A complete explanation of the diversity of animal colour patterns requires an understanding of both the developmental mechanisms generating them and their adaptive value. However, only two previous studies, which involved computer-generated evolving prey, have attempted to make this link. This study examines variation in the camouflage patterns displayed on the flanks of many felids. After controlling for the effects of shared ancestry using a fully resolved molecular phylogeny, this study shows how phenotypes from plausible felid coat pattern generation mechanisms relate to ecology. We found that likelihood of patterning and pattern attributes, such as complexity and irregularity, were related to felids' habitats, arboreality and nocturnality. Our analysis also indicates that disruptive selection is a likely explanation for the prevalence of melanistic forms in Felidae. Furthermore, we show that there is little phylogenetic signal in the visual appearance of felid patterning, indicating that camouflage adapts to ecology over relatively short time scales. Our method could be applied to any taxon with colour patterns that can reasonably be matched to reaction–diffusion and similar models, where the kinetics of the reaction between two or more initially randomly dispersed morphogens determines the outcome of pattern development.
camouflage; background matching; pattern formation; reaction–diffusion models; melanism; disruptive selection
Movement is the enemy of camouflage: most attempts at concealment are disrupted by motion of the target. Faced with this problem, navies in both World Wars in the twentieth century painted their warships with high contrast geometric patterns: so-called “dazzle camouflage”. Rather than attempting to hide individual units, it was claimed that this patterning would disrupt the perception of their range, heading, size, shape and speed, and hence reduce losses from, in particular, torpedo attacks by submarines. Similar arguments had been advanced earlier for biological camouflage. Whilst there are good reasons to believe that most of these perceptual distortions may have occurred, there is no evidence for the last claim: changing perceived speed. Here we show that dazzle patterns can distort speed perception, and that this effect is greatest at high speeds. The effect should obtain in predators launching ballistic attacks against rapidly moving prey, or modern, low-tech battlefields where handheld weapons are fired from short ranges against moving vehicles. In the latter case, we demonstrate that in a typical situation involving an RPG7 attack on a Land Rover the reduction in perceived speed is sufficient to make the grenade miss where it was aimed by about a metre, which could be the difference between survival or not for the occupants of the vehicle.
Even if an animal matches its surroundings perfectly in colour and texture, any mismatch between the spatial phase of its pattern and that of the background, or shadow created by its three-dimensional relief, is potentially revealing. Nevertheless, for camouflage to be fully broken, the shape must be recognizable. Disruptive coloration acts against object recognition by the use of high-contrast internal colour boundaries to break up shape and form. As well as the general outline, characteristic features such as eyes and limbs must also be concealed; this can be achieved by having the colour patterns on different, but adjacent, body parts aligned to match each other (i.e. in phase). Such ‘coincident disruptive coloration’ ensures that there is no phase disjunction where body parts meet, and causes different sections of the body to blend perceptually. We tested this theory using field experiments with predation by wild birds on artificial moth-like targets, whose wings and (edible pastry) bodies had colour patterns that were variously coincident or not. We also carried out an experiment with humans searching for analogous targets on a computer screen. Both experiments show that coincident disruptive coloration is an effective mechanism for concealing an otherwise revealing body form.
camouflage; disruptive coloration; crypsis; animal coloration; defensive coloration
Parental care often increases offspring survival, but is costly to the parents. A trade-off between the cost and benefit of care is expected, so that when care provisioning by both parents is essential for the success of young, for instance in extremely cold or hot environments, the parents should rear their young together. We investigated the latter hypothesis in a ground nesting shorebird, the Kentish plover Charadrius alexandrinus in an extremely hot environment, the Arabian Desert. Midday ground temperature was often above 50°C in our study site in Abu Dhabi (United Arab Emirates), thus leaving the eggs unattended even for a few minute risks overheating and death of embryos.
Through the use of video surveillance systems we recorded incubation routines of male and female Kentish plovers at 28 nests over a full day (24 h). We show that ambient temperature had a significant influence on incubation behaviour of both sexes, and the relationships are often non-linear. Coordinated incubation between parents was particularly strong in midday with incubation shared approximately equally between the male and the female. The enhanced biparental incubation was due to males increasing their nest attendance with ambient temperature.
Our results suggest biparental care is essential during incubation in the Kentish plover in extremely hot environments. Shared incubation may also help the parents to cope with heat stress themselves: they can relieve each other frequently from incubation duties. We suggest that once the eggs have hatched the risks associated with hot temperature are reduced: the chicks become mobile, and they gradually develop thermoregulation. When biparental care of young is no longer essential one parent may desert the family. The relaxed demand of the offspring may contribute to the diverse breeding systems exhibited by many shorebirds.
For scientific, ethical and economic reasons, experiments involving animals should be appropriately designed, correctly analysed and transparently reported. This increases the scientific validity of the results, and maximises the knowledge gained from each experiment. A minimum amount of relevant information must be included in scientific publications to ensure that the methods and results of a study can be reviewed, analysed and repeated. Omitting essential information can raise scientific and ethical concerns. We report the findings of a systematic survey of reporting, experimental design and statistical analysis in published biomedical research using laboratory animals. Medline and EMBASE were searched for studies reporting research on live rats, mice and non-human primates carried out in UK and US publicly funded research establishments. Detailed information was collected from 271 publications, about the objective or hypothesis of the study, the number, sex, age and/or weight of animals used, and experimental and statistical methods. Only 59% of the studies stated the hypothesis or objective of the study and the number and characteristics of the animals used. Appropriate and efficient experimental design is a critical component of high-quality science. Most of the papers surveyed did not use randomisation (87%) or blinding (86%), to reduce bias in animal selection and outcome assessment. Only 70% of the publications that used statistical methods described their methods and presented the results with a measure of error or variability. This survey has identified a number of issues that need to be addressed in order to improve experimental design and reporting in publications describing research using animals. Scientific publication is a powerful and important source of information; the authors of scientific publications therefore have a responsibility to describe their methods and results comprehensively, accurately and transparently, and peer reviewers and journal editors share the responsibility to ensure that published studies fulfil these criteria.
Perception of the body's outline and three-dimensional shape arises from visual cues such as shading, contour, perspective and texture. When a uniformly coloured prey animal is illuminated from above by sunlight, a shadow may be cast on the body, generating a brightness contrast between the dorsal and ventral surfaces. For animals such as caterpillars, which live among flat leaves, a difference in reflectance over the body surface may degrade the degree of background matching and provide cues to shape from shading. This may make otherwise cryptic prey more conspicuous to visually hunting predators. Cryptically coloured prey are expected to match their substrate in colour, pattern and texture (though disruptive patterning is an exception), but they may also abolish self-shadowing and therefore either reduce shape cues or maintain their degree of background matching through countershading: a gradation of pigment on the body of an animal so that the surface closest to illumination is darker. In this study, we report the results from a series of field experiments where artificial prey resembling lepidopteran larvae were presented on the upper surfaces of beech tree branches so that they could be viewed by free-living birds. We demonstrate that countershading is superior to uniform coloration in terms of reducing attack by free-living predators. This result persisted even when we fixed prey to the underside of branches, simulating the resting position of many tree-living caterpillars. Our experiments provide the first demonstration, in an ecologically valid visual context, that shadowing on bodies (such as lepidopteran larvae) provides cues that visually hunting predators use to detect potential prey species, and that countershading counterbalances shadowing to enhance cryptic protection.
countershading; crypsis; predation; animal coloration; defensive coloration
Camouflage typically involves colour patterns that match the background. However, it has been argued that concealment may be achieved by strategic use of apparently conspicuous markings. Recent evidence supports the theory that the presence of contrasting patterns placed peripherally on an animal's body (disruptive coloration) provides survival advantages. However, no study has tested a key prediction from the early literature that disruptive coloration is effective even when some colour patches do not match the background and have a high contrast with both the background and adjacent pattern elements (disruptive contrast). We test this counter-intuitive idea that conspicuous patterns might aid concealment, using artificial moth-like targets with pattern elements designed to match or mismatch the average luminance (lightness) of the trees on which they were placed. Disruptive coloration was less effective when some pattern elements did not match the background luminance. However, even non-background-matching disruptive patterns reduced predation relative to equivalent non-disruptive patterns or to unpatterned controls. Therefore, concealment may still be achieved even when an animal possesses markings not found in the background. Disruptive coloration may allow animals to exploit backgrounds on which they are not perfectly matched, and to possess conspicuous markings while still retaining a degree of camouflage.
camouflage; disruptive coloration; crypsis; predation; visual search; animal coloration
Many animals use concealing markings to reduce the risk of predation. These include background pattern matching (crypsis), where the coloration matches a random sample of the background and disruptive patterns, whose effectiveness has been hypothesized to lie in breaking up the body into a series of apparently unrelated objects. We have previously established the effectiveness of disruptive coloration against avian predators, using artificial moth-like stimuli with colours designed to match natural backgrounds as perceived by birds. Here, we investigate the mechanism by which disruptive patterns reduce detectability, using a computational vision model of edge detection applied to photographs of our experimental stimuli, calibrated for bird colour vision. We show that, disruptive coloration is effective by exploiting edge detection algorithms that we use to model early visual processing. Thus, ‘false’ edges are detected within the body rather than at its periphery, so inhibiting successful detection of the animal's body outline.
disruptive coloration; background matching; edge detection; vision; camouflage
In psychological studies of visual perception, symmetry is accepted as a potent cue in visual search for cryptic objects, yet its importance for non-human animals has been assumed rather than tested. Furthermore, while the salience of bilateral symmetry has been established in laboratory-based search tasks using human subjects, its role in more natural settings, closer to those for which such perceptual mechanisms evolved, has not, to our knowledge, been investigated previously. That said, the salience of symmetry in visual search has a plausible adaptive rationale, because biologically important objects, such as prey, predators or conspecifics, usually have a plane of symmetry that is not present in their surroundings. We tested the conspicuousness to avian predators of cryptic artificial, moth-like targets, with or without bilateral symmetry in background-matching coloration, against oak trees in the field. In two independent experiments, symmetrical targets were predated at a higher rate than otherwise identical asymmetrical targets. There was a small, but significant, fitness cost to symmetry in camouflage patterns. Given that birds are the most commonly invoked predators shaping the evolution of defensive coloration in insects, this raises the question of why bilateral asymmetry is not more common in cryptic insects.
defensive coloration; bilateral symmetry; bird vision; predation risk; visual search
Studies of birds have a disproportionate representation in the literature on life-history evolution, because of the (apparent) ease with which the costs and benefits can be quantified and manipulated. During reproduction, birds frequently show a highly conserved pattern of mass change and changes in mass loss during breeding have been widely considered to be a valid short-term measure of the costs of reproduction. Experimental manipulations of the breeding attempts of birds usually argue that the presence of a response shows that a cost of reproduction exists, but there is little consensus as to how the size of these costs can be measured.
We model this mass loss by considering how a parent can maximise its lifetime reproductive success, using a theoretical framework that is particularly suited to modelling parental care in altricial birds. If lifetime reproductive success is taken to be the sum of a parent's current and future reproductive success, we show that the exact forms of these components will influence the optimal amount of mass a parent should lose. In particular, we demonstrate that the shape of the relationship between parental investment and chick survival will lead to differing degrees of investment between parents of different initial qualities: parents with initially high levels of energy reserves could conceivably invested a lesser, similar or greater amount of resources than parents with initially low reserves, and these initially 'heavy' parents could potentially end up being lighter than the initially 'lighter' individuals.
We argue that it is difficult to make predictions about the dependence of a parent's final mass on its initial mass, and therefore mass loss should only be used as a short-term measure of the costs of reproduction with caution. The model demonstrates that we require a better understanding of the relationship between mass loss and both current and future reproductive success of the parent, before predictions about mass loss can be made and tested. We discuss steps that could be taken to increase the accuracy of our predictions.
A variety of techniques are used to study the colours of animal signals, including the use of visual matching to colour charts. This paper aims to highlight why they are generally an unsatisfactory tool for the measurement and classification of animal colours and why colour codes based on HTML (really RGB) standards, as advocated in a recent paper, are particularly inappropriate. There are many theoretical arguments against the use of colour charts, not least that human colour vision differs markedly from that of most other animals. However, the focus of this paper is the concern that, even when applied to humans, there is no simple 1:1 mapping from an RGB colour space to the perceived colours in a chart (the results are both printer- and illumination-dependent). We support our criticisms with data from colour matching experiments with humans, involving self-made, printed colour charts.
Colour matching experiments with printed charts involving 11 subjects showed that the choices made by individuals were significantly different between charts that had exactly the same RGB values, but were produced from different printers. Furthermore, individual matches tended to vary under different lighting conditions. Spectrophotometry of the colour charts showed that the reflectance spectra of the charts varied greatly between printers and that equal steps in RGB space were often far from equal in terms of reflectance on the printed charts.
In addition to outlining theoretical criticisms of the use of colour charts, our empirical results show that: individuals vary in their perception of colours, that different printers produce strikingly different results when reproducing what should be the same chart, and that the characteristics of the light irradiating the surface do affect colour perception. Therefore, we urge great caution in the use of colour charts to study animal colour signals. They should be used only as a last resort and in full knowledge of their limitations, with specially produced charts made to high industry standards.
Fluorescence has so far been found in 52 parrot species when illuminated with ultraviolet-A (UVA) 'black' lamps, and two attempts have been made to determine whether such fluorescence plays any role in sexual signalling. However, the contribution of the reflectance versus fluorescence to the total radiance from feathers, even in the most studied species to date (budgerigars), is unclear. Nor has the plumage of this study species been systematically assessed to determine the distribution of fluorescent patches. We therefore used spectrofluorometry to determine which areas of budgerigars fluoresce and the excitation and emission spectra involved; this is the first time that such a technique has been applied to avian plumage. We found that both the yellow crown and (normally hidden) white downy chest feathers exhibit strong UVA-induced fluorescence, with peak emissions at 527 nm and 436 nm, respectively. Conversely, the bright-green chest and dark-blue tail feathers do not fluoresce. When comparing reflectance spectra (400-700 nm) from the yellow crown using illuminants with a proportion of UVA comparable to daylight, and illuminants with all UVA removed, no measurable difference resulting from fluorescence was found. This suggests that under normal daylight the contribution of fluorescence to radiance is probably trivial. Furthermore, these spectra revealed that males had fluorescent crowns with substantially higher reflectance than those of females, in both the UV waveband and at longer wavelengths. Reflectance spectrophotometry was also performed on a number of live wild-type male budgerigars to investigate the chromatic contrast between the different plumage areas. This showed that many plumage regions are highly UV-reflective. Overall our results suggest that rapid surveys using UVA black lamps may overestimate the contribution of fluorescence to plumage coloration, and that any signalling role of fluorescence emissions, at least from the yellow crown of budgerigars, may not be as important as previously thought.
Why do different species of birds start their dawn choruses at different times? We test the hypothesis that the times at which different species start singing at dawn are related to their visual capability at low light intensities. Birds with large eyes can achieve greater pupil diameters and hence, all other things being equal, greater visual sensitivity and resolution than birds with small eyes. We estimated the maximum pupil diameter of passerine birds by measuring the diameter of the exposed eye surface, and measured the times of the first songs at dawn of songbirds present in different bird communities, and the light intensities at these times. Using phylogenetic comparative analyses, we found that songbirds with large eyes started to sing at lower light intensities (and therefore earlier) than species with smaller eyes. These relationships were stronger when differences in body size were controlled for statistically, and were consistent between two phylogenies and when species were treated as independent data points. Our results therefore provide robust support for the hypothesis that visual capability at low light levels influences the times at which birds start to sing at dawn.