Epizootics of wild fish induced by farm fish

Abstract

The continuing decline of ocean fisheries and rise of global fish consumption has driven aquaculture growth by 10% annually over the last decade. The association of fish farms with disease emergence in sympatric wild fish stocks remains one of the most controversial and unresolved threats aquaculture poses to coastal ecosystems and fisheries. We report a comprehensive analysis of the spread and impact of farm-origin parasites on the survival of wild fish populations. We mathematically coupled extensive data sets of native parasitic sea lice (Lepeophtheirus salmonis) transmission and pathogenicity on migratory wild juvenile pink (Oncorhynchus gorbuscha) and chum (Oncorhynchus keta) salmon. Farm-origin lice induced 9-95% mortality in several sympatric wild juvenile pink and chum salmon populations. The epizootics arise through a mechanism that is new to our understanding of emerging infectious diseases: fish farms undermine a functional role of host migration in protecting juvenile hosts from parasites associated with adult hosts. Although the migratory life cycles of Pacific salmon naturally separate adults from juveniles, fish farms provide L. salmonis novel access to juvenile hosts, in this case raising infection rates for at least the first approximately 2.5 months of the salmon's marine life (approximately 80 km of the migration route). Spatial segregation between juveniles and adults is common among temperate marine fishes, and as aquaculture continues its rapid growth, this disease mechanism may challenge the sustainability of coastal ecosystems and economies.

Fig. 1.

Study area and sample sites for one of the data sets (April 28 to May 8, Tribune Channel; Fig. 2). Approximately 50 pink and 50 chum salmon were collected at each sample site (stars) and nonlethally assayed for sea lice. The remaining Tribune Channel data sets had a similar structure. The three active salmon farms under study are identified by filled squares. An additional farm (white square near the western end of Tribune Channel) could have contributed lice but was excluded from the analysis because of its peripheral position relative to the sample sites. Fallow and smolt farms are not shown. Gilford Island is situated east of northern Vancouver Island, BC, Canada.

Fig. 2.

Sea lice transmission dynamics and survival of juvenile chum salmon (A) and pink salmon (B) migrating past three active salmon farms. The seaward migration of salmon is from left to right, and the farm locations are shown by vertical dotted lines in the first row. The data were collected along the Tribune Channel migration corridor in 2004 (see Fig. 1). The three columns correspond to three replicate sets of samples taken April 18–28 (TR-I), April 28 to May 8 (TR-II), and May 21–29 (TR-III), 2004 (note the change in scale). The first row shows the estimated spatial distributions of planktonic copepodids originating from all sources (thick gray line), from farm salmon (three thin curves), from ambient sources (horizontal thin line), and the second generation of farm-origin lice (dashed curve, TR-III only). Reproduction of lice parasitizing the juvenile salmon was not considered in TR-I and -II because of the absence of gravid female lice in those data sets. The middle three rows depict the mean abundances of lice (±95% bootstrap confidence interval) and maximum-likelihood model fits (black lines) along the migration route for the developmental progression through parasitic copepodid, chalimus, and motile stages. The bottom row depicts the estimated remaining juvenile salmon population that survived sea lice infestation. Temperature and salinity were measured at each site and averaged 9.0°C and 30.2‰ (TR-I), 10.4°C and 26.1‰ (TR-II), and 12.3°C and 22.2‰ (TR-III).

Fig. 2.

Sea lice transmission dynamics and survival of juvenile chum salmon (A) and pink salmon (B) migrating past three active salmon farms. The seaward migration of salmon is from left to right, and the farm locations are shown by vertical dotted lines in the first row. The data were collected along the Tribune Channel migration corridor in 2004 (see Fig. 1). The three columns correspond to three replicate sets of samples taken April 18–28 (TR-I), April 28 to May 8 (TR-II), and May 21–29 (TR-III), 2004 (note the change in scale). The first row shows the estimated spatial distributions of planktonic copepodids originating from all sources (thick gray line), from farm salmon (three thin curves), from ambient sources (horizontal thin line), and the second generation of farm-origin lice (dashed curve, TR-III only). Reproduction of lice parasitizing the juvenile salmon was not considered in TR-I and -II because of the absence of gravid female lice in those data sets. The middle three rows depict the mean abundances of lice (±95% bootstrap confidence interval) and maximum-likelihood model fits (black lines) along the migration route for the developmental progression through parasitic copepodid, chalimus, and motile stages. The bottom row depicts the estimated remaining juvenile salmon population that survived sea lice infestation. Temperature and salinity were measured at each site and averaged 9.0°C and 30.2‰ (TR-I), 10.4°C and 26.1‰ (TR-II), and 12.3°C and 22.2‰ (TR-III).

Fig. 3.

Survival of juvenile chum salmon over a range of sea lice abundances. Sixty juvenile chum salmon initially infested with H₀ lice (all copepodids or chalimus I/II) were introduced into flow-through ocean enclosures and provisioned with salmon feed. Each image corresponds to an individual enclosure. The black line shows the trajectory for the daily number of survivors. The light-gray lines are the trajectories of 1,000 simulations of the best-fit model. The model was simulated as a Markov chain tracking the number of survivors in time. Each day, the number of mortalities was drawn from the number of survivors on the previous day using a binomial distribution with mortality probability calculated from the best-fit survival model. For all treatment replicates, the model has the same parameter values, except for H₀, which is specific to each enclosure.