Effects of ambient acidity on chemosensory learning: an example of an environmental constraint on acquired predator recognition in wild juvenile Atlantic salmon (Salmo salar)

Abstract –  In many prey fish species, learning the identity of novel predators may be facilitated when novel predator cues and an aversive stimulus are presented together. Damage-released chemical alarm cues are typically released from the skin of prey individuals following mechanical damage and are known to mediate the learned recognition of novel predators. While such chemically mediated acquired predator recognition can provide increased survival benefits to prey, environmental constraints impeding learning may exist. For example, in several fish species the ability to detect chemical alarm cues is impaired in under acidic conditions and as such, inhibits this chemically mediated learning. In this experiment, we studied in two streams of different mean acidity level (pH c . 6.0 and 7.0), to assess if wild juvenile Atlantic salmon ( Salmo salar ) had the ability to acquire the recognition of a novel lemon essence odour when paired with conspecific chemical alarm cues. Our results demonstrate that under acidic conditions, no learned recognition of the novel odour occurred. In neutral conditions, however, salmon recognised the novel odour as a predation threat. This result suggests that ambient acidity creates an environmental constraint on chemically mediated learned recognition of a novel cue.     

Antipredator behaviour of naïve Arctic charr young in the presence of predator odours and conspecific alarm cues

Abstract –  We investigated how Arctic charr young respond behaviourally to olfactory cues from skin-damaged conspecifics, charr-fed pikeperch, and the combination of food-deprived pikeperch and skin-damaged conspecific cues in a two-channel Y-maze fluviarium test arena. Significant antipredator responses were found to skin-damaged conspecifics in three behavioural traits, to charr-fed pikeperch in two traits and to the combination of pikeperch and skin-damaged conspecific cues in all six behaviours investigated. The combination of predator and conspecific cues significantly increased spatial avoidance and cautiousness to approach the source of scent compared with odours from charr-fed predators. The results suggest that damage-released alarm cues exist in charr, and they strengthen the antipredator responses in conspecifics. As the charr used different behaviours and levels of response in the presence of different cues, they seem to have sophisticated skills to distinguish between different odour combinations and be able to adjust their behaviour according to the current predation risk level.     

Alarm substances elicit limited population‐level responses in fathead minnow

Abstract – Alarm substances, chemical cues released by injured prey, are associated with increased predation risk. In the laboratory, fathead minnows limit conspicuous behaviours, such as foraging and nest guarding, when exposed to these cues. Although such responses could lead to reductions in growth and reproduction, with subsequent demographic consequences (e.g., recruitment), effects of alarm substances at the population level are largely unknown. In three field experiments, ponds and cattle troughs stocked with fathead minnow populations were treated with alarm substances or a water control over the summer breeding and growing season. Alarm substances had no effect on male parental behaviour. In one experiment, spawning occurred earlier with exposure to alarm substances; however, there was no subsequent effect on recruitment of young in this or in the other two experiments. Despite individual‐level effects in short‐term experiments, repeated exposure to alarm substances over a season had no measureable impact at the population scale.     

Size‐dependent stress response in juvenile Arctic charr (Salvelinus alpinus) under prolonged predator conditioning

Predator conditioning can be used to improve post‐release antipredator recognition of hatchery‐reared salmonids. However, possible negative stress‐related effects of prolonged predator conditioning on juvenile fish physiology are poorly understood. We studied the effects of prolonged (91 days) predator odour exposure on whole‐body cortisol level and spleen size in six full‐sib families of juvenile hatchery‐bred Arctic charr (Salvelinus alpinus). Chemical cues from water containing charr‐fed pikeperch (Sander lucioperca) were used as the predator exposure stimuli and lakewater was used as a chemical control. Our study revealed that juvenile body cortisol levels post‐predator conditioning were affected by treatment, fish size and their interaction. Importantly, among the smaller (i.e. slowest growing) charr, the predator‐exposed fish had higher cortisol levels than control fish, while the opposite pattern was true for the larger fish. These results suggest that chemical cues from charr‐fed predators induce a prolonged stress response in juvenile charr. As prolonged predation exposure seems to elevate stress levels in a size‐dependent manner, the larger, faster growing fish could possibly have intrinsically lower stress responses to predation threats than smaller, slower growing fish. Possible coupling between stress sensitivity and growth requires further attention due to the likely implications for the management of unintended domestication among captive‐reared salmonids.     

Effects of predator-induced visual and olfactory cues on 0+ perch (Perca fluviatilis L.) foraging behaviour

Abstract –  Foraging juvenile fish with relatively high food demands are usually vulnerable to various aquatic and avian predators. To compromise between foraging and antipredator activity, they need exact and reliable information about current predation risk. Among direct predator-induced cues, visual and olfactory signals are considered to be most important. Food intake rates and prey-size selectivity of laboratory-reared, naive young-of-the-year (YOY) perch, Perca fluviatilis , were studied in experiments with Daphnia magna of two size classes: 2.8 and 1.3 mm as prey and northern pike, Esox lucius , as predator. Neither total intake rate nor prey-size selectivity was modified by predator kairomones alone (water from an aquarium with a pike was pumped into the test aquaria) under daylight conditions. Visual presentation of pike reduced total food intake by perch. This effect was significantly more pronounced (synergistic) when visual and olfactory cues were presented simultaneously to foraging perch. Moreover, the combination of cues caused a significant shift in prey-size selection, expressed as a reduced proportion of large prey in the diet. Our observations demonstrate that predator-induced olfactory cues alone are less important modifiers of the feeding behaviour of naive YOY perch than visual cues under daylight conditions. However, pike odour acts as a modulatory stimulus enhancing the effects of visual cues, which trigger an innate response in perch.     

Foraging behaviour of juvenile pink salmon (Oncorhynchus gorbuscha) and size‐dependent predation risk

Two hypotheses related to effects of juvenile pink salmon (Oncorhynchus gorbuscha) foraging behaviour and size on their predation risk were evaluated using field data collected in Prince William Sound, Alaska 1 995–97. My results supported the hypothesis that low macrozooplankton density leads to dispersion of juvenile salmon from shallow nearshore habitats and greater predation risk, but zooplankton type was an important factor. When the biomass of large copepods (primarily Neocalanus spp.) declined, salmon dispersed from shallow nearshore habitats, and mean daily individual predator consumption of salmon increased by a factor of 5. A concomitant five‐fold increase in the probability of occurrence of salmon in predator stomachs supported the notion that increased predation on salmon was caused by a greater overlap between predator and prey when salmon dispersed offshore, not an increase in the number of salmon consumed per feeding bout. The results also generally supported the hypothesis that the timing of predation events modifies the nature of size‐dependent predation losses of salmon to different predator groups (small and large planktivores and piscivores). Size‐dependent vulnerabilities of salmon to predators were a function of both predator and prey sizes. When simulated predation was shifted from May to June, the vulnerability of salmon became more dependent on their growth than initial size. But, the size‐ and growth‐dependent vulnerabilities of salmon differed more among predator groups than between May and June, suggesting that changes in the composition of predator fields could more strongly affect the nature of size‐dependent predation than changes in the timing of predation losses.     

Predation risk allocation or direct vigilance response in the predator interaction between perch (Perca fluviatilis L.) and pike (Esox lucius L.)?

Abstract –  Predation risk allocation hypothesis predicts that a prey's response to predator depends on prey's previous experience on predator. Here we tested whether the group of three perch respond differentially to pike, predator of perch, depending on the timing of high constant (HC) and high unpredictable (HU) risk periods within low constant risk periods in short-term (10 h) experiments, and whether the response is stronger during a HU risk period than during a HC risk period. Perch clearly erected the dorsal fin in response to predation risk treatments (pike odour only, odour and visible pike). Decrease in activity and increase in shoaling behaviour were observed mainly during high risk periods. However, the perch's responses to pike did not differ statistically between periods of various levels of predation risk or depending on the timing of high risk situations within constant low risk periods, and thus, suggesting that perch respond mainly to changes in the current predation risk.     

Variability and stability in predation landscapes: A cross‐ecosystem comparison on the potential for predator control in temperate marine ecosystems

Predation can play an important role in population, community and ecosystem processes. When predator guilds are diverse, fluctuations in individual predator populations may have small influences on the guild at large, suggesting that predator diversity stabilizes the amount of predation prey experience. The strength of this phenomenon depends on how synchronously populations within predator assemblages vary and whether all predators are equally important consumers. We utilized a database of biomasses of fish species across ten temperate marine ecosystems paired with diet composition and feeding rate information from mass‐balance food web models to develop a predation index that weights the importance of predators on a prey based on predator feeding habits. Using the index, we asked how diverse sources of predation in these ecosystems are and how much diversity stabilizes variability in predation. Predator assemblages displayed a wide range of diversity; in one‐third of assemblages, a single predator group accounted for over half of all predation. Abundances of predator populations within assemblages generally varied independently of one another (neither synchronously nor asynchronously), implying an intermediate stabilization on predation intensity by predator diversity. Accounting for interaction strength (versus mere presence) is critical for interpreting the predator landscape; doing so led to a wider range in predator assemblage diversity and less synchronous assemblages. This work challenges conventional notions that marine food webs are diverse and therefore less susceptible to predator control. Future work should consider the temporal variability of the predator assemblages and account for differences in mortality induced by each predator population.     

Foraging arena theory

There is a critical need for quantitative models that can help evaluate trade‐off decisions related to the impacts of harvesting and protection of aquatic ecosystems within an ecosystem context. Ecosystem models used to evaluate such trade‐offs need to have the capability of capturing the dynamic stability that can arise when predator‐prey interactions are restricted to spatial and temporal arenas. Foraging arenas appear common in aquatic systems and are created by a wide range of mechanisms, ranging from restrictions of predator distributions in response to predation risk caused by their own predators, to risk‐sensitive foraging behaviour by their prey. Foraging arenas partition the prey in each predator‐prey interaction in a food web into vulnerable and invulnerable states, with exchange between these states potentially limiting overall trophic flow. Inclusion of vulnerability exchange processes in models for recruitment processes and food web responses to disturbances like harvesting leads to very different predictions about dynamic stability, trophic cascades and maintenance of ecological diversity than do models based on large‐scale mass action (random mixing) interactions between prey and predators. Although a number of methods to estimate these critical exchange rates are presented, none are considered fully satisfactory. The most important challenge for the practical application of models that incorporate foraging arena theory today is not only developing new or improved methods for measuring exchange rates but also evaluating how such rates vary in responses to major fishery‐induced changes in abundances of predators.     

Food abundance affects both morphology and behaviour of juvenile perch

Abstract –  Behaviour and morphology were both shown to differ between 1+ perch from two lakes that in earlier studies showed differences in size-specific predation risk. As the level of nourishment is known to affect behaviour and morphology, we fed perch of the two lakes in tanks for 40 days with two food levels, to study whether observed differences remain stable with changes in food availability. The perch fed in excess grew significantly, while the perch at the low food conditions lost weight, clearly indicating undernourishment. In aquarium experiments, the starved perch from both lakes were much bolder in the trade-off between foraging and predator avoidance than their well-fed conspecifics. In addition, the shape of perch differed significantly between feeding treatments. At low food levels perch got a more slender body, while at high food levels they developed a deeper body and a relatively smaller head. Independent of feeding level, the comparison between the two lakes revealed a clearly deeper body and a larger head area for one population, a shape difference that remained stable after the feeding period. The results give evidence that the level of nourishment is an important factor that quickly alters risk-taking behaviour. In body morphology, however, more stable shape characteristics must be distinguished from more flexible ones. Consequently, the level of nourishment is a potential factor that may quickly hide other proximate cues and must be considered attentively in studies, in which shape changes and behaviour are related to environmental factors like diet, predation pressure or habitat diversity.