Motion: enhancing signals and concealing cues

ABSTRACT Animal colour patterns remain a lively focus of evolutionary and behavioural ecology, despite the considerable conceptual and technical developments over the last four decades. Nevertheless, our current understanding of the function and efficacy of animal colour patterns remains largely shaped by a focus on stationary animals, typically in a static background. Yet, this rarely reflects the natural world: most animals are mobile in their search for food and mates, and their surrounding environment is usually dynamic. Thus, visual signalling involves not only animal colour patterns, but also the patterns of animal motion and behaviour, often in the context of a potentially dynamic background. While motion can reveal information about the signaller by attracting attention or revealing signaller attributes, motion can also be a means of concealing cues, by reducing the likelihood of detection (motion camouflage, motion masquerade and flicker-fusion effect) or the likelihood of capture following detection (motion dazzle and confusion effect). The interaction between the colour patterns of the animal and its local environment is further affected by the behaviour of the individual. Our review details how motion is intricately linked to signalling and suggests some avenues for future research. This Review has an associated Future Leader to Watch interview with the first author.

Do bovids evolve hindquarter markings for anti-predation?

Conspicuous coloration in animals serves many functions such as anti-predation. Anti-predation strategies include motion dazzle and flash behavior. Motion dazzle markings can reduce the probability of being preyed on because the predators misjudge their movement. In flash behavior, prey demonstrate conspicuous cue while fleeing; the predators follow them, however the prey hide their markings and the predators assume that the prey has vanished. To investigate whether bovids use conspicuous hindquarter markings as an anti-predatory behavior, we undertook phylogenetically controlled analyses to explore under what physiological characteristics and environmental factors bovids might have this color pattern. The results suggested that rump patches and tail markings were more prevalent in bovids living in larger-sized groups, which supports the hypothesis of intraspecific communication. Moreover, we observed the occurrence of conspicuous white hindquarter markings in bovids having smaller body size and living in larger groups, suggesting a motion dazzle function. However, the feature of facultative exposing color patterns (flash markings) was not associated with body size, which was inconsistent with predictions and implied that bovids may not adopt this as an anti-predator strategy. It was concluded that species in bovids with conspicuous white hindquarter markings adopt motion dazzle as an anti-predation strategy while fleeing and escaping from being prey on.

The evolution of patterning during movement in a large-scale citizen science game

The motion dazzle hypothesis posits that high contrast geometric patterns can cause difficulties in tracking a moving target and has been argued to explain the patterning of animals such as zebras. Research to date has only tested a small number of patterns, offering equivocal support for the hypothesis. Here, we take a genetic programming approach to allow patterns to evolve based on their fitness (time taken to capture) and thus find the optimal strategy for providing protection when moving. Our ‘Dazzle Bug’ citizen science game tested over 1.5 million targets in a touch screen game at a popular visitor attraction. Surprisingly, we found that targets lost pattern elements during evolution and became closely background matching. Modelling results suggested that targets with lower motion energy were harder to catch. Our results indicate that low contrast, featureless targets offer the greatest protection against capture when in motion, challenging the motion dazzle hypothesis.

Microhabitat use and body size drive the evolution of colour patterns in snapping shrimps (Decapoda: Alpheidae: Alpheus)

Background matching and disruptive coloration are common strategies used by animals to increase concealment, whereas motion-dazzle may prevent capture after recognition. Studies have related background matching to habitat dependency and survival success, whereas for animals with highly contrasting patterns it has been shown that they are able to explore a broader range of habitats due to disruptive coloration, and possibly via motion-dazzle. However, the effects of these strategies are likely to be influenced by body size and to work better for smaller species. We applied phylogenetic comparative methods to test the hypothesis that smaller snapping shrimps (genus Alpheus) with high-contrast stripes would be able to utilize more microhabitats than non-striped and larger species. We used a published phylogeny of the American species of Alpheus, studies that have described alpheid microhabitats and size, and high-resolution photographs of each species in the phylogeny. Our categorical analysis suggested that generalist snapping shrimps are more likely to have stripes than specialist shrimps, and this effect was stronger in smaller species. Similarly, we found an interacting effect of body size and habitat use on the degree of luminance contrast: smaller generalist species had higher contrast values than average-sized and habitat-specialist species. Therefore, predators, body size and frequency of microhabitats are likely to have influenced the evolution of colour patterns in Alpheus.

No evidence for motion dazzle in an evolutionary citizen science game

The motion dazzle hypothesis posits that high contrast geometric patterns can cause difficulties in tracking a moving target, and has been argued to explain the patterning of animals such as zebras. Research to date has only tested a small number of patterns, offering equivocal support for the hypothesis. Here, we take a genetic programming approach to allow patterns to evolve based on their fitness (time taken to capture) and thus find the optimal strategy for providing protection when moving. Our ‘Dazzle Bug’ citizen science game tested over 1.5 million targets in a touch screen game at a popular visitor attraction. Surprisingly, we found that targets lost pattern elements during evolution and became closely background matching. Modelling results suggested that targets with lower motion energy were harder to catch. Our results indicate that low contrast, featureless targets offer the greatest protection against capture when in motion, challenging the motion dazzle hypothesis.

What makes motion dazzle markings effective against predation?

Motion dazzle markings comprise patterns such as stripes and zig-zags that are postulated to protect moving prey by making predators misjudge the prey’s speed or trajectory. Recent experiments have provided conflicting results on their effect on speed perception and attack success. We focus on motion dazzle stripes and investigate the influence of four parameters—stripe orientation, stripe contrast, target size, and target speed—on perceived speed and attack success using a common experimental paradigm involving human “predators” attacking virtual moving targets on a computer touchscreen. We found that high-contrast stripes running parallel or perpendicular to the direction of motion reduce attack success compared to conspicuous uniform targets. Surprisingly, parallel stripes induced underestimation of speed, while perpendicular stripes induced overestimation of speed in relation to uniform black, suggesting that misjudgment of speed per se is sufficient to reduce attack accuracy. Across all the experiments, we found some support for parallel stripes inducing underestimation of target speed but these stripes reduced attack success only when targets were small, moved at an intermediate speed, and had high internal contrast. We suggest that prey features (e.g., size or speed) are an important determinant of capture success and that distortion of speed perception by a color pattern does not necessarily translate to reduced capture success of the prey. Overall, our results support the idea that striped patterns in prey animals can reduce capture in motion but are effective under a limited set of conditions.

Diverted by dazzle: perceived movement direction is biased by target pattern orientation

‘Motion dazzle’ is the hypothesis that predators may misjudge the speed or direction of moving prey which have high-contrast patterning, such as stripes. However, there is currently little experimental evidence that such patterns cause visual illusions. Here, observers binocularly tracked a Gabor target, moving with a linear trajectory randomly chosen within 18° of the horizontal. This target then became occluded, and observers were asked to judge where they thought it would later cross a vertical line to the side. We found that internal motion of the stripes within the Gabor biased judgements as expected: Gabors with upwards internal stripe motion relative to the overall direction of motion were perceived to be crossing above Gabors with downwards internal stripe movement. However, surprisingly, we found a much stronger effect of the rigid pattern orientation. Patches with oblique stripes pointing upwards relative to the direction of motion were perceived to cross above patches with downward-pointing stripes. This effect occurred only at high speeds, suggesting that it may reflect an orientation-dependent effect in which spatial signals are used in direction judgements. These findings have implications for our understanding of motion dazzle mechanisms and how human motion and form processing interact.

Contrast, contours and the confusion effect in dazzle camouflage

‘Motion dazzle camouflage’ is the name for the putative effects of highly conspicuous, often repetitive or complex, patterns on parameters important in prey capture, such as the perception of speed, direction and identity. Research into motion dazzle camouflage is increasing our understanding of the interactions between visual tracking, the confusion effect and defensive coloration. However, there is a paucity of research into the effects of contrast on motion dazzle camouflage: is maximal contrast a prerequisite for effectiveness? If not, this has important implications for our recognition of the phenotype and understanding of the function and mechanisms of potential motion dazzle camouflage patterns. Here we tested human participants' ability to track one moving target among many identical distractors with surface patterns designed to test the influence of these factors. In line with previous evidence, we found that targets with stripes parallel to the object direction of motion were hardest to track. However, reduction in contrast did not significantly influence this result. This finding may bring into question the utility of current definitions of motion dazzle camouflage, and means that some animal patterns, such as aposematic or mimetic stripes, may have previously unrecognized multiple functions.

PROTECTIVE COLORATION IN ANIMALS

Animals have range of defensive markings which helps to the risk of predator detection (camouflage), warn predators of the prey’s unpalatability (aposematism) or fool a predator into mimicry, masquerade. Animals also use colors in advertising, signalling services such as cleaning to animals of other species, to signal sexual status to other members of the same species. Some animals use color to divert attacks by startle (dalmatic behaviour), surprising a predator e.g. witheyespots or other flashes of color or possibly by motion dazzle, confusing a predator attack by moving a bold pattern like zebra stripes. Some animals are colored for physical protection, such as having pigments in the skin to protect against sunburn; some animals can lighten or darken their skin for temperature regulation. This adaptive mechanism is known as protective coloration. After several years of evolution, most animals now achieved the color pattern most suited for their natural habitat and role in the food chains. Animals in the world rely on their coloration for either protection from predators, concealment from prey or sexual selection. In general the purpose of protective coloration is to decrease an organism’s visibility or to alter its appearance to other organisms. Sometimes several forms of protective coloration are superimposed on one animal.