The effect of hunger and cestode parasitism on the shoaling decisions of small freshwater fish

Individual minnows Phoxinus phoxinus and three-spined sticklebacks Gasterosteus aculeatus were provided with a mutually exclusive choice between joining a shoal of conspecifics and foraging alone in a maze. The shoaling decisions and foraging behaviour of individual fish were studied when the fish were satiated and after 24- and 48-h periods of food deprivation. Hunger level was found to have a significant effect on shoaling behaviour. When satiated, fish of both species spent a greater proportion of time within one body length of the shoal and spent less time out of visual contact with the shoal than after periods of food deprivation. The effect of the cestode parasite Schistocephalus solidus on the shoaling behaviour of stickleback hosts was complex. When satiated, infected fish spent less time than uninfected fish within one body length of the shoal, preferring to remain outside the shoal, yet within visual contact, although when food deprived there was no difference in the proportion of time spent by infected and uninfected fish close to the shoal. The possible ecological significance of this change in behaviour is discussed with reference to the manipulation hypothesis of host-parasite interactions.     

Sticklebacks from streams are more bold than sticklebacks from ponds

Risk-taking behaviour has important consequences for fitness. Here, we show that risk-taking behaviour in sticklebacks consistently varies according to the habitat of origin. We compared the risk-taking behaviour of individual sticklebacks from three pond and three stream populations. Specifically, we measured willingness to forage under predation risk following a simulated attack by a model heron predator. Sticklebacks from stream populations were more willing to forage under predation risk than fish from pond populations. Sticklebacks from streams resumed eating after the simulated attack faster and spent more time eating compared to sticklebacks from ponds. We discuss these findings in terms of differences in life history and predation pressure in the two habitat types.     

Experience of natural prey and feeding efficiency in three-spined sticklebacks (Gasterosteus aculeatus L.)

The possibility that efficiency of feeding on different prey in three-spined sticklebacks ( Gasterosteus aculeatus L.) increases by experience of such items was investigated experimentally by comparing sticklebacks reared with only non-moving prey (frozen brine shrimps) with sticklebacks caught in the wild from localities where a wide range of prey species was available. Fish without experience of natural food scored less well than those from the wild on various components of foraging and so had reduced feeding efficiency. However, feeding efficiency in naive fish improved after just a few days of experience with natural prey. Such experience-induced changes in foraging efficiency will alter the profitability of prey items for individual fish.     

Behavioural and heart rate responses to food limitation and predation risk: an experimental study on rainbow trout

Food-restricted rainbow trout Oncorhynchus mykiss maintained a lower basal heart rate than satiated fish, probably as a result of reduced metabolic rate. Food-restricted fish were also more active during feeding and were more willing to take risks than satiated fish. Both satiated and food-restricted fish were positioned lower in the tank after the predator attack. Heart rate increased more during feeding in the food-restricted fish compared to the satiated, but energy status had no general effect on the relation between heart rate and behaviour. Hence, the increase in heart rate was mainly a response to the more active foraging behaviour in the food-restricted fish. Moreover, behavioural activity in the food-restricted fish was associated with a higher heart rate after the predator attack than when the fish was undisturbed, which may reflect physiological preparation for flight. These findings suggest that behavioural and cardiac responses are coadapted to meet variation in food availability and predation risk in the wild.     

Group Choice as a Function of Group Size Differences and Assessment Time in Fish: The Influence of Species Vulnerability to Predation

The shoal-choice behaviour of two species of fish that differ in their vulnerability to predation was compared. Individuals of threespine stickleback, Gasterosteus aculeatus, and creek chub, Semotilus atromaculatus, were presented with a simultaneous choice of two equidistant stimulus shoals of conspecifics that differed in membership size (5 vs. 6 fish, 5 vs. 7, 5 vs. 8, 5 vs. 9 and 5 vs. 10). Test fish were allowed to view the stimulus shoals from a standard distance for either 10–20 or 120–150s before being frightened with a stimulus from an overhead light and released to join either shoal. We observed which shoal (the smaller or the larger one) the test fish approached. Preference for the larger stimulus shoal generally increased with increasing shoal size difference and with the duration of the assessment period, and was more pronounced in chub (the more vulnerable of the two species). For the short assessment period, chub showed a significantly stronger preference for the larger stimulus shoal than sticklebacks, whereas there was no significant difference between species for the long assessment period. Furthermore, chub responded more readily to small differences in shoal size (of 1–3 fish) than sticklebacks, for both short and long assessment periods. The above results are consistent with the hypothesis that chub, as the more vulnerable of the two species (in terms of predation), should be able to identify the larger of two shoals more quickly and should be more sensitive to small differences in shoal size than sticklebacks.     

A comparison of the behavioural responses of parasitized and non-parasitized three-spined sticklebacks, Gasterosteus aculeatus L., to progressive hypoxia

Eighty sticklebacks (32 parasitized, 48 uninfected) were subjected to a serial reduction in dissolved oxygen (DO) concentration until they showed continuous aquatic surface respiration for longer than 10s (> 10s ASR). An analysis of results showed that (1) parasitized adult male and female sticklebacks reacted to low DO significantly earlier than non-parasitized controls; (2) severity of parasite infection was significantly correlated with DO at which > 10s ASR occurred; (3) gravid, non-parasitized females show ASR at a relatively high DO, with a threshold response similar to that of parasitized fish.
It is suggested that the metabolic respiratory demand of the parasitic tapeworm larvae causes the stickleback to modify its behaviour at lowered DO. This behavioural modification causes the fish to surface, where they are likely to be at risk from predatory birds. Field data on DO levels at the study site show that environmental conditions in the shallow lake margins approach the range required to affect the behaviour of heavily parasitized sticklebacks.     

Effect of cycles of feed deprivation on growth and food consumption of immature three-spined sticklebacks and European minnows

Individual juvenile three-spined sticklebacks Gasterosteus aculeatus and European minnow Phoxinus phoxinus , from sympatric populations, were subjected to four cycles of 1 week of food deprivation and 2 weeks of ad libitum feeding. Mean specific growth rate during the weeks of deprivation was negative and did not differ between species. The three-spined stickleback showed sufficient growth compensation to recover to the growth trajectory shown by control fish daily fed ad libitum . The compensation was generated by hyperphagia during the re-feeding periods, and in the last two periods of re-feeding, the gross growth efficiencies of deprived three-spined sticklebacks were greater than in control fish. The expression of the compensatory changes in growth and food consumption became clearer over the successive periods of re-feeding. The European minnow developed only a weak compensatory growth response and the mass trajectory of the deprived fish deviated more and more from the control trajectory. During re-feeding periods, there were no significant differences in food consumption or gross growth efficiency between control and deprived European minnows. The differences between the two species are discussed in terms of the possible costs of compensatory growth, the control of growth and differences in feeding biology.     

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.     

Effects of Schistocephalus solidus infection on brain monoaminergic activity in female three-spined sticklebacks Gasterosteus aculeatus.

The three-spined stickleback Gasterosteus aculeatus is an intermediate host of the tapeworm Schistocephalus solidus. Changes in predator avoidance, foraging and shoaling behaviour have been reported in sticklebacks infested with S. solidus, but the mechanisms underlying parasite-induced behavioural changes are not understood. Monoamine neurotransmitters are involved in the control of behaviour and central monoaminergic systems are sensitive to various stressors. Thus, the behavioural effects of S. solidus infestation might be a reflection of changes in brain monoaminergic activity in the stickleback host. The concentrations of 5-hydroxytryptamine (5-HT), dopamine (DA), norepinephrine (NE) and their metabolites 5-hydroxy-indoleacetic acid (5-HIAA), homovanilic acid (HVA) and 3-methoxy-4-hydroxyphenylglycol (MHPG) were measured in the telencephalons, hypothalami and brainstems of parasitized and non-parasitized female sticklebacks held in the laboratory. The ratios of 5-HIAA:5-HT were significantly elevated in both the hypothalami and brainstems of infected sticklebacks. The concentrations of 5-HT and NE were significantly reduced in the telencephalons of infected fish as compared with controls, but there was no elevation of metabolite concentrations. The results are consistent with chronic stress in infected fish, but may also reflect other alterations of neuroendocrine status resulting from parasite infection.     

Interference affects food-finding rate in schooling sticklebacks

Experiments on sticklebacks seeking for food patches show that foraging in schools enhances food-finding rate of individuals. A stochastic information-sharing model characterizes food-seeking behaviour in which food-finding by one in a school of fish results in food-sharing by many. The model predicts the food-finding rate of a randomly selected individual in a school of n fish to be that of a solitary forager weighted by the inverse of the school size, 1/n. In sticklebacks this seems not to be the case, however. Though the food-finding rate of individuals in the school reduces with n , the improvement is much slower than predicted by the basic model. We argue that a variant of the information-sharing model accounting for interference among individuals affecting their food-seeking behaviour fits the data better.     

Fuel, fasting, fear: routine metabolic rate and food deprivation exert synergistic effects on risk-taking in individual juvenile European sea bass

1. Individuals of the same species often exhibit consistent differences in metabolic rate, but the effects of such differences on ecologically important behaviours remain largely unknown. In particular, it is unclear whether there is a cause-and-effect relationship between metabolic rate and the tendency to take risks while foraging. Individuals with higher metabolic rates may need to take greater risks while foraging to obtain the additional food required to satisfy their energy requirements. Such a relationship could be exacerbated by food deprivation if a higher metabolic demand also causes greater mass loss and hunger. 2. We investigated relationships among metabolic rate, risk-taking and tolerance of food deprivation in juvenile European sea bass. Individual fish were tested for risk-taking behaviours following a simulated predator attack, both before and after a 7-day period of food deprivation. The results were then related to their routine metabolic rate (RMR), which was measured throughout the period of food deprivation. 3. The amount of risk displayed by individual fish before food deprivation showed no relationship with RMR. After food deprivation, however, the amount of risk among individuals was positively correlated with RMR. In general, most fish showed an increase in risk-taking after food deprivation, and the magnitude of the increase in risk-taking was correlated with the rate of individual mass loss during food deprivation, which was itself strongly correlated with RMR. 4. The observation that RMR was related to risk-taking behaviour after food deprivation, but not before, suggests that although RMR can influence risk-taking, the strength of the relationship is flexible and context dependent. The effects of RMR on risk-taking may be subtle or non-existent in regularly feeding animals, but may lead to variability in risk-taking among individuals when food is scarce or supply is unpredictable. This synergistic relationship between RMR and food deprivation could lead to an increased likelihood of being predated for individuals with a relatively high intrinsic energy demand during times when food is scarce.     

Coevolution of foraging behavior with intrinsic growth rate: risk-taking in naturally and artificially selected growth genotypes of <Emphasis Type="Italic">Menidia menidia</Emphasis>

Although there is accumulating evidence of growth-rate optimization by natural selection, the coevolution of growth rate and risk-taking behavior has not been sufficiently documented. The Atlantic silverside fish, Menidia menidia, displays countergradient variation in growth across a latitudinal gradient: genotypes from Nova Scotia (NS), for example, grow in length twofold faster than those from South Carolina (SC). Past work has established that fast growth is adaptive in northern climates, but the trade-off is poorer swimming performance and higher susceptibility to predators. We compared escape behavior and willingness to forage under threat of predation among growth genotypes reared and tested under common-garden conditions. When chased with a predator model, NS fish occupied shelter more quickly than SC fish. When food was supplied after a chase, NS fish reemerged from the shelter much more quickly than SC fish and immediately commenced feeding, whereas many SC fish displayed timid behavior and did not feed. When food was absent following a chase, however, NS fish remained in the shelter longer than did SC fish and both displayed timid behavior. Hence, the fast-growing NS genotype was bolder than SC fish in the presence of food, but shyer in the absence of food. These behaviors are adaptive given the physiological constraints intrinsic to each genotype. Experiments on captive populations of silversides that had been artificially selected for fast or slow growth confirmed that foraging behavior is genetically correlated with intrinsic growth rate, although in these trials the fast-growth genotype was always more bold, regardless of food availability, as would be expected in the absence of predators. We conclude that risk-taking foraging behavior coevolves adaptively with intrinsic growth rate in M. menidia.     

Shoaling behaviour of sticklebacks infected with the microsporidian parasite, <Emphasis Type="Italic">Glugea anomala</Emphasis>

We compared the shoaling behaviour of three-spined sticklebacks, Gasterosteus aculeatus, infected with the microsporidian, Glugea anomala, to that of non-infected conspecifics. Infected fish lost significantly more weight than non-infected fish during a period of food deprivation, suggesting a metabolic cost to parasitism. In binary shoal choice tests, non-infected test fish showed an association preference for a shoal of non-infected over a shoal of infected conspecifics; infected test fish displayed no preference. Infected fish, however, showed a higher overall tendency to shoal than non-parasitised fish. Furthermore, infected fish occupied front positions within a mixed school. We consider the behavioural differences between infected and uninfected fish in the context of their potential benefits to the fish hosts and the parasites.     

Pattern of hyperphagia in immature three-spined sticklebacks after short-term food deprivation

Juvenile three-spined sticklebacks Gasterosteus aculeatus were fed live enchytraeid worms, and mean daily ad libitum consumption in the absence of periods of deprivation was 11·7% of initial body weight. Then, six groups of five replicate fish were subjected to 1, 3 and 6 days without food. Each period of deprivation was followed by 1 day of ad libitum feeding. The sequential order of deprivations differed between groups. Over the sequence of deprivations and re-feedings, mean cumulative consumption did not differ between groups. Mean daily consumption was 19·8% of initial body weight after a 1-day deprivation, 22·3% after 3 days and 19·5% after 6 days. However, consumption in the 24 h after a given length of deprivation also depended on the prior history of deprivation. Specific growth rate over the experiment did not differ between groups. The results provide evidence for an effective regulation of appetite in growing sticklebacks.     

Short-term cues used by foraging trout in a California stream

Stream salmonids choose foraging locations to maximize the energy benefit of foraging within the constraints of size-mediated dominance hierarchies and predation risk. But, because stream habitats are temporally variable, fish must use a search process to monitor changing habitat conditions as a means of locating potentially-better foraging locations. I explored the cues used by the cutthroat trout, Oncorhynchus clarki clarki, when searching for food at the pool scale by artificially increasing prey availability at different locations by using special feeders and by manipulating pool velocities. Behavior of individually marked fish was monitored from stream bank platforms under unmanipulated control conditions and under seven experimental sets of conditions involving different combinations of feeder location and velocity manipulation. Under natural conditions fish elected to forage in the deepest (>50 cm), fastest (0.10–0.25 m s⁻¹) locations and within 1 m of structure cover, but would readily move to shallower (<30 cm) water away from cover if velocities were manipulated to be highest there. Although fish did not locate feeders unless they were placed in high-velocity areas, when high velocity was provided fish would move into very shallow water (<20 cm) if prey were delivered there. Responses of individual trout to manipulations indicated that water velocity was the main physical cue used by fish to decide where to forage, and that fish could also learn about new food sources by observing conspecifics. Overall, results indicated fish were not “perfect searchers” that could quickly locate new food resources over short time scales, even when the new resources were within a few meters of the fish’s normal foraging location. When given the correct cues, however, fish could detect new food sources and defend them against subordinate fish. Movement of new fish into and out of the study pools during the ten-day observation period was common, consistent with the idea that trout used movement as a means of exploring and learning about habitat conditions at the reach scale.     

The Importance of Egg Size and Social Effects for Behaviour of Arctic Charr Juveniles

Early behaviour can determine food intake and growth rate with important consequences for life history and survival in fishes. Egg size is known to affect growth rate of young Arctic charr but its influence on the development of behaviour is poorly documented. It is believed that egg size influence on growth and potentially on the behaviour of young fish decreases over time, minimized by the effects of social factors. Shortly after first feeding, we examined differences in mobility and foraging of Arctic charr in relation to egg size and social environment. The behaviour of juveniles from small and large eggs was compared five times over the course of development and in three different experimental settings: long‐term isolation (isolation before hatching), short‐term isolation vs. group rearing and mixed size group vs. homogeneous size groups. Egg size affected foraging behaviour and mobility of fish: fish coming from large eggs were more mobile and foraged more than fish coming from small eggs. Social environment affected foraging behaviour, mobility and space use: fish in a group were more mobile, foraged more and responded faster to food delivery than isolated fish. The interaction of egg size and social effects was seen primarily in foraging activities but did not affect mobility or space use. Large fish in groups foraged more than the three other groups: large fish in isolation, small fish in groups and small fish in isolation. Agonistic behaviour was rarely observed and there was no significant effect of group composition on agonistic behaviour. We discuss the importance of egg size and social effects at early stages of development with a focus on the evolutionary ecology of Arctic charr.     

Foraging Rules for Group Feeders: Area Copying Depends upon Food Density in Shoaling Goldfish

The decision rules governing forage area copying behaviour were investigated in shoaling fish. Shoaling goldfish were offered two equal food patches, one of which was adjacent to an equal-sized shoal feeding behind a transparent barrier. When food was low, goldfish foraged according to an area copying rule, but under high and zero food area copying disappeared. Only under high food density did equal numbers of fish feed at both sites as predicted by foraging theory. Under zero food the fish were less certain about where to forage. Precise visual cues from feeding fish were required: non-feeders did not attract area copiers. Furthermore, area copying was task-dependent since it reappeared strongly if fish were not able to forage on patches like their fellows. Control experiments eliminated an increase in group size for anti-predator advantage as an explanation. Two sequential decisions: to stay or move, and to join or leave may explain the results, which are not accommodated by simple optimality models. These decisions may be based on a comparison of current food intake with the anticipation of a higher reward by foraging socially.     

Increased Noise Levels Have Different Impacts on the Anti-Predator Behaviour of Two Sympatric Fish Species

Animals must avoid predation to survive and reproduce, and there is increasing evidence that man-made (anthropogenic) factors can influence predator−prey relationships. Anthropogenic noise has been shown to have a variety of effects on many species, but work investigating the impact on anti-predator behaviour is rare. In this laboratory study, we examined how additional noise (playback of field recordings of a ship passing through a harbour), compared with control conditions (playback of recordings from the same harbours without ship noise), affected responses to a visual predatory stimulus. We compared the anti-predator behaviour of two sympatric fish species, the three-spined stickleback (Gasterosteus aculeatus) and the European minnow (Phoxinus phoxinus), which share similar feeding and predator ecologies, but differ in their body armour. Effects of additional-noise playbacks differed between species: sticklebacks responded significantly more quickly to the visual predatory stimulus during additional-noise playbacks than during control conditions, while minnows exhibited no significant change in their response latency. Our results suggest that elevated noise levels have the potential to affect anti-predator behaviour of different species in different ways. Future field-based experiments are needed to confirm whether this effect and the interspecific difference exist in relation to real-world noise sources, and to determine survival and population consequences.     

Foraging behaviour in Drosophila larvae: mushroom body ablation

Drosophila larvae and adults exhibit a naturally occurring genetically based behavioural polymorphism in locomotor activity while foraging. Larvae of the rover morph exhibit longer foraging trails than sitters and forage between food patches, while sitters have shorter foraging trails and forage within patches. This behaviour is influenced by levels of cGMP-dependent protein kinase (PGK) encoded by the foraging (for) gene. Rover larvae have higher expression levels and higher PGK activities than do sitters. Here we discuss the importance of the for gene for studies of the mechanistic and evolutionary significance of individual differences in behaviour. We also show how structure-function analysis can be used to investigate a role for mushroom bodies in larval behaviour both in the presence and in the absence of food. Hydroxyurea fed to newly hatched larvae prevents the development of all post-embryonically derived mushroom body (MB) neuropil. This method was used to ablate MBs in rover and sitter genetic variants of foraging to test whether these structures mediate expression of the foraging behavioural polymorphism. We found that locomotor activity levels during foraging of both the rover and sitter larval morphs were not significantly influenced by MB ablation. Alternative hypotheses that may explain how variation in foraging behaviour is generated are discussed.     

Reduction of predation risk under the cover of darkness: Avoidance responses of mayfly larvae to a benthic fish

Summary Mayfly larvae of Paraleptophlebia heteronea (McDunnough) had two antipredator responses to a nocturnal fish predator (Rhinichthys cataractae (Valenciennes)): flight into the drift and retreat into interstitial crevices. Drift rates of Paraleptophlebia abruptly increased by 30 fold when fish were actively foraging in the laboratory streams but, even before fish were removed, drift began returning to control levels because larvae settled to the substrate and moved to areas of low risk beneath stones. This drifting response was used as an immediate escape behavior which likely decreases risk of capture from predators which forage actively at night. Surprisingly, drift most often occurred before contact between predator and prey, and we suggest that in darkness this mayfly may use hydrodynamic pressure waves for predator detection, rather than chemical cues, since fish forage in an upstream direction. Although drifting may represent a cost to mayfly larvae in terms of relocation to a new foraging area with unknown food resources, the immediate mortality risk probably out-weighs the importance of staying within a profitable food patch because larvae can survive starvation for at least 2 d. In addition to drifting, mayflies retreated from upper, exposed substrate surfaces to concealed interstitial crevices immediately after a predator encounter, or subsequent to resettlement on the substrate after predator-induced drift. A latency period was associated with this response and mayflies remained in these concealed locations for at least 3 h after dace foraging ceased. Because this mayfly feeds at night and food levels are significantly lower in field refugia under stones, relative to exposed stone surfaces, predator avoidance activity may limit foraging time and, ultimately, reduce the food intake of this stream mayfly.