Spectral composition and visual foraging in the three‐spined stickleback (Gasterosteidae: Gasterosteus aculeatus L.): elucidating the role of ultraviolet wavelengths

Visual signalling can be affected by both the intensity and spectral distribution of environmental light. In shallow aquatic habitats, the spectral range available for visually mediated behaviour, such as foraging, can reach from ultraviolet (UV) to long wavelengths in the human visible range. However, the relative importance of different wavebands in foraging behaviour is generally unknown. Here, we test how the spectral composition of ambient light influences the behaviour of three‐spined sticklebacks (Gasterosteus aculeatus) when foraging for live cladoceran Daphnia magna. Although paying particular attention to the UV waveband, we measured the foraging preferences of sticklebacks for prey presented under four different spectral conditions. These conditions selectively removed UV (UV–), short‐wave (SW–), mid‐wave (MW–) or long‐wave (LW–) light from the entire spectrum. The absence of UV and long wavelengths strongly reduced prey attractiveness for G. aculeatus compared with conditions without short‐wave and mid‐wave light. To control for potential light habitat preferences in the main experiment, we conducted a further choice experiment without prey stimuli. Fish in these trials did not discriminate significantly between the different spectral conditions. When comparing both experiments, it was observed that, although filter preferences for MW– and LW– conditions were virtually consistent, they differed at shorter wavelengths, with a reduced preference for UV– conditions and, at the same time, an increased preference for SW– conditions in the presence of prey. Thus, prey choice seems to be strongly affected by visual information at the short‐wave end of the spectrum. The foraging preferences were also mirrored by the chromatic contrast values between prey and the experimental background, as calculated for each lighting condition using a series of physiological models on stickleback perception. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 105 , 359–368.     

Use of water flow direction to provide spatial information in a small-scale orientation task

Experiments were designed to investigate whether three-spined sticklebacks Gasterosteus aculeatus can use direction of water flow as an orientation cue. The fish had to learn the location of a food patch in a channel where water flow direction was the only reliable indicator of the food patch position. Fish from two ponds and two rivers were trained and tested in the spatial task to determine whether river three-spined sticklebacks are more adept at using water flow as a spatial cue than fish from ponds. All fish were able to use water flow to locate the food patch but one of the two river groups was significantly faster at learning the patch location. When the task was reversed so that fish that had formerly been trained to swim downstream now had to learn to swim upstream and vice versa both river groups learned the reversed task faster than the two pond groups. In a second experiment, to investigate whether fish from ponds or rivers vary in the type of spatial cue that they prefer to use, fish from one pond and one river were given a choice between two different types of spatial cue: flow direction or visual landmarks. A test trial in which these two cues were put into conflict revealed that the river population showed a strong preference for flow direction whilst the pond population preferred to use visual landmarks.     

Do house mice use UV cues when foraging?

Research on the behavioural ecology of ultraviolet (UV-A, wavelengths of 320–400 nm, hereafter: UV) sensitivity in terrestrial vertebrates has mainly focused on sexual signalling and foraging in birds and reptiles, whereas the fact that some rodents are also sensitive to UV light has been somewhat ignored. Here, we present the results of two behavioural experiments, which tested whether rodents use UV cues in foraging. In the first experiment we asked whether the colour contrast in the UV waveband is used as a foraging cue. House mice were offered UV-reflecting and UV-absorbing artificial food items in two different illuminations where UV light was either present or absent. The food items were offered to two groups of mice, one group on a UV-reflecting and the other on a UV-absorbing background. The second experiment investigated more specifically whether UV cues are especially important in dawn and dusk when short wavelengths are high in the proportion of available light. House mice showed no preference between the food items regardless of illumination or background. Therefore, our results indicate that house mice do not use UV cues in foraging.     

Species difference in adaptive use of public information in sticklebacks

Animals foraging on variable food sources can refine their estimates of patch quality by monitoring the success of others (i.e. collect 'public information'). Here, we show that both three-spined sticklebacks (Gasterosteus aculeatus) and nine-spined sticklebacks (Pungitius pungitius) use past cues provided by others to locate food but only nine-spined sticklebacks use prior public information to assess patch quality, regardless of whether demonstrators were conspecifics or heterospecifics. Moreover, nine-spined but not three-spined sticklebacks preferentially hid in vegetation during the demonstration, a position from which they could observe both patches simultaneously and collect public information. We conclude that species differences in the use of public information can be explained by variations in habitat choice and response to predation. Our findings expand current understanding of the scope of public-information use in animals by showing that fishes can use public-information in a foraging context and from heterospecifics. The study suggests that public-information use is an adaptation that allows animals vulnerable to predation to acquire valuable foraging information at low risk.     

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.     

Route and landmark learning by rats searching for food

Many foraging animals rely on visual landmarks and/or habitual paths to locate important resources. We examined the degree to which rats rely on these cues when they predicted conflicting food locations. In this foraging task, rats were required to find food which could be located using either a fixed route or a nearby visual landmark. In tests, we found that their subsequent search-based estimates of the food location were the same when animals had acquired a long-term memory of the route, the landmark, or both. We show that the degree to which animals rely on the cues depends not only on the discrepancy between the two cues, but also on whether animals can match the testing “view” with a learned “view” that has been acquired during training.     

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.     

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.     

Ultraviolet light influences habitat preferences in a fish under predation risk

Environmental light conditions are of general importance in predator–prey interactions. In aquatic systems, prey individuals experience different levels of predation risk depending on the properties of the visual environment, such as structural complexity or water transparency. To reduce the threat of predation, prey should move to habitats providing better protection against visual predators. We studied the role of UV wavelengths in habitat choice behaviour under predation risk in a fish, the three-spined stickleback (Gasterosteus aculeatus) that uses UV signals in different contexts of intraspecific communication. In a laboratory experiment sticklebacks were exposed to a predatory threat and given the choice between two escape habitats, one providing full-spectrum conditions including UV light (UV+) and one without UV wavelengths (UV−). Fish from two rearing treatments were tested, one group had been raised under natural lighting conditions (UV+), the other group under UV-deficient lighting conditions (UV−). Sticklebacks from the UV+ group preferred the UV− habitat as a refuge which suggests that predator avoidance behaviour is UV-related in this species with UV− conditions presumably being advantageous for prey fish. However, individuals from the UV− treatment group were equally attracted to both presented light habitats. It is possible that these fish could not discriminate between the two light habitats due to physiological limitations caused by their rearing conditions. Further control trials with neutral-density filters revealed that the UV− habitat preference of UV+ fish in the main experiment was rather not influenced by a difference in achromatic brightness between the UV+ and UV− habitat.     

A review of competitive resource sharing under constraints in sticklebacks

The best strategy for an animal competing intraspecifically for food depends on its relative competitive ability, its needs, and on the strategies its competitors are using. Three different investigations using threespined sticklebacks, Gasterosteus aculeatus , as predators and Daphnia or Tubifex worms as prey are reviewed: (1) six sticklebacks differing in competitive ability compete for two food patches, of which one is twice as profitable as the other; (2) two sticklebacks differing in competitive ability compete in one patch for two types of prey, of which one is three times as profitable as the other; (3) parasitised and healthy sticklebacks have to decide alone, and in competition with each other, how close they dare approach on their own to a live predator waiting close to profitable food. The best strategy from the point of view of the stickleback is different from that of its parasite. The two parasite species studied, Schistocephalus solidus and Glugea anomala, ought to influence their host's behaviour in opposite directions.     

Captive cotton‐top tamarins' (Saguinus oedipus oedipus) use of landmarks to localize hidden food items

Seventeen captive cotton‐top tamarins (Saguinus oedipus oedipus) were individually tested on their use of spatial relationships between landmarks to locate multiple hidden food items. In two experiments, the tamarins were presented with a spatial‐foraging task in which positions of hidden food rewards were fixed in relation to an array of visual cues. In Experiment 1, the cues+hidden food configuration was rotated 90° and the tamarins were successful in locating the food items significantly above chance levels (P<0.01). In Experiment 2 the cues+hidden food configuration was translated (up, down or sideways) from the previously learned configuration, and the monkeys successfully localized the hidden food items (P<0.001). Results indicate that the tamarins relied on the spatial relationship between the multiple landmarks to locate hidden food items rather than on an associative or beacon strategy. The results of these experiments support the contention that when contextually appropriate these captive New World monkeys have the capacity to rely on the spatial relationship or positions of several cues as an array to localize points in their environment. Am. J. Primatol. 71:316–323, 2009. © 2009 Wiley‐Liss, Inc.     

Comparative Analysis of Japanese Three-Spined Stickleback Clades Reveals the Pacific Ocean Lineage Has Adapted to Freshwater Environments while the Japan Sea Has Not

Divergent selection and adaptive divergence can increase phenotypic diversification amongst populations and lineages. Yet adaptive divergence between different environments, habitats or niches does not occur in all lineages. For example, the colonization of freshwater environments by ancestral marine species has triggered adaptive radiation and phenotypic diversification in some taxa but not in others. Studying closely related lineages differing in their ability to diversify is an excellent means of understanding the factors promoting and constraining adaptive evolution. A well-known example of the evolution of increased phenotypic diversification following freshwater colonization is the three-spined stickleback. Two closely related stickleback lineages, the Pacific Ocean and the Japan Sea occur in Japan. However, Japanese freshwater stickleback populations are derived from the Pacific Ocean lineage only, suggesting the Japan Sea lineage is unable to colonize freshwater. Using stable isotope data and trophic morphology, we first show higher rates of phenotypic and ecological diversification between marine and freshwater populations within the Pacific Ocean lineage, confirming adaptive divergence has occurred between the two lineages and within the Pacific Ocean lineage but not in the Japan Sea lineage. We further identified consistent divergence in diet and foraging behaviour between marine forms from each lineage, confirming Pacific Ocean marine sticklebacks, from which all Japanese freshwater populations are derived, are better adapted to freshwater environments than Japan Sea sticklebacks. We suggest adaptive divergence between ancestral marine populations may have played a role in constraining phenotypic diversification and adaptive evolution in Japanese sticklebacks.     

Behavioural evidence for ultraviolet vision in a tetraonid species – foraging experiment with black grouse Tetrao tetrix

In addition to wavelengths visible to humans (400–700 nm), many birds are able to detect near ultraviolet light (320–400 nm). Most studies of ultraviolet (UV) vision in birds have concentrated on the importance of UV vision in intraspecific signalling, especially in passerine birds. However, birds may also use UV vision for other purposes, e.g. foraging. We performed a laboratory experiment to test whether a tetraonid species, black grouse Tetrao tetrix , could detect the difference between UV-reflecting and non-UV-reflecting food items (two colour morphs of bilberry Vaccinium myrtillus ). Black grouse preferred UV-reflecting berries when UV light was used for illumination, but showed no preference in the absence of UV light. This observation establishes a potential UV sensitivity in this species; such a sensitivity should be considered in behavioural experiments with this species.     

Influence of visual targets and landmarks on honey bee foraging and waggle dancing

Animals use diverse sensory stimuli to navigate their environment and to recognize rewarding food sources.Honey bees use visual atributes of the targeted food source,such as its color,shape,size,direction and distance from the hive,and the landmarks around it to navigate during foraging.They transmit the location information of the food source to other bees if it is highly rewarding.To investigate the relative importance of these attributes,we trained bees to feeders in two different experiments.In the first experiment,we asked whether bees prefer to land on(a)a similar feeder at a different distance on the same heading or on(b)a visually distinct feeder located at the exact same location.We found that,within a short foraging range,bees relied heavily on the color and the shape of the food source and to a lesser extent on its distance from the hive.In the second experiment,we asked if moving the main landmark or the feeder(visual target)influenced recruitment dancing for the feeder.We found that foragers took longer to land and danced fewer circuits when the location of the food source,or a major landmark associated with it,changed.These results demonstrate that prominent visual atributes of food sources and landmarks are evidently more reliable than distance information and that foraging bees heavily utilize these visual cues at the later stages of their journey.     

Competition avoidance drives individual differences in response to a changing food resource in sticklebacks

Within the same population, individuals often differ in how they respond to changes in their environment. A recent series of models predicts that competition in a heterogeneous environment might promote between‐individual variation in behavioural plasticity. We tested groups of sticklebacks in patchy foraging environments that differed in the level of competition. We also tested the same individuals across two different social groups and while alone to determine the social environment's influence on behavioural plasticity. In support of model predictions, individuals consistently differed in behavioural plasticity when the presence of conspecifics influenced the potential payoffs of a foraging opportunity. Whether individuals maintained their level of behavioural plasticity when placed in a new social group depended on the environmental heterogeneity. By explicitly testing predictions of recent theoretical models, we provide evidence for the types of ecological conditions under which we would expect, and not expect, variation in behavioural plasticity to be favoured.     

Small Variations in Early-Life Environment Can Affect Coping Behaviour in Response to Foraging Challenge in the Three-Spined Stickleback

Context

An increasing concern in the face of human expansion throughout natural habitats is whether animal populations can respond adaptively when confronted with challenges like environmental change and novelty. Behavioural flexibility is an important factor in estimating the adaptive potential of both individuals and populations, and predicting the degree to which they can cope with change.

Study Design

This study on the three-spined stickleback (Gasterosteus aculeatus) is an empiric illustration of the degree of behavioural variation that can emerge between semi-natural systems within only a single generation. Wild-caught adult sticklebacks (P, N = 400) were randomly distributed in equal densities over 20 standardized semi-natural environments (ponds), and one year later offspring (F1, N = 652) were presented with repeated behavioural assays. Individuals were challenged to reach a food source through a novel transparent obstacle, during which exploration, activity, foraging, sociability and wall-biting behaviours were recorded through video observation. We found that coping responses of individuals from the first generation to this unfamiliar foraging challenge were related to even relatively small, naturally diversified variation in developmental environment. All measured behaviours were correlated with each other. Especially exploration, sociability and wall-biting were found to differ significantly between ponds. These differences could not be explained by stickleback density or the turbidity of the water.

Findings

Our findings show that a) differences in early-life environment appear to affect stickleback feeding behaviour later in life; b) this is the case even when the environmental differences are only small, within natural parameters and diversified gradually; and c) effects are present despite semi-natural conditions that fluctuate during the year. Therefore, in behaviourally plastic animals like the stickleback, the adaptive response to human-induced habitat disturbance may occur rapidly (within one generation) and vary strongly based on the system’s (starting) conditions. This has important implications for the variability in animal behaviour, which may be much larger than expected from studying laboratory systems, as well as for the validity of predictions of population responses to change.     

Context-dependent visual preferences in starlings and blue tits: mate choice and light environment

There is considerable interest in the role that ultraviolet (UV) cues play in the foraging and mate choice decisions of birds. However, with the exception of the zebra finch, Taeniopygia guttata, it is not yet clear whether ultraviolet preferences are context specific, or whether birds show a general preference for full-avian-spectrum environments (320-700 nm) irrespective of the activity in which they are engaged. We investigated whether European starlings, Sturnus vulgaris, and blue tits, Parus caeruleus, show general (nonresource based) or context-specific preferences for full-spectrum environments. We found that neither species showed a general preference for UV-present (UV+) over UV-deficient (UV−) environments, when those environments contained no resources (experiment 1). Furthermore, neither species showed a UV+ preference when cages contained food, water and perches (starlings; experiment 2) or food, perches and heterospecifics (blue tits; Hunt et al. 1999. Animal Behaviour, 58, 809-815). However, both species did show highly significant preferences for UV+ conditions when viewing potential mates. Such experiments are necessary before one can conclude that particular wavebands have specific relevance to mate choice. In fact, our results suggest that the importance of particular wavelength compositions do indeed vary with behavioural context.     

UV matters in shoaling decisions

Shoaling behaviour in fish is influenced by numerous factors, such as familiarity, kinship, group size and shoal composition. Grouping decisions are based on both olfactory and visual cues. The visual system of many vertebrates is extended into the ultraviolet (UV) wave range as in three-spined sticklebacks (Gasterosteus aculeatus, L.). We investigated whether the presence or absence of UV wavelengths has an influence on shoaling behaviour in this species. Reproductively non-active three-spined sticklebacks were given the choice between two shoals, equal in numbers of individuals, which could be seen either through a UV-transmitting [UV(+)] or a UV-blocking [UV(-)] filter. Test fish preferred to join the shoal seen under UV(+) conditions. Due to differences in quantal flux between the UV(+) and UV(-) filters used, control experiments with neutral-density optical filters were performed in order to clarify the role of luminance. Here, test fish spent significantly more time near shoals that were seen in a darker environment, suggesting a potential trade-off between UV radiation and lower brightness during shoal choice.To our knowledge, these results demonstrate for the first time that shoaling decisions are influenced by UV wavelengths.     

Influence of lighting environment on social preferences in sticklebacks from two different photic habitats. II. Shoaling and mate preferences of lab-bred fishes

Different environmental conditions may lead to diverse morphological, behavioral, and physiological adaptations of different populations of the same species. Lighting conditions, for example, vary vastly especially between aquatic habitats, and have been shown to elicit adaptations. The availability of short-wave ultraviolet (UV) light is especially fluctuating, as UV wavelengths are attenuated strongly depending on water properties. The island of North Uist, Scotland, comprises 2 differential habitat types, tea-stained and clear-water lakes, varying considerably in UV transmission. In previous studies, wild-caught 3-spined stickleback Gasterosteus aculeatus populations (3 populations of each habitat type) were tested with respect to their shoaling and mate preferences for fish viewed under UV-present and UV-absent conditions. The results revealed a habitat-dependent preference of UV cues during shoal choice (tea-stained populations: preference for UV-absent condition in tea-stained water; clear-water populations: no preference in clear-water) but an overall preference for UV-present conditions during mate choice. To assess genetic influences on these behavioral patterns, similar experiments were conducted with lab-bred F1-generations of the same stickleback populations that were raised in a common environment (i.e. standardized clear-water conditions). Offspring of sticklebacks from tea-stained lakes tended to prefer shoals viewed under UV-absent conditions (only in tea-stained water), while sticklebacks from clear-water lakes showed a significant preference for the shoal viewed under UV-present conditions in clear-water but not in tea-stained water. Mate-preference experiments demonstrated that females from the tea-stained lakes significantly preferred and females from the clear-water lakes preferred by trend the male viewed under UV-present conditions in the clear-water treatment. The results for both shoaling- and mate-preference tests were largely similar for wild-caught and lab-bred sticklebacks, thus hinting at a genetic basis for the preference patterns.