, Volume 760, Issue 1, pp 145–158 | Cite as

Deleterious interaction of light impairment and organic matter enrichment on Isoetes lacustris (Lycopodiophyta, Isoetales)

  • Eglantine Chappuis
  • Ana Lumbreras
  • Enric Ballesteros
  • Esperança Gacia
Primary Research Paper


Light reduction and increased organic matter load often occur together in lakes undergoing eutrophication. We aimed at experimentally testing the relative importance of light availability, organic matter enrichment and their interactions in the collapse of healthy populations of Isoetes lacustris. We conducted an in situ shading (65 and 35% of incident light) and organic matter enrichment (10% enrichment) experiment in a Pyrenean pond (NE Spain). We followed plant performance using growth indicators, carbon balance indicators and individual survival. Severe light reduction (35%) resulted in a lengthening of the new leaves and no effects on mortality. Organic matter enrichment resulted in lower production and increased individual mortality. The combination of both stresses resulted in stronger negative effects and the highest mortality rate, which helps explaining I. lacustris die-offs observed after damming. Under severe light reduction (35%), plants used corm starch to keep growing. Consequently, starch percentage decreased and sucrose percentage increased as it was transported to the growing leaves. The most extreme changes were observed under severe light reduction and fertilization, which extremely increased the ratio between sucrose and total non-structural carbohydrates (TNC). Thus, I. lacustris sucrose:TNC ratio is a good indicator of light reduction and organic matter enrichment stresses.


Nutrient enrichment Carbohydrate Oligotrophic soft-water lakes Sucrose Starch Aquatic macrophytes 



EG and EC are members of the Environmental Changes Ecology Group (GECA), an Excellence Research Group (SGR-DGR) of the Generalitat de Catalunya (Ref. 2014 SGR 1249. 2014–2017). This study was funded by the Red de Parques Nacionales of the Spanish Ministry of the Environment (ref. 118/2003) and Intramural CSIC (Consejo Superior de Investigaciones Científicas) ref. 0065. We are thankful to Jonatan Ortiz for his help in field work.


  1. Abeli, T., E. Barni, C. Siniscalco, C. Amosso & G. Rossi, 2012. A cost-effective model for preliminary site evaluation for the reintroduction of a threatened quillwort. Aquatic Conservation-Marine and Freshwater Ecosystems 22: 66–73.CrossRefGoogle Scholar
  2. Alcoverro, T., R. C. Zimmerman, D. G. Kohrs & R. S. Alberte, 1999. Resource allocation and sucrose mobilization in light-limited eelgrass Zostera marina. Marine Ecology Progress Series 187: 121–131.CrossRefGoogle Scholar
  3. Alcoverro, T., M. Manzanera & J. Romero, 2001. Annual metabolic carbon balance of the seagrass Posidonia oceanica: the importance of carbohydrate reserves. Marine Ecology Progress Series 211: 105–116.CrossRefGoogle Scholar
  4. Almestrand, A. & A. Lundh, 1951. Studies on the vegetation and hydrochemistry of Scanian Lakes I–III. C.W.K. Gleerups Forlag, Lund.Google Scholar
  5. Arts, G. H. P., 2002. Deterioration of Atlantic soft water macrophyte communities by acidification, eutrophication and alkalinisation. Aquatic Botany 73: 373–393.CrossRefGoogle Scholar
  6. Baastrup-Spohr, L., L. L. Iversen, J. Dahl-Nielsen & K. Sand-Jensen, 2013. Seventy years of changes in the abundance of Danish charophytes. Freshwater Biology 58: 1682–1693.CrossRefGoogle Scholar
  7. Ballesteros, E., E. Gacia & L. Camarero, 1989. Composition, distribution and biomass of benthic macrophyte communities from an alpine lake in Central Pyrenees: the lake Baciver. Annals Limnologie 25: 177–184.CrossRefGoogle Scholar
  8. Barko, J. W. & R. M. Smart, 1983. Effects of organic matter additions to sediment on the growth of aquatic plants. Journal of Ecology 71: 161–175.CrossRefGoogle Scholar
  9. Barko, J. W. & R. M. Smart, 1986. Sediment related mechanisms of growth limitation in submersed macrophytes. Ecology 67: 1328–1340.CrossRefGoogle Scholar
  10. Bond, T., D. Sear & T. Sykes, 2014. Estimating the contribution of in-stream cattle faeces deposits to nutrient loading in an English Chalk stream. Agricultural Water Management 131: 156–162.CrossRefGoogle Scholar
  11. Bornette, G. & S. Puijalon, 2011. Response of aquatic plants to abiotic factors: a review. Aquatic Sciences 73: 1–14.CrossRefGoogle Scholar
  12. Brock, W. A. & D. Starrett, 2003. Managing systems with non-convex positive feedback. Environmental & Resource Economics 26: 575–602.CrossRefGoogle Scholar
  13. Brouewer, E. & J. G. M. Roelofs, 2001. Degraded soft-water lakes: possibilities for restauration. Restauration Ecology 9: 155–166.CrossRefGoogle Scholar
  14. Burkholder, J. M., K. M. Mason & H. B. Glasgow, 1992. Water-column nitrate enrichment promotes decline of eelgrass Zostera marina; evidence from a seasonal mesocosm experiment. Marine Ecology Progress Series 81: 163–178.CrossRefGoogle Scholar
  15. Camarero, L. & J. Catalan, 2012. Atmospheric phosphorus deposition may cause lakes to revert from phosphorous limitation back to nitrogen limitation. Nature Communications 3: 118.CrossRefGoogle Scholar
  16. Camargo, J. A., A. Alonso & M. de la Puente, 2005. Eutrophication downstream from small reservoirs in mountain rivers of Central Spain. Water Research 39: 3376–3384.CrossRefPubMedGoogle Scholar
  17. Catalan, J., L. Camarero, E. Gacia, E. Ballesteros & M. Felip, 1994. Nitrogen in the Pyrenean lakes (Spain). Hydrobiologia 274: 17–27.CrossRefGoogle Scholar
  18. Chappuis, E., E. Gacia & E. Ballesteros, 2011. Changes in aquatic macrophyte flora over the last century in Catalan water bodies (NE Spain). Aquatic Botany 95: 268–277.CrossRefGoogle Scholar
  19. Chappuis, E., E. Gacia & E. Ballesteros, 2014. Environmental factors explaining the distribution and diversity of vascular aquatic macrophytes in a highly heterogeneous Mediterranean region. Aquatic Botany 113: 72–82.CrossRefGoogle Scholar
  20. Croel, R. C. & J. M. Kneitel, 2011. Cattle waste reduces plant diversity in vernal pool mesocosms. Aquatic Botany 95: 140–145.CrossRefGoogle Scholar
  21. Farmer, A. M. & D. H. N. Spence, 1987. Environmental control of the seasonal growth of the submersed aquatic macrophyte Lobelia dortmanna L. New Phytologist 106: 289–299.Google Scholar
  22. Gacia, E., 1992. Ecologia dels macròfits submergits dels estanys del Pirineu: estructura i dinàmica de les poblacions de l’Estany Baciver (Vall d’Aran). University of Barcelona, Barcelona. Doctoral Thesis.Google Scholar
  23. Gacia, E. & E. Ballesteros, 1993a. Diel acid fluctuations in Pyrenean Isoetes species – The effects of seasonality and emersion. Archiv für Hydrobiologie 128: 187–196.Google Scholar
  24. Gacia, E. & E. Ballesteros, 1993b. Population and individual variability of Isoetes lacustris L. with depth in a Pyrenean lake. Aquatic Botany 46: 35–47.CrossRefGoogle Scholar
  25. Gacia, E. & E. Ballesteros, 1994. Production of Isoetes lacustris in a Pyrenean lake: seasonality and ecological factors involved in the growing period. Aquatic Botany 48: 77–89.CrossRefGoogle Scholar
  26. Gacia, E. & E. Ballesteros, 1996. The effect of increased water level on Isoetes lacustris L in Lake Baciver, Spain. Journal of Aquatic Plant Management 34: 57–59.Google Scholar
  27. Gacia, E. & E. Ballesteros, 1998. Effects of building up a dam in a shallow high mountain lake (Baciver, Central Pyrenees). Oecologia Aquatica 11: 55–66.Google Scholar
  28. Gacia, E., E. Ballesteros, L. Camarero, O. Delgado, A. Palau, J. L. Riera & J. Catalan, 1994. Macrophytes from lakes in the eastern Pyrenees: community composition and ordination in relation to environmental factors. Freshwater Biology 32: 73–81.CrossRefGoogle Scholar
  29. Gacia, E., E. Chappuis, A. Lumbreras, J. L. Riera & E. Ballesteros, 2009. Functional diversity of macrophyte communities within and between Pyrenean lakes. Journal of Limnology 68: 25–36.CrossRefGoogle Scholar
  30. Gacia, E., N. Marbà, J. Cebrián, R. Vaquer-Sunyer, N. Garcias-Bonet & C. M. Duarte, 2012. Thresholds of irradiance for seagrass (Posidonia oceanica) meadow metabolism: an experimental approach. Marine Ecology Progress Series 466: 69–79.Google Scholar
  31. Gao, H., J. Cai, W. Han, H. Huai, Y. Chen & C. Wei, 2014. Comparison of starches isolated from three different Trapa species. Food Hydrocolloids 37: 174–181.CrossRefGoogle Scholar
  32. Hautier, Y., P. A. Niklaus & A. Hector, 2009. Competition for light causes plant biodiversity loss after eutrophication. Science 324: 636–638.CrossRefPubMedGoogle Scholar
  33. Hickey, R. J., 1986. Isoetes megaspore surface morphology: nomenclature, variation and systematic importance. American Fern Journal 76: 1–16.CrossRefGoogle Scholar
  34. Holmer, M., H. S. Jensen, K. K. Christiensen, C. Wigand & F. O. Andersen, 1998. Sulfate reduction in lake sediments inhabited by the isoetid macrophytes Littorella uniflora and Isoetes lacustris. Aquatic Botany 60: 307–324.CrossRefGoogle Scholar
  35. Hussner, A., H. P. Hoelken & P. Jahns, 2010. Low light acclimated submerged freshwater plants show a pronounced sensitivity to increasing irradiances. Aquatic Botany 93: 17–24.CrossRefGoogle Scholar
  36. Hutchinson, G. E., 1975. A Treatise on Limnology. Limnological Botany. Wiley, New York.Google Scholar
  37. Jones, C. G., J. H. Lawron & M. Shachak, 1994. Organisms as ecosystem engineers. Oikos 69: 373–386.CrossRefGoogle Scholar
  38. Keeley, J. E., 1998. CAM photosynthesis in submerged aquatic plants. Botanical Review 64: 121–175.CrossRefGoogle Scholar
  39. Keeley, J. E., C. M. Walker & R. P. Mathews, 1983. Crassulacean acid metabolism in Isoetes bolanderi in high elevation oligotrophic lakes. Oecologia 58: 63–69.CrossRefGoogle Scholar
  40. Klimes, L., J. Klimesova & H. Cizkova, 1999. Carbohydrate storage in rhizomes of Phragmites australis: the effects of altitude and rhizome age. Aquatic Botany 64: 105–110.CrossRefGoogle Scholar
  41. Koch, K. E., 1996. Carbohydrate-modulated gene expression in plants. Annual Review of Plant Physiology and Plant Molecular Biology 47: 509–540.CrossRefPubMedGoogle Scholar
  42. Kovach, C. W., J. P. Kurdziel, R. Bowman, J. Wagner & J. M. Lawrence, 1992. The effects of stress and disturbance on proximate composition, allocation of production, photosynthesis, respiration, and chlorophyll levels in Hygrophila polysperma (Roxb.) Anders. (Acanthaceae). Environmental and Experimental Botany 32: 479–486.Google Scholar
  43. Kowalewski, G. A., R. Kornijów, S. McGowan, M. Woszczyk, M. Suchora, K. Bałaga, A. Kaczorowska, M. Gąsiorowski, K. Szeroczyńska & A. Wasiłowska, 2013. Persistence of protected, vulnerable macrophyte species in a small, shallow eutrophic lake (eastern Poland) over the past two centuries: Implications for lake management and conservation. Aquatic Botany 106: 1–13.CrossRefGoogle Scholar
  44. Kraska, M., P. Klimaszyk & R. Piotrowicz, 2013. Anthropogenic changes in properties of the water and spatial structure of the vegetation of the Lobelia lake Lake Modre in the Bytw Lakeland. Oceanological and Hydrobiological Studies 42: 302–313.CrossRefGoogle Scholar
  45. Lavery, P. S., K. McMahon, M. Mulligan & A. Tennison, 2009. Interactive effects of timing, duration of experimental shading on Amphibolis griffithii. Marine Ecology Progress Series 394: 21–33.CrossRefGoogle Scholar
  46. Levin, S. A., 2009. The Princeton Guide to Ecology. Princeton University Press, Princeton.CrossRefGoogle Scholar
  47. Madsen, T. V., B. Olesen & J. Bagger, 2002. Carbon acquisition and carbon dynamics by aquatic isoetids. Aquatic Botany 73: 351–371.CrossRefGoogle Scholar
  48. Marbà, N., M. A. Hemminga, M. A. Mateo, C. M. Duarte, Y. E. M. Mass, J. Terrados & E. Gacia, 2002. Carbon and nitrogen translocation between seagrass ramets. Marine Ecology Progress Series 226: 287–300.CrossRefGoogle Scholar
  49. Moss, B., E. Jeppesen, M. Sondergaard, T. Lauridsen & Z. W. Liu, 2013. Nitrogen, macrophytes, shallow lakes and nutrient limitation: resolution of a current controversy? Hydrobiologia 710: 3–21.CrossRefGoogle Scholar
  50. Murphy, K. J., 2002. Plant communities and plant diversity in soft-water lakes of northern Europe. Aquatic Botany 73: 28–324.CrossRefGoogle Scholar
  51. Muztar, A. J., S. J. Slinger & J. H. Burton, 1979. Chemical composition of aquatic macrophytes. IV. Carotenoids, soluble sugars and starch in relation to their pigmenting, and ensiling potential. Canadian Journal of Plant Science 59: 1093–1098.CrossRefGoogle Scholar
  52. Owens, C. S. & J. D. Madsen, 1998. Phenological studies of carbohydrate allocation in Hydrilla. Journal of Aquatic Plant Management 36: 40–44.Google Scholar
  53. Pearsall, W. H., 1920. The aquatic vegetation of the English lakes. Journal of Ecology 8: 163–201.CrossRefGoogle Scholar
  54. Portielje, R. & D. T. Van der Molen, 1998. Trend-analysis of eutrophication variables in lakes in The Netherlands. Water Science and Technology 37: 235–240.CrossRefGoogle Scholar
  55. Pulich, W. M., 1986. Variation in leaf soluble amino-acids and ammonium content in subtropical seagrasses related to salinity stress. Plant Physiology 80: 283–286.PubMedCentralCrossRefPubMedGoogle Scholar
  56. Pulido, C., E. C. H. E. T. Lucassen, O. Pedersen & J. G. M. Roelofs, 2011a. Influence of quantity and lability of sediment organic matter on the biomass of two isoetids, Littorella uniflora and Echinodorus repens. Freshwater Biology 56: 939–951.CrossRefGoogle Scholar
  57. Pulido, C., D. J. H. Keijsers, E. C. H. E. T. Lucassen, O. Perdersen & J. G. M. Roelofs, 2011b. Elevated alkalinity and sulfate adversely affect the aquatic macrophyte Lobelia dortmanna. Aquatic Ecology 46: 283–295.CrossRefGoogle Scholar
  58. Pulido, C., K. Sand-Jensen, E. Lucassen, J. G. M. Roelofs, K. P. Brodersen & O. Pedersen, 2012. Improved prediction of vegetation composition in NW European softwater lakes by combining location, water and sediment chemistry. Aquatic Sciences 74: 351–360.CrossRefGoogle Scholar
  59. Riera, J. L., M. Felip, E. Chappuis, J. Tresserra, L. Camarero, 2014. Efectes de l’activitat ramadera sobre les aportacions de nitrogen als estanys del Parc Nacional d’Aigüestortes i Estany de Sant Maurici. In: La investigació al Parc Nacional d’Aigüestortes i Estany de Sant Maurici: IX Jornades sobre Recerca al Parc Nacional d’Aigüestortes i Estany de Sant Maurici. pp. 19–29.Google Scholar
  60. Risgaard-Petersen, N. & K. Jensen, 1997. Nitrification and denitrification in the rhizosphere of the aquatic macrophyte Lobelia dortmanna L. Limnology and Oceanography 42: 529–537.CrossRefGoogle Scholar
  61. Roitsch, T., 1999. Source-sink regulation by sugar and stress. Current Opinion in Plant Biology 2: 198–206.CrossRefPubMedGoogle Scholar
  62. Rorslett, B. & S. W. Johansen, 1995. Dynamic response of the submerged macrophyte, Isoetes lacustris, to alternating light levels under field conditions. Aquatic Botany 51: 223–242.CrossRefGoogle Scholar
  63. Rosa, M., C. Prado, G. Podazza, R. Interdonato, J. A. González, M. Hilal & F. E. Prado, 2009. Soluble sugars: metabolism, sensing and abiotic stress. Plant Signaling and Behavior 4: 388–393.PubMedCentralCrossRefPubMedGoogle Scholar
  64. Salgado, J., C. Sayer, L. Carvalho, T. Davidson & I. Gunn, 2010. Assessing aquatic macrophyte community change through the integration of palaeolimnological and historical data at Loch Leven, Scotland. Journal of Paleolimnology 43: 191–204.CrossRefGoogle Scholar
  65. Sand-Jensen, K., T. Riis, O. Vestergaard & S. E. Larsen, 2000. Macrophyte decline in Danish lakes and streams over the past 100 years. Journal of Ecology 88: 1030–1040.CrossRefGoogle Scholar
  66. 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
  67. Smolders, A. J. P., M. C. van Riel & J. G. M. Roelofs, 2000. Accumulation of free amino acids as an early indication for physiological stress (nitrogen overload) due to elevated ammonium levels in vital Stratiotes aloides L. stands. Archiv für Hydrobiologie 150: 169–175.Google Scholar
  68. Smolders, A. J. P., E. Lucassen & J. G. M. Roelofs, 2002. The isoetid environment: biogeochemistry and threats. Aquatic Botany 73: 325–350.CrossRefGoogle Scholar
  69. Smolders, A. J. P., L. P. M. Lamers, C. den Hartog & J. G. M. Roelofs, 2003. Mechanisms involved in the decline of Stratiotes aloides L. in The Netherlands: sulphate as a key variable. Hydrobiologia 506–509: 603–610.CrossRefGoogle Scholar
  70. Sousa, W. T. Z., S. M. Thomaz, K. J. Murphy, M. J. Silveira & R. P. Mormul, 2009. Environmental predictors of the occurrence of exotic Hydrilla verticillata (L.f.) Royle and native Egeria najas Planch. in a sub-tropical river floodplain: the Upper River Parana, Brazil. Hydrobiologia 632: 65–78.CrossRefGoogle Scholar
  71. Underwood, A. J., 1981. Techniques of analysis of variance in experimental marine biology and ecology. Oceanography and Marine Biology: an Annual Review 19: 513–605.Google Scholar
  72. Vermaat, J. E. & F. C. A. Verhagen, 1995. Freezer-independent preservation of carbohydrate samples from water plants: a methodological test. Aquatic Botany 51: 155–161.CrossRefGoogle Scholar
  73. Vöge, M., 1997. Plant size and fertility of Isoetes lacustris L in 20 lakes of Scandinavia: a field study. Archiv für Hydrobiologie 139: 171–185.Google Scholar
  74. Wallsten, M., 1981. Changes of lakes in Uppland, central Sweden, during 40 years. Uppsala Universitet, Evolutionary Biology Centre: 84.Google Scholar
  75. Xie, D., D. Yu, C. Xia & W. You, 2014. Stay dormant or escape sprouting? Turion buoyancy and sprouting abilities of the submerged macrophyte Potamogeton crispus L. Hydrobiologia 726: 43–51.CrossRefGoogle Scholar
  76. Zimmerman, R. C. & R. S. Alberte, 1995. Light availability, root anoxia and patterns of carbon allocation in the marine angiosperm Zostera marina L. (eelgrass). Plant Physiology 108: 24–24.Google Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Eglantine Chappuis
    • 1
  • Ana Lumbreras
    • 1
    • 2
  • Enric Ballesteros
    • 1
  • Esperança Gacia
    • 1
  1. 1.Centre d’Estudis Avançats de Blanes (CEAB-CSIC)BlanesSpain
  2. 2.Instituto de Ciências Agrárias e Ambientais Mediterrânicas (ICAAM)Universidade de ÉvoraÉvoraPortugal

Personalised recommendations