Abundance and toxicity of Planktothrix rubescens in the pre-alpine Lake Ammersee, Germany

Abstract

Regular occurrences of the cyanobacterium Planktothrix rubescens have been observed in several lakes that have undergone recent re-oligotrophication, e.g. Lake Ammersee. Planktothrix species are known to produce microcystins, potent phosphatase inhibitors that have been associated with morbidities and mortalities in humans and animals. The aim of this study was to characterise the temporal and spatial abundance and toxicity of P. rubescens in Lake Ammersee.

P. rubescens cell densities and biovolumes were calculated via fluorescence image analyses. P. rubescens was present during the entire observation period from 1999 to 2004, albeit at different cell densities. Maximum biovolumes of 45 cm³ m⁻² were observed in May 2001. Filaments were regularly distributed over the entire water column during winter and stratified in distinct metalimnic layers during summer, reaching maximum cell densities of ≤15,000 (winter) and ≤77,000 cells ml⁻¹ (summer). The results demonstrate that P. rubescens abundance is strongly influenced by water transparency, i.e. illumination in the metalimnion. Moreover, the P. rubescens abundance appears to result from regular phosphate depletion in the epilimnion, possibly additionally benefiting from high nitrogen loads.

Microcystin (MC) was detectable in 27 and 38 of 54 seston samples via HPLC and Adda-ELISA measurements, respectively. The main microcystin congeners in the seston samples were [Asp³]-MC-RR and [Asp³,Dhb⁷]-MC-RR. Microcystin concentrations correlated significantly with the respective phycoerythrin (PE)-concentrations. The variation in the MC/PE-ratios was low suggesting that the microcystin production of P. rubescens in Lake Ammersee is consistent and indicates that the appearance of P. rubescens coincides with measurable microcystin levels. Moreover, the observation of pronounced metalimnic oxygen depletions appears to be causally related to recurring high P. rubescens abundance.

In conclusion the results suggest that aquatic organisms such as indigenous fish populations (e.g. coregonids) are regularly confronted with potentially adverse P. rubescens densities, which might provide a possible explanation for the often observed impaired health and growth retardation of coregonid populations in P. rubescens containing pre-alpine lakes.

Introduction

Cyanobacteria are important constituents of phytoplankton communities and ubiquitous in lakes of different nutritional status. Approximately 50 of 2000 known cyanobacterial species are recognised to produce toxic molecules, e.g. alkaloids and peptides (Sivonen and Jones, 1999). Many of these toxins have been associated with mortalities of wild and domestic animals as well as severe human intoxications. Among these toxins, microcystins¹ are most frequently found and have gained attention due to their potent inhibition of protein phosphatases and associated morbidities and mortalities in humans and animals (Falconer, 2001, Briand et al., 2003).

Microcystin-producing cyanobacteria are present in coastal and inland waters, primarily in naturally eutrophic waterbodies and waters that have experienced nutritional enrichment due to anthropogenic influences (eutrophication) (Bartram et al., 1999). However, in contrast to presently eutrophicated water bodies with Anabaena sp., Aphanizomenon sp. and Microcystis aeruginosa blooms, regular mass occurrences of the cyanobacterium Planktothrix rubescens have been observed in lakes that had undergone recent re-oligotrophication. This especially includes lakes in the pre-mountainous areas of the Alps characterised by an ice-age modulated landscape of hills and valleys (pre-alpine regions) (Table 1).

The mass occurrence of P. rubescens is predominantly ascribed to two forms of specialisation providing for an ecological niche as well as a competitive advantage over green algae: i.e. an efficient regulation of buoyancy via semi-permeable gas vesicles enabling P. rubescens filaments to stratify effectively in the water column and the production of allophycocyanin, phycocyanin and phycoerythrin, photopigments enabling maximum utilisation of light energy and existence under low light conditions (Feuillade, 1994, Walsby and Schanz, 2002). Consequently, P. rubescens stratify in compact metalimnic layers overshadowed by the epilimnic community during summer stratification. Moreover, P. rubescens filaments can grow at low light conditions during circulation in the late autumn to early spring months or even below an ice cover during winter (Blikstad-Halstvedt et al., 2007).

Metalimnic blooms of Planktothrix species are often observed to co-occur with marked oxygen deficiencies in the metalimnion (Lindholm and Meriluoto, 1991, Salmaso, 2000, Ernst et al., 2001, Buzzi, 2002, Krupa and Czernas, 2003). Indeed, the senescence of cyanobacterial blooms may generate an increased oxygen demand and consequently result in massive oxygen depletion. In addition, cyanobacterial senescence provides for the release of cyanobacterial toxins (Malbrouck and Kestemont, 2006). In comparison to other cyanobacterial species, Planktothrix sp. have been shown to contain the highest concentrations of microcystin per gram dry weight (Fastner et al., 1999b). Depending on the P. rubescens abundance, toxicity and distribution, both the release of cyanobacterial toxins as well as metalimnic oxygen deficiencies may result in adverse effects on aquatic organisms (Sivonen and Jones, 1999, Wiegand and Pflugmacher, 2005), especially on coregonids² (Ernst et al., 2006a, Ernst et al., 2007).

The aims of this study were therefore

• to characterise the spatial and seasonal abundance of P. rubescens in Lake Ammersee,

• to characterise the variability of microcystin content in P. rubescens and

• to investigate the temporal co-occurrence of alterations in P. rubescens abundance and metalimnic oxygen depletion.

Exemplified by the indigenous coregonid (whitefish) population, the findings are finally discussed in the context of possible adverse effects on aquatic organisms.