Ambient pH and the response to chemical alarm cues in juvenile Atlantic salmon (Salmo salar): mechanisms of reduced behavioral responses.

Even at sublethal concentrations, various anthropogenic pollutants may disrupt the transfer of chemosensory information, often inducing maladaptive behavioral responses. Recent studies of freshwater prey fishes have shown impaired abilities to respond to damage-released chemical alarm cues from conspecifics under weakly acidic conditions (pH ; 6.0). Several factors acting individually or collectively may account for such chemosensory impairment. By itself, acidification may chemically disrupt the alarm cues and affect fish olfactory functions. Alternatively, differences in local environmental conditions may affect biochemical composition, quantity of chemical alarm cues produced by epidermal tissue, or both, leading to variations in alarm response. Our goal was to assess whether the ability to produce and detect onspecific chemical alarm cues is similar in individuals reared under neutral versus acidic conditions. We conducted two experiments in which we measured the behavioral response of wild juvenile Atlantic salmon Salmo salar exposed to chemical alarm cues. In particular, we looked for differences in the ability of individual fish to (1) produce alarm cues capable of eliciting consistent antipredator behavior in conspecifics and (2) detect alarm cues upon the fish’s introduction into a stream with a pH differing from that of the stream of origin; the latter experiment involved reciprocal transplant of fish between neutral (pH range ; 7.0–7.3) and acidic (pH range ; 5.9–6.3) sites. Our results demonstrate that the ability to produce and respond to chemical alarm cues is maintained in Atlantic salmon reared under acidic conditions and did not differ from that of fish reared under neutral conditions. Overall, these data suggest that no permanent olfactory damage occurred under reduced pH and, likewise, no significant difference in functional alarm cue production existed between Atlantic salmon reared under neutral and acidic conditions. Short-term reduction in olfactory sensitivity and degradation of the chemical alarm cues under acidic conditions are the likely mechanisms affecting detection of these important chemicals by prey fish

Impaired detection of chemical alarm cues by juvenile wild Atlantic salmon (Salmo salar) in a weakly acidic environment

Many prey fishes rely on damage-released chemical alarm cues to detect and avoid predators. The ability to use these cues has been shown to confer considerable survival benefits to individuals. While several laboratory studies and a single field study have demonstrated that an ambient pH of 6.0 impairs fishes in their ability to detect these alarm cues, no study had yet compared the response to alarm cue exposures across populations residing in multiple streams of a different acidity level. In our study, we conducted live behavioural observations in five nursery streams, ranging in pH from 5.71 to 7.49 on two age classes (young of the year and parr) of wild juvenile Atlantic salmon (Salmo salar). We aimed to assess if the detection of these chemical alarm cues was constantly dependant on the ambient pH or if variations in the detection occurred among populations of the different streams regardless of the ambient acidity level. Our results demonstrated that salmon present in any acidic stream did not respond to alarm cues, while those in neutral streams exhibited typical alarm responses

Effects of acidification on olfactory-mediated behaviour in freshwater and marine ecosystems: a synthesis

For many aquatic organisms, olfactory-mediated behaviour is essential to the maintenance of numerous fitness-enhancing activities, including foraging, reproduction and predator avoidance. Studies in both freshwater and marine ecosystems have demonstrated significant impacts of anthropogenic acidification on olfactory abilities of fish and macroinvertebrates, leading to impaired behavioural responses, with potentially far-reaching consequences to population dynamics and community structure. Whereas the ecological impacts of impaired olfactory-mediated behaviour may be similar between freshwater and marine ecosystems, the underlying mechanisms are quite distinct. In acidified freshwater, molecular change to chemical cues along with reduced olfaction sensitivity appear to be the primary causes of olfactory-mediated behavioural impairment. By contrast, experiments simulating future ocean acidification suggest that interference of high CO₂ with brain neurotransmitter function is the primary cause for olfactory-mediated behavioural impairment in fish. Different physico-chemical characteristics between marine and freshwater systems are probably responsible for these distinct mechanisms of impairment, which, under globally rising CO₂ levels, may lead to strikingly different consequences to olfaction. While fluctuations in pH may occur in both freshwater and marine ecosystems, marine habitat will remain alkaline despite future ocean acidification caused by globally rising CO₂ levels. In this synthesis, we argue that ecosystem-specific mechanisms affecting olfaction need to be considered for effective management and conservation practices

Sensory complement model helps to predict diel alarm response patterns in juvenile Atlantic salmon (Salmo salar) under natural conditions

Fish rely on both chemical and visual cues to evaluate predation risk. Decisions with respect to activity partitioning in time (i.e., night vs. day) rely on accurate assessment of predation risk relative to energy intake; predation risk is generally thought to be lower at night at the expense of feeding opportunities. At night, the sensory complement model predicts greater reliance on chemical perception of risk. Under this condition, a lower ability to use vision should result in a more conservative response to chemical cues than during the day. We tested this hypothesis under natural conditions by comparing the alarm response of young-of-the-year Atlantic salmon (Salmo salar L., 1758) under summer day and night conditions in salmon nursery streams. We found that salmon responded to the alarm cues to a significantly greater extent at night. This suggests that the sensory complement model may be correct and that nocturnal perception of risk may be generally higher than previously believed for juvenile salmon in the wild. In the absence of a more precise indicator of risk (e.g., vision), a greater reliance on chemosensory risk assessment at night may cause fish to shift to more risk-adverse behaviour

Effects of acidification on olfactory-mediated behaviour in freshwater and marine ecosystems: a synthesis

For many aquatic organisms, olfactory-mediated behaviour is essential to the maintenance of numerous fitness-enhancing activities, including foraging, reproduction and predator avoidance. Studies in both freshwater and marine ecosystems have demonstrated significant impacts of anthropogenic acidification on olfactory abilities of fish and macroinvertebrates, leading to impaired behavioural responses, with potentially far-reaching consequences to population dynamics and community structure. Whereas the ecological impacts of impaired olfactory-mediated behaviour may be similar between freshwater and marine ecosystems, the underlying mechanisms are quite distinct. In acidified freshwater, molecular change to chemical cues along with reduced olfaction sensitivity appear to be the primary causes of olfactory-mediated behavioural impairment. By contrast, experiments simulating future ocean acidification suggest that interference of high CO₂ with brain neurotransmitter function is the primary cause for olfactory-mediated behavioural impairment in fish. Different physico-chemical characteristics between marine and freshwater systems are probably responsible for these distinct mechanisms of impairment, which, under globally rising CO₂ levels, may lead to strikingly different consequences to olfaction. While fluctuations in pH may occur in both freshwater and marine ecosystems, marine habitat will remain alkaline despite future ocean acidification caused by globally rising CO₂ levels. In this synthesis, we argue that ecosystem-specific mechanisms affecting olfaction need to be considered for effective management and conservation practices