Pacific salmon migrations and homing: mechanisms and adaptive significance

Pacific salmon are noted for their lengthy foraging migrations and for their precise homing ability. Extensive sampling has documented the general migratory patterns of the major populations, but many basic aspects of their marine ecology are still poorly understood. Their life history pattern has been interpreted as an adaptation to exploit the higher productivity of the marine environment over that in fresh water. The adaptive significance of homing is implied by the specializations of populations for their natal habitat and the competitive superiority of locally adapted populations over transplants from other rivers. However, the establishment of new populations by strays and the levels of gene flow between natural populations have only recently received much attention. Research on salmon migrations has also focused on the mechanisms that guide homing at sea and in fresh water. While salmon have highly developed sensory systems, the ways in which inputs are integrated to guide migration through diverse and complex habitats are still being investigated.     

Anadromy and the marine migrations of Pacific salmon and trout: Rounsefell revisited

Anadromy is a defining trait in salmonid fishes but it is expressed to different extents among the species in the family, as reviewed in a classic paper by Rounsefell (1958). The present paper re-examines the subject, assessing the degree of anadromy within the genus Oncorhynchus, using Rounsefell’s six criteria: extent of migrations at sea, duration of stay at sea, state of maturity attained at sea, spawning habits and habitats, post-spawning mortality, and occurrence of freshwater forms of the species. The genus ranges from pink salmon (O. gorbuscha), the most fully anadromous species in the family, to entirely non-anadromous species closely related to rainbow trout (O. mykiss), including Mexican golden trout (O. chrysogaster), Gila and Apache trout (O. gilae), and sub-species of cutthroat trout (O. clarki). This paper provides updated information on anadromy and marine migration patterns, emphasizing the iteroparous species, cutthroat (O. clarki) and rainbow (O. mykiss) trout. These two species display widely ranging patterns of anadromy, including truly “landlocked” populations and residents with easy access to the sea. Anadromous rainbow trout (known as steelhead) populations also vary greatly in their distribution at sea, incidence of repeat spawning, and associated traits. We conclude, as did Rounsefell, that anadromy is not a single trait with two conditions (anadromous or non-anadromous). Rather, it reflects a suite of life history traits that are expressed as points along continua for each species and population. Further research is needed in the marine ecology of all species but especially trout, as they are less well known but apparently more variable in patterns of anadromy and life history than salmon species.     

Variation in responses to spawning Pacific salmon among three south-eastern Alaska streams

1. Pacific salmon are thought to stimulate the productivity of the fresh waters in which they spawn by fertilising them with marine‐derived nutrients (MDN). We compared the influence of salmon spawners on surface streamwater chemistry and benthic biota among three south‐eastern Alaska streams. Within each stream, reaches up‐ and downstream of barriers to salmon migration were sampled during or soon after spawners entered the streams. 2. Within streams, concentrations of dissolved ammonium and soluble reactive phosphorus (SRP), abundance of epilithon (chlorophyll a and ash‐free dry mass) and biomass of chironomids were significantly higher in reaches with salmon spawners. In contrast, biomass of the mayflies Epeorus spp. and Rhithrogena spp. was significantly higher in reaches lacking spawners. 3. Among streams, significant differences were found in concentrations of dissolved ammonium, dissolved organic carbon, nitrate and SRP, abundance of epilithon, and the biomass of chironomids and Rhithrogena. These differences did not appear to reflect differences among streams in spawner density, nor the changes in water chemistry resulting from salmon spawners. 4. Our results suggest that the ‘enrichment’ effect of salmon spawners (e.g. increased streamwater nutrient concentrations) was balanced by other concurrent effects of spawners on streams (e.g. sediment disturbance). Furthermore, the collective effect of spawners on lotic ecosystems is likely to be constrained by conditions unique to individual streams, such as temperature, background water chemistry and light attenuation.     

Using maximum heart rate as a rapid screening tool to determine optimum temperature for aerobic scope in Pacific salmon Oncorhynchus spp

The mean ±s.e. optimum temperature (T(opt)) for aerobic scope in juvenile coho salmon Oncorhynchus kisutch was determined to be 17·0 ± 0·7° C. The repeated measures protocol took 3 weeks to complete the T(opt) determination using 12 fish tested at five temperatures separated by 2° C increments. This experiment also demonstrated that the T(opt) was associated with maximum heart rate (f(H)) failing to maintain a Q(10) -related increase with temperature. When maximum f(H) was produced in anaesthetized fish with pharmacological stimulation and f(H) measured from electrocardiogram recordings during acute warming, the Arrhenius break temperature (ABT) for Q(10) discontinuities in maximum f(H) (mean ±s.e. = 17·1 ± 0·5° C for 15 ppm clove oil and 16·5 ± 0·2° C for 50 ppm MS-222) was statistically indistinguishable from the T(opt) measured using aerobic scope. Such a determination took only 3 days rather than 3 weeks. Therefore, it is proposed that determining ABT for discontinuities in maximum f(H) in anaesthetized fish presents itself as a valuable, high-throughput screening tool to assess T(opt) in fishes, a metric that has become recognized as being extremely valuable in fish biology and fisheries management.     

The Atlantic salmon in fresh water: spawning,rearing and production

Summary Fluvial salmonids have evolved to use the diversity of habitats in natural streams for different life history stages and at different seasons. Required freshwater habitat of Atlantic salmon can be classified generally as that suitable (i) for spawning, (ii) for feeding during the major growing period, and (iii) for overwintering.Spawning habitat of salmon is usually in rapid water at the tail of pools on the upstream edge of a gravel bar, ideally with depths about 25 cm, in mean water velocities of about 30–45 cm s^-1, with maximum velocities about 2 body lengths s^-1, and with a substrate of irregularly shaped stones of cobble, pebble, and gravel.Underyearling salmon (<7 cm TL) are most common in shallow (<15 cm) pebbly riffles, whereas older and larger parr (>7 cm TL) are usually in riffles deeper than 20 cm with a coarse substrate. Depth preference increases with size. Multiple linear regression models quantifying parr habitat have identified substrate as an important variable, with a positive relationship to an index of coarseness. Negative relationships were found with mean stream width, range of discharge, and overhanging cover. Water chemistry, especially alkalinity, nitrates, and phosphates, are important regulators of production. Although similar variables had importance, coefficients among rivers differed. Interactions occur among variables. Further studies are required to quantify productive capacity of habitat for parr. Results suggest that useful models can be derived and if a river system is mapped, and stratified by habitat, then smolt yield could be predicted and the required egg deposition could be estimated.In winter, young salmon shelter among coarse substrate or move to pools, but continue feeding, with larger parr being more active.Feeding is in general opportunistic. Food consists mainly of insects, taken primarily in the water column, but also from the surface and at the bottom. Young salmon in flowing water are highly territorial but are less so in slow or still waters. In fast water, parr use their large pectoral fins to apply themselves to the substrate, allowing them to occupy this type of habitat with little expenditure of energy. Height above the substrate decreases with water velocity, but increases with temperature and social status. Although riffles are preferred habitat, and are relatively more productive, lentic waters can be occupied where there are few predators or severe competitors and may provide significant smolt yield in some systems. Selective segregation minimizes competition between salmon and brook charr or brown trout, but brook charr and brown trout may have negative effects on underyearling salmon, and on parr in pools, whereas salmon have negative effects on small brook charr and brown trout in riffles and flats. Competition by both interference and exploitation results in interactive segregation when the resource, mainly food, becomes limiting.Limited downstream movement of underyearling salmon may occur during the summer. Older juveniles may make upstream movements, but generally migrate downstream, with most movements in the spring, and a lesser peak of activity in the autumn. Dispersal tends to be mainly downstream, indicating that for full distribution, spawning areas are best located upstream. High densities of yearling parr may have negative effects on growth and survival of underyearlings in some river systems, but apparently not in others, so that future research is required in this regard. Density-dependent growth is evident where food is limiting, and can provide an indicator of densities of cohorts so that if a quantitative relationship has been derived, mean size from a sample can give an estimate of the density at that station, with minimum size occurring at carrying capacity. Such regressions vary between habitats with differing productive capabilities, so that future research could provide useful models for assessing productive capacity of a habitat, and optimum densities. Life history strategies can change with changes in density-dependent growth rates. Present stock-recruitment functions do not take environmental variables into consideration, and have limited applicability. Further research is required to determine optimum spawning requirements for salmon in different types of river systems in different geographical areas.     

Environmental variability and the ecological effects of spawning Pacific salmon on stream biofilm

1. Variation in resource subsidies can create or reinforce heterogeneity in recipient ecosystems. Related activities of organisms delivering resource subsidies, such as ecosystem engineering by Pacific salmon spawners (Oncorhynchus spp.), also alter heterogeneity. We studied whether heterogeneity in stream environmental conditions and spawner abundances were reflected in the net ecological effects of salmon (i.e. enrichment by resource subsidies and disturbance by ecosystem engineering) on benthic biofilm. 2. We sampled seven Southeast Alaska streams over 3 years, both before and during the salmon run. In each stream and year, stream environmental characteristics and their influence on responses of benthic biofilm [mean and coefficient of variation of chlorophyll a (chl a), ash‐free dry mass (AFDM) and autotrophic index (AFDM:chl a)] to spawners were assessed. 3. Streams and periods before and during the salmon run were distinct based on their environmental characteristics. The responses of most biofilm metrics to spawners were stream‐ and year‐specific, suggesting that the ecological effect of spawners ranged from net enrichment to net disturbance depending on the stream or year studied. The environmental context, especially temperature, large wood, and sediment size, explained >50% of biofilm variability during the run, but <30% over the entire study, suggesting that salmon can alter environmental constraints. 4. Precision of biofilm estimates improved by increasing either the number of streams or the number of years sampled (i.e. spatial or temporal replication). However, combining data from different North Pacific Rim ecoregions inflated the confidence interval as compared with a single ecoregion, indicating the importance of regional environmental contexts for net salmon effects. 5. Our results suggest that biofilm responses to salmon can vary greatly, even within a single ecoregion, and that environmental conditions can modify net salmon effects. Consequently, generalisations about biofilm responses across the native range of salmon may be challenging.     

A comparison of cystatin activity in the various tissues of chum salmon Oncorhynchus keta between feeding and spawning migrations

• 1.1. Cystatin was found to be widely distributed in various tissues of chum salmon. Most of the cystatins in the salmon tissues appeared to have a molecular weight between 10,000 and 20,000. They were considered to belong to the low molecular weight form cystatin, the type 1 and/or type 2 cystatins.
• 2.2. The activity in the liver of the salmon in spawning migration was significantly higher than that of the fish in feeding migration, while the activities of the serum, kidney, intestine, stomach, gill, skin and white muscle in spawning migration were apparently lower than that of the fish in feeding migration.
• 3.3. Such differences in the cystatin activity were considered to relate closely to the physiological conditions such as sexual maturation and/or starvation during spawning migration of the fish.

     

Effects of overripening on spawning behaviour and reproductive success of Atlantic salmon females spawning in a controlled flow channel

The influence of overripening on salmonid egg quality has often been described in artificial breeding. However, no information exists on the impact of this factor on fish reproducing naturally, although it is likely to be critical, especially in disturbed environments. Pairs of Atlantic salmon in which the size of the male and the female was evenly matched were released in a spawning channel from 1 to 12 days after ovulation. Handling did not affect egg quality. Overripening had a negative effect on egg viability. Egg mortality, infertility and malformations increased with the number of days after ovulation. In females which had just matured, 16·7% of their recovered eggs were dead, 3·1% were unfertilized and 1·7% were malformed, as compared to 25·4, 9·7 and 5·4%, respectively, in females that had been mature for at least a week. Overripening played a role in both female spawning behaviour and capacity to spawn, as females which had been mature for over a week released their eggs more quickly while they retained more ova in their abdominal cavity than early spawning females. Thus, in studies of reproductive behaviour and in particular of sexual selection, it is critical to take into account the maturation status of females since the duration of spawning activity is used by various authors to determine female sexual motivation. Alternatively, overripening may decrease the female selectivity for mates.     

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.     

Daily feeding rhythm and rations of Pacific salmon of the genus Oncorhynchus in the period of marine prespawning migrations

The daily feeding rhythm and rations of the humpback salmon Oncorhynchus gorbuscha, the sockeyed salmon O. nerka, and the chum salmon O. keta during marine prespawning migrations is investigated with consideration of materials collected at daily stations in waters off eastern Kamchatka in June–July 1999 and 2001 (from catches of drift nets). The bulk of humpback salmon and sockeyed salmon food consists of euphausiids, hyperiids, large copepods, pteropods, and fish juveniles. In the food of chum salmon, pteropods dominated. In a 24-h period, salmon manifest a pronounced evening peak of stomach fullness, while at night feeding discontinues. Samples collected in the morning consisted of fish who had just started feeding after the night pause. In addition to nightly period of rest, all species manifested a daytime decrease in foraging activity, though less pronounced than in the night. The daily rhythm of Pacific salmons’s feeding depends on the vertical migrations of their food items (representatives of sound-scattering layers). During the marine feeding period, the most intensive feeding is recorded in the humpback salmon and chum salmon. The daily ration of the humpback salmon is lower than that of the chum salmon but includes animals of higher food value. Due to a high digestion rate in combination with a large stomach volume, the chum salmon can consume a large quantity of low-calorific food in a short time. The daily ration of the sockeyed salmon is considerably lower than that of other salmon species.     

Effects of Pacific salmon spawning and carcass availability on the caddisfly Ecclisomyia conspersa (Trichoptera: Limnephilidae)

1. The effects of spawning coho (Oncorhynchus kisutch) and chum salmon (Oncorhynchus keta) on the limnephilid caddisfly Ecclisomyia conspersa were evaluated by experimentally excluding salmon from the upper 14‐m stretch of a spawning channel by a wire‐meshed fence. Density, and development and growth rates, of larvae upstream of the fence (without salmon) were compared with those downstream (with salmon). 2. Larval density in the stretch with salmon declined during spawning, but increased again after spawning subsided and the carcasses of dead fish became available. In the stretch with salmon, larval density on salmon carcasses was seven to 37 times greater than on the adjacent channel substratum. The rate of larval development in the stretch with salmon was greater than that in the stretch without salmon. Two months after carcasses became available, 98% of larvae sampled from the stretch with salmon were in the fifth instar, compared to only 23% from the stretch without salmon. Body weight of E. conspersa in the stretches with and without salmon increased by an average of 3.04 and 2.38 mg, respectively, over a 6‐month period. 3. ¹⁵N values of larvae from the stretch with salmon increased following the arrival of the fish, suggesting that the larvae were feeding on salmon‐derived material, such as eggs and carcasses, which contain a high proportion of the heavier stable isotope. In contrast, ¹⁵N values of larvae from the stretch without salmon remained relatively constant throughout the experiment. The availability of salmon carcasses as a high‐quality food source late in larval development may increase survival and fecundity of E. conspersa. 4. These substantial differences were consistent with the view that they were due to the experimental exclusion of salmon and salmon carcasses from the upstream stretch, though the study was un‐replicated and thus precludes ascribing causation more definitely.     

Male size effects on fertilization success: lack of evidence in chinook salmon spawning under experimental conditions

Synopsis Anadromous salmonid females exhibit indicators of mate choice based on male size. Direct benefits to females of mating with larger males have not been identified for semelparous Pacific salmon, Oncorhynchus spp. We tested the null hypothesis that females forced to spawn naturally in a stream channel and artificially (gametes removed manually) with males about half their body mass would experience egg fertilization rates similar to that of females forced to spawn with males of about equal mass. Fertilization rates did not differ significantly between large- and small-male pairs. The fertilization rates were also very similar for eggs deposited naturally and those that we fertilized artificially. Therefore, fertilization success does not appear to be the mechanism responsible for female mate choice based on male size. Benefits of females mating with larger males probably have only indirect (i.e., genetic) benefits to a females offspring, as suggested by previous authors.     

Spawning migrations in landlocked Atlantic salmon: time series modelling of river discharge and water temperature effects

River discharge and water temperature are frequently cited as controlling the upstream migration of adult salmonids to their spawning areas. The results of earlier studies on the effect of these environmental factors were examined. The statistical methods employed in some of these studies failed to consider the serial correlation often found in migration time series. To assess the effects of discharge and temperature on the migratory activity of the landlocked Atlantic salmon (ouananiche, Salmo salar ), 12 years of data on spawning migrations in the Mistassini R., Quebec, Canada, were analysed and the results obtained by ordinary least squares regression and time series regression were compared. In six of the 12 years, upstream migratory movement was related negatively to changes in river flow, suggesting that fish favour falling water phases for ascent. Water temperature appeared to have little effect on migratory movement. The mean body size of migrating fish decreased significantly throughout the summer; early migrants were on average 11.4% larger (mean fork length 522mm) than late migrants (469 mm). Larger, 3-lake-year salmon migrated 7.2 days earlier than 2-lake-year salmon. Because the residuals from ordinary regression exhibited strong autocorrelation, time series regression was more appropriate than ordinary regression for the analysis of migration time Series.     

Effects of spawning Pacific salmon on the isotopic composition of biota differ among southeast Alaska streams

1. Adult Pacific salmon (Oncorhynchus spp.) transport marine nutrients to fresh waters and disturb sediments during spawning. The relative importance of nutrient fertilisation and benthic disturbance by salmon spawners can be modulated by environmental conditions (e.g. biological, chemical and physical conditions in the catchment, including human land use). 2. To determine the importance of the environmental context in modifying the uptake and incorporation of salmon‐derived material into stream biota, we measured the nitrogen (δ¹⁵N) and carbon (δ¹³C) isotopic composition of benthic algae (i.e. epilithon) and juvenile coho salmon (Oncorhynchus kisutch) in seven streams across a timber‐harvest gradient (8–69% catchment area harvested), both before and during the salmon run. Conditional bootstrap modelling simulations were used to assess variability in the response of epilithon and juvenile coho salmon to spawning salmon. 3. In response to spawning salmon, epilithon exhibited enrichment in both δ¹⁵N (mean: 1.5‰) and δ¹³C (2.3‰). Juvenile coho were also enriched in both δ¹⁵N (0.7‰) and δ¹³C (1.4‰). Conditional bootstrap models indicate decreased variation in data as spatial replication increases, suggesting that the number of study sites can influence the results of Pacific salmon isotope studies. 4. Epilithon isotopic enrichment was predicted by environmental conditions, with δ¹⁵N enrichment predicted by stream temperature and timber harvest (R² = 0.87) and δ¹³C enrichment by discharge, sediment size, timber harvest and spawner density (R² = 0.96). Furthermore, we found evidence for a legacy effect of salmon spawners, with pre‐spawner δ¹⁵N and δ¹³C of both epilithon and juvenile coho predicted by salmon run size in the previous year. 5. Our results show that the degree of incorporation of salmon‐derived nitrogen and carbon differs among streams. Furthermore, the environmental context, including putative legacy effects of spawning salmon, can influence background isotopic concentrations and utilisation of salmon‐derived materials in southeast Alaska salmon streams. Future studies should consider the variation in isotopic composition of stream biota when deciding on the number of study sites and samples needed to generate meaningful results.     

Evaluating the use of spawning success to estimate reproductive success in a Caribbean reef fish

Observations on egg batch production by known female Stegastes partitus and the fates of those egg batches within the nests of known males revealed that spawning success was not a reliable predictor of hatching success and, hence, reproductive success because of high egg batch mortality. Moreover, while numbers of eggs per batch increased with increasing female length, both inter- and intra-individual variation in batch size was considerable, demonstrating that spawning events cannot be considered equivalent. These two findings indicate that spawning success cannot be assumed to provide a direct quantitative substitute for a measure of reproductive success in this benthic spawning reef fish.     

Coral spawning in the western Pacific Ocean is related to solar insolation: evidence of multiple spawning events in Palau

Coral reproductive schedules have long been related to concomitant increases in regional sea surface temperature (SST). Yet, corals also mass spawn in the tropics, where SSTs vary little throughout the year. Here we show that the rise toward and fall from solar insolation maxima, which is the electromagnetic energy incident on the surface of the earth, coincide with coral spawning events in tropical Palau. Two insolation maxima (a consequence of the vernal and autumnal equinoxes) in the tropics lead to multiple spawning events per year. SSTs are poor predictors of coral spawning in the tropics. Multiple spawning events increase the rate of genetic recombination, which in turn may facilitate the likelihood of speciation and explain, in part, the high coral diversity in the tropics. We also show that mass spawning coincides with near-maximum solar insolation (5.0–7.2 kWh/m²/day) events from 33°N to 30°S in the western Pacific Ocean, and should be considered as one of the primary variables driving coral reproductive cycles.     

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.     

Multiple paternity and variance in male fertilization success within Atlantic salmon Salmo salar redds in a naturally spawning population

The incidence and magnitude of multiple paternity were estimated for a natural, unmanipulated spawning population of Atlantic salmon Salmo salar. Egg nests were surveyed in the autumn and sub‐samples were excavated the following spring. Parentage data derived from microsatellite DNA revealed an unexpectedly high level of multiple paternity. Within a single redd, females may mate with as many as 16 different males, including small mature male parr and large anadromous males. Multiple paternity was most pronounced in areas of highest redd density, corresponding with increased abundances of mature male parr. In addition, there was considerable variation in success among males, although this variability did not depend upon the number of males participating in spawning. This work underscores the value of undertaking genetic studies on the mating systems of fishes in unmanipulated, natural environments.     

Low cardiac and aerobic scope in a coastal population of sockeye salmon Oncorhynchus nerka with a short upriver migration

This study showed that a coastal population (Harrison) of Fraser River sockeye salmon Oncorhynchus nerka had a lower aerobic and cardiac scope compared with interior populations with more challenging upriver spawning migrations, providing additional support to the idea that Fraser River O. nerka populations have adapted physiologically to their local migratory environment.