The road to extinction is paved with good intentions: negative association of fish hatcheries with threatened salmon

Hatchery programmes for supplementing depleted populations of fish are undergoing a worldwide expansion and have provoked concern about their ramifications for populations of wild fish. In particular, Pacific salmon are artificially propagated in enormous numbers in order to compensate for numerous human insults to their populations, yet the ecological impacts of this massive hatchery effort are poorly understood. Here we test the hypothesis that massive numbers of hatchery-raised chinook salmon reduce the marine survival of wild Snake River spring chinook, a threatened species in the USA. Based on a unique 25-year time-series, we demonstrated a strong, negative relationship between the survival of chinook salmon and the number of hatchery fish released, particularly during years of poor ocean conditions. Our results suggest that hatchery programmes that produce increasingly higher numbers of fish may hinder the recovery of depleted wild populations.     

Some consequences of Pacific salmon hatchery production in Kamchatka: changes in age structure and contributions to natural spawning populations

Aggregate hatchery production of Pacific salmon in the Kamchatka region of the Russian Federation is very low (< 0.5% of total harvest, with five hatcheries releasing approximately 41 M juvenile salmon annually), but contributions in certain rivers can be substantial. Enhancement programs in these rivers may strongly influence fitness and production of wild salmon. In this paper we document significant divergence in demographic traits in hatchery salmon populations in the Bolshaya River and we estimate the proportion of hatchery chum salmon in the total run in the Paratunka River to demonstrate the magnitude of enhancement in this system. We observed a reduction in the expression of life history types in hatchery populations (ranging from 1 to 9 types) compared to wild populations (17 types) of sockeye salmon in the Bolshaya River. We found similar trends in Chinook salmon in the same river system. This reduced life history diversity may make these fish less resilient to changes in habitat and climate. We estimate hatchery chum salmon currently contribute 17-45% to the natural spawning population in the Paratunka River. As hatchery fish increase in numbers at natural spawning sites, this hatchery production may affect wild salmon production. It is important to investigate the risk of introgression between hatchery and wild salmon that can lead to reduction in salmon fitness in Kamchatka rivers, as well as the potential of ecological interactions that can have consequences on status of wild salmon and overall salmon production in this region.     

Innate and enhanced predator recognition in hatchery-reared chinook salmon

We used a laboratory behaviour assay to investigate how innate predator recognition, handling stress, retention time, and number of conditioning events might affect chemically mediated anti-predator conditioning for hatchery-reared chinook salmon, Oncorhynchus tshawytscha. Juvenile chinook salmon with no prior exposure to predatory stimuli exhibited innate fright responses to northern pikeminnow, Ptychocheilis oregonensis, odour, regardless of whether the salmon came from a population that exists in sympatry or allopatry with northern pikeminnows. Juvenile chinook salmon exhibited enhanced predator recognition following a single conditioning event with conspecific extract and northern pikeminnow odour. Handling similar to what hatchery salmon might experience prior to release did not substantially reduce the conditioned response. When we conditioned juvenile chinook salmon in hatchery rearing vessels, fish from tanks treated once exhibited a conditioned response to northern pikeminnow odour in aquaria, but only for one behaviour (feeding response), and fish treated twice did not respond. The results suggest that enhanced recognition of predator stimuli occurs quickly, but may be to some extent context-specific, which may limit conditioned fright responses after release into the natural environment.     

Environmental rearing conditions produce forebrain differences in wild Chinook salmon Oncorhynchus tshawytscha

Recent studies suggest that hatchery-reared fish can have smaller brain-to-body size ratios than wild fish. It is unclear, however, whether these differences are due to artificial selection or instead reflect differences in rearing environment during development. Here we explore how rearing conditions influence the development of two forebrain structures, the olfactory bulb and the telencephalon, in juvenile Chinook salmon (Oncorhynchus tshawytscha) spawned from wild-caught adults. First, we compared the sizes of the olfactory bulb and telencephalon between salmon reared in a wild stream vs. a conventional hatchery. We next compared the sizes of forebrain structures between fish reared in an enriched NATURES hatchery and fish reared in a conventional hatchery. All fish were size-matched and from the same genetic cohort. We found that olfactory bulb and telencephalon volumes relative to body size were significantly larger in wild fish compared to hatchery-reared fish. However, we found no differences between fish reared in enriched and conventional hatchery treatments. Our results suggest that significant differences in the volume of the olfactory bulb and telencephalon between hatchery and wild-reared fish can occur within a single generation.     

Lack of trophic competition among wild and hatchery juvenile chum salmon during early marine residence in Taku Inlet,Southeast Alaska

Early marine trophic interactions of wild and hatchery chum salmon (Oncorhynchus keta) were examined as a potential cause for the decline in harvests of adult wild chum salmon in Taku Inlet, Southeast Alaska. In 2004 and 2005, outmigrating juvenile chum salmon were sampled in nearshore habitats of the inlet (spring) and in epipelagic habitat at Icy Strait (summer) as they approached the Gulf of Alaska. Fish were frozen for energy density determination or preserved for diet analyses, and hatchery stocks were identified from the presence of thermal marks on otoliths. We compared feeding intensity, diets, energy density, and size relationships of wild and hatchery stocks (n = 3123) across locations and weeks. Only hatchery fish feeding intensity was negatively correlated with fish abundance. In both years, hatchery chum salmon were initially larger and had greater energy density than wild fish, but lost condition in early weeks after release as they adapted to feeding on wild prey assemblages. Diets differed between the stocks at all inlet locations, but did not differ for hatchery salmon between littoral and neritic habitats in the outer inlet, where the stocks overlapped most. Both diets and energy density converged by late June. Therefore, if density-dependent interactions affect wild chum salmon, these effects must be very rapid because survivors in Icy Strait showed few differences. Our study also demonstrates that hatchery release strategies used near Taku Inlet successfully promote early spatial segregation and prey partitioning, which reduce the probability of competition between wild and hatchery chum salmon stocks.     

Rearing and migration of juvenile Chinook salmon (<Emphasis Type="Italic">Oncorhynchus tshawytscha</Emphasis>) in a large river floodplain

Off-channel habitat has become increasingly recognized as key for migratory fishes such as juvenile Chinook salmon (Oncorhynchus tshawytscha). Hence, floodplain habitat has been identified as critical for the continued persistence of California’s Central Valley salmon, particularly the Yolo Bypass, the primary floodplain of the Sacramento River. To provide insight into factors supporting juvenile salmon use of this 240 km², partially leveed floodplain, we examined inter- and intra-annual relationships between environmental correlates and residency time, apparent growth, emigration, migratory phenotype, and survival over more than a decade for natural-origin (“wild”) fish and experimentally-released hatchery fish. Flood duration was positively associated with hatchery juveniles residing longer and achieving larger size. Wild juveniles grew larger and emigrated later with cumulative temperature experience (accumulated thermal units) and warmer average annual temperatures during flood years. Within years, both wild and hatchery salmon departed the floodplain as flood waters receded. Parr-sized juveniles dominated outmigrant composition, though fry and smolt-sized juveniles were also consistently observed. Survival to the ocean fishery was not significantly different between hatchery fish that reared in the Yolo Bypass versus those that reared in the main stem Sacramento River. Our study indicates improved frequency and duration of connectivity between the Sacramento River and the Yolo Bypass could increase off-channel rearing opportunities that expand the life history diversity portfolio for Central Valley Chinook salmon.     

Consequences to fitness‐related traits of hybridization between farmed and wild Atlantic salmon, Salmo salar

Increasing concern has been expressed about the genetic effects of cultured salmonid fishes on natural populations. Avoidance of extreme negative outcomes was one reason for the establishment of a genetic management policy for the State of Alaska. However, domestication within the hatchery may still cause divergence from the wild donor population. This divergence could potentially lead to adverse impacts on wild stocks through straying and introgression. This study examines potential domestication in two Alaskan chinook salmon stocks. The Little Port Walter (LPW) Hatchery Chickamin River stock resulted from a small collection of wild broodstock in 1976. The LPW Unuk stock was founded with a larger number of individuals in 1976 and has had subsequent infusion of wild gametes. These lines have been maintained at LPW through ocean ranching of tagged smolts. Comparisons are made between the hatchery lines, progeny of wild chinook collected from the Chickamin and Unuk Rivers, and hybrids between the hatchery and wild groups. Mature ocean‐ranched female chinook salmon returning to the facility were periodically graded for ripeness and spawned. Body size and meristic measurements were collected from these mature spawners. Maturation timing, fecundity, and individual egg size of these fourth generation hatchery fish are compared with that of offspring of wild fish from the same donor stock. Stock of origin is confirmed for all spawners and offspring using microsatellite DNA analysis.     

Comparison of maturation timing,egg size and fecundity between hatchery lines of chinook salmon and their wild donor stocks

Increasing concern has been expressed about the genetic effects of cultured salmonid fishes on natural populations. Avoidance of extreme negative outcomes was one reason for the establishment of a genetic management policy for the State of Alaska. However, domestication within the hatchery may still cause divergence from the wild donor population. This divergence could potentially lead to adverse impacts on wild stocks through straying and introgression. This study examines potential domestication in two Alaskan chinook salmon stocks. The Little Port Walter (LPW) Hatchery Chickamin River stock resulted from a small collection of wild broodstock in 1976. The LPW Unuk stock was founded with a larger number of individuals in 1976 and has had subsequent infusion of wild gametes. These lines have been maintained at LPW through ocean ranching of tagged smolts. Comparisons are made between the hatchery lines, progeny of wild chinook collected from the Chickamin and Unuk Rivers, and hybrids between the hatchery and wild groups. Mature ocean‐ranched female chinook salmon returning to the facility were periodically graded for ripeness and spawned. Body size and meristic measurements were collected from these mature spawners. Maturation timing, fecundity, and individual egg size of these fourth generation hatchery fish are compared with that of offspring of wild fish from the same donor stock. Stock of origin is confirmed for all spawners and offspring using microsatellite DNA analysis.     

Atlantic salmon straying from the River Imsa

Mean estimated straying rate for Atlantic salmon Salmo salar L. leaving the River Imsa as smolts during 1976–1999 was 15% for hatchery fish and 6% for wild conspecifics. Hatchery Atlantic salmon selected for production traits during four or more generations strayed >50%. The straying rate was higher for Atlantic salmon staying 2 rather than 1 year at sea before attaining maturity. For spawning, 96% of the strays entered streams within 420 km from the River Imsa, and c . 80% entered streams within 60 km of the mouth of the River Imsa, whether the fish were wild or hatchery released. Within the 60 km zone, the number of strays caught in a river increased with the Atlantic salmon catch in that river, but there was no significant relationship between straying rate and water discharge or distance from the river to the River Imsa. The observed straying rate of hatchery Atlantic salmon decreased with increasing number of fish entering the River Imsa. Sexual maturation as parr did not influence the tendency to stray. The results suggest that the establishment of temporary zones, free of fish farms, outside important Atlantic salmon rivers by the fisheries authorities in Norway should be large, whole fjords, to be effective.     

Overview of salmon stock enhancement in southeast Alaska and compatibility with maintenance of hatchery and wild stocks

Modern salmon hatcheries in Southeast Alaska were established in the 1970s when wild runs were at record low levels. Enhancement programs were designed to help rehabilitate depressed fisheries and to protect wild salmon stocks through detailed planning and permitting processes that included focused policies on genetics, pathology, and management. Hatcheries were located away from significant wild stocks, local sources were used to develop hatchery broodstocks, and juveniles are marked so management can target fisheries on hatchery fish. Initially conceived as a state-run system, the Southeast Alaska (SEAK) program has evolved into a private, non-profit concept centered around regional aquaculture associations run by fishermen and other stakeholders that pay for hatchery operations through landing fees and sale of fish. Today there are 15 production hatcheries and 2 research hatcheries in SEAK that between 2005 and 2009 released from 474 to 580 million (average 517 million) juvenile salmon per year. During this same period commercial harvest of salmon in the region ranged from 28 to 71 million salmon per year (average 49 million). Contributions of hatchery-origin fish to this harvest respectively averaged 2%, 9%, 19%, 20%, and 78% for pink, sockeye, Chinook, coho, and chum salmon. Both hatchery and wild salmon stocks throughout much of Alaska have experienced high marine survivals since the 1980s and 1990s resulting in record harvests over the past two decades. Although some interactions between hatchery salmon and wild salmon are unavoidable including increasing concerns over straying of hatchery fish into wild salmon streams, obvious adverse impacts from hatcheries on production of wild salmon populations in this region are not readily evident.     

The impact of supplementation in winter-run chinook salmon on effective population size

Supplementation of young raised at a protected site, such as a hatchery, may influence the effective population size of an endangered species. A supplementation program for the endangered winter-run chinook salmon from the Sacramento River, California, has been releasing fish since 1991. A breeding protocol, instituted in 1992, seeks to maximize the effective population size from the captive spawners by equaling their contributions to the released progeny. As a result, the releases in 1994 and 1995 appear not to have decreased the overall effective population size and may have increased it somewhat. However, mistaken use of non-winter-run chinook spawners resulted in artificial crosses between runs with a potential reduction in effective population size, and imprinting of the released fish on Battle Creek, the site of the hatchery, resulted in limiting the contribution of the released fish to the target mainstem population. Rapid genetic analysis of captured spawners and a new rearing facility on the Sacramento River should alleviate these problems and their negative effect on the effective population size in future years.     

Spatial and trophic overlap of marked and unmarked Columbia River Basin spring Chinook salmon during early marine residence with implications for competition between hatchery and naturally produced fish

Ecological interactions between natural and hatchery juvenile salmon during their early marine residence, a time of high mortality, have received little attention. These interactions may negatively influence survival and hamper the ability of natural populations to recover. We examined the spatial distributions and size differences of both marked (hatchery) and unmarked (a high proportion of which are natural) juvenile Chinook salmon in the coastal waters of Oregon and Washington from May to June 1999–2009. We also explored potential trophic interactions and growth differences between unmarked and marked salmon. Overlap in spatial distribution between these groups was high, although catches of unmarked fish were low compared to those of marked hatchery salmon. Peak catches of hatchery fish occurred in May, while a prolonged migration of small unmarked salmon entered our study area toward the end of June. Hatchery salmon were consistently longer than unmarked Chinook salmon especially by June, but unmarked salmon had significantly greater body condition (based on length-weight residuals) for over half of the May sampling efforts. Both unmarked and marked fish ate similar types and amounts of prey for small (station) and large (month, year) scale comparisons, and feeding intensity and growth were not significantly different between the two groups. There were synchronous interannual fluctuations in catch, length, body condition, feeding intensity, and growth between unmarked and hatchery fish, suggesting that both groups were responding similarly to ocean conditions.     

Genetic implications of hatchery rearing in Atlantic salmon: effects of rearing environment on genetic composition

In an experiment to investigate genetic consequences of hatchery rearing in salmon, allozyme variation at five polymorphic loci was examined in Atlantic salmon of known initial genetic composition, which were reared throughout freshwater life in the hatchery or stocked into the wild as swim-up fry. The genetic composition of the juveniles in the hatchery remained homogeneous from fertilization up to stocking, and from stocking to 2+ in the wild, however, those remaining at the hatchery developed genetic differences among smolting and nonsmolting 1+ parr. These differences were attributed to conditions leading to early smolting at 1+ among the hatchery fish, with 1+ smolts diverging from the gene pool from which they were derived, whereas those stocked into the wild did not smolt until a year later and retained the original genetic composition. The results are discussed in relation to hatchery rearing of salmon and implications for the use of reared fish in stocking and enhancement programmes.     

Conservation planning for freshwater–marine carryover effects on Chinook salmon survival

Experiences of migratory species in one habitat may affect their survival in the next habitat, in what is known as carryover effects. These effects are especially relevant for understanding how freshwater experience affects survival in anadromous fishes. Here, we study the carryover effects of juvenile salmon passage through a hydropower system (Snake and Columbia rivers, northwestern United States). To reduce the direct effect of hydrosystem passage on juveniles, some fishes are transported through the hydrosystem in barges, while the others are allowed to migrate in‐river. Although hydrosystem survival of transported fishes is greater than that of their run‐of‐river counterparts, their relative juvenile‐to‐adult survival (hereafter survival) can be less. We tested for carryover effects using generalized linear mixed effects models of survival with over 1 million tagged Chinook salmon, Oncorhynchus tshawytscha (Walbaum) (Salmonidae), migrating in 1999–2013. Carryover effects were identified with rear‐type (wild vs. hatchery), passage‐type (run‐of‐river vs. transported), and freshwater and marine covariates. Importantly, the Pacific Decadal Oscillation (PDO) index characterizing cool/warm (i.e., productive/nonproductive) ocean phases had a strong influence on the relative survival of rear‐ and passage‐types. Specifically, transportation benefited wild Chinook salmon more in cool PDO years, while hatchery counterparts benefited more in warm PDO years. Transportation was detrimental for wild Chinook salmon migrating early in the season, but beneficial for later season migrants. Hatchery counterparts benefited from transportation throughout the season. Altogether, wild fish could benefit from transportation approximately 2 weeks earlier during cool PDO years, with still a benefit to hatchery counterparts. Furthermore, we found some support for hypotheses related to higher survival with increased river flow, high predation in the estuary and plume areas, and faster migration and development‐related increased survival with temperature. Thus, pre‐ and within‐season information on local‐ and broad‐scale conditions across habitats can be useful for planning and implementing real‐time conservation programs.     

Functions of restored wetlands for juvenile salmon in an industrialized estuary

The Duwamish estuary is an industrialized waterway located in Seattle, WA, USA. Despite a history of habitat loss, naturally produced juvenile Chinook salmon use the estuary. In addition to experiencing degraded habitat in the estuary, wild salmon growth may be affected by competition with more than three million hatchery fish released yearly into the river. Restoring habitat to benefit salmon in the Duwamish River is a priority for trustees of public resources, and a number of wetland restoration sites have been created there. We tested the function of restored sites in the Duwamish estuary for juvenile Chinook salmon by comparing fish densities from enclosure nets or beach seines at three paired restored/un-restored sites and by applying environmental and diet data to a bioenergetics model. We also examined temporal and diet overlap of wild juvenile Chinook salmon with other salmon species and with hatchery-reared Chinook salmon using non-metric multidimensional scaling (NMDS). At a brackish upstream site with a relatively large opening to the river, we found higher densities of juvenile Chinook salmon at the restored site. NMDS results indicated that juvenile Chinook salmon fed on different taxa at the restored sites than at the reference sites. However, modeled growth was similar at restored and reference sites. Co-occurring juvenile chum and Chinook salmon fed differently, with chum eating smaller prey, and Chinook salmon eating larger prey. Co-occurring hatchery and wild juvenile Chinook salmon had similar diets, indicating that they may compete for prey. However, modeled growth was positive and did not differ between hatchery and wild fish, suggesting that food was not limiting. Bioenergetics models indicated that overall juvenile Chinook salmon growth potential at the brackish water site was consistently higher than at more saline sites. Our results suggest that restoration sites in the Duwamish estuary that have larger access openings and are located in brackish water may have increased function over other configurations.     

Evidence for competition at sea between Norton Sound chum salmon and Asian hatchery chum salmon

Increasing production of hatchery salmon over the past four decades has led to concerns about possible density-dependent effects on wild Pacific salmon populations in the North Pacific Ocean. The concern arises because salmon from distant regions overlap in the ocean, and wild salmon populations having low productivity may compete for food with abundant hatchery populations. We tested the hypothesis that adult length-at-age, age-at-maturation, productivity, and abundance of a Norton Sound, Alaska, chum salmon population were influenced by Asian hatchery chum salmon, which have become exceptionally abundant and surpassed the abundance of wild chum salmon in the North Pacific beginning in the early 1980s. We found that smaller adult length-at-age, delayed age-at-maturation, and reduced productivity and abundance of the Norton Sound salmon population were associated with greater production of Asian hatchery chum salmon since 1965. Modeling of the density-dependent relationship, while controlling for other influential variables, indicated that an increase in adult hatchery chum salmon abundance from 10 million to 80 million adult fish led to a 72% reduction in the abundance of the wild chum salmon population. These findings indicate that competition with hatchery chum salmon contributed to the low productivity and abundance of Norton Sound chum salmon, which includes several stocks that are classified as Stocks of Concern by the State of Alaska. This study provides new evidence indicating that large-scale hatchery production may influence body size, age-at-maturation, productivity and abundance of a distant wild salmon population.     

Genetic changes in an Atlantic salmon population resulting from escaped juvenile farm salmon

The study was undertaken on three adjacent rivers in NW Ireland, on one of which an Atlantic salmon Salmo salar freshwater juvenile rearing unit is situated. Two markers which distinguished farm and wild populations were used. An Ava II-B RFLP in the ND1 region of mtDNA was at a frequency of 0.58 in the farm strain but absent in the wild populations. Allele E at minisatellite locus Ssa- A45/2/l was at a frequency of 0.91 in farm samples, but at a maximum of 0.41 in the populations in the two rivers adjacent to the one with the juvenile rearing unit. The farm strain showed a significant reduction in mean heterozygosity (0.281 ± 0.057), over three minisatellite loci examined, compared to wild samples (0.532 ± 0.063). The occurrence of farm genotypes and the independent occurrence of mtDNA and minisatellite markers in several parr samples from the river indicated that escaped juvenile salmon completed their life cycle, bred and interbred with native fish, upon their return to the river. Escaped fish homed accurately, as adults, to the site of escape, i.e. the area adjacent to the hatchery outflow in the upstream part of the river. Breeding of males in the lower part of the river was also indicated but this could have been due to mature male parr which had moved downstream. The return of adults of farm origin to the river to breed was indicated by the presence of the Ava II-B haplotype in adults netted in the estuary.     

Juvenile salmon in estuaries: comparisons between North American Atlantic and Pacific salmon populations

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.     

Understanding the adaptive consequences of hatchery-wild interactions in Alaska salmon

About 31% of salmon harvested in Alaska comes from the hatchery production of hundreds of millions of pink and chum salmon and smaller numbers of sockeye, Chinook, and coho salmon. The numbers of hatchery-reared juveniles released in some areas are greater than the numbers of juveniles from wild populations. However, virtually nothing is known about the effects of hatchery fish on wild populations in Alaska. Possible effects of these interactions can be inferred from studies of salmonids in other areas, from studies of other animals, and from theory. Numerous studies show a complex relationship between the genetic architecture of a population and its environment. Adaptive responses to nature and anthropogenic selection can be influenced by variation at a single gene, or more often, by the additive effects of several genes. Studies of salmonids in other areas show that hatchery practices can lead to the loss of genetic diversity, to shifts in adult run timing and earlier maturity, to increases in parasite load, to increases in straying, to altered levels of boldness and dominance, to shifts in juvenile out-migration timing, and to changes in growth. Controlled experiments across generations show, and theory predicts, that the loss of adaptive fitness in hatchery salmon, relative to fitness in wild salmon, can occur on a remarkably short time scale. All of these changes can influence survival and impose selective regimes that influence genetically based adaptive traits. The preservation of adaptive potential in wild populations is an important buffer against diseases and climate variability and, hence, should be considered in planning hatchery production levels and release locations. The protection of wild populations is the foundation for achieving sustained harvests of salmon in Alaska.