Intensive fish farming and the evolution of pathogen virulence: the case of columnaris disease in Finland.

Ecological changes affect pathogen epidemiology and evolution and may trigger the emergence of novel diseases. Aquaculture radically alters the ecology of fish and their pathogens. Here we show an increase in the occurrence of the bacterial fish disease Flavobacterium columnare in salmon fingerlings at a fish farm in northern Finland over 23 years. We hypothesize that this emergence was owing to evolutionary changes in bacterial virulence. We base this argument on several observations. First, the emergence was associated with increased severity of symptoms. Second, F. columnare strains vary in virulence, with more lethal strains inducing more severe symptoms prior to death. Third, more virulent strains have greater infectivity, higher tissue-degrading capacity and higher growth rates. Fourth, pathogen strains co-occur, so that strains compete. Fifth, F. columnare can transmit efficiently from dead fish, and maintain infectivity in sterilized water for months, strongly reducing the fitness cost of host death likely experienced by the pathogen in nature. Moreover, this saprophytic infectiousness means that chemotherapy strongly select for strains that rapidly kill their hosts: dead fish remain infectious; treated fish do not. Finally, high stocking densities of homogeneous subsets of fish greatly enhance transmission opportunities. We suggest that fish farms provide an environment that promotes the circulation of more virulent strains of F. columnare. This effect is intensified by the recent increases in summer water temperature. More generally, we predict that intensive fish farming will lead to the evolution of more virulent pathogens.

High Gyrodactylus salaris infection rate in triploid Atlantic salmon Salmo salar.

We describe an unusually high infection rate of Gyrodactylus salaris Malmberg in juvenile Atlantic salmon Salmo salar L. of Baltic Sea origin, which are generally believed to be more resistant to G. salaris than East Atlantic salmon populations. Based on analyses of mitochondrial (complete cytochrome oxidase 1 [CO1] gene, 1548 bp) and nuclear (ADNAM1, 435 bp; internal transcribed spacer [ITS] rDNA region, 1232 bp) DNA fragments, the closest relatives of the characterized Estonian G. salaris strain were parasites found off the Swedish west coast and in Raasakka hatchery, Iijoki (Baltic Sea, Finland). Analyses of 14 microsatellite loci of the host S. salarrevealed that approximately 40% of studied fish were triploids. We subsequently identified triploid Atlantic salmon of Baltic origin as more susceptible to G. salaris infection than their diploid counterparts, possibly due to compromised complement-dependent immune pathways in triploid salmon. This is in accordance with earlier studies that have shown elevated susceptibility of triploids to various viral or bacterial pathogens, and represents one of the first reports of increased susceptibility of triploid salmonid fish to an ectoparasite. However, further experimental work is needed to determine whether triploid Atlantic salmon is generally more susceptible to G. salaris compared to their diploid counterparts, irrespective of the particular triploidization method and population of origin.

Leucocytozoonosis and trypanosomiasis in redstarts in Finland.

Leucocytozoon spp. and Trypanosoma spp. blood parasites in the redstart (Phoenicurus phoenicurus) were studied during spring migration 1994 in southern Finland (53 individuals) and the breeding season 1992-1994 in northern Finland (69). Parasite prevalence was higher during the breeding season (48%) than during the migration period (13%), with no age or sex differences in the breeding site birds. In both periods, redstarts were infected by the same blood parasites Leucocytozoon shaartusicum (46% prevalence at the breeding site and 71% during the migration period) and Trypanosoma avium, complex (58% and 43%, respectively). One individual at the breeding site had contracted L. dubreuili and one at the stop-over site had T. everetti. Our results may support the assumption that tissue-hidden parasites relapse during the breeding season when birds may have diminished immune response related to egg production and brood rearing. Another explanation could be that the high abundance of ornithophilic vectors enhance parasite transmission during breeding season in northern Finland.

Chilodonella spp. at four fish farms in northern Finland.

A total of 4.1% infestation with Chilodonella spp. was found among fish studied in 144 tanks in 1987-1989, representing 14.0% of the tanks in which fish are reared at four salmonid farms in northern Finland. Two species were found, C. hexasticha and C. piscicola, and both occurred on salmon (Salmo salar L.), sea trout [S. trutta m. trutta (L.)] and brown trout [S. t. m. lacustris (L.)]. Variability was observed in the length and width of the C. piscicola specimens and the number of ciliary rows or kineties. Large specimens which had more kineties than average for C. piscicola were found mainly on the skin of salmon aged 1-2 years. The number of kineties in the right ciliary band was found in stepwise logistic regression analysis to be of importance when typing C. piscicola specimens. Fingerlings were found to be more susceptible to Chilodonella infestation than older fish, and mortality varied in the range 2-10% in the course of the epizootics in the three fish species. Most mortality cases were caused by C. hexasticha, occurring mainly on the gills of the fish. Chilodonella piscicola was most often found in salmon and occurred at lower water temperatures than C. hexasticha (mean water temperature when found for the first time being 13 degrees C and 16 degrees C, respectively).

Triaenophorus nodulosus and T. crassus in fish from northern Finland.

10,288 fish specimens of 34 species from three water bodies in northern Finland were studied mainly in 1978-1982 Triaenophorus nodulosus and T. crassus parasites. Six of the 31 species from the Bothnian Bay were found to harbour T. nodulosus plerocercoids, four of the 11 from the cold, oligotrophic Lake Yli-Kitka in northeastern Finland and only one of the 6 from the small, eutrophic Lake Kuivasjärvi. The ruff (Gymnocephalus cernuus) was most essential intermediate host in the lakes, as supported by stomach analysis of predator fish. Although the highest prevalences were found in adult burbot (Lota lota) in two of the areas, these fish are more likely a blind end in the life cycle of T. nodulosus in the present case. T. crassus larvae were found only in three coregonid species and once in the intestine of a lamprey (Lampetra fluviatilis) from the sea. Neither the prevalence nor the intensity of infection in most of the intermediate fish hosts of T. nodulosus was seen to increase with the length of the fish. The only exception was the ruff in Lake Yli-Kitka, where a sharp increase was encountered. No prominent seasonal variation in Triaenophorus larvae infections was found in any of the cases. The prevalence of T. nodulosus infection in its final host, the pike (Esox lucius), was highest in the sea (93%) and lowest in the eutrophic lake (47%). Seasonally, the lowest T. nodulosus infections were found in June-July in the two lakes. A clear maturation cycle was also found, with the youngest worms in the summer months in all cases. T. crassus was found in every third pike in the sea and its proportion in relation to T. nodulosus is higher in the smallest and largest fish. In only 12%t of the pikes did the number of T. crassus exceed that of T. nodulosus, however, the mean ratio being 1:13 to favour of T. nodulosus. The results give an indication that the composition of the fish fauna in each water body has a considerable influence on the T. nodulosus burden and its distribution among its potential intermediate fish hosts. With the most stable environmental conditions and the greatest variety of fish species, the parasite burden in the Bothnian Bay is most evenly distributed among the 6 intermediate hosts. The fewer fish species occur in the water body, as in the present eutrophic lake, the more the significance of a few or even one intermediate host will increase.

Occurrence of Proteocephalus percae and P. cernuae in the perch and ruff in northern Finland.

The occurrence of two palearctic Proteocephalus species, P. percae and P. cernuae, in the perch and ruff, respectively, was studied in two areas of northern Finland in 1977-1983. In the Bothnian Bay, 243 perch (Perca fluviatilis) and 406 ruff (Gymnocephalus cernuus) were studied, of which 60% and 40%, respectively, were infected, while in Lake Yli-Kitka the prevalences were 10% in 213 perch and 24% in 307 ruff. Higher mean intensities of infection were found in the Bothnian Bay fish than in those from the lake, but no infected fish had as many as 10 worms. Proteocephalus infection in the perch and ruff did not vary significantly according to the length of the fish in either area, except that no P. percae were found in perch smaller than 70 mm in the lake. There was a prominent seasonal variation in the occurrence of P. cernuae in the ruff in both areas, but especially in the lake, where no proteocephalids were found in the ruff in July-October. Overlapping of generations was evident in P. percae in the sea perch, although only by virtue of the lack of mature worms at the end of the summer. Some mature proteocephalids were also found in winter in both fish species in the sea and in the ruff of the lake. The higher mean intensity values in winter, especially in P. cernuae infection in the sea ruff, may be explained partly by the active feeding of the ruff at this time in spite of very low water temperatures. Feeding activity in the perch is lower in the winter, and hence a lower mean intensity of P. percae infection was seen especially in the lake material at that time.