Relationship between metabolism, sex and reproductive tactics in young Atlantic salmon (Salmo salar L.).

Atlantic salmon can differ markedly in their growth and in the timing of reproductive maturation, leading to the dramatic contrast between the large anadromous adults and the diminutive mature male parr. This study examined the growth rates, anatomical and physiological characteristics of parr during the adoption of their discrete life histories to ascertain whether these properties can explain tactic choice. To minimise the impact of habitat differences upon these attributes, salmon were reared in the laboratory until 1.5years of age, when the "decisions" to undergo smoltification or to mature as parr had been taken. At 1.5years, both males and females showed bimodal size-frequency distributions. Neither the population of origin nor the paternal reproductive tactic influenced the "decision" to mature or the growth trajectories. Growth rate (% massday(-1) during their final 10months) and the % male and female offspring in the upper modal group were strongly correlated and varied markedly among families. Mean growth rate per family was negatively correlated with mean metabolic rate per family at emergence. Growth rate decreased as a function of parr size in January and the growth rates of upper modal fish were displaced upwards relative to those of lower modal fish. Most males in the smaller size mode matured, whereas all other fish began smoltification. Mature male parr did not differ from similarly sized female pre-smolt in routine metabolic rate, but these smaller fish had higher metabolic rates than larger male and female pre-smolts. However, mature parr differed markedly from similarly sized females and from larger male and female pre-smolts in possessing higher oxidative and lower glycolytic capacities in muscle. Overall, these data are consistent with the interpretation that growth rates dictate the distribution of parr between upper and lower modal groups. Individuals from faster growing families would be more likely to pass the threshold for smoltification and to accelerate growth, whereas those from slower growing families would remain in the lower mode. The use of metabolic capacities, e.g. metabolic rate, was linked with modal group, whereas muscle oxidative capacity was linked with male maturity. Mean family metabolic rate at emergence was negatively linked with mean growth during the subsequent year, suggesting that metabolic efficiency facilitates growth and eventually smoltification.

Alternative developmental pathways and the propensity to migrate: a case study in the Atlantic salmon.

Migratory behaviour with its associated phenotypic changes is generally viewed as an adaptive strategy because it incurs survival or reproductive advantages to migrants. The development of a migrant phenotype is believed to be controlled by threshold mechanisms, where individuals emigrate only after surpassing a particular body size but delay migration if below. For such a strategy to respond to natural selection, part of the phenotypic variance in the propensity to migrate must be explained by variation in additive genetic effects. Here, we use data gathered in the field and from a common rearing experiment to test for a genetic basis associated with seaward migration in Atlantic salmon (Salmo salar L.). We document a high heritability of the liability trait underlying the propensity to emigrate in juvenile salmon, and significant differences between offspring grouped according to their sires in body-size threshold values above which emigration takes place. The presence of additive genetic variance in both the liability and thresholds makes the onset of migration a process sensitive to selection and may therefore constitute an important explanatory mechanism for the interpopulation differences in the size at seaward migration observed in this species.

River and estuary movements of yellow-stage American eels Anguilla rostrata, using a hydrophone array.

Patterns of summertime movement and habitat use of yellow-stage American eels Anguilla rostrata within York River and estuary and Gaspé Bay (Gaspesia, Québec, Canada) were examined using acoustic telemetry. Fifty fish were tagged with acoustic transmitters and released, either in the river or in the upper estuary, and their patterns of movement and habitat use were monitored at short spatial and temporal scales during the summer months using a dense hydrophone array. Approximately half of the fish released in the river swam to the estuary; two-thirds of the fish released within the estuary did not move out of the estuary. Anguilla rostrata were detected more frequently and had a greater areal range of detections during night, suggesting greater nocturnal activity. Longitudinal movements within the estuary tended to occur nocturnally, with upstream movements from early to late evening, and downstream movements from late evening to early morning. Approximately one-third of fish showed a regular pattern of movement, tending to reside in the deeper, downstream part of the estuary during day and in the shallower, more upstream part of the estuary during night. Approximately a quarter of fish, located in the upper estuary, remained upstream during both night and day. The remaining fish showed patterns intermediate between these two.

Do local adaptation and the reproductive tactic of Atlantic salmon (Salmo salar L.) affect offspring metabolic capacities?

Atlantic salmon (Salmo salar L.) is an iteroparous, anadromous species that exhibits some of the greatest within-population variability in size and age at maturity of all vertebrates. In the conditional reproductive strategy of salmonids, the male reproductive tactic expressed is believed to depend on an individual male's status relative to others in the population and therefore depends on his capacity to attain a physiological threshold, the exact nature of which is unknown. Although the threshold is influenced by local biotic and abiotic conditions, it is likely to be under genetic control. Our study examined whether the early growth, muscle metabolic capacities, routine metabolic rate, and spontaneous swimming of salmon alevins reared in laboratory conditions varied with the population of origin, maternal investment, and the paternal reproductive tactic. Our experimental design allowed us to establish that neither the population of origin nor the paternal reproductive tactic influenced the physiological capacities of alevins. The strong influence of the mother on alevin metabolic capacities suggests that the bioenergetic differences in metabolic capacities, realized metabolic rates, and activity levels that could eventually dictate the reproductive tactic of male offspring may originate in maternal effects.

The genetic basis of early-life morphological traits and their relation to alternative male reproductive tactics in Atlantic salmon.

Although heritability estimates for traits potentially under natural selection are increasingly being reported, their estimation remains a challenge if we are to understand the patterns of adaptive phenotypic change in nature. Given the potentially important role of selection on the early life phenotype, and thereby on future life history events in many fish species, we conducted a common garden experiment, using the Atlantic salmon (Salmo salar L.), with two major aims. The first objective is to determine how the site of origin, the paternal sexual tactic and additive genetic effects influence phenotypic variation of several morphological traits at hatching and emergence. The second aim is to test whether a link exists between phenotypic characteristics early in life and the incidence of male alternative tactics later in life. We found no evidence of a site or paternal effect on any morphological trait at hatching or emergence, suggesting that the spatial phenotypic differences observed in the natural river system from which these fish originated are mainly environmentally driven. However, we do find significant heritabilities and maternal effects for several traits, including body size. No direct evidence was found correlating the incidence of precocious maturation with early life characteristics. We suggest that under good growing conditions, body size and other traits at early developmental stages are not reliable cues for the surpassing of the threshold values associated with male sexual development.

Competition, predation and flow rate as mediators of direct and indirect effects in a stream food chain.

Using semi-natural stream channels, we estimated the effects of competition and predation exerted by juvenile and adult exotic rainbow trout (Oncorhynchus mykiss) on the diel activity pattern of juvenile native Atlantic salmon (Salmo salar), a secondary consumer. We also evaluated the direct and indirect effects of competition, predation and abiotic factors (water depth and velocity) on the growth rate of salmon, the biomass of invertebrate grazers (primary consumers) and the biomass of periphytic algae (primary producers; chlorophyll a). The presence of chemical cues emanating from adult predatory trout reduced the daily activity of juvenile Atlantic salmon. In contrast, competition imposed by juvenile rainbow trout forced Atlantic salmon to be more active during the day, even if adult rainbow trout were also present. We found no effect of either competition or of predatory cues on the growth rate of Atlantic salmon, and no evidence of indirect effects on either the biomass of invertebrates or the biomass of chlorophyll a. In contrast, we demonstrated that this food chain (fish--invertebrate grazers--periphytic algae) was under the control of a critical abiotic factor, the water velocity, and of bottom-up processes. We concluded that the exotic species directly increases the risk of predation of the native Atlantic salmon, but behavioral compensation probably limits the effects on growth rate. The competition and predation imposed by the invaders had no indirect effects on lower trophic levels. Top-down effects may have been mitigated by the dominant influence of water velocity controlling all components of the food chain and by elevated levels of primary production.

Heritability of life-history tactics and genetic correlation with body size in a natural population of brook charr (Salvelinus fontinalis).

A common dimorphism in life-history tactic in salmonids is the presence of an anadromous pathway involving a migration to sea followed by a freshwater reproduction, along with an entirely freshwater resident tactic. Although common, the genetic and environmental influence on the adoption of a particular life-history tactic has rarely been studied under natural conditions. Here, we used sibship-reconstruction based on microsatellite data and an 'animal model' approach to estimate the additive genetic basis of the life-history tactic adopted (anadromy vs. residency) in a natural population of brook charr, Salvelinus fontinalis. We also assess its genetic correlation with phenotypic correlated traits, body size and body shape. Significant heritability was observed for life-history tactic (varying from 0.52 to 0.56 depending on the pedigree scenario adopted) as well as for body size (from 0.44 to 0.50). There was also a significant genetic correlation between these two traits, whereby anadromous fish were genetically associated with bigger size at age 1 (r(G) = -0.52 and -0.61). Our findings thus indicate that life-history tactics in this population have the potential to evolve in response to selection acting on the tactic itself or indirectly via selection on body size. This study is one of the very few to have successfully used sibship-reconstruction to estimate quantitative genetic parameters under wild conditions.

The disruption of dominance hierarchies by a non-native species: an individual-based analysis.

We studied the effects of the exotic rainbow trout (Oncorhynchus mykiss) on the performance and the dominance hierarchy of native Atlantic salmon (Salmo salar) at the group and individual level using laboratory and semi-natural experiments. At the group level, we compared the effects of interspecific and intraspecific competition (substitutive and additive design) on behavioural responses and growth of young-of-the-year Atlantic salmon. At the individual level, the same design was used to evaluate: (1) the temporal consistency of behavioural responses, dominance hierarchy and growth rate of Atlantic salmon; (2) the pattern of correlations between behaviours; and (3) the relationship between individual growth rate and behaviour. In the laboratory, group-level analyses revealed a weak but similar effect of rainbow trout and intraspecific competition on the behaviour and growth of Atlantic salmon. In contrast, individual-based analyses demonstrated that rainbow trout (but not intraspecific competition) strongly affected behavioural strategy, dominance hierarchy and growth trajectory of individual Atlantic salmon. Specifically, behaviours, dominance status and growth rate of salmon were temporally consistent in the intraspecific environment, while these patterns were disrupted when rainbow trout were present. Similarly, we found that rainbow trout strongly affected behavioural correlations and the relationships between individual growth rate and behaviour. The semi-natural experiments confirmed these results as interspecific competition affected relationships between individual growth rate of salmon, initial weight and activity index. Overall, individual-based analyses highlighted important mechanisms that were concealed at the group level, and that may be crucial to understand ecological and evolutionary consequences of exotic species. Moreover, these results demonstrated that competition with an exotic species disrupts the hierarchical relationship among native individuals and may therefore represent a potential for a shift in selective pressure.

Living with uncertainty: genetic imprints of climate shifts in East Pacific anchovy (Engraulis mordax) and sardine (Sardinops sagax).

In the upwelling zone of the northeastern Pacific, cold nutrient-rich conditions alternate with warm nutrient-poor intervals on timescales ranging from months to millennia. In this setting, the abundances of Pacific sardine (Sardinops sagax) and northern anchovy (Engraulis mordax) fluctuate by several orders of magnitude, with sardine dominating during warm conditions and anchovy dominating during cool conditions. Two population models can explain the response of these fishes to adverse conditions. Under the basin model, species distributions contract to a central (optimal) range during population crashes. Expectations of this model may include a single range-wide population with a decline in genetic diversity on both sides of a central refuge. In contrast, the self-recruitment model invokes a series of local oceanographic domains that maintain semi-isolated subpopulations. During adverse conditions, some subpopulations cannot complete the life cycle within the local environment and are extirpated. Expectations of this model include some degree of population genetic structure and no clear gradient in genetic diversity. We examined mitochondrial DNA cytochrome b sequences to assess these competing models for anchovy (N = 196; 539 bp) and sardine (N = 107; 425 bp). The mitochondrial DNA gene genealogies are shallow but diverse for both species. Haplotype frequencies are homogeneous among subpopulations, but genetic diversities peak for both species along Baja California and adjacent southern California. Mismatch distributions and Tajima's D-values reveal distinctive signatures of population bottlenecks and expansions. Sardine haplotypes coalesce at approximately 241,000 years bp, with an initial female effective population size Nf0 = 0 followed by exponential growth to Nf1 = 115 million. Anchovy haplotypes coalesce at approximately 282,000 years bp, with an initial population size of Nf0 = 14,000, followed by exponential growth to Nf1 = 2.3 million. These results indicate a founder event for sardine and a severe population decline for anchovy in the California Current during the late Pleistocene. Overall, these data support the basin model on decadal timescales, although local recruitment may dominate on shorter timescales.

Occurrence of Proteocephalus tetrastomus (Rudolphi, 1810) (Cestoda: Proteocephalidea) in larval rainbow smelt (Osmerus mordax) in North America: identification of a potential pathogen confirmed.

A morphological evaluation and genetic analysis (sequencing of ITS2 region of rDNA) of proteocephalidean cestodes from rainbow smelt (Osmerus mordax) in the Saint Lawrence Estuary, Canada, has shown their conspecificity with Proteocephalus tetrastomus, a specific parasite of smelt (Osmeridae), previously known only from northern Europe, Russia, and Japan. The parasite occurs only in larval, but not adult, smelt in the Saint Lawrence Estuary. Prevalence of larval smelt infection was 42% (n = 50), mean intensity 2.1 +/- 2.4 and mean abundance 1.1 +/- 1.0.

A genetic evaluation of mating system and determinants of individual reproductive success in Atlantic salmon (Salmo salar L.).

The primary objective of this study was to use highly polymorphic microsatellite loci to estimate individual reproductive success in Atlantic salmon based on the number of surviving juveniles (young of the year) at the population level under natural conditions. We inferred reproductive strategies adopted by both sexes by applying a maximum likelihood method to determine parent-offspring genotype relationships. A high degree of variance in individual reproductive success for both males and females was revealed. The high number of mates used by both sexes is not concordant with previous behavioral studies proposing that females are mainly monogamous in this species. We found little evidence supporting the prediction from previous reports of a positive relationship between individual size and realized reproductive success for either males or females. For both sexes, however, there was a significant correlation between the number of mates and the number of offspring. These results indicate that this species' mating system is more flexible than previously thought and suggest that factors such as potential genetic benefits or environmental uncertainty may also be driving the evolution and the plasticity of mating systems in Atlantic salmon.

Ecological determinants and temporal stability of the within-river population structure in Atlantic salmon (Salmo salar L.).

A gene diversity analysis was performed using microsatellite loci in order to (i) describe the extent and pattern of population structure in Atlantic salmon (Salmo salar L.) within a river system; (ii) establish the importance of quantifying the signal:noise ratio in accurately estimating population structure; and (iii) assess the potential usefulness of two evolutionary models in explaining within-river population structure from the ecological and habitat characteristics of Atlantic salmon. We found weak, yet highly significant microscale spatial patterning after accounting for variance among temporal replicates within sites. Lower genetic distances were observed among temporal samples at four sampling sites whereas no evidence for temporal stability was observed at the other three locations. The component of genetic variance attributable to either temporal instability and/or random sampling errors was almost three times more important than the pure spatial component. This indicates that not considering signal:noise ratio may lead to an important overestimation of genetic substructuring in situations of weak genetic differentiation. This study also illustrates the usefulness of the member-vagrant hypothesis to generate a priori predictions regarding the number of subpopulations that should compose a species, given its life-history characteristics and habitat structure. On the other hand, a metapopulation model appears better suited to explain the extent of genetic divergence among subpopulations, as well as its temporal persistence, given the reality of habitat patchiness and environment instability. We thus conclude that the combined use of both models may offer a promising avenue for studies aiming to understand the dynamics of genetic structure of species found in unstable environments.

Age, growth and fecundity of the silver mullet, Mugil curema (Pisces: Mugilidae), in coastal areas of northeastern Venezuela.

We studied fecundity and growth in populations of the silver mullet, Mugilcurema, in coastal areas of northeastern Venezuela between March 1992 and July 1993. The average number of oocytes in gonads of 23-42 cm adults was 54 x 10(4), and the relative fecundity was 1,311 oocytes g-1 of fish. The size of mature oocytes did not vary in different portions of the same gonad (p > 0.05) or among the adults in three populations studied. The average egg diameter for adults was 426 microns (CI = 4.34). Age of juveniles, collected from the La Restinga Lagoon at about monthly intervals, from counts of growth lines on the otoliths ranged from 50 to 240 days. The relation of age (number of growth lines) to standard length follows an exponential growth curve. The growth of juveniles varied seasonally and was greatest during the rainy season (April to August), when temperatures were highest. The time of spawning has probably been adapted so that peak recruitment into the lagoons occurs just prior to the rainy season when conditions for growth are most favorable.

A molecular analysis of relationships and biogeography within a species complex of Holarctic fish (genus Osmerus).

Episodes of trans-Arctic faunal exchange and isolation between the north Pacific and Atlantic ocean basins have been implicated as important historic geological events contributing to extant patterns of genetic diversity and structure in Holarctic faunas. We made a further test of the significance of such biogeographic events by examining mitochondrial DNA (mtDNA) restriction fragment length and cytochrome b sequence polymorphism among north Pacific and Arctic, north-western Atlantic (north-eastern North American), and north-eastern Atlantic (European) regional forms of the boreal smelt, genus Osmerus. Our analyses also assessed whether the regional forms within this 'species complex': (i) represent a single widely distributed and polytypic species, or is composed of three geographically distinct species, and (ii) resulted from a single split from north Pacific ancestral Osmerus or two independent Pacific-Atlantic divergences. MtDNA sequence divergence estimates among forms ranged from 5.6-8.9% and from 6.1-8.5% based on restriction fragment and 300 base pairs of cytochrome b sequencing, respectively. Divergence within forms averaged less than 0.5% for fragment analysis and no differences were detected from sequence analysis. Provisional dating of lineage separations in Osmerus based on our sequence divergence estimates suggested a mid-Pliocene to early Pleistocene time frame for diversification among the forms. These estimated lineage separation dates support the idea that geological events in 'Beringia' and the surrounding trans-Arctic area (e.g. opening of the Bering Seaway, Pleistocene glacial advances), occurring over a similar time frame, have influenced radiation in Osmerus. Phenetic and parsimony analyses of the sequence divergence estimates and of sequence polymorphisms suggested that the north Pacific/Arctic form and the north-western Atlantic form shared a common ancestor more recently than either has with the north-eastern Atlantic form, thus supporting the hypothesis that the species complex has arisen from two independent Pacific-Atlantic divergences probably beginning during the mid-Pliocene.

Congener-specific analysis of the accumulation of polychlorinated biphenyls (PCBs) by aquatic organisms in the maximum turbidity zone of the St. Lawrence estuary, Québec, Canada.

The polychlorinated biphenyl (PCB) contamination of the biota of the St. Lawrence estuary maximum turbidity zone (MTZ) was investigated. The species analyzed consist of zooplankton (mostly Neomysis americana), larval smelt (Osmerus mordax), juvenile smelt, juvenile tomcod (Microgadus tomcod) and adult smelt, tomcod and capelin (Mallotus villosus). A significant increase in total PCB contamination from zooplankton to all fish developmental stages indicates that the St. Lawrence MTZ is a site of significant PCB contamination. The total PCB contamination of adult smelt and tomcod sampled in the St. Lawrence MTZ was greater than the limit of 0.1 ppm set by the International Joint Commission for the protection of predators. For zooplankton, tomcod and capelin, significant correlations were found between lipid content and PCB contamination. The congener-specific analyses showed that the bioconcentration factor of the individual congeners varied with the species involved and with the molecular structure of the congener. It was found that the chlorine atoms in positions 2, 4 and 5 on at least one phenyl ring of the PCB molecule was a dominant factor causing accumulation of PCBs in aquatic organisms. The pattern of PCB congeners found in beluga (Delphinapterus leucas) whale tissues is similar to the PCB pattern found in the St. Lawrence estuary MTZ biota.

Computer-automated method to study cardiac conditioning to a chemical cue in young salmon.

An apparatus was designed in which young Atlantic salmon (Salmo salar) are rapidly conditioned to reduce heart rate using a chemical-electric shock conditioning procedure. A chemical calibration system permitting efficient stimulus control is described as well as the electronic systems and computer software used to control all events of an experimental session and to quantify cardiac and chemical data. Efficient stimulus control and computer-automated recording techniques minimize inter-trial intervals and the time required for the measurement and analysis of cardiac responses. Data are presented showing that 15-month-old Atlantic salmon can be trained to reduce by 20% their heart rate to the synthetic chemical morpholine within 5 training trials whereas 10-month-old fish did not do so until 15 training trials.