Skip to main content

Advertisement

SpringerLink
Log in

Spatial distribution patterns of the hyporheic invertebrate communities in a polluted river in Romania

  • Primary research paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

The purpose of this study was to examine the sensitivity, in a field situation, of the hyporheic fauna to pollution by heavy metals and also to test the use of oxidative stress enzymes produced by this fauna as a sensitive indicator of oxidative stress generated by chemical contamination. This was done by surveying the patterns of distribution, structure, and composition of hyporheic invertebrate communities in one of the most polluted rivers in Romania. Twelve permanent sampling stations with differing water qualities were established along a 180 km transect of the Arieş River. Data on hyporheic invertebrate abundance and richness, chemistry of the surface and hyporheic water and interstitial suspended particles were analyzed via multifactorial analyses. In the downstream, more polluted stations, epigean species were less abundant and hyporheic communities, especially macrocrustaceans and oligochetes, became dominant. The higher levels of hyporheic invertebrate biodiversity in the moderately polluted stations compared to highly polluted, and the increase of the number of some hyporheos (especially macrocrustaceans) in the moderately polluted stations, suggested that the hyporheic fauna was more tolerant of heavy metal pollution than the surface water fauna of the area. However, the different richness and abundance of hyporheic fauna in sites of similar water chemistry suggested that additional factors, such as sediment structure are shaping the spatial distribution of hyporheic fauna. Strong correlations between superoxide dismutase (SOD) activity in pooled tissues extracts and some chemical parameters suggest that oxidative stress enzymes may prove to be sensitive indicators of chemical pollution in hyporheic zones.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Bork, J., S. E. Berkhoff, S. Bork & H. J. Hahn, 2009. Using subsurface metazoan fauna to indicate groundwater–surface water interactions in the Nakdong River floodplain. South Korea Hydrogeology Journal 17: 61–75.

    CAS  Google Scholar 

  • Bou, C., 1974. Recherches sur les eaux souterraines. 25—Méthodes de récolte dans les eaux souterraines interstitielles. Annales de Spéléologie 29: 611–619.

    Google Scholar 

  • Boulton, A. J., 2000a. River ecosystem health down under: assessing ecological condition in riverine groundwater zones in Australia. Ecosystem Health 6: 118–198.

    Article  Google Scholar 

  • Boulton, A. J., 2000b. The subsurface macrofauna. In Jones, J. B. & P. J. Mulholland (eds), Streams and Ground Waters. Academic Press, San Diego: 337–361.

    Chapter  Google Scholar 

  • Boulton, A. J., S. Findlay, P. Marmonier, E. H. Stanley & H. M. Valett, 1998. The functional significance of the hyporheic zone in streams and rivers. Annual Review of Ecology, Evolution, and Systematics 29: 59–81.

    Article  Google Scholar 

  • Bourg, A. C. M. & C. Bertin, 1993. Biogeochemical processes during the infiltration of river water into an alluvial aquifer. Environmental Science & Technology 27: 661–666.

    Article  CAS  Google Scholar 

  • Bradford, M. M., 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72: 248–254.

    Article  PubMed  CAS  Google Scholar 

  • Bretschko, G., 1991. Bedsediments, groundwater and stream limnology. Verhandlungen der Internationalen Vereinigung fur Theoretische und Angewandte Limnologie 24: 1957–1960.

    Google Scholar 

  • Brown, R. J., S. D. Rundle, T. H. Hutchinson, T. D. Williams & M. B. Jones, 2003. Small-scale detritus-invertebrate interactions: Influence of detrital biofilm composition on development and reproduction in a meiofaunal copepod. Archiv für Hydrobiologie 157: 117–129.

    Article  Google Scholar 

  • Brunke, M. & T. Gonser, 1997. The ecological significance of exchange processes between rivers and groundwater. Freshwater Biology 37: 1–33.

    Article  Google Scholar 

  • Cantú-Medellín, N., N. O. Olguín-Monroy, L. C. Méndez-Rodríguez & T. Zenteno-Savín, 2009. Antioxidant enzymes and heavy metal levels in tissues of the black chocolate clam Megapitaria squalida in Bahía de La Paz, Mexico. Archives of Environmental Contamination and Toxicology 56: 60–66.

    Article  PubMed  Google Scholar 

  • Chafiq, M., J. Gibert & C. Claret, 1999. Interactions among sediments, organic matter, and microbial activity in the hyporheic zone of an intermittent stream. Canadian Journal of Fisheries and Aquatic Sciences 56(3): 487–495.

    Article  Google Scholar 

  • Connell, J. H., 1978. Diversity in tropical rain forests and coral reefs. Science 199: 1302–1310.

    Article  PubMed  CAS  Google Scholar 

  • Cravo, A., B. Lopes, A. Serafim, R. Company, L. Barreira, T. Gomes & M. J. Bebianno, 2009. A multibiomarker approach in Mytilus galloprovincialis to assess environmental quality. Journal of Environmental Monitoring 11(9): 1673–1686.

    Article  PubMed  CAS  Google Scholar 

  • Creuzé des Châtelliers, M., D. Poinsart & J.-P. Bravard, 1994. Geomorphology of alluvial groundwater ecosystems. In Gibert, J., D. L. Danielopol & J. A. Stanford (eds), Groundwater Ecology. Academic Press, San Diego: 158–185.

    Google Scholar 

  • Culver, D. C., 1982. Cave Life: Evolution and Ecology. Harvard University Press, Cambridge.

    Google Scholar 

  • Danielopol, D. L., M. Creuzé des Châtteliers, F. Mösslacher, P. Pospisil & R. Popa, 1994. Adaption of Crustacea to interstitial habitats: a practical agenda for ecological studies. In Gibert, J., D. L. Danielopol & J. A. Stanford (eds), Groundwater Ecology. Academic, New York: 218–243.

    Google Scholar 

  • Danielopol, D. L., R. Rouch, P. Pospisil, P. Torreiter & F. Mößlacher, 1997. Ecotonal animal assemblages; their interest for groundwater studies. In Gibert, J., J. Mathieu & F. Fournier (eds), Groundwater/Surface Water Ecotones: Biological and Hydrological Interactions and Management Options. Cambridge University Press, Cambridge: 11–20.

    Chapter  Google Scholar 

  • Datry, T., F. Malard & J. Gibert, 2005. Response of invertebrate assemblages to increased groundwater recharge rates in a phreatic aquifer. Journal of the North American Benthological Society 24: 461–477.

    Google Scholar 

  • de Oliveira, U. O., A. S. da Rosa Araujo, A. Bello′-Klein, R. S. M. da Silvaa & L. C. Kucharski, 2005. Effects of environmental anoxia and different periods of reoxygenation on oxidative balance in gills of the estuarine crab Chasmagnathus granulate. Comparative Biochemistry and Physiology Part B 140: 51–57.

    Article  Google Scholar 

  • Dole-Olivier, M.-J., 1998. Surface water-groundwater exchanges in three dimensions on a backwater of the Rhône River. Freshwater Biology 40: 93–109.

    Article  Google Scholar 

  • Dole-Olivier, M.-J., F. Malard, D. Martin, T. Leférbure & J. Gibert, 2009. Relationships between environmental variables and groundwater biodiversity at the regional scale. Freshwater Biology 54: 797–813.

    Article  CAS  Google Scholar 

  • El Adnani, M., A. Ait Boughrous, M. Y. Khebiza, A. El Gharmali, M. L. Sbai, A. S. Errouane, L. Loukili Idrissi & A. Nejmeddine, 2007. Impact of mining wastes on the physicochemical and biological characteristics of groundwater in a mining area in Marrakech (Morocco). Environmental Technology 28: 71–82.

    Article  PubMed  CAS  Google Scholar 

  • Fan, W. H., G. Tang, C. M. Zhao, Y. Duan & R. Zhang, 2009. Metal accumulation and biomarker responses in Daphnia magna following cadmium and zinc exposure. Environmental Toxicology & Chemistry 28(2): 305–310.

    Article  CAS  Google Scholar 

  • Febria, C. M., R. R. Fulthorpe & D. D. Williams, 2009. Characterizing seasonal changes in physicochemistry and bacterial community composition in hyporheic sediments. Hydrobiologia. doi:10.1007/s10750-009-9882-x.

  • Forray, F. L., 2001. Aplicarea analizei factoriale în studiul poluării râului Arieş (Munţii Apuseni). Studia Universitatis Babeş-Bolyai (Geologia) 46: 47–58.

    Google Scholar 

  • Fuller, C. C. & J. W. Harvey, 2000. Reactive uptake of trace metals in the hyporheic zone of a mining-contaminated stream, Pinal Creek, Arizona. Environmental Science & Technology 34: 1150–1155.

    Article  CAS  Google Scholar 

  • Geret, F., A. Serafim, L. Barreira & M. J. Bebianno, 2002. Effect of cadmium on antioxidant enzyme activities and lipid peroxidation in the gills of the clam Ruditapes decussates. Biomarkers 7(3): 242–256.

    Article  PubMed  CAS  Google Scholar 

  • Griebler, C. & F. Mösslacher, 2003. Grundwasser-eine ökosystemische Betrachtung. In Griebler, C. & F. Mösslacher (eds), Grundwasserökologie. UTB-Facultas Verlag, Wien: 253–310.

    Google Scholar 

  • Hahn, H. J., 2006. The GW-fauna-index: a first approach to a quantitative ecological assessment of groundwater habitats. Limnologica 36: 119–137.

    Google Scholar 

  • Hahn, H. J. & D. Matzke, 2005. A comparison of stygofauna communities inside and outside groundwater bores. Limnologica 35: 31–44.

    Google Scholar 

  • Hakenkamp, C. C. & M. A. Palmer, 2000. The ecology of hyporheic meiofauna. In Jones, J. B. & P. J. Mulholland (eds), Streams and Ground Waters. Academic, San Diego: 307–335.

    Chapter  Google Scholar 

  • Hancock, P. J., 2002. Human impacts on the stream-groundwater exchange zone. Environmental Management 29(6): 763–781.

    Article  PubMed  Google Scholar 

  • Hendricks, S. P. & D. S. White, 1995. Seasonal biogeochemical patterns in surface water, subsurface hyporheic, and riparian ground water in a temperate stream ecosystem. Archiv für Hydrobiologie 134: 459–490.

    CAS  Google Scholar 

  • Hinkle, S., J. Duff, F. Triska, A. Laenen, E. Gates, K. Bencala, D. Wentz & S. Silva, 2001. Linking hyporheic flow and nitrogen cycling near the Willamette River—a large river in Oregon, USA. Journal of Hydrology 244: 157–180.

    Article  CAS  Google Scholar 

  • Malard, F. & F. Hervant, 1999. Oxygen supply and the adaptations of animals in groundwater. Freshwater Biology 41: 1–30.

    Article  Google Scholar 

  • Malard, F., J.-L. Reygrobellet, J. Mathieu & M. Lafont, 1994. The use of invertebrate communities to describe groundwater flow and contaminant transport in a fractured rock aquifer. Archiv für Hydrobiologie 131(1): 93–110.

    Google Scholar 

  • Malard, F., S. Plénet & J. Gibert, 1996. The use of invertebrates in ground water monitoring: a rising research field. Ground Water Monitoring and Remediation 16: 103–113.

    Article  CAS  Google Scholar 

  • Manduzio, H., T. Monsinjon, C. Galap, F. Leboulenger & B. Rocher, 2004. Seasonal variations in antioxidant defences in blue mussels Mytilus edulis collected from a polluted area: major contributions in gills of an inducible isoform of Cu/Zn-superoxide dismutase and of glutathione S-transferase. Aquatic Toxicology 70(1): 83–93.

    Article  PubMed  CAS  Google Scholar 

  • Moldovan, O., Iepure, S. & A. Perşoiu, 2005. Biodiversity and protection of Romanian karst areas: the example of interstitial fauna. In Stevanovič, Z. & P. Milanovič (eds), Water Resources and Environmental Problems in Karst. Proceedings International Conference & Field Seminar, Beograd & Kotor, 13–19 September 2005: 831–836.

  • Momeu, L., K. W. Battes, F. Pricope, A. Avram, K. P. Battes, M. Cîmpean, D. Ureche & I. Stoica, 2007. Preliminary data on algal, macroinvertebrate and fish communities from the Arieş catchment area, Transylvania, Romania. Studia Universitatis Babeş-Bolyai (Biología) 52: 25–36.

    Google Scholar 

  • Morel, F. M. M., 1983. Principles of Aquatic Chemistry. Wiley, New York.

    Google Scholar 

  • Moser, D. P., J. K. Fredrickson, D. R. Geist, E. V. Arntzen, A. D. Peacock & S.-M. W. Li, 2003. Biogeochemical processes and microbial characteristics across groundwater-surface water boundaries of the Hanford Reach of the Colombia River. Environmental Science & Technology 37: 5127–5134.

    Article  CAS  Google Scholar 

  • Mösslacher, F. & J. Notenboom, 1999. Groundwater biomonitoring. In Gerhardt, A. (ed.), Biomonitoring of Polluted Water. Environmental Science Forum 96: 119–140.

  • Mösslacher, F. & M. Creuzé des Châtelliers, 1996. Physiological and behavioural adaptations of an epigean and a hyporheic dwelling population of Asellus aquaticus (L.) (Crustacea, Isopoda). Archiv für Hydrobiologie 138: 187–198.

    Google Scholar 

  • Munk, L., G. Faure, D. Pride & J. Bigham, 2002. Sorption of trace metals to an aluminum precipitate in a stream receiving acid rock-drainage; Snake River, Summit County, Colorado. Applied Geochemistry 17: 421–430.

    Article  CAS  Google Scholar 

  • Notenboom, J., S. Plénet & M.-J. Turquin, 1994. Groundwater contamination and its impact on groundwater animals and ecosystems. In Gibert, J., D. L. Danielopol & J. A. Stanford (eds), Groundwater Ecology. Academic Press, San Diego: 477–504.

    Google Scholar 

  • Pagés, J., 2004. Multiple factor analysis: main features and application to sensory data. Revista Colombiana de Estadistica 27: 1–26.

    Google Scholar 

  • Plénet, S., 1995. Freshwater amphipods as biomonitors of metal pollution in surface and interstitial aquatic systems. Freshwater Biology 33: 127–137.

    Article  Google Scholar 

  • Plénet, S., 1999. Metal accumulation by an epigean and a hypogean freshwater amphipod: considerations for water quality assessment. Water Environment Research 71: 1298–1309.

    Article  Google Scholar 

  • Plénet, S. & J. Gibert, 1994. Invertebrate community responses to physical and chemical factors at the river/aquifer interaction zone. I. Upstream from the city of Lyon. Archiv für Hydrobiologie 132: 165–189.

    Google Scholar 

  • Plénet, S., H. Hugueny & J. Gibert, 1996. Invertebrate community responses to physical and chemical factors at the river/aquifer interaction zone. II. Downstream from the city of Lyon. Archiv für Hydrobiologie 136: 65–88.

    Google Scholar 

  • Pyle, G. G. & R. S. Mirza, 2007. Copper-impaired chemosensory function and behavior in aquatic animals. Human Ecological Risk Assessment 13: 492–505.

    Article  CAS  Google Scholar 

  • Rouch, R. & D. Danielopol, 1987. L’origine de la faune aquatique souterraine, entre le paradigme du refuge et le modèle de la colonization active. Stygologia 3: 345–372.

    Google Scholar 

  • Rusu, M., H. L. Banciu, M. Banciu, T. Brad & O. T. Moldovan, 2010. Oxidative stress enzymes as biomarkers of heavy metal pollution in interstitial invertebrates. Studia Universitatis Babes-Bolyai 2: 61–66.

    Google Scholar 

  • Schmid-Araya, J. M., 1998. Small-sized invertebrates in a gravel stream: community structure and variability of benthic rotifers. Freshwater Biology 39: 25–39.

    Article  Google Scholar 

  • Ukeda, H., T. Shimamura, M. Tsubouchi, Y. Harada, Y. Nakai & M. Sawamura, 2002. Spectrophotometric assay of superoxide anion formed in Maillard reaction based on highly water-soluble tetrazolium salt. Analytical Sciences 18: 1151–1154.

    Article  PubMed  CAS  Google Scholar 

  • Van Damme, P. A., C. Hamel, A. Ayala & L. Bervoets, 2008. Macroinvertebrate community response to acid mine drainage in rivers of the High Andes (Bolivia). Environmental Pollution 156: 1061–1068.

    Article  PubMed  Google Scholar 

  • Williams, D. D. & R. R. Fulthorpe, 2003. Using invertebrate and microbial communities to assess the condition of the hyporheic zone of a river subject to 80 years of contamination by chlorobenzenes. Canadian Journal of Zoology 8: 789–802.

    Article  Google Scholar 

  • Wong, S. W., P. T. Leung, A. B. Djurisić & K. M. Leung, 2010. Toxicities of nano zinc oxide to five marine organisms: influences of aggregate size and ion solubility. Analytical and Bioanalytical Chemistry 396(2): 609–618.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We are grateful to Frank Fiers for useful discussions and suggestions, to Géza Rajka, Ákos Nagy and Nimrod Nemeth for help with samplings, to Vlad Paul for insect larvae identification, and to Mihai Terente for the map. Claire Stephens was very helpful in improving the content and the English of the manuscript. Stuart Halse, Koen Martens and two anonymous reviewers made valuable remarks improving considerably the manuscript quality. This study was funded through the grants 31_032/2007 (CNMP, Ministry of Education, Research and Innovation, Romania) and SYNTHESYS BE-TAF 4681 (European Union-funded Integrated Activities grant).

Author information

Authors and Affiliations

  1. “Emil Racovitza” Institute of Speleology, Romanian Academy, Clinicilor 5, 400006, Cluj-Napoca, Romania

    Oana Teodora Moldovan, Traian Brad, Ioana Meleg & Sanda Iepure

  2. Faculty of Biology and Geology, “Babeş-Bolyai” University, Cluj-Napoca, Romania

    Manuela Banciu, Horia Leonard Banciu & Mirela Cîmpean

  3. Romanian Waters National Administration, Someş Tisa Division, Cluj-Napoca, Romania

    Claudia Pavelescu

  4. National Institute of Research and Development for Optoelectronics, Research Institute for Analytical Instrumentation, Bucharest, Romania

    Erika Levei

  5. “Emil Racovitza” Institute of Speleology, Romanian Academy, Bucureşti, Romania

    Constantin Marin & Ioan Povară

Authors
  1. Oana Teodora Moldovan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Erika Levei
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Constantin Marin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Manuela Banciu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Horia Leonard Banciu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Claudia Pavelescu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Traian Brad
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Mirela Cîmpean
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Ioana Meleg
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Sanda Iepure
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Ioan Povară
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Oana Teodora Moldovan.

Additional information

Handling editor: Stuart Anthony Halse

Rights and permissions

Reprints and permissions

About this article

Cite this article

Moldovan, O.T., Levei, E., Marin, C. et al. Spatial distribution patterns of the hyporheic invertebrate communities in a polluted river in Romania. Hydrobiologia 669, 63–82 (2011). https://doi.org/10.1007/s10750-011-0651-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-011-0651-2

Keywords

Search

Navigation