, Volume 817, Issue 1, pp 349–362 | Cite as

Evidence for a new regime shift between floating and submerged invasive plant dominance in South Africa

  • E. F. StrangeEmail author
  • J. M. Hill
  • J. A. Coetzee


Classical biological control for the management of floating invasive plants has been highly successful in South Africa. However, restoring ecosystem services has been compromised by a new suite of submerged invasive plants. This study proposes that biological control of floating invasive macrophytes acts as a catalyst in a regime shift between floating and submerged invasive plant dominance. Regime shifts are large and sudden changes in the structure and functioning of ecosystems. The proposed shift is driven by the rapid decomposition of floating plants and subsequent increase in availability of nutrients and light. A mesocosm experiment explored the effect of biological control on floating Pistia stratiotes L. (Araceae) upon the growth of invasive submerged Egeria densa Planch. (Hydrocharitaceae), and native submerged plant species of the same family; Lagarosiphon major (Ridl.) Moss (Hydrocharitaceae). The results revealed a cascade effect of biological control of P. stratiotes on the availability of nitrogen, resulting in increased relative growth rates and invasive capacity for E. densa. In contrast, the native L. major could not compete with healthy or damaged P. stratiotes. These findings highlight the vulnerability of South African freshwater systems to submerged plant invasions and demonstrate the importance of a more holistic approach to invasive plant management.


Macrophyte Invasion Competition Alternate stable states Biological control 



This research was funded through the Department of Environmental Affairs, Natural Resource Management Programme’s Working for Water programme. Further funding for this work was provided by the South African Research Chairs Initiative of the Department of Science and Technology and the National Research Foundation of South Africa. Thanks are extended to the staff of the Centre for Biological Control (South Africa) for their help in the building and maintenance of the experiments, particularly Rosie Mangan and Rosalie Smith for plant collection and care. The authors also thank Jordie Netten for her valuable and constructive comments on earlier drafts of this manuscript.


  1. Andersen, T., J. Carstensen, E. Hernandez-Garcia & C. M. Duarte, 2009. Ecological thresholds and regime shifts: approaches to identification. Trends in Ecology & Evolution 24: 49–57.CrossRefGoogle Scholar
  2. Barko, J. W., R. M. Smart, D. G. McFarland & R. L. Chen, 1988. Interrelationships between the growth of Hydrilla verticillata (Lf.) Royle and sediment nutrient availability. Aquatic Botany 32: 205–216.CrossRefGoogle Scholar
  3. Basson, M. S., P. H. Van Niekerk & J. A. Van Rooyen, 1997. Overview of Water Resources Availability and Utilization in South Africa. Department of Water Affairs and Forestry, Pretoria.Google Scholar
  4. Beisner, B. E., D. T. Haydon & K. Cuddington, 2003. Alternative stable states in ecology. Frontiers in Ecology and the Environment 1: 376–382.CrossRefGoogle Scholar
  5. Benton, T. G., M. Solan, J. M. Travis & S. M. Sait, 2007. Microcosm experiments can inform global ecological problems. Trends in Ecology & Evolution 22: 516–521.CrossRefGoogle Scholar
  6. Bickel, T. O. & G. P. Closs, 2008. Fish distribution and diet in relation to the invasive macrophyte Lagarosiphon major in the littoral zone of Lake Dunstan, New Zealand. Ecology of Freshwater Fish 17: 10–19.CrossRefGoogle Scholar
  7. Biggs, R., S. R. Carpenter & W. A. Brock, 2009. Turning back from the brink: detecting an impending regime shift in time to avert it. PNAS 106: 826–831.CrossRefPubMedPubMedCentralGoogle Scholar
  8. Bini, L. M., S. M. Thomaz, K. J. Murphy & A. F. M. Camargo, 1999. Aquatic macrophyte distribution in relation to water and sediment conditions in the Itaipu Reservoir, Brazil. Hydrobiologia 415: 147–154.CrossRefGoogle Scholar
  9. Brix, H. & H. H. Shierup, 1989. The use of aquatic macrophytes in water pollution control. Ambio 18: 100–107.Google Scholar
  10. Cabrera-Walsh, G., Y. Magalí Dalto, F. M. Mattioli, R. I. Carruthers & L. W. Anderson, 2013. Biology and ecology of Brazilian elodea (Egeria densa) and its specific herbivore, Hydrellia sp., in Argentina. BioControl 58: 1–15.CrossRefGoogle Scholar
  11. Cao, T., P. Xie, Z. Li, L. Ni, M. Zhang & J. Xu, 2009. Physiological stress of high NH4 + concentration in water column on the submersed macrophyte Vallisneria natans L. Bulletin of Environmental Contamination and Toxicology 82: 296–299.CrossRefPubMedGoogle Scholar
  12. Caraco, N., J. Cole, S. Findlay & C. Wigand, 2006. Vascular plants as engineers of oxygen in aquatic systems. BioScience 56: 219–225.CrossRefGoogle Scholar
  13. Carrillo, Y., A. Guarín & G. Guillot, 2006. Biomass distribution, growth and decay of Egeria densa in a tropical high mountain reservoir (NEUSA, Colombia). Aquatic Botany 85: 7–15.CrossRefGoogle Scholar
  14. Carvalheiro, L. G., Y. M. Buckley, R. Ventim, S. V. Fowler & J. Memmott, 2008. Apparent competition can compromise the safety of highly specific biocontrol agents. Ecology Letters 11: 690–700.CrossRefPubMedGoogle Scholar
  15. Center, T. D., 1994. Biological control of weeds: water hyacinth [Eichhornia crassipes] and water lettuce [Pistia stratiotes]. Food and Agriculture Organization of the United Nations. [accessed July 12 2016].
  16. Champion, P. D., & R. D. Wells, 2014. Proactive management of aquatic weeds to protect the nationally important Northland dune lakes, New Zealand. Proceedings from: 19th Australasian Weeds Conference, 1–4 September 2014, Tasmania, Australia: 139–142.Google Scholar
  17. Chen, R. L. & J. W. Barko, 1988. Effects of freshwater macrophytes on sediment chemistry. Journal of Freshwater Ecology 4: 279–289.CrossRefGoogle Scholar
  18. Chimney, M. J. & K. C. Pietro, 2006. Decomposition of macrophyte litter in a subtropical constructed wetland in south Florida (USA). Ecological Engineering 27: 301–321.CrossRefGoogle Scholar
  19. Cilliers, C. J., 1991. Biological control of water lettuce, Pistia stratiotes (Araceae), in South Africa. Agriculture, Ecosystems & Environment 37: 225–229.CrossRefGoogle Scholar
  20. Coetzee, J. A., M. P. Hill, M. J. Byrne & A. Bownes, 2011. A review of the biological control programmes on Eichhornia crassipes (C.Mart.) Solms (Pontederiaceae), Salvinia molesta D.S.Mitch. (Salviniaceae), Pistia stratiotes L. (Araceae), Myriophyllum aquaticum (Vell.) Verdc. (Haloragaceae) and Azolla filiculoides Lam. (Azollaceae) in South Africa. African Entomology 19: 451–468.CrossRefGoogle Scholar
  21. Conversi, A., V. Dakos, A. Gårdmark, S. Ling, C. Folke, P. J. Mumby, C. Greene, M. Edwards, T. Blenckner, M. Casini & A. Pershing, 2015. A holistic view of marine regime shifts. Philosophical Transactions of the Royal Society B: Biological Science 370(1659): 20130279.CrossRefGoogle Scholar
  22. Cook, C. D. & K. Urmi-König, 1984. A revision of the genus Egeria (Hydrocharitaceae). Aquatic Botany 19: 73–96.CrossRefGoogle Scholar
  23. Daehler, C. C., 2003. Performance comparisons of co-occurring native and alien invasive plants: implications for conservation and restoration. Annual Review of Ecology Evolution and Systematics 34: 183–211.CrossRefGoogle Scholar
  24. Davis, M. A., J. P. Grime & K. Thompson, 2000. Fluctuating resources in plant communities: a general theory of invasibility. Journal of Ecology 88: 528–534.CrossRefGoogle Scholar
  25. Dawson, W., M. Fischer & M. Van Kleunen, 2011. The maximum relative growth rate of common UK plant species is positively associated with their global invasiveness. Global Ecology and Biogeography 20: 299–306.CrossRefGoogle Scholar
  26. De Wit, C. T. & J. P. Van den Bergh, 1965. Competition between herbage plants. Netherlands Journal of Agricultural Science 13: 212–221.Google Scholar
  27. DeAngelis, D. L. & J. C. Waterhouse, 1987. Equilibrium and nonequilibrium concepts in ecological models. Ecological Monographs 57: 1–21.CrossRefGoogle Scholar
  28. Diop, O., J. A. Coetzee & M. P. Hill, 2010. Impact of different densities of Neohydronomus affinis (Coleoptera: Curculionidae) on Pistia stratiotes (Araceae) under laboratory conditions. African Journal of Aquatic Science 35: 267–271.CrossRefGoogle Scholar
  29. Evans, G. C., 1972. Relative growth rate. In Anderson, D. J., P. Greig-Smith & F. A. Pitelka (eds), Studies in Ecology, Vol. 1., The quantitative analysis of plant growth University of California Press. Berkeley, California: 295–314.Google Scholar
  30. Folke, C., S. Carpenter, B. Walker, M. Scheffer, T. Elmqvist, L. Gunderson & C. S. Holling, 2004. Regime shifts, resilience and biodiversity in ecological management. Annual Review of Ecology Evolution and Systematics 35: 557–581.CrossRefGoogle Scholar
  31. Fordham, D. A., 2015. Mesocosms reveal ecological surprises from climate change. PLoS Biology 13: e1002323.CrossRefPubMedPubMedCentralGoogle Scholar
  32. FrÜh, D., S. Stoll & P. Haase, 2012. Physicochemical and morphological degradation of stream and river habitats increases invasion risk. Biological Invasions 14: 2243–2253.CrossRefGoogle Scholar
  33. Gaertner, M., R. Biggs, M. Te Beest, C. Hui, J. Molofsky & D. M. Richardson, 2014. Invasive plants as drivers of regime shifts: identifying high-priority invaders that alter feedback relationships. Diversity and Distributions 20: 733–744.CrossRefGoogle Scholar
  34. Grotkopp, E., M. Rejmanek & T. L. Rost, 2002. Toward a causal explanation of plant invasiveness: seedling growth and life-history strategies of 29 pine (Pinus) species. The American Naturalist 159: 396–419.PubMedGoogle Scholar
  35. Henry-Silva, G. G., A. F. M. Camargo & M. M. Pezzato, 2008. Growth of free-floating aquatic macrophytes in different concentrations of nutrients. Hydrobiologia 610: 153–160.CrossRefGoogle Scholar
  36. Hill, B. H., 1979. Uptake and release of nutrients by aquatic macrophytes. Aquatic Botany 7: 87–93.CrossRefGoogle Scholar
  37. Hill, M. P., 2003. The impact and control of alien aquatic vegetation in South African aquatic ecosystems. African Journal of Aquatic Science 28: 19–24.CrossRefGoogle Scholar
  38. Hill, M. P. & J. Coetzee, 2017. The biological control of aquatic weeds in South Africa: current status and future challenges. Bothalia-African Biodiversity & Conservation 47: 1–12.Google Scholar
  39. Hoagland, D. R. & D. I. Arnon, 1938. Growing Plants Without Soil by the Water Culture Method. California Agricultural Experimental Station, University of California, College of Agriculture, Berkeley: 29–32.Google Scholar
  40. Hood, G. H. & R. J. Naiman, 2000. Vulnerability of riparian zones to invasion by exotic vascular plants. Plant Ecology 148: 105–114.CrossRefGoogle Scholar
  41. Janes, R. A., J. W. Eaton & K. Hardwick, 1996. The effects of floating mats of Azolla filiculoides Lam. and Lemna minuta Kunth. on the growth of submerged macrophytes. Hydrobiologia 340: 23–26.CrossRefGoogle Scholar
  42. Janse, J. H. & P. J. T. M. Van Puijenbroek, 1998. Effects of eutrophication in drainage ditches. Environmental Pollution 102: 547–552.CrossRefGoogle Scholar
  43. Jewell, W. J., 1971. Aquatic weed decay: dissolved oxygen utilization and nitrogen and phosphorus regeneration. Water Pollution Control Federation 43: 1457–1467.Google Scholar
  44. Jha, H. K., B. S. Singh & A. K. Varshney, 2015. Local survey of Hydrilla verticillata (L.F.) Royle: an invasive and valuable aquatic weed. The Journal of the Indian Botanical Society 94: 149–152.Google Scholar
  45. Kelly, R., C. Harrod, C. A. Maggs & N. Reid, 2015. Effects of Elodea nuttallii on temperate freshwater plants, microalgae and invertebrates: small differences between invaded and uninvaded areas. Biological Invasions 17: 2123–2138.CrossRefGoogle Scholar
  46. Kinzig, A., P. Ryan, M. Etienne, H. Allison, T. Elmqvist & B. Walker, 2006. Resilience and regime shifts: assessing cascading effects. Ecology and Society 11: 20.CrossRefGoogle Scholar
  47. Kolar, C. S. & D. M. Lodge, 2001. Progress in invasion biology. Trends in Ecology & Evolution 16: 199–204.CrossRefGoogle Scholar
  48. Longhi, D., M. Bartoli & P. Viaroli, 2008. Decomposition of four macrophytes in wetland sediments: organic matter and nutrient decay and associated benthic processes. Aquatic Botany 89: 303–310.CrossRefGoogle Scholar
  49. López-Núñez, F. A., R. H. Heleno, S. Ribeiro, H. Marchante & E. Marchante, 2017. Four-trophic level food webs reveal the cascading impacts of an invasive plant targeted for biocontrol. Ecology 98: 782–793.CrossRefPubMedGoogle Scholar
  50. Madeira, P. T., J. A. Coetzee, T. D. Center, E. E. White & P. W. Tipping, 2007. The origin of Hydrilla verticillata recently discovered at a South African dam. Aquatic Botany 87: 176–180.CrossRefGoogle Scholar
  51. Martin, G. D. & J. A. Coetzee, 2011. Pet stores, aquarists and the internet trade as modes of introduction and spread of invasive macrophytes in South Africa. Water SA 37: 371–380.CrossRefGoogle Scholar
  52. Matthews, J., K. R. Koopman, R. Beringen, B. Ode, R. Pot, G. Velde, J. L. C. H. Van Valkenburg & R. S. E. W. Leuven, 2014. Knowledge Document for Risk Analysis of the Non-native Brazilian Waterweed (Egeria densa) in the Netherlands. Department of Environmental Science, Radboud University, Nijmegen.Google Scholar
  53. McConnachie, A. J., M. P. Hill & M. J. Byrne, 2004. Field assessment of a frond-feeding weevil, a successful biological control agent of red water fern, Azolla filiculoides, in southern Africa. Biological Control 29: 326–331.CrossRefGoogle Scholar
  54. Midgley, J. M., M. P. Hill & M. H. Villet, 2006. The effect of water hyacinth, Eichhornia crassipes (Martius) Solms-Laubach (Pontederiaceae), on benthic biodiversity in two impoundments on the New Year’s River, South Africa. African Journal of Aquatic Science 31: 25–30.CrossRefGoogle Scholar
  55. Mitchell, D. S., 1985. Surface-floating aquatic macrophytes. In Denny, P. (ed.), the ecology and Management of African Wetland Vegetation, Vol. 6., Geobotany Springer, Netherlands: 109–124.CrossRefGoogle Scholar
  56. Morris, K., K. A. Harrison, P. C. E. Bailey & P. I. Boon, 2004. Domain shifts in the aquatic vegetation of shallow urban lakes: the relative roles of low light and anoxia in the catastrophic loss of the submerged angiosperm Vallisneria americana. Marine & Freshwater Research 55: 749–758.CrossRefGoogle Scholar
  57. Morrison, G., O. S. Fatoki, E. Zinn & D. Jacobsson, 2001. Sustainable development indicators for urban water systems: a case study evaluation of King William’s Town, South Africa, and the applied indicators. Water SA 27: 219–232.CrossRefGoogle Scholar
  58. Netten, J. J. C., G. H. P. Arts, R. Gylstra, E. H. Van Nes, M. Scheffer & R. M. M. Roijackers, 2010. Effect of temperature and nutrients on the competition between free-floating Salvinia natans and submerged Elodea nuttallii in mesocosms. Fundamental and Applied Limnology 177: 125–132.CrossRefGoogle Scholar
  59. Nofemela, R. S., 2013. The effect of obligate hyperparasitoids on biological control: differential vulnerability of primary parasitoids to hyperparasitism can mitigate trophic cascades. Biological Control 65: 218–224.CrossRefGoogle Scholar
  60. Oberholster, P. J. & P. J. Ashton, 2008. State of the Nation Report: An Overview of the Current Status of Water Quality and Eutrophication in South African Rivers and Reservoirs. Parliamentary Grant Deliverable, Council for Scientific and Industrial Research (CSIR), Pretoria.Google Scholar
  61. Odume, O. N., C. G. Palmer, F. O. Arimoro & P. K. Mensah, 2016. Chironomid assemblage structure and morphological response to pollution in an effluent-impacted river, Eastern Cape, South Africa. Ecological Indicators 67: 391–402.CrossRefGoogle Scholar
  62. Pistori, R. E. T., A. F. M. Camargo & G. G. Henry-Silva, 2004. Relative growth rate and doubling time of the submerged aquatic macrophyte Egeria densa Planch. Acta Limnologica Brasiliensia 16: 77–84.Google Scholar
  63. Pokorný, J. & E. Rejmánková, 1983. Oxygen regime in a fishpond with duckweeds (Lemnaceae) and Ceratophyllum. Aquatic Botany 17: 125–137.CrossRefGoogle Scholar
  64. Polis, G. A., A. L. Sears, G. R. Huxel, D. R. Strong & J. Maron, 2000. When is a trophic cascade a trophic cascade? Trends in Ecology & Evolution 15: 473–475.CrossRefGoogle Scholar
  65. R Development Core Team, 2014. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
  66. Rietkerk, M. & J. Van de Koppel, 1997. Alternate stable states and threshold effects in semi-arid grazing systems. Oikos 79: 69–76.CrossRefGoogle Scholar
  67. Scheffer, M., 2009. Alternative stable states and regime shifts in ecosystems. In Levin, S. A., R. S. Carpenter, H. C. J. Godfray, A. P. Kinzig, M. Loreau, J. B. Losos, B. Walker & B. S. Wilcove (eds), The Princeton Guide to Ecology. Princeton University Press, Princeton: 359–406.Google Scholar
  68. Scheffer, M., S. Szabó, A. Gragnani, E. H. van Nes, S. Rinaldi, N. Kautsky, J. Norberg, R. M. M. Roijackers & R. J. M. Franken, 2003. Floating plant dominance as a stable state. Proceedings of the National Academy of Sciences 100: 4040–4045.CrossRefGoogle Scholar
  69. Schefffer, M. & S. R. Carpenter, 2003. Catastrophic regime shifts in ecosystems: linking theory to observation. Trends in Ecology & Evolution 18: 648–656.CrossRefGoogle Scholar
  70. Schoener, T. W., 1973. Population growth regulated by intraspecific competition for energy or time: some simple representations. Theoretical Population Biology 4: 56–84.CrossRefPubMedGoogle Scholar
  71. Schroder, A., L. Persson & A. M. De Roos, 2005. Direct experimental evidence for alternative stable states: a review. Oikos 110: 3–19.CrossRefGoogle Scholar
  72. Sharip, Z., S. Schooler, M. R. Hipsey & R. Hobbs, 2012. Eutrophication, agriculture and water level control shift aquatic plant communities from floating-leaved to submerged macrophytes in Lake Chini, Malaysia. Biological Invasions 14: 1029–1044.CrossRefGoogle Scholar
  73. Shilla, D., T. Asaeda, T. Fujino & B. Sanderson, 2006. Decomposition of dominant submerged macrophytes: implications for nutrient release in Myall Lake, NSW Australia. Wetlands Ecology and Management 14: 427–433.CrossRefGoogle Scholar
  74. Simberloff, D., 2014. Biological invasions: what’s worth fighting and what can be won? Ecological Engineering 65: 112–121.CrossRefGoogle Scholar
  75. Smart, R. M., J. W. Barko, & D. W. McFarland, 1994. Competition between Hydrilla. verticillata and Vallisneria americana under different environment conditions. Technical Report A-94-1. NTIS No. AD A279 172. US Army Engineer Waterways Experiment Station, Vicksburg.Google Scholar
  76. Spivak, A. C., M. J. Vanni & E. M. Mette, 2011. Moving on up: can results from simple aquatic mesocosm experiments be applied across broad spatial scales? Freshwater Biology 56: 279–291.CrossRefGoogle Scholar
  77. Stewart, R. I., M. Dossena, D. A. Bohan, E. Jeppesen, R. L. Kordas, M. E. Ledger, M. Meerhoff, B. Moss, C. Mulder, J. B. Shurin & B. Suttle, 2013. Mesocosm experiments as a tool for ecological climate-change research. In Woodward, G. & E. J. O’Gorman (eds), Global Change in Multispecies Systems: Advances in Ecological Research. Elsevier, London: 71–182.CrossRefGoogle Scholar
  78. Stiers, I., N. Crohain, G. Josens & L. Triest, 2011. Impact of three aquatic invasive species on native plants and macroinvertebrates in temperate ponds. Biological Invasions 13: 2715–2726.CrossRefGoogle Scholar
  79. Suding, K. N., K. L. Gross & G. R. Houseman, 2004. Alternative states and positive feedbacks in restoration ecology. Trends in Ecology & Evolution 19: 46–53.CrossRefGoogle Scholar
  80. Téllez, T. R., E. M. D. R. López, G. L. Granado, E. A. Pérez, R. M. López & J. M. S. Guzmán, 2008. The water hyacinth, Eichhornia crassipes: an invasive plant in the Guadiana River Basin (Spain). Aquatic Invasions 3: 42–53.CrossRefGoogle Scholar
  81. Tyler, A. C., J. G. Lambrinos & E. D. Grosholz, 2007. Nitrogen inputs promote the spread of an invasive marsh grass. Ecological Applications 17: 1886–1898.CrossRefPubMedGoogle Scholar
  82. Uddin, M. N. & R. W. Robinson, 2017. Can Nutrient Enrichment Influence the Invasion of Phragmites australis?. In Press, Science of The Total Environment. Scholar
  83. Van Ginkel, C. E., 2011. Eutrophication: present reality and future challenges for South Africa. Water SA 37: 693–701.Google Scholar
  84. Vermaat, J. E., L. Santamaria & P. J. Roos, 2000. Water flow across and sediment trapping in submerged macrophyte beds of contrasting growth form. Archiv für Hydrobiologie 148: 549–562.CrossRefGoogle Scholar
  85. Viaroli, P., M. Bartoli, G. Giordani, M. Naldi, S. Orfanidis & J. M. Zaldivar, 2008. Community shifts, alternative stable states, biogeochemical controls and feedbacks in eutrophic coastal lagoons: a brief overview. Aquatic Conservation: Marine and Freshwater Ecosystems 18: 105–117.CrossRefGoogle Scholar
  86. Walker, B. & J. A. Meyers, 2004. Thresholds in ecological and social–ecological systems: a developing database. Ecology and Society 9: 3.CrossRefGoogle Scholar
  87. 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.CrossRefPubMedGoogle Scholar
  88. Weyl, P. S. & J. A. Coetzee, 2014. The invasion status of Myriophyllum spicatum L. in southern Africa. Management of Biological Invasions 5: 31–37.CrossRefGoogle Scholar
  89. Yarrow, M., V. H. Marín, M. Finlayson, A. Tironi, L. E. Delgado & F. Fischer, 2009. The ecology of Egeria densa planchon (Liliopsida: Alismatales): A wetland ecosystem engineer. Revista Chilena de Historia Natural 82: 299–313.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Zoology and EntomologyCentre for Biological Control, Rhodes UniversityGrahamstownSouth Africa
  2. 2.Department of BotanyCentre for Biological Control, Rhodes UniversityGrahamstownSouth Africa

Personalised recommendations