology letters, 4 (4), 423-425.
Forsström, T., Vasemägi, A., 2016. Can environmental DNA (eDNA) be used for detection and monitoring of introduced crab species in the Baltic Sea? Marine Pollution Bulletin, 109, 350-355.
Froese, R., Pauly D., 2021. FishBase. World Wide Web electronic publication. www.fishbase.org. (Accessed 25 January 2022).
Glamuzina, L., Dobroslavić, T., 2020. Summer fish migrations in the River Neretva (South-Eastern Adriatic coast, Croatia) as a consequence of salinization. NAŠE MORE: znanstveni časopis za more i pomorstvo, 67, 103-116.
Has-Schön, E., Bogut, I., Rajković, V., Bogut, S., Čačić, M. et al., 2008. Heavy metal distribution in tissues of six fish species included in human diet, inhabiting freshwaters of the Nature Park “Hutovo Blato” (Bosnia and Herzegovina). Archives of Environmental Contamination and Toxicology, 54, 75-83.
Hänfling, B., Handley, L.L., Read, D.S., Hahn, C., Li, J. et al., 2016. Environmental DNA metabarcoding of lake fish communities reflects long-term data from established survey methods. Molecular Ecology 25, 3101-3119.
Harrison, A.J., Walker, A.M., Pinder, A.C., Briand, C., Aprahamian, M.W., 2014. A review of glass eel migratory behaviour, sampling techniques and abundance estimates in estuaries: implications for assessing recruitment, local production and exploitation. Reviews in Fish Biology and Fisheries, 24, 967-983.
Hinlo, R., Furlan, E., Suitor, L., Gleeson, D., 2017. Environmental DNA monitoring and management of invasive fish: Comparison of eDNA and fyke netting. Management of Biological Invasions, 8, 89-100.
Jacoby, D.M.P., Casselman, J.M., Crook, V., DeLucia, M.-B., Ahn, H. et al., 2015. Synergistic patterns of threat and the challenges facing global anguillid eel conservation. Global Ecology and Conservation, 4, 321-333.
Kanjuh, T., Mrdak, D., Piria, M., Tomljanović, T., Joksimović, A. et al., 2018. Relationships of otolith dimension with body length of European eel Anguilla anguilla (Linnaeus, 1758) from Adriatic catchment of Montenegro. Acta Adriatica: International journal of Marine Sciences, 59, 91-96.
Keller, T., 1995. Food of cormorants Phalacrocorax carbo sinensis wintering in Bavaria, southern Germany. Ardea, 83, 185-192.
Klymus, K.E., Merkes, C.M., Allison, M.J., Goldberg, C.S., Helbing, C.C. et al., 2019. Reporting the limits of detection and quantification for environmental DNA assays. Environmental DNA, 1-12.
Lawson Handley, L., Read, D.S., Winfield, I.J., Kimbell, H., Johnson, H. et al., 2019. Temporal and spatial variation in distribution of fish environmental DNA in England’s largest lake. Environmental DNA, 1, 26-39.
Lieschke, J.A., Dean, J.C., Pickworth, A., 2019. Extending the effectiveness of electrofishing to estuarine habitats: Laboratory and field assessments. Transactions of the American Fisheries Society, 148, 584-591.
Lyon, J.P., Bird, T., Nicol, S., Kearns, J., O’Mahony, J. et al., 2014. Efficiency of electrofishing in turbid lowland rivers: implications for measuring temporal change in fish populations. Canadian Journal of Fisheries and Aquatic Sciences, 71, 878-886.
McColl‐Gausden, E. F., Weeks, A. R., Coleman, R. A., Robinson, K.L., Song, S. et al., 2021. Multispecies models reveal that eDNA metabarcoding is more sensitive than backpack electrofishing for conducting fish surveys in freshwater streams. Molecular Ecology, 30, 3111-3126.
Miller, M.J., Feunteun, E., Tsukamoto, K., 2016. Did a “perfect storm” of oceanic changes and continental anthropogenic impacts cause northern hemisphere anguillid recruitment reductions? ICES Journal of Marine Science, 73, 43-56.
Milošević, D., Bigović, M., Mrdak, D., Milašević, I., Piria, M., 2021. Otolith morphology and microchemistry fingerprints of European eel, Anguilla anguilla (Linnaeus, 1758) stocks from the Adriatic Basin in Croatia and Montenegro. Science of The Total Environment, 786, 147478.
Moriarty, C., 2003. The yellow eel. p. 89-105. In: Eel biology. Aida, K., Tsukamoto, K., Yamauchi, K. (Eds). Springer, Tokyo, Japan.
Mrakovčić, M., Brigić, A., Buj, I., Ćaleta, M., Mustafić, P. et al., 2006. Red book of freshwater fishes of Croatia. (in Croatian with English abstract). Ministarstvo kulture, Državni zavod za zaštitu prirode, Zagreb, 253 pp.
Nielsen, T., Prouzet, P., 2008. Capture-based aquaculture of the wild European eel (Anguilla anguilla). FAO Fisheries Technical Paper, 508, 141-149.
Palandačić, A., Bonacci, O., Snoj, A., 2012. Molecular data as a possible tool for tracing groundwater flow in karst environment: example of Delminichthys adspersus in Dinaric karst system. Ecohydrology, 5(6), 791-797.
Parolini, M., Binelli, A., Matozzo, V., Marin, M.G., 2010. Persistent organic pollutants in sediments from the Lagoon of Venice - a possible hazard for sediment-dwelling organisms. Journal of Soils and Sediments, 10, 1362-1379.
Piggott, M.P., 2016. Evaluating the effects of laboratory protocols on eDNA detection probability for an endangered freshwater fish. Ecology and Evolution, 6, 2739-2750.
Pinto, M.I., Burrows, H.D., Sontag, G., Vale, C., Noronha, J.P., 2016. Priority pesticides in sediments of European coastal lagoons: a review. Marine Pollution Bulletin, 112, 6-16.
Pike, C., Crook, V. Gollock, M., 2020. Anguilla anguilla. The IUCN Red List of Threatened Species 2020, e. T60344A152845178.
Piria, M., Šprem, N., Tomljanović, T., Slišković, M., Jelić Mrčelić, G. et al., 2014. Length weight relationships of the European eel Anguilla anguilla (Linnaeus, 1758) from six karst catchments of the Adriatic basin, Croatia. Croatian Journal of Fisheries: Ribarstvo, 72, 32-35.
Pottier, G., Beaumont, W.R., Marchand, F., Le Bail, P.Y., Azam, D. et al., 2020. Electrofishing in streams of low water conductivity but high biodiversity value: Challenges, limits and perspectives. Fisheries Management and Ecology, 27, 52-63.
QGIS Development Team, 2022. QGIS Geographic Information System. Open Source Geospatial Foundation Project. http://qgis.osgeo.org (Accessed 8 December 2021).
Riascos-Flores, L., Bruneel, S., Van der Heyden, C., Deknock, A., Van Echelpoel, W. et al., 2021. Polluted paradise: Occurrence of pesticide residues within the urban coastal zones of Santa Cruz and Isabela (Galapagos, Ecuador). Science of the Total Environment, 763, 142956.
Ridanović, L., Ridanović, S., Jurica, D., Spasojević, P., Bijedić, D., 2010. Evaluation of water temperature and dissolved oxygen regimes in River Neretva. BALWOIS Ohrid, 2010, 1-8.
Robinson, C.V., Uren Webster, T.M., Cable, J., James, J., Consuegra, S., 2018. Simultaneous detection of invasive signal crayfish, endangered white-clawed crayfish and the crayfish plague pathogen using environmental DNA. Biological Conservation, 222, 241-252.
Stein, F.M., Wong, J.C., Sheng, V., Law, C.S., Schröder, B. et al., 2016. First genetic evidence of illegal trade in endangered European eel (Anguilla anguilla) from Europe to Asia. Conservation Genetics Resources, 8, 533-537.
Storelli, M.M., Barone, G., Garofalo, R., Marcotrigiano, G.O., 2007. Metals and organochlorine compounds in eel (Anguilla anguilla) from the Lesina lagoon, Adriatic Sea (Italy). Food Chemistry, 100, 1337-1341.
Thalinger, B., Deiner, K., Harper, L.R., Rees, H.C., Blackman, R.C. et al. 2021. A validation scale to determine the readiness of environmental DNA assays for routine species monitoring. Environmental DNA, 3, 823-836.
Thomsen, P.F., Willerslev, E., 2015. Environmental DNA - An emerging tool in conservation for monitoring past and present biodiversity. Biological Conservation, 183, 4-18.
Vörös, J., Márton, O., Schmidt, B.R., Gál, J.T., Jelić, D., 2017. Surveying Europe’s only cave-dwelling chordate species (Proteus anguinus) using environmental DNA. PloS one, 12, e0170945.
Violi, L., Falcone, G., De Luca, A.I., Chies, L., 2015. Sustainability European Eel Population: A Statistical Survey on Production, Conservation Status and Market Trends. Calitatea, 16 (148), 83.
Wang, S., Yan, Z., Hänfling, B., Zheng, X., Wang, P. et al., 2021. Methodology of fish eDNA and its applications in ecology and environment. Science of the Total Environment, 755.
Weldon, L., O’Leary, C., Steer, M., Newton, L. Macdonald, H. et al., 2020. A comparison of European eel Anguilla anguilla eDNA concentrations to fyke net catches in five Irish lakes. Environmental DNA, 2, 587-600.
