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The continuing decline of ocean fisheries and rise of global fish consumption …

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- Epizootics of wild fish induced by farm fish

The ecological mechanism underlying this emerging infectious disease is that farm fish undermine a functional role of host migration in protecting wild juvenile hosts from parasites associated with adult hosts. Under natural conditions, L. salmonis is common on adult Pacific salmon (26, 27) but rare on juvenile pink and chum salmon during their first months at sea (25). This is because juvenile salmon enter the sea without lice several months before the return of wild adult salmon (21). However, in areas containing salmon farms, wild juvenile salmon are sympatric with large abundances of domesticated salmon (and their parasites) during their early marine life. Farms provide parasites novel access to these juvenile hosts, resulting in measurable and sometimes severe impacts on salmon survival.

Although most of the lice observed in this study were farm-origin, there were also ambient-origin lice. This was measured in areas landward of the farms where lice abundances were low and spatially uniform. These data can be thought of as a control and conform well to the null models where lice abundances are spatially uniform in the absence of farms. Low abundances of lice have also been observed on juvenile pink and chum salmon during their first months at sea in areas distant from salmon farms (25). These lice represent the combined contributions from resident alternate hosts, Chinook salmon (Oncorhynchus tshawytscha), sea-run cutthroat trout (Oncorhynchus clarki), and Dolly Varden (Salvelinus malma). These species are orders of magnitude less abundant than both farm salmon and returning adult pink and chum salmon, which are the primary natural hosts for lice (26). The different abundances of these hosts mean that farm salmon provide lice a significant novel transmission route, which in this case operates for at least the first 2.5 months of the salmon's marine life (80 km of migration route).

Usually considered benign on adult salmon, L. salmonis was a severe pathogen of juvenile pink and chum salmon. Generally, an abundance of more than two motile lice was lethal, and survival of hosts with one or two motile lice was poor (survival of uninfected hosts was nearly 100%; see Fig. 8, which is published as supporting information on the PNAS web site). As the lice progressed through their life cycle, they also increased in pathogenicity, but the patterns differed between host species. For pink salmon, the onset of increased pathogenicity occurred abruptly with the emergence of preadult lice, but for chum salmon, it was more widely distributed around adult lice (Table 4). The high pathogenicity and abundance of lice resulted in a farm-induced cumulative epizootic mortality of wild juvenile salmon that ranged from 9% to 95%. These results were consistent across multiple data sets spanning temporal, spatial, and taxonomic replication. The estimated mortality of wild salmon is high but consistent with direct field observations of the epizootics, where schools of infested moribund juvenile salmon were abundant.

We did not consider the possibility that food limitation or predation risk would be more severe for infected hosts. Generally, poor nutrition is thought to reduce the resistance of fish hosts to disease (28, 29), and parasitized prey are known to be more vulnerable to predation (30, 31). These interactions would likely increase mortality estimates. Only one assumption, relatively low motile louse mortality over the timescale of the survival trials, could cause an overestimate of the per-capita impact of lice. However, empirical data suggest motile lice are long-lived (32), at least as long as their occurrence in the survival trials (16–36 days). It is unlikely that an alternate problem may have predisposed salmon to the epizootics; research programs by universities, conservation organizations, provincial and federal governments, and industry have not identified a prevalent viral or bacterial pathogen or other physical stressor.

The life cycles of most temperate marine fishes involve a period of spatial segregation between juveniles and adults. This segregation may protect juveniles from parasites associated with adults. For salmon, migration provides a temporal refuge from lice in early marine life. Farm salmon can eliminate this refuge, resulting in high epizootic mortality in wild salmon populations. These effects may not be limited to salmon but may extend to other species coming under culture around the world. Those that have migratory or highly dispersed life histories would be most at risk. As aquaculture continues its rapid growth into new regions, habitats, and species, this disease mechanism may challenge the sustainability of coastal ecosystems and economies.

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