Sensory mechanisms of natal stream imprinting and homing in Oncorhynchus spp.

Juvenile Oncorhynchus spp. can memorise their natal stream during downstream migration; juveniles migrate to feed during their growth phase and then they migrate long distances from their feeding habitat to their natal stream to reproduce as adults. Two different sensory mechanisms, olfaction and navigation, are involved in the imprinting and homing processes during short-distance migration within the natal stream and long-distance migration in open water, respectively. Here, olfactory functions are reviewed from both neurophysiological studies on the olfactory discrimination ability of natal stream odours and neuroendocrinological studies on the hormonal controlling mechanisms of olfactory memory formation and retrieval in the brain. These studies revealed that the long-term stability of dissolved free amino-acid composition in the natal stream is crucial for olfactory imprinting and homing. Additionally, the brain–pituitary–thyroid and brain–pituitary–gonadal hormones play important roles in olfactory memory formation and retrieval, respectively. Navigation functions were reviewed from physiological biotelemetry techniques with sensory interference experiments during the homing migration of anadromous and lacustrine Oncorhynchus spp. The experiments demonstrated that Oncorhynchus spp. used compass navigation mechanisms in the open water. These findings are discussed in relation to the sensory mechanisms involved in natal stream imprinting and homing in Oncorhynchus spp.     

Evidence of Atlantic salmon Salmo salar fry movement between fresh water and a brackish environment

This study reports descent of Atlantic salmon Salmo salar fry from their natal streams to brackish waters of the Baltic Sea and their use of this environment as an alternative rearing habitat before ascending back to freshwater streams. To the authors' knowledge, residency in a brackish environment has not previously been demonstrated in S. salar fry. Recruitment success and evolutionary significance of this alternative life‐history strategy are presently not known.     

Morphometric and ultrastructural comparison of the olfactory system in elasmobranchs: The significance of structure–function relationships based on phylogeny and ecology

This study investigated the relationship between olfactory morphology, habitat occupancy, and lifestyle in 21 elasmobranch species in a phylogenetic context. Four measures of olfactory capability, that is, the number of olfactory lamellae, the surface area of the olfactory epithelium, the mass of the olfactory bulb, and the mass of the olfactory rosette were compared between individual species and groups, comprised of species with similar habitat and/or lifestyle. Statistical analyses using generalized least squares phylogenetic regression revealed that bentho‐pelagic sharks and rays possess significantly more olfactory lamellae and larger sensory epithelial surface areas than benthic species. There was no significant correlation between either olfactory bulb or rosette mass and habitat type. There was also no significant difference between the number of lamellae or the size of the sensory surface area in groups comprised of species with similar diets, that is, groups preying predominantly on crustaceans, cephalopods, echinoderms, polychaetes, molluscs, or teleosts. However, some groups had significantly larger olfactory bulb or rosette masses than others. There was little evidence to support a correlation between phylogeny and morphology, indicating that differences in olfactory capabilities are the result of functional rather than phylogenetic adaptations. All olfactory epithelia exhibited microvilli and cilia, with microvilli in both nonsensory and sensory areas, and cilia only in sensory areas. Cilia over the sensory epithelia originated from supporting cells. In contrast to teleosts, which possess ciliated and microvillous olfactory receptor types, no ciliated olfactory receptor cells were observed. This is the first comprehensive study comparing olfactory morphology to several aspects of elasmobranch ecology in a phylogenetic context. J. Morphol., 2008. © 2008 Wiley‐Liss, Inc.     

Stimulus-specific development of learning ability during habitat shift in pre to post-recruitment stage jack mackerel

Marine fishes often experience major habitat shifts during their life history, and previous studies have shown that the learning capability of fish change ontogenetically and in accordance with such habitat shifts. However, because all of these studies used a single type of conditioned stimuli (CS), they failed to detect qualitative changes in learning capability. Here we tested the hypothesis that preparedness for learning changes ontogenetically in jack mackerel Trachurus japonicus, which undergo a drastic change in habitat preference during their life history as they move from offshore pelagic waters to coastal and demersal rocky reefs. Groups of juveniles measuring 40 mm standard length (SL) (pelagic stage) and 60 mm SL (demersal stage) were conditioned to food rewards in response to three different CS; the presence of a surface structure, mid-water structure, and aeration. The results showed that small juveniles tended to become conditioned to the surface stimulus faster than they did to the mid-water stimulus. Conversely, large juveniles responded to the mid-water stimulus significantly more quickly than they did to the surface stimulus. These results suggest that stimulus-specific learning capability in T. japonicus changes ontogenetically, facilitating adaptation to their life-history strategy.     

Gene expression of neuronal soluble N-ethylmaleimide-sensitive factor attachment protein receptor complex components in the olfactory organ and brain during seaward and homeward migration by pink salmon (Oncorhynchus gorbuscha)

The expression of synaptic vesicle exocytosis-regulator SNARE complex component genes (snap25, stx1 and vamp2) was examined in the olfactory nervous system during seaward and homeward migration by pink salmon (Oncorhynchus gorbuscha). The expression levels of snares in the olfactory organ were higher in seaward fry than in feeding and homeward adults, reflecting the development of the olfactory nervous system. The expression of snap25a, b and stx1a was upregulated or stable in the adult olfactory bulb and telencephalon. This upregulated expression suggested alterations in olfactory neuronal plasticity that may be related to the discrimination of natal rivers. The expression of stx1b was downregulated in the adult olfactory bulb, but remained stable in the adult telencephalon. The expression of vamp2 was initially strong in seaward fry, but was downregulated in adults in both the olfactory bulb and telencephalon. Pink salmon has the lowest diversity of maturation age, the largest population, and the most evolutional position in Pacific salmon (genus Oncorhynchus). The expression of snares in the olfactory center of pink salmon reflected the timing of sexual maturation and homeward migration. The present results and our previous studies indicate that snares show distinct expression patterns between two salmon species that depend on physiological and ecological features of migration.     

Elevated CO2 impairs olfactory‐mediated neural and behavioral responses and gene expression in ocean‐phase coho salmon (Oncorhynchus kisutch)

Elevated concentrations of CO₂ in seawater can disrupt numerous sensory systems in marine fish. This is of particular concern for Pacific salmon because they rely on olfaction during all aspects of their life including during their homing migrations from the ocean back to their natal streams. We investigated the effects of elevated seawater CO₂ on coho salmon (Oncorhynchus kisutch) olfactory‐mediated behavior, neural signaling, and gene expression within the peripheral and central olfactory system. Ocean‐phase coho salmon were exposed to three levels of CO₂, ranging from those currently found in ambient marine water to projected future levels. Juvenile coho salmon exposed to elevated CO₂ levels for 2 weeks no longer avoided a skin extract odor that elicited avoidance responses in coho salmon maintained in ambient CO₂ seawater. Exposure to these elevated CO₂ levels did not alter odor signaling in the olfactory epithelium, but did induce significant changes in signaling within the olfactory bulb. RNA‐Seq analysis of olfactory tissues revealed extensive disruption in expression of genes involved in neuronal signaling within the olfactory bulb of salmon exposed to elevated CO₂, with lesser impacts on gene expression in the olfactory rosettes. The disruption in olfactory bulb gene pathways included genes associated with GABA signaling and maintenance of ion balance within bulbar neurons. Our results indicate that ocean‐phase coho salmon exposed to elevated CO₂ can experience significant behavioral impairments likely driven by alteration in higher‐order neural signal processing within the olfactory bulb. Our study demonstrates that anadromous fish such as salmon may share a sensitivity to rising CO₂ levels with obligate marine species suggesting a more wide‐scale ecological impact of ocean acidification.     

Interspecific relationships between emerging Atlantic salmon, Salmo salar, and coho salmon, Oncorhynchus kisutch, juveniles

Interspecific relationships between Atlantic salmon and coho salmon were studied at early life stages in laboratory and semi-natural stream channels. During emergence, the survival and dispersal patterns were similar for the two species in single or mixed populations. Survival of Atlantic salmon fry was reduced in the presence of older coho fry. However, no predation was observed. Microdistribution differed between the two species, with Atlantic salmon fry more numerous in riffles when coho were present.
Coho juveniles had a pelagic and gregarious distribution, in contrast to the benthic behaviour of the Atlantic salmon. In laboratory streams, Atlantic salmon fry moved out or adopted a subordinate cryptic behaviour which allowed them to escape predation while negatively affecting their growth.     

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.     

The role of olfaction throughout juvenile development: Functional adaptations in elasmobranchs

Seven elasmobranch species, a group known for their highly‐developed sense of smell, were examined for developmental changes in the number of olfactory lamellae, the size of the surface area of the sensory olfactory epithelium and the mass of both the olfactory rosettes (primary input to the CNS), and the olfactory bulbs. Within each species, juveniles possessed miniature versions of the adult olfactory organs, visually not distinguishable from these and without any obvious structural differences (e.g., with respect to the number of lamellae and the extent of secondary folding) between differently sized individuals. The size of the olfactory organs was positively correlated with body length and body mass, although few species showed proportional size scaling. In Aetobatus narinari and Aptychotrema rostrata, olfactory structures increased in proportion to body size. With respect to the growth of the olfactory bulb, all species showed allometric but not proportional growth. Olfaction may be of particular importance to juveniles in general, which are often subjected to heavy predation rates and fierce inter/intraspecific competition. Accordingly, it would be advantageous to possess a fully functional olfactory system early on in development. Slow growth rates of olfactory structures could then be attributed to a greater reliance on other sensory systems with increasing age or simply be regarded as maintaining an already optimized olfactory system. J. Morphol., 2010. © 2009 Wiley‐Liss, Inc.     

Habitat fragmentation by damming threatens coexistence of stream-dwelling charr and salmon in the Fuji River,Japan

Habitat fragmentation by damming can affect the persistence of single species population and also coexistence of two or more species through intensified competition. This study examined the effects of habitat fragmentation by damming on the coexistence of two stream-dwelling salmonids: the southern form of white-spotted charr (Salvelinus leucomaenis japonicus) and the red-spotted masu salmon (Oncorhynchus masou ishikawae). We examined charr, salmon, and dam distributions in 27 streams of the Fuji River basin, central Japan. In the 1970s, there were streams with five sympatric and 22 allopatric populations (n = 13 for charr, n = 9 for salmon). However, from the 1970s to 2004, 356 impassable dams were constructed in the surveyed streams, and four of the five sympatric streams became allopatric. In the extant sympatric stream, more than 20 dams fragmented habitat. Species distributions were separated by dams (with decreasing altitude) in the following order: extirpation area, charr-dominant area, and salmon-dominant area. Within the uppermost sympatric section (i.e., situated between the dams), salmon congregated in the largest uppermost pool just below the dam; despite these conditions, salmon frequency increased in the downstream direction at the stream scale. The results suggest that habitat fragmentation threatens the coexistence of stream-dwelling charr and salmon at both the basin and stream scales. We believe that exclusion of one species by another is likely in extremely fragmented habitats with minimal gradients and little variation in physical conditions (through reduced stream gradient and increased sand sedimentation caused by damming). In addition, multiple sites of damming ensure that there are no salmonid refuges from the collapse of metapopulation structure. In such fragmented habitats, even small tributaries serve important roles, as they are used mainly by salmonid fry and juveniles. We propose that habitats of native salmonids should be maximized by reconnecting fragmented habitats as part of a broader management plan.     

Surface ultrastructure of the olfactory rosette of an air-breathing catfish,Heteropneustes fossilis (Bloch)

The surface architecture of the olfactory rosette ofHeteropneustes fossilis (Bloch) has been studied by scanning electron microscopy. The olfactory rosette is an oval structure composed of a number of lamellae arranged pinnately on a median raphe. The raphe is invested with epithelial cells and pits which represent goblet cell openings. On the basis of cellular characteristics and their distribution the lateral surface of each olfactory lamella is identified as sensory, ciliated non-sensory and non-ciliated non-sensory epithelium. The sensory epithelium is provided with receptor and supporting cells. The ciliated non-sensory epithelium is covered with dense cilia obscuring the presence of other cell types. The non-ciliated non-sensory epithelium is with many polygonal areas containing cells.     

Olfactory gene expression in migrating adult sockeye salmon Oncorhynchus nerka

Expression of 12 olfactory genes was analysed in adult sockeye salmon Oncorhynchus nerka nearing spawning grounds and O. nerka that had strayed from their natal migration route. Variation was found in six of these genes, all of which were olfc olfactory receptors and had lower expression levels in salmon nearing spawning grounds. The results may reflect decreased sensitivity to natal water olfactory cues as these fish are no longer seeking the correct migratory route. The expression of olfactory genes during the olfactory‐mediated spawning migration of Pacific salmon Oncorhynchus spp. is largely unexplored and these findings demonstrate a link between migratory behaviours and olfactory plasticity that provides a basis for future molecular research on salmon homing.     

Development of a unique eye: photoreceptors of the pelagic predator Atlanta peroni (Gastropoda, Heteropoda)

 The eyes of different larval stages and juveniles of Atlanta peroni are generally composed of a cornea, a lens and a retina. In juveniles a distinct pigmented shield is visible and an enormous humour is located behind the lens. Larvae have only two sensory cells and the photoreceptors are of the ciliary type. In juveniles a striking feature is the shape of the retina. It is ribbon-shaped and new sensory cells are present which are arranged in three rows. The photoreceptors are of the ciliary type as well. Contrary to the arrangement in larvae, the ciliary plasmalemma in juveniles forms numerous lamellar stacks. In accordance with the sensory cells the stacks are organized in three parallel rows. The lamellae of adjacent stacks within a row overlap each other. The latter unique feature has not yet been found in any other representative of the Heteropoda. These findings demonstrate that (a) the eyes are altered during the development from larvae into juveniles, (b) the larval sensory cells are reduced and replaced by new sensory cells in juveniles and (c) the eyes of juvenile and adult A. peroni are well adapted for their life as visual predators. Accepted: 20 February 1999     

Using otolith chemical and structural analysis to investigate reservoir habitat use by juvenile Chinook salmon Oncorhynchus tshawytscha

Isotopic composition of ⁸⁷Sr:⁸⁶Sr and natural elemental tracers (Sr, Ba, Mg, Mn and Ca) were quantified from otoliths in juvenile and adult Chinook salmon Oncorhynchus tshawytscha to assess the ability of otolith microchemistry and microstructure to reconstruct juvenile O. tshawytscha rearing habitat and growth. Daily increments were measured to assess relative growth between natal rearing habitats. Otolith microchemistry was able to resolve juvenile habitat use between reservoir and natal tributary rearing habitats (within headwater basins), but not among catchments. Results suggest that 90% (n = 18) of sampled non‐hatchery adults returning to the Middle Fork Willamette River were reared in a reservoir and 10% (n = 2) in natal tributary habitat upstream from the reservoir. Juveniles collected in reservoirs had higher growth rates than juveniles reared in natal streams. The results demonstrate the utility of otolith microchemistry and microstructure to distinguish among rearing habitats, including habitats in highly altered systems.     

Cortisol and Pacific Salmon: A New Look at the Role of Stress Hormones in Olfaction and Home-stream Migration

Pacific salmon (genus Oncorhynchus) exhibit an interesting anduncommon life-history pattern that combines semelparity, anadromy,and navigation (homing). During smoltification, young salmonimprint on the chemical composition of their natal stream water(the home-stream olfactory bouquet or "HSOB"); they then migrateto the ocean where they spend a few years feeding prior to migratingback to their natal freshwater stream to spawn. Upstream migrationis guided by the amazing ability to discriminate between thechemical compositions of different stream waters and thus identifyand travel to their home-stream. Pacific salmon demonstratemarked somatic and neural degeneration changes during home-streammigration and at the spawning grounds. The appearance of thesepathologies is correlated with a marked elevation in plasmacortisol levels. While the mechanisms of salmonid homing arenot completely understood, it is known that adult salmon continuouslyutilize two of their primary sensory systems, olfaction andvision, during homing. Olfaction is the primary sensory systeminvolved in freshwater homing and "HSOB" recognition, and willbe emphasized here. Previously, we proposed that the increasein plasma cortisol during Pacific salmon home-stream migrationis adaptive because it enhances the salmon's ability to recallthe imprinted memory of the "HSOB" (Carruth, 1998; Carruth etal., 2000b). Elevated plasma concentrations of cortisol couldprime the hippocampus or other olfactory regions of the brainto recall this memory and, therefore, aid in directing the fishto their natal stream. Thus, specific responses of salmon tostressors could enhance reproductive success.     

Ontogenetic changes in habitat selection during settlement in a coral reef fish: ecological determinants and sensory mechanisms

The behavior of marine larvae during and after settlement can help shape the distribution and abundance of benthic juveniles and therefore the intensity of ecological interactions on reefs. Several laboratory choice-chamber experiments were conducted to explore sensory capabilities and behavioral responses to ecological stimuli to better understand habitat selection by “pre-metamorphic” (larval) and “post-metamorphic” (juvenile) stages of a coral reef fish (Thalassoma hardwicke). T. hardwicke larvae were attracted to benthic macroalgae (Turbinaria ornata and Sargassum mangarevasae), while slightly older post-metamorphosed juveniles chose to occupy live coral colonies (Pocillopora damicornis). Habitat choices of larvae were primarily based upon visual cues and were not influenced by the presence of older conspecifics. In contrast, juveniles selected live coral colonies and preferred those occupied by older conspecifics; choices made by juveniles were based upon both visual and olfactory cues from conspecifics. Overall, the laboratory experiments suggest that early life-history stages of T. hardwicke use a range of sensory modalities that vary through ontogeny, to effectively detect and possibly discriminate among different microhabitats for settlement and later occupation. Habitat selection, based upon cues provided by environmental features and/or by conspecifics, might have important consequences for subsequent competitive interactions.     

Gross brain morphology of the armoured catfish Rineloricaria heteroptera,Isbrücker and Nijssen (1976), (Siluriformes: Loricariidae: Loricariinae): A descriptive and quantitative approach

The gross morphology of the brain of Rineloricaria heteroptera and its relation to the sensory/behavioural ecology of the species is described and discussed. The sexual and ontogenetic intraspecific variation in the whole brain length and mass, as well as within/between the eight different brain subdivisions volumes, is also examined and discussed. Negative allometry for the whole brain length/mass and relative growth of the telencephalon and optic tecta was observed. Positive allometry was observed for the relative growth of the olfactory bulbs and medulla oblongata . Univariate and multivariate statistical analyses did not reveal significant differences in the brain subdivision growth rates among sexes and/or developmental stages, except for the optic tectum and some portions of the medulla oblongata , with juveniles and males showing more developed optic tecta and medullary subdivisions, respectively. The growth rates for each brain subdivision were relatively constant, and the slopes of the growth equations were almost parallel, except for those of the olfactory bulbs and medulla oblongata subdivisions, suggesting some degree of tachyauxesis of subdivisions against the entire brain. The corpus cerebelli was the more voluminous brain subdivision in most specimens (principally adults), followed by the optic tectum (the more voluminous subdivision in juveniles), hypothalamus, and telencephalon, in that order. Differences in the number of lamellae and relative size of the olfactory organ were also detected among developmental stages, which were more numerous and larger in adults. Based on these results, it is possible to infer an ontogenetic shift in the habitat/resource use and behaviour of R. heteroptera . Vision, primarily routed through the optic tectum, could be fundamental in early stages, whereas in adults, olfaction and taste, primarily routed through the olfactory bulbs and medulla oblongata , play more important roles.     

Anatomy and morphometry of the olfactory organ of the wels Silurus glanis L. (Siluridae, Pisces)

The anatomical structure of the olfactory organs, nerve tracts and brain was described in Silurus glanis. The changes connected with aging were considered. The olfactory lamellae are thin and tightly set in a rosette. In the 1 year old individuals there are 48...51 lamellae in a single rosette. This number increases gradually with age and in the 9...10 year old welses reaches 150. The surface area of the lamellae of a single rosette also indicates an increase: in the 1 year old specimen it equals 117 mm2, while in the adult individual (5...6 year old)--1040 mm2. This is due to the increase in both the size of each lamella and the number of the lamellae. The obtained results are discussed with regard to other author's data. It has been found that the dynamics of the increase of the surface area of the olfactory epithelium in fish are closely related to the way of life and not to the systematic affiliation of the species.