1. Martin Krkošek*,^†,
2. Mark A. Lewis*,
3. Alexandra Morton^‡,
4. L. Neil Frazer^§, and
5. John P. Volpe^¶

+Author Affiliations

1. *Centre for Mathematical Biology, Departments of Mathematical and Statistical Sciences and Biological Sciences, University of Alberta, Edmonton, AB, Canada T6G 1G1;
2. ^‡Raincoast Research Society, Simoom Sound, BC, Canada V0P 1S0;
3. ^§Department of Geology and Geophysics, School of Ocean and Earth Science and Technology, University of Hawaii, 2525 Correa Road, Honolulu, HI 96822; and
4. ^¶School of Environmental Studies, University of Victoria, 3800 Finnerty Road, Victoria, BC, Canada V8P 5C2

1. Edited by Stephen R. Carpenter, University of Wisconsin, Madison, WI, and approved August 24, 2006 (received for review April 29, 2006)

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 ≈2.5 months of the salmon's marine life (≈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.

• aquaculture
• emerging infectious disease
• migration
• salmon
• sea lice

Ocean fisheries and ecosystems are in decline (1, 2). The collapse and low resilience of exploited fish stocks (3) and declines in the abundance of global fishery landings (4) illustrate the challenges facing the sustainability of ocean fisheries (4, 5). These effects are partly mitigated by the rise of aquaculture, in which the farming of herbivorous fishes promises to improve global fish supplies (6). However, the decline of ocean fisheries and ecosystems can also be exacerbated by the industrial farming of carnivorous fishes such as salmon (6–8). By feeding farm salmon proteins and oils extracted from wild fish, there is a net loss of fish supply (6). Escaped farm salmon spread domesticated genes into wild populations (9) and have the potential to invade and displace native wild stocks (10–12). Finally, the spread of infectious pathogens from farm to wild salmon may also threaten wild stocks (13). Despite decades of work, the extent and impacts of parasite transmission from farm to wild salmon have remained contentious and unresolved (14, 15).

Most emerging infectious diseases in wildlife arise through complex interactions among humans, wildlife, and domesticated animals (16). The spread of nonnative parasites from livestock to wildlife has reduced the abundance (16–18) and resilience (19) of some wildlife populations and has challenged the conservation of other threatened or endangered species (16, 17, 20). For many marine fishes, aquaculture can change the dynamics of normally benign native parasites by providing parasites novel access to juvenile hosts. For Pacific salmon, juveniles are not sympatric with adults (and their parasites) for their first several months of marine life (21). However, salmon farms can undermine this temporal refuge from lice early in the salmon's life cycle. During their first months at sea, wild salmon are sympatric with large abundances of domesticated salmon (and their parasites). This change in the timing and magnitude of parasite transmission in a host's life history may undermine a functional role of migration in protecting juvenile fish from parasites associated with adult fish.

The rise of salmon farming has coincided with the emergence of native sea lice (Lepeophtheirus salmonis) infestations of sympatric wild juvenile salmonids. Afflicted areas include Norway (22), Scotland (23), Ireland (24), and Canada (25). The infestations are concurrent with declines in affected populations, but the causal linkages are obfuscated by the myriad factors affecting wild fish populations, such as density dependence, climate, fishing, and habitat degradation. Here, we present extensive data sets and mathematical models that couple louse transmission and pathogenicity to estimate the impact of farms on the survival of wild juvenile pink (Oncorhynchus gorbuscha) and chum (Oncorhynchus keta) salmon migrating through an archipelago off the west coast of Canada. The analysis yields quantitative insights into the mechanisms and extent of impacts of aquaculture on disease dynamics in wild fish populations. More generally, the results inform the development of marine conservation and disease theory and its application in fisheries and aquaculture management.