Can allelopathically active submerged macrophytes stabilise clear-water states in shallow lakes?
Introduction
Most of the world's lakes are small and shallow (Wetzel, 1990), and many of them display two strongly contrasting states: a clear state dominated by aquatic vegetation, and a turbid state characterised by a high phytoplankton biomass. These states represent alternative equilibria due to stabilising mechanisms that tend to keep the system in either the vegetation dominated or the phytoplankton-dominated state. Shifts between these equilibria are generally abrupt and difficult to reverse (Scheffer, Hosper, Meijer, Moss, & Jeppesen, 1993). A loss of submerged vegetation and a switch to the turbid state have often been documented in temperate shallow lakes in response to eutrophication (Blindow, 1992; Körner, 2002; Sand-Jensen, Riis, Vestergaard, & Larsen, 2000). Both shading by phytoplankton and/or epiphyton (attached algae growing on the plants’ surfaces) seem to be responsible for the disappearance of submerged macrophytes. Phillips, Eminson, and Moss (1978) already argued that a nutrient-mediated increase in the density of epiphyton rather than an increase of phytoplankton is the most important factor for the loss of submerged macrophytes. The detrimental role of epiphyton (Jones & Sayer, 2003) may be due to competition for light and carbon dioxide (Jones, Eaton, & Hardwick, 2000). Reduced macrophyte growth then results in less negative effects on phytoplankton and ultimately in turbid conditions.
The negative effect of submerged macrophytes on phytoplankton may depend on various mechanisms: provision of refuge for phytoplankton-grazing zooplankton against predation by planktivorous fish, reduced nutrient availability, increased sinking losses, reduced light availability, and the release of allelopathically active substances (Scheffer et al., 1993). The latter is subject of much debate because final proof for allelopathy in situ is difficult or even inaccessible (Gross, Hilt, Lombardo, & Mulderij, 2007). Several authors independently suggested a possible involvement of allelopathy behind observed phytoplankton patterns in whole-lake studies of vegetated, shallow lakes (Blindow et al., 2002; Lombardo, 2005; Mjelde & Faafeng, 1997). However, none could provide any evidence in favour of or against allelopathy, and the debate on the role of allelopathy at ecosystem level remains open.
We reviewed the available literature in order to assess the ability of submerged macrophytes to significantly suppress phytoplankton growth through the production and release of allelopathically active substances and the possible prevalence of this mechanism in eutrophic shallow lakes. The major focus is on community and ecosystem level effects. We specifically address the following questions:
- (1)
Which submerged macrophyte species exhibit allelopathic activity against phytoplankton, how frequent do they occur in shallow lakes and what macrophyte coverage is required for an effective phytoplankton inhibition?
- (2)
Are allelopathically active substances produced and released by aquatic macrophytes in sufficient quantity?
- (3)
Are the relevant phytoplankton (and epiphyton) species significantly inhibited by these substances?
- (4)
Which environmental factors may influence the allelopathic interference between submerged macrophytes and algae or cyanobacteria?
Section snippets
Active species
Allelopathic effects of submerged macrophytes on phytoplankton have been shown for at least 37 species (Mulderij, 2006). Studies directly comparing the activity of submerged macrophytes against phytoplankton are, however, scarce. Ranking of macrophytes according to their allelopathic activity depends on the tested phytoplankton species (Nakai, Inoue, Hosomi, & Murakami, 1999) and the concentration of the extracts (Elakovich & Wooten, 1995). Differences of two orders of magnitude between the
Total content of active substances
Although a number of allelopathically active substances were found in different macrophytes (Gross, 2003a), most are still unidentified (Table 1). M. spicatum, the best investigated species, contains up to 30% polyphenols based on dry weight and up to 6% of the major algicidal tellimagrandin II in apical meristems, the plant parts with highest polyphenol concentrations (Gross, Meyer, & Schilling, 1996; Gross, unpublished results). Different seasonal patterns of polyphenol concentrations were
Proof of in vitro and in situ allelopathic activity
Proving allelopathic effects of macrophytes on phytoplankton in an ecologically meaningful way is not easy. Experimental approaches mainly comprise the use of plant extracts, exudates or purified compounds and coexistence experiments or dialysis bag experiments at laboratory to field scale. None of these approaches per se addresses all of Willis’ (1985) pre-requisites to prove allelopathy (Gross et al., 2007). One of the main problems is the in situ interference of allelopathy and nutrient
Conclusions
Allelopathy can contribute to the stabilisation of clear-water states in shallow lakes, when proven allelopathically active species such as Myriophyllum, Ceratophyllum, Elodea, Najas or certain Characeae dominate the submerged vegetation, and when phytoplankton growth is the main reason for turbid conditions. Allelopathically induced growth inhibition of phytoplankton can occur when macrophytes infest a large part of the lake volume, when within patches plant density is high (>100 g dry mass m−2)
Acknowledgements
We thank all students, technicians and colleagues from the Leibniz-Institute of Freshwater Ecology and Inland Fisheries in Berlin and Neuglobsow and the University of Konstanz who have been involved in our studies during the previous years. Gerben van Geest kindly provided macrophyte data from The Netherlands. Jürgen Matthes and Ilona Korczynski fortunately contributed morphological data of lakes in Mecklenburg-Western Pomerania. We were financially supported by the German Research Foundation
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