Hydrobiologia

, Volume 671, Issue 1, pp 227–240 | Cite as

Assessing lake typologies and indicator fish species for Italian natural lakes using past fish richness and assemblages

  • Pietro Volta
  • Alessandro Oggioni
  • Roberta Bettinetti
  • Erik Jeppesen
Primary Research Paper

Abstract

In order to establish a fish-based typology of Italian lakes and identify possible reference and indicator fish species for each lake type, we analysed historical data on fish assemblages of all Italian natural lakes >0.5 km2 from the period prior to the major decline in water quality in the 1950s. General linear regression models showed the ecoregion and lake altitude being the best predictors of fish species richness. The number of species was significantly higher in the Alpine than in the Mediterranean ecoregion. Among Alpine lakes, the number of fish species increased significantly with lake volume whilst decreased with altitude. In the Mediterranean lakes, none of the selected parameters was significant. Cluster analysis of fish assemblages (presence/absence) divided the lakes of the Alpine and Mediterranean ecoregions into four and two types, respectively. Pike (Esox lucius), rudd (Scardinius erythrophthalmus) and tench (Tinca tinca) were the main indicator species for the small and mostly shallow lakes in both the Alpine (Type 1) and Mediterranean (Type 6) ecoregions, minnow (Phoxinus phoxinus) for the alpine high altitude lakes (Type 2) and landlocked shad (Alosa fallax lacustris), European whitefish (Coregonus lavaretus) and burbot (Lota lota) for the large and very deep alpine lakes (Type 4). The European whitefish was the only indicator species for the deep Mediterranean lakes (Type 5). These species and associated fish assemblages may be useful indicators in future assessments of the ecological status of Italian lakes according to the European Directives (2000/60/EC and 2008/105/EC).

Keywords

Fish fauna Biodiversity Bioindicators Reference conditions Biomonitoring Pollutants 

Notes

Acknowledgments

P. Volta (PV) and E. Jeppesen (EJ) were partially funded by the EU-FP7 WISER project; PV also by LIFE+ INHABIT and CIPAIS (Commissione Internazionale per la Protezione delle Acque Italo-Svizzere), and EJ also by EU-FP7 REFRESH, CRES and The Danish Council for Independent Research: Natural Sciences (272-08-0406). We thank Anne Mette Poulsen for most valuable editorial comments and the two anonymous referees for the valuable comments which improved the manuscript importantly.

Supplementary material

10750_2011_720_MOESM1_ESM.doc (27 kb)
List of historical documents used for the reconstruction of lake types based on fish assemblages (DOC 27 kb)

References

  1. Abell, M., M. L. Thieme, C. Revenga, M. Bryer, M. Kottelat, N. Bugutskaya, B. Coad, N. Mandrak, S. Contreras Balderas, W. Bussing, M. L. J. Stiassny, P. Skelton, G. R. Allen, P. Unmack, A. Naseka, R. Ng, N. Sindorf, J. Robestson, E. Armijo, J. V. Higgins, T. J. Heibel, E. Wikramanayake, D. Olson, H. L. Lopez, R. E. Reis, J. G. Lundberg, M. H. Sabaj Perez & P. Petry, 2008. Freshwater ecoregions of the world: a new map of biogeographic units for freshwater biodiversity conservation. BioScience 403: 403–414.CrossRefGoogle Scholar
  2. Albert, J. S. & W. G. Crampton, 2010. Geography and ecology of diversification in Neotropical freshwaters. Nature Education Knowledge 1: 13.Google Scholar
  3. Amarasinghe, U. S. & R. L. Welcomme, 2002. An analysis of fish species richness in natural lakes. Environmental Biology of Fishes 65: 327–339.CrossRefGoogle Scholar
  4. Argillier, C., O. Pronier & P. Irz, 2002. A typology of fish communities in French lakes. II. Fish assemblages in lakes below 1500 m in altitude. Bulletin Francaise Pęche Pisciculture 365–366: 365–366.Google Scholar
  5. Barron, M. G., C. Nardo & J. J. Yurk, 1996. Bioavailability of PCBs in channel catfish exposed to a treated municipal effluent. Environmental Technology 17: 557–560.CrossRefGoogle Scholar
  6. Becker, R. A., J. M. Chambers & A. R. Wilks, 1988. The New S Language: A Programming Environment for Data Analysis and Graphics. Wadsworth & Brooks/Cole, Pacific Grove, CA.Google Scholar
  7. Belpaire, C. & G. Goemans, 2007. The European eel Anguilla anguilla, a rapporteur of the chemical status for the water framework directive? Vie et Milieu – Life and Environment 57: 235–252.Google Scholar
  8. Bettinetti, R., S. Galassi, S. Quadroni, P. Volta, E. Ciccotti, F. Capoccioni & G. A. De Leo, 2010. Use of Anguilla anguilla for biomonitoring persistent organic pollutants (POPs) in brackish and riverine waters in Central and Southern Italy. Water Air & Soil Pollution. doi: 10.1007/s11270-010-0590-y.
  9. Bianco, P. G., 1995. Mediterranean endemic freshwater fishes of Italy. Biological Conservation 72: 159–170.CrossRefGoogle Scholar
  10. Bianco, P. G., 1998. Diversity of Barbinae fishes in southern Europe with description of a new genus and a new species (Cyprinidae). Italian Journal of Zoology 65(Suppl.): 125–136.CrossRefGoogle Scholar
  11. Bianco, P. G. & V. Ketmaier, 2001. Anthropogenic changes in the freshwater fish fauna of Italy, with reference to the central region and Barbus graellsii, a newly established alien species of Iberian origin. Journal of Fish Biology 59: 190–208.CrossRefGoogle Scholar
  12. Carol, J., L. Benejam, C. Alcaraz, A. Vila-Gispert, L. Zamora, E. Navarro, J. Armengol & E. Garcia-Berthou, 2006. The effects of limnological features on fish assemblages of 14 Spanish reservoirs. Ecology of Freshwater Fish 15: 66–77.CrossRefGoogle Scholar
  13. Diekmann, M., U. Bramick, R. Lemcke & T. Mehner, 2005. Habitat-specific fishing revealed distinct indicator species in German lowland lake fish communities. Journal of Applied Ecology 42: 901–909.CrossRefGoogle Scholar
  14. Eckmann, R., 1995. Fish richness in lakes of the northeastern lowlands in Germany. Ecology of Freshwater Fish 4: 62–69.CrossRefGoogle Scholar
  15. Eros, T., J. Heino, D. Schmera & M. Rask, 2009. Characterising functional trait diversity and trait-environment relationships in fish assemblages of boreal lakes. Freshwater Biology 54: 1788–1803.CrossRefGoogle Scholar
  16. EU, 2000. Directive 2000/60/EC of the European Parliament and the Council of 23 October 2000 establishing a framework for community action in the field of water policy. The European Parliament and the Council of the European Union, Brussels: 72 pp.Google Scholar
  17. EU, 2008. Directive 2008/105/EC of the European Parliament and of the Council of 16 December 2008 on environmental quality standards in the field of water policy, amending and subsequently repealing Council Directives 82/176/EEC, 83/513/EEC, 84/156/EEC, 84/491/EEC, 86/280/EEC and amending Directive 2000/60/EC of the European Parliament and of the Council. The European Parliament and the Council of the European Union, Brussels: 14 pp.Google Scholar
  18. Faith, D. P., P. R. Minchin & L. Belbin, 1987. Compositional dissimilarity as a robust measure of ecological distance. Vegetation 69: 57–68.CrossRefGoogle Scholar
  19. Gablehouse, D. W. Jr., 1984. A length categorization system to assess fish stocks. North American Journal of Fisheries Management 4: 273–285.CrossRefGoogle Scholar
  20. Galassi, S. & R. Cassi, 2001. Key species for monitoring persistent and bioaccumulable pesticides. Fresenius Environmental Bulletin 10: 451–454.Google Scholar
  21. Galli, P., G. Strona, F. Benzoni, G. Crosa & F. Stefani, 2007. Monogenoids from freshwater fish in Italy, with comments on alien species. Comparative Parasitology 74: 264–272.CrossRefGoogle Scholar
  22. Gandolfi, G., S. Zerunian, P. Torricelli & A. Marconato, 1991. I Pesci delle acque interne italiane. Istituto Poligrafico e Zecca dello Stato (Eds), Rome.Google Scholar
  23. Garcia, X. F., M. Diekmann, U. Bramick, R. Lemcke & T. Mehner, 2006. Correlations between type-indicator fish species and lake productivity in German lowland lakes. Journal of Fish Biology 68: 1144–1157.CrossRefGoogle Scholar
  24. Gassner, H. & J. Wanzenböck, 2007. Application of population size structure indices to Austrian whitefish (Coregonus sp.) stocks. Fundamental and Applied Limnology. Special Issues: Advances in Limnology 60: 377–384.Google Scholar
  25. Gassner, H., J. Wanzenbock, D. Zick, G. Tischler & B. Pamminger-Lahnsteiner, 2005. Development of a fish based lake typology for natural Austrian lakes >50 ha based on the reconstructed historical fish communities. International Review of Hydrobiology 90: 422–432.CrossRefGoogle Scholar
  26. Godinho, F. N., M. T. Ferreira & M. I. Portugal e Castro, 1998. Fish assemblage composition in relation to environmental gradients in Portuguese reservoirs. Aquatic Living Resources 11: 325–334.CrossRefGoogle Scholar
  27. Griffiths, A., 2006. Pattern and process in the ecological biogeography of European freshwater fish. Journal of Animal Ecology 75: 734–751.CrossRefGoogle Scholar
  28. Guilizzoni, P., G. Bonomi, G. Galanti & D. Ruggiu, 1982. Basic trophic status and recent development of some Italian Lakes as revealed by plant pigments and other chemical components in sediment cores. Memorie dell’Istituto italiano di Idrobiologia 40: 79–98.Google Scholar
  29. Heino, J., T. Eros, J. Kotanen & M. Rask, 2010. Describing lake fish communities: do presence-absence and biomass data show similar spatial and environmental relationships? Boreal Environmental Research 15: 69–80.Google Scholar
  30. Hewitt, G. M., 1999. Post-glacial recolonization of European biota. Biological Journal of the Linnean Society 68: 87–112.CrossRefGoogle Scholar
  31. Holmgren, K. & M. Appelberg, 2000. Size structure of benthic freshwater fish communities in relation to environmental gradients. Journal of Fish biology 57: 1312–1330.CrossRefGoogle Scholar
  32. Irz, P., A. Laurent, S. Messad, O. Pronier & C. Argillier, 2002. Influence of site characteristics on fish community patterns in French reservoirs. Ecology of Freshwater Fishes 11: 123–136.CrossRefGoogle Scholar
  33. Irz, P., C. Argillier & T. Oberdorff, 2004. Native and introduced fish species richness in French lakes: local and regional influences. Global Ecology and Biogeography 13: 335–344.CrossRefGoogle Scholar
  34. Jackson, D. A. & H. H. Harvey, 1989. Biogeographic association in fish assemblages: local vs regional processes. Ecology 70: 1472–1484.CrossRefGoogle Scholar
  35. Jeppesen, E., J. P. Jensen, M. Søndergaard, T. L. Lauridsen & F. Landkildehus, 2000. Trophic structure, species richness and biodiversity in Danish lakes: changes along a phosphorus gradient. Freshwater Biology 45: 201–218.CrossRefGoogle Scholar
  36. Ketmaier, V., P. G. Bianco, M. E. Cobollo & E. De Matthaeis, 2003. Genetic differentiation and biogeography in southern European populations of the genus Scardinius (Pisces, Cyprinidae) based on allozyme data. Zoologica Scripta 32: 13–22.CrossRefGoogle Scholar
  37. Koponen, K., M. S. Myers, O. Ritola, S. E. Huuskonen & P. Lindström-Seppa, 2001. Histopathology of feral fish from a PCB-contaminated freshwater lake. Ambio 30: 122–126.PubMedGoogle Scholar
  38. Lorenzoni, M., R. Pace, G. Pedicillo, P. Viali & A. Carosi, 2009. Growth, catches and reproductive biology of ruffe Gymnocephalus cernuus in Lake Piediluco (Umbria, Italy). Folia Zoologica 58: 420–435.Google Scholar
  39. Marchetto, A., A. Lami, S. Musazzi, J. Masaferro, L. Langone & P. Guilizzoni, 2004. Lake Maggiore (N. Italy) trophic history: fossil diatoms, plant pigments, chironomids and comparison with long-term limnological data. Quaternary International 113: 97–110.CrossRefGoogle Scholar
  40. Marchetto, F., S. Zaccara, F. M. Muenzel & W. Salzburger, 2010. Phylogeography of the Italian vairone (Telestes muticellus, Bonaparte 1837) inferred by microsatellite markers: evolutionary history of a freshwater fish species with a restricted and fragmented distribution. BMC Evolutionary Biology 10: 111.PubMedCrossRefGoogle Scholar
  41. Margaritora, F. G., 1992. Limnology in Latium: the volcanic lakes. Memorie dell’Istituto Italiano di Idrobiologia 50: 319–336.Google Scholar
  42. Marshall, T. R. & P. A. Ryan, 1987. Abundance patterns and community attributes of fishes relative to environmental gradients. Canadian Journal of Fisheries and Aquatic Sciences 44: 198–215.CrossRefGoogle Scholar
  43. Mehner, T., M. Diekmann, U. Bramick & R. Lemcke, 2005. Composition of fish communities in German lakes as related to lake morphology, trophic state, shore structure and human use intensity. Freshwater Biology 50: 70–85.CrossRefGoogle Scholar
  44. Mehner, T., K. Holmgren, T. L. Lauridsen, E. Jeppesen & M. Diekmann, 2007. Lake depth and geographical position modify lake fish assemblages of the European ‘Central Plains’ ecoregion. Freshwater Biology 52: 2285–2297.CrossRefGoogle Scholar
  45. Noble, R. A. A., I. G. Cowx, D. Goffaux & P. Kestemont, 2007. Assessing the health of European rivers using functional ecological guilds of fish communities: standardising species classification and approaches to metric selection. Fisheries Management and Ecology 14: 453–463.CrossRefGoogle Scholar
  46. Nõges, T., 2009. Relationships between morphometry, geographic location and water quality parameters of European lakes. Hydrobiologia 633: 33–43.CrossRefGoogle Scholar
  47. Oksanen, J., R. Kindt, P. Legendre, B. O’Hara & M. H. H. Stevens, 2010. VEGAN: Community Ecology Package. R Package. Version 1.8-8. http://cran.r-project.org/, http://r-forge.r-project.org/projects/vegan/.
  48. Orban, E., T. Nevigato, M. Masci, G. Di Lena, I. Casini, R. Caproni, L. Gambelli, P. De Angelis & M. Rampacci, 2007. Nutritional quality and safety of European perch (Perca fluviatilis) from three lakes of Central Italy. Food Chemistry 100: 482–490.CrossRefGoogle Scholar
  49. Pedicillo, G., A. Bicchi, V. Angeli, A. Carosi, P. Viali & M. Lorenzoni, 2008. Growth of black bullhead Ameiurus melas (Rafinesque, 1820) in Corbara Reservoir (Umbria, Italy). Knowledge and Management of Aquatic Ecosystems 389: 05.CrossRefGoogle Scholar
  50. Penczak, T., W. Galicka, Ł. Głowacki, H. Koszaliński, A. Kruk, G. Zięba, J. Kostrzewa & L. Marszał, 2004. Fish assemblage changes relative to environmental factors and time in the Warta River, Poland, and its oxbow lakes. Journal of Fish Biology 64: 483–501.CrossRefGoogle Scholar
  51. Persson, L., S. Diehl, L. Johansson, G. Anderson & S. F. Hamrin, 1991. Shifts in fish communities along the productivity gradient of temperate lakes – patterns and the importance of size structured interactions. Journal of Fish Biology 38: 281–293.CrossRefGoogle Scholar
  52. R Development Core Team, 2010. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL:http://www.R-project.org.
  53. Reyjol, Y., B. Hugueny, D. Pont, P. G. Bianco, U. Beier, N. Caiola, F. Casals, I. Cowx, A. Economou, T. Ferreira, G. Haidvogl, R. Noble, A. de Sostoa, T. Vigneron & T. Virbickas, 2007. Patterns in species richness and endemism of European freshwater fish. Global Ecology and Biogeography 16: 65–75.CrossRefGoogle Scholar
  54. Salmaso, N., G. Morabito, L. Garibaldi & R. Mosello, 2007. Trophic development of the deep lakes south of the Alps: a comparative analysis. Fundamental and Applied Limnology – Archiv für Hydrobiologie 170: 177–196.CrossRefGoogle Scholar
  55. Schmutz, S., M. Kaufmann, B. Vogel, M. Jungwirth & S. Muhar, 2000. A multilevel concept for fish-based, river-type-specific assessment of ecological integrity. Hydrobiologia 422(423): 279–289.CrossRefGoogle Scholar
  56. Steedman, R. J., T. H. Whillans, A. P. Behm, K. E. Bray, K. I. Cullis, M. M. Holland, S. J. Stoddart & R. J. White, 1996. Use of historical information for conservation and restoration of Great Lakes aquatic habitat. Canadian Journal of Fisheries and Aquatic Sciences 53: 415–423.CrossRefGoogle Scholar
  57. Tammi, J., M. Appelberg, U. Beier, T. Hesthagen, A. Lappalainen & M. Rask, 2003. Fish status survey of Nordic lakes: effects of acidification, eutrophication and stocking activity on present fish species composition. Ambio 32: 98–105.PubMedGoogle Scholar
  58. Tartari, G., E. Buraschi, C. Monguzzi, A. Marchetto, D. Copetti, L. Previtali, S. Taiti, G. Barbiero & R. Pagnotta, 2004. Progetto Limno: Qualità delle Acque Lacustri italiane, Vol. 1. Sintesi dei risultati. Quaderni IRSA 120: 1–333.Google Scholar
  59. Tonn, W. M., J. J. Magnusson, M. Rask & J. Toivonen, 1990. Incontinental comparison of small-lake fish assemblages: the balance between local and regional processes. American Naturalist 136: 345–375.CrossRefGoogle Scholar
  60. Tortonese, E., 1971. Osteichthyes, parte I. Fauna d’Italia, Vol. X. Calderini, Bologna.Google Scholar
  61. Tortonese, E., 1975. Osteichthyes, parte II. Fauna d’Italia, Vol. XI. Calderini, Bologna.Google Scholar
  62. Volta, P., 2010. Analysis of the population structure of Coregonus lavaretus (Linneus 1758) in three deep Italian lakes using stock density indexes. Studi Trentini Scienze Naturali 87: 257–260.Google Scholar
  63. Volta, P. & G. Giussani, 2010. Weight–length relationships (WLRs) and von Bertalanffy growth function (VBGF) parameters of Alosa agone, Rutilus pigus and the anadromous Salmo trutta from a deep south-alpine lake: Lago Maggiore (northern Italy). Journal of Applied Ichthyology 26: 474–476.CrossRefGoogle Scholar
  64. Volta, P. & N. Jepsen, 2008. The recent invasion of Rutilus rutilus (L.) (Pisces: Cyprinidae) in a large South-Alpine lake: Lago Maggiore. Journal of Limnology 67: 163–170.Google Scholar
  65. Volta, P. & A. Oggioni, 2010. Key- and type-specific fish species in natural lakes of Italian Alpine ecoregion reconstructed from historical data: a preliminary index to assess the quality status of fish fauna according to WFD 2000/60/CE. Studi Trentini Scienze Naturali 87: 97–104. in Italian.Google Scholar
  66. Volta, P., P. Tremolada, M. C. Neri, G. Giussani & S. Galassi, 2009. Age-dependent bioaccumulation of organochlorine compounds in fish and their selective biotransformation in top predators from Lake Maggiore (Italy). Water Air & Soil Pollution 197: 193–209.CrossRefGoogle Scholar
  67. Wetzel, R. G., 1975. Limnology. W. B. Saunders Co., Philadelphia/London/Toronto.Google Scholar
  68. WFD CIS, 2003. Rivers and lakes – typology, reference conditions and classification systems. In: Guidance Document No. 10. Published by the Directorate General Environment the European Commission, Brussels.Google Scholar
  69. Zhao, S. Q., J. Y. Fang, C. H. Peng, Z. Y. S. L. Tang & Z. Y. S. L. Piao, 2006. Patterns of fish species richness in China’s lakes. Global Ecology and Biogeography 4: 386–394.CrossRefGoogle Scholar
  70. Zick, D., H. Gassner, M. Rinnerthaler, P. Jäger & R. Patzner, 2007. Application of population size structure indices to Arctic charr Salvelinus alpinus (L.) in Alpine lakes in Austria. Ecology of Freshwater Fish 16: 54–63.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Pietro Volta
    • 1
  • Alessandro Oggioni
    • 1
  • Roberta Bettinetti
    • 2
  • Erik Jeppesen
    • 3
    • 4
    • 5
  1. 1.CNR-Institute of Ecosystem StudyVerbania PallanzaItaly
  2. 2.Department of Chemical and Environmental SciencesUniversity of InsubriaComoItaly
  3. 3.National Environmental Research InstituteAarhus UniversitySilkeborgDenmark
  4. 4.Greenland Climate Research Centre (GCRC)Greenland Institute of Natural ResourcesNuukGreenland
  5. 5.Sino-Danish Centre for Education and Research (SDC)BeijingChina

Personalised recommendations