Why birds eat colourful grit: colour preferences revealed by the colour of gizzard stones

Colour preferences from sexual or social contexts are assumed to have arisen owing to preferences for specific kinds of food, representing a sensory bias, but once colour preferences have evolved in a sexual context, they may also be expressed during foraging. We tested whether preferences for specific body colours (i.e. plumage and soft parts) were related to colour preferences for grit ingested by birds. Birds eat grit to facilitate break down of food by the gizzard, and this function is independent of the colour of grit, but depends on the physical properties of stones. Bird species were significantly consistent in colour of grit, and grit of different colours varied in prevalence among species, even when analyses were restricted to a sample from a single locality. There were positive correlations between presence of lilac and red grit in the gizzard and presence of sexually dichromatic lilac and red colour on the body. There was a positive correlation between red grit colour and red sexually monochromatic body colour. Bird species with many different sexual colours, but not sexually monochromatic colours on their body had many different colours of grit. Males had more lilac and red grit than females, with this effect differing among species, whereas that was not the case for grit of other colours. These findings are consistent with the sensory bias hypothesis that birds express preferences for grit of specific colours and a high diversity of colours related to sexual colouration of the body, even when the colour of such grit is only visible to the individual at the moment of ingestion.     

The modelling of avian visual perception predicts behavioural rejection responses to foreign egg colours

How do birds tell the colours of their own and foreign eggs apart? We demonstrate that perceptual modelling of avian visual discrimination can predict behavioural rejection responses to foreign eggs in the nest of wild birds. We use a photoreceptor noise-limited colour opponent model of visual perception to evaluate its accuracy as a predictor of behavioural rates of experimental egg discrimination in the song thrush Turdus philomelos. The visual modelling of experimental and natural eggshell colours suggests that photon capture from the ultraviolet and short wavelength-sensitive cones elicits egg rejection decisions in song thrushes, while inter-clutch variation of egg coloration provides sufficient contrasts for detecting conspecific parasitism in this species. Biologically realistic sensory models provide an important tool for relating variability of behavioural responses to perceived phenotypic variation.     

Most and Least Preferred Colours Differ According to Object Context: New Insights from an Unrestricted Colour Range

Humans like some colours and dislike others, but which particular colours and why remains to be understood. Empirical studies on colour preferences generally targeted most preferred colours, but rarely least preferred (disliked) colours. In addition, findings are often based on general colour preferences leaving open the question whether results generalise to specific objects. Here, 88 participants selected the colours they preferred most and least for three context conditions (general, interior walls, t-shirt) using a high-precision colour picker. Participants also indicated whether they associated their colour choice to a valenced object or concept. The chosen colours varied widely between individuals and contexts and so did the reasons for their choices. Consistent patterns also emerged, as most preferred colours in general were more chromatic, while for walls they were lighter and for t-shirts they were darker and less chromatic compared to least preferred colours. This meant that general colour preferences could not explain object specific colour preferences. Measures of the selection process further revealed that, compared to most preferred colours, least preferred colours were chosen more quickly and were less often linked to valenced objects or concepts. The high intra- and inter-individual variability in this and previous reports furthers our understanding that colour preferences are determined by subjective experiences and that most and least preferred colours are not processed equally.     

Colour preferences and colour vision in poultry chicks

The dramatic colours of biological communication signals raise questions about how animals perceive suprathreshold colour differences, and there are long-standing questions about colour preferences and colour categorization by non-human species. This study investigates preferences of foraging poultry chicks (Gallus gallus) as they peck at coloured objects. Work on colour recognition often deals with responses to monochromatic lights and how animals divide the spectrum. We used complementary colours, where the intermediate is grey, and related the chicks' choices to three models of the factors that may affect the attractiveness. Two models assume that attractiveness is determined by a metric based on the colour discrimination threshold either (i) by chromatic contrast against the background or (ii) relative to an internal standard. An alternative third model is that categorization is important. We tested newly hatched and 9-day-old chicks with four pairs of (avian) complementary colours, which were orange, blue, red and green for humans. Chromatic contrast was more relevant to newly hatched chicks than to 9-day-old birds, but in neither case could contrast alone account for preferences; especially for orange over blue. For older chicks, there is evidence for categorization of complementary colours, with a boundary at grey.     

Colour spaces in ecology and evolutionary biology

The recognition that animals sense the world in a different way than we do has unlocked important lines of research in ecology and evolutionary biology. In practice, the subjective study of natural stimuli has been permitted by perceptual spaces, which are graphical models of how stimuli are perceived by a given animal. Because colour vision is arguably the best‐known sensory modality in most animals, a diversity of colour spaces are now available to visual ecologists, ranging from generalist and basic models allowing rough but robust predictions on colour perception, to species‐specific, more complex models giving accurate but context‐dependent predictions. Selecting among these models is most often influenced by historical contingencies that have associated models to specific questions and organisms; however, these associations are not always optimal. The aim of this review is to provide visual ecologists with a critical perspective on how models of colour space are built, how well they perform and where their main limitations are with regard to their most frequent uses in ecology and evolutionary biology. We propose a classification of models based on their complexity, defined as whether and how they model the mechanisms of chromatic adaptation and receptor opponency, the nonlinear association between the stimulus and its perception, and whether or not models have been fitted to experimental data. Then, we review the effect of modelling these mechanisms on predictions of colour detection and discrimination, colour conspicuousness, colour diversity and diversification, and for comparing the perception of colour traits between distinct perceivers. While a few rules emerge (e.g. opponent log–linear models should be preferred when analysing very distinct colours), in general model parameters still have poorly known effects. Colour spaces have nonetheless permitted significant advances in ecology and evolutionary biology, and more progress is expected if ecologists compare results between models and perform behavioural experiments more routinely. Such an approach would further contribute to a better understanding of colour vision and its links to the behavioural ecology of animals. While visual ecology is essentially a transfer of knowledge from visual sciences to evolutionary ecology, we hope that the discipline will benefit both fields more evenly in the future.     

The taphonomy of colour in fossil insects and feathers

Colouration is an important multifunctional attribute of modern animals, but its evolutionary history is poorly resolved, in part because of our limited ability to recognize and interpret fossil evidence of colour. Recent studies on structural and pigmentary colours in fossil insects and feathers have illuminated important aspects of the anatomy, taphonomy, evolution and function of colour in these fossils. An understanding of the taphonomic factors that control the preservation of colour is key to assessing the fidelity with which original colours are preserved and can constrain interpretations of the visual appearance of fossil insects and theropods. Various analytical approaches can identify anatomical and chemical evidence of colour in fossils; experimental taphonomic studies inform on how colour alters during diagenesis. Preservation of colour is controlled by a suite of factors, the most important of which relate to the diagenetic history of the host sediment, that is, maximum burial temperatures and fluid flow, and subsurface weathering. Future studies focussing on key morphological and chemical aspects of colour preservation relating to cuticular pigments in insects and keratinous structures and nonmelanin pigments in feathers, for example, will resolve outstanding questions regarding the taphonomy of colour and will enhance our ability to infer original colouration and its functions in fossil insects and theropods.     

Bumblebees (Bombus terrestris) and honeybees (Apis mellifera) prefer similar colours of higher spectral purity over trained colours

Differences in the concentration of pigments as well as their composition and spatial arrangement cause intraspecific variation in the spectral signature of flowers. Known colour preferences and requirements for flower-constant foraging bees predict different responses to colour variability. In experimental settings, we simulated small variations of unicoloured petals and variations in the spatial arrangement of colours within tricoloured petals using artificial flowers and studied their impact on the colour choices of bumblebees and honeybees. Workers were trained to artificial flowers of a given colour and then given the simultaneous choice between three test colours: either the training colour, one colour of lower and one of higher spectral purity, or the training colour, one colour of lower and one of higher dominant wavelength; in all cases the perceptual contrast between the training colour and the additional test colours was similarly small. Bees preferred artificial test flowers which resembled the training colour with the exception that they preferred test colours with higher spectral purity over trained colours. Testing the behaviour of bees at artificial flowers displaying a centripetal or centrifugal arrangement of three equally sized colours with small differences in spectral purity, bees did not prefer any type of artificial flowers, but preferentially choose the most spectrally pure area for the first antenna contact at both types of artificial flowers. Our results indicate that innate preferences for flower colours of high spectral purity in pollinators might exert selective pressure on the evolution of flower colours.     

Looking like mother makes mallard ducklings dominant over their siblings

Colour variation in time and space among animals may affect social relationships such as pairing and dominance interactions. For instance, some birds are naturally sensitive to leg colour, with some colours being more visible or attractive than others. The colour of the leg-rings used to mark birds may thus be related to behavioural and reproductive variables. Most studies have investigated this effect for adults during reproduction, but leg-ring colour may also affect the behaviour of young birds. We tested the potential effect of leg-ring colours on the within-brood dominance hierarchy of mallard (Anas platyrhynchos) ducklings while each brood formed a stable and exclusive family unit with its mother. Ducklings did not acquire a within-brood dominance rank according to the colour of their own ring. This result suggests that mallards may not have a sensory bias for a given colouration. However, ducklings wearing a ring of the same colour as one of the two rings of their mother were dominant over their siblings. We discuss the potential behavioural and methodological implications of this result.     

Visual preference of flower-visiting crab spiders (Ebrechtella tricuspidata) for host flowers

1. Crab spiders (Thomisidae) are common flower-visiting spiders that ambush prey on inflorescences. As such, they require specific flowers or substrates for hunting, which are most often selected using sensory cues (e.g. vision). However, few studies have examined the visual preference of crab spiders for particular flowers. In this study, the visual preferences of the crab spider Ebrechtella tricuspidata for different inflorescence characteristics (e.g. colour and shape) were investigated. 2. The results showed that adult spiders explored all colours and shapes, whereas juvenile spiders displayed an overall preference for long (red) and short (purple) wavelength colours. Thus, differences in colour were not particularly important for E. tricuspidata with regard to visual attractiveness and selection. 3. However, inflorescence shape (e.g. tulip) was found to be a more desirable trait for selection, which was probably due to the provision of shelter. 4. These results also suggest that male preference for female spiders depended somewhat on the background colour (wavelength) of the flower on which the female was located.     

Innate and Learned Colour Preference in the Zebrafish, Danio rerio

Receiver biases towards specific sensory signals have been demonstrated in insects, birds and fish, both in the context of foraging and mate choice. In some cases, signals important in sexual selection appear to have evolved by exploiting a pre-existing bias in the sensory system. For instance, female preferences for male nuptial colouration may have arisen from selection on foraging practices. Using the zebrafish ( Danio rerio ), a species in which red is not a factor in mate choice, we tested for a foraging bias towards the colour red. We further investigated the plasticity of foraging biases by raising groups of fish on diets consisting solely of red, blue, green or white food. When we subsequently tested their colour preferences in a foraging context, each group responded most strongly to red, irrespective of the colour of food with which they had been conditioned. We also detected a significant effect of conditioning on colour preferences; fish responded more strongly to the colour that matched diet colour than to other colours. The observed receiver bias towards red may have evolved as an adaptive preference for carotenoid compounds in their diet. While the bias to red appears to be innate, our results indicate that learning is also important in shaping foraging biases.     

Colour association influences honey bee choice between sucrose concentrations

Certain colours associated with floral food resources are more quickly learned by honey bees (Apis mellifera) than are other colours. But the impact of colour, and other floral cues, on bee choice behaviour has not yet been determined. In these experiments, colour association and sugar concentration of reward were varied to assess how they interact to affect bee choice behaviour. Thirty-five bees were individually given binary choices between blue and yellow artificial flowers that contained either the same rewards or rewards of different sucrose concentrations. Honey bee choice between sucrose concentrations was affected by colour association and this effect was greatest when absolute difference between rewards was the lowest. The honey bee's ability to maximize energetic profitability during foraging is constrained by floral cue effectiveness.     

Colour processing in complex environments: insights from the visual system of bees

Colour vision enables animals to detect and discriminate differences in chromatic cues independent of brightness. How the bee visual system manages this task is of interest for understanding information processing in miniaturized systems, as well as the relationship between bee pollinators and flowering plants. Bees can quickly discriminate dissimilar colours, but can also slowly learn to discriminate very similar colours, raising the question as to how the visual system can support this, or whether it is simply a learning and memory operation. We discuss the detailed neuroanatomical layout of the brain, identify probable brain areas for colour processing, and suggest that there may be multiple systems in the bee brain that mediate either coarse or fine colour discrimination ability in a manner dependent upon individual experience. These multiple colour pathways have been identified along both functional and anatomical lines in the bee brain, providing us with some insights into how the brain may operate to support complex colour discrimination behaviours.     

Biological significance of distinguishing between similar colours in spectrally variable illumination: bumblebees (<Emphasis Type="Italic">Bombus terrestris</Emphasis>) as a case study

Individual bumblebees were trained to choose between rewarded target flowers and non-rewarded distractor flowers in a controlled illumination laboratory. Bees learnt to discriminate similar colours, but with smaller colour distances the frequency of errors increased. This indicates that pollen transfer might occur between flowers with similar colours, even if these colours are distinguishable. The effect of similar colours on reducing foraging accuracy of bees is evident for colour distances high above discrimination threshold, which explains previous field observations showing that bees do not exhibit complete flower constancy unless flower colour between species is distinct. Bees tested in spectrally different illumination conditions experienced a significant decrease in their ability to discriminate between similar colours. The extent to which this happens differs in different areas of colour space, which is consistent with a von Kries-type model of colour constancy. We find that it would be beneficial for plant species to have highly distinctive colour signals to overcome limitations on the bees performance in reliably judging differences between similar colours. An exception to this finding was flowers that varied in shape, in which case bees used this cue to compensate for inaccuracies of colour vision.     

Change in male coloration associated with artificial selection on foraging colour preference

Sensory drive proposes that natural selection on nonmating behaviours (e.g. foraging preferences) alters sensory system properties and results in a correlated effect on mating preferences and subsequently sexual traits. In colour‐based systems, we can test this by selecting on nonmating colour preferences and testing for responses in colour‐based female preferences and male sexual coloration. In guppies (Poecilia reticulata), individual functional links of sensory drive have been demonstrated providing an opportunity to test the process over more than one link. We measured male coloration and female preferences in populations previously artificially selected for colour‐based foraging behaviour towards two colours, red and blue. We found associated changes in male coloration in the expected direction as well as weak changes in female preferences. Our results can be explained by a correlated response in female preferences due to artificial selection on foraging preferences that are mediated by a shared sensory system or by other mechanisms such as colour avoidance, pleiotropy or social experiences. This is the first experimental evidence that selection on a nonmating behaviour can affect male coloration and, more weakly, female preferences.     

Geographic patterns in fruit colour diversity: do leaves constrain the colour of fleshy fruits?

We tested for geographic patterns in fruit colour diversity. Fruit colours are thought to promote detection by seed dispersers. Because seed dispersers differ in their spectral sensitivities, we predicted that fruit colour diversity would be higher in regions with higher seed disperser diversity (i.e. the tropics). We collected reflectance data on 232 fruiting plant species and their natural backgrounds in seven localities in Europe, North and South America, and analysed fruit colour diversity according to the visual system of birds—the primary consumer types of these fruits. We found no evidence that fruit colours are either more conspicuous or more diverse in tropical areas characterised by higher seed disperser diversity. Instead, fruit colour diversity was lowest in central Brazil, suggesting that fruit colours may be more diverse in temperate regions. Although we found little evidence for geographic variation in fruit hues, the spectral properties of fruits were positively associated with the spectral properties of backgrounds. This result implies that fruit colours may be influenced by selection on the reflectance properties of leaves, thus constraining the evolution of fruit colour. Overall, the results suggest that fruit colours in the tropics are neither more diverse nor more conspicuous than temperate fruits, and that fruit colours may be influenced by correlated selection on leaf reflectance properties. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Shell colour variation in Littorina saxatilis Olivi (Prosobranchia: Littorinidae): a multi-factor approach

The marine snail Littorina saxatilis is highly polymorphic for shell colour. It lives in the heterogeneous intertidal zone, where there are sharp transitions in a number of abiotic factors that may influence the relative fitness of morphs. We investigated the hypothesis of selected variation by relating the colour distribution to five factors (wave exposure, substratum, shore level, sex, snail age), and to interactions between them. We compared patterns from geographical areas in Sweden, Iceland and Russia. Cryptic morphs (tessellated and different dark colours) generally dominated (80–98%) while conspicuous morphs (white, yellow, red and banded) were less common (2–20%). The colour frequencies were often related to wave exposure, substratum and shore level. Frequencies rarely varied with age and never with sex. In order to test the assumption that the different colours are genetically determined we cross-bred snails from Iceland in the laboratory. Both the presence of bands and the ground colours of the shell were inherited, and we have tentative support for a one-locus two-allele model for banding. Our results support a model of selected inherited colour variation, involving a number of different selective agents, the importance of which may vary between populations on local and geographical scales.     

The Absolute Threshold of Colour Vision in the Horse

Arrhythmic mammals are active both during day and night if they are allowed. The arrhythmic horses are in possession of one of the largest terrestrial animal eyes and the purpose of this study is to reveal whether their eye is sensitive enough to see colours at night. During the day horses are known to have dichromatic colour vision. To disclose whether they can discriminate colours in dim light a behavioural dual choice experiment was performed. We started the training and testing at daylight intensities and the horses continued to choose correctly at a high frequency down to light intensities corresponding to moonlight. One Shetland pony mare, was able to discriminate colours at 0.08 cd/m², while a half blood gelding, still discriminated colours at 0.02 cd/m². For comparison, the colour vision limit for several human subjects tested in the very same experiment was also 0.02 cd/m². Hence, the threshold of colour vision for the horse that performed best was similar to that of the humans. The behavioural results are in line with calculations of the sensitivity of cone vision where the horse eye and human eye again are similar. The advantage of the large eye of the horse lies not in colour vision at night, but probably instead in achromatic tasks where presumably signal summation enhances sensitivity.     

Rethinking Colour Constancy

Colour constancy needs to be reconsidered in light of the limits imposed by metamer mismatching. Metamer mismatching refers to the fact that two objects reflecting metameric light under one illumination may reflect non-metameric light under a second; so two objects appearing as having the same colour under one illuminant can appear as having different colours under a second. Yet since Helmholtz, object colour has generally been believed to remain relatively constant. The deviations from colour constancy registered in experiments are usually thought to be small enough that they do not contradict the notion of colour constancy. However, it is important to determine how the deviations from colour constancy relate to the limits metamer mismatching imposes on constancy. Hence, we calculated metamer mismatching’s effect for the 20 Munsell papers and 8 pairs of illuminants employed in the colour constancy study by Logvinenko and Tokunaga and found it to be so extensive that the two notions—metamer mismatching and colour constancy—must be mutually exclusive. In particular, the notion of colour constancy leads to some paradoxical phenomena such as the possibility of 20 objects having the same colour under chromatic light dispersing into a hue circle of colours under neutral light. Thus, colour constancy refers to a phenomenon, which because of metamer mismatching, simply cannot exist. Moreover, it obscures the really important visual phenomenon; namely, the alteration of object colours induced by illumination change. We show that colour is not an independent, intrinsic attribute of an object, but rather an attribute of an object/light pair, and then define a concept of material colour in terms of equivalence classes of such object/light pairs. We suggest that studying the shift in material colour under a change in illuminant will be more fruitful than pursuing colour constancy’s false premise that colour is an intrinsic attribute of an object.     

Individual selection, kin selection, and the shifting balance in the evolution of warning colours: the evidence from butterflies

It is difficult to imagine how warning colours evolve in unpalatable prey. Firstly, novel warningly coloured variants gain no protection from their colours, since predators have not previously encountered and learnt their colour patterns. This leads to a frequency-dependent disadvantage of a rare variant within a species. Secondly, novel warningly coloured variants may be more conspicuous than non-aposematic prey.
Nevertheless, it is obvious that many palatable butterflies have bright colours used in intraspecific communication and in duping predators. Other palatable butterflies are already warningly coloured. Should such butterflies evolve unpalatability, perhaps because of a host-plant shift, these bright colours would be preadapted to a warning role. Warning colours could then continue to evolve by enhancement of memorable characteristics of these patterns, or by mimicry.
Even within lineages of warningly coloured, unpalatable butterflies, colour patterns have continued to evolve rapidly. This diversity of warning colour patterns could have evolved in a number of ways, including individual and kin selection, and by the shifting balance. Evidence for these mechanisms is discussed, as are the similarities between the evolution of warning colours and more general evolutionary processes, including sexual selection and speciation.     

Alternative use of chromatic and achromatic cues in a hawkmoth

The diurnal hummingbird hawkmoth Macroglossum stellatarum can learn the achromatic (intensity-related) and the chromatic (wavelength-related) aspect of a spectral colour. Free-flying moths learn to discriminate two colours differing in the chromatic aspect of colour fast and with high precision. In contrast, they learn the discrimination of two stimuli differing in the achromatic aspect more slowly and less reliably. When trained to use the chromatic aspect, they disregard the achromatic aspect, and when trained to use the achromatic aspect, they disregard the chromatic aspect, at least to some degree. In a conflicting situation, hummingbird hawkmoths clearly rely on the chromatic aspect of colour. Generally, the moths pay attention to the most reliable cue that allows them to discriminate colours in the learning situation. This is usually the chromatic aspect of the colour but they can learn to attend to the achromatic aspect instead. There is no evidence for relative colour learning, i.e. moths do not learn to choose the longer or shorter of two wavelengths, but it is possible that they learn to choose the darker or brighter shade of a colour, and thereby its relative intensities.