https://doi.org/10.4081/jlimnol.2022.2136
The increasing spread of the European barbel in the Italian large lowland rivers is threatening the native species
Submitted: 28 March 2023
Accepted: 4 September 2023
Published: 21 September 2023
Accepted: 4 September 2023
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All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.
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Correction in: Erratum: The increasing spread of the European barbel in the Italian large lowland rivers is threatening the native species (https://doi.org/10.4081/jlimnol.2022.2164)
Freshwater ecosystems are heavily altered by human activities, with anthropic introductions of non-native species substantially contributing to their biotic degradation. The invasion by alien species can alter ecosystem balances with direct and indirect impacts across different levels of biotic organization. The number of invasive alien species is particularly high in Mediterranean fresh waters including rivers draining in the northern Adriatic basins. Here, the Padanian barbel Barbus plebejus endemic to the Padano-Venetian district, is threatened by the introduction of the European barbel Barbus barbus via competition and introgressive hybridization. In this study, we genetically characterised using the partial mitochondrial DNA Cytochrome b gene, barbels present in two main tributaries of the Po River, the lower Ticino and Oglio rivers where the two species are suspected to co-occur. Since the two river sections are highly regulated and present severe hydrological alterations caused by dams and other hydraulic structures, the aim of the study was to provide information on the barbel populations composition in these systems to foster the implementation of more suitable management plans aimed at the conservation of the native species. A total of 86 barbel have been analysed (50 in the Ticino River and 36 in the Oglio River) corresponding to 13 haplotypes of which 8 were phylogenetically attributed to B. barbus and five to B. plebejus. The high haplotypic diversity and the unimodal trend evidenced by the mismatch distribution analysis for B. barbus haplotypes support a potential demographic expansion. Altogether, these results highlighted that B. barbus is progressively expanding in northern Italy while posing a serious risk for the conservation of the native B. plebejus, stressing the need to actively focus ecosystem and fisheries management regulations to stop B. barbus from spreading further throughout northern Italy.
Aljanabi SM, Martinez I, 1997. Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic Acids Res 25:4692-4693.
DOI: https://doi.org/10.1093/nar/25.22.4692
Avise JC, 2000. Phylogeography: The history and formation of species. Harvard, Harvard University Press: 464 pp.
DOI: https://doi.org/10.2307/j.ctv1nzfgj7
Bernatchez L, 2001. The evolutionary history of brown trout (Salmo trutta L.) inferred from phylogeographic nested clade and mismatch analyses of mitochondrial DNA variation. Evolution 55:351-379.
DOI: https://doi.org/10.1111/j.0014-3820.2001.tb01300.x
Bianco P, 2003. Barbus plebejus Bonaparte 1939, p. 339-364. In: P. Banarescu and N. Bogutskaya (eds.), The freshwater fishes of Europe. Wiesbaden, AULA-Verlag.
Bianco PG, 1995. A revision of the Italian Barbus species (Cypriniforms: Cyprinidae). Ichthyol Explor Freshw 6:305-324.
Bianco PG, 2014. An update on the status of native and exotic freshwater fishes of Italy. J Appl Ichth 30:62-77.
DOI: https://doi.org/10.1111/jai.12291
Bock DG, Caseys C, Cousens RD, Hahn MA, Heredia SM, Hübner S, et al., 2015. What we still don't know about invasion genetics. Mol Ecol 24:2277-2297.
DOI: https://doi.org/10.1111/mec.13032
Briolay J, Galtier N, Brito RM, Bouvet Y, 1998. Molecular phylogeny of cyprinidae inferred fromcytochrome bDNA sequences. Mole Phyl Evol 9:100-108.
DOI: https://doi.org/10.1006/mpev.1997.0441
Britton JR, Pegg J, 2011. Ecology of European barbel Barbus barbus: implications for river fishery and conservation management. Rev Fisher Sci 19:321-330.
DOI: https://doi.org/10.1080/10641262.2011.599886
Buonerba L, Zaccara S, Delmastro GB, Lorenzoni M, Salzburger W, Gante HF, 2015. Intrinsic and extrinsic factors act at different spatial and temporal scales to shape population structure distribution and speciation in Italian Barbus (Osteichthyes: Cyprinidae). Mol Phylogenet Evol 89:115-129.
DOI: https://doi.org/10.1016/j.ympev.2015.03.024
Clement M, Posada D, Crandall K, 2000. TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657-1660.
DOI: https://doi.org/10.1046/j.1365-294x.2000.01020.x
Cucherousset J, Olden JD, 2011. Ecological impacts of non-native freshwater fishes. Fisheries 36:215-230.
DOI: https://doi.org/10.1080/03632415.2011.574578
Cucherousset J, Olden JD, 2020. Are domesticated freshwater fish under appreciated culprit of ecosystem change. Fish Fisher 21:1253-1258.
DOI: https://doi.org/10.1111/faf.12499
Darriba D, Taboada GL, Doallo R, Posada D, 2012. jModelTest 2: more models new heuristics and parallel computing. Nat. Meth. 9:772-772.
DOI: https://doi.org/10.1038/nmeth.2109
David P, Thébault E, Anneville O, Duyck PF, Chapuis E, Loeuille N, 2017. Impacts of invasive species on food webs: a review of empirical data, p. 1-60. In: DA Bohan, AJ Dumbrell and F Massol (eds.), Networks of invasion: a synthesis of concepts. Oxford, Academic Press.
DOI: https://doi.org/10.1016/bs.aecr.2016.10.001
De Santis V, Quadroni S, Britton RJ, Carosi A, Gutmann Roberts C, Lorenzoni M, et al., 2021. Biological and trophic consequences of genetic introgression between endemic and invasive Barbus fishes. Biol Inv 23:3351-3368.
DOI: https://doi.org/10.1007/s10530-021-02577-6
Didham RK, Tylianakis JM, Hutchison MA, Ewers RM, Gemmell NJ, 2005. Are invasive species the drivers of ecological change? Trends Ecol Evol 20:470-474.
DOI: https://doi.org/10.1016/j.tree.2005.07.006
Dlugosch KM, Parker IM, 2008. Founding events in species invasions: genetic variation adaptive evolution and the role of multiple introductions. Mol Ecol 17:431-449.
DOI: https://doi.org/10.1111/j.1365-294X.2007.03538.x
Estoup A, Guillemaud T, 2010. Reconstructing routes of invasion using genetic data: why how and so what? Mol Ecol 19:4113-4130.
DOI: https://doi.org/10.1111/j.1365-294X.2010.04773.x
European Union, 1992. Council Directive 92/43/EEC of 21 May 1992 on the conservation of natural habitats and of wild fauna and flora. Available from: https://eur-lex.europa.eu/legal-content/EN/TXT/?uri=celex%3A31992L0043
Freyhof J, Bergner L, Ford M, 2020. Threatened freshwater fishes of the Mediterranean basin biodiversity hotspot: distribution, extinction risk and the impact of hydropower. EuroNatur and RiverWatch: 348 pp.
Gante HF, Alves MJ, Dowling TE, 2008. Development of cytochrome b primers for mitotyping of barbels (Barbus spp.). Mol Ecol Res 8:786-789.
DOI: https://doi.org/10.1111/j.1755-0998.2007.02064.x
Geiger MF, Schreiner C, Delmastro GB, Herder F, 2016. Combining geometric morphometrics with molecular genetics to investigate a putative hybrid complex: a case study with barbels Barbus spp. (Teleostei: Cyprinidae). J Fish Biol 88:1038-1055.
DOI: https://doi.org/10.1111/jfb.12871
Grant W, Bowen B, 1998. Shallow population histories in deep evolutionary lineages of marine fishes: insights from sardines and anchovies and lessons for conservation. J Hered 89:415-426.
DOI: https://doi.org/10.1093/jhered/89.5.415
Hall TA, 1999. BioEdit: a user-friendly biological sequencealignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95-98.
Hänfling B, 2007. Understanding the establishment success of non-indigenous fishes: lessons from population genetics. J Fish Biol 71:115-135.
DOI: https://doi.org/10.1111/j.1095-8649.2007.01685.x
Hänfling B, Bolton P, Harley M, Carvalho G, 2005. A molecular approach to detect hybridisation between crucian carp (Carassius carassius) and non-indigenous carp species (Carassius spp. and Cyprinus carpio). Freshwater Biol 50:403-417.
DOI: https://doi.org/10.1111/j.1365-2427.2004.01330.x
Hardouin EA, Andreou D, Zhao Y, Chevret P, Fletcher DH, Britton JR, Gozlan RE, 2018. Reconciling the biogeography of an invader through recent and historic genetic patterns: the case of topmouth gudgeon Pseudorasbora parva. Biol Inv 20:2157-2171.
DOI: https://doi.org/10.1007/s10530-018-1693-4
Hayden B, Pulcini D, Kelly-Quinn M, O'Grady M, Caffrey J, McGrath, Mariani S, 2010. Hybridisation between two cyprinid fishes in a novel habitat: genetics morphology and life-history traits. BMC Evol Biol 10:169.
DOI: https://doi.org/10.1186/1471-2148-10-169
Hermoso V, Clavero M, 2011. Threatening processes and conservation management of endemic freshwater fish in the Mediterranean basin: a review. Mar Freshwr Res 62:244-254.
DOI: https://doi.org/10.1071/MF09300
Hobbs RJ, Huenneke LF, 1992. Disturbance diversity invasion: Implications for conservation. Conserv Biol 6:324-337.
DOI: https://doi.org/10.1046/j.1523-1739.1992.06030324.x
Jackson MC, Wasserman RJ, Grey J, Ricciardi A, Dick JTA, Alexander ME, 2017. Novel and disrupted trophic links following invasion in freshwater ecosystems, p. 55-97. In: DA Bohan, AJ Dumbrell and F Massol (eds.), Networks of invasion: a synthesis of concepts. Oxford, Academic Press.
DOI: https://doi.org/10.1016/bs.aecr.2016.10.006
Kotlík P, Berrebi P, 2001. Phylogeography of the barbel (Barbus barbus) assessed by mitochondrial DNA variation. Mol Ecol 9:2177-2185.
DOI: https://doi.org/10.1046/j.0962-1083.2001.01344.x
Kotlík P, Bogutskaya N, Ekmekci FG, 2004. Circum Black Sea phylogeography of Barbus freshwater fishes: divergence in the Pontic glacial refugium. Mol Ecol 13:87-95.
DOI: https://doi.org/10.1046/j.1365-294X.2003.02021.x
Kottelat M, Freyhof J, 2007. Handbook of European freshwater fishes. Cornol, Publications Kottelat: 646 pp.
Laini A, Bolpagni R, Cancellario T, Guareschi S, Racchetti E, Viaroli P, 2018. Testing the response of macroinvertebrate communities and biomonitoring indices under multiple stressors in a lowland regulated river. Ecol Indic 90:47-53.
DOI: https://doi.org/10.1016/j.ecolind.2018.02.051
Lanave C, Preparata G, Saccone C, Serio G, 1984. A new method for calculating evolutionary substitution rates. J Mol Evol 20:86-93.
DOI: https://doi.org/10.1007/BF02101990
Lawson Handley LJ, Estoup A, Evans DM, Thomas CE, Lombaert E, Facon B, et al., 2011. Ecological genetics of invasive alien species. BioControl 56:409-428.
DOI: https://doi.org/10.1007/s10526-011-9386-2
Librado P, Rozas J, 2009. DnaSP: A software for comprehensive analysis of DNA polymorphism data. Bioinform 25:1451-1452.
DOI: https://doi.org/10.1093/bioinformatics/btp187
Meraner A, Baric S, Pelster B, Dalla Via J, 2010. Microsatellite DNA data point to extensive but incomplete admixture in a marble and brown trout hybridisation zone. Conserv Genet 11:985-998.
DOI: https://doi.org/10.1007/s10592-009-9942-9
Meraner A, Venturi A, Ficetola GF, Rossi S, Candiotto A, Gandolfi A, 2013. Massive invasion of exotic Barbus barbus and introgressive hybridization with endemic Barbus plebejus in Northern Italy: where how and why? Mol Ecol 22:5295-5312.
DOI: https://doi.org/10.1111/mec.12470
Mollot G, Pantel JH, Romanuk TN, 2017. The effects of invasive species on the decline in species richness: a global meta-analysis. In: DA Bohan, AJ Dumbrell and F Massol (eds.), Networks of invasion: a synthesis of concepts, p. 61-83. Oxford, Academic Press.
DOI: https://doi.org/10.1016/bs.aecr.2016.10.002
Monroe JB, Baxter CV, Olden JD, Angermeier PL, 2009. Freshwaters in the public eye: understanding the role of images and media in aquatic. Fisheries 34:581-585.
DOI: https://doi.org/10.1577/1548-8446-34.12.581
Oziolor EM, Reid NM, Yair S, Lee KM, Guberman VerPloeg S, Bruns PC, et al., 2019. Adaptive introgression enables evolutionary rescue from extreme environmental pollution. Science 364:455-457.
DOI: https://doi.org/10.1126/science.aav4155
Pimentel D, Lach L, Zuniga R, Morrison D, 2000. Environmental and economic costs of nonindigenous species in the United States. BioSci J 50:53-65.
DOI: https://doi.org/10.1641/0006-3568(2000)050[0053:EAECON]2.3.CO;2
Puzzi CM, Trasforini S, Sartorelli M, Tamborini D, 2017. [La ricostituzione e monitoraggio del corridoio ecologico fluviale del fiume Ticino].[Article in Italian]. Proceedings Nat. Congr. AIIAD 2016, Popoli, Italy. Ital J Freshw Ichthyol 4.
Quadroni S, De Santis V, Carosi A, Vanetti I, Zaccara S, Lorenzoni M, 2023a. Past and present environmental factors differentially influence genetic and morphological traits of Italian barbels (Pisces: Cyprinidae). Water 15:325.
DOI: https://doi.org/10.3390/w15020325
Quadroni S, Servanzi L, Crosa G, 2023b. [Studio della disponibilità di habitat e delle sue variazioni in funzione delle scelte gestionali].[Report in Italian]. Report 5.3 progetto INTERREG Italia-Svizzera “ParchiVerbanoTicino”: 29 pp.
Racchetti E, Salmaso F, Pinardi M, Quadroni S, Soana E, Sacchi E, et al., 2019. Is flood irrigation a potential driver of river-groundwater interactions and diffuse nitrate pollution in agricultural watersheds? Water 11:2304.
DOI: https://doi.org/10.3390/w11112304
Rambaut A, 2016. FigTree. Available from: http://tree.bio.ed.ac.uk/software/figtree/
Ronquist F, Teslenko M, Van der Mark P, Ayres DL, Aaron Darling A, et al., 2012. MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Bio 61:539-542.
DOI: https://doi.org/10.1093/sysbio/sys029
Salmaso F, Crosa G, Espa P, Quadroni S, 2021. Climate change and water exploitation as co-impact sources on river benthic macroinvertebrates. Water 13:2778.
DOI: https://doi.org/10.3390/w13192778
Salmaso F, Quadroni S, Gentili G, Crosa G, 2016. Thermal regime of a highly regulated Italian river (Ticino River) and implications for aquatic communities. J Limnol 76:1437
DOI: https://doi.org/10.4081/jlimnol.2016.1437
Scribner KT, Page KS, Bartron ML, 2000. Hybridization in freshwater fishes: a review of case studies and cytonuclear methods of biological inference. Rev Fish Biol Fish 10:293-323.
DOI: https://doi.org/10.1023/A:1016642723238
Sheath DJ, Williams CF, Reading AJ, Britton JR, 2015. Parasites of non-native freshwater fishes introduced into England and Wales suggest enemy release and parasite acquisition. Biol Inv 17:2235-2246.
DOI: https://doi.org/10.1007/s10530-015-0857-8
Simberloff D, Martin JL, Genovesi P, Maris V, Wardle DA, Aronson J, et al., 2013. Impacts of biological invasions: what’s what and the way forward. Trends Ecol Evol 28:58-66.
DOI: https://doi.org/10.1016/j.tree.2012.07.013
Smith KG, Darwall WRT, 2006. The status and distribution of freshwater fish endemic to the Mediterranean Basin. Gland, IUCN: 44 pp.
DOI: https://doi.org/10.2305/IUCN.CH.2006.MRA.1.en
Strayer DL, 2006. Challenges for freshwater invertebrate conservation. North Am Benthol Soc 25:271-287.
DOI: https://doi.org/10.1899/0887-3593(2006)25[271:CFFIC]2.0.CO;2
Strayer DL, Dudgeon D, 2010. Freshwater biodiversity conservation: recent progress and future challenges. J North Am Benthol Soc 29:344-358
DOI: https://doi.org/10.1899/08-171.1
Swofford DL, 2003. PAUP*: phylogenetic analysis using parsimony version 4.0 b10.
Tsigenopoulos CS, Karakousis Y, Berrebi P, 1999. The North Mediterranean Barbus lineage: phylogenetic hypotheses and taxonomic implications based on allozyme data. J Fish Biol 54:267-286.
DOI: https://doi.org/10.1111/j.1095-8649.1999.tb00829.x
Tsigenopoulos CS, Kotlik P, Berrebi P, 2002. Biogeography and pattern of gene flow among Barbus species (Teleostei: Cyprinidae) inhabiting the Italian Peninsula and neighbouring Adriatic drainages as revealed by allozyme and mitochondrial sequence data. Biol J Linn 75:83-99.
DOI: https://doi.org/10.1046/j.1095-8312.2002.00007.x
Zaccara S, Antognazza CM, Buonerba L, Britton RJ, Crosa G, 2014. Human-mediated contact zone between endemic and invasive Barbus species (Osteichthyes: Cyprinidae) in a regulated lowland river: genetic inferences and conservation implications. Ital J Zool 81:571-583.
DOI: https://doi.org/10.1080/11250003.2014.944225
Zaccara S, Quadroni S, De Santis V, Vanetti I, Carosi A, Britton R, Lorenzoni M, 2019a. Genetic and morphological analyses reveal a complex biogeographic pattern in the endemic barbel populations of the southern Italian peninsula. Ecol Evol 9:10185-10197.
DOI: https://doi.org/10.1002/ece3.5521
Zaccara S, Quadroni S, Vanetti I, Carosi A, La Porta G, Crosa G, et al., 2019b. Morphologic and genetic variability in the Barbus fishes (Teleostei Cyprinidae) of Central Italy. Zool Scr 48:289-301.
DOI: https://doi.org/10.1111/zsc.12341
Zaccara S, Quadroni S, De Santis V, Vanetti I, Carosi A, Crosa G, et al., 2021. Genetic and phenotypic displacement of an endemic Barbus complex by invasive European barbel Barbus barbus in central Italy. Biol Inv 23:521-535.
DOI: https://doi.org/10.1007/s10530-020-02379-2
Zerunian S, 2003.[Piano d'azione generale per la conservazione dei Pesci d'acqua dolce italiani].[Report in Italian]. Quad. Cons. Natura 17. Min. Ambiente - Ist. Naz. Fauna Selvatica.
Zwickl DJ, 2006. Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. PhD Thesis, The University ofTexas at Austin. Available from: https://repositories.lib.utexas.edu/handle/2152/2666
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Angela Boggero, National Research Council, Water Research Institute (CNR-IRSA), Verbania Pallanza, ItalySupporting Agencies
INTERREG Italian-Swiss project “ParchiVerbanoTicino”How to Cite
Antognazza, Caterina Maria, Silvia Quadroni, Isabella Vanetti, Vanessa De Santis, Giuseppe Crosa, and Serena Zaccara. 2023. “The Increasing Spread of the European Barbel in the Italian Large Lowland Rivers Is Threatening the Native Species”. Journal of Limnology 81 (s2). https://doi.org/10.4081/jlimnol.2022.2136.
Copyright (c) 2023 The Author(s)
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