Cryptically Patterned Moths Perceive Bark Structure When Choosing Body Orientations That Match Wing Color Pattern to the Bark Pattern

Many moths have wing patterns that resemble bark of trees on which they rest. The wing patterns help moths to become camouflaged and to avoid predation because the moths are able to assume specific body orientations that produce a very good match between the pattern on the bark and the pattern on the wings. Furthermore, after landing on a bark moths are able to perceive stimuli that correlate with their crypticity and are able to re-position their bodies to new more cryptic locations and body orientations. However, the proximate mechanisms, i.e. how a moth finds an appropriate resting position and orientation, are poorly studied. Here, we used a geometrid moth Jankowskia fuscaria to examine i) whether a choice of resting orientation by moths depends on the properties of natural background, and ii) what sensory cues moths use. We studied moths’ behavior on natural (a tree log) and artificial backgrounds, each of which was designed to mimic one of the hypothetical cues that moths may perceive on a tree trunk (visual pattern, directional furrow structure, and curvature). We found that moths mainly used structural cues from the background when choosing their resting position and orientation. Our findings highlight the possibility that moths use information from one type of sensory modality (structure of furrows is probably detected through tactile channel) to achieve crypticity in another sensory modality (visual). This study extends our knowledge of how behavior, sensory systems and morphology of animals interact to produce crypsis.     

Camouflage through an active choice of a resting spot and body orientation in moths

Cryptic colour patterns in prey are classical examples of adaptations to avoid predation, but we still know little about behaviours that reinforce the match between animal body and the background. For example, moths avoid predators by matching their colour patterns with the background. Active choice of a species‐specific body orientation has been suggested as an important function of body positioning behaviour performed by moths after landing on the bark. However, the contribution of this behaviour to moths’ crypticity has not been directly measured. From observations of geometrid moths, Hypomecis roboraria and Jankowskia fuscaria, we determined that the positioning behaviour, which consists of walking and turning the body while repeatedly lifting and lowering the wings, resulted in new resting spots and body orientations in J. fuscaria and in new resting spots in H. roboraria. The body positioning behaviour of the two species significantly decreased the probability of visual detection by humans, who viewed photographs of the moths taken before and after the positioning behaviour. This implies that body positioning significantly increases the camouflage effect provided by moth’s cryptic colour pattern regardless of whether the behaviour involves a new body orientation or not. Our study demonstrates that the evolution of morphological adaptations, such as colour pattern of moths, cannot be fully understood without taking into account a behavioural phenotype that coevolved with the morphology for increasing the adaptive value of the morphological trait.     

Disruptive coloration provides camouflage independent of background matching

Natural selection shapes the evolution of anti-predator defences, such as camouflage. It is currently contentious whether crypsis and disruptive coloration are alternative mechanisms of camouflage or whether they are interrelated anti-predator defences. Disruptively coloured prey is characterized by highly contrasting patterns to conceal the body shape, whereas cryptic prey minimizes the contrasts to background. Determining bird predation of artificial moths, we found that moths which were dissimilar from the background but sported disruptive patterns on the edge of their wings survived better in heterogeneous habitats than did moths with the same patterns inside of the wings and better than cryptic moths. Despite lower contrasts to background, crypsis did not provide fitness benefits over disruptive coloration on the body outline. We conclude that disruptive coloration on the edge camouflages its bearer independent of background matching. We suggest that this result is explainable because disruptive coloration is effective by exploiting predators' cognitive mechanisms of prey recognition and not their sensory mechanisms of signal detection. Relative to disruptive patterns on the body outline, disruptive markings on the body interior are less effective. Camouflage owing to disruptive coloration on the body interior is background-specific and is as effective as crypsis in heterogeneous habitats. Hence, we hypothesize that two proximate mechanisms explain the diversity of visual anti-predator defences. First, disruptive coloration on the body outline provides camouflage independent of the background. Second, background matching and disruptive coloration on the body interior provide camouflage, but their protection is background-specific.     

Resting orientation enhances prey survival on strongly structured background

Prey can use various camouflage types as defense against predators. One of the most common and important types is background matching, which occurs if an animal matches the background in color, brightness, and pattern. Although background matching has been studied intensively, the effects of the resting orientation of prey on the effectiveness of camouflage through background matching are not well known in natural conditions. Several past experimental studies have been conducted on resting orientation in the lab often using the visual system of humans. Their results revealed that the detection rates of predators hinge on the combination of the resting orientation of artificial moths and their background. Here, we studied whether survival rates of artificial moth-like models depend on their resting orientation in the wild where the visual conditions and detection distances vary. We used a 2 × 2 design of two resting positions of a horizontally and a vertically striped morph on tree bark. Our results show that the survival probability of moths depended mainly on the orientation of stripes relative to the vertical structure of tree bark. Thus, resting orientation relative to background affected survival. After reanalyzing Endler’s (Biol J Linn Soc 22:187–231, 1984) data on resting habitats of 317 species of North American moths, we found that horizontally striped moths occurred frequently on small herbs and tree bark. We suggest that it would be beneficial for striped moths to orient non-randomly on strongly structured background, like furrows of tree bark. We further suggest that background matching was more important than coincident disruptive coloration in determining the survival rates of our artificial moths.     

Experiments on resting site selection by the typical and melanic forms of the moth, Allophyes oxyacanthae (Caradrinidae)

Six families of the cryptic moth, Allophyes oxyucanthae , four of which contained both the typical and melanic forms of this polymorphic species, were tested for evidence of resting site selection in a large box lined with oak bark of three reflectances. Moths from different families were tested separately. Typicals from all four families tended to show a preference for the background which most closely matched their reflectance and on which they were most cryptic. Melanic moths from different families showed different resting site selection behaviour; those from two families preferring dark bark, on which melanics were most cryptic, while those from other families did not. The significance of these results in relation to previous suggestions about the control of resting site selection is discussed     

Adaptive body patterning,three‐dimensional skin morphology and camouflage measures of the slender filefish Monacanthus tuckeri on a Caribbean coral reef

The slender filefish is a master of adaptive camouflage and can change its appearance within 1–3 s. Videos and photographs of this animal's cryptic body patterning and behavior were collected in situ under natural light on a Caribbean coral reef. We present an ethogram of body patterning components that includes large‐ and small‐scale spots, stripes and bars that confer a variety of cryptic patterns amidst a range of complex backgrounds. Field images were analyzed to investigate two aspects of camouflage effectiveness: (1) the degree of colour resemblance between animals and their nearby visual stimuli; and (2) the visibility of each fish's actual body outline vs. its illusory outline. Most animals more closely matched the colour of nearby visual stimuli than that of the surrounding background. Three‐dimensional dermal flaps complement the melanophore skin patterns by enhancing the complexity of the fish's physical skin texture to disguise its actual body shape, and the morphology of these structures was studied. The results suggest that the body patterns, skin texture, postures and swimming orientations putatively hinder both the detection and recognition of the fish by potential visual predators. Overall, the rapid speed of change of multiple patterns, colour blending with nearby backgrounds, and the physically complicated edge produced by dermal flaps effectively camouflage this animal among soft corals and macroalgae in the Caribbean Sea.     

Lepidopteran wing patterns and the evolution of satyric mimicry

The hypothesis of satyric mimicry postulates that the colour patterns of an animal may make its identity ambiguous, and this ambiguity interferes with the process of perception in vertebrate predators for a sufficient time to allow the potential prey to take evasive action. It has now been found that eyespots and other designs on the wings of many insect species are often coupled with other wing patterns and designs. These composite images often closely resemble heads and bodies of vertebrates (including birds and reptiles) and of various invertebrates. Such images can be perceived in living insects, although only rarely in set specimens because of displacement of the components. Visual processing by non‐mammalian vertebrates generally involves attention to detail, suggesting that, at least initially, and unlike humans, they perceive embedded images on insect wings and bodies and ignore the whole or Gestalt. They are therefore likely to be confused by the ambiguity of the potential prey. It can be calculated that a delay of the order of only tenths of a second in the attack on a stationary insect by a predator could result in failure of capture. It is proposed in the present review that the concept of satyric mimicry be extended to include complex imagery of other organisms. Such iconic images, which often represent toxic or dangerous animals, are particularly common amongst saturniid moths and nymphalid and danaid butterflies (including the Monarch butterfly, Danaus plexippus). © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109 , 203–214.     

Cuttlefish use visual cues to determine arm postures for camouflage

To achieve effective visual camouflage, prey organisms must combine cryptic coloration with the appropriate posture and behaviour to render them difficult to be detected or recognized. Body patterning has been studied in various taxa, yet body postures and their implementation on different backgrounds have seldom been studied experimentally. Here, we provide the first experimental evidence that cuttlefish (Sepia officinalis), masters of rapid adaptive camouflage, use visual cues from adjacent visual stimuli to control arm postures. Cuttlefish were presented with a square wave stimulus (period = 0.47 cm; black and white stripes) that was angled 0°, 45° or 90° relative to the animals' horizontal body axis. Cuttlefish positioned their arms parallel, obliquely or transversely to their body axis according to the orientation of the stripes. These experimental results corroborate our field observations of cuttlefish camouflage behaviour in which flexible, precise arm posture is often tailored to match nearby objects. By relating the cuttlefishes' visual perception of backgrounds to their versatile postural behaviour, our results highlight yet another of the many flexible and adaptive anti-predator tactics adopted by cephalopods.     

Progressive background in moths, and a quantitative measure of crypsis

A method is presented for quantitative estimation of the degree of crypsis of species seen by visual predators against known backgrounds. It is based upon a comparison between transects taken across animal and background colour patterns. The method was applied to day-resting moths in deciduous forest in New Jersey. Each species is found for two to four weeks at characteristic dates, and there is a constant turnover of species. In both moths and backgrounds there is a regular change in the colour pattern parameters from winter through spring to early summer. Moths are on average more cryptic at their normal dates than they would be if present earlier or later in the year. Species with known resting sites are on average more cryptic on their resting sites than other background habitats. Species that rest on more than one background habitat are less cryptic on their preferred habitats than are specialists. Species that rest under leaves and are not visible from above are not very cryptic. Specific v. general resemblance, disruptive coloration, and factors affecting 'aspect diversity' are discussed. The new method of estimating crypsis is useful for studies of crypsis as well as in sexual selection. It is necessary to know much about the resting sites and behaviour of moths, as well as other functions of colour patterns, to understand colour pattern evolution.     

Fine nanostructural variation in the wing pattern of a moth <Emphasis Type="Italic">Chiasmia eleonora</Emphasis> Cramer (1780)

Butterflies and moths possess diverse patterns on their wings. Butterflies employ miscellaneous colour in the wings whereas moths use a combination of dull colours like white, grey, brown and black for the patterning of their wings. The exception is some of the toxic diurnal moths which possess bright wing colouration. Moths possess an obscure pattern in the dorsal part of the wings which may be a line, zigzag or swirl. Such patterns help in camouflage during resting period. Thus, the dorsal wing pattern of the moth is used for both intra- as well as inter-specific signal communication. Chiasmia eleonora is a nocturnal moth of greyish black colouration. The dorsal hindwing possesses yellow and black colour patches. A white-coloured oblique line crosses both left and right fore- and hindwings to form a V-shaped pattern across the dorsal wing. This V-shaped pattern possesses a UV signal. Closer to the body, the colour appears darker, which fades towards the margin. The fine nanostructural variation is observed throughout the wings. This study elucidates the wing pattern of the geometrid moth C. eleonora using high-resolution microscopy techniques that has not been described in previous studies.     

Coral reef flounders,Bothus lunatus,choose substrates on which they can achieve camouflage with their limited body pattern repertoire

Camouflage is a common tactic to avoid detection or recognition by predators and prey. Flounders have adaptive camouflage but a limited body pattern repertoire. We tested whether peacock flounders actively select or avoid certain substrates to more effectively use their limited camouflaging ability. We acquired and analyzed ten 30‐min videos of individual flounders on a coral reef in Bonaire, Dutch Caribbean. Using Manly's beta resource selection indices, we were able to confirm that peacock flounders at this location preferred to settle on neutral‐coloured substrates, such as sand and dead coral. Moreover, they avoided live coral, cyanobacteria, and sponges, which are often brightly coloured (e.g. yellow, orange, and purple). Quantitative analyses of photographs of settled flounders indicate that they use uniform and mottled camouflage patterns, and that the small‐to‐moderate spatial scale of their physiologically controlled light and dark skin components limits their camouflage capabilities to substrates with similar colour and spatial frequencies. These fishes changed their body pattern very fast. We did not observe disruptive body patterns, which are generally characterized by large‐scale skin components and higher contrast. The results suggest that flounders are using visual information to actively choose substrates on which they can achieve general background resemblance. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114 , 629–638.     

Selective bird predation on the peppered moth: the last experiment of Michael Majerus

Colour variation in the peppered moth Biston betularia was long accepted to be under strong natural selection. Melanics were believed to be fitter than pale morphs because of lower predation at daytime resting sites on dark, sooty bark. Melanics became common during the industrial revolution, but since 1970 there has been a rapid reversal, assumed to have been caused by predators selecting against melanics resting on today's less sooty bark. Recently, these classical explanations of melanism were attacked, and there has been general scepticism about birds as selective agents. Experiments and observations were accordingly carried out by Michael Majerus to address perceived weaknesses of earlier work. Unfortunately, he did not live to publish the results, which are analysed and presented here by the authors. Majerus released 4864 moths in his six-year experiment, the largest ever attempted for any similar study. There was strong differential bird predation against melanic peppered moths. Daily selection against melanics (s ≈ 0.1) was sufficient in magnitude and direction to explain the recent rapid decline of melanism in post-industrial Britain. These data provide the most direct evidence yet to implicate camouflage and bird predation as the overriding explanation for the rise and fall of melanism in moths.     

A fish‐eye view of cuttlefish camouflage using in situ spectrometry

Cuttlefish are colour blind yet they appear to produce colour‐coordinated patterns for camouflage. Under natural in situ lighting conditions in southern Australia, we took point‐by‐point spectrometry measurements of camouflaged cuttlefish, Sepia apama, and various natural objects in the immediate visual surrounds to quantify the degree of chromatic resemblance between cuttlefish and backgrounds to potential fish predators. Luminance contrast was also calculated to determine the effectiveness of cuttlefish camouflage to this information channel both for animals with or without colour vision. Uniform body patterns on a homogeneous background of algae showed close resemblance in colour and luminance; a Uniform pattern on a partially heterogeneous background showed mixed levels of resemblance to certain background features. A Mottle pattern with some disruptive components on a heterogeneous background showed general background resemblance to some benthic objects nearest the cuttlefish. A noteworthy observation for a Disruptive body pattern on a heterogeneous background was the wide range in spectral contrasts compared to Uniform and Mottle patterns. This suggests a shift in camouflage tactic from background resemblance (which hinders detection by the predator) to more specific object resemblance and disruptive camouflage (which retards recognition). © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109 , 535–551.     

Fearful symmetry? Intra-individual comparisons of asymmetry in cryptic vs. signalling colour patterns in butterflies

The signalling role of asymmetry has attracted considerable recent interest among evolutionary biologists. Although it has been studied primarily within the context of sexual selection, symmetry of signals may play a role also in inter-specific communication, such as predator–prey interactions. Both theory and experimental evidence suggest that asymmetry may impair the efficacy of visual warning signals used to deter potential predators, but increase the protective value of non-signalling, cryptic colour patterns used to decrease the risk of detection. Here we tested the prediction from this hypothesis by means of intra-individual comparisons of asymmetry in colour pattern elements in three species of moths (Arctia caja (L.), Noctua orbona (L.), Smerinthus ocellata (L.)) that possess cryptic fore wing patterns and signalling hind wing patterns. Mean asymmetries constituted 4.3% (range 2.1–7.0%) of trait size for colour pattern elements, whereas individual asymmetry levels reached as high as 26%. Asymmetry tended to be somewhat larger in cryptic patterns on fore wings than in signalling patterns on hind wings in five of six comparisons, but in only one case was the difference statistically significant. In addition, pattern elements were somewhat more asymmetric on fore wings also in Saturnia pavonia (L.), which possesses identical signalling eyespots on both fore and hind wings. The relatively low levels of asymmetry also in cryptic patterns imply either that selection does not favour increased asymmetry in cryptic patterns, or that the evolution of pronounced asymmetry is developmentally or genetically constrained.     

Experiments on resting site selection by nocturnal moths

When different species of moths are presented with a choice between black and white resting backgrounds, there is a strong correlation between the colour selected and the reflectance of the forewings. Under more natural conditions, light-coloured moths usually rest on fresh vegetation whilst dark-winged species select tree bark or rest upon the ground, and different defensive strategies appear to have been adopted by species in these two latter situations. Studies on the mechanism of background selection, and on background selection in polymorphic species, are reviewed.     

The predation costs of symmetrical cryptic coloration

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.     

Display behaviour and dewlap colour as predictors of contest success in brown anoles

Many animals display visual signals in male contests for access to females and territories. These visual signals can be multimodal and stimulate different aspects of a signal receiver's visual system. Over two summers, we tested whether aspects of behaviour and dewlap colour might function as signals that predict contest success when males compete for access to either mates or territories in male brown anole lizards. We found that behaviour (PC1, a correlated composite of head‐bob, push‐up, and dewlap extension frequency) and an aspect of dewlap colour (PC3, the relative amounts of ultraviolet, yellow, orange, and red of the dewlap margin) were retained in the minimum adequate model predicting contest success across years and social contexts. Winners showed significant differences in behaviour (winners displayed more) and dewlap margin PC3 (winners had lower PC3 scores) compared to contest losers. These findings suggest that display behaviour and dewlap colour might serve as signals indicating a male's ability to win contests for access to females and territories. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111 , 646–655.     

Shiny wing scales cause spec(tac)ular camouflage of the angled sunbeam butterfly,Curetis acuta

The angled sunbeam butterfly, Curetis acuta (Lycaenidae), is a distinctly sexually dimorphic lycaenid butterfly from Asia. The dorsal wings of female and male butterflies have a similar pattern, with a large white area in the female and an orange area in the male, framed within brown–black margins. The ventral wings of both sexes are silvery white, which is caused by stacks of overlapping, non‐pigmented, and specular‐reflecting scales. With oblique illumination, the reflected light of the ventral wings is strongly polarized. We show that the silvery reflection facilitates camouflage in a shaded, foliaceous environment. The ecological function of the silvery reflection is presumably two‐fold: for intraspecific signalling in flight, and for reducing predation risk at rest and during hibernation. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109 , 279–289.     

Camouflage by edge enhancement in animal coloration patterns and its implications for visual mechanisms.

Animal camouflage patterns may exploit, and thus give an insight into, visual processing mechanisms. In one common type of camouflage the borders of the coloured patterns are enhanced by high contrast lines. This type of camouflage is seen on many frogs and we use it as the basis for speculating about vision in a small, frog-eating snake. It is argued that a simple categorization of intensity profiles, such as that invoked by a mechanism that detects phase-congruence, occurs at an early stage of snake vision. We show that edge-detectors using a phase-congruence strategy will be unable to distinguish between 'natural' step-edges and the enhanced border profiles commonly seen on cryptic animals, and that the camouflage will be effective over a wide range of spatial scales.