Pheromones and the water source preferences of adult coho salmon Oncorhynchus kisutch Walbaum

It has been proposed that population-specific pheromones released by juvenile salmonids guide the adults on their homing migration (Nordeng, 1977). To evaluate this hypothesis, adult coho salmon, Oncorhynchus kisutch , were tested in a two-choice apparatus with a variety of water sources. Coho salmon preferred home water without coho odours over an unfamiliar water source (city water). Adults preferred water conditioned by juveniles of their own population over plain city water, but did not prefer water conditioned by juveniles of their own population over that of another.     

A possible role for imprinted genes in inbreeding avoidance and dispersal from the natal area in mice

The expression of a subset of mammalian genes is subject to parent of origin effects (POE), most of which can be explained by genomic imprinting. Analysis of mutant animals has demonstrated that a number of imprinted genes influence brain development and behaviour. Here we provide evidence for POE on olfactory related behaviour and sensitivity to maternal odour cues. This was investigated by examining the odour preference behaviour of reciprocal cross F(1) mice made by embryo transfer to genetically unrelated foster parents. We determined that both adult males and females show an avoidance of female urinary odours of their genetic maternal but not paternal origin. This was found not to be due to any previous exposure to these odours or due to self-learning, but may be related to direct effects on the olfactory system, as reciprocal F(1) males show differential sensitivity to female odour cues. Currently the most robust theory to explain the evolution of imprinting is the conflict hypothesis that focuses on maternal resource allocation to the developing foetus. Kinship considerations are also likely to be important in the selection of imprinted genes and we discuss our findings within this context, suggesting that imprinted genes act directly on the olfactory system to promote post-weaning dispersal from the natal area.     

Expression of olfactory receptors in different life stages and life histories of wild Atlantic salmon (Salmo salar)

It has been hypothesized that salmonids use olfactory cues to return to their natal rivers and streams. However, the key components of the molecular pathway involved in imprinting and homing are still unknown. If odorants are involved in salmon homing migration, then olfactory receptors should play a critical role in the dissipation of information from the environment to the fish. Therefore, we examined the expression profiles of a suite of genes encoding olfactory receptors and other olfactory-related genes in the olfactory rosettes of different life stages in two anadromous and one non-anadromous wild Atlantic salmon populations from Newfoundland, Canada. We identified seven differentially expressed OlfC genes in juvenile anadromous salmon compared to returning adults in both populations of anadromous Atlantic salmon. The salmon from the Campbellton River had an additional 10 genes that were differentially expressed in juveniles compared to returning adults. There was no statistically significant difference in gene expression of any of the genes in the non-anadromous population (P < 0.01). The function of the OlfC gene products is not clear, but they are predicted to be amino acid receptors. Other studies have suggested that salmon use amino acids for imprinting and homing. This study, the first to examine the expression of olfactory-related genes in wild North American Atlantic salmon, has identified seven OlfC genes that may be involved in the imprinting and homeward migration of anadromous Atlantic salmon.     

Patterns of genomic variation in Coho salmon following reintroduction to the interior Columbia River

Coho salmon were extirpated in the mid‐20th century from the interior reaches of the Columbia River but were reintroduced with relatively abundant source stocks from the lower Columbia River near the Pacific coast. Reintroduction of Coho salmon to the interior Columbia River (Wenatchee River) using lower river stocks placed selective pressures on the new colonizers due to substantial differences with their original habitat such as migration distance and navigation of six additional hydropower dams. We used restriction site‐associated DNA sequencing (RAD‐seq) to genotype 5,392 SNPs in reintroduced Coho salmon in the Wenatchee River over four generations to test for signals of temporal structure and adaptive variation. Temporal genetic structure among the three broodlines of reintroduced fish was evident among the initial return years (2000, 2001, and 2002) and their descendants, which indicated levels of reproductive isolation among broodlines. Signals of adaptive variation were detected from multiple outlier tests and identified candidate genes for further study. This study illustrated that genetic variation and structure of reintroduced populations are likely to reflect source stocks for multiple generations but may shift over time once established in nature.     

HOMING AND OLFACTION IN SALMONIDS: A CRITICAL REVIEW WITH SPECIAL REFERENCE TO THE ATLANTIC SALMON

(1) Based on data from the literature, the phenomenon of homing in salmonids is examined with special reference to the Atlantic salmon. Wild, native fish demonstrate an excellent homing ability, judged from percent return to the home river (1–3 %) and straying to non-native watersheds (less than 3 % of returning fish). (2) The homing ability in wild fish is shown to be closely related to the existence of reproductively isolated populations between and within watersheds, as demonstrated by data from salmonid ecology and biochemical genetics. (3) Two main hypotheses have dominated the literature on salmonid homing during recent years: (a) An ‘imprinting’ hypothesis based on a process of learning of stream odours during seaward migration, coupled with sun-orientation for open sea navigation, (b) A ‘pheromone’ hypothesis related to odours from fish and based on inheritance and the seasonal migrating schedules of discrete populations. (4) The olfactory sense has been demonstrated as mandatory for salmonids, both in near range and open sea navigation. According to genetic, sensory and ecological aspects of homing, the pheromone hypothesis is therefore concluded to be the most appropriate. (5) Fish produced from artificially fertilized eggs, released within native systems or transplanted, demonstrate a reduced homing ability. Since hatchery-raised fish demonstrate a survival in sea equivalent to that of wild fish, a genetic disturbance of navigational ability has been suggested, resulting from the production of population hybrids by man. (6) Studies made in the fields of behaviour, electrophysiology and chemistry strongly suggest that population-specific fish odours are involved in home-stream recognition by salmonids. (7) An evaluation of ‘imprinting’ experiments related to artificial organic compounds reveals that: (a) the odorant properties of the applied chemicals must be questioned, (b) imprinting related to olfaction may be based on a weak theoretical foundation, (c) returns obtained in census experiments may be adequately explained through ecological interpretations, and (d) behavioural preferences obtained from exposure to non-natural compounds may be founded on mechanisms not associated with homing. (8) A logical link between the use of olfaction and the role of genetics in salmonid homing is emphasized, together with its practical implications for salmonid management.     

Repeated antipredator conditioning: a pathway to habituation or to better avoidance?

Hatchery‐reared juveniles of Arctic charr Salvelinus alpinus were conditioned to the odours of Arctic charr‐fed pikeperch Sander lucioperca in the absence of any other cues. Accordingly, there was no physical threat of capture for the Arctic charr. It was evident from the subsequent survival tests that a single exposure to predator odours was enough to increase Arctic charr survival compared to predator‐naïve control fish whist under direct threat from live predators. Instead of habituating to predator odours, the fish conditioned repeatedly (four times) improved their spatial avoidance of predator cues in the course of training. The repeated conditioning also further enhanced the survival of the test fish as compared to the singly conditioned fish. The economical and ethical advantages of training with chemical cues, combined with its high reliability, could promote the success of fish reintroductions especially through repeated antipredator conditioning.     

Factors affecting the recognition of population-specific odours by juvenile coho salmon*

Juvenile coho salmon Oncorhynchus kisutch from the Quinsam, Big Qualicum and Puntledge Rivers, British Columbia, Canada, discriminated between the chemical emanations of similarly aged salmon from their own and another population. However, common rearing during the embryonic, larval and early free-swimming stages rendered families more attractive to each other than they were otherwise. Preference among populations was also influenced by quantity of odour produced by the fish. Some fish, notably the Quinsam River population, appeared to produce greater quantities of attractants than other fish. Finally, the salmon also preferred water conditioned by faeces of members of their own population over blank water and, in one of two experiments, over water conditioned by faeces of non-population members, suggesting that at least some of the odourants mediating intraspecific discriminations are present in faeces. These results confirm earlier studies demonstrating that salmonid populations differ in odours distinguishable by conspecifics but indicate that experiments investigating this phenomenon must be designed carefully to avoid bias owing to differences other than population-specific traits. The role of population recognition in the lives of salmonids is unclear; it might be a manifestation of more general imprinting for homing, of sibling recognition, or it might play a role in mate choice.     

Interlocus variance of F(ST) provides evidence for directional selection over an olfactory receptor gene in Coho salmon (Oncorhynchus kisutch) populations

Coho salmon (Oncorhynchus kisutch) utilize olfactory cues to recognize and home to natal streams during spawning migrations. Chemically distinct river systems may promote directional selection for appropriately tuned olfactory receptor repertoires among Coho populations. Here, we use F_ST outlier methods to test for a signal of selection over olfactory receptor gene-linked markers, characterized in Coho populations from four geographically proximate, but ecologically distinct rivers. We report evidence for directional selection over one such marker, OkiOR3001, and document substantially higher levels of genetic structure among Coho populations from Oregon coastal lakes than previously observed with putatively neutral microsatellites.     

Residence time and habitat use of coho salmon in Humboldt Bay, California: an acoustic telemetry study

We monitored the movement of coho salmon (Oncorhynchus kisutch) smolts with acoustic transmitters from freshwater, through the freshwater/estuary ecotone, through the estuary, and to ocean entry to determine residence time and habitat use in Humboldt Bay, California. Tagged fish were monitored with a fixed receiver network and mobile tracking conducted from a boat. Coho salmon observed during the two-year study resided in Humboldt Bay beginning at least as early as late April and resided through the beginning of July. Coho salmon smolts spent more time in the freshwater/estuary ecotone compared to the lower estuary and spent an average of 10–12 days migrating to Humboldt Bay. Coho salmon smolts resided in Humboldt Bay, a marine embayment, for an average of 15–22 days prior to leaving the bay for the open ocean. Coho salmon smolts, as observed from mobile tracking, used deep channels and channel margins more often than floating eelgrass mats, pilings, and docks. In addition, tagged fish were more often detected in the central portions of Humboldt Bay characterized by deep channels with narrow intertidal margins. There were fewer detections in other portions of the bay characterized by shallow channels with large intertidal mudflats and eelgrass meadows. Relatively short transmitter life (70 days) precluded determining the latest date of coho salmon smolt residency in Humboldt Bay. In addition, tag size limited use to the largest emigrating smolts and may not represent the behaviors of the smaller-sized smolts which were more abundant.     

Season- and size-dependent risk taking in juvenile coho salmon: experimental evaluation of asset protection

Using juvenile coho salmon, Oncorhynchus kisutch, we tested predictions arising from dynamic optimization models of foraging under predation risk. Coho juveniles from two size groups raised in the laboratory were individually fed varying food rations. Their willingness to risk predation was measured as the time to resume foraging after presentation of a predator model. Small fish (mean weight 1.5 g) resumed feeding earlier than larger fish (3.5 g) as predicted by dynamic models under summer photoperiod but not under autumn photoperiod. Contrary to predictions, larger fish did not increase risk taking and small fish decreased risk taking between summer and autumn treatments. Food ration significantly influenced time to resume feeding only in small coho. A simple mechanistic model we proposed to explain feeding motivation under risk as a function of body size and prior growth rate was not sufficient to explain observed variation in risk taking. This study suggests that coho salmon use photoperiod and their own body size as cues for long-term, state-dependent adjustments of feeding behaviour. The lower risk taking of larger fish is probably an example of asset protection, whereby larger animals accept less predation risk to protect their greater accumulated fitness value. The decrease of risk taking in small fish in the autumn was possibly caused by a switch of life history trajectory towards delayed smolting. Copyright 1999 The Association for the Study of Animal Behaviour.     

Chinook and Coho salmon hybrids linked to habitat and climatic changes on Vancouver Island,British Columbia

Between 2013 and 2019, 63 presumed Chinook salmon Oncorhynchus tshawytscha sampled primarily in the Strait of Georgia (0.63% of total sample) were identified as potential Chinook–Coho (Oncorhynchus kisutch) hybrids by the presence of anomalous microsatellite genotypes. Their hybrid origin was confirmed by single nucleotide polymorphism amplification of two species‐specific amplicons. Mitochondrial DNA indicated that most of these fish resulted from the hybridization of Coho salmon females and Chinook salmon males. Although no diagnostic external features were identified, several individuals displayed an abnormal scale arrangement on the caudal peduncle. One hybrid juvenile examined for meristics exhibited a pyloric caeca count intermediate between published values for Chinook and Coho salmon. Most hybrids originated in the Cowichan River during the 2014 brood year. Their prevalence in the watershed is a naturally occurring event, likely exacerbated by prolonged low water levels which limit habitat and delay Chinook salmon spawning, in addition to the differential abundance of the parental species. This research is the first to document ongoing natural hybridization (Chinook–Coho salmon crosses) and link it to habitat and climatic changes, and includes the identification of eight F1 adults and two juvenile backcross or F2 hybrids. The potential negative impacts of hybridization, particularly in Coho salmon through potential introgression, warrant hybrid identification as an ecosystem monitoring tool within a survey program.     

Underwater Video Reveals Strong Avoidance of Chemical Alarm Cues by Prey Fishes

A diversity of fishes release chemical cues upon being attacked by a predator. These cues, commonly termed alarm cues, act as sources of public information warning conspecifics of predation risk. Species which are members of the same prey guild (i.e. syntopic and share predators) often respond to one another's alarm cues. The purpose of this study was to discriminate avoidance responses of fishes to conspecific alarm cues and cues of other prey guild members from responses to unknown damaged fish odours and novel odours. We used underwater video to measure avoidance responses of freshwater littoral species, namely fathead minnows (Pimephales promelas), finescale dace (Chrosomus neogaeus), and brook stickleback (Culaea inconstans), to both injured fish cues and novel non‐fish odours. The cyprinids (minnows and dace) showed significant avoidance of minnow cues over swordtail cues, morpholine, and the control of distilled water and tended to avoid fathead cues over cues of known prey guild members (stickleback). Cyprinids also significantly avoided cues of stickleback over unknown heterospecific cues (swordtail) and tended to avoid stickleback cues over morpholine and the distilled water control. Stickleback significantly avoided fathead minnow extract over the distilled water and tended to avoid stickleback and swordtail over distilled water. We conclude that fishes in their natural environment can show dramatic changes in behaviour upon exposure to alarm cues from conspecifics and prey guild members. These responses do not represent avoidance of cues of any injured fish or any novel odour.     

Olfactory navigation during spawning migrations: a review and introduction of the Hierarchical Navigation Hypothesis

Migrations are characterized by periods of movement that typically rely on orientation towards directional cues. Anadromous fish undergo several different forms of oriented movement during their spawning migration and provide some of the most well‐studied examples of migratory behaviour. During the freshwater phase of the migration, fish locate their spawning grounds via olfactory cues. In this review, we synthesize research that explores the role of olfaction during the spawning migration of anadromous fish, most of which focuses on two families: Salmonidae (salmonids) and Petromyzontidae (lampreys). We draw attention to limitations in this research, and highlight potential areas of investigation that will help fill in current knowledge gaps. We also use the information assembled from our review to formulate a new hypothesis for natal homing in salmonids. Our hypothesis posits that migrating adults rely on three types of cues in a hierarchical fashion: imprinted cues (primary), conspecific cues (secondary), and non‐olfactory environmental cues (tertiary). We provide evidence from previous studies that support this hypothesis. We also discuss future directions of research that can test the hypothesis and further our understanding of the spawning migration.     

A comprehensive hypothesis on the migration of European glass eels (Anguilla anguilla)

The European eel (Anguilla anguilla) is a catadromous fish that spawns in the Sargasso Sea. As larvae, eels cross the Atlantic Ocean and reach the continental slope of Europe, where they metamorphose into post‐larval glass eels. These reach the continent, where some enter fresh water, some remain in marine waters, and others move between fresh and marine waters. After 5–25 years, as adult silver eels, they migrate back from fresh water to the Sargasso Sea to spawn and die. The glass eel stage is a critical step during which the eels cross the continental shelf and recruit to estuaries, where they facultatively transition to fresh water. Extensive research has been conducted to understand the behavioural mechanisms and environmental cues that aid and guide glass eels' migration. Glass eels follow odours and salinity gradients, they avoid light, and they change orientation and depth according to the tides. Recent work revealed that European glass eels also use Earth's magnetic field and lunar cues to orient. However, while we understand many aspects of their orientation behaviour, a unifying theory describing how glass eels migrate from the continental slope to fresh water is lacking. The goal of this review is to develop a comprehensive hypothesis on the migration of European glass eels, integrating previous knowledge on their orientation behaviour with recent findings on magnetic and celestial orientation. This review follows the journey of a hypothetical glass eel, describing the nature and the role of orientation cues involved at each step. I propose that, although glass eels have the sensory capacity to use multiple cues at any given time, their migration is based on a hierarchical succession of orientation mechanisms dictated by the physical properties of the environments that they occupy: (i) lunar and magnetic cues in pelagic water; (ii) chemical and magnetic cues in coastal areas; and (iii) odours, salinity, water current and magnetic cues in estuaries.     

Development of the olfactory system of the white sucker,Catostomus commersoni,in relation to imprinting and homing: a comparison to the salmonid model

Synopsis White suckers,Catastomus commersoni, use olfactory cues to return to the same spawning stream year after year. If we assume that they follow a model similar to the well-known salmon model, olfactory imprinting must occur very early in their development. We describe the time of migration from the nursery stream in relation to the development of the white sucker olfactory system to determine if the requisite anatomical structures are present which would permit imprinting. At hatching the olfactory placode is present and beginning to differentiate, the lumen of the olfactory capsule is starting to form, and the olfactory tract projects into the telencephalon. Larvae migrate approximately 2 weeks later or at a size of 14 mm TL. At this time olfactory cilia are present, the olfactory tract is robust and the telencephalon is beginning to differentiate. Therefore, it appears that the fundamental neural structures necessary for imprinting are present. A comparison with salmon, however, clearly demonstrates that the white sucker olfactory apparatus is not as well developed as that of salmon at time of migration. This raises the question of the ability of white suckers to imprint in the same manner as salmon and whether the salmonid model is applicable to white suckers. Alternative imprinting hypotheses are discussed.     

Prey naivety in the behavioural responses of juvenile Chinook salmon (Oncorhynchus tshawytscha) to an invasive predator

1. Non‐native predators might inflict proportionally higher mortality on prey that have no previous experience of them, compared to species that have coexisted with the predator for some time. 2. We tested whether juvenile Chinook salmon (Oncorhynchus tshawytscha) were less able to recognise a non‐native than a native predator, by investigating behavioural responses to the chemical cues of the invasive smallmouth bass (Micropterus dolomieu) and the native northern pikeminnow (Ptychocheilus oregonensis) in both laboratory and field experiments. 3. Laboratory results demonstrated strong innate antipredator responses of individual juvenile Chinook salmon to northern pikeminnow; fish spent 70% of time motionless and exhibited 100% greater panic response than in controls. By contrast, antipredator responses to the chemical cues of smallmouth bass did not differ from controls. 4. These results were supported by similar differences in recognition of these predator odours by groups of juvenile Chinook salmon in fully natural conditions, though responses reflected a greater range of antipredator behaviours by individuals. In field trials, responses to northern pikeminnow odour resulted in increased flight or absence, reductions in swimming and foraging, and increased time spent near the substratum, compared to smallmouth bass odour. 5. Given that survival of juvenile fish is facilitated by predator recognition, our results support the hypothesis that naivety may be an important factor determining the effect of non‐native predators on prey populations. Efforts to manage the effect of native and non‐native predators may benefit by considering complex behavioural interactions, such as these at the individual and group levels.     

Riverine movements of hatchery-reared Atlantic salmon (Salmo salar) upon return as adults

Synopsis Hatchery-reared Atlantic salmon returning as adults to Maine's Penobscot River drainage basin were tagged with radio transmitters to permit long-term observation of their movements. Locations of salmon carrying small stomachemplaced transmitters were periodically determined primarily from an airplane; canoes and road vehicles were also used. Objectives were to determine the patterns, routes and rates of salmon movement; to assess the effect of dams on the migration; and to compare the behavior of salmon that had been imprinted as smolts to headwaters with that of salmon released as smolts near the head of tide. No consistent pattern of salmon movement emerged. Movement was erratic with wandering both up and downstream interspersed with position holding. A weak seasonal aspect to the movement was detected, with the minimum numbers moving in early September and the rates and distances of movement decreasing as the season progressed. Salmon often remained at various locations in the rivers for periods of time before subsequently moving. Salmon were also apparently impeded by dams, as on numerous occasions they were observed to approach a dam, then move back downstream. Some differences in behavior were found between the salmon imprinted as smolts to headwaters and those released as smolts at head of tide. Several imprinted salmon homed to a particular tributary when unimpeded by dams or homed by surmounting a dam, and several moved up to the base of the dam. Few unimprinted salmon moved up that tributary. The variable behavior and lack of strong upstream movement may be due to the salmon's lack of genome adapted to the Penobscot River drainage, the scarcity of conspecifics with their possible pheromonal influence, and the lack of a home stream and concomitant motivation to stimulate unimprinted salmon to progress upstream.