Pattern contrast influences wariness in naïve predators towards aposematic patterns.

An apparent and common feature of aposematic patterns is that they contain a high level of achromatic (luminance) contrast, for example, many warning signals combine black spots and stripes with a lighter colour such as yellow. However, the potential importance of achromatic contrast, as distinct from colour contrast, in reducing predation has been largely overlooked. Here, using domestic chicks as a model predator, we manipulated the degree of achromatic contrast in warning patterns to test if high luminance contrast in aposematic signals is important for deterring naïve predators. We found that the chicks were less likely to approach and eat prey with high contrast compared to low contrast patterns. These findings suggest that aposematic prey patterns with a high luminance contrast can benefit from increased survival through eliciting unlearned biases in naïve avian predators. Our work also highlights the importance of considering luminance contrast in future work investigating why aposematic patterns take the particular forms that they do.

Underwater caustics disrupt prey detection by a reef fish.

Natural habitats contain dynamic elements, such as varying local illumination. Can such features mitigate the salience of organism movement? Dynamic illumination is particularly prevalent in coral reefs, where patterns known as 'water caustics' play chaotically in the shallows. In behavioural experiments with a wild-caught reef fish, the Picasso triggerfish (Rhinecanthus aculeatus), we demonstrate that the presence of dynamic water caustics negatively affects the detection of moving prey items, as measured by attack latency, relative to static water caustic controls. Manipulating two further features of water caustics (sharpness and scale) implies that the masking effect should be most effective in shallow water: scenes with fine scale and sharp water caustics induce the longest attack latencies. Due to the direct impact upon foraging efficiency, we expect the presence of dynamic water caustics to influence decisions about habitat choice and foraging by wild prey and predators.

Optimizing colour for camouflage and visibility using deep learning: the effects of the environment and the observer's visual system.

Avoiding detection can provide significant survival advantages for prey, predators, or the military; conversely, maximizing visibility would be useful for signalling. One simple determinant of detectability is an animal's colour relative to its environment. But identifying the optimal colour to minimize (or maximize) detectability in a given natural environment is complex, partly because of the nature of the perceptual space. Here for the first time, using image processing techniques to embed targets into realistic environments together with psychophysics to estimate detectability and deep neural networks to interpolate between sampled colours, we propose a method to identify the optimal colour that either minimizes or maximizes visibility. We apply our approach in two natural environments (temperate forest and semi-arid desert) and show how a comparatively small number of samples can be used to predict robustly the most and least effective colours for camouflage. To illustrate how our approach can be generalized to other non-human visual systems, we also identify the optimum colours for concealment and visibility when viewed by simulated red-green colour-blind dichromats, typical for non-human mammals. Contrasting the results from these visual systems sheds light on why some predators seem, at least to humans, to have colouring that would appear detrimental to ambush hunting. We found that for simulated dichromatic observers, colour strongly affected detection time for both environments. In contrast, trichromatic observers were more effective at breaking camouflage.

How is sexual conflict over parental care resolved? A meta-analysis.

Biparental care of offspring is both a form of cooperation and a source of conflict. Parents face a trade-off between current and future reproduction: caring less for the current brood allows individuals to maintain energy reserves and increase their chances of remating. How can selection maintain biparental care, given this temptation to defect? The answer lies in how parents respond to changes in each other's effort. Game-theoretical models predict that biparental care is evolutionarily stable when reduced care by one parent leads its partner to increase care, but not so much that it completely compensates for the lost input. Experiments designed to reveal responses to reduced partner effort have mainly focused on birds. We present a meta-analysis of 54 such studies, and conclude that the mean response was indeed partial compensation. Males and females responded differently and this was in part mediated by the type of manipulation used.

The influence of flicker rate on plasma corticosterone levels of European starlings, Sturnus vulgaris.

Recent reviews have highlighted the differences between human and avian vision with regard to temporal resolution and the potential problems it may cause for avian welfare and video playback experiments. Birds tend to have much higher critical fusion frequencies than do humans (>100 Hz vs 50-60 Hz in humans), which means that they perceive light as flickering up to and over 100 Hz. This is higher than most television monitors (which have refresh rates of 50 or 60 Hz) and normal fluorescent lighting (100 or 120 Hz), and because humans find flickering light aversive, it has been suggested that birds will as well. If this were the case, then there would be welfare implications of maintaining them under such lighting and also a potential effect on their behavioral responses in video playback experiments. However, there is some behavioral evidence that indicates that birds do not appear to find flicker aversive and may even prefer flickering lighting. The authors aimed to determine whether a passerine, the European starling, found flicker aversive by measuring the corticosterone stress response in birds maintained under high- or low-frequency fluorescent lighting (35-40 kHz vs 100 Hz) for 1 or 24 h. The results suggest that low-frequency lighting is potentially more stressful because, where differences exist, birds in the low-frequency treatment always showed higher basal corticosterone. However, the evidence is not consistent because in half of the blocks, there were no significant treatment effects and, where there were, the time course of the effects was variable.

Ultraviolet vision, fluorescence and mate choice in a parrot, the budgerigar Melopsittacus undulatus.

As in many parrots, the plumage of the budgerigar Melopsittacus undulatus reflects near-ultraviolet (UVA) wavelengths (300-400 nm) and exhibits UVA-induced fluorescence. However, there have, to our knowledge, been no tests of whether the yellow fluorescence observed under intense UVA illumination has any role in signalling. Four experiments were carried out on wild-type budgerigars, where the presence and absence of UV reflectance and fluorescence were manipulated using filters. Few studies have attempted to separate the contribution of UV reflectance to plumage hue as opposed to brightness or distinguish between a role in sexual as opposed to social preferences. However, our first experiments show that not only do females consistently prefer UV-reflecting males, but also that the observed preferences are due to removal of UV affecting the perceived hue rather than brightness. Furthermore, we found no effect of the light environment on male response to females, suggesting that the female preferences relate to plumage colour per se. Whilst UV reflectance appears important in heterosexual choice by females, it has no detectable influence on same-sex association preferences. The results from the second series of experiments suggest that enhancement of the budgerigar's yellow coloration through fluorescence has no effect on male attractiveness. However, the fluorescent plumage may play a role in signalling by virtue of the fact that it absorbs UVA and so increases contrast with nearby UV-reflecting plumage. Our study provides convincing evidence that UV reflectances can play a role in mate choice in non-passerines, but no evidence that the yellow fluorescence observed under UVA illumination is itself important as a signal.

Is the ultraviolet waveband a special communication channel in avian mate choice?

There is growing evidence that ultraviolet (UV) wavelengths play an important role in avian mate choice. One of the first experiments to support this idea showed that female zebra finches (Taeniopygia guttata) prefer UV-reflecting males to males whose ultraviolet reflection has been removed. The effect was very strong despite little or no UV reflection from several plumage areas. However, it is not clear how the importance of the UV waveband compares to other regions of the bird-visible spectrum. We tested whether the response of female zebra finches to the removal of male UV reflection is greater than to the removal of other wavebands. We presented females with a choice of males whose appearance was manipulated using coloured filters. The filters removed single blocks of the avian visible spectrum corresponding closely to the spectral sensitivities of each of the zebra finch's single cone classes. This resulted in males that effectively had no UV (UV-), no short-wave (SW-), no medium-wave (MW-) or no long-wave (LW-) plumage reflection. Females preferred UV- and SW- males. LW- and MW- males were least preferred, suggesting that female zebra finches show the greatest response to the removal of longer wavelengths. Quantal catches of the single cone types viewing body areas of the male zebra finch are presented for each treatment. Our study suggests it is important to consider the role of the UV waveband in avian mate choice in conjunction with the rest of the avian visible spectrum.

The effects of the light environment on prey choice by zebra finches.

Recent research has highlighted the extent to which birds utilise ultraviolet vision in mate choice and foraging. However, neither the importance of the ultraviolet compared with other regions of the visual spectrum nor the use of wavelength cues in other visual tasks have been explored. We assessed the individual choices of zebra finches (Taeniopygia guttata) for different-coloured seeds (red and white millet) under lighting conditions in which filters selectively removed blocks of the avian-visible spectrum corresponding to the spectral sensitivity of the four retinal cone types that subserve colour vision in this species. The effects corresponded to those predicted from the calculated distances between seed types, and between each seed type and the background, in a simple model of tetrachromatic colour space. As predicted for this foraging task, the removal of long-wavelength information had a greater influence than the removal of shorter wavelengths, including ultraviolet wavelengths. These results have important implications for predator-prey interactions and suggest that future studies of natural foraging should consider variations in the light environment.

Separating the effects of predation risk and interrupted foraging upon mass changes in the blue tit Parus caeruleus.

The optimal amount of reserves that a small bird should carry depends upon a number of factors, including the availability of food and environmental predation risk levels. Theory predicts that, if predation risk increases, then a bird should maintain a lower level of reserves. Previous experiments have given mixed results: some have shown reduced reserves and some, increased reserves. However, the birds in these studies may have been interpreting a staged predation event as a period when they were unable to feed rather than a change in predation risk: theory predicts that, if the food supply within the environment is variable, then reserves should be increased. In the present study, we presented blue tits (Parus caeruleus) with a potential predator and compared this response (which could have been potentially confounded by perceived interruption effects) with a response to an actual interruption in the environment during both long and short daytime lengths. During long (but not short) days, the birds responded in line with theoretical predictions by increasing their reserves in response to interruption and reducing them in response to predation. These results are examined in the light of other experimental manipulations and we discuss how well experimental tests have tested the predictions made by theoretical models.

Visual pigments, cone oil droplets and ocular media in four species of estrildid finch.

A microspectrophotometric study was conducted on the retinal photoreceptors of four species of bird: cut-throat finches (Amadina fasciata), gouldian finches (Erythrura gouldiae), white-headed munias (Lonchura maja) and plum-headed finches (Neochmia modesta). Spectral characteristics of the photoreceptors in all four species were very similar. Rods contained a medium-wavelength-sensitive visual pigment with a wavelength of maximum absorbance at 502-504 nm. Four spectrally distinct types of single cone contained a visual pigment with wavelength of maximum absorbance at either 370-373 nm (ultraviolet-sensitive), 440-447 nm (short-wavelength-sensitive); 500 nm (medium-wavelength-sensitive) or 562-565 nm (long-wavelength-sensitive). Oil droplets in the ultraviolet-sensitive single cones showed no detectable absorption between 330 nm and 800 nm. Oil droplets in the short-, medium-, and long-wavelength-sensitive single cones had cut-off wavelengths at 415-423 nm, 510-520 nm and 567-575 nm, respectively. Double cones contained the visual pigment with wavelength of maximum absorbance at 562-565 nm observed in long-wavelength-sensitive single cones. Only the principal member of the double cone pair contained an oil droplet (P-type, cut-off wavelength at 414-489 nm depending on species and retinal location). Spectral transmittance of the intact ocular media of each species was measured along the optic axis. Wavelengths of 0.5 transmittance for all species were very similar (316-318 nm).

Visual pigments, oil droplets, ocular media and cone photoreceptor distribution in two species of passerine bird: the blue tit (Parus caeruleus L.) and the blackbird (Turdus merula L.).

The spectral absorption characteristics of the retinal photoreceptors of the blue tit (Parus caeruleus) and blackbird (Turdus merula) were investigated using microspectrophotometry. The retinae of both species contained rods, double cones and four spectrally distinct types of single cone. Whilst the visual pigments and cone oil droplets in the other receptor types are very similar in both species, the wavelength of maximum sensitivity (lambda(max)) of long-wavelength-sensitive single and double cone visual pigment occurs at a shorter wavelength (557 nm) in the blackbird than in the blue tit (563 nm). Oil droplets located in the long-wavelength-sensitive-single cones of both species cut off wavelengths below 570-573 nm, theoretically shifting cone peak spectral sensitivity some 40 nm towards the long-wavelength end of the spectrum. This raises the possibility that the precise lambda(max) of the long-wavelength-sensitive visual pigment is optimised for the visual function of the double cones. The distribution of cone photoreceptors across the retina, determined using conventional light and fluorescence microscopy, also varies between the two species and may reflect differences in their visual ecology.

Retinal asymmetry in birds.

Vertebrate sensory systems are generally based on bilaterally symmetrical sense organs. It is evident, nevertheless, that birds preferentially use either their left or right eye for viewing novel or familiar stimuli [1], and perform visual discrimination tasks under monocular viewing conditions better with one eye than with the other [2] [3]. Because of the nearly complete contralateral decussation of the optic nerves in birds [4], it has been assumed that this division of labour is due solely to cerebral hemispheric specialisation, generated as a result of uneven photostimulation of the eyes of the developing embryo during the last three or four days before hatching [5] [6]. Here, however, we present evidence that in the European starling, Sturnus vulgaris, even the retinae are morphologically asymmetrical in terms of photoreceptor distribution. This is the first evidence for such asymmetry in any bird and suggests that retinal photoreceptor composition should be assessed during studies involving the lateralisation of visually mediated behaviours.

Trade-off between mating opportunities and parental care: brood desertion by female Kentish plovers.

Why do some parents care for their young whereas others divorce from their mate and abandon their offspring? This decision is governed by the trade-off between the value of the current breeding event and future breeding prospects. In the precocial Kentish plover Charadrius alexandrinus females frequently, but not always, abandon their broods to be cared for by their mate, and seek new breeding partners within the same season. We have shown previously that females' remating opportunities decline with date in the season, so brood desertion should be particularly favourable for early breeding females. However, the benefits are tempered by the fact that single-parent families have lower survival expectancies than those where the female remains to help the male care for the young. We therefore tested the prediction that increasing the value of the current brood (by brood-size manipulation) should increase the duration of female care early in the season, but that in late breeders, with reduced remating opportunities, desertion and thus the duration of female care should be independent of current brood size. These predictions were fulfilled, indicating that seasonally modulated trade-offs between current brood value and remating opportunities can be important in the desertion decisions of species with flexible patterns of parental care.

Visual pigments, cone oil droplets, ocular media and predicted spectral sensitivity in the domestic turkey (Meleagris gallopavo).

A microspectrophotometric survey conducted on the retinal photoreceptors of the domestic turkey (Meleagris gallopavo) revealed the presence of five different types of vitamin A1-based visual pigment (rhodopsin) in seven different types of photoreceptor. A single class of rod contained a medium wavelength-sensitive visual pigment (wavelength of maximum absorbance, lambda max, 504 nm). Four different types of single cone contained visual pigment maximally sensitive to wavelengths in either the long (LWS, lambda max 564 nm), medium (MWS, lambda max 505 nm), short (SWS, lambda max 460 nm) or violet (VS, lambda max 420 nm) spectral ranges. The LWS, MWS and SWS single cones contained pigmented oil droplets with cut-off wavelengths (lambda cut) at 514, 490 and 437 nm, respectively. The VS single cone contained a transparent oil droplet which displayed no significant absorbance above 330 nm. A single class of double cone was also identified, both the principal and accessory members of which contained the LWS cone visual pigment. The principal member contained an oil droplet with a lambda cut at 436 nm. No oil droplet was observed in the accessory member. The use of a glycerol-based cell mountant, which reduced wavelength dependent measurement artefacts in the microspectrophotometric measurements, is described. Predictions of cone effective spectral sensitivity, incorporating measurements of the spectral transmission of the ocular media, suggest that turkeys have considerable sensitivity to wavelengths in the ultraviolet-A (UV-A, 315-400 nm) spectral range. This has implications for both the visual ecology of wild birds and the welfare of intensively farmed individuals.

Plumage Reflectance and the Objective Assessment of Avian Sexual Dichromatism.

Assessment of color using human vision (or standards based thereon) is central to tests of many evolutionary hypotheses. Yet fundamental differences in color vision between humans and other animals call this approach into question. Here we use techniques for objectively assessing color patterns that avoid reliance on species-specific (e.g., human) perception. Reflectance spectra are the invariant features that we expect the animal's color cognition to have evolved to extract. We performed multivariate analyses on principal components derived from >2,600 reflectance spectra (300-720 nm) sampled in a stratified random design from different body regions of male and female starlings in breeding plumage. Starlings possess spatially complex plumage patterns and extensive areas of iridescence. Our study revealed previously unnoticed sex differences in plumage coloration and the nature of iridescent and noniridescent sex differences. Sex differences occurred in some body regions but not others, were more pronounced at some wavelengths (both ultraviolet and human visible), and involved differences in mean reflectance and spectral shape. Discriminant analysis based on principal components were sufficient to sex correctly 100% of our sample. If hidden sexual dichromatism is widespread, then it has important implications for classifications of animals as mono- or dimorphic and for taxonomic and conservation purposes.

Tetrachromacy, oil droplets and bird plumage colours.

There is a growing body of data on avian eyes, including measurements of visual pigment and oil droplet spectral absorption, and of receptor densities and their distributions across the retina. These data are sufficient to predict psychophysical colour discrimination thresholds for light-adapted eyes, and hence provide a basis for relating eye design to visual needs. We examine the advantages of coloured oil droplets, UV vision and tetrachromacy for discriminating a diverse set of avian plumage spectra under natural illumination. Discriminability is enhanced both by tetrachromacy and coloured oil droplets. Oil droplets may also improve colour constancy. Comparison of the performance of a pigeon's eye, where the shortest wavelength receptor peak is at 410 nm, with that of the passerine Leiothrix, where the ultraviolet-sensitive peak is at 365 nm, generally shows a small advantage to the latter, but this advantage depends critically on the noise level in the sensitivity mechanism and on the set of spectra being viewed.

Visual pigments, oil droplets and cone photoreceptor distribution in the european starling (Sturnus vulgaris)

Microspectrophotometric measurements of retinal photoreceptors from the European starling (Sturnus vulgaris) revealed four classes of single cone, containing visual pigments with wavelengths of maximum absorbance (max) at 563, 504, 449 and close to 362 nm. The two longer-wave-sensitive single cones contained brightly coloured oil droplets which cut off light below 572 and 514 nm, respectively. The 449 nm max pigment was associated with a 'colourless' oil droplet with peak measured absorptance below 400 nm. The ultraviolet-sensitive visual pigment was paired with a transparent oil droplet which showed no significant absorption above 350 nm. A single class of double cone was identified, both members of which contained the longwave-sensitive (max 563 nm) visual pigment. The principal member of the double cone contained an oil droplet with a topographically variable cut-off wavelength below 471 nm; the oil droplet found in the accessory member was only measured in the ventral retina and displayed three distinct peaks of absorption at approximately 430, 450 and 480 nm. Rod photoreceptors had a max at 503 nm. A new polynomial for fitting visual pigment templates to ultraviolet-sensitive visual pigment data is given. Topographic density measurements of the different cone classes were made using Nitroblue-tetrazolium chloride to label selectively bleached photoreceptors. The two classes of shortwave-sensitive single cone were more abundant in the dorsal retina, and longwave-sensitive single cones were notably less abundant in the dorso-temporal region of the retina, which subserves binocular vision.