Abstract
Climate is a major driver of species distribution and biological invasions worldwide. In this study, we combined the catches of a widespread and invasive species, the common carp (Cyprinus carpio), with climate data to assess the importance of climate variables on the ability of the species to maintain self-sustaining populations in European lakes. Data were collected on common carp populations in 378 lakes in six European countries over a 16-year period (551 sampling campaigns). All catches followed the same standardized sampling procedure (European CEN gillnets). Climate data consisted of daily averages of air temperature and precipitation. Population self-sustainability was determined by the relative catches of different size classes and the presence of juveniles. The climate data were used to train a classification tree model to characterize the effects of climate on common carp population viability. Results indicated that climate is an important predictor of common carp population viability, which is particularly enhanced under dry conditions and elevated temperatures during spring and summer months. Areas of high population viability strongly overlapped with the invasive range of the species. According to Intergovernmental Panel on Climate Change (IPCC) climate projections, some areas where common carp currently have a low probability of maintaining viable populations will shift toward climatic conditions that enhance their viability and invasion potential.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
(2020) The IUCN Red List of Threatened Species. In: IUCN Red List Threat. Species. https://www.iucnredlist.org/en. Accessed 8 Apr 2020
Achleitner D, Gassner H, Luger M (2012) Comparison of three standardised fish sampling methods in 14 alpine lakes in Austria. Fish Manag Ecol 19:352–361. https://doi.org/10.1111/j.1365-2400.2012.00851.x
Adámek Z, Pardo MA, Vilizzi L, Roberts J (2015) Successful reproduction of common carp Cyprinus carpio in irrigation waterways. Fish Manag Ecol 22:279–285. https://doi.org/10.1111/fme.12123
Alexander TJ, Vonlanthen P, Periat G et al (2015) Evaluating gillnetting protocols to characterize lacustrine fish communities. Fish Res 161:320–329. https://doi.org/10.1016/j.fishres.2014.08.009
Arlinghaus R, Mehner T (2003) Socio-economic characterisation of specialised common carp (Cyprinus carpio L.) anglers in Germany, and implications for inland fisheries management and eutrophication control. Fish Res 61:19–33. https://doi.org/10.1016/S0165-7836(02)00243-6
Arula T, Laur K, Simm M, Ojaveer H (2015) Dual impact of temperature on growth and mortality of marine fish larvae in a shallow estuarine habitat. Estuar Coast Shelf Sci 167:326–335. https://doi.org/10.1016/j.ecss.2015.10.004
Badiou PHJ, Goldsborough LG (2015) Ecological impacts of an exotic benthivorous fish, the common carp (Cyprinus carpio L.), on water quality, sedimentation, and submerged macrophyte biomass in wetland mesocosms. Hydrobiologia 755:107–121. https://doi.org/10.1007/s10750-015-2220-6
Balon EK (1995) Origin and domestication of the wild carp, Cyprinus carpio: from Roman gourmets to the swimming flowers. Aquaculture 129:3–48. https://doi.org/10.1016/0044-8486(94)00227-F
Balon EK (2004) About the oldest domesticates among fishes. J Fish Biol 65:1–27. https://doi.org/10.1111/j.0022-1112.2004.00563.x
Beissinger SR, McCullough DR (2002) Population viability analysis. The University of Chicago Press, Chicago
Bio A, Couto A, Costa R et al (2009) Biomanipulation of Furnas Lake, Azores: effects of repeated fish removal. SIL Proc 1922–2010(30):1207–1209. https://doi.org/10.1080/03680770.2009.11923913
Biro PA, Post JR, Booth DJ (2007) Mechanisms for climate-induced mortality of fish populations in whole-lake experiments. Proc Natl Acad Sci 104:9715–9719. https://doi.org/10.1073/pnas.0701638104
Boukal DS, Jankovský M, Kubečka J, Heino M (2012) Stock–catch analysis of carp recreational fisheries in Czech reservoirs: Insights into fish survival, water body productivity and impact of extreme events. Fish Res 119–120:23–32. https://doi.org/10.1016/j.fishres.2011.12.003
Breukelaar AW, Lammens EHRR, Breteler JGPK, Tátrai I (1994) Effects of benthivorous bream (Abramis brama) and carp (Cyprinus carpio) on sediment resuspension and concentrations of nutrients and chlorophyll a. Freshw Biol 32:113–121. https://doi.org/10.1111/j.1365-2427.1994.tb00871.x
CEN - Comité Européen de Normalisation (2005) Water quality - Sampling of fish with multi-mesh gillnets (CEN 14757). Brussels
Carosi A, Ghetti L, Padula R, Lorenzoni M (2019) Potential effects of global climate change on fisheries in the Trasimeno Lake (Italy), with special reference to the goldfish Carassius auratus invasion and the endemic southern pike Esox cisalpinus decline. Fish Manag Ecol 26:500–511. https://doi.org/10.1111/fme.12318
Comte L, Buisson L, Daufresne M, Grenouillet G (2013) Climate-induced changes in the distribution of freshwater fish: observed and predicted trends. Freshw Biol 58:625–639. https://doi.org/10.1111/fwb.12081
Cowx IG, Welcomme RL (1998) Rehabilitation of rivers for fish. Fishing New Books, Oxford
Crivelli AJ (1981) The biology of the common carp, Cyprinus carpio L. in the Camargue, southern France. J Fish Biol 18:271–290. https://doi.org/10.1111/j.1095-8649.1981.tb03769.x
Crivelli AJ (1983) The destruction of aquatic vegetation by carp. Hydrobiologia 106:37–41. https://doi.org/10.1007/BF00016414
Cutler F original by LB and A, Wiener R port by AL and M (2018) randomForest: Breiman and Cutler’s Random Forests for Classification and Regression. Version 4.6–14URL https://CRAN.R-project.org/package=randomForest
Drake JM (2008) Population viability analysis. In: Jørgensen SE, Fath BD (eds) Encyclopedia of ecology. Academic Press, Oxford, pp 2901–2907
Eccel E, Cordano E, Toller G, Mach FE (2016) ClimClass: Climate Classification According to Several Indices. Version 2.1.0URL https://CRAN.R-project.org/package=ClimClass
Elith J, Graham CH, Anderson RP et al (2006) Novel methods improve prediction of species’ distributions from occurrence data. Ecography 29:129–151. https://doi.org/10.1111/j.2006.0906-7590.04596.x
Ellender B, Weyl O (2014) A review of current knowledge, risk and ecological impacts associated with non-native freshwater fish introductions in South Africa. Aquat Invasions 9:117–132. https://doi.org/10.3391/ai.2014.9.2.01
Emmrich M, Pédron S, Brucet S et al (2014) Geographical patterns in the body-size structure of European lake fish assemblages along abiotic and biotic gradients. J Biogeogr 41:2221–2233. https://doi.org/10.1111/jbi.12366
FAO (2019) FAO yearbook. Fishery and Aquaculture Statistics 2017/FAO annuaire. Statistiques des pêches et de l’aquaculture 2017/ FAO anuario. Estadísticas de pesca y acuicultura 2017. Rome
Froese R, Pauly D (2021) FishBase. www.fishbase.org. Accessed 13 Apr 2020
Funge-Smith S (2018) Review of the state of the world fishery resources: Inland fisheries. 399
Grenouillet G, Schmidt-Kloiber A (2006) Fish Indicator Database. Euro-limpacs project, Workpackage 7 - Indicators of ecosystem health, Task 4. In: www.freshwaterecology.info
Guisan A, Zimmermann NE (2000) Predictive habitat distribution models in ecology. Ecol Model 135:147–186. https://doi.org/10.1016/S0304-3800(00)00354-9
HELCOM (2006) Assessment of Coastal Fish in the Baltic Sea. Helsinki
Habel JC, Zachos FE, Dapporto L et al (2015) Population genetics revisited – towards a multidisciplinary research field. Biol J Linn Soc 115:1–12. https://doi.org/10.1111/bij.12481
Hastie T, Tibshirani R, Friedman J (2009) The elements of statistical learning: data mining, inference, and prediction, 2nd edn. Springer-Verlag, New York
Haubrock P, Criado A, Monteoliva A et al (2018) Control and eradication efforts of aquatic alien fish species in Lake Caicedo Yuso-Arreo. Manag Biol Invasions 9:267–278. https://doi.org/10.3391/mbi.2018.9.3.09
Hickley P, Chare S (2004) Fisheries for non-native species in England and Wales: angling or the environment? Fish Manag Ecol 11:203–212. https://doi.org/10.1111/j.1365-2400.2004.00395.x
Hijmans RJ, Williams E, Vennes C (2017) geosphere: Spherical Trigonometry. Version 1.5–7URL https://CRAN.R-project.org/package=geosphere
Ho TK (1995) Random decision forests. In: Proceedings of the Third International Conference on Document Analysis and Recognition (Volume 1) - Volume 1. IEEE Computer Society, USA, p 278
Horvath L, Tamas G, Seagrave C (2002) Carp and pond fish culture, 2nd edn. Wiley-Interscience
Horvath L, Tamas G, Coche AG (1985) Common carp, pt. 1: Mass production of eggs and early fry
Hoverman JT, Johnson PTJ (2012) Ponds and lakes: a journey through the life aquatic. Nat Educ Knowl 3:17
Intergovernmental Panel for the Climate Change (2014) Climate Change 2014 – Impacts, Adaptation and Vulnerability: Part A: Global and Sectoral Aspects: Working Group II Contribution to the IPCC Fifth Assessment Report. In: Camb. Core. /core/books/climate-change-2014-impacts-adaptation-and-vulnerability-part-a-global-and-sectoral-aspects/1BE4ED76F97CF3A75C64487E6274783A. Accessed 20 Apr 2020
Kolada A (2014) The effect of lake morphology on aquatic vegetation development and changes under the influence of eutrophication. Ecol Indic 38:282–293. https://doi.org/10.1016/j.ecolind.2013.11.015
Lauchlan SS, Nagelkerken I (2020) Species range shifts along multistressor mosaics in estuarine environments under future climate. Fish Fish 21:32–46. https://doi.org/10.1111/faf.12412
Lele SR, Keim JL, Solymos P (2019) ResourceSelection: resource selection (probability) functions for use-availability data
Lowe S, Browne M, Boudjelas S, De Poorter M (2000) 100 of the World’s Worst Invasive Alien Species: A Selection From the Global Invasive Species Database. The Invasive Species Specialist Group (ISSG) a specialist group of the Species Survival Commission (SSC) of the World Conservation Union (IUCN). Hollands Printing Ltd, New Zealand
Lovas-Kiss Á, Vincze O, Löki V et al (2020) Experimental evidence of dispersal of invasive cyprinid eggs inside migratory waterfowl. Proc Natl Acad Sci. https://doi.org/10.1073/pnas.2004805117
Maceda-Veiga A, López R, Green AJ (2017) Dramatic impact of alien carp Cyprinus carpio on globally threatened diving ducks and other waterbirds in Mediterranean shallow lakes. Biol Conserv 212:74–85. https://doi.org/10.1016/j.biocon.2017.06.002
Mack RN, Simberloff D, Lonsdale WM et al (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710. https://doi.org/10.1890/1051-0761(2000)010[0689:BICEGC]2.0.CO;2
Macklin R, Brazier B, Harrison S et al (2016) A review of the status and range expansion of common carp (Cyprinus carpio L.) in Ireland. Aquat Invasions 11:75–82. https://doi.org/10.3391/ai.2016.11.1.08
Maiztegui T, Baigún CRM, de Souza JRG et al (2019) Population responses of common carp Cyprinus carpio to floods and droughts in the Pampean wetlands of South America. NeoBiota 48:25–44. https://doi.org/10.3897/neobiota.48.34850
Marr SM, Olden JD, Leprieur F et al (2013) A global assessment of freshwater fish introductions in mediterranean-climate regions. Hydrobiologia 719:317–329. https://doi.org/10.1007/s10750-013-1486-9
Maynou F, Sabatés A, Raya V (2020) Changes in the spawning habitat of two small pelagic fish in the Northwestern Mediterranean. Fish Oceanogr 29:201–213. https://doi.org/10.1111/fog.12464
McCallum KP, Guerin GR, Breed MF, Lowe AJ (2014) Combining population genetics, species distribution modelling and field assessments to understand a species vulnerability to climate change. Austral Ecol 39:17–28. https://doi.org/10.1111/aec.12041
Mehner T, Keeling C, Emmrich M et al (2015) Effects of fish predation on density and size spectra of prey fish communities in lakes1. Can J Fish Aquat Sci. https://doi.org/10.1139/cjfas-2015-0034
Mehner T, Rapp T, Monk CT et al (2019) Feeding aquatic ecosystems: whole-lake experimental addition of angler’s ground bait strongly affects omnivorous fish despite low contribution to lake carbon budget. Ecosystems 22:346–362. https://doi.org/10.1007/s10021-018-0273-x
Meijer M-L, de Haan MW, Breukelaar AW, Buiteveld H (1990) Is reduction of the benthivorous fish an important cause of high transparency following biomanipulation in shallow lakes? In: Gulati RD, Lammens EHRR, Meijer M-L, van Donk E (eds) Biomanipulation tool for water management. Springer, Netherlands, pp 303–315
Morris W, Nature Conservancy (U.S.) (1999) A practical handbook for population viability analysis. The Nature Conservancy, Arlington, VA
Murphy CA, Grenouillet G, García-Berthou E (2015) Natural abiotic factors more than anthropogenic perturbation shape the invasion of Eastern Mosquitofish (Gambusia holbrooki). Freshw Sci 34:965–974. https://doi.org/10.1086/681948
NASA (2020) NASA - POWER. https://power.larc.nasa.gov/. Accessed 8 Apr 2020
Niesar M, Arlinghaus R, Rennert B, Mehner T (2004) Coupling insights from a carp, Cyprinus carpio, angler survey with feeding experiments to evaluate composition, quality and phosphorus input of groundbait in coarse fishing. Fish Manag Ecol 11:225–235. https://doi.org/10.1111/j.1365-2400.2004.00400.x
Nunn AD, Bolland JD, Harvey JP, Cowx IG (2007) Establishment of self-sustaining populations of non-native fish species in the River Trent and Warwickshire Avon, UK, indicated by the presence of 0+ fish. Aquat Invasions 2:190–196. https://doi.org/10.3391/ai.2007.2.3.6
Ooms J, Lang DT, Hilaiel L (2020) jsonlite: a robust, high performance JSON parser and generator for R. Version 1.6.1URL https://CRAN.R-project.org/package=jsonlite
Ottersen G, Hjermann DØ, Stenseth NC (2006) Changes in spawning stock structure strengthen the link between climate and recruitment in a heavily fished cod (Gadus morhua) stock. Fish Oceanogr 15:230–243. https://doi.org/10.1111/j.1365-2419.2006.00404.x
Oyugi D, Cucherousset J, Baker D, Britton J (2012) Effects of temperature on the foraging and growth rate of juvenile common carp, Cyprinus carpio. J Therm Biol 37:89–94. https://doi.org/10.1016/j.jtherbio.2011.11.005
Oyugi DO, Cucherousset J, Ntiba MJ et al (2011) Life history traits of an equatorial common carp Cyprinus carpio population in relation to thermal influences on invasive populations. Fish Res 110:92–97. https://doi.org/10.1016/j.fishres.2011.03.017
Paumier A, Drouineau H, Boutry S et al (2020) Assessing the relative importance of temperature, discharge, and day length on the reproduction of an anadromous fish (Alosa alosa). Freshw Biol 65:253–263. https://doi.org/10.1111/fwb.13418
Peterson AT (2003) Predicting the geography of species’ invasions via ecological niche modeling. Q Rev Biol 78:419–433. https://doi.org/10.1086/378926
Porreca AP, Pederson CL, Laursen JR, Colombo RE (2013) A comparison of electrofishing methods and fyke netting to produce reliable abundance and size metrics. J Freshw Ecol 28:585–590. https://doi.org/10.1080/02705060.2013.810555
R Core Team (2020) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
Rapp T, Cooke SJ, Arlinghaus R (2008) Exploitation of specialised fisheries resources: the importance of hook size in recreational angling for large common carp (Cyprinus carpio L.). Fish Res 94:79–83. https://doi.org/10.1016/j.fishres.2008.06.019
Reside AE, Critchell K, Crayn DM et al (2019) Beyond the model: expert knowledge improves predictions of species’ fates under climate change. Ecol Appl. https://doi.org/10.1002/eap.1824
Ribeiro F, Crain PK, Moyle PB (2004) Variation in condition factor and growth in young-of-year fishes in floodplain and riverine habitats of the Cosumnes River, California. Hydrobiologia 527:77–84. https://doi.org/10.1023/B:HYDR.0000043183.86189.f8
Ribeiro F, Elvira B, Collares-Pereira MJ, Moyle PB (2008) Life-history traits of non-native fishes in Iberian watersheds across several invasion stages: a first approach. Biol Invasions 10:89–102. https://doi.org/10.1007/s10530-007-9112-2
Roberts JJ, Fausch KD, Peterson DP, Hooten MB (2013) Fragmentation and thermal risks from climate change interact to affect persistence of native trout in the Colorado River basin. Glob Change Biol 19:1383–1398. https://doi.org/10.1111/gcb.12136
Slatkin M (1987) Gene flow and the geographic structure of natural populations. Science 236:787–792. https://doi.org/10.1126/science.3576198
Smalås A, Strøm JF, Amundsen P-A et al (2020) Climate warming is predicted to enhance the negative effects of harvesting on high-latitude lake fish. J Appl Ecol 57:270–282. https://doi.org/10.1111/1365-2664.13535
Souza AT, Ilarri MI, Timóteo S et al (2018) Assessing the effects of temperature and salinity oscillations on a key mesopredator fish from European coastal systems. Sci Total Environ 640–641:1332–1345. https://doi.org/10.1016/j.scitotenv.2018.05.348
Specziár A, Turcsányi B (2014) Effect of stocking strategy on distribution and recapture rate of common carp Cyprinus carpio L., in a large and shallow temperate lake: implications for recreational put-and-take fisheries management. J Appl Ichthyol 30:887–894. https://doi.org/10.1111/jai.12488
Sutherland WJ, Freckleton RP, Godfray HCJ et al (2013) Identification of 100 fundamental ecological questions. J Ecol 101:58–67. https://doi.org/10.1111/1365-2745.12025
Szücs I, Stündl L, Váradi L (2007) Carp farming in central and eastern europe and a case study in multifunctional aquaculture species and system selection for sustainable aquaculture. Wiley, Berlin, pp 389–414
Taylor AH, Tracey SR, Hartmann K, Patil JG (2012) Exploiting seasonal habitat use of the common carp, Cyprinus carpio, in a lacustrine system for management and eradication. Mar Freshw Res 63:587–597. https://doi.org/10.1071/MF11252
Tempero GW, Ling N, Hicks BJ, Osborne MW (2006) Age composition, growth, and reproduction of koi carp (Cyprinus carpio) in the lower Waikato region, New Zealand. N Z J Mar Freshw Res 40:571–583. https://doi.org/10.1080/00288330.2006.9517446
Verberk W (2011) Explaining general patterns in species abundance and distributions. Nat Edu Knowl 3:38
Vidal N, de Mello FT, González-Bergonzoni I et al (2020) Long-term study of the reproductive timing of the Neotropical catfish Iheringichthys labrosus (Lütken, 1874): influence of temperature and river discharge. Ecol Freshw Fish 29:334–345. https://doi.org/10.1111/eff.12518
Vilizzi L (2012) The common carp, Cyprinus carpio, in the Mediterranean region: origin, distribution, economic benefits, impacts and management. Fish Manag Ecol 19:93–110. https://doi.org/10.1111/j.1365-2400.2011.00823.x
Vilizzi L, Copp GH (2017) Global patterns and clines in the growth of common carp Cyprinus carpio. J Fish Biol 91:3–40. https://doi.org/10.1111/jfb.13346
Vilizzi L, Tarkan AS, Copp GH (2015) Experimental Evidence from Causal Criteria Analysis for the Effects of Common Carp Cyprinus carpio on Freshwater Ecosystems: A Global Perspective. Rev Fish Sci Aquac 23:253–290. https://doi.org/10.1080/23308249.2015.1051214
Weber MJ, Brown ML (2012) Maternal effects of common carp on egg quantity and quality. J Freshw Ecol 27:409–417. https://doi.org/10.1080/02705060.2012.666890
Wisz M, Pottier J, Kissling WD et al (2013) The role of biotic interactions in shaping distributions and realised assemblages of species: implications for species distribution modelling. Biol Rev 88:15–30. https://doi.org/10.1111/j.1469-185x.2012.00235.x
Zambrano L, Martínez-Meyer E, Menezes N, Peterson AT (2006) Invasive potential of common carp (Cyprinus carpio) and Nile tilapia (Oreochromis niloticus) in American freshwater systems. Can J Fish Aquat Sci 63:1903–1910. https://doi.org/10.1139/f06-088
Acknowledgements
This work has received funding from the European Union’s Horizon 2020 research and innovation programme under grant agreement No. 677039” project CLIMEFISH and from ERDF/ESF project “Biomanipulation as a tool for improving water quality of dam reservoirs” (No. CZ.02.1.01/0.0/0.0/16_025/0007417). The Foundation for Science and Technology supported Marine and Environmental Sciences Centre (MARE) through the strategic plan of the (UID/Multi/04326/2019). IJ was supported by J. E. Purkyně Fellowship of the Czech Academy of Sciences. PV and PS were supported by LIFE15 NAT/IT/000823 IdroLIFE project. This publication reflects the views only of the authors, and the Commission cannot be held responsible for any use that may be made of the information contained therein.
Funding
This work has received funding from the European Union’s Horizon 2020 research and innovation programme under grant agreement No. 677039″ project CLIMEFISH and from ERDF/ESF project “Biomanipulation as a tool for improving water quality of dam reservoirs” (No. CZ.02.1.01/0.0/0.0/16_025/0007417) Horizon 2020 Framework Programme,677039,ERDF/ESF,CZ.02.1.01/0.0/0.0/16_025/0007417,Jan Kubečka
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
There are no conflicts of interest.
Availability of data and material
Raw data will be available under reasonable request.
Ethical approval
Not applicable.
Code availability
Not applicable.
Consent to participate
All authors agreed in the participation in the manuscript.
Consent for publication
All authors agree in the publication of the manuscript.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Souza, A.T., Argillier, C., Blabolil, P. et al. Empirical evidence on the effects of climate on the viability of common carp (Cyprinus carpio) populations in European lakes. Biol Invasions 24, 1213–1227 (2022). https://doi.org/10.1007/s10530-021-02710-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-021-02710-5