Feeding and Refuge Use by Small Fish in the Presence of Cyanobacteria Blooms

We studied the effect of cyanobacteria on foraging and refuge use in small fish. We measured pike larval feeding in the presence of cyanobacteria by counting leftover prey. Our results showed that feeding by pike larvae on zooplankton prey decreased significantly in the presence of non-toxic cyanobacteria. The behaviour can be due to lowered vision caused by turbidity or clogging of the gills. Further, we tested whether the three-spined stickleback use toxic cyanobacteria as a refuge against predators in a choice experiment. The choice experiment was performed in a Y-maze fluviarum, where the fish could select between two different environments. Our results support the refuge use hypothesis because the three-spined stickleback clearly preferred toxic cyanobacteria to the chemical predator signal. To conclude, cyanobacteria decrease feeding rates in fish larvae, but may function as important refuge for e.g. sticklebacks, during predation pressure in pelagic algal blooms.     

The effects of habitat‐ and diet‐based cues on association preferences in the three‐spined stickleback (Gasterosteus aculeatus)

A number of recent papers have investigated the potential of familiarity to organize the distributions of free‐ranging animals. It is not clear, however, to which extent individual recognition or a more general recognition of a group odour is responsible for familiarity preferences. First, we tested the sensory basis of the recognition of familiars in three‐spined stickleback ( Gasterosteus aculeatus ). When allowed to choose between a familiar and an unfamiliar stimulus shoal on the basis of both visual and chemical communication, visual communication only and chemical communication only, the preference of focal fish for familiars was shown to be dependent on the presence of chemical cues. We subsequently investigated the mechanisms underlying such association preferences, specifically the effects of recent habitat and diet on preferences. Experimental fish were divided into four treatment groups consisting of two environment treatments (saline and freshwater) and two diet treatments ( Daphnia spp. and chironimid larvae). Focal fish subsequently showed significant association preferences for groups of unfamiliar fish that had undergone the same environment or diet treatment as themselves, suggesting self‐referent matching. These data indicate that individual recognition is not a pre‐requisite for the expression of familiarity preferences.     

Threat‐sensitive predator avoidance by pike larvae

The threat‐sensitive predator avoidance (TSPA) hypothesis was tested on hatchery‐reared pike Esox lucius larvae. Larval swimming activity, food attacks upon zooplankton, escapes, immobility behaviour, vigilance, as well as time in vegetation under different predation risk were measured. Single larvae were video‐filmed in aquaria allowing them to have visual contact with a small or a large perch Perca fluviatilis as predator. The odds of fleeing increased significantly if the larvae were exposed to a large predator instead of a small one. Swimming activity and foraging decreased significantly in the presence of a predator compared to the control. On the other hand, no significant effect was detected in time spent in the vegetation, and in vigilance of larvae, measured as time intervals between food attacks. The findings suggest that pike larvae primarily flee in the presence of a large predator, whereas they remain immobile, and forage, when possible, in the presence of a small predator. Sometimes a lack of response between the large and the small predator treatments was detected, which suggests that the antipredator response has a threshold, and when increasing the threat, the prey response does not increase. In the present paper it is demonstrated that hatchery‐reared pike larvae respond to the level of threat, and thereby seem to be risk adjusting as predicted.     

The effect of Schistocephalus solidus infection on meal size of three‐spined stickleback

The effect of infection with the pseudophyllidean cestode Schistocephalus solidus on the meal size of individually housed three‐spined stickleback Gasterosteus aculeatus was quantified. Infected fish harboured plerocercoid loads that contributed from 1·1 to 33·9% of their total mass. Across this range of infection levels, the presence of S. solidus infection had no significant directional effect on standard length ( L _S) corrected meal size of host three‐spined sticklebacks. Amongst multiply infected fish there was a significant negative relationship between L _S‐corrected meal size and the proportion of host mass contributed by S. solidus parasites. This relationship, however, did not hold for singly‐infected fish. Furthermore, the data suggest that multiply‐infected fish that harbour a combined mass of parasites contributing < c . 15% to host body mass might exhibit meal sizes that exceed those of length‐matched uninfected fish. The results suggest that although heavy infections can significantly reduce the meal size of heavily infected three‐spined sticklebacks, in the early stages of multiple S. solidus infections host food intake may increase. The probable causes of these differential effects on meal size and their consequences for the host‐parasite system are discussed.     

Turbidity decreases anti-predator behaviour in pike larvae, <Emphasis Type="Italic">Esox lucius</Emphasis>

Synopsis We tested how algal turbidity and light conditions influence anti-predator behaviour of first-feeding pike. Results showed that pike larvae were able to detect the predator by both chemical and visual signals in turbid water. However, the anti-predator behaviour was reduced in turbid water compared with clear water. Larvae hid in the vegetation in the presence of predator cues more in clear water than in turbid water. The attack rate on zooplankton in clear water was lower in the presence of predator cues, whereas no such difference was detected in turbid water. Both of these results indicate that turbidity acted as a refuge for larvae. Light proved to be an important regulating factor for feeding pike in the absence of predators, demonstrated as lowered attack rates in 50 light level in both clear and turbid water. This indicates that long-term turbidity may be critical for small larvae, which need to feed continuously to survive.     

Differences in response to hypoxia in the three‐spined stickleback from lotic and lentic localities: dominance and an anaerobic metabolite

Dominance hierarchies of the three‐spined stickleback Gasterosteus aculeatus from river and pond populations were subjected to hypoxia (20%, range ± 1%). Under hypoxia, the hierarchies were less stable in terms of rank position and tissue L‐lactate was higher in river fish than pond fish under normoxia and hypoxia. Dominant fish gained mass under normoxia but lost mass under hypoxic conditions possibly due to them maintaining high levels of aggression.     

Effects of macroalgal exudates and oxygen deficiency on survival and behaviour of fish larvae

Filamentous algae may create anoxic, i.e. oxygen free, conditions during night and fish larvae that commonly spend their first months in the littoral may therefore be subject to anoxia. We conducted two different experiments; firstly, we measured behaviour of pike larvae (Esox lucius L.), such as frequency of prey attacks and time in vegetation, in the presence of a chemical predator cue and oxygen deficiency. In the second experimental set-up, pike larval survival was monitored in water with added macro-algal exudates (excreted from Pilayella littoralis) and a low oxygen level (3 mg l^− 1). Our results showed that oxygen concentration and the chemical predator signal, caused by three-spined sticklebacks, had strong significant effects on the larval prey attacks. The prey attacks were strongly reduced at 3 mg oxygen l^− 1. However, survival of the larvae was not affected by low oxygen and macro-algal exudates. Pike larvae are very tolerant to hypoxia and exudates excreted by the littoral vegetation, whereas prey attacks are strongly decreased in hypoxia when a predator is around. This may have negative consequences for pike larval growth and recruitment in eutrophicated environments.     

Body condition and reproductive capacity of three‐spined stickleback infected with the cestode Schistocephalus solidus

The relationship between reproductive ability and the residual index of body condition in three‐spined stickleback Gasterosteus aculeatus from a population infected with the cestode macroparasite Schistocephalus solidus in Walby Lake, Alaska, was examined. In general, reproductive activities resulted in significantly lower levels of body condition in three‐spined stickleback during the latter part of the breeding season, and relatively high levels of S. solidus infection intensified the energetic drain. Although female body condition did not differ significantly due just to the presence of S. solidus , increased parasite index did have a significant negative effect on female body condition. Males showed significantly lower levels of body condition in response to S. solidus infection alone and in association with a greater parasite index. Males had greater mean parasite indices than females. Females had significantly lower body condition than males, which may be due to discrepancies in energy expenditure between the sexes during reproduction. Females with greater body condition were significantly more likely to produce a clutch of eggs than those with lower condition, suggesting a threshold effect of body condition on reproductive capacity.     

Invasive pike establishment in Cook Inlet Basin lakes,Alaska: diet,native fish abundance and lake environment

Northern pike (Esox lucius) were introduced to the northern Susitna Basin of south-central Alaska in the 1950’s, and have since spread throughout the upper Cook Inlet Basin. Extirpations of several native fish populations have been documented in this area. It is hypothesized here that invasive pike remodel the ecology of lakes by removing vulnerable prey types and that these changes are reflected in the diet of invasive pike. Trends in pike diet suggest that pike switch to less desirable but more abundant macroinvertebrate prey as preferred fish prey are eliminated. The impacts of pike introduction were studied in detail for one species of resident fish, the threespine stickleback (Gasterosteus aculeatus). Stickleback abundance decreases as pike invasion progresses. Conductivity is a significant environmental predictor of stickleback abundance, with higher conductivity apparently mitigating population reduction. Higher conductivity water may lessen the physiological costs of developing more robust armor, which reduces vulnerability to predation. Maximum lake depth also appears to predict stickleback abundance, though this trend was only marginally significant. Deeper lakes may provide an open-water refuge from pike predation by allowing stickleback to exist outside of the pike inhabited littoral zone. These findings indicate the importance of diverse habitat types and certain chemical and physical characteristics to the outcome of invasion by fish predators.     

Prey selection by the larvae of three species of littoral fishes on natural zooplankton assemblages

The prey selection of larvae of three common littoral fish species (pike, Esox lucius; roach,Rutilus rutilus; and three-spined stickleback, Gasterosteus aculeatus) was studied experimentally in the laboratory by using natural zooplankton assemblages. Zooplankton prey was offered at four different concentrations to study the functional responses of the planktivores. The diets of pike and sticklebacks were formed mainly of copepod juveniles and adults, which dominated the prey communities, although sticklebacks ate also cladocerans. The diet of roach larvae consisted of rotifers, cladocerans and copepods, without prey selection, in equal proportions indicating a more omnivorous diet. All fish larvae were able to feed selectively although in sticklebacks prey selection was less pronounced. Pike and roach larvae preferred large prey to smaller prey types. Patterns of prey selection are discussed in the context of size-selection theory and apparent vs. true selection.     

Piscivore efficiency and refuging prey: the importance of predator search mode

In predator-prey interactions, the efficiency of the predator is dependent on characteristics of both the predator and the prey, as well as the structure of the environment. In a field enclosure experiment, we tested the effects of a prey refuge on predator search mode, predator efficiency and prey behaviour. Replicated enclosures containing young of the year (0+) and 1-year-old (1+) perch were stocked with 3 differentially sized individuals of either of 2 piscivorous species, perch (Perca fluviatilis), pike (Esox lucius) or no piscivorous predators. Each enclosure contained an open predator area with three small vegetation patches, and a vegetated absolute refuge for the prey. We quantified the behaviour of the predators and the prey simultaneously, and at the end of the experiment the growth of the predators and the mortality and habitat use of the prey were estimated. The activity mode of both predator species was stationary. Perch stayed in pairs in the vegetation patches whereas pike remained solitary and occupied the corners of the enclosure. The largest pike individuals stayed closest to the prey refuge whereas the smallest individuals stayed farthest away from the prey refuge, indicating size-dependent interference among pike. Both size classes of prey showed stronger behavioural responses to pike than to perch with respect to refuge use, distance from refuge and distance to the nearest predator. Prey mortality was higher in the presence of pike than in the presence of perch. Predators decreased in body mass in all treatments, and perch showed a relatively stronger decrease in body mass than pike during the experiment. Growth differences of perch and pike, and mortality differences of prey caused by predation, can be explained by predator morphology, predator attack efficiency and social versus interference behaviour of the predators. These considerations suggest that pike are more efficient piscivores around prey refuges such as the littoral zones of lakes, whereas perch have previously been observed to be more efficient in open areas, such as in the pelagic zones of lakes.     

Antipredator behaviour of 0+ year Perca fluviatilis: effect of vegetation density and turbidity

In this study, the combined influence of vegetation density and water turbidity on habitat utilization of a prey fish, 0+ year perch Perca fluviatilis , under predation risk (pike, Esox lucius ) was investigated. The vegetated habitat was overall preferred over the open habitat in the presence of a predator. The level of turbidity, and to a lesser extent vegetation density, however, influenced the response of 0+ year perch. The use of the vegetated habitat was lower in very turbid than in clear and turbid conditions, suggesting reduced antipredator behaviour in very turbid water. The effect of vegetation density on antipredator behaviour was only present in clear water, where the use of a structural refuge decreased with increasing vegetation density. No such effect was observed in turbid and very turbid water. The results showed that the structuring role of vegetation or habitat complexity may diminish with increased turbidity. The observed masking effect of turbidity suggests that predator‐prey interactions in vegetated habitats are more complex than what has generally been thought.     

The relationship between dominance behaviour and growth as a function of habitat stability and community complexity: a test using salmon and trout

Predation shortly after release is the main source of mortality among hatchery‐reared fish used to restore or enhance endangered salmonid populations. We found, that hatchery‐reared salmonid young originating from endangered stocks have weak innate responses to their natural fish predators. The ability to avoid predation in fish can be improved through social learning from experienced to naïve individuals. Huge benefits would be achieved, if social learning processes could be successfully applied on a large scale to enhance viability of hatchery fish prior to release into the wild. By using model predators together with chemical cues from real predators we tested if social learning could be used to train hatchery‐reared salmonid young to avoid fish predators. As there are clear differences in social behaviour among the salmonid species, we first examined whether these differences affect the probability and efficiency of learning anti‐predator skills from trained demonstrators. We compared anti‐predator responses of observers (fish trained by using experienced fish as demonstrators) with those of control fish, which had been 'trained' by untrained naïve conspecifics. We also examined how the efficiency of social learning depends on the ratio of experienced to naïve fish involved in social transmission trials. The results of these experiments will give guidelines how social learning could be utilized in developing hatchery scale training protocols.     

Fish cognition: what can we learn, and what do they need to learn?

Fish provide a wonderful opportunity to explore processes that shape and select cognitive ability. In this presentation, I will illustrate three aspects of work that my colleagues and I have used to investigate fish learning and memory over the last decade. First, I will discuss how comparing different populations sampled from contrasting habitats allows differences in cognitive ability to be related to the evolutionary ecology of the fish. I will use examples that have investigated how differences in learning ability between populations of the same species can arise. Here, the examples will be taken from the ubiquitous three‐spined stickleback, and a Panamanian poecilid, Brachyraphis .
The second approach has used fish cognition as a tool to quantify behaviour to enable assessment of different aspects of fish welfare. For example, the recent work investigating pain perception in trout required the use of a learning task to quantify how fish behaviour was modified after noxious stimulation. Ways in which these, and similar, processes can be used in future studies of fish welfare will be discussed.
The final part of the presentation will consider recent work that addresses the problems of releasing hatchery‐reared fish for restocking purposes. Although a common practice, most of the hatchery‐reared fish die shortly after they are released. Much of the observed mortality apparently stems from the fishes' inexperience with a variable environment. Experiments with juvenile cod and brown trout suggest that both age, and the early rearing environment, have profound effects on fish learning and behaviour. I will discuss how simple modifications to current rearing practices may have large beneficial effects on the post‐release survival of hatchery‐reared fish.     

Acquired Recognition of Chemical Stimuli from Pike,Esox lucius,by Brook Sticklebacks,Culaea inconstans (Osteichthyes,Gasterosteidae)

In this study we test whether brook sticklebacks (Culaea inconstans) can acquire predator recognition through releaser-induced recognition learning, i.e. simultaneous exposure to aversive ('releasing') stimuli and neutral stimuli causing learned aversion to the neutral stimuli. We exposed wild-caught pike-naive brook sticklebacks (collected from a creek containing fathead minnows, Pimephales promelas, but not pike, Esox lucius) to chemical stimuli from pike that were mixed with brook stickleback skin extract, fathead minnow skin extract, or a control of distilled water. In subsequent tests 2 d later, when only pike stimuli were presented, sticklebacks conditioned with stickleback skin extract and fathead minnow skin extract exhibited antipredator behaviour (i.e. increased schooling and movement toward the substrate), while those conditioned with distilled water did not. Sticklebacks conditioned with stickleback skin extract responded to pike with a more intense response, in terms of movement toward the substrate, than those conditioned with fathead minnow skin extract, suggesting that conspecific skin extract may be a stronger stimulus than heterospecific skin extract for learning recognition of predators. To our knowledge this is the first study to demonstrate that an acanthopterygian fish can acquire predator recognition through the pairing of conspecific alarm pheromone with the cue of a predator. Furthermore, our results are the first to demonstrate that fish can acquire predator recognition through the pairing of a heterospecific alarm pheromone with the cue of a predator. These results suggest that brook sticklebacks will benefit by being in close proximity to fathead minnows. Acquired predator recognition has long-term consequences in mediating predator-prey interactions.     

Ecological causes of morphological evolution in the three‐spined stickleback

The central assumption of evolutionary theory is that natural selection drives the adaptation of populations to local environmental conditions, resulting in the evolution of adaptive phenotypes. The three‐spined stickleback (Gasterosteus aculeatus) displays remarkable phenotypic variation, offering an unusually tractable model for understanding the ecological mechanisms underpinning adaptive evolutionary change. Using populations on North Uist, Scotland we investigated the role of predation pressure and calcium limitation on the adaptive evolution of stickleback morphology and behavior. Dissolved calcium was a significant predictor of plate and spine morph, while predator abundance was not. Stickleback latency to emerge from a refuge varied with morph, with populations with highly reduced plates and spines and high predation risk less bold. Our findings support strong directional selection in three‐spined stickleback evolution, driven by multiple selective agents.     

Sex differences in pectoral muscles but not in pectoral fins in the three‐spined stickleback Gasterosteus aculeatus

The pectoral muscle index ( I _PM)( I _PM = 100 M _PM M⁻¹, where M _PM and M are the pectoral muscle and body masses, respectively) fin‐area and fin ray length were studied over a year in male and female three‐spined stickleback Gasterosteus aculeatus from a marine population (Öresund, Sweden) kept under simulated natural light and temperature conditions. A castration‐replacement experiment was used to test androgen effects on the I _PM, fin‐area and fin ray length. Non‐breeding males were castrated or sham‐operated in winter ( i.e . the fish had low levels of androgens). Castrated control and sham‐operated fish were implanted with empty Silastic capsules and castrated groups with capsules containing the androgens testosterone or 11‐ketoandrostenedione into the abdominal cavity. The experiment was terminated after 41 days, when the controls had matured. No morphological differences were found in pectoral fins between sexes during the year, except during the peak breeding season (May), where females showed larger fin‐area and longer fin ray in length compared to males. No effects of androgens treatment or of castration on pectoral fin‐area or fin ray length was observed. Breeding and non‐breeding males showed higher I _PM compared to females. The lower I _PM in females than in males could not be explained by the larger gonads in the former alone, as a sex difference in I _PM was still present after deduction of the ovaries from the female body mass. The I _PM was higher in sham‐operated compared to castrated fish. No effects of androgens treatment on I _PM was observed.     

Do competing males cooperate? Familiarity and its effect on cooperation during predator inspection in male three‐spined sticklebacks (Gasterosteus aculeatus)

We investigated the trade‐off between conflict and cooperation, using predator inspection behaviour in sticklebacks as a model system. Male three‐spined sticklebacks ( Gasterosteus aculeatus ) compete for territories during the breeding season and it has been demonstrated that the level of aggression between territorial neighbours declines with time, a phenomenon known as the dear enemy effect. In this experiment we examine whether this increase in familiarity between territorial neighbours can facilitate an increase in cooperation during predator inspection events. This was analyzed using male sticklebacks from four pond populations, two with and two without predatory rainbow trout ( Oncorhyncus mykiss ). Males were each exposed to five different treatments: (1) the presentation of a live rainbow trout when alone; (2) with a newly revealed territorial neighbour; (3) with this neighbour after two days of familiarization; (4) with another unfamiliar neighbour (termed a 'floater'); and (5) a second solitary trial (to provide controls at the start and end of the experiment). As predicted, fish from predator‐sympatric populations showed higher levels of predator inspection and lower rates of misdirected territorial aggression towards the predator throughout. However, familiarity between neighbouring males did not facilitate an increase in predator inspection behaviour. Instead, predator inspection behaviour decreased throughout treatments involving the presence of any sort of neighbouring male. Familiarity between neighbours did not influence their ability to cooperatively inspect, but only the nature of any aggressive territorial behaviours, all of which detracted equally from individual inspection effort.     

The Influence of Structural Complexity on Fish–zooplankton Interactions: A Study Using Artificial Submerged Macrophytes

Aquatic macrophytes produce considerable structural variation within the littoral zone and as a result the vegetation provides refuge to prey communities by hindering predator foraging activities. The behavior of planktivorous fish Pseudorasbora parva (Cyprinidae) and their zooplankton prey Daphnia pulex were quantified in a series of laboratory experiments with artificial vegetation at densities of 0, 350, 700, 1400, 2100 and 2800 stemsm^–2. Swimming speeds and foraging rates of the fish were recorded at different prey densities for all stem densities. The foraging efficiency of P. parva decreased significantly with increasing habitat complexity. This decline in feeding efficiency was related to two factors: submerged vegetation impeded swimming behavior and obstructed sight while foraging. This study separated the effects of swimming speed variation and of visual impairment, both due to stems, that led to reduced prey–predator encounters and examined how the reduction of the visual field volume may be predicted using a random encounter model.     

The aberrant stickleback Gasterosteus aculeatus in the Karlskrona archipelago, SE Sweden

The aberrant stickleback in the Karlskrona archipelago is probably a completely new form within the three‐spined stickleback Gasterosteus aculeatus complex. Males of this type differ from sympatric, normal stickleback males by being smaller and by having less striking nuptial coloration. They also build nests in algae above the bottom, whereas normal stickleback males build their nest at the bottom. Moreover, observations suggest that aberrant stickleback males have emancipated from most of the care of nest and offspring as they appear to transport fertilized eggs from the nest to the surroundings where they are left unattended. Whether this can be explained by sex‐specific reproductive strategies or by any other means is investigated. Preliminary results suggest the aberrant stickleback to be genetically distinct from regular morphs. The project will investigate this further and hopefully clarify whether the aberrant type has evolved in the Karlskrona archipelago, thus probably in sympatry with normal sticklebacks, or if it is of allopatric origin. With reproductively important morphological and behavioural deviations, our first guess would be that isolation is mediated through sexual selection. If this is true, isolation may have been relatively rapid making a sympatric origin less unlikely. The aberrant form is very rare and endangered. Presently, it is only found at two sites, both of which are threatened by an impending ferry terminal construction. A major aim of the project is to help preserve the aberrant stickleback. Most importantly, aberrants will be collected for captive breeding and introduction to new localities.