Choice of feeding station in Atlantic salmon, Salmo salar, parr: effects of predation risk, season and life history strategy

The current speed at which underyearling salmon parr held feeding stations was examined from late summer to early winter in laboratory flume tanks that offered a choice between (a) areas with high water flow, high food availability but high predation risk and (b) areas with low flow, little food but shelter from predators. In August, those fish that would become smolts aged 1 + (and which by late winter formed the upper modal group, UMG, of the bimodal size distribution) adopted positions in faster currents than did the fish which would take a further year to reach the smolt stage (the lower modal group, LMG). However, the chosen current speed of UMG fish decreased through the period of study, so that by December all fish were found in areas of low flow, and hence little food. Both date and water temperature had independent effects on the chosen current speed of UMG fish.
The effect of predation risk was investigated using a model trout. A brief sight of this predator caused 47% of fish that had been in the main, exposed currents to move to slacker, sheltered areas; they took 1 h, on average, to return to their previous position. The fish that remained in position upon seeing the predator reduced their rate of tail beating, presumably increasing crypticity. Eventual UMG parr were less likely than were LMG fish to move away upon seeing a predator. The fish moved to faster currents than normal 2–3 h after seeing the predator, possibly compensating for the earlier reduction in feeding rate.     

Otolith and somatic growth rates in Atlantic salmon parr, Salmo salar L: evidence against coupling

It is often assumed that otolith growth is in some way dependent on somatic growth (i.e. that the two processes are coupled). We examined the relationships between sagitta radius and fork length in 0+ Atlantic salmon parr that would subsequently smolt aged 1 + (UMG fish) or 2+ (LMG fish). Repeated measurements of fork lengths of individually marked parr, taken over a 211-day period from first feeding, were compared to sagitta radii on the same measuring dates (obtained by analysis of daily increments). The results showed that there was a linear relationship between fork length and otolith radius in UMG parr. However, this was not true for LMG parr. These fish enter a state of natural anorexia in their first autumn (despite excess food), but their otoliths continued to grow at the same rate despite the virtual cessation of somatic growth; they had therefore developed disproportionately large otoliths by the end of the study period. The relative growth rates of soma and otoliths first changed in LMG fish in late July/early August; this is the most precise estimate yet obtained of the timing of divergence in the developmental pathways of UMG and LMG parr. The rate of sagitta accretion was consistently lower in LMG parr, possibly indicating a lower metabolic rate in these fish. The results are discussed in relation to previous theories of the relationship between otolith and somatic growth.     

Life-history patterns in a southern population of Atlantic salmon

Juvenile Atlantic salmon Salmo salar in the river Esva, Asturias, north-west Spain, developed a bimodal growth pattern during their first growing season. Segregation between the two modes was apparent by late autumn. All fish in the upper modal group (UMG) grew throughout the year and migrated downstream in the following spring (by April) at the age of 14 months. Some lower modal group (LMG) fish (56% of the main stem, 31% and 50% of the two tributaries) silvered like smolts and apparently migrated downstream the same spring, although c. 1·5 months after UMG fish. Larger LMG fish appeared more likely than smaller ones to migrate. LMG fish did not grow in winter, but they grew fast between March and May. Maturing male parr were detected first at 5 months old in July, and they occurred initially among the faster growers, >6·8 cm long. In spite of this, length of maturing males did not change from late summer and throughout the winter, whereas that of non-maturing UMG and LMG fishes continued to diverge from September onwards. These findings suggest that favourable conditions for growth (very early start of a long growing season) at the southern limit of the species' range may influence the life-history pattern of this population.     

Effects of light level and growth history on attack distances of visually foraging juvenile salmon in experimental tanks

The effects of light level, developmental pathway, and previous growth history on the foraging attack distances of juvenile Atlantic salmon Salmo salar were examined in circular rearing tanks. Former manipulation of growth rates had no significant influence on distances moved to intercept food items despite the fact that it caused substantial differences in post-treatment growth. Attack distances of fish that were entering a state of overwinter dormancy (lower modal group; LMG) were shorter than those of actively feeding (and growing) fish (upper modal group; UMG). These differences were explained generally by differences in body size between the two groups, suggesting that actual effort per attack was unassociated with growth requirements. Significant differences between growing and non-growing fish in attack distances could contribute to the variation in growth rates through their effect on feeding rates, but were unlikely to have affected energetic costs. This may be due to the fact that attack distances were consistently short throughout the study period as is also evident from the pattern of change between night and daytime. Whereas in the first experiment (daylight v . twilight) fish moved further to reach food during the day, in the second (daylight v . overcast night) nocturnal attack distances matched (LMG fish) or exceeded (UMG fish) diurnal attack distances. Thus diurnal attack distances were probably minimized in the second experiment. These results are interpreted within a framework of overwintering strategies.     

Seasonal variation in trypsin activity in juvenile Atlantic salmon upper and lower modal groups

Juvenile salmon in their first year of growth showed a bimodal distribution of body lengths by December. For experimental purposes samples of fish from the upper 2% of body lengths were taken as representing the upper modal group (UMG), whilst fish from the bottom 5% of body lengths were taken to represent the lower modal group (LMG). The population of fish from which the samples were taken were fed ad libitum from December to July. During the winter months to March, neither group increased in weight. Growth resumed between March and July. The LMG fish had a very low food intake, as indicated by the relative weight of digesta in the stomach, in the winter months. However, following resumption of feeding, the relative weight of stomach digesta of the LMG fish exceeded that of the UMG fish between May and July. The activity of trypsin in the intestinal digesta followed a similar pattern, the LMG fish showing a higher trypsin activity in the spring months. Starvation of UMG fish for 5 days in winter resulted in accumulation of trypsin in the pancreatic tissues, whilst injection of the trypsin releasing hormone cholecystokinin (CCK) into starving UMG fish resulted in reduction of trypsin in the secretory tissues. CCK also caused reduction of trypsin in the pancreatic tissues of LMG fish, suggesting that the pancreas of this group is potentially fully functional during the winter period. Ultrastructure studies of the pancreatic acinar cells showed evidence for lower secretory activity in the LMG fish, as indicated by smaller numbers of zymogen granules, less well developed Golgi systems and a smaller number of active secreting cells. It appears that trypsin secretion by the pancreas in LMG fish is at a low level during the winter, in response to the reduced amounts of food passing through the gut, which is ultimately controlled by changes in food intake, lowered metabolic level and lowered appetite levels.     

Life histories of Atlantic salmon altered by winter temperature and summer rearing in fresh- or sea-water

Increased growth during winter increased the incidence of age 1+ Salmo salar smolts in spring. High condition factor in spring and good growth in summer was associated with a high incidence of sexually mature males in autumn. In two experiments, groups (n=160–237 per group) of individually identified parr, either ungraded (lower and upper modal groups: LMG, UMG) or size-graded (LMG only), were reared at either 10, 6 or 3 °C overwinter (Nov to May). At 10 °C, up to 51% of parr originally in the LMG became smolts in spring at age 1+. In contrast, at either 6 or 3 °C (control), < 6% of LMG parr became smolts. The probability of being recruited into the UMG overwinter was positively related to initial body size, and was increased by size-grading. Smolt recruitment was two-fold higher among females compared to males; a proportion of males by age 0+ had already opted to mature at age 1+ rather than smolt at age 1+. In contrast, smolting at age 1+ was not inhibited in males previously mature at age 0+. During summer (May to Nov), all experimental groups were reared at ambient temperature, each subdivided between fresh water (max 21 °C) or seawater (max 15 °C). Good growth in seawater of winter recruits into the UMG confirmed they had completed smolting. Mortality in seawater among parr was 41–83%, and among smolts was 10–22%. Specific growth rate during summer was inversely related to winter rearing temperature. The incidence of sexual maturity in autumn at age 1+ among male parr was positively related to winter rearing temperature, fork length and condition factor in May, but there was large variation among individuals with respect to body size and maturity. Summer rearing in seawater reduced growth and the incidence of maturation. Parr and post-smolt maturity was 84–99% and 100% in fresh water respectively, 21–58% and 0% in seawater.     

Social Status and Feeding in Atlantic Salmon Salmo salar Parr: The Effect of Visual Exposure to a Dominant

Groups of four Atlantic salmon parr were established and the dominant individual identified. Feeding responses were then observed in the remaining (subordinate) fish housed in one of three conditions: in the same compartment as the dominant fish (full exposure), separated from it by a transparent partition (visual exposure) or behind an opaque partition (isolated). Subordinate parr in the full exposure condition responded to and ate fewer food pellets than did the dominant fish. However, subordinate parr in the visual exposure condition and in the isolation condition fed actively, indicating that neither visual intimidation nor long-term stress-induced reduction of appetite were responsible for the reduced food intake of subordinate parr in direct contact with dominants. Dominant parr and subordinates in the visual exposure condition, but not subordinates in the exposed condition, moved further from their feeding station when attacking food items that were contested by a competitor compared with the distance moved for uncontested items. The presence of a competitor therefore forced both dominant and visually exposed subordinates to pay higher costs while foraging.     

Allozyme heterozygosity, date of first feeding and life history strategy in Atlantic salmon

The relations between allozyme heterozygosity, relative date of first feeding and life history strategy in juvenile Atlantic salmon Salmo salar were examined using eggs obtained from a 400 family cross (20 male × 20 female adult Atlantic salmon). Multilocus heterozygosity, through its positive associations with the timing of first feeding and growth rate, was correlated with life history strategy in juvenile Atlantic salmon, albeit under genotype × environmental (temperature, food availability) regulation. Under hatchery conditions, a 10 day difference was observed in the relative date of first feeding between early and late first feeding Atlantic salmon. Early first feeding Atlantic salmon exhibited a significantly higher mean heterozygosity, grew faster at ambient water temperature (April to November) and a significantly higher proportion adopted the early freshwater maturation (age 0+ years, male fish) or early migrant (age 1+ years, mainly female fish) strategies compared to late first feeding Atlantic salmon. Elevated water temperatures over the winter (December to April, >10·5° C) provided additional growth opportunity allowing previously mature male parr (mainly early first feeders) and lower modal group parr (mainly late first feeders) to adopt the early migrant strategy by the following spring.     

Growth history and intrinsic factors influence risk assessment at a critical life transition for a fish

Making the appropriate decision in the face of predation risk dictates the fate of prey, and predation risk is highest at life history boundaries such as settlement. At the end of the larval phase, most coral reef fishes enter patches of reef containing novel predators. Since vision is often obscured in the complex surroundings, chemical information released from damaged conspecific is used to forewarn prey of an active predator. However, larvae enter the reef environment with their own feeding and growth histories, which will influence their motivation to feed and take risks. The present study explored the link between recent growth, feeding history, current performance and behavioural risk taking in newly settling stages of a coral reef damselfish (Pomacentrus amboinensis). Older and larger juveniles in good body condition had a stronger response to chemical alarm cues of injured conspecifics; these fish spent a longer time in shelter and displayed a more dramatic decrease in foraging behaviour than fish in lower body condition. Feeding experiments supported these findings and emphasized the importance of body condition in affecting risk assessment. Evidently, larval growth history and body condition influences the likelihood of taking risks under the threat of predation immediately after settlement, thereby affecting the probability of survival in P. amboinensis.     

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.     

The response of bleak to predator odour of unfed and recently fed pike

Feeding and growth responses of bleak Alburnus alburnus to the odour of unfed and recently fed pike Esox lucius were quantified in laboratory experiments. Bleak reacted more strongly to the latter than to the former and feeding rates were lowered by 35 and 20%, respectively. The decreases in feeding rates were not an effect of the absence of fish from the feeding place, but of a lowered feeding efficiency due mainly to diminished time spent foraging. The lowered consumption rate of bleak exposed to the odour of recently fed pike caused a decrease in their individual growth rate. The stronger reaction to the recently fed pike stimulus supports the view that alarm substance is a marker for predator odour. In the absence of any further signal from the predator, the bleak became habituated to the predator odour and showed the reaction for only 5 days.     

Daily feeding rhythms in Atlantic salmon I: feeding and aggression in parr under ambient environmental conditions

Daily feeding patterns of tank-reared Atlantic salmon Salmo salar parr under ambient conditions and their relationship with patterns of aggression were investigated during spring and autumn. A single, early afternoon feeding peak was observed during spring but no consistent pattern emerged from the autumn trial (fish did tend to feed in synchrony, even though the population's feeding pattern varied between days). Aggression was highest at first light during both spring and autumn, reducing thereafter throughout the day. Feeding and aggression were out of phase during spring, with the level of feeding increasing as aggression decreased. It is suggested that the high levels of early morning aggression are associated with re-establishment of the social order that breaks down after a period of darkness; in the spring this may have inhibited feeding.     

Social dominance and body size in Atlantic salmon parr, Salmo solar L.

Dominance relationships between pairs of Atlantic salmon parr of known size were assessed at various times during their first year of life. In tests conducted between first feeding and early July, the larger of two fish was dominant in only 54% of pairs, regardless of the magnitude of the size difference between the fish. In September, there was a stronger association between size and status, especially in pairs with a large size differential, where the dominant was larger in 72% of cases. In groups of parr tested in April of the following year, there was no relationship between size and status, the larger of two fish being dominant in 48% of cases, regardless of the magnitude of the size differential. This result suggests that status in early social interactions may depend on behavioural properties rather than size and that the larger size of dominant fish reported in a number of salmonids might be a consequence and not a cause of high status.     

The autecology of the chub, Squalius cephalus (L.), of the River Lugg and the Afon Llynfi

(1) Seasonal variation in the intensity of feeding activity was demonstrated in two chub populations. Feeding activity was higher in summer and more pronounced in the young age-classes. The intensity of feeding activity was significantly correlated with temperature. (2) The diet of the total chub populations embraced a wide range of food items but vegetable material predominated. Substrate material was frequently encountered which suggested considerable feeding on the river bed. Fish were the most important animal food, by volume, in the River Lugg but Trichoptera larvae were most important in the Afon Llynfi. No remains of salmon parr or trout were found in chub stomachs but grayling were eaten. The most important prey fish, by volume, was the eel but cyprinids, especially minnows, were most important by frequency of occurrence. (3) Seasonal variation in the composition of the diet could be related to availability of food organisms but some selection was shown. Vegetable foods were most important in summer; animal foods, Trichoptera larvae in particular, were important in winter. (4) Analysis of the variation in the composition of the diet with age revealed several trends, notably a decrease in the importance of plant material, aquatic and aerial insects with age and a corresponding increase in the importance of larger prey foods such as fish, frogs and crayfish. (5) The commonly held view that chub are deleterious to salmonid stocks was examined. The absence of direct predation and the small likelihood of direct competition suggests that this view is incorrect.     

Rapid habituation by mosquito larvae to predator kairomones

Larvae of some species of mosquitoes have been shown to respond to water‐borne kairomones from predators by reducing bottom‐feeding and replacing it with surface filter‐feeding, which uses less movement and is thus less likely to attract a predator. However, if no predator attack takes place, then it would be more efficient to use a risk allocation strategy of habituating their response depending on the predator and the overall risk. The larvae of Culiseta longiareolata Macquart live in temporary rain‐filled pools, where they are exposed to a high level of predation. Within one hour, they responded to kairomones from dragonfly or damselfly nymphs, or to the fish Aphanius, by significantly reducing bottom‐feeding activity. Continued exposure to the predator kairomones resulted in habituation of their response to damselflies, a slower habituation to fish, but no habituation to dragonflies even after 30 h. In contrast, the larvae of Culex quinquefasciatus Say normally live in highly polluted and thus anaerobic water, where the predation risk will be much lower. They also showed a significant reduction in bottom‐feeding after 1 h of exposure to predator kairomones but had completely habituated this response within 6 h of continuous exposure. Some species of mosquito larvae can thus show a very rapid habituation to predator kairomones, while others only habituate slowly depending on the predator and overall predation risk.     

Differences in growth between maturing and non-maturing male Atlantic salmon, Salmo salar L., parr

Sibling male Atlantic salmon parr that matured tended to be the larger fish in January, but their monthly specific growth rates between January and July did not differ from those of non-maturing fish. Maturing fish had lower condition factors in March, but greater increases in condition factor during April, exceeding those of non-maturing males by May. In maturing males, feeding rates between July and September, and specific growth rates in August and September, were lower than those of immature fish. Consequently, the mean size of immatures equalled or exceeded that of maturing males by October. Maturation rates were strongly correlated with increases in mean condition factor only during April.     

Alternative reproductive tactics in atlantic salmon: factors affecting mature parr success

In Atlantic salmon, as in most salmonids, males can mature early in the life cycle, as small freshwater fish, termed parr, and/or undergo a sea migration before maturing as full-size adults. The alternative life histories are contingent on environmental and social circumstances, such as growth rate, territory quality or any other factor that affects the individual''s state. In order to model the choice of life history in this group of commercially valuable species, it is necessary to understand not only the relative contribution of the different male types to subsequent generations, but also to know the factors that affect reproductive success in each type. In this paper we present the results of a study designed to investigate the factors that affect the reproductive success of mature parr. We used highly polymorphic minisatellite DNA markers to analyse paternity in a series of mating experiments where the number and body size of parr were manipulated. The fraction of eggs fertilized by mature parr ranged from 26 to 40 per cent, with individual parr fertilizing up to 26 per cent of the eggs. A strong positive correlation was found between parr size and reproductive success. The relative success of parr decreased with increasing parr number. Data from this and other studies on variation in the timing and degree of parr reproductive success are discussed in relation to the evolution of male mating strategies and life history in salmonids.     

Reciprocity in predator–prey interactions: exposure to defended prey and predation risk affects intermediate predator life history and morphology

A vast body of literature exists documenting the morphological, behavioural and life history changes that predators induce in prey. However, little attention has been paid to how these induced changes feed back and affect the predators’ life history and morphology. Larvae of the phantom midge Chaoborus flavicans are intermediate predators in a food web with Daphnia pulex as the basal resource and planktivorous fish as the top predator. C. flavicans prey on D. pulex and are themselves prey for fish; as D. pulex induce morphological defences in the presence of C. flavicans this is an ideal system in which to evaluate the effects of defended prey and top predators on an intermediate consumer. We assessed the impact on C. flavicans life history and morphology of foraging on defended prey while also being exposed to the non-lethal presence of a top fish predator. We tested the basic hypothesis that the effects of defended prey will depend on the presence or absence of top predator predation risk. Feeding rate was significantly reduced and time to pupation was significantly increased by defended morph prey. Gut size, development time, fecundity, egg size and reproductive effort respond to fish chemical cues directly or significantly alter the relationship between a trait and body size. We found no significant interactions between prey morph and the non-lethal presence of a top predator, suggesting that the effects of these two biological factors were additive or singularly independent. Overall it appears that C. flavicans is able to substantially modify several aspects of its biology, and while some changes appear mere consequences of resource limitation others appear facultative in nature.     

Learn and live: predator experience and feeding history determines prey behaviour and survival

Determining how prey learn the identity of predators and match their vigilance with current levels of threat is central to understanding the dynamics of predator–prey systems and the determinants of fitness. Our study explores how feeding history influences the relative importance of olfactory and visual sensory modes of learning, and how the experience gained through these sensory modes influences behaviour and survival in the field for a juvenile coral reef damselfish. We collected young fish immediately prior to their settlement to benthic habitats. In the laboratory, these predator-naïve fish were exposed to a high- or low-food ration and then conditioned to recognize the olfactory cues (odours) and/or visual cues from two common benthic predators. Fish were then allowed to settle on reefs in the field, and their behaviour and survival over 70 h were recorded. Feeding history strongly influenced their willingness to take risks in the natural environment. Conditioning in the laboratory with visual, olfactory or both cues from predators led fish in the field to display risk-averse behaviour compared with fish conditioned with sea water alone. Well-fed fish that were conditioned with visual, chemical or a combination of predator cues survived eight times better over the first 48 h on reefs than those with no experience of benthic predator cues. This experiment highlights the importance of a flexible and rapid mechanism of learning the identity of predators for survival of young fish during the critical life-history transition between pelagic and benthic habitats.     

Embryonic learning and developmental carry-over effects in an invasive anuran

Carry-over effects influence trait responses in later life stages as a result of early experience with environmental cues. Predation risk is an influential stressor and selection exists for early recognition of threats. In particular, invasive species may benefit from carry-over effects by preemptively recognizing and responding to novel predators via latent developmental changes and embryonic learning. In a factorial experiment, we conditioned invasive American bullfrog embryos (Lithobates catesbeianus) to the odor of a novel fish predator, largemouth bass (Micropterus salmoides) alone or in combination with injured conspecific cues. We quantified developmental carryover in the larval life stage and found that individuals conditioned to the highest risk (fish and injured conspecific cues) grew into longer bodied larvae relative to larvae from lower risk treatments. We also assessed embryonic learning, a behavioral carry-over effect, and found an interaction between embryonic conditioning and larval exposure. Behavioral responses were only found in scenarios when predation risk varied in intensity across life history stages, thus requiring a more flexible antipredator strategy. This indicates a potential trade-off between the two strategies in larval growth and development rates, and time until metamorphosis. Our results suggest that early predator exposure and carry-over effects have significant impacts on life history trajectories for American bullfrogs. This research contributes to our understanding of a potentially important invasion mechanism in an anuran species of conservation concern.