Sustainability of gastropod introduction for ecological engineering solution in infiltration basins: feeding strategy of V. viviparus

  • Valerian EstragnatEmail author
  • Laurence Volatier
  • Jean-Bastien Gambonnet
  • Frédéric Hervant
  • Pierre Marmonier
  • Florian Mermillod-Blondin
Primary Research Paper


The present study aimed at evaluating the sustainability of ecological engineering solutions based on the introduction of the gastropod V. viviparus for maintaining the hydrological performances of infiltration basins clogged by benthic biofilms. This sustainability depends on the ability of gastropods to deal with variations in trophic resources throughout seasonal changes and so their feeding strategy. It is expected from literature that V. viviparus is a generalist species, well adapted for ecological engineering approaches. With this objective, laboratory and field experiments were developed to measure the ability of gastropods to maintain energy body stores under several food sources and seasons, in relation with their physiological state. Our results showed that V. viviparus was not a strict generalist: it tended to be more efficient to constitute energy reserves when feeding on algae under laboratory conditions and its energy stores were positively correlated with primary productivity of the benthic biofilm in the field. Despite this higher efficiency of V. viviparus to produce energy reserves from algal resources, the survival and the levels of energy reserves measured on the field, even when trophic conditions were the harshest (low algal development), make this species a good candidate for ecological engineering approaches.


Trophic strategy Ecological engineering Biofilm Physiological state Gastropod Algae 



We express our gratitude to Pauline Barbe and Mélissa Tenaille for their help during the collection of organisms and the experimentation, and to Laurent Simon and Félix Vallier who were involved in chemical analyses. Our thanks also go to Météo-France and Eau du Grand Lyon for the data they provided. This research was done on the Research Platform of Crépieux-Charmy (Plateforme de Recherche de Crépieux-Charmy) and received financial and technical support from the Lyon Metropole and Veolia Water (Eau du Grand Lyon).

Author contributions

All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Jean-Bastien Gambonnet, Laurence Volatier, Florian Mermillod-Blondin, Frédéric Hervant and Valerian Estragnat. The first draft of the manuscript was written by Valerian Estragnat, Florian Mermillod-Blondin and Laurence Volatier. All authors contributed critically to the drafts and gave final approval for publication.


This study was funded by the Lyon Metropole and Veolia Water (Eau du Grand Lyon).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national and/or institutional guidelines for the care and use of animals were followed.

Supplementary material

10750_2019_4128_MOESM1_ESM.docx (95 kb)
Supplementary material 1 (DOCX 94 kb)


  1. Barclay, M. C., W. Dall & D. M. Smith, 1983. Changes in lipid and protein during starvation and the moulting cycle in the tiger prawn, Penaeus esculentus Haswell. Journal of Experimental Marine Biology and Ecology 68: 229–244.CrossRefGoogle Scholar
  2. Barranguet, C., B. Veuger, S. A. M. Van Beusekom, P. Marvan, J. J. Sinke & W. Admiraal, 2005. Divergent composition of algal-bacterial biofilms developing under various external factors. European Journal of Phycology 40: 1–8.CrossRefGoogle Scholar
  3. Bellinger, B. J., M. R. Gretz, D. S. Domozych, S. N. Kiemle & S. E. Hagerthey, 2010. Composition of extracellular polymeric substances from periphyton assemblages in the florida everglades. Journal of Phycology 46: 484–496.CrossRefGoogle Scholar
  4. Bolnick, D. I., R. Svanbäck, J. A. Fordyce, L. H. Yang, J. M. Davis, C. D. Hulsey & M. L. Forister, 2003. The ecology of individuals: incidence and implications of individual specialization. The American Naturalist 161: 1–28.CrossRefGoogle Scholar
  5. Calow, P., 1975. The feeding strategies of two freshwater gastropods, Ancylus fluviatilis Müll. and Planorbis contortus Linn. (Pulmonata), in terms of ingestion rates and absorption efficiencies. Oecologia 20: 33–49.CrossRefGoogle Scholar
  6. Carpenter, S., J. Kitchell & J. Hodgson, 1985. Cascading trophic interactions and lake productivity. BioScience 35: 634–639.CrossRefGoogle Scholar
  7. Clavel, J., R. Julliard & V. Devictor, 2011. Worldwide decline of specialist species: toward a global functional homogenization?. Frontiers in ecology and the environment. Wiley-Blackwell, New York: 222–228.Google Scholar
  8. Cook, P. M., 1949. A ciliary feeding mechanism in Viviparus viviparus (L.). Journal of Molluscan Studies 27: 265–271.Google Scholar
  9. Costa, O. Y. A., J. M. Raaijmakers & E. E. Kuramae, 2018. Microbial extracellular polymeric substances: ecological function and impact on soil aggregation. Frontiers in Microbiology 9: 1696.CrossRefGoogle Scholar
  10. Cruz-Rivera, E. & M. E. Hay, 2001. Macroalgal traits and the feeding and fitness of an herbivorous amphipod: the roles of selectivity, mixing, and compensation. Marine Ecology Progress Series 218: 249–266.CrossRefGoogle Scholar
  11. Decho, A. W., 1990. Microbial exopolymer secretions in ocean environments: their role (s) in food webs and marine processes. Oceanography and Marine Biology 28: 9–16.Google Scholar
  12. Decho, A. W. & D. J. W. Moriarty, 1990. Bacterial exopolymer utilization by a harpacticoid copepod: a methodology and results. Limnology and Oceanography 35: 1039–1049.CrossRefGoogle Scholar
  13. Devictor, V., J. Clavel, R. Julliard, S. Lavergne, D. Mouillot, W. Thuiller, P. Venail, S. Villéger & N. Mouquet, 2010. Defining and measuring ecological specialization. Journal of Applied Ecology 47: 15–25.CrossRefGoogle Scholar
  14. Devictor, V., R. Julliard, J. Clavel, F. Jiguet, A. Lee & D. Couvet, 2008. Functional biotic homogenization of bird communities in disturbed landscapes. Global Ecology and Biogeography 17: 252–261.CrossRefGoogle Scholar
  15. Elendt, B. P., 1989. Effects of starvation on growth, reproduction, survival and biochemical composition of Daphnia magna. Archiv für Hydrobiologie 116: 415–433.Google Scholar
  16. Estragnat, V., F. Mermillod-Blondin, M. Jully, D. Lemoine, L. Lassabatere & L. Volatier, 2018. Does the efficiency of grazer introduction to restore and preserve the hydraulic performance of infiltration basins depend on the physical and biological characteristics of the infiltration media? Ecological Engineering 116: 127–132.CrossRefGoogle Scholar
  17. Fang, F., W. T. Lu, Q. Shan & J. S. Cao, 2014. Characteristics of extracellular polymeric substances of phototrophic biofilms at different aquatic habitats. Carbohydrate Polymers 106: 1–6.CrossRefGoogle Scholar
  18. Fink, P. & E. Von Elert, 2006. Physiological responses to stoichiometric constraints: nutrient limitation and compensatory feeding in a freshwater snail. Oikos 115: 484–494.CrossRefGoogle Scholar
  19. Flores, L., A. Larrañaga & A. Elosegi, 2013. Compensatory feeding of a stream detritivore alleviates the effects of poor food quality when enough food is supplied. Freshwater Science 33: 134–141.CrossRefGoogle Scholar
  20. Futuyma, D. J. & G. Moreno, 1988. The evolution of ecological specialization. Annual Review of Ecology and Systematics 19: 207–233.CrossRefGoogle Scholar
  21. Gette-Bouvarot, M., F. Mermillod-Blondin, R. Angulo-Jaramillo, C. Delolme, D. Lemoine, L. Lassabatere, S. Loizeau & L. Volatier, 2014. Coupling hydraulic and biological measurements highlights the key influence of algal biofilm on infiltration basin performance. Ecohydrology 7: 950–964.CrossRefGoogle Scholar
  22. Gette-Bouvarot, M., L. Volatier, L. Lassabatere, D. Lemoine, L. Simon, C. Delolme & F. Mermillod-Blondin, 2015. Ecological engineering approaches to improve hydraulic properties of infiltration basins designed for groundwater recharge. Environmental Science & Technology 49: 9936–9944.CrossRefGoogle Scholar
  23. Graça, M. A. S., L. Maltby & P. Calow, 1993. Importance of fungi in the diet of Gammarus pulex and Asellus aquaticus I: feeding strategies. Oecologia 93: 139–144.CrossRefGoogle Scholar
  24. Grasshoff, K., M. Ehrdardt & K. Kremling, 1983. Methods of seawater analysis. Verlag Chemie, Berlin.Google Scholar
  25. Groendahl, S. & P. Fink, 2016. The effect of diet mixing on a nonselective herbivore. PLoS ONE 11: e0158924.CrossRefGoogle Scholar
  26. Gust, M., T. Buronfosse, O. Geffard, M. Coquery, R. Mons, K. Abbaci, L. Giamberini & J. Garric, 2011. Comprehensive biological effects of a complex field poly-metallic pollution gradient on the New Zealand mudsnail Potamopyrgus antipodarum (Gray). Aquatic Toxicology 101: 100–108.CrossRefGoogle Scholar
  27. Hill, W. R., S. C. Weber & A. J. Stewart, 1992. Food limitation of two lotic grazers: quantity, quality, and size-specificity. Journal of the North American Benthological Society 11: 420–432.CrossRefGoogle Scholar
  28. Höckelmann, C. & M. Pusch, 2000. The respiration and filter-feeding rates of the snail Viviparus viviparus (Gastropoda) under simulated stream conditions. Fundamental and Applied Limnology Schweizerbart’sche Verlagsbuchhandlung 149: 553–568.CrossRefGoogle Scholar
  29. Holt, R. D., 2009. Bringing the Hutchinsonian niche into the 21st century: ecological and evolutionary perspectives. Proceedings of the National Academy of Sciences 106: 19659–19665.CrossRefGoogle Scholar
  30. Jakubik, B., 2009. Food and feeding of Viviparus viviparus (L.) (Gastropoda) in dam reservoir and river habitats. Polish Journal of Ecology 57: 321–330.Google Scholar
  31. Jakubik, B., 2012. Life strategies of Viviparidae (Gastropoda: caenogastropoda: Architaenioglossa) in various aquatic habitats: Viviparus viviparus (Linnaeus, 1758) and V. contectus (Millet, 1813). Folia Malacologica 20: 145–179.CrossRefGoogle Scholar
  32. Jakubik, B., P. Koperski & K. Lewandowski, 2014. Diversity of mollusca in lowland river-lake system: lentic versus lotic patches. Polish Journal of Ecology 62: 335.CrossRefGoogle Scholar
  33. Levins, R., 1968. Evolution in changing environments: some theoretical explorations. Princeton University Press, Princeton.Google Scholar
  34. Mermillod-Blondin, F., L. Simon, C. Maazouzi, A. Foulquier, C. Delolme & P. Marmonier, 2015. Dynamics of dissolved organic carbon (DOC) through stormwater basins designed for groundwater recharge in urban area: assessment of retention efficiency. Water Research 81: 27–37.CrossRefGoogle Scholar
  35. Murphy, J. & J. P. Riley, 1958. A single-solution method for the determination of soluble phosphate in sea water. Journal of the Marine Biological Association of United Kingdom 37: 9–14.CrossRefGoogle Scholar
  36. Poisot, T., J. D. Bever, A. Nemri, P. H. Thrall & M. E. Hochberg, 2011. A conceptual framework for the evolution of ecological specialisation. Ecology Letters 14: 841–851.CrossRefGoogle Scholar
  37. Rizzo, W. M., S. K. Dailey, G. J. Lackey, R. R. Christian, B. E. Berry & R. L. Wetzel, 1996. A metabolism-based trophic index for comparing the ecological values of shallow-water sediment habitats. Estuaries 19: 247–256.CrossRefGoogle Scholar
  38. Staats, N., L. J. Stal, B. De Winder & L. R. Mur, 2000. Oxygenic photosynthesis as driving process in exopolysaccharide production of benthic diatoms. Marine Ecology Progress Series 193: 261–269.CrossRefGoogle Scholar
  39. Stewart, T. J., J. Traber, A. Kroll, R. Behra & L. Sigg, 2013. Characterization of extracellular polymeric substances (EPS) from periphyton using liquid chromatography-organic carbon detection-organic nitrogen detection (LC-OCD-OND). Environmental Science and Pollution Research 20: 3214–3223.CrossRefGoogle Scholar
  40. Tsvetkov, I. L., A. P. Popov & A. S. Konichev, 2003. Acid phosphatase complex from the freshwater Snail Viviparus viviparus L. under standard conditions and intoxication by cadmium ions. Biochemistry (Moscow) 68: 1327–1334.CrossRefGoogle Scholar
  41. UNESCO, 1966. Determination of photosynthetic pigments in sea water. Report Scor-Unesco. Working paper 17, Monographs on Oceanographic Methodology.Google Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Univ Lyon, Université Claude Bernard Lyon 1, CNRS, ENTPE, UMR5023, Écologie des Hydrosystèmes Naturels et AnthropisésVilleurbanneFrance

Personalised recommendations