Register      Login
Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

Inter-population variability in growth and reproduction of invasive bleak Alburnus alburnus (Linnaeus, 1758) across the Iberian Peninsula

D. Latorre A , G. Masó A L , A. Hinckley B , D. Verdiell-Cubedo A , A. S. Tarkan C D , A. Vila-Gispert A , G. H. Copp E F , J. Cucherousset G , E. da Silva H , C. Fernández-Delgado I , E. García-Berthou A , R. Miranda J , F. J. Oliva-Paterna K , A. Ruiz-Navarro K , J. M. Serrano B and D. Almeida A M
+ Author Affiliations
- Author Affiliations

A GRECO, Institute of Aquatic Ecology, University of Girona, C/ M. Aurèlia Capmany 69, E-17003 Girona, Spain.

B Department of Ecology, Complutense University of Madrid, C/ José Antonio Novais 12, E-28040 Madrid, Spain.

C Faculty of Fisheries, Muğla Sıtkı Koçman University, TR-48000 Mentese, Muğla, Turkey.

D Department of Ecology and Vertebrate Zoology, Faculty of Biology and Environmental Protection, 12/16 Banacha Street, PL-90-237, University of Łódź, Poland.

E Salmon & Freshwater Team, Cefas, Pakefield Road, Lowestoft, Suffolk, NR33 OHT, UK.

F Department of Life & Environmental Sciences, Bournemouth University, Poole, BH12 5BB, UK.

G CNRS, Université Toulouse III Paul Sabatier, ENFA, UMR 5174 EDB (Laboratoire Évolution & Diversité Biologique), 118 Rue Narbonne, F-31062 Toulouse, France.

H Department of Anatomy, Cell Biology & Zoology, University of Extremadura, Avenida de Elvas, s/n, E-06006 Badajoz, Spain.

I Department of Zoology, University of Córdoba, Campus de Rabanales, Edificio Charles Darwin, E-14014 Córdoba, Spain.

J Department of Environmental Biology, School of Sciences, University of Navarra, C/ Irunlarrea 1, E-31080 Pamplona, Spain.

K Department of Zoology and Physical Anthropology, University of Murcia, Avenida Teniente Flomesta 5, E-30100 Murcia, Spain.

L Present address: Department of Biodiversity and Ecological Restoration, Instituto Pirenaico de Ecología (IPE-CSIC), Avenida Nuestra Señora de la Victoria 16, E-22700 Jaca, Spain.

M Corresponding author. Present address: Departamento de Ciencias Médicas Básicas, Facultad de Medicina, Universidad San Pablo-CEU, CEU Universities, Campus de Montepríncipe, E-28925 Alcorcón, Madrid, Spain. Email: david.almeida@udg.edu

Marine and Freshwater Research 69(8) 1326-1332 https://doi.org/10.1071/MF17092
Submitted: 6 April 2017  Accepted: 5 December 2017   Published: 26 March 2018

Abstract

The native European freshwater cyprinid fish, common bleak Alburnus alburnus (Linnaeus, 1758), is an invasive non-native fish in the Iberian Peninsula, where it threatens the valuable endemic fish fauna. Despite the bleak’s invasive status, there is a dearth of studies on the biological traits of non-native populations in Europe’s Mediterranean region, and the present study aimed to compare bleak growth and reproductive traits across the principal rivers of Iberia with those from a native ‘reference’ bleak population in France. Non-native bleak from the River Tagus had the highest back-calculated total lengths (TLs), growth rate and body condition, but the lowest reproductive investment and smallest egg size of all studied populations. Whereas, these latter two traits were the highest in the River Ebro, where fecundity was the lowest for all Iberian rivers. The youngest age and the smallest TL at maturity were observed in the River Ebro. The River Segura had the lowest back-calculated TLs and growth rate, the highest fecundity and proportion of females, and the oldest age at maturity. Population traits of bleak in the River Saône (the native ‘reference’ population) were generally different from those in Iberian rivers, except for the River Ebro. This wide inter-population variability contributes to the species’ successful establishment in novel habitats.

Additional keywords: back-calculation, body condition, freshwater fish, non-native species, sex ratio.


References

Agrawal, A. A. (2001). Phenotypic plasticity in the interactions and evolution of species. Science 294, 321–326.
Phenotypic plasticity in the interactions and evolution of species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnsFGqsr4%3D&md5=9ad9a515376680bf60696aba0db08fa8CAS |

Alcaraz, C., and García-Berthou, E. (2007). Food of an endangered cyprinodont (Aphanius iberus): ontogenetic diet shift and prey electivity. Environmental Biology of Fishes 78, 193–207.
Food of an endangered cyprinodont (Aphanius iberus): ontogenetic diet shift and prey electivity.Crossref | GoogleScholarGoogle Scholar |

Almeida, D., and Grossman, G. D. (2012). Utility of direct observational methods for assessing competitive interactions between non-native and native freshwater fishes. Fisheries Management and Ecology 19, 157–166.
Utility of direct observational methods for assessing competitive interactions between non-native and native freshwater fishes.Crossref | GoogleScholarGoogle Scholar |

Almeida, D., Ribeiro, F., Leunda, P. A., Vilizzi, L., and Copp, G. H. (2013). Effectiveness of an invasiveness screening tool for non-native freshwater fishes (FISK) to perform risk identification assessments in the Iberian Peninsula. Risk Analysis 33, 1404–1413.
Effectiveness of an invasiveness screening tool for non-native freshwater fishes (FISK) to perform risk identification assessments in the Iberian Peninsula.Crossref | GoogleScholarGoogle Scholar |

Almeida, D., Stefanoudis, P. V., Fletcher, D. H., Rangel, C., and da Silva, E. (2014). Population traits of invasive bleak Alburnus alburnus between different habitats in Iberian fresh waters. Limnologica 46, 70–76.
Population traits of invasive bleak Alburnus alburnus between different habitats in Iberian fresh waters.Crossref | GoogleScholarGoogle Scholar |

Andreu-Soler, A., Oliva-Paterna, F. J., Verdiell, D., and Torralva, M. (2004). Primeras citas de Alburnus alburnus (Linnaeus, 1758) y Tinca tinca (Linnaeus, 1758) (Actinopterygii, Cyprinidae) en la cuenca del río Segura (Murcia, sudeste de la Península Ibérica). Anales de Biología 26, 222–224.

Bøhn, T., Sandlund, O. T., Amundsen, P. A., and Primicerio, R. (2004). Rapidly changing life history during invasion. Oikos 106, 138–150.
Rapidly changing life history during invasion.Crossref | GoogleScholarGoogle Scholar |

Bonisławska, M., Formicki, K., Korzelecka-Orkisz, A., and Winnicki, A. (2001). Fish egg size variability: biological significance. Electronic Journal of Polish Agricultural Universities – Fisheries 4, 2.

Clavero, M., and García-Berthou, E. (2006). Homogenization dynamics and introduction routes of invasive freshwater fish in the Iberian Peninsula. Ecological Applications 16, 2313–2324.
Homogenization dynamics and introduction routes of invasive freshwater fish in the Iberian Peninsula.Crossref | GoogleScholarGoogle Scholar |

Copp, G. H., and Fox, M. G. (2007). Growth and life history traits of introduced pumpkinseed (Lepomis gibbosus) in Europe, and the relevance to invasiveness potential. In ‘Freshwater Bioinvaders: Profiles, Distribution and Threats’. (Ed. F. Gherardi.) pp. 289–306. (Springer: Berlin, Germany.) 10.1007/978-1-4020-6029-8_15

Copp, G. H., Tarkan, A. S., Masson, G., Godard, M. J., Koščo, J., Novomeská, A., Miranda, R., Cucherousset, J., Pedicillo, G., and Blackwell, B. (2016). A review of growth and life-history traits of native and non-native European populations of black bullhead Ameiurus melas. Reviews in Fish Biology and Fisheries 26, 441–469.
A review of growth and life-history traits of native and non-native European populations of black bullhead Ameiurus melas.Crossref | GoogleScholarGoogle Scholar |

Cucherousset, J., Copp, G. H., Fox, M. G., Sterud, E., van Kleef, H. H., Verreycken, H., and Záhorská, E. (2009). Life-history traits and potential invasiveness of introduced pumpkinseed Lepomis gibbosus populations in northwestern Europe. Biological Invasions 11, 2171–2180.
Life-history traits and potential invasiveness of introduced pumpkinseed Lepomis gibbosus populations in northwestern Europe.Crossref | GoogleScholarGoogle Scholar |

European Commission (2014). Commission Directive 2014/101/EU of 30 October 2014 amending Directive 2000/60/EC of the European Parliament and of the Council establishing a framework for Community action in the field of water policy. Official Journal of the European Union – Legislation 311, 32–35.

Fox, M. G., and Crivelli, A. J. (2001). Life history traits of pumpkinseed (Lepomis gibbosus) populations introduced into warm thermal environments. Archiv für Hydrobiologie 150, 561–580.
Life history traits of pumpkinseed (Lepomis gibbosus) populations introduced into warm thermal environments.Crossref | GoogleScholarGoogle Scholar |

Fox, M. G., Vila-Gispert, A., and Copp, G. H. (2007). Life history traits of introduced Iberian pumpkinseed (Lepomis gibbosus) relative to native populations: can differences explain colonization success? Journal of Fish Biology 71, 56–69.
Life history traits of introduced Iberian pumpkinseed (Lepomis gibbosus) relative to native populations: can differences explain colonization success?Crossref | GoogleScholarGoogle Scholar |

Francis, R. I. C. C. (1990). Back-calculation of fish length: a critical review. Journal of Fish Biology 36, 883–902.
Back-calculation of fish length: a critical review.Crossref | GoogleScholarGoogle Scholar |

Froese, R., and Binohlan, C. (2003). Simple methods to obtain preliminary growth estimates for fishes. Journal of Applied Ichthyology 19, 376–379.
Simple methods to obtain preliminary growth estimates for fishes.Crossref | GoogleScholarGoogle Scholar |

Hickley, P., and Dexter, F. K. (1979). A comparative index for quantifying growth in length of fish. Aquaculture Research 10, 147–151.
A comparative index for quantifying growth in length of fish.Crossref | GoogleScholarGoogle Scholar |

Johnson, P. C. D., Barry, S. J. E., Ferguson, H. M., and Müller, P. (2015). Power analysis for generalized linear mixed models in ecology and evolution. Methods in Ecology and Evolution 6, 133–142.
Power analysis for generalized linear mixed models in ecology and evolution.Crossref | GoogleScholarGoogle Scholar |

Keith, P., Persat, H., Feunteun, E., and Allardi, J. (2011). ‘Les Poissons d’Eau Douce de France.’ (Muséum National d’Histoire Naturelle: Paris, France.)

Leunda, P. M. (2010). Impacts of non-native fishes on Iberian freshwater ichthyofauna: current knowledge and gaps. Aquatic Invasions 5, 239–262.
Impacts of non-native fishes on Iberian freshwater ichthyofauna: current knowledge and gaps.Crossref | GoogleScholarGoogle Scholar |

Lujić, J., Kostić, D., Bjelić-Čabrilo, O., Popović, E., Miljanović, B., Marinović, Z., and Marković, G. (2013). Ichthyofauna composition and population parameters of fish species from the special nature reserve ‘Koviljsko-Petrovaradinski Rit’ (Vojvodina, Serbia). Turkish Journal of Fisheries and Aquatic Sciences 13, 665–673.
Ichthyofauna composition and population parameters of fish species from the special nature reserve ‘Koviljsko-Petrovaradinski Rit’ (Vojvodina, Serbia).Crossref | GoogleScholarGoogle Scholar |

Maceda-Veiga, A., Monleon-Getino, A., Caiola, N., Casals, F., and de Sostoa, A. (2010). Changes in fish assemblages in catchments in north-eastern Spain: biodiversity, conservation status and introduced species. Freshwater Biology 55, 1734–1746.

Mackay, I., and Mann, K. H. (1969). Fecundity of two cyprinid fishes in the River Thames, Reading, England. Journal of the Fisheries Research Board of Canada 26, 2795–2805.
Fecundity of two cyprinid fishes in the River Thames, Reading, England.Crossref | GoogleScholarGoogle Scholar |

Mann, R. H. K., and Penczak, T. (1984). The efficiency of a new electrofishing technique in determining fish numbers in a large river in central Poland. Journal of Fish Biology 24, 173–185.
The efficiency of a new electrofishing technique in determining fish numbers in a large river in central Poland.Crossref | GoogleScholarGoogle Scholar |

Masó, G., Latorre, D., Tarkan, A. S., Vila-Gispert, A., and Almeida, D. (2016). Inter-population plasticity in growth and reproduction of invasive bleak, Alburnus alburnus (Cyprinidae, Actinopterygii), in northeastern Iberian Peninsula. Folia Zoologica 65, 10–14.
Inter-population plasticity in growth and reproduction of invasive bleak, Alburnus alburnus (Cyprinidae, Actinopterygii), in northeastern Iberian Peninsula.Crossref | GoogleScholarGoogle Scholar |

Mooney, H. A., and Hobbs, R. J. (2000). ‘Invasive Species in a Changing World.’ (Island Press: Washington, DC, USA.)

Muñoz-Mas, R., Vezza, P., Alcaraz-Hernández, J. D., and Martínez-Capel, F. (2016). Risk of invasion predicted with support vector machines: a case study on northern pike (Esox lucius, L.) and bleak (Alburnus alburnus, L.). Ecological Modelling 342, 123–134.
Risk of invasion predicted with support vector machines: a case study on northern pike (Esox lucius, L.) and bleak (Alburnus alburnus, L.).Crossref | GoogleScholarGoogle Scholar |

Reyjol, Y., Hugueny, B., and Pont, D. (2007). Patterns in species richness and endemism of European freshwater fish. Global Ecology and Biogeography 16, 65–75.
Patterns in species richness and endemism of European freshwater fish.Crossref | GoogleScholarGoogle Scholar |

Ribeiro, F., Elvira, B., Collares-Pereira, M. J., and Moyle, P. B. (2008). Life-history traits of non-native fishes in Iberian watersheds across several invasion stages: a first approach. Biological Invasions 10, 89–102.
Life-history traits of non-native fishes in Iberian watersheds across several invasion stages: a first approach.Crossref | GoogleScholarGoogle Scholar |

Rinchard, J., and Kestemont, P. (1996). Comparative study of reproductive biology in single- and multiple-spawner cyprinid fish. I. Morphological and histological features. Journal of Fish Biology 49, 883–894.
Comparative study of reproductive biology in single- and multiple-spawner cyprinid fish. I. Morphological and histological features.Crossref | GoogleScholarGoogle Scholar |

Sakai, A. K., Allendorf, F. W., and Holt, J. S. (2001). The population biology of invasive species. Annual Review of Ecology and Systematics 32, 305–332.
The population biology of invasive species.Crossref | GoogleScholarGoogle Scholar |

Tarkan, A. S., Copp, G. H., Top, N., Özdemir, N., Önsoy, B., Bilge, G., Filiz, H., Yapıcı, S., Ekmekçi, G., Kırankaya, Ş., Emiroğlu, Ö., Gaygusuz, Ö., Gürsoy-Gaygusuz, Ç., Oymak, A., Özcan, G., and Saç, G. (2012). Are introduced gibel carp Carassius gibelio in Turkey more invasive in artificial than in natural waters? Fisheries Management and Ecology 19, 178–187.
Are introduced gibel carp Carassius gibelio in Turkey more invasive in artificial than in natural waters?Crossref | GoogleScholarGoogle Scholar |

Tarkan, A. S., Almeida, D., Godard, M. J., Gaygusuz, Ö., Rylands, M., Sayer, C. D., Zięba, G., and Copp, G. H. (2016). A review and meta-analysis of growth and life-history traits of a declining European freshwater fish, crucian carp Carassius carassius. Aquatic Conservation 26, 212–224.
A review and meta-analysis of growth and life-history traits of a declining European freshwater fish, crucian carp Carassius carassius.Crossref | GoogleScholarGoogle Scholar |

Vinyoles, D., Robalo, J. I., de Sostoa, A., Almodóvar, A., Elvira, B., Nicola, G. G., Fernández-Delgado, C., Santos, C. S., Doadrio, I., Sardà-Palomera, F., and Almada, V. C. (2007). Spread of the alien bleak Alburnus alburnus (Linnaeus, 1758) (Actinopterygii cyprinidae) in the Iberian Peninsula: the role of reservoirs. Graellsia 63, 101–110.
Spread of the alien bleak Alburnus alburnus (Linnaeus, 1758) (Actinopterygii cyprinidae) in the Iberian Peninsula: the role of reservoirs.Crossref | GoogleScholarGoogle Scholar |

Walford, L. A. (1946). A new graphic method of describing the growth of animals. The Biological Bulletin 90, 141–147.
A new graphic method of describing the growth of animals.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaH28%2FktFGhsA%3D%3D&md5=5c42ec6fbc35293066d6415f77f6a113CAS |

Warton, D. I., and Hui, F. K. C. (2011). The arcsine is asinine: the analysis of proportions in ecology. Ecology 92, 3–10.
The arcsine is asinine: the analysis of proportions in ecology.Crossref | GoogleScholarGoogle Scholar |