E. T. Valtonen

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.

Parasite resistance and avoidance behaviour in preventing eye fluke infections in fish

This paper examines the efficiency of acquired resistance in protecting the fish host, rainbow trout (Oncorhynchus mykiss), against the trematode parasite Diplostomum spathaceum, and the hypothesis that fish recognize areas where infective stages are aggregated and show avoidance behaviour. We found that when fish with a low level of infection were held in restricted cages in natural conditions they became infected and developed cataracts as a result of this infection. This suggests that acquired resistance is insufficient in protecting fish against the parasite or the deleterious effects of infection in conditions where fish could not avoid the parasite. Behavioural experiments in the laboratory showed that fish reacted to the parasite cercariae by avoiding the infection source, which decreased the rate of parasite establishment. We conclude that by using a combination of behavioural avoidance and physiological resistance, fish could defend against the parasite more effectively.

Eye fluke-induced cataract formation in fish: quantitative analysis using an ophthalmological microscope.

We examined the parasite-induced cataract formation in rainbow trout (Oncorhynchus mykiss) using slit-lamp microscopy to determine the relationship between cataract intensity and number of Diplostomum spathaceum parasites that were established in the lens. Cataract intensity increased significantly with parasite burden, but was also affected by the pattern of exposure to the parasite cercariae. The slit-lamp methodology proved useful in scoring the cataracts since it provides a 3-dimensional view into the lens and gives an actual picture of the location and intensity of the cataracts, which allows detailed investigations of mechanisms underlying cataract formation in various fish species. Potential applications of the method in fish farming and parasitological studies are discussed.

Dactylogyrids on the gills of roach in central Finland: Features of infection and species composition

Monogenean parasites were examined from the gills of 660 roach (Rutilus rutilus) in four interconnected lakes in Central Finland between February and November 1986 and in three of the same lakes between February and December 1988. One of the lakes is eutrophic and polluted due to a paper and pulp mill, one is oligotrophic and in a natural state, and the other two lakes are eutrophic. The prevalence of Dactylogyrus infection was always high. Differences between the lakes and the years were observed in the intensity of infection, which was significantly higher in the polluted lake. The intensity was also higher in older fish. Nine Dactylogyrus species were found, and of these D. crucifer and D. nanus were numerically dominant in all of the lakes studied, especially in the oligotrophic lake. In 1986 D. fallax, D. similis and D. suecicus constituted significant proportions of the fauna in the polluted lake. D. micracanthus was most common in the eutrophic lakes. In 1988 the species composition in the polluted lake was most similar to that in the eutrophic lake.

The structure of parasite component communities in brackish water fishes of the northeastern Baltic Sea.

We used nestedness analysis to seek non-random patterns in the structure of component communities of metazoan parasites collected from 31 sympatric fish species from the northeastern Bothnian Bay, the most oligohaline area of the Baltic Sea. Only 8 marine parasite species were found among the 63 species recorded, although some marine fish species reproduce in the bay and others occasionally visit the area. Marine parasite species can utilize both freshwater and marine fish species as intermediate or final hosts, and marine fish can harbour freshwater parasite species. This exchange of parasite species between marine and freshwater fish has probably resulted from ecological factors acting over short time scales rather than from evolutionary processes acting over longer time; the key factor probably being the immediate presence of suitable intermediate and definitive hosts. Marine fish were expected to harbour species-poor parasite communities consisting mainly of generalists acquired from the sympatric freshwater fish species, which would result in a nested pattern among the different component communities. However, an anti-nested pattern was found in the component communities of metazoan parasites of fishes from the Bothnian Bay. A likely explanation for the observed pattern is that there are specialist parasite species, the majority of which are cestodes, in some of the freshwater fish species which otherwise have depauperate parasite communities.

Fish population size, and not density, as the determining factor of parasite infection: a case study

The diversity and abundance of parasites vary widely among populations of the same host species. These infection parameters are, to some extent, determined by characteristics of the host population or of its habitat. Recent studies have supported predictions derived from epidemiological models regarding the influence of host population density: parasite abundance and parasite species richness are expected to increase with increasing host population density, at least for directly transmitted parasites. Here, we test this prediction using a natural system in which populations of the crucian carp, Carassius carassius (L.), occur alone, with no other fish species, in a series of 9 isolated ponds in Finland. The ectoparasite communities in these fish populations consist of only 4 species of monogeneans (Dactylogyrus formosus, D. wegeneri, D. intermedius and Gyrodactylus carassii); the total and relative abundance of these 4 species varies among ponds, with one or two of the species missing from certain ponds. Across ponds, only one factor, total fish population size, explained a significant portion of the variance in both the mean number of monogenean species per fish and the mean total abundance of monogenean individual per fish. In contrast, fish population density did not influence either monogenean abundance or species richness, and neither did any of the other variables investigated (mean fish length per pond, number (of fish examined per pond, distance to the nearest lake, and several water quality measures). In our system, proximity among fish individuals (i.e. host population density) may not be relevant to the proliferation of monogeneans; instead, the overall availability of host individuals in the host population appeared to be the main constraint limiting parasite population growth.

Transmission, infectivity and survival of Diplostomum spathaceum cercariae.

The transmission dynamics of the cercariae of Diplostomum spathaceum were investigated under laboratory conditions using cercariae collected from naturally infected Lymnaea stagnalis. Cercariae were kept in a constant temperature of 20 degrees C and the survival and infectivity to naïve young rainbow trout recorded at 3-h intervals until few cercariae were alive. Mortality initially remained constant but increased rapidly after 20 h. While a model of constant mortality fitted the survival data, an age-dependent model provided a better fit and implied that cercariae tended to carry similar quantities of resources and once these were exhausted the cercariae died. Cercarial infectivity also showed an age-dependent pattern although infectivity tended (P = 0.09) to increase with age over the first 6 h of life and then fall. The per capita transmission rate of cercariae was investigated by experimentally infecting rainbow trout under standardized conditions, first with an increasing cercarial density and second, by keeping density constant but increasing numbers of cercariae. The per capita transmission rate was frequency dependent and averaged 0.341/h (+/- 0.036).

Patterns of cercarial production from Diplostomum spathaceum: terminal investment or bet hedging?

In the production of the infective cercariae of trematodes, the terminal investment hypothesis of life-history theory predicts that the rate of host exploitation and cercarial production should increase during the period of cercarial shedding since the reproductive value of the parasite decreases during this period. In contrast, a bet hedging hypothesis that focuses on the success of transmission when host contact rate is variable predicts that cercarial production should decrease in an attempt to keep the host alive for longer and thus would increase the probability of successful transmission. We examined these two hypotheses under laboratory conditions and recorded the production of Diplostomum spathaceum cercariae from naturally infected snail hosts, Lymnaea stagnalis. The average number of cercariae produced per day decreased as the snail host approached death counter to the terminal investment hypothesis. The finding supports the prediction of the bet hedging hypothesis and implies that the pattern of cercarial production may be explained by reduced virulence of the parasite within the snails to ensure extended total production time of cercariae. Nevertheless, survival of infected snails was still lower than uninfected snails suggesting that ultimately the infection still increased snail mortality rate. Cercarial production varied between days but was not cyclic, probably because of the physiology of the sporocysts within snails. Fewer cercariae were released at night, which may increase transmission efficiency to diurnally-active fish hosts. The mechanisms associated with daily cercarial production are discussed.

Perch (Perca fluviatilis L.) parasites reflect ecosystem conditions: a comparison of a natural lake and two acidic reservoirs in Finland.

Parasite communities of perch were studied in a natural lake (Vetämäjärvi) and two reservoirs (the Kyrkösjärvi and Liikapuro reservoirs) located in Western Finland. All water bodies studied are small, shallow and humic. However, the reservoirs are more acidic than the lake (pH 5.9 and 5.3 vs. 6.4). Altogether, 18 parasite species were found, but the component communities were reduced in the harsh conditions of the reservoirs (12 and six species) as compared with the lake (17 species). In addition, the mean number of metazoan parasite specimens per fish was markedly lower in the reservoirs (64.3 and 14.3 specimens) than in the lake (116.1 specimens). Our prediction on the depauperation of parasite communities in reservoirs as compared with the lake was confirmed. Many ectoparasite groups were rare and most of the digenean parasites using molluscs as their intermediate host were absent from the reservoirs due to the inability of molluscs to tolerate the acidic water. The only digenean parasite found in the less acidic reservoir was Bunodera luciopercae. There were also species that preferred reservoirs as was expected. The protozoan ciliate Capriniana piscium benefiting acidic water and Acanthocephalus lucii, due to the abundance of its intermediate host, were most prevalent in the reservoir conditions.

Vertebrate diets derived from trophically transmitted fish parasites in the Bothnian Bay

Parasites that are transmitted through predator–prey interactions may be used as indicators of trophic relationships between organisms. Yet, they are rarely used as such in the construction of topological (predator–prey) food webs. We constructed food webs of vertebrate trophic interactions using observed diet alone, trophically transmitted parasites alone, and the combination of the two based on data from 31 species of fish from the Bothnian Bay, Finland. The fish food web contained 530 links derived from observed diet, 724 links inferred from parasitism, and 1,058 links calculated from a combination of both stomach contents and parasites. This sub-web constructed from stomach contents had a mean of 17.1 links per fish species, while that using parasites had 23.4 links per fish. Combining the two diet indicators yielded 34.1 links per fish species, illustrating the complementarity of the two methods. Mean number of prey species per fish species was 12.5 using observed diet items, 15.8 using parasites, and 24.5 using both measures together. Mean number of predators per fish species was 7.4 using observed diet, 11.7 using parasites and 15.0 using both. A positive correlation was found between the mean number of parasites and the number of prey taxa in the diet among the fishes. Omnivorous fish had the highest diversity of both parasite species and prey items, while benthophagous fish had among the lowest. Mean total abundance and mean total prevalence of parasites correlated positively with fish size, with piscivores being the largest with the highest abundance and prevalence, while planktivores and benthivores had the lowest. Trophically transmitted parasites may be used to help construct vertebrate sub-webs and derive information about food web processes. Parasites alone provided equivalent if not more information than observed diet. However, resolution is improved by using parasites and observed diet together.