Lake Steinsfjorden is one of the most important Norwegian locations for the red-listed noble crayfish (Astacus astacus
]. This crayfish species native to Europe has severely declined over the past decades, and is now classified as “vulnerable” on the IUCN red list [2
] and ”endangered” on the Norwegian red list [3
]. However, the great cultural and economic interest in the noble crayfish as a delicacy for human consumption is a strong driver for its protection in Norway. Thus, the Norwegian legislation and management of noble crayfish allows for a strictly regulated fishery [4
]. Lake Steinsfjorden accounts for approximately 25–30% of the annual harvest in Norway [1
]. The lake is also used for agricultural irrigation and recreational purposes, such as fishing, swimming and water sports. The dimictic and mesotrophic lake has a surface area of 13.9 km2
and a maximum depth of 24 m [7
]. The lake is located in southeastern Norway (Figure 1
) and is connected to the larger and deeper Lake Tyrifjorden through a narrow shallow passage with a low water exchange [7
For decades, L. Steinsfjorden has experienced regular cyanobacterial blooms, usually Planktothrix agardhii
and Planktothrix rubescens
], both known microcystin (MC) producers. Planktothrix
spp. are known to form metalimnetic blooms during the growth season in mesotrophic lakes like L. Steinsfjorden [7
]. Metalimnetic blooms at 10–12 meters depth are more common than surface blooms in this lake. During the autumnal circulation the Planktothrix
filaments become evenly distributed in the whole water body of L. Steinsfjorden and can even survive in large biomasses under the ice cover during winter. In some years after the ice melt, large quantities of viable Planktothrix
filaments can be observed in shallow areas and piling up on the shores (Figure 2
]. The accumulated Planktothrix
biomass is a potential food source for the omnivorous noble crayfish and could therefore lead to an uptake of MCs in crayfish.
MCs are toxic cyclic heptapeptides that usually contain the unusual β-amino acid 3-amino-9-methoxy-2,6,8-trimethyl-10-phenyl-4,6-decadienoic acid (Adda). So far, at least 279 MC analogues have been reported [11
], most commonly MC-LR, -LA and -RR. Although none of these three variants have been reported from L. Steinsfjorden, 17 other MC variants have been reported in water samples or Planktothrix
cultures isolated from the lake [12
Decapods, including crayfish and freshwater shrimps, have been found to accumulate MCs in various organs, especially the hepatopancreas and gonads [13
]. They may be able to conjugate MCs, as elevated levels of glutathione S
-transferase can be found in contaminated crabs [14
]. Decapod health effects of MCs are not well studied, but mortalities of white shrimp have been reported in Texas aquaculture ponds under blooms dominated by Microcystis aeruginosa
spp., leading to the accumulation of 55 μg/g MC-LR in the shrimp hepatopancreas, but with a toxin concentration below 0.1 μg/g in the tail muscle [13
]. It has been shown for North-American signal crayfish (Pacifastacus leniusculus
) that when fed on toxic cyanobacteria, MCs are accumulated in their hepatopancreas without apparent negative influence on the crayfish health [15
]. However, the 14-day duration of the experiment may not be sufficient to answer this question. The accumulation of MCs may vary in different decapod species, and red swamp crayfish (Procambarus clarkii
) was found to accumulate considerable MC concentrations in the intestine [16
]. Only a few studies address the presence of MCs in the noble crayfish [12
]. One report suggested that noble crayfish in L. Steinsfjorden might take up and retain microcystins [19
] and a subsequent study confirmed the presence of MCs in 10 noble crayfish from L. Steinsfjorden [12
], suggesting that a more comprehensive study should be performed.
MCs constitute a hazard to humans when these toxins enter drinking water sources, or into the food chain in the form of contaminated edible aquatic animals such as fish and decapods [13
]. To protect consumers from the adverse effects of MCs, the World Health Organisation (WHO) has proposed a provisional upper limit in drinking water of 1 µg/L for MC-LR and a tolerably daily intake (TDI) of 0.04 µg/kg [20
]. However, it is unclear whether MCs pose a risk to crayfish health, or to the vertebrates and human consumers that eat crayfish from lakes affected by cyanobacterial blooms. In the Barataria estuary system of southeastern Louisiana, high concentrations of MCs were found in the estuarine blue crab (Callinectes sapidus
) living in the hyper-eutrophic freshwater lake Lac des Allemands. Here, the highest tissue concentrations of MCs were detected in the hepatopancreas with 820 μg/kg, and 105 μg/kg in the edible muscle [21
]. A meal of these animals would clearly exceed the TDI guideline.
Since L. Steinsfjorden is an important noble crayfish locality that accounts for a substantial part of the annual noble crayfish harvest in Norway, the aim was to study the degree of uptake of MCs by the crayfish and the distribution of these toxins in the different crayfish tissues. The aim was also to evaluate any potential health risks to humans associated with consumption of noble crayfish from this lake, using the same TDI recommendations as for drinking water. Information on the levels of MCs in selected organs and edible parts of noble crayfish from this exposed, but stable, crayfish population could also shed new light on the dynamics of MC uptake and depuration.
Lake Steinsfjorden experienced a bloom of Planktothrix in 2014 and 2015 and microcystins were found in the lake water. Noble crayfish from the lake had MCs in all four investigated tissues (intestine, stomach, hepatopancreas and tail muscle) and 8 of 10 tested stomach samples contained markers for Planktothrix spp., showing the cyanobacterium to be part of the noble crayfish diet. No unexpected mortalities were observed, and circumstantial evidence suggests a high tolerance to MCs in noble crayfish. Edible parts (tail muscle plus encapsulated intestine) contained low levels of MCs, just above the WHO TDI in September 2015. Removing the intestine from the tail reduced the MC content of the edible parts by 2–4-fold, to well below the TDI.
The finding of MCs at elevated levels in October 2016 more than one year after the Planktothrix bloom might indicate very slow depuration of MCs in the crayfish tissues and/or new supply through bioaccumulation in the food web, but also calls for more studies of alternative MCs sources in the lake. The results further suggest that surveillance of Planktothrix spp. and MCs in the lake water is unsuitable for predicting MC levels in noble crayfish in L. Steinsfjorden.