Investigations on the Impact of Toxic Cyanobacteria on Fish as exemplified by the Coregonids in Lake Ammersee

Abstract

Toxic cyanobacteria affect organisms of all stages of development and trophic levels, especially aquatic organisms such as fish. Among the most toxic cyanobacteria are species of the genus Planktothrix, including Planktothrix rubescens. During the last decades, P. rubescens has become one of the predominant species of the phytoplankton community in several lakes in the pre-alpine regions. In some of those lakes (e.g. Lake Ammersee) the rise of P. rubescens has been observed to coincide with pronounced slumps in fishery yields bringing the professional fishery into existential difficulties. These slumps have primarily been characterised by prominent growth reduction of coregonids (Coregonus sp.), resulting in reduced fish fitness which appears to be associated with the regular disappearance of specific age groups of coregonid. As Lake Ammersee coregonids have repeatedly displayed blue coloured gut contents indicating coregonid contact with cyanobacteria, it appeared plausible that the challenge to this coregonid population might be causally related to the occurrence of toxic P. rubescens. The aim of the study was therefore to characterise the density, distribution and toxicity of P. rubescens in Lake Ammersee, to investigate environmental observations in controlled experimental exposure studies with respect to possible detrimental effects on coregonids and to assess the evidence linking P. rubescens exposure and adverse effects on feral coregonids in Lake Ammersee. Field studies demonstrated that P. rubescens was present during the entire observation period from 1999-2004, albeit at varying cell densities. Filaments were regularly distributed over the entire water column during winter and stratified in distinct metalimnic layers during summer. P. rubescens mass occurrence was demonstrated to be strongly influenced by water transparency, i.e. illumination in the metalimnion. Microcystins were detectable in 27 and 38 of 54 monthly seston samples via HPLC and ELISA measurements, respectively. The impact of P. rubescens on coregonids was examined in experimental exposure studies, where the environmentally observed P. rubescens cell densities and various forms of application were considered. Coregonids exposed to P. rubescens showed abnormalities representing a behavioural and physiological stress response. Histopathological alterations in liver, gastrointestinal tract and kidney suggested tissue damage and therefore alteration in normal organ function. The fact that these alterations were also immunopositive for microcystin indicated an uptake of microcystins and causality of tissue damage and the presence of microcystin. In addition, susceptibility to ectoparasitic infestation and increased mortality in exposed fish suggested these P. rubescens associated effects to impair fish fitness. The pathology and stress response of exposed coregonids was comparable across the different exposure experiments. Although, even low cell densities (≈1500 cells/ml) resulted in significant injury, the progression and severity of the observed adverse effects occurred in a dose-dependent manner, indicating that the higher the P. rubescens cell densities and hence microcystin concentrations, the more pronounced and earlier the onset of the adverse effects. P. rubescens cell densities greater than 1500 cells/ml were demonstrated to occur in Lake Ammersee during 47% of the 261 weeks observed, thus suggesting that Lake Ammersee coregonids are indeed regularly confronted with detrimental P. rubescens exposure situations. This is corroborated by field observations demonstrating P. rubescens filaments in gut contents of Lake Ammersee coregonids which additionally gives evidence that feral coregonids actually ingest P. rubescens. Field investigations demonstrated this exposure to result in an accumulation of P. rubescens components within the coregonid intestine, as the investigated fish showed a significant accumulation of cyanobacterial biliproteins explaining the prominent blue colouration of gut contents and implying possible coregonid exposure to P. rubescens toxins. Indeed, coregonids sampled during P. rubescens bloom episodes contained significant microcystin accumulation in the gut content, unambiguously demonstrating microcystin exposure of feral coregonids in Lake Ammersee. The detection of covalently-bound microcystin in liver tissue of Lake Ammersee coregonids furthermore demonstrates microcystins to traverse the ileal membrane and to accumulate in the liver. As corroborated by the experimental exposure studies, this makes substantial detrimental effects on the coregonids appear inevitable. In conclusion, prolonged occurrence of toxic P. rubescens can thus be expected to substantially affect feral coregonids. The current investigation hence substantiates the initial hypothesis of a causal relationship between mass occurrences of P. rubescens and challenged coregonid populations in pre-alpine lakes such as Lake Ammersee.