, Volume 738, Issue 1, pp 49–59 | Cite as

The response of two submerged macrophytes and periphyton to elevated temperatures in the presence and absence of snails: a microcosm approach

Primary Research Paper


Global warming may affect snail–periphyton–macrophyte relationships in lakes with implications also for water clarity. We conducted a 40-day aquaria experiment to elucidate the response of submerged macrophytes and periphyton on real and artificial plants to elevated temperatures (3°C) under eutrophic conditions, with and without snails present. With snails, the biomass and length of Vallisneria spinulosa leaves increased more at the high temperature, and at both temperatures growth was higher than in absence of snails. The biomass of periphyton on V. spinulosa as well as on artificial plants was higher at the highest temperature in the absence but not in the presence of snails. The biomass of Potamogeton crispus (in a decaying state) declined in all treatments and was not affected by temperature or snails. While total snail biomass did not differ between temperatures, lower abundance of adults (size >1 cm) was observed at the high temperatures. We conclude that the effect of elevated temperature on the snail–periphyton–macrophyte relationship in summer differs among macrophyte species in active growth or senescent species in subtropical lakes and that snails, when abundant, improve the chances of maintaining actively growing macrophytes under eutrophic conditions, and more so in a warmer future with potentially denser growth of periphyton.


Snail–periphyton–macrophyte relationship Elevated temperature Freshwater ecosystem Submerged macrophyte 


  1. Atkinson, D., 1994. Temperature and organism size – a biological law for ectotherms? Advances in Ecological Research 25: 1–58.CrossRefGoogle Scholar
  2. Brönmark, C., 1985. Interactions between macrophytes, epiphytes and herbivores: an experimental approach. Oikos 45: 26–30.CrossRefGoogle Scholar
  3. Brönmark, C., 1989. Interactions between epiphytes, macrophytes and freshwater snails: a review. Journal of Molluscan Studies 55: 299–311.CrossRefGoogle Scholar
  4. Brönmark, C., 1994. Effects of tench and perch on interactions in a freshwater, benthic food chain. Ecology 75: 1818–1828.CrossRefGoogle Scholar
  5. Brönmark, C. & J. E. Vermaat, 1998. Complex Fish–Snail–Epiphyton Interactions and Their Effects on Submerged Freshwater Macrophytes. The Structuring Role of Submerged Macrophytes in Lakes. Springer, New York: 47–68.CrossRefGoogle Scholar
  6. Brönmark, C., S. P. Klosiewski & R. A. Stein, 1992. Indirect effects of predation in a freshwater, benthic food chain. Ecology 73: 1662–1674.CrossRefGoogle Scholar
  7. Carlsson, N. O., C. Brönmark & L. A. Hansson, 2004. Invading herbivory: the golden apple snail alters ecosystem functioning in Asian wetlands. Ecology 85: 1575–1580.CrossRefGoogle Scholar
  8. Cattaneo, A. & J. Kalff, 1986. The effect of grazer size manipulation on periphyton communities. Oecologia 69: 612–617.CrossRefGoogle Scholar
  9. Dillon, R. T., 2000. The Ecology of Freshwater Molluscs. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
  10. González-Bergonzoni, I., M. Meerhoff, T. A. Davidson, F. Teixeira-de Mello, A. Baattrup-Pedersen & E. Jeppesen, 2012. Meta-analysis shows a consistent and strong latitudinal pattern in fish omnivory across ecosystems. Ecosystems 15: 492–503.CrossRefGoogle Scholar
  11. Guariento, R. D., A. Caliman, F. A. Esteves, R. L. Bozelli, A. Enrich-Prast & V. F. Farjalla, 2009. Substrate influence and temporal changes on periphytic biomass accrual and metabolism in a tropical humic lagoon. Limnologica 39: 209–218.CrossRefGoogle Scholar
  12. Hough, R. A., M. D. Fornwall, B. J. Negele, R. L. Thompson & D. A. Putt, 1989. Plant community dynamics in a chain of lakes: principal factors in the decline of rooted macrophytes with eutrophication. Hydrobiologia 173: 199–217.CrossRefGoogle Scholar
  13. Huang, X. F., W. M. Chen & Q. M. Cai, 1999. Survey, observation and analysis of lake ecology. Standard Methods for Observation and Analysis in Chinese Ecosystem Research Network, Series V. Standards Press of China, Beijing (in Chinese).Google Scholar
  14. Jeppesen, E., T. L. Lauridsen, T. Kairesalo & M. R. Perrow, 1998. Impact of submerged macrophytes on fish–zooplankton interactions in lakes. The Structuring Role of Submerged Macrophytes in Lakes. Springer, New York: 91–114.Google Scholar
  15. Jones, J. I. & C. D. Sayer, 2003. Does the fish–invertebrate–periphyton cascade precipitate plant loss in shallow lakes? Ecology 84: 2155–2167.CrossRefGoogle Scholar
  16. Kishi, D., M. Murakami, S. Nakano & K. Maekawa, 2005. Water temperature determines strength of top–down control in a stream food web. Freshwater Biology 50: 1315–1322.CrossRefGoogle Scholar
  17. Kosten, S., E. Jeppesen, V. L. M. Huszar, N. Mazzeo, E. H. Van Nes, E. T. H. M. Peeters & M. Scheffer, 2011. Ambiguous climate impacts on competition between submerged macrophytes and phytoplankton in shallow lakes. Freshwater Biology 56: 1540–1553.CrossRefGoogle Scholar
  18. Köhler, J., J. Hachoł & S. Hilt, 2010. Regulation of submersed macrophyte biomass in a temperate lowland river: interactions between shading by bank vegetation, epiphyton and water turbidity. Aquatic Botany 92: 129–136.CrossRefGoogle Scholar
  19. Li, K. Y., Z. W. Liu, Y. H. Hu & H. W. Yang, 2009. Snail herbivory on submerged macrophytes and nutrient release: implications for macrophyte management. Ecological Engineering 35: 1664–1667.CrossRefGoogle Scholar
  20. Lodge, D. M., 1991. Herbivory on freshwater macrophytes. Aquatic Botany 41: 195–224.CrossRefGoogle Scholar
  21. McKee, D., K. Hatton, J. W. Eaton, D. Atkinson, A. Atherton, I. Harvey & B. Moss, 2002. Effects of simulated climate warming on macrophytes in freshwater microcosm communities. Aquatic Botany 74: 71–83.CrossRefGoogle Scholar
  22. Meerhoff, M., C. Iglesias, F. T. De Mello, J. M. Clemente, E. Jensen, T. L. Lauridsen & E. Jeppesen, 2007. Effects of habitat complexity on community structure and predator avoidance behaviour of littoral zooplankton in temperate versus subtropical shallow lakes. Freshwater Biology 52: 1009–1021.CrossRefGoogle Scholar
  23. Moss, B., 1990. Engineering and biological approaches to the restoration from eutrophication of shallow lakes in which aquatic plant communities are important components. Biomanipulation Tool for Water Management, Springer: 367–377.Google Scholar
  24. Moss, B., S. Kosten, M. Meerhoff, R. W. Battarbee, E. Jeppesen, N. Mazzeo, K. Havens, G. Lacerot, Z. W. Liu, L. De Meester, H. Paerl & M. Scheffer, 2011. Allied attack: climate change and eutrophication. Inland Waters 1: 101–105.CrossRefGoogle Scholar
  25. Nicolle, A., P. Hallgren, J. Von Einem, E. S. Kritzberg, W. Graneli, A. Persson, C. Brönmark & L. A. Hansson, 2012. Predicted warming and browning affect timing and magnitude of plankton phenological events in lakes: a mesocosm study. Freshwater Biology 57: 684–695.CrossRefGoogle Scholar
  26. Patrick, D. A., N. Boudreau, Z. Bozic, G. S. Carpenter, D. M. Langdon, S. R. LeMay, S. M. Martin, R. M. Mourse, S. L. Prince & K. M. Quinn, 2012. Effects of climate change on late-season growth and survival of native and non-native species of watermilfoil (Myriophyllum spp.): implications for invasive potential and ecosystem change. Aquatic Botany 103: 83–88.CrossRefGoogle Scholar
  27. Phillips, G., D. Eminson & B. Moss, 1978. A mechanism to account for macrophyte decline in progressively eutrophicated freshwaters. Aquatic Botany 4: 103–126.CrossRefGoogle Scholar
  28. Roberts, E., J. Kroker, S. Körner & A. Nicklisch, 2003. The role of periphyton during the re-colonization of a shallow lake with submerged macrophytes. Hydrobiologia 506: 525–530.CrossRefGoogle Scholar
  29. Rogers, K. & C. Breen, 1980. Growth and reproduction of Potamogeton crispus in a South African lake. Journal of Ecology 68: 561–571.CrossRefGoogle Scholar
  30. Rooney, N. & J. Kalff, 2000. Inter-annual variation in submerged macrophyte community biomass and distribution: the influence of temperature and lake morphometry. Aquatic Botany 68: 321–335.CrossRefGoogle Scholar
  31. Saitoh, M., K. Narita & S. Isikawa, 1970. Photosynthetic nature of some aquatic plants in relation to temperature. Botanical Magazine Tokyo 83: 10–12.CrossRefGoogle Scholar
  32. Scheffer, M., S. H. Hosper, M. L. Meijer, B. Moss & E. Jeppesen, 1993. Alternative equilibria in shallow lakes. Trends in Ecology & Evolution 8: 275–279.CrossRefGoogle Scholar
  33. Schriver, P., J. Bøgestrand, E. Jeppesen & M. Søndergaard, 1995. Impact of submerged macrophytes on fish–zooplanl phytoplankton interactions: large-scale enclosure experiments in a shallow eutrophic lake. Freshwater Biology 33: 255–270.CrossRefGoogle Scholar
  34. Sheridan, J. A. & D. Bickford, 2011. Shrinking body size as an ecological response to climate change. Nature Climate Change 1: 401–406.CrossRefGoogle Scholar
  35. Shurin, J. B., J. L. Clasen, H. S. Greig, P. Kratina & P. L. Thompson, 2012. Warming shifts top–down and bottom–up control of pond food web structure and function. Philosophical Transactions of the Royal Society B: Biological Sciences 367: 3008–3017.CrossRefGoogle Scholar
  36. Solomon, S., D. Qin, M. Manning, Z. Chen, M. Marquis, K. B. Averyt, M. Tignor & H. L. Miller, 2007. Climate Change 2007: The Physical Science Basis, Contribution of Working Group 1 to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press.Google Scholar
  37. Strand, J. A. & S. E. Weisner, 2001. Morphological plastic responses to water depth and wave exposure in an aquatic plant (Myriophyllum spicatum). Journal of Ecology 89: 166–175.CrossRefGoogle Scholar
  38. Tarkowska-Kukuryk, M. & T. Mieczan, 2012. Effect of substrate on periphyton communities and relationships among food web components in shallow hypertrophic lake. Journal of Limnology 71: 279–290.CrossRefGoogle Scholar
  39. Thomas, J. D., 1990. Mutualistic interactions in freshwater modular systems with molluscan components. Advances in Ecological Research 20: 125–178.CrossRefGoogle Scholar
  40. Titus, J. E. & M. S. Adams, 1979. Coexistence and the comparative light relations of the submersed macrophytes Myriophyllum spicatum L. and Vallisneria americana Michx. Oecologia 40: 273–286.CrossRefGoogle Scholar
  41. Trochine, C., M. E. Guerrieri, L. Liboriussen, T. L. Lauridsen & E. Jeppesen, 2014. Effects of nutrient loading, temperature regime and grazing pressure on nutrient limitation of periphyton in experimental ponds. Freshwater Biology 59: 905–917.CrossRefGoogle Scholar
  42. Underwood, G. J. C., J. D. Thomas & J. H. Baker, 1992. An experimental investigation of interactions in snail–macrophyte–epiphyte systems. Oecologia 91: 587–595.CrossRefGoogle Scholar
  43. Van Dijk, G. M., 1993. Dynamics and attenuation characteristics of periphyton upon artificial substratum under various light conditions and some additional observations on periphyton upon Potamogeton pectinatus L. Hydrobiologia 252: 143–161.CrossRefGoogle Scholar
  44. Wang, C., S. H. Zhang, P. F. Wang, J. Hou, W. Li & W. J. Zhang, 2008. Metabolic adaptations to ammonia-induced oxidative stress in leaves of the submerged macrophyte Vallisneria natans (Lour.) Hara. Aquatic Toxicology 87: 88–98.PubMedCrossRefGoogle Scholar
  45. Wang, H. J., B. Z. Pan, X. M. Liang & H. Z. Wang, 2006. Gastropods on submersed macrophytes in Yangtze lakes: community characteristics and empirical modelling. International Review of Hydrobiology 91: 521–538.CrossRefGoogle Scholar
  46. Wang, H. J., H. Z. Wang, X. M. Liang & S. K. Wu, 2014. Total phosphorus thresholds for regime shifts are nearly equal in subtropical and temperate shallow lakes with moderate depths and areas. Freshwater Biology. doi:10.1111/fwb.12372.Google Scholar
  47. Wojdak, J. M., 2005. Relative strength of top–down, bottom–up, and consumer species richness effects on pond ecosystems. Ecological Monographs 75: 489–504.CrossRefGoogle Scholar
  48. Wu, S. K., P. Xie, G. D. Liang, S. B. Wang & X. M. Liang, 2006. Relationships between microcystins and environmental parameters in 30 subtropical shallow lakes along the Yangtze River, China. Freshwater Biology 51: 2309–2319.CrossRefGoogle Scholar
  49. Xiong, W., D. Yu, Q. Wang, C. Liu & L. Wang, 2008. A snail prefers native over exotic freshwater plants: implications for the enemy release hypotheses. Freshwater Biology 53: 2256–2263.Google Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  1. 1.Key Laboratory of Aquatic Botany and Watershed Ecology, Wuhan Botanical GardenChinese Academy of SciencesWuhanChina
  2. 2.Department of BioscienceAarhus UniversitySilkeborgDenmark
  3. 3.Sino-Danish Centre for Education and Research (SDC)BeijingChina
  4. 4.Hubei Key Laboratory of Wetland Evolution & Ecological Restoration, Wuhan Botanical GardenChinese Academy of SciencesWuhanChina
  5. 5.University of Chinese Academy of SciencesBeijingChina

Personalised recommendations