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Summary of the low-level visual cues so far known to be used in the expression of the Disruptive body pattern in S. officinalis. A given visual environment provides low-level cues. If these cues include edgy objects of an area approximately the area of the animal's white square then Disruptive components will be expressed. Visual depth and background contrast increase the expression of some Disruptive components (Kelman et al. 2008). Synchronized expression of Disruptive components leads to the so-called Disruptive body pattern.
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The cuttlefish, Sepia officinalis, provides a fascinating opportunity to investigate the mechanisms of camouflage as it rapidly changes its body patterns in response to the visual environment. We investigated how edge information determines camouflage responses through the use of spatially high-pass filtered 'objects' and of isolated edges. We then...
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... example, textural change might be combined with luminance, colour, motion or depth (Landy & Graham 2004). Mounting evidence shows that cuttlefish perceive and use multiple cues to determine what body pattern should be used ( figure 1). Here, we see that although the second-order stimulus (objects defined by texture) results in the use of Disruptive components such as the white square and head bar (i.e. ...
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Cuttlefish rapidly change their appearance in order to camouflage on a given background in response to visual parameters, giving us access to their visual perception. Recently, it was shown that isolated edge information is sufficient to elicit a body pattern very similar to that used when a whole object is present. Here, we examined contour comple...
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... Cephalopods integrate the overall spatial scale of their background [44][45][46] as well as the intensity and level of contrast 44,[47][48][49] . They respond strongly to the edges present in their visual scene, particularly to terminal edges over smooth curves 50,51 , and are sensitive to the relative phase of different spatial frequencies within the scene 46 . They also integrate depth information about their surroundings 45,52,53 . ...
... Apart from exhibiting an impressive repertoire of skin patterns and a sophisticated visual system, this characteristic allows them to change skin patterning instantly [32,33]. Despite being color-blind [34], cuttlefish are able to closely emulate background colors [35] and are particularly responsive to edges and differences in contrast [36,37]. Although this species displays a continuum of chromatic body patterns, three types are commonly recognizable based on the size of light and dark spots. ...
Ocean warming and acidification have been shown to elicit deleterious effects on cephalopod mollusks, especially during early ontogeny, albeit effects on behavior remain largely unexplored. This study aimed to evaluate, for the first time, the effect of end-of-the-century projected levels of ocean warming (W; + 3 °C) and acidification (A; 980 µatm pCO2) on Sepia officinalis hatchlings’ exploratory behavior and ability to camouflage in different substrate complexities (sand and black and white gravel). Cuttlefish were recorded in open field tests, from which mobility and exploratory avoidance behavior data were obtained. Latency to camouflage was registered remotely, and pixel intensity of body planes and background gravel were extracted from photographs. Hatching success was lowered under A and W combined (AW; 72.7%) compared to control conditions (C; 98.8%). Motion-related behaviors were not affected by the treatments. AW delayed camouflage response in the gravel substrate compared to W alone. Moreover, cuttlefish exhibited a higher contrast and consequently a stronger disruptive pattern under W, with no changes in background matching. These findings suggest that, although climate change may elicit relevant physiological challenges to cuttlefish, camouflage and mobility of these mollusks are not undermined under the ocean of tomorrow.
... The body pattern model proposes that cuttlefish integrate low-level sensory cues to categorize the background and co-ordinate component expression to produce a small number of overall body patterns. [2][3][4] The feature matching model proposes that each component is expressed in response to one (or more) local visual features, and the overall pattern depends upon the combination of features in the background. Consistent with the feature matching model, six of the backgrounds elicited a specific set of one to four components, whereas the seventh elicited eleven components typical of a disruptive body pattern. ...
... Multiple visual cues elicit a shift from mottle to disruptive patterns, including the presence of edges, the size of objects, and visual depth. 3,7,14,15 A fourth pattern is expressed categorically in response to 3D objects. 12 Although widely used for interpreting cuttlefish camouflage behavior, the body pattern model ( Figure 1B) does not easily explain why cuttlefish have some 30 pattern components, rather than flexibly combining a few patterns as flatfish do. ...
To camouflage themselves on the seafloor, European cuttlefish Sepia officinalis control the expression of about 30 pattern components to produce a range of body patterns.¹ If each component were under independent control, cuttlefish could produce at least 2³⁰ patterns. To examine how cuttlefish deploy this vast potential, we recorded cuttlefish on seven experimental backgrounds, each designed to resemble a pattern component, and then compared their responses to predictions of two models of sensory control of component expression. The body pattern model proposes that cuttlefish integrate low-level sensory cues to categorize the background and co-ordinate component expression to produce a small number of overall body patterns.2, 3, 4 The feature matching model proposes that each component is expressed in response to one (or more) local visual features, and the overall pattern depends upon the combination of features in the background. Consistent with the feature matching model, six of the backgrounds elicited a specific set of one to four components, whereas the seventh elicited eleven components typical of a disruptive body pattern. This evidence suggests that both modes of control are important, and we suggest how they can be implemented by a recent hierarchical model of the cuttlefish motor system.
... In this literature review, we excluded reviews, conceptual models, and any empirical studies focusing on irreversible color change, ontogenetic color change, or behavioral color change (e.g., wetting). This review consisted of studies published between 1 Jan 1990 and 28 Oct 2020, using the following search terms: (camouflage* OR crypsis OR cryptic) AND (color chang* OR colour chang* OR plastic* Buresch et al., 2015, Zylinski et al., 2009, Kelman et al., 2007Artificial, Semi-Natural ...
Color change serves many antipredator functions and may allow animals to better match environments or disrupt outlines to prevent detection. Rapid color change could potentially provide camouflage to animals that frequently move among microhabitats. Determining the adaptiveness of whole-animal rapid color changes in natural habitats with respect to predator visual systems would greatly broaden our fundamental understanding of the evolution of rapid color change. We tested whether whole-body color change provides water anoles (Anolis aquaticus) with camouflage against avian predators and whether these rapid changes allow them to shift between environment matching and edge disruption. We manipulated A. aquaticus placement in natural microhabitats and used digital image analysis to quantify color matching, pattern matching, and edge disruption produced by microhabitat-induced color change. Color change reduced lizard detectability to predators in microhabitat-specific ways. Environment matching was favored when lizards were in solid-colored microhabitats, regardless of exposure to predators. Edge disruption was instead induced by high exposure and varied by body region. We provide the first evidence that rapid color change permits a tetrapod to flexibly employ the most optimal camouflaging strategy by form (e.g., color matching vs. edge disruption) to minimize detection in the eyes of its predators.
... This capability could affect the predatory performance of octopuses, allowing them to track down a hidden prey, detecting their presence in dark burrows due to their bioluminescence [60,61]. The diffuse light sensing ability could have a significant role in their ability to change color to camouflage through background matching, guiding the highly specialized chromatic elements in their skin to display complex and rapidly changing color patterns at the peripheral level, without using the central nervous system, speeding up the response to environmental changes, as observed for other species [62][63][64][65][66]. Interestingly, the enlarged suckers found in the same area of the arm did not express a higher level of Ov-GRK1, these suckers, only found in males, probably have other specific roles. ...
In their foraging behavior octopuses rely on arm search movements outside the visual field of the eyes. In these movements the environment is explored primarily by the suckers that line the entire length of the octopus arm. In this study, for the first time, we report the complete characterization of a light-sensing molecule, Ov-GRK1, in the suckers, skin and retina of Octopus vulgaris. We sequenced the O. vulgaris GRK1 gene, defining a phylogenetic tree and performing a 3D structure model prediction. Furthermore, we found differences in relative mRNA expression in different sucker types at several arm levels, and localized it through in situ hybridization. Our findings suggest that the suckers in octopus arms are much more multimodal than was previously shown, adding the potential for light sensing to the already known mechanical and chemical sensing abilities.
... For decades, scientists in the field of cephalopod vision have focused on the goal of creating a complete characterization of the sophisticated coleoid body patterning abilities. As a result, existing reports are sufficient to describe and explain several known body patterns in cephalopods for camouflage and communication (Hanlon and Messenger, 1988;Hanlon, 2007;Langridge et al., 2007;Zylinski et al., 2009;How et al., 2017). Nevertheless, a theoretical framework on cephalopod body patterning, which does not include the dimension of time, will be inherently inadequate in modeling, holistically, the range of dynamic, rapid transformations observed in animals living in the wild. ...
The speed of adaptive body patterning in coleoid cephalopods is unmatched in the natural world. While the literature frequently reports their remarkable ability to change coloration significantly faster than other species, there is limited research on the temporal dynamics of rapid chromatophore coordination underlying body patterning in living, intact animals. In this exploratory pilot study, we aimed to measure chromatophore activity in response to a light flash stimulus in seven squid, Doryteuthis pealeii. We video-recorded the head/arms, mantle, and fin when squid were presented with a light flash startle stimulus. Individual chromatophores were detected and tracked over time using image analysis. We assessed baseline and response chromatophore surface area parameters before and after flash stimulation, respectively. Using change-point analysis, we identified 4,065 chromatophores from 185 trials with significant surface area changes elicited by the flash stimulus. We defined the temporal dynamics of chromatophore activity to flash stimulation as the latency, duration, and magnitude of surface area changes (expansion or retraction) following the flash presentation. Post stimulation, the response’s mean latency was at 50 ms (± 16.67 ms), for expansion and retraction, across all body regions. The response duration ranged from 217 ms (fin, retraction) to 384 ms (heads/arms, expansion). While chromatophore expansions had a mean surface area increase of 155.06%, the retractions only caused a mean reduction of 40.46%. Collectively, the methods and results described contribute to our understanding of how cephalopods can employ thousands of chromatophore organs in milliseconds to achieve rapid, dynamic body patterning.
... However, the octopus has always been described as a predominately "visual" animal with a complex visual system characterised by the presence of highly developed eyes [22,[79][80][81][82]. Analogously to vertebrate, octopus eyes are equipped with an un-inverted retina, a cornea, an iris, and a lens. ...
... In captivity, octopuses have shown preferences for selected preys [103][104][105], making their food choice by using their sophisticated sense organs. Among these, much attention has been given to vision [22,[79][80][81][82]. They also possess sensitive olfactory organs that they use to detect chemicals in the water [23,57,106,107]. ...
Octopus vulgaris possesses highly sophisticated sense organs, processed by the nervous system to generate appropriate behaviours such as finding food, avoiding predators, identifying conspecifics, and locating suitable habitat. Octopus uses multiple sensory modalities during the searching and selection of food, in particular, the chemosensory and visual cues. Here, we examined food choice in O. vulgaris in two ways: (1) We tested octopus’s food preference among three different kinds of food, and established anchovy as the preferred choice (66.67%, Friedman test p < 0.05); (2) We exposed octopus to a set of five behavioural experiments in order to establish the sensorial hierarchy in food choice, and to evaluate the performance based on the visual and chemical cues, alone or together. Our data show that O. vulgaris integrates sensory information from chemical and visual cues during food choice. Nevertheless, food choice resulted in being more dependent on chemical cues than visual ones (88.9%, Friedman test p < 0.05), with a consistent decrease of the time spent identifying the preferred food. These results define the role played by the senses with a sensorial hierarchy in food choice, opening new perspectives on the O. vulgaris’ predation strategies in the wild, which until today were considered to rely mainly on visual cues.
... They have been known for well-developed eyes, complex visual behavior and excellent color discrimination even with a single photoreceptor type [9,[14][15][16][17], for highly developed vestibular system, a 'lateral line analogue,' for a primitive 'hearing' system [18][19][20][21] and a discrete olfactory organ [22][23][24][25][26][27][28]. ...
... The best understood system here is the cuttlefish, because the changing appearance of its skin tells you directly how it perceives its background (Hanlon & Messenger, 2018). For example strong edges in its visual field will cause it to produce disruptive patterns with false relief, excellent camouflage on a stony background (Zylinski, Osorio & Shohet, 2009). How individual quail 'know' the pattern on the eggs they will lay, and accordingly select appropriate nest scrapes, is rather more mysterious (Lovell et al., 2013) and an example of the challenge facing vision scientists unlucky enough not to work on cephalopods. ...
Animal camouflage has long been used to illustrate the power of natural selection, and provides an excellent testbed for investigating the trade‐offs affecting the adaptive value of colour. However, the contemporary study of camouflage extends beyond evolutionary biology, co‐opting knowledge, theory and methods from sensory biology, perceptual and cognitive psychology, computational neuroscience and engineering. This is because camouflage is an adaptation to the perception and cognition of the species (one or more) from which concealment is sought. I review the different ways in which camouflage manipulates and deceives perceptual and cognitive mechanisms, identifying how, and where in the sequence of signal processing, strategies such as transparency, background matching, disruptive coloration, distraction marks, countershading and masquerade have their effects. As such, understanding how camouflage evolves and functions not only requires an understanding of animal sensation and cognition, it sheds light on perception in other species.
... More, several authors showed that both check size and achromatic contrast affected the body patterns. Other characteristics of the objects present in the vicinity of cuttlefish are taken into account by juveniles such as the presence of egdes, the spatial phase and the three dimensionality (Chiao et al., 2005;Zylinski et al., 2009;Ulmer et al., 2013). ...
Ette thèse est centrée sur les capacités sensorielles, cognitives et sur les effets du stress chez deux espèces de seiche : Sepia officinalis et Sepia pharaonis. Nous avons d’abord démontré que les embryons répondent à différents stimuli environnementaux (lumière, proies, prédateurs, encre de seiche) mettant en évidence que l'information sensorielle passe à travers la capsule de l'œuf, ce qui permet une continuité sensorielle transnatale. De telles réponses sont possibles puisque leur système chimiosensoriel et visuel sont fonctionnels avant l'éclosion. Nous avons également montré que les embryons des deux espèces sont capables d'apprentissage simple (empreinte alimentaire) et associatif (conditionnement classique) et que ces capacités précoces pourraient augmenter leurs chances de survie avant et après l'éclosion en permettant la reconnaissance des proies et des prédateurs. Enfin, nous avons montré que le stress embryonnaire naturel (odeur de prédateur) et artificiel (lumière) ont des effets modérés voire nuls sur les capacités d’apprentissage périnatal. Ces résultats comportementaux ont été observés sans grande différence entre les deux espèces qui vivent pourtant dans des environnements très éloignés. Pris ensemble, ces résultats démontrent que les embryons de seiche ne sont pas isolés de leur environnement mais détectent et traitent les informations environnementales qui modulent leur comportement après l’éclosion.
