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

Abstract

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.

Figure 1.

Columnaris disease in salmon (Salmo salar) fingerlings at a fish farm located in Northern Finland by River Iijoki. (a) Bars represent the proportion of infected rearing units in a given year and the line represents the sum of day degrees when the water temperature exceeded 18°C. (b) Mortality of fish owing to columnaris disease given as an average value (±s.e.) among those tanks per year where infection by Flavobacterium columnare caused mortality. Data for 1986 have been removed because the mortality could not be separated from that of furunculosis outbreaks. In 1992, 1998 and 2000 there was no mortality owing to columnaris disease. White bars indicate the years when oxytetracyclin treatment against columnaris disease was not used. (c) Diversity of symptoms related to columnaris disease of moribund 0+ -aged salmon. The symptoms (necrosis, erosion or inflammation of tissue) in skin, tail, saddleback area, jaws or gills. Number of fish studied is presented above each bar. (d) Use of oxytetracyclin treatments per infected tank owing to columnaris disease.

Figure 2.

Virulence, disease symptoms and growth characteristics at different temperatures in seven genetically characterized Flavobacterium columnare strains collected from disease outbreaks at fish farms. (a) Cumulative mortality in rainbow trout fingerlings infected experimentally with the F. columnare strains at 25°C. Redrawn from Suomalainen et al. 2006a. (b) Diversity of disease symptoms in rainbow trout infected with the F. columnare strains at 25°C. Redrawn from Suomalainen et al. 2006a. (c) The relationship between virulence and infectivity of the seven studied strains. Virulence is expressed as the slope parameter from a logistic regression model including mortality as dependent and strain and time as explanatory variables, with deviation contrast where strain H2 was the reference category. Infectivity is expressed as the proportion of infected individuals. (d) Chondroitin (chon) AC lyase activity (mean ± s.e.) of low (L1–L3) and high (H1–H3) virulence strains of F. columnare at 20 or 25°C. Chondroitin AC lyase activities are calculated as a change during a 5 min assay in the concentration of chondroitin sulphate micrograms per milligram of total protein in the bacterial culture. Redrawn from Suomalainen et al. 2006b. (e) In vitro growth of F. columnare strains of low (L1–L3) and high (H1–H4) virulence in five different temperatures. Redrawn from Suomalainen et al. 2006a.