An assessment of hybridization potential between Atlantic and Pacific salmon

Salmon hold an iconic status along the Atlantic and Pacific coasts of North America, historically providing critical ecosystem services and substantial economic benefits to these regions. Overharvest, fish passage barriers and habitat destruction, in combination with other factors, have resulted in extirpation of approximately 30 % of Pacific (Oncorhynchus spp.) and 90 % of Atlantic salmon (Salmo salar) populations in the contiguous United States (Parrish et al. 1998; Gustafson et al. 2007). Many of the remaining native populations of Atlantic salmon, and Pacific salmon are protected under the U.S. Endangered Species Act (Ford 2011). Significant population declines are also occurring on both coasts in southern Canada (Irvine et al. 2005), where conservation actions are ongoing. This conservation crisis has resulted in extensive research to inform management decisions associated with recovery of endangered salmon populations. Collectively, there is a large and productive research effort in North America focused on conservation of endangered salmon populations. Numerous partnerships are in place to facilitate collaborations among researchers within each of the respective Pacific and Atlantic salmon research communities. In contrast, opportunities for sharing information across these two communities are less structured and usually occur on a small scale—e.g., at international meetings. Publications from these international meetings have typically been collections of concept papers each focused on Atlantic salmon or Pacific salmon (e.g., Lynch et al. 2002; Waples and Hendry 2008). Our goal was to help establish new collaborations between these highly productive research communities by teaming up Atlantic and Pacific salmon biologists. We organized a ‘‘Teaming Up’’ symposium that was held at the 2012 Annual Meeting of the American Fisheries Society in St. Paul, Minnesota, USA. This meeting helped connect scientists with similar interests and it was the catalyst for many new collaborative papers in this special issue. These new teams of Pacific and Atlantic salmon biologists identified areas where collaboration between these research communities W. R. Ardren (&) U.S. Fish and Wildlife Service, Western New England Complex, 11 Lincoln St., Essex Junction, VT 05452, USA e-mail: william_ardren@fws.gov

All anadromous fishes, including juvenile salmon, encounter estuarine habitats as they transition from riverine to marine environments. We compare the estuarine use between juvenile Atlantic salmon (Salmo salar) in the Penobscot River estuary and Pacific salmon (Oncorhynchus spp.) in the Columbia River estuary. Both estuaries have been degraded by anthropogenic activities. Atlantic and Pacific salmon populations in both basins rely heavily on hatchery inputs for persistence. Pacific salmon, as a group, represent a continuum of estuarine use, from species that move through rapidly to those that make extensive use of estuarine habitats. While Atlantic salmon estuarine use is predominantly similar to rapidly moving Pacific salmon, they can exhibit nearly the entire range of Pacific salmon estuarine use. Both slow and rapidly migrating Atlantic and Pacific salmon actively feed in estuarine environments, consuming insect and invertebrate prey. Interactions between juvenile salmon and estuarine fish communities are poorly understood in both estuaries, although they experience similar avian and marine mammal predators. Estuaries are clearly important for Atlantic and Pacific salmon, yet our understanding of this use is currently insufficient to make informed judgments about habitat quality or overall estuary health. This review of salmonid migration through and residency within estuaries identifies actions that could hasten restoration of both Atlantic and Pacific salmon populations.

In Atlantic salmon, as in most salmonids, males can mature early in the life cycle, as small freshwater fish, termed parr, and/or undergo a sea migration before maturing as full-size adults. The alternative life histories are contingent on environmental and social circumstances, such as growth rate, territory quality or any other factor that affects the individual's state. In order to model the choice of life history in this group of commercially valuable species, it is necessary to understand not only the relative contribution of the different male types to subsequent generations, but also to know the factors that affect reproductive success in each type. In this paper we present the results of a study designed to investigate the factors that affect the reproductive success of mature parr. We used highly polymorphic minisatellite DNA markers to analyse paternity in a series of mating experiments where the number and body size of parr were manipulated. The fraction of eggs fertilized by mature parr ranged from 26 to 40 per cent, with individual parr fertilizing up to 26 per cent of the eggs. A strong positive correlation was found between parr size and reproductive success. The relative success of parr decreased with increasing parr number. Data from this and other studies on variation in the timing and degree of parr reproductive success are discussed in relation to the evolution of male mating strategies and life history in salmonids.

Soybean meal-induced enteritis in Atlantic salmon (Salmo salar) and Chinook salmon (Oncorhynchus tshawytscha) but not in pink salmon (O. gorbuscha)

Electrophysiological recordings from the olfactory epithelium have shown that 17 alpha,20 beta-dihydroxy-4-pregnen-3-one 20-sulphate (17,20 beta-P-sulphate; a conjugate of the oocyte-maturation-inducing steroid in teleosts) is a potent odorant in precocious male Atlantic salmon (Salmo salar L.) parr. However, the olfactory epithelium of these fish only appeared to be responsive to the steroid after stimulation with the urine of ovulated female Atlantic salmon. Immature fish did not respond at any time. Stimulation with urine from immature and precocious male Atlantic salmon parr did not make the olfactory epithelium of precocious male salmon parr responsive to the steroid. 17,20 beta-P-sulphate was found in the urines of ovulated females, precocious male parr and mature male Atlantic salmon. The findings are discussed in relation to the possible role of 17,20 beta-P-sulphate in the physiology of Atlantic salmon.

Two unambiguous discoveries involving rainbow trout require scientific name changes. First, the rainbow trout has been demonstrated to be the same species as the Kamchatka trout. Second, studies of osteology and biochemistry of trout and salmon show that rainbow and cutthroat trout, and their close relatives, the golden, Mexican golden, Gila, and Apache trouts, are more closely related to Pacific salmons (Oncorhynchus) than to brown trout and Atlantic salmon (Salmo). The different names required by these two discoveries will cause some confusion in communications in which the formal classification is used, so we present evidence to acquaint biologists and managers with the rationale for the changes. The species name of the rainbow trout becomes mykiss, an older Latinized indigenous name of the Kamchatka trout. The generic designation of rainbow and cutthroat trout poses a more subjective problem, involving four possibilities: Salmo, Oncorhynchus, Rhabdofario, and Parasalmo. The balance of evidence indicates to us that the generic name for Pacific trouts and salmons should be Oncorhynchus. We suggest recognition of two divergent sister lineages, (1) Atlantic trout and salmon, and (2) Pacific trouts and salmons, as the genera Salmo and Oncorhynchus, respectively. Alternative generic classifications considered include the following: (a) Enlarge Salmo to include all Atlantic and Pacific trouts and salmons. This would be well supported by morphological and biochemical characters, but would fail to emphasize the distinctions between the Pacific and Atlantic groups. (b) Use a separate generic name, Rhabdofario, for rainbow and cutthroat trout, and their inland relatives. This would be valid, but would fail to recognize the gradation between Pacific trouts and Pacific salmons. (c) Continue to assign Pacific trout to the genus Salmo, separate from Oncorhynchus. This would be stable, but at the expense of evolutionary information in the classification—rainbow and cutthroat trout are on the same branch of evolution as the Pacific salmon. To reflect these biological relationships in the classification of trouts and salmons will contribute to better understanding of their life histories and better predictions for their management.

Canadian salmonid aquaculture provides a sustainable protein source; however, there are concerns that Atlantic salmon (Salmo salar L.) mariculture reduces wild Pacific salmon survival through interspecific disease transfer. Tenacibaculosis, caused by species of Gram‐negative bacteria in the genus Tenacibaculum, has the potential to be transmitted interchangeably between farmed Atlantic salmon and wild Pacific salmon, though there is a lack of corroboration establishing transmission. To provide evidence for interspecific horizontal transmission of tenacibaculosis from Atlantic salmon to Pacific salmon, Atlantic salmon were bath‐exposed to an isolate of Tenacibaculum maritimum and cohabitated with naïve Atlantic or Chinook salmon (Oncorhynchus tshawytscha W.) for 25 days. Exposed and naïve cohabitant Atlantic salmon exhibited morbidity with multifocal superficial and ulcerative epidermal lesions with intralesional T. maritimum (culture, histology, and qPCR). At 108 CFU mL−1, exposed and naïve cohabitant Atlantic salmon had 43% and 60% mortality, respectively. Contrastingly, cohabitant Chinook salmon experienced no morbidity or mortality, despite successful culture of T. maritimum (108 CFU mL−1n = 5/6 fish; 106 CFU mL−1n = 0/6 fish) from skin swabs. These findings suggest that BC Chinook salmon do not develop clinical tenacibaculosis through interspecific horizontal transmission from farmed Atlantic salmon with mouthrot under the tested conditions and that the presence of T. maritimum alone is insufficient for disease. Further research needs to clarify the genetic differences between hosts and pathogens in different geographical locations, and investigate additional T. maritimum isolates, alternative Tenacibaculum species, environmental variables, and temporal scales that could lead to clinical tenacibaculosis in Chinook salmon.

Range-wide regional assignment of Atlantic salmon (Salmo salar) using genome wide single-nucleotide polymorphisms

Farmed non-native Atlantic salmon (Salmo salar) is the largest agriculture export product of British Columbia, Canada. Chronic low-volume escapes of salmon from farms into Pacific waters (“leakage”) are typically undetectable (Britton et al. 2011). Analysis of escape-reporting from farmers indicates that reports greatly underestimate the true number of Atlantic salmon inadvertently released from open-net pen rearing sites (Morton and Volpe 2002). To quantify the spatial extent of escaped Atlantic salmon in Canadian Pacific rivers, we systematically snorkel-surveyed 41 known Pacific salmon (Oncorhynchus spp.)-supporting rivers and creeks on Vancouver Island over a span of 3 years. We estimated and accounted for imperfect detections using multi-season occupancy models. We detected Atlantic salmon in 36.6 % of surveyed rivers. After accounting for imperfect detection, occupancy models estimated that over half of surveyed streams across the study area contained Atlantic salmon, and that 97 % of streams with high native salmon diversity were occupied by Atlantic salmon. Even in intensive snorkel surveys, Atlantic salmon are detected in occupied streams only 2/3 the time, suggesting abundance and distribution of non-native salmon is greater than indicated by the only existing data. Further, Atlantic salmon are more likely to occupy streams with high native Pacific salmon diversity—and more likely to maintain occupancy across years—potentially increasing competitive pressure on native salmonids. Understanding local biotic and abiotic predictors of Atlantic salmon occupancy, stream colonization, and local extinction requires more data; the same is true for the effects of escaped Atlantic salmon on local salmon diversity and sustainability. These data for the first time show that Atlantic salmon occupy Pacific coastal rivers for multiple years. The impact of Atlantic salmon occupancy in British Columbia rivers must be factored into policy decisions regarding the future of salmon farming in the provincial waters.

Trade-off between resource allocation and acquisition in anadromous adult male Atlantic salmon (Salmo salar L.)

Piscine orthoreovirus Strain PRV-1 is the causative agent of heart and skeletal muscle inflammation (HSMI) in Atlantic salmon ( Salmo salar Linnaeus, 1758). Given its high prevalence in net pen salmon, debate has arisen on whether PRV poses a risk to migratory salmon, especially in British Columbia (BC) where commercially important wild Pacific salmon are in decline. Various strains of PRV have been associated with diseases in Pacific salmon, including erythrocytic inclusion body syndrome (EIBS), HSMI-like disease, and jaundice/anemia in Japan, Norway, Chile and Canada. We examined the developmental pathway of HSMI and jaundice/anemia associated with PRV-1 in farmed Atlantic and chinook ( Oncorhynchus tshawytscha (Walbaum, 1792)) salmon in BC, respectively. In situ hybridization localized PRV-1 within developing lesions in both diseases. The two diseases showed dissimilar pathological pathways, with inflammatory lesions in heart and skeletal muscle in Atlantic salmon and degenerative-necrotic lesions in kidney and liver in chinook salmon, plausibly explained by differences in PRV load tolerance in red blood cells. Viral genome sequencing revealed no consistent differences in PRV-1 variants intimately involved in the development of both diseases suggesting that migratory chinook salmon may be at more than a minimal risk of disease from exposure to the high levels of PRV occurring in salmon farms.

The ability of Atlantic salmon ( Salmo salar L.) parr to discriminate between the urine from sibling and non-sibling fish was studied by using electrophysiological and behavioural techniques. Urine was collected from four sibling groups of Atlantic salmon parr which had been reared separately. Urine from all four groups were potent odorants in the Atlantic salmon parr, eliciting responses that were recordable from the olfactory epithelium. However, the mean recorded responses were significantly greater in Atlantic salmon parr that were stimulated with the urine from sibling than from non-sibling fish. Urine from all four groups elicited display behaviour in the Atlantic salmon parr which often occurs during aggressive interactions between parr when defending territories. Atlantic salmon parr also moved towards the source of sibling urine but moved away from non-sibling urine. The results are discussed in relation to the role of urine and the adaptive significance of sibling recognition in the Atlantic salmon.

Interactions of Atlantic salmon in the Pacific Northwest: IV. Impacts on the local ecosystems

Identification and semi-quantification of Atlantic salmon in processed and mixed seafood products using Droplet Digital PCR (ddPCR)

Atlantic salmon (Salmo salar) are distributed over large areas in the north Atlantic Ocean. They usually move very quickly from freshwater to oceanic areas, whereas there is considerable variation among Pacific salmon in early marine movements. In some areas, Atlantic salmon of exploitable size are sufficiently abundant that commercial high seas fisheries have developed. Such areas are off west Greenland, where North American and European fish are harvested, and in the Norwegian Sea, north of the Faroe Islands, where mainly European fish are exploited. Atlantic salmon feed on a wide range of large crustaceans, pelagic fish, and squid in the marine environment, supporting the hypothesis that Atlantic salmon are opportunistic feeders. In the ocean the salmon grow relatively quickly and the sea age when they become sexually mature depends on both genetics and on growing conditions. Natural marine mortality of salmon is highest during the first few months at sea and the major mortality factor is probably predation. However, marine mortality of Atlantic salmon has increased in recent years, apparently correlated with a decline in sea surface temperatures. Similar relationships between environmental conditions and the growth and survival of Pacific salmon have been reported. Atlantic salmon life histories most closely mimic stream-type chinook salmon or steelhead trout among the Pacific species. Finally, Atlantic and Pacific salmon return to their home rivers with high precision and possible mechanisms controlling the oceanic homing migration are presented and discussed.