In situ and laboratory studies on the behaviour and survival of Pacific salmon (genus Oncorhynchus)

Juvenile Pacific salmon display a marked surface water orientation during downstream migration, estuarine and nearshore coastal rearing phases. Many estuaries in British Columbia are vertically stratified with a shallow, well-defined halocline which can restrict the dispersion of wastes discharged into less saline surface waters and impose constraints upon aquatic organisms. In situ experiments in an estuary receiving a surface discharge of treated pulp mill wastes, revealed conditions which were lethal to underyearling salmon at, and below the halocline (4.0–6.5 m depth). Behavioural bioassays determined that juvenile chinook salmon were biased towards the water surface and avoided waters at depth. Dissolved oxygen was the variable which affected this distribution most significantly. Surface waters receiving effluent from another pulp mill were lethal to juvenile salmon within 350 m, and a significant vertical avoidance response occurred within 350–950 m of the outfalls. The behavioural response was significantly correlated with in situ temperature, pH and colour (effluent).As a complement to field experiments we developed a 4500 l water column simulator (WCS) to examine salmon behaviour in the laboratory. We investigated the surface water orientation behaviour of juvenile salmon in relation to variations in salinity and dissolved oxygen. Under simulated vertically stratified estuarine conditions, the fish moved freely between overlying fresh water and salt water. Induction of hypoxic conditions in fresh water elicited a downward distribution shift towards the halocline and oxygenated, but more saline, waters. Avoidance reactions (50% level) occurred consistently up to 7–8 mg · l^–1 dissolved oxygen. Salmon continued to examine the hypoxic freshwater zone despite sub-optimal conditions.     

Environmental deterioration increases tadpole vulnerability to predation

Human-induced environmental change is occurring at an unprecedented rate and scale. Many freshwater habitats, in particular, have been degraded as a result of increased salinity. Little is known about the effects of anthropogenic salinization on freshwater organisms, especially at sublethal concentrations, where subtle behavioural changes can have potentially drastic fitness consequences. Using a species of Australian frog (Litoria ewingii), we experimentally examined the effects of salinization on tadpole behaviour and their vulnerability to a predatory dragonfly nymph (Hemianax papuensis). We found that tadpoles exposed to an ecologically relevant concentration of salt (15% seawater, SW) were less active than those in our freshwater control (0.4% SW). Tadpoles in elevated salinity also experienced a higher risk of predation, even though the strike rate of the predator did not differ between salt and freshwater treatments. In a separate experiment testing the burst-speed performance of tadpoles, we found that tadpoles in saltwater were slower than those in freshwater. Thus, it would appear that salt compromised the anti-predator response of tadpoles and made them more susceptible to being captured. Our results demonstrate that environmentally relevant concentrations of aquatic contaminants can, even at sublethal levels, severely undermine the fitness of exposed organisms.     

Fitness and community consequences of avoiding multiple predators

We investigated the fitness and community consequences of behavioural interactions with multiple predators in a four-trophic-level system. We conducted an experiment in oval flow-through artificial-stream tanks to examine the single and interactive sublethal effects of brook trout and stoneflies on the size at emergence of Baetis bicaudatus (Ephemeroptera: Baetidae), and the cascading trophic effects on algal biomass, the food resource of the mayflies. No predation was allowed in the experiment, so that all effects were mediated through predator modifications of prey behaviour. We reared trout stream Baetis larvae from just before egg development until emergence in tanks with four treatments: (1) water from a holding tank with two brook trout (trout odour), (2) no trout odour + eight stoneflies with glued mouthparts, (3) trout odour + stoneflies and (4) no trout odour or stoneflies. We ended the experiment after 3 weeks when ten male and ten female subimagos had emerged from each tank, measured the size of ten male and ten female mature nymphs (with black wing pads), and collected algal samples from rocks at six locations in each tank. To determine the mechanism responsible for sublethal and cascading effects on lower trophic levels we made day and night observations of mayfly behaviour for the first 6 days by counting mayflies drifting in the water column and visible on natural substrata in the artificial streams. Trout odour and stoneflies similarly reduced the size of male and female Baetis emerging from artificial streams, with non-additive effects of both predators. While smaller females are less fecund, a fitness cost of small male size has not been determined. The mechanism causing sublethal effects on Baetis differed between predators. While trout stream Baetis retained their nocturnal periodicity in all treatments, stoneflies increased drift dispersal of mayflies at night, and trout suppressed night-time feeding and drift of mayflies. Stoneflies had less effect on Baetis behaviour when fish odour was present. Thus, we attribute the non-additivity of effects of fish and stoneflies on mayfly growth to an interaction modification whereby trout odour reduced the impact of stoneflies on Baetis behaviour. Since stonefly activity was also reduced in the presence of fish odour, this modification may be attributed to the effect of fish odour on stonefly behaviour. Only stoneflies delayed Baetis emergence, suggesting that stoneflies had a greater sublethal effect on Baetis fitness than did trout. Delayed emergence may reduce Baetis fitness by increasing risks of predation and parasitism on larvae, and increasing competition for mates or oviposition sites among adults. Finally, algal biomass was higher in tanks with both predators than in the other three treatments. These data implicate a behavioural trophic cascade because predators were not allowed to consume prey. Therefore, differences in algal biomass were attributed to predator-induced changes in mayfly behaviour. Our study demonstrates the importance of considering multiple predators when measuring direct sublethal effects of predators on prey fitness and indirect effects on lower trophic levels. Identification of an interaction modification illustrates the value of obtaining detailed information on behavioural mechanisms as an aid to understanding the complex interactions occurring among components of ecological communities. Received: 20 March 1997 / Accepted: 29 September 1997     

Behaviour of growth hormone transgenic coho salmon Oncorhynchus kisutch in marine mesocosms assessed by acoustic tag telemetry

Underwater acoustic tag telemetry was used to assess behavioural differences between juvenile wild‐type (i.e. non‐transgenic, NT) and growth hormone (GH) transgenic (T) coho salmon Oncorhynchus kisutch in a contained simulated ocean environment. T O. kisutch were found across days to maintain higher baseline swimming speeds than NT O. kisutch and differences in response to feeding were detected between T and NT genotypes. This is the first study to assess behaviour of GH transgenic salmonids in a marine environment and has relevance for assessing whether behavioural effects of GH overexpression seen in freshwater environments can be extrapolated to oceanic phases of the life cycle.     

Dying from the lesser of three evils: facilitation and non‐consumptive effects emerge in a model with multiple predators

Prey modify their behaviour to avoid predation, but dilemmas arise when predators vary in hunting style. Behaviours that successfully evade one predator sometimes facilitate exposure to another predator, forcing the prey to choose the lesser of two evils. In such cases, we need to quantify behavioural strategies in a mix of predators. We model optimal behaviour of Atlantic cod Gadus morhua larvae in a water column, and find the minimal vulnerability from three common predator groups with different hunting modes; 1) ambush predators that sit‐and‐wait for approaching fish larvae; 2) cruising invertebrates that eat larvae in their path; and 3) fish which are visually hunting predators. We use a state‐dependent model to find optimal behaviours (vertical position and swimming speed over a diel light cycle) under any given exposure to the three distinct modes of predation. We then vary abundance of each predator and quantify direct and indirect effects of predation. The nature and strength of direct and indirect effects varied with predator type and abundance. Larvae escaped about half the mortality from fish by swimming deeper to avoid light, but their activity level and cumulative predation from ambush predators increased. When ambush invertebrates dominated, it was optimal to be less active but in more lit habitats, and predation from fish increased. Against cruising predators, there was no remedy. In all cases, the shift in behaviour allowed growth to remain almost the same, while total predation were cut by one third. In early life stages with high and size‐dependent mortality rates, growth rate can be a poor measure of the importance of behavioural strategies.     

Sea lice escape predation on their host

Parasites seldom have predators but often fall victim to those of their hosts. How parasites respond to host predation can have important consequences for both hosts and parasites, though empirical investigations are rare. The exposure of wild juvenile salmon to sea lice (Lepeophtheirus salmonis) from salmon farms allowed us to study a novel ecological interaction: the response of sea lice to predation on their juvenile pink and chum salmon hosts by two salmonid predators-coho smolts and cut-throat trout. In approximately 70% of trials in which a predator consumed a parasitized prey, lice escaped predation by swimming or moving directly onto the predator. This trophic transmission is strongly male biased, probably because behaviour and morphology constrain female movement and transmission. These findings highlight the potential for sea lice to be transmitted up marine food webs in areas of intensive salmon aquaculture, with implications for louse population dynamics and predatory salmonid health.     

Maternal predator-exposure has lifelong consequences for offspring learning in threespined sticklebacks

Learning is an important form of phenotypic plasticity that allows organisms to adjust their behaviour to the environment. An individual''s learning performance can be affected by its mother''s environment. For example, mothers exposed to stressors, such as restraint and forced swimming, often produce offspring with impaired learning performance. However, it is unclear whether there are maternal effects on offspring learning when mothers are exposed to ecologically relevant stressors, such as predation risk. Here, we examined whether maternal predator-exposure affects adult offsprings’ learning of a discrimination task in threespined sticklebacks (Gasterosteus aculeatus). Mothers were either repeatedly chased by a model predator (predator-exposed) or not (unexposed) while producing eggs. Performance of adult offspring from predator-exposed and unexposed mothers was assessed in a discrimination task that paired a particular coloured chamber with a food reward. Following training, all offspring learned the colour-association, but offspring of predator-exposed mothers located the food reward more slowly than offspring of unexposed mothers. This pattern was not driven by initial differences in exploratory behaviour. These results demonstrate that an ecologically relevant stressor (predation risk) can induce maternal effects on offspring learning, and perhaps behavioural plasticity more generally, that last into adulthood.     

As good as dead? Sublethal predation facilitates lethal predation on an intertidal clam

Although ecologists have speculated that sublethal predation can impact prey dynamics, consequences of these predator effects have seldom been experimentally tested. In soft‐sediment marine communities, fishes crop extended feeding siphons of buried clams, potentially causing clams to reduce their burial depth, thereby enhancing their susceptibility to excavating lethal predators. We simulated cropping of the confamilial clams, Protothaca staminea and Venerupis philippinarum, by removing the top 40% of siphons, which caused each species to burrow 33–50% shallower than conspecifics with intact siphons. To examine subsequent consequences of reduced burial depth, we exposed cropped and intact clams to natural levels of predation in the field. Because of a naturally longer siphon, Protothaca, even after cropping, remained at relatively safe burial depths. In contrast, siphon cropping nearly doubled the mortality rate of Venerupis. Thus, while sublethal predation facilitates lethal predation, this linkage depends on specific life history characteristics, even among ecologically similar species.     

Effect of salinity on the swimming behaviour of the estuarine calanoid copepod Eurytemora affinis

The calanoid copepod, Eurytemora affinis, is the dominant zooplanktonspecies in most of European and North American estuaries, andtheir population maintenance within an environment of net seawardflow has mainly been explained by endogenous rhythms of circatidalswimming activity. However, no attention has been paid to thepotential link between the swimming behaviour of this speciesand salinity. The swimming behaviour of males, non-ovigerousfemales and ovigerous females from a continuous culture wasinvestigated under different salinity conditions. Increase anddecrease in salinity, respectively, increased and decreasedthe overall swimming activity of both males and non-ovigerousfemales. The complexity of the swimming paths of males and non-ovigerousfemales significantly increased with salinity. In contrast,ovigerous females were less motile and mainly sank. These observationssuggest an endogenous behavioural adaptive strategy to salinityfluctuations and the intrinsic ability of E. affinis to undergoshort-scale vertical migration triggered by changes in salinity.This supports field observations reporting increased abundanceof E. affinis in the water column during flood tides and providesa behavioural basis for the maintenance of viable populationsunder net ouflow conditions.     

Intraspecific variation in behaviour: effects of evolutionary history, ontogenetic experience and sex

Geographical variation in behaviour within species is common. However, how behavioural plasticity varies between and within locally adapted populations is less studied. Here, we studied behavioural plasticity induced by perceived predation risk and food availability in pond (low predation - high competition) vs. coastal marine (high predation - low competition) nine-spined sticklebacks (Pungitius pungitius) reared in a common garden experiment. Pond sticklebacks were more active feeders, more risk-taking, aggressive and explorative than marine sticklebacks. Perceived predation risk decreased aggression and risk-taking of all fish. Food restriction increased feeding activity and risk-taking. Pond sticklebacks became more risk-taking than marine sticklebacks under food shortage, whereas well-fed fish behaved similarly. Among poorly fed fish, males showed higher drive to feed, whereas among well-fed fish, females did. Apart from showing how evolutionary history, ontogenetic experience and sex influence behaviour, the results provide evidence for habitat-dependent expression of adaptive phenotypic plasticity.     

Species specific behavioural patterns (digging and swimming) and reaction to novel objects in wild type, Wistar, Sprague-Dawley and Brown Norway rats

Background

The purpose of the present study was to analyse species-specific forms of behaviour (digging and swimming) and response to novelty in laboratory rats and their wild type counterparts at a very early stage of laboratorization. Three behavioural phenomena were taken into account: burrowing, spontaneous swimming, and neophobic behaviour.

Principal Findings

Wild-type rats and three strains of laboratory rats were involved in experiments: Warsaw-Wild-Captive-Pisula-Stryjek (WWCPS), Wistar, Sprague-Dawley, and Brown Norway rats were compared in spontaneous swimming test, while WWCPS and Wistar rats were studied in burrowing and neophobia experiments. Wild rats were found to be faster at building tunnels than Wistar rats and at constructing more complex burrow systems. The experiment on neophobia showed that Wistar rats exhibited less neophobic responses and were more often trapped. WWCPS rats showed highly neophobic behaviour and were rarely trapped in this experiment. The experiment on swimming showed that WWCPS rats showed more complex water tank related activity than their laboratory counterparts. They swam and explored under surface environment.

Conclusions

The three experiments showed profound behavioural differences in quasi-natural forms of behaviour between wild type rats (WWCPS) and three laboratory strains frequently used in behavioural studies.     

Fish kairomone regulation of internal swarm structure in Daphnia pulex (Cladocera: Crustacea)

In this laboratory experiment, swarms of D. pulex were artificially created by placing thirty individuals in small chambers containing 130 ml of water. The swimming behaviour of the animals was measured using a video camera and a programme to digitize observations. The D. pulex swimming in water with fish kairomones had a more uniform swimming speed compared with animals in control water. If aggregated prey individuals benefit from a reduced predation risk, and this risk is further reduced by uniformity of swarm members, the uniformity of swimming speed can be interpreted as an behavioural adjustment to minimize the vulnerability to predation. This revised version was published online in July 2006 with corrections to the Cover Date.     

Light-mediated predation by northern squawfish on juvenile chinook salmon

Northern squawfish Ptychocheilus oregonensis cause significant mortality of juvenile salmon in the lower Columbia River Basin (U.S.A.). The effects of light intensity on this predator-prey interaction were examined with laboratory experiments and modelling studies. In laboratory experiments, the rate of capture of subyearling chinook salmon Oncorhynchus tshawytscha by northern squawfish was inversely related to light intensity. In a large raceway, about five times more salmon were captured during 4 h periods of relative darkness (0–03 Ix) than during periods with high light intensity (160 Ix). The rate of predation could be manipulated by increasing or decreasing light intensity.
A simulation model was developed for visual predators that encounter, attack, and capture juvenile salmon, whose schooling behaviour was light-sensitive. The model was fitted to laboratory results using a Monte Carlo filtering procedure. Model-predicted predation rate was especially sensitive to the visual range of predators at low light intensity and to predator search speed at high light. Modelling results also suggested that predation by northern squawfish on juvenile salmon may be highest across a narrow window of fight intensity.     

Behaviour in a standardized assay,but not metabolic or growth rate,predicts behavioural variation in an adult aquatic top predator Esox lucius in the wild

This study tested for links among behaviour, state and life‐history variables as predicted by the pace‐of‐life hypothesis in adult pike Esox lucius. First, a standardized open‐field behavioural assay was developed to assess individual behaviour of wild‐captured adult E. lucius. Behaviour within the standardized assay predicted swimming behaviour in the lake, providing an ecological validation of the assay. There was no relationship between standardized behaviour and any of the life‐history and state variables, including metabolism, body condition, juvenile growth rate and adult growth rate in contrast to predictions from the pace‐of‐life hypothesis. This study demonstrates that it is possible to assess ecologically relevant behavioural variation in a large‐bodied top predator using a standard open‐field assay, but it is noteworthy that this standardized behaviour is not systematically related to standard metabolism or growth.     

The effect of predation risk on the predatory behaviour of a sit-and-wait predator,Ranatra dispar (Heteroptera: Nepidae), the water stick insect

Two primary defence behaviours, fore-leg extension to enhance crypsis and swimming to bottom and remaining motionless, of a predatory water bug,Ranatra dispar, are described along with their subsequent effect on foraging behaviour. It was hypothesised that hungry predators would respond less and for a shorter duration compared with recently fed individuals when exposed to a model threat stimulus, thereby tending to take a higher risk of predation during feeding than satiated animals. A greater proportion of animals responded overall with the leg extension response compared with the swimming response, although the mean duration of the former was significantly shorter than the latter response. A significantly higher proportion of nonfasted predators responded, and for a longer duration than fasted individuals. The type of model used significantly effected the proportion of animals that responded with leg extensions but not on its duration. In contrast, both number of animals and the duration of the swim/motionless behaviour were significantly effected by stimulus type. The subsequent effect of these 2 behavioural responses on feeding behaviour was examined and showed that although about the same number of predators removed prey from their mouthparts during both responses, significantly more prey were dropped, and therefore lost, during swimming. The results clearly indicate the significant effects that defensive behaviours have on time budgets in foraging behaviour.     

Predator-induced reaction patterns of landlocked <Emphasis Type="Italic">Galaxias maculatus</Emphasis> to visual and chemical cues

Anti-predator behaviour often represents a trade-off between the benefits of reducing predation risk and the drawbacks of limiting access to resources (e.g. food availability, mating and nesting sites). The effectiveness of avoidance behaviour relies on the ability to detect predator cues, which may provide reliable information on predation risk. Using controlled laboratory experiments, we studied the relative importance of visual and chemical cues in the triggering of anti-predator responses in Galaxias maculatus, where Oncorhyncus mykiss was used as the predator. Metabolic cost was also estimated, measured as oxygen consumption. Exposure to different types of predator cue induced diverse behavioural responses in G. maculatus. Detection of the exotic predator, using both visual and chemical stimuli, resulted in reduced G. maculatus swimming activity and changes in respiratory rate.     

The Interaction between Water Currents and Salmon Swimming Behaviour in Sea Cages

Positioning of sea cages at sites with high water current velocities expose the fish to a largely unknown environmental challenge. In this study we observed the swimming behaviour of Atlantic salmon (Salmo salar L.) at a commercial farm with tidal currents altering between low, moderate and high velocities. At high current velocities the salmon switched from the traditional circular polarized group structure, seen at low and moderate current velocities, to a group structure where all fish kept stations at fixed positions swimming against the current. This type of group behaviour has not been described in sea cages previously. The structural changes could be explained by a preferred swimming speed of salmon spatially restricted in a cage in combination with a behavioural plasticity of the fish.     

Adaptive flexibility in the behaviour of juvenile Atlantic salmon: short-term responses to food availability and threat from predation

Juvenile Atlantic salmon Salmo salar were shown experimentally to make adaptive behavioural decisions as a short-term response to changes in food availability and predation risk. Restricted food availability caused an increase in activity, whereas activity was decreased under predation threat. Although changes in activity were not more pronounced among the hunger-motivated fish, suggesting that they were not balancing risk and hunger, hungrier fish spent less time in refuges in the presence of a predator, indicating that they were more willing to take risks than satiated fish. Aggressive interactions among juvenile Atlantic salmon were decreased by predation threat, but were highest when predators were absent and food was abundant.     

Latent behavioural toxicity of copper to sea catfish, Arius felis, and sheepshead, Archosargus probatocephalus

To assess quantitatively the latent (delayed) toxicity of acutely sublethal exposure to copper on the locomotor and orientation behaviour of marine teleosts, the movements of individual sea catfish, Arius felis , and sheepshead porgy, Archosargus probatocephalus , were monitored electronically in a multiple-choice rosette tank immediately after 72-h static exposure to copper (0.0, 0.1, 0.2, or 0.4 mg Cu l⁻¹) and 1 week later. Initial hyperactivity following copper-exposure was exhibited by all fish of both species (except controls), as indicated by significant changes in the behavioural variables used to quantify locomotor activity. In addition, the orientation angles of successive movements in the monitor tank increased significantly for sea catfish, producing a decrease in the frequency of turning. Orientation angles of sheepshead showed a significant enhancement of the 'normal' tendency of this species to make small-angle turns in the tank, and to return immediately to the compartment just vacated (indicative of an increase in the frequency of turning). One week following exposure, all copper-exposed fish exhibited extreme hypoactivity which was significantly different from their behaviour immediately after exposure, and from the behaviour of control fish. This hypoactivity did not correspond, therefore, to 'normal' activity in either species. The delayed effect of copper exposure on orientation was to exacerbate significantly the species specific turning behaviour seen immediately following exposure. These results are discussed in terms of presumed accumulated physiological damage resulting from the exposure to copper and the initial hyperactivity such exposure elicits, and of general behavioural ecology.