Assessment of the risk to Norwegian biodiversity and aquaculture from pink salmon (Oncorhynchus gorbuscha). Scientific Opinion of the Panel on Alien Organisms and Trade in Endangered Species of the Norwegian Scientific Committee for Food and Environment
Hindar, Kjetil; Hole, Lars Robert; Kausrud, Kyrre Linné; Malmstrøm, Martin; Rimstad, Espen; Robertson, Lucy; Sandlund, Odd Terje; Thorstad, Eva Bonsak; Vollset, Knut; de Boer, Hugo; Eldegard, Katrine; Järnegren, Johanna; Kirkendall, Lawrence Richard; Måren, Inger Elisabeth; Nilsen, Erlend Birkeland; Rueness, Eli Knispel; Nielsen, Anders; Velle, Gaute
Peer reviewed, Journal article
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OriginalversjonVKM Report. 2020, 2020:01 1-157.
The Norwegian Environment Agency and the Norwegian Food Safety Authority asked the Norwegian Scientific Committee for Food and Environment to assess the risk to Norwegian biodiversity, to the productivity of native salmonid populations, and to aquaculture, from the spread and establishment of pink salmon in Norwegian rivers, and to assess mitigation measures to prevent the spread and establishment of this alien species. Pink salmon is native to rivers around the northern Pacific Ocean. The species usually has a strict two-year life cycle, with populations spawning in even and odd years being genetically isolated. Fertilized eggs of pink salmon were transferred from Sakhalin Island to Northwest Russia in the late 1950s, and fry were released in rivers draining to the White Sea. The first abundant return to rivers in Northwest Russia, as well as to Norway and other countries in northwestern Europe, was recorded in 1960. Stocking with fish from Sakhalin was terminated in 1979. By then, no self-sustaining populations had been established. From 1985 onwards, stocking in White Sea rivers was resumed with fish from rivers in the more northerly Magadan oblast on the Russian Pacific, resulting in the establishment of reproducing populations. Stocking was continued until 1999, when the last batch of even-year fertilized eggs was imported, and the fry released in spring 2000. Thus, all pink salmon caught after 2001 in the Northeast Atlantic and the Atlantic side of the Arctic Ocean including the Barents Sea, as well as in rivers draining into these seas, are the result of reproduction in the wild. Pink salmon is now established with abundant and increasing stocks in Northwest Russia and regular occurrence in rivers in eastern Finnmark. Catches of odd-year adult pink salmon in Northwest Russia were usually below 100 tonnes before 2001 and increased to an annual average of 220.5 tonnes during the period 2001-2017. Even-year returns are smaller than odd-year returns both in Northwest Russia and in Norway. The number of pink salmon recorded in Norwegian rivers peaked in 2017, with a high number of fish in eastern Finnmark, and substantial numbers recorded in rivers all along the coast of Norway and in other European countries. In 2019, the area with abundant returns expanded in comparison with 2017, to include rivers in western Finnmark and Troms. The recorded numbers were perhaps lower in southern Norway in 2017 than in 2019 (full statistics not available when this report was finalised), but also in southern Norway there were more pink salmon in 2019 than in any year before 2017. The large numbers of pink salmon in western Finnmark and Troms in 2019 may indicate an expansion of the area in Norway with abundant odd-year pink salmon returns. In some small rivers in eastern Finnmark, between 1000 and 1500 pink salmon were fished out by local people in 2019, demonstrating the magnitude of the potential impact in terms of numbers of pink salmon. We cannot rule out that this will not happen over larger parts of Norway in the coming years. The even-year strain of pink salmon only occurs in low numbers in Russian rivers, as well as Norwegian, rivers. Adult pink salmon enter the rivers from early July, and spawning occurs in August-September. Spawning habitat requirements are like those of native salmonids: Atlantic salmon, brown trout, and Arctic charr. Spawning of pink salmon occurs earlier than the native salmonids, but observations in 2019 indicate a possible overlap with native salmonids in September in northern Norway. Pink salmon eggs hatch in late winter or spring, and the alevins remain in the gravel until most of the yolk sac has been resorbed. Emerging fry are approximately 30 mm in length. Functionally, they are smolt already at this stage, with a silvery colouration and saltwater tolerance. The fry/smolt start feeding on small invertebrates in some rivers, while the fry/smolt migrate without feeding in other rivers. They impact juveniles of native salmonids through competition for food and space and the invertebrate fauna through predation. The impact depends on the duration of their stay. This is assumed to be very short, but some observations indicate that fry/smolt that emerge from spawning redds far upstream may feed and grow to 60-70 mm before entering the sea. Pink salmon smolt may spend some time in estuaries and coastal waters before moving to the open sea. The next approximately 12 months are spent feeding in the open seas before returning to the coast to seek rivers for spawning. Homing is less precise in pink salmon than in other anadromous salmonids. All spawners die shortly after spawning. Methods This risk assessment is based on an extensive literature search, contact with scientists in North America, western Europe, Russia, Norway, the county governor in Troms and Finnmark, and local anglers’ associations, and other stakeholders in Norway. We have investigated whether ocean temperatures play an important role in the variation of pink salmon year class abundance, and whether the annual abundance of adult pink salmon is increasing with rising sea temperatures. This is an important aspect of a risk assessment in a 50-yr perspective. We have used a semi-quantitative risk assessment. The overall risk is the product of the magnitude of the consequences of the event and the likelihood that the event will occur, as judged by the project group experts. The level of confidence in the risk assessment is described, and uncertainties and data gaps identified. Results The dynamics and environmental impact of introduced pink salmon in Norwegian rivers, coastal waters, and the ocean, depend on their abundance. In all habitats and for all life stages, high abundance may have serious repercussions, whereas low numbers may be of little consequence. An increasing abundance of reproducing pink salmon will likely present hazards to biodiversity and river ecosystems. Establishment of reproducing pink salmon over larger areas in Norway will probably increase the regularity of abundant returns to Norwegian waters. The invertebrate fauna will be negatively affected where large numbers of pink salmon juveniles use it as a food source. This is more likely in long than in short rivers. The river pearl mussel, Margaritifera margaritifera, may be particularly vulnerable, as it has a larval stage in juvenile Atlantic salmon or brown trout, but cannot use pink salmon as a host. Pathogens that may be affected by the increased occurrence of pink salmon in Norway include viruses, bacteria, and parasites (eukaryotic organisms). Very little is known about the susceptibility of pink salmon to viral pathogens. Among 11 viral pathogens assessed, only three or four are known to infect pink salmon. The project group assesses that the potential impact for aquaculture is moderate if infectious haematopoietic necrosis virus is spread by pink salmon in the marine ecosystems. Salmonid alphavirus (SAV)-infected pink salmon, potentially infected through contact with Atlantic salmon aquaculture, moving from south to north could introduce a risk of spread of this virus and the resulting pancreas disease. The project group assesses that the overall potential impact of SAV for aquaculture in the marine ecosystems is low with medium to low confidence. The project group assesses that the potential impacts for aquaculture if Renibacterium salmoninarum and Piscirickettsia salmonis are spread by pink salmon in the marine ecosystems are moderate with low confidence. The potential negative impact on biodiversity in the marine ecosystems and productivity of native salmonid species is assessed as low to minimal for all viral and bacterial pathogens considered, apart from for Renibacterium salmoninarum and viral haemorrhagic septicaemia virus for which the risks were assessed as moderate. Parasites can potentially represent a major hazard to both wild and farmed salmonids, and we have considered three groups of parasites; (1) those that may impact the health and welfare of native salmonids (in the wild and in aquaculture), (2) zoonotic parasites, and (3) aquatic organisms that have a parasitic stage in their life cycle, but are of relevance and interest in Norwegian ecosystems. The abundance and spread of some of these parasites may be affected by the incursion of pink salmon. Hybridization between pink salmon (genus Oncorhynchus) and native salmonids (genera Salmo and Salvelinus) has not been documented in the wild. In the laboratory, intergeneric hybridizations between these species have produced only sterile offspring. Interactions with native salmonids may occur in two ways: through competition for food or through competition for space in the river before spawning and on the spawning grounds. If feeding in the river, pink salmon fry ingest the same prey as native salmonid fry. Thus, competition for food and space may occur if there are high densities of pink salmon for a substantial period. High densities of pink salmon fry may also influence the ability of native salmonid fry to establish territories. On the other hand, emerging pink salmon fry may serve as food for older life stages of native salmonids. Competition for spawning grounds may be restricted due to pink salmon spawning earlier in the autumn. However, there may be temporal overlap between Arctic charr and pink salmon spawning in northern Norway, and a possible overlap in both time and space with early-spawning brown trout. High numbers of pink salmon spawners may have a crowding effect on native salmonids before the actual spawning time. Agonistic behaviour, like chasing of up-migrating Atlantic salmon and brown trout by pink salmon, is known to occur. The effect of this aggressive behaviour on the spawning success of native salmonids is not known. Pink salmon spawners transport organic matter and nutrients from the sea to the rivers. Water quality will be influenced by pink salmon carcasses in rivers after spawning. Decomposition of dead spawners will release organic matter and nutrients (phosphorous and nitrogen) into the water. In nutrient-poor rivers, this will enhance production of algae and zoobenthos, and likely benefit juvenile native salmonids. The impact will likely be negative in more nutrient-rich rivers. Any effect from nutrient input on water quality is likely governed by the number of dead fish, river morphology, and the current nutrient status of the river. Dead and decomposing spawners benefit scavengers of all types and may therefore also affect terrestrial food webs and biodiversity. In the coastal and marine systems, juvenile and adult pink salmon will constitute a new and additional prey for many predators. Pink salmon in the seas may feed on similar prey as native salmonids, and high densities of pink salmon may negatively affect native salmonids as well as the marine ecosystem, as seen in the North Pacific Ocean. Hazards for the aquaculture industry are mainly associated with spreading of disease-causing pathogens. This is directly related to the number of pink salmon in the waters around aquaculture installations. The higher the number of pink salmon, the higher is the probability of individuals carrying pathogens that may be transferred to aquaculture fish. If pink salmon come to dominate the number of salmonids in rivers, this will negatively affect both the economic value of salmon angling, and the value in terms of an important ecosystem service, as catches may be dominated by 1.5 kg fish (that are not fit for human consumption, except early in the season) compared with the larger Atlantic salmon. Under present climatic conditions, pink salmon may spawn and produce offspring in all rivers along the Norwegian coast. Regular occurrence of the odd-year strain has so far only been seen in rivers in eastern Finnmark, where we believe self-sustaining populations have been established. The change from 2017 to 2019 may indicate that the area with rivers receiving high numbers is expanding westwards and southwards into Troms. Establishment of self-sustaining populations depend, in general, on a suffiently high survival of offspring after hatching and when they leave the rivers, and during the marine phase. Abundant returns of pink salmon are correlated with ocean surface temperatures in the North Atlantic Ocean and Barents Sea. Using sea-surface temperature data from 1900 to 2019, we find that the number of pink salmon returning can be relatively well predicted (adjusted R2 > 0.5 for a positive relationship) by sea-surface temperature in the area south of Svalbard and of the cohort size two years previously for all three data sets considered. Hence, the increasing sea surface temperatures and reduced ice cover over the last 20 years may benefit pink salmon in the ocean and be one reason for the increasing number of pink salmon in Northwest Russian and Norwegian waters. However, the average surface temperature of the Arctic Ocean seems to be increasing so rapidly at present that the ecosystem is probably in flux. The effects of this rapid change are unpredictable; however, it is likely that a climate warming over the next 50 years will facilitate the establishment of circumpolar pink salmon populations in Arctic rivers. Whether a warmer climate will benefit pink salmon in all Norwegian rivers remains unclear, as it is considered a cold-water species. However, pink salmon seem to be able to adapt to new conditions over a few generations. Conclusions It has already been demonstrated that pink salmon can occur in large numbers and high densities in Norwegian rivers. The impact of pink salmon on biodiversity and ecosystems in Norwegian waters depends on their numbers. This is valid for all aspects of the river systems. A low number of pink salmon are likely of little consequence, whereas abundant spawning pink salmon in a river may have substantial impact on native salmonids, as well as on water quality and biodiversity. Thousands of spawners will possibly produce millions of offspring that may impact small invertebrates and crustaceans negatively and compete with native salmonids for food and space after hatching. The impact in the sea also depends on the abundance of pink salmon, as they may compete with native salmonids and other species for food as well as have other impacts on the food-web of marine ecosystem. The likelihood of spreading of disease to native wild fish, as well as to aquaculture fish, is also directly correlated with the number of pink salmon. However, only a few fish may have a serious impact if heavily infested with a pathogen to which native wild fish or aquaculture fish are susceptible, and conditions favour transmission. The current increasing trend in sea-surface temperatures and reduced ice cover seem to benefit the survival of pink salmon in the sea, and the projected climate change may enhance this. The impact of a warmer climate on the river stages of pink salmon is less clear. The effects of further climate change may introduce unexpected interactions with pathogens and with other species, as the accelerating change since about 2010 has been moving the Arctic Ocean into previously unobserved temperature regimes. Feasible measures to reduce the impact of pink salmon in rivers include targeted fishing adapted to local conditions. Experience from 2017 and 2019 shows that such efforts are effective and can decrease or even eliminate the threat of pink salmon to native salmonids and biodiversity in individual rivers, at least in smaller rivers. In order to reduce the number of pink salmon and the recurring returns of pink salmon spawners to Norwegian coastal waters and rivers in general, however, concerted action on a regional, national and international level is required.
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