Antoine O.H.C. Leduc

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.

Combined effects of chemical and visual information in eliciting antipredator behaviour in juvenile Atlantic salmon Salmo salar.

Under natural conditions, both young-of-the-year (YOY; 0+ year) and parr (1+ year) Atlantic salmon Salmo salar exhibited strong antipredator behaviour (e.g. increase in latency to resume foraging) following the exposure to damage-released chemical alarm cues relative to a stream water control. Subsequent exposure to a novel visual stimulus had contrasting results. Parr increased their reactive distance to the visual stimulus if they had been previously exposed to a chemical alarm cue, whereas YOY did not. On the other hand, both YOY and parr took significantly longer to resume foraging when exposed to a visual stimulus if they had been previously exposed to a chemical alarm cue than control groups. While YOY and parr differed in the type and intensity of antipredator responses to both chemical and visual stimuli, perhaps due to differential costs and benefits associated with age, both used the chemical and the visual information in a combined manner.

Learning to recognize novel predators under weakly acidic conditions: the effects of reduced pH on acquired predator recognition by juvenile rainbow trout

Summary. Recent studies have demonstrated that under weakly acidic conditions (pH 6.0), many prey fishes, including juvenile rainbow trout (Onchorhynchus mykiss), do not exhibit overt antipredator responses to conspecific chemical alarm cues. In laboratory trials, we investigated the potential effects of reduced pH on the ability of hatchery reared, predator naïve juvenile rainbow trout to acquire the recognition of a novel predator (yellow perch, Perca flavenscens). Initially, we exposed trout to the odour of a predatory yellow perch, buffered to pH 6.0 (weakly acidic) or pH 7.0 (neutral) paired with conspecific skin extracts (also buffered to pH 6.0 or 7.0) or a distilled water control. Juvenile trout exhibited significant increase in antipredator behaviour when exposed to neutral skin extract (pH 7.0). When retested 48 hours later to perch odour alone (pH 7.0), only trout initially conditioned with neutral skin extracts (pairs with either neutral or acidic perch odour) exhibited a learned recognition of perch odour as a predator risk. Those initially exposed to weakly acidic skin extract or the distilled water control did not show a learned response to predator odour. These results demonstrate that the ability to acquire the recognition of novel predators is impaired under weakly acidic conditions, as would occur in natural waterways affected by acidic precipitation.

Effects of acid rainfall on juvenile Atlantic salmon (Salmo salar) antipredator behaviour: loss of chemical alarm function and potential survival consequences during predation

Many organisms rely on chemosensory cues to mediate predation risks. Recent studies have demonstrated impaired chemosensory detection ability under weak acidification. Because rainfall may lead to episodic acidification of surface water, we assessed the effects of acid rain on chemosensory alarm functions. Under natural conditions, we quantified alarm behaviour of juvenile Atlantic salmon (Salmo salar) exposed to conspecific chemical alarm cues before and following rainfall. Before rainfall, salmon were capable of an alarm response in the study streams. After rainfall, salmon from Devils Brook did not respond to the alarm cues whereas the detection of salmon from Catamaran Brook (a comparable stream having higher acid neutralising capacity) was maintained. To relate these findings to predator-prey encounters, we performed a second experiment where we staged encounters between prey (rainbow trout, Oncorhynchus mykiss) and predator (largemouth bass, Micropterus salmoides) exposed to acidified and unacidified rainbow trout chemical alarm cues. Trout exposed to acidified alarm cues survived for a significantly shorter amount of time than trout exposed to unacidified alarm cues, whereas no difference in overall predator behaviour was observed. Our results suggest that episodic acidification in small nursery streams may disrupt the chemical information mediated by the chemical alarm cues that can translate into higher survival costs for prey.

Ambient pH and the Response to Chemical Alarm Cues in Juvenile Atlantic Salmon: Mechanisms of Reduced Behavioral Responses

Abstract 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 conspecific 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 ...

In situ effects of human disturbances on coral reef-fish assemblage structure: temporary and persisting changes are reflected as a result of intensive tourism

Non-lethal human disturbances are often drivers of change in animal population and community structure. To gauge their severity, short-term behaviour (e.g. avoidance and habituation) has been argued to be a sensitive measure. However, many of these behavioural changes may occur only if disturbance-free habitat is readily accessible. In coral-reef fish, we tested whether human disturbances from intensive (i.e. loud music, swimming, snorkelling, splashing and fish feeding by numerous visitors) tourist visitations resulted in assemblage structure shifts led by short-term behaviour. We monitored fish assemblage before, during and after tourist visitations to monitor changes associated with behaviour. Additionally, we monitored two adjacent reefs not visited by tourists because of difficult approach by boat. We posited that if short-term benefits of relocating to disturbance-free habitat outweigh the costs of tolerating disturbances, fish assemblage structure should shift along with tourist visitation levels. By contrast, if sensitive species are unable or unwilling to relocate, we predicted greater levels of assemblage heterogeneity between the visited and control reefs. Our results showed that in situ human visitations led to significant shifts in assemblage structure, resulting from short-term behavioural changes. Additionally, we showed significant between-reefs differences, whereby control reefs were characterised by higher species richness, larger fish sizes and variations in relative trophic guild prevalence. Our results suggest that short-term relocations to adjacent disturbance-free reefs may not mitigate the effects of human disturbances.

Social context, competitive interactions and the dynamic nature of antipredator responses of juvenile rainbow trout Oncorhynchus mykiss

The effects of food ration and social context, as well as possible interactions, on the antipredator behaviour of juvenile rainbow trout Onchorhynchus mykiss were investigated in a pair of laboratory studies. In experiment 1, pairs of dominant and subordinate O. mykiss were exposed to conspecific alarm cues when maintained under high or low food rations. Under high food rations, dominant individuals responded to predation risk, whereas subordinates used the opportunity to feed. Under low food ration, however, the opposite pattern was observed, where subordinates responded to predation cues and dominants did not. Experiment 2 consisted of performing the same experiment, however separating the dominant and subordinate O. mykiss 3 h before testing. When tested separately, dominant and subordinate individuals did not differ in their responses to alarm cues, regardless of food ration. These results demonstrate that there is a complex interaction between current energy status and social context on decision making by prey animals.

Global trends on reef fishes’ ecology of fear: Flight initiation distance for conservation

Escape behaviors have a great potential as an indicator of the efficacy of management. For instance, the degree of fear perceived by fishes targeted by fisheries is frequently higher in unprotected marine areas than in areas where some protection is provided. We systematically reviewed the literature on how fear, which we define as variation in escape behavior, was quantified in reef fishes. In the past 25 years, a total of 33 studies were identified, many of which were published within the last five years and nearly 40% of those (n = 13) focused on Indo-Pacific reefs, showing that there are still many geographical gaps. While eleven escape metrics were identified to evaluate fish escape, flight initiation distance (FID) was the most commonly employed (n = 23). FID was used to study different questions of applied and theoretical ecology, which involved 14 reef fish families. We also used a formal meta-analysis to investigate the effects of fishing by comparing FID inside and outside marine protected areas. Fishes outside MPAs had increased FID compared to those inside MPAs. The Labridae family had a significantly higher effect sizes than Acanthuridae and Epinephelidae, suggesting that fishes in this family may be indicators of effective MPAs using FID. We conclude that protocols aimed to quantify fear in fishes, which provide accurate assessments of fishing effects on fish escape behavior, will help gauge the compliance of marine protected areas.