Journal of Plankton Research Vol.15 no.7 pp.867-872, 1993

SHORT COMMUNICATION

Mortality of dogs associated with a mass development of Nodulariaspumigena (Cyanophyceae) in a brackish lake at the German NorthSea coast

Stefan NehringInstitut fur Meereskunde an der Universit&t Kiel, Dusternbrooker Weg 20,D-24105 Kiel, FRG

Abstract. Mortality of two dogs, after exposure to water of a brackish lake on the German North Seacoast in 1990, is considered to be caused by a toxic Nodularia spumigena Mertens bloom.

Massive blooms of phytoplankton are common summer events and filamentouscyanobacteria often dominate the phytoplankton community in areasN^ith highnutrient load (Berg et al., 1986; Kononen, 1992). The ecological impact ofcyanobacterial blooms is significant and they have been reported as a possiblethreat to human health (Carmichael et al., 1990). At present, however, mostmass occurrences of toxic algae in brackish ponds, lakes and basins on the NorthSea coast have been overlooked so far. This short report about a bloom of thepotentially toxic cyanobacterium Nodularia spumigena Mertens in a brackishbathing lake, and the associated deaths of dogs, stresses the necessity for agreater awareness of the hazards of toxic algae and cyanobacteria in watersfrequented by humans and animals.

In August 1990, a calm and sunny month, the water of the 'Banter See', apublic bathing lake in the city of Wilhelmshaven on the German North Seacoast, was covered with cyanobacteria floating on the surface (Figure 1A). Thelake has an area of —1.1 km2 with a mean depth of 9 m (Figure 2, no. 9). Being aformer part of the city harbour, it is now isolated from the marine harbour by adam and has a salinity of ~10%o.

After swimming in the lake on 26 August 1990 and, probably, having drunkwater or licked it off their fur, two dogs showed the first symptoms of poisoning(vomiting, diarrhoea) within 5 h after exposure to the water. Ten hours later,one dog, a 4.5-year-old setter, became apathetic. On 28 August one of the dog'skidneys failed and on 29 August the dog had to be put to death. On 31 Augustthe other dog, a 2.5-year-old Welsh terrier, had to be put to death.

An autopsy on the setter by the Staatliches VeterinaruntersuchungsamtOldenburg revealed a high-grade centrolobulary degeneration of the liver withhaemorrhages. The lungs showed high blood-plenty with an oedema of mediumdegree. In the abdominal cavity, a large amount of a strong bloody fluid wasfound and the stomach contained a small amount of green-brown jelly. Thethorax wall and the diaphragm showed medium intermusculary haemorrhages.Bacteriological tests of the organs were negative. The centrolobulary liver

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degeneration was related to a poisoning by a hepatotoxic substance. Thehaemorrhages resulted from the severe liver disease and were due to aconditional depression of the blood coagulation.

Unfortunately, no information on the bloom development in the lake up tothe end of August is available. The first water samples were taken from thewater surface on 29 August. The samples showed high concentrations of thefilamentous cyanobacterium N.spumigena (Figure IB). The intracellular gasvesicles generate buoyancy and maintain the cells floating in the water. Thewhole area of the Banter See was covered with flocks of living N.spumigena.Cell counts revealed a density of 128 000 filaments I"1 or 1.7 x 107 cells I"1.Owing to predominant easterly winds during August, a large amount of theflocks drifted to the west end of the lake and formed an —1000 m2 covering

Fig. 1. (A) Accumulation of N.spumigena scum at the west end of the Banter See on 31 August 1990.(B) Nodularia spumigena. (C) Prorocentrum minimum var. triangulatum. Scale bars: 100 pun in (B),20 jim in (C).

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dense carpet with a thickness of ~6 cm. A large part of these algal masses waspumped off by the fire-brigade directly into the North Sea. This pumping wasstopped by the end of August so that a 50 m2 algal carpet was left over, whichsank to the bottom of the lake by the end of September. The municipalauthorities closed the Banter See as a consequence of the events on 31 August.

The bloom of N.spumigena was associated with a bloom of the dinoflagellateProrocentrum minimum var. triangulatum, which is not known to be toxic(Elbrachter, personal communication) (Figure 1C). Cell numbers were esti-mated to be 1.12 x 106 cells I"1. Supplementary, on 29 August, a bacteriologicalexamination of the A/odu/aWa-containing water by the Landes-Hygiene-Institut,Oldenburg, revealed high loadings with Escherichia coli (>2000 cells ml"1) andfaecal coliforms (>11 000 cells ml"1), whereby the bathing water limit wasgreatly exceeded.

Measurements carried out by Tiefbauamt Wilhelmshaven showed watertemperatures of ~21.5°C at the beginning of August, and these were still at15.TC at the end of September. Highest levels of dissolved phosphate were6.6 u,M on 30 April and 10.3 u,M on 7 August, but in June and July <1.1 u.Mwas found. Nitrate and nitrite concentrations were generally below the detectionlimit, whereas ammonium, mostly <2 u.M, reached maximum levels of 5.6 jxMon 18 September. During the N.spumigena bloom, a significant increase in pHlevels from 8.0 to 9.1 was observed. Oxygen saturation was ~100% up to thebeginning of September, but on 18 September, due to sedimentation andsubsequent remineralization of the bloom, only 60% saturation was observed atthe surface and only 40% at the lake bottom. In spite of this fact, no fish kill wasobserved.

Blooms and accumulations of Nodularia may have toxic effects on animals.The first report on N.spumigena causing animal death is that of Francis (1878)..Blooms of toxic Nodularia in freshwater have been reported from several partsof the world. From the Baltic sea, there are reports of blooms of N.spumigenaassociated with poisoning of ducks (Kalbe andTiess, 1964), dogs (Persson etal.,1984; Edler et al., 1985) and young cattle (GuBmann et al., 1985), but for thearea of the North Sea coast no mass development of N.spumigena has beenreported so far (Figure 2) (Table I).

The concurrent large amounts of N.spumigena in the Banter See stronglysuggest that the dogs were affected by algal toxins. The results of the autopsy,suggesting a poisoning by a hepatotoxic agent, agree well with the characteriz-ation of the toxin isolated from N.spumigena. This potent hepatotoxicpentapeptide (LD50 30-50 u,g kg"1 i.p. mouse; Carmichael et al., 1990), namedNodularin, induces massive haemorrhages in the liver of mammals, causes adisruption of the lobular and sinusoidal structure, and has some effects on thekidneys (Eriksson et al., 1988; Sandstr0m et al., 1990). Up to now, mortality ofdogs caused by N.spumigena has exclusively been reported from the Baltic Seaarea, with a time lag of 1-15 days from exposure to death (Persson et al., 1984;Edler et al., 1985).

Allergic problems in humans after contact with blooms of several cyano-bacterial species have been described (Carmichael et al., 1990) and often

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Fig. 2. Known cases of animal poisoning as a consequence of toxic Nodularia spumigena blooms inEurope [duclcs (number 1), dogs (2-6, 8, 9), young cattle (7)].

Table I. Known cases of animal poisoning as a consequence of toxic Nodularia spumigena blooms inEurope; for locations see Figure 2

Location

1 Kl. Jasmunder Bodden2 Aarhus3 Ystad4 Sud-GotlandS Karlshamn6 Simrishamn7 Strelasund8 Porvoo9 Banter See

Date

4-8.7.19636-16.8.19757-8.8.1982 .8.8.19828-10.8.19828-15.8.1982"

27-28.8.198378.1984

26.8.1990

Animal

-400 ducks20 dogs (30 dogs sick)2 dogs1 dog3 dogs3 dogs

16 young cattle4 dogs2 dogs

Reference

Kalbe and Tiess, 1964Lindstrom, 1976Edlere/o/., 1985*

GuBmann era/., 1985Persson era/., 1984Nehring

•In Swedish, published by Lind et al. (1983) and Lundberg et al. (1983).bToxicity was confirmed by Berg et al. (1986).

freshwater bathing lakes have been closed. To my knowledge, there are noofficial reports of human poisoning by N.spumigena, but Gorham (1964) andHeany (1971) have noted, assuming that man may be as susceptible to algal toxinas are other mammals, that a 68 kg man would have to ingest 1.14-3.4 1 of theblue-gTeen algal scum of a hepatotoxic Microcystis aeruginosa bloom

145 u.g kg"1 i.p. mouse) to ensure a lethal dose. It is, however, reasonable tobelieve that humans, especially small children, may accidentally ingest toxiccyanobacteria in an amount which may have serious consequences, e.g. notimmediately diagnosable liver damage. Calm or mild wind conditions may

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favour the accumulation of blooms and the formation of scums near theshoreline.

In view of the present low N/P ratio, toxic cyanobacterial blooms will be aspecial problem in the Banter See since nitrogen-fixing cyanobacteria areindependent of dissolved inorganic nitrogen, but are favoured by inorganicphosphorus (cf. Smith, 1983). In addition, a seed population for N.spumigenabloom might originate from resting stages of this species in the sediment (cf.Huber, 1984). Nodularia agglomeration is a microbiotope of high bacterialactivity (Hoppe, 1981) and, therefore, in N.spumigena blooms the presence of aconsiderable amount of pathogenic bacteria is always to be expected.

At present, there is little knowledge on the conditions that may influence thetoxicity of a bloom. According to Skulberg et al. (1984), toxic blooms ofcyanobacteria are increasing in European waters affected by eutrophication.Often, both health and water management authorities have vague ideas aboutthe risks of toxic algal blooms in brackish water bodies. Therefore, thephytoplankton of brackish public bathing basins, lakes and ponds should becarefully controlled in order to reduce the risks for humans and animals.

Acknowledgements

I thank Karl-J.Hesse for valuable discussions and comments on the manuscript,and Wolfgang Huckriede for the drafting of diagram.

References

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Received on December 15, 1992; accepted on March 15, 1993

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