Rapid Adaptive Camouflage in Cephalopods
Summary and Keywords
Visual camouflage change is a hallmark of octopus, squid, and cuttlefish and serves as their primary defense against predators. They can change their total body appearance in less than a second due to one principal feature: every aspect of this sensorimotor system is neurally refined for speed. Cephalopods live in visually complex environments such as coral reefs and kelp forests and use their visual perception of backgrounds to rapidly decide which camouflage pattern to deploy. Counterintuitively, cuttlefish have evolved a small number of pattern designs to achieve camouflage: Uniform, Mottle, and Disruptive, each with variation. The expression of these body patterns is based on several fundamental scene features. In cuttlefish, there appear to be several “visual assessment shortcuts” that enable camouflage patterning change in as little as 125 milliseconds. Neural control of the dynamic body patterning of cephalopods appears to be organized hierarchically via a set of lobes within the brain, including the optic lobes, the lateral basal lobes, and the anterior/posterior chromatophore lobes. The motor output of the central nervous system (CNS) in terms of the skin patterns that are produced is under sophisticated neural control of chromatophores, iridophores, and three-dimensional skin papillae. Moreover, arm postures and skin papillae are also regulated visually for additional aspects of concealment. This coloration system, often referred to as rapid neural polyphenism, is unique in the animal kingdom and can be explained and interpreted in the context of sensory and behavioral ecology.
Neural control of ultra-rapid changes in skin color and pattern is a hallmark of cephalopods. This system is highly refined for speed of change and for the diversity of body patterns that can change the appearance of the animal for a wide variety of signaling and camouflage. This is fundamentally a sensorimotor system in which the cephalopod (a) visually senses the background, (b) integrates this information, (c) decides on an appropriate camouflage pattern, and (d) activates thousands (sometimes millions) of chromatophores, iridophores, and three-dimensional skin papillae to produce the skin pattern. This skin pattern, when coordinated with the appropriate posture and behavior, collectively produces camouflage. In this article, some main features of this unique system are highlighted and some gaps in knowledge are pointed out to facilitate future research.
Rapid Neural Polyphenism
The diversity of body patterns used for camouflage can be appreciated by the very small sample of underwater images in Figure 1. The three most common types of near-shore shallow cephalopods are cuttlefish, octopus, and squid; all three groups have well-developed camouflage that is adapted to a wide range of habitats, including visually complex ones such as coral reefs and kelp forests. The appearance of any single cephalopod can change dramatically; that is, its apparent phenotype is dynamic and diverse, or polyphenic. Note that the cuttlefish in Figure 1A can look very different, as can the octopus in 1B and the squid in 1C. Even more polyphenism is produced for signaling and communication (summarized in Hanlon & Messenger, 2018).
Extensive field work and laboratory experimentation have revealed that, contrary to expectation, cuttlefish and other cephalopods appear to predominantly utilize three basic pattern designs (each with variation) to camouflage themselves on an extremely wide range of visual backgrounds: Uniform, Mottle, and Disruptive (UMD) (Figure 2). Uniform body patterns have little or no contrast; they can range from all light to all dark. Mottle body patterns are composed of small- to moderate-scale light and dark patches (or mottles) distributed across the body surface. There is low to moderate contrast between the light and dark patches, which can vary somewhat in shape and size, yet there is usually some repetition of those patches across the body surface. Disruptive body patterns are characterized by large-scale light and dark components of multiple shapes, orientations, scales, and contrasts (Chiao et al., 2010; Hanlon et al., 2007, 2009; Hanlon & Messenger, 1988).
There is some disagreement about how many camouflage patterns cephalopods have. Our work on the European cuttlefish, Sepia officinalis, indicates three pattern designs as Uniform, Mottle, and Disruptive. This evaluation is based on: (a) tens of thousands of photographs of this species in the lab and in the field, most of which can be qualitatively binned into three pattern groups; (b) the translation of photo images of the body pattern into graphs of contrast vs. granularity (explained in the section Cuttlefish Perception of Visual Backgrounds); and (c) the unparalleled speed of pattern change, which suggests some simplifying factors to enable swifter visual processing and decision-making. Some investigators think there is a continuum of camouflage patterns in cuttlefish and other cephalopods, but no current methods or data are yet available to sort out this basic question. Expansion of the granularity program (e.g., to include shape and orientation to the light and dark pattern components) to more precisely quantify pattern design would be an initial step in this direction. Comparative imagery and field data on other cephalopods are also needed to determine how widely the UMD scenario extends. In addition, more quantitative measurements over time are also needed to show that although many options are available, the animals still prefer to use only a few “inbuilt patterns.” There may be five or 10 basic pattern templates shown by other species, and it is worthwhile to remind ourselves that the definition of pattern then becomes important.
Speed of change is a prominent feature of this neural system and samples are illustrated in Figure 3. Some whole patterns are expressed more quickly than others: the squid in Figure 3A changes its Uniform pattern from dark to light in a third of a second. It is critical to understand that various components of patterns can be expressed more rapidly than the whole body pattern (which typically includes several components); these components were measured to be as fast as 125 milliseconds (ms). Figure 3B shows that specific skin papillae can be expressed in 770 ms, and this expression can be at any degree of expression. For the octopus, which generally has more complex skin, the change time for chromatophores and iridophores all over the body can take a bit more than a second (Figure 3C). It may be worth noting that these are observations, and that the animal when stressed by predators, or excited by conspecifics, could activate skin elements even more quickly.
Neurally Controlled Skin Pigments and Reflectors
Skin coloration results from chromatophore organs, iridophore cells, and leucophore cells. Each is in a different skin layer, generally with chromatophores shallowest, leucophores deepest, and iridophores in between. Chromatophores generally produce pigmentary coloration, whereas iridophores and leucophores produce structural (or reflective) coloration. Chromatophores operate with many muscles and nerves, iridophores have some nerves and no muscles, and leucophores have no muscles or nerves (and are thus “static”). The best overall review still remains that of Messenger (2001) and the interested reader should consult that treatise for many details of this system. Here some recent findings and selected gaps of knowledge are highlighted.
The chromatophore is a neuromuscular organ comprising five cell types: neurons, glial cells, radial muscles, sheath cells, and the large central chromatocyte that is filled with a flexible cytoelastic sac containing pigmented granules. Fundamentally, upon neural stimulation the radially arranged muscles contract and the punctate chromatocyte is rapidly pulled out into a flat disc of color (Figures 4A, B). The neuromechanics of this system are unstudied. When some chromatophores are stimulated and others are not, patterns are produced in the skin (Figure 4D). The details of synaptic connections are not fully characterized, although it seems that there are numerous connections all along the proximate portion of the muscles (Messenger, Cornwell, & Reed, 1997) to accommodate all the flexibility required in soft moving tissue and the enormous expansion of the pigment saccule.
The major excitatory neuromuscular transmitter is thought to be L-glutamate (Florey, Dubas, & Hanlon, 1985; Messenger et al., 1997), but is diversified postsynaptically by acting on multiple classes of glutamate receptors. For example, glutamate may act through both α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) and N-methyl-D-aspartate (NMDA) receptors to generate specific effects on chromatophore expansion (Lima, Nardi, & Brown, 2003; Mattiello, Fiore, Brown, d’Ischia, & Palumbo, 2010). Furthermore, in the cuttlefish Sepia officinalis, chromatophores are also expanded by FMRFamide-related peptides, generating prolonged chromatophore expansion (Loi, Saunders, Young, & Tublitz, 1996; Loi & Tublitz, 2000). Expanded chromatophores can be triggered to retract, with serotonin acting as an inhibitory neuromodulator (Florey, 1966; Florey & Kriebel, 1969; Messenger, 2001; Messenger et al., 1997; Rosen & Gilly, 2017). Together these neurotransmitter signaling systems have the potential to generate chromatophore activity over a range of timescales and play a central role in generating both acute and chronic body patterning for communication and camouflage. That said, there is still a great deal yet to be learned about localized excitation and inhibition, some of which is certainly species-specific (note: most of the work has been done only on a few loliginid squid species and on the cuttlefish Sepia officinalis).
A large gap in knowledge is the organization and functions of the peripheral nerve network. The radial muscles are very long and the chromatophores are densely packed, so that there is extensive overlap of nerves and muscles, as illustrated in Figure 4F. The synchrony of elaborate pigmentary dynamic displays such as the “passing cloud” may be orchestrated jointly by nerves and muscles but these mechanisms have not yet been sorted out (Froeschgaetzi & Froesch, 1977; Laan, Gutnick, Kuba, & Laurent, 2014; Messenger, 2001).
The radial muscles are innervated directly by motor neurons running directly from the chromatophore lobe in the brain without any synapses (Dubas, Hanlon, Ferguson, & Pinsker, 1986; Gaston & Tublitz, 2004). However, aspects of central control of chromatophores (as well as the dynamic variety of iridophores; see section Iridiphores) are poorly understood (Figure 2, bottom; Messenger, 2001). Intermediate motor centers—the lateral basal lobes—regulate the chromatophore lobes to some extent (Novicki, Budelmann, & Hanlon, 1990), and these in turn are regulated by the optic lobes (Messenger, 2001).
The optic lobes are large, complex structures, each taking up one-third of the total brain volume (Young, 1974). Despite their name, they have functions beyond visual processing. The central medulla is not only a visual memory store, but also a higher motor center in Octopus vulgaris and the cuttlefish Sepia officinalis (Boycott, 1961; Young, 1971, 1974). In Sepia officinalis, direct electrical stimulation in the medulla evoked various body patterns unilaterally or bilaterally, but stimulating the lateral basal lobes and chromatophore lobes only elicited a uniform darkening, either ipsilaterally or bilaterally (Boycott, 1961). In a recent study, the optic lobe was stimulated electrically to investigate the neural basis of body patterning in the oval squid Sepioteuthis lessoniana (Liu & Chiao, 2017). It was evident that most areas in the optic lobe mediated predominantly ipsilateral expansion of chromatophores present on the mantle but not on the head and arms. Furthermore, the expanded areas after electrical stimulation were correlated positively with an increase in stimulating voltage and stimulation depth. These findings suggest a unilaterally dominant and vertically converged organization of the optic lobe in this species. Furthermore, analyzing the elicited body pattern components and their corresponding stimulation sites revealed that the same components can be elicited by stimulating different parts of the optic lobe and that various subsets of these components can be co-activated by stimulating the same area. These results are difficult to explain but seem to imply that many body pattern components have multiple motor units in the optic lobe and these are organized in a mosaic manner. Clearly there is a need to expand these findings with more detailed neuroanatomy combined with electrophysiology, neuroimaging, and other techniques.
Most cephalopod iridophores are static. These cells have small plates (“platelets”) that reflect light via thin film interference when the viewing angle and incident light angle are in specific agreement; otherwise they are invisible. In loliginid squids (e.g., of the genus Loligo, Doryteuthis, Lolliguncula, and probably others) there are dynamic iridophores that can turn on/off as well as tune different colors that span the visible range. These iridophores have a peculiar neural arrangement: a cholinergic non-synaptic system driven by acetylcholine (ACh) (Cooper & Hanlon, 1986; Hanlon, Cooper, Budelmann, & Pappas, 1990). Iridophore reflectance change is caused by volume transmission (Zoli & Agnati, 1996) where en passant neural terminals release ACh at distances greater than a synaptic cleft and diffusion allows ACh to reach its targeted muscarinic receptors that line the “platelets.” The expression of iridescence is thus slower than the neuromuscular chromatophores; it is on the order of several to many seconds in vitro with bath application of ACh or in vitro neurophysiological preparations (Wardill, Gonzalez-Bellido, Crook, & Hanlon, 2012). Stimulation of iridescence nerves in the mantle turns on iridescence; continued stimulation delivers more ACh and this shifts the color of the iridophore from long to short wavelength (Figure 4C) as the “platelets” become thinner and the interplatelet distance increases. Practically nothing is known about central nervous system (CNS) control of iridescence. However, the origin or nature of the nerve cells that deliver the ACh to the iridophore has been recently revealed. Gonzalez-Bellido, Wardill, Buresch, Ulmer, and Hanlon (2014) determined that the peripheral wiring of iridophores is different from that of chromatophores insofar as the iridescence signals are routed through a peripheral center in the mantle called the stellate ganglion, and the iridescence motor neurons originate within this ganglion (Figure 4G). This suggests some aspect of peripheral control of iridescence. A good deal is known about the intracellular processes that control the reflectin proteins that reflect light after ACh is delivered to the cell (e.g., Izumi et al., 2010; Levenson, Bracken, Bush, & Morse, 2016). Yet the neural system that initiates and regulates this system of dynamic structural coloration remains enigmatic.
3D Skin Papillae
Dynamic control of physical skin texture is unique to cephalopods. Cuttlefish and octopus can make their skin flat or highly bumpy by expressing bumps called papillae (Figure 4E), which are muscular hydrostats that operate much like a tongue or an elephant trunk (Allen, Bell, Kuzirian, & Hanlon, 2013). Certain nerves control papillae extension while other nerves control retraction (Figure 4H), and the cell bodies of each reside in the stellate ganglion (Figure 4G), yet the functional significance of this is unknown (Gonzalez-Bellido, Scaros, Hanlon, & Wardill, 2018). Where in the CNS the skin papillae are controlled is not well understood. Expressed papillae greatly enhance camouflage (Figures 1A, B; 3C), whereas flat smooth skin makes swimming and jet escape more hydrodynamically efficient. Each papilla is a complex set of muscles, nerves, chromatophores, iridophores, and leucophores, and understanding how each one works in unison to provide both physical and optical appearance for effective camouflage remains a very large challenge.
Visual Perception that Guides Camouflage Choice
Cuttlefish Perception of Visual Backgrounds
Cuttlefish can camouflage themselves against almost any background, yet their ability to quickly alter their body patterns on different visual backgrounds poses a vexing challenge: how to pick the correct body pattern among their repertoire. The ability of cuttlefish to change appropriately requires a visual system that can rapidly assess complex visual scenes and produce the motor responses—the neurally controlled body patterns—that achieve camouflage.
Testing the visual cues that drive the adjustment of body patterning and posture is possible with cuttlefish because camouflage is their primary defense and they are behaviorally driven to camouflage themselves on almost any background (Hanlon & Messenger, 2018); thus both natural and artificial backgrounds can be presented to cuttlefish to observe their camouflaging response. The common European cuttlefish, Sepia officinalis, is particularly suited for this research because it adapts well to laboratory environments, and it ranges widely from the North Sea to equatorial Africa, including the Mediterranean, and thus must adapt to diverse visual backgrounds.
A behavioral, non-invasive sensorimotor assay to test rapid adaptive camouflage was introduced by Marshall and Messenger (1996) and developed in more detail by Chiao and Hanlon (2001a, 2001b). However, comprehensive studies of visual perception required more refined quantification of the motor output that resulted from the sensory input in this sensorimotor system. This is akin to a human visual psychophysical approach, where specifically designed visual stimuli are presented to assess the perceptual processes by quantifying the performance of a subject.
Various image statistics have been used to quantify the global properties of the body patterns produced by cuttlefish. Among them, a useful set of summary statistics can be obtained by taking the two-dimensional Fourier transform of the cuttlefish body pattern and extracting information reflecting the contribution of different spatial frequencies to the image of the body pattern (Barbosa et al., 2008b). In other words, these three pattern types differ in granularity (or spatial scale) and Fourier energy (or contrast). This method enables us to distinguish Uniform, Mottle, and Disruptive pattern types because each has a different curve shape (Figure 5A). Although cuttlefish are capable of producing hybrid patterns that combine features from the three basic patterns, this represents a parsimonious solution of producing diverse body patterns quickly in nature.
In cuttlefish, the Disruptive body pattern can be composed of 11 distinctive components (five light, six dark; Figure 6) or some limited combination of a few of the 11 components. While the global analysis of body patterns allows us to classify three basic pattern types in cuttlefish, this approach does not quantify the expression of individual skin components. Thus, some feature-based image analyses are required to characterize their expression. Using a manual grading scheme, researchers have scored the activation of individual light and dark components (Kelman, Osorio, & Baddeley, 2008; Mäthger, Barbosa, Miner, & Hanlon, 2006), which are independent physiological units that can be shown to operate singly or in combination with each other to form Disruptive body patterns (Hanlon & Messenger, 1988). By analyzing these manually scored component activations using the Principal Component Analysis (PCA), the dimensionality can be significantly reduced and the “strength” of body patterning can be derived (Kelman et al., 2008) That is, if most of the 11 disruptive components are shown, this is a “strong disruptive” pattern, and if only a few are shown, this is considered a “weak disruptive” pattern. Later, an automated method was developed to quantify the activation of various light and dark skin components responsible for disruptive body patterns in cuttlefish S. officinalis (Figure 5B) (Chiao, Chubb, Buresch, Siemann, & Hanlon, 2009).
Which properties of the background determine whether a cuttlefish will produce a Uniform, Mottle, or Disruptive pattern? This issue has received much attention over the past decade and is central to our understanding of visual perception mechanisms that regulate rapid adaptive camouflage in cuttlefish (see review: Chiao, Chubb, & Hanlon, 2015). The exceptionally fast change implies that the visual system must extract key background features efficiently for pattern selection and pattern generation.
Our earliest work using checkerboard backgrounds demonstrated that check sizes similar to the size of the white square (WS—a salient skin component on the cuttlefish mantle) evoke disruptive body patterns (Chiao & Hanlon, 2001a). In subsequent experiments, several researchers established that check sizes roughly 40–120% of WS area can also evoke disruptive body patterns, while smaller check sizes near 4–12% of WS area are likely to elicit mottle patterns, and larger check sizes around 400–1200% of WS area make most animals express uniform body patterns (Barbosa et al., 2007, 2008b; Kelman, Baddeley, Shohet, & Osorio, 2007; Kelman et al., 2008; Mäthger et al., 2006; Zylinski, Osorio, & Shohet, 2009a). Using random background textures differing in scale but identical in all other respects, body patterning of cuttlefish was further shown to be indeed scale-dependent (Chiao et al., 2009).
It is typically assumed that variations in the scene contrast are more important than the mean luminance of the scene in controlling cuttlefish body patterning. However, our results showed that with other factors equal, substrates with lower mean luminance tend to evoke stronger disruptive responses (Chiao, Chubb, & Hanlon, 2007). This background intensity effect is largely independent of the spatial scale of the substrate (Chiao et al., 2010). In other words, the darker substrate evoked a significantly larger disruptive response than the lighter substrate. Thus, low background intensity typically results in stronger disruptive patterns in cuttlefish.
Generally, the response patterns produced by a cuttlefish tend to resemble the contrast of the benthic background. However, other aspects of the animal’s pattern are likely to change as the contrast of a fixed-patterned background is manipulated. For example, when the contrasts of checkerboard backgrounds of different sizes were varied, on high-contrast checkerboards, cuttlefish body patterning depended on check size, whereas on low-contrast checkerboards—irrespective of check size—cuttlefish showed low-contrast uniform/stipple patterns (Barbosa et al., 2008b; Zylinski et al., 2009a). As substrate contrast increased, so did the contrast of the animals’ body patterns, until at high contrast, full expression of either mottle or disruptive patterns was observed (Chiao et al., 2010). One might expect such changes in body patterning with increasing background contrast because visual predators are highly sensitive to differences in contrast.
Effective camouflage for a benthic organism such as cuttlefish must deceive predators viewing from above as well as from the side; thus the choice of camouflage body pattern is expected to be sensitive to visible variations both in the ground plane (i.e., the horizontal substrate) and perpendicular to the ground plane (i.e., vertical aspects of the visual background). Most experiments have dealt only with the former. When high-contrast background patterns were presented on the walls of the test arena, cuttlefish also emitted disruptive body patterns (Barbosa, Litman, & Hanlon, 2008a). However, there were differences in the expression of disruptive pattern components if the checkerboard was presented simultaneously on the bottom and wall, or solely on the wall or the bottom. These results demonstrate that cuttlefish respond to visual background contrast variations both in the ground plane and perpendicular to the ground plane. This makes sense because, in their natural habitat, there are many vertical structures and benthic fish predators would be viewing cuttlefish laterally and the background for them would be vertical structures.
The edge of an object provides useful information for object identification, and the visual systems of many animals are highly sensitive to edges. Previous researchers have shown that cuttlefish body patterns are influenced strongly by visual edges in the substrate (Chiao, Kelman, & Hanlon, 2005; Zylinski, Osorio, & Shohet, 2009b). However, complete edges of objects are rare in cluttered visual environments. Instead, edge segments (lines and corners) are more abundant in complex backgrounds. In a follow-up study, how cuttlefish body patterning is differentially controlled by various aspects of edges was examined systematically (Chiao et al., 2013). Strikingly, it was found that high-contrast edge fragments (including abrupt points of termination) evoked substantially stronger body pattern responses than low-contrast edge fragments, whereas the body pattern responses evoked by high-contrast closed edges (i.e., circles without points of termination) were no stronger than those produced by low-contrast edges. This suggests that line terminators vs. continuous edges influence expression of disruptive body pattern components via different mechanisms that are controlled by contrast in different ways. Interestingly, a separate study showed that cuttlefish respond to circles fragmented by gaps differently than they do to randomly scattered circle fragments (Zylinski, Darmaillacq, & Shashar, 2012). This suggests that cuttlefish are sensitive to the co-linearity of the components in the circles fragmented by gaps.
The presence of white (or light) elements on the dark background is an important factor regulating a cuttlefish’s choice of body patterns. An almost entirely homogeneous dark background that contains even a single white element of roughly the same area as the WS of the cuttlefish will evoke a disruptive body pattern (Chiao & Hanlon, 2001a). This response to sparse white background elements is surprisingly invariant with respect to their shapes (Chiao & Hanlon, 2001b) or the size and age of the cuttlefish (Barbosa et al., 2007). In a subsequent study, however, it was found that although disks of both contrast polarities evoked relatively weak disruptive body patterns, black disks activated different skin components than white disks (Chiao et al., 2013). Thus, the patterning response is sensitive to the contrast polarity of the substrate; that is, the skin components activated by the substrate comprising black disks on a gray background tend to be dark, whereas those activated by white disks on a gray background tend to be light. In the most recent study, how cuttlefish camouflage patterns are influenced by the proportions of texture elements (texels) of different grayscales present in visually cluttered environments was investigated (Chubb et al., 2018). The main result is that darker-than-average texels (i.e., texels of negative contrast polarity) predominate in controlling cuttlefish’s disruptive body patterns. This finding may be explained by the fact that elements of negative contrast polarity are closely associated with the presence of edges produced by overlapping objects in the cuttlefish natural habitat, thus disruptive pattern responses are likely to achieve effective camouflage.
Visual depth (both real and pictorial depth) appears to be one key factor in evoking disruptive patterns (Kelman et al., 2008). The role of an isolated 3D object vs. a continuous background substrate in controlling the patterning responses produced by cuttlefish was thus assessed systematically (Buresch et al., 2011). The result showed that the 3D object exerted a strong influence on patterning responses only if the object was marked by a high-contrast pattern. In this case, cuttlefish showed a strong tendency to take their sensory cues from the pattern of the object. However, uniform gray objects exerted no measurable influence on responding. Thus, contrast of 3D objects is an important visual cue for masquerade (i.e., looking like another object rather than resembling the substrate). In a follow-up experiment, when a uniformly white smooth rock was presented, cuttlefish moved to the rock and deployed a uniform body pattern with mostly smooth skin; when a rock with small-scale fragments of contrasting shells was presented, the cuttlefish deployed mottled body patterns with strong papillae expression (Panetta, Buresch, & Hanlon, 2017). These robust and reversible responses further suggest that dynamic masquerade in cuttlefish relies on not only body pattern change but also 3D skin morphing. In a separate study, Zylinski, Osorio, and Johnsen (2016) showed that cuttlefish can perceive shape from shading and fine tune their WS component shading to render the appearance of surface curvature to a human observer, which might benefit camouflage in the presence of pebble-like objects. This fine-tuning of body patterning in response to pictorial depth cues and directional illumination suggests that cuttlefish are capable of using shading as a cue to 3D form by combining low-level information about light intensity with high-level knowledge about objects and the environment, an indication of sophisticated visual perception for camouflage.
In addition to regulation of 3D physical skin texture, cuttlefish can also enhance their camouflage via body posture. In an experiment, it was found that cuttlefish adjusted the orientation of their raised arms to align with the orientation of stripes on a wall (horizontal, 45, and 90 degrees), and when there were no stripes, the cuttlefish did not raise their arms at all (Barbosa, Allen, Mäthger, & Hanlon, 2012). This result corroborates our field observations of cuttlefish camouflage behavior in which flexible, precise arm posture is often tailored to match nearby objects.
How does a cuttlefish so quickly analyze the scene and put on an appropriate body pattern to conceal itself within a given background? Part of the answer lies in the counterintuitive finding that cuttlefish appear to have evolved only three basic pattern templates (Uniform, Mottle, Disruptive, each with variation) with which to achieve concealment (e.g., Hanlon, 2007). Thus, one working hypothesis is that the pattern deployed by a cuttlefish in response to a particular visual background reflects a two-stage process in which a relatively simple set of “visual sampling rules” is first used to select one of the three basic pattern types, which is then further refined in a second stage of processing that depends on subtler statistical features of the background. A somewhat comparable idea has been proposed by Zylinski et al. (2009a), in which a simple model focusing on cuttlefish edge detection is used to determine pattern types, then finer control of skin coloration is modulated by other substrate features. In any case, it is the remarkable speed of change (including orchestration of 2–3 million chromatophore organs in the skin) that suggests some sort of refined parsimonious visual sensing/perception process.
It is apparent that multiple visual features including spatial scale, background intensity, background contrast, object edges, object contrast polarity, object depth, presence of 3D objects, dark elements in the scene, and so forth are important cues for cuttlefish to achieve effective camouflage (Chiao et al., 2015; Hanlon, 2007; Hanlon et al., 2011; Zylinski et al., 2009a; Zylinski & Osorio, 2011). One can think of the eye as a sensor of diverse visual backgrounds, and cuttlefish acquire visual information by actively sensing surrounding environments with vertebrate-like eyes (Messenger, 1991; Packard, 1972). Significant visual processing that extracts multiple visual features of substrates occurs in the optic lobe, the largest brain area in cephalopods. The parallel nature of this visual information processing is somewhat akin to human vision (Zylinski & Osorio, 2011). However, little is known about feature integration in the cuttlefish brain and the resultant motor act that produces the body pattern for camouflage. Although using the psychophysical approach to examine the relationship between sensory input (visual environments) and motor output (body patterns) has generated fruitful results in past decades, the neural pathway and connection for higher-level visual processing (e.g., objection recognition) are difficult to assess in cuttlefish. Zylinski and Osorio (2011) proposed, like primate visual processing, that cuttlefish may start from an image-based processing in which low-level cues (contrast, scale, edge, etc.) are extracted to determine the boundary of an object, then a viewer-based processing is implemented and intermediate-level cues (depth, objects, texture, etc.) are used to understand the nature of the visual environment. Exactly how this visual processing scheme is rendered to achieve camouflage in cuttlefish remains to be determined. The entire process (minus papillae and arm postures) is summarized in Figure 6, which illustrates our current representation of visual perception and motor control mechanisms that regulate rapid adaptive camouflage in the cuttlefish S. officinalis.
Color Blind Camouflage?
Many visual predators have keen color perception, and thus camouflage patterns should provide some degree of color matching in addition to other visual factors such as pattern, contrast, and texture. However, most cephalopods, including the cuttlefish, appear to lack color perception. There are two lines of evidence supporting cuttlefish color blindness. (a) Visual pigment: by measuring spectral absorption of retinal extracts, Brown and Brown (1958) reported that cuttlefish S. officinalis have only one visual pigment with a maximal absorption (λmax) at 492 nanometer (nm). Studying the rhodopsin gene of cuttlefish further suggested that only a single type of rhodopsin is expressed in S. officinalis, and the predicted λmax of spectral sensitivity is also 492 nm based on the amino acid composition (Bellingham, Morris, & Hunt, 1998). (b) Behavioral response: by presenting gravel substrates of varying colors including red, white, blue, and yellow, and observing cuttlefish body pattern responses, Marshall and Messenger (1996) reported that cuttlefish S. officinalis produced a bold coarse mottled pattern when placed on red and white gravel, presumably in an attempt to “match” the coarse patterning of the gravel, whereas the animals showed an overall uniform pattern on blue and yellow gravel, suggesting that these shades appeared not as two contrasting colors but instead as a uniformly colored gravel background. A similar approach with varying color contrast of checkerboard backgrounds reconfirmed that cuttlefish S. officinalis are indeed color blind (Mäthger et al., 2006). Interestingly, a recent theoretical study proposed an alternative mechanism of achieving color vision with only a single type of photoreceptor in cuttlefish, in which an off-axis pupil and the principle of chromatic aberration are combined to provide color blind cephalopods with a way to distinguish colors (Stubbs & Stubbs, 2016). However, although cuttlefish have a W-shaped pupil, the function of this peculiar pupil is mainly for balancing a vertically uneven light field and improving image contrast for the dimmer parts of the scene (Mäthger, Hanlon, Hakansson, & Nilsson, 2013). Thus, the color vision mechanism in cuttlefish, if it exists, remains elusive.
While cuttlefish are apparently color blind, they seem to have the ability to color match and/or brightness match with surrounding substrates, although this has not yet been studied quantitatively with underwater photographs and color standards; nor has it been done when matching such images to the color sensitivity of different marine predators. Hyperspectral imaging technology is being developed to test this in the near future (Chiao, Wickiser, Allen, Genter, & Hanlon, 2011).
A previous study has provided molecular evidence for distributed light sensing in the skin of cuttlefish S. officinalis, in which they showed that opsin transcripts are expressed in the fin and ventral skin, but the amino acid sequence of the opsin polypeptide found in these extraocular tissues is identical or very similar to the one identified in the retina (Mäthger, Roberts, & Hanlon, 2010). Although this result suggests that color discrimination by the skin opsins is unlikely due to the presence of only one type of opsin, this finding does provide a possible peripheral mechanism of light sensing and subsequent skin patterning through other skin structures (chromatophores and iridophores) that may assist color and brightness match. Further studies confirmed that dermal photoreception exists in cephalopods by showing that visual phototransduction components, including rhodopsin, retinochrome, and Gqα proteins, are all detectable in the chromatophore skin layer and other tissues of squid and cuttlefish (Kingston, Kuzirian, Hanlon, & Cronin, 2015a; Kingston, Wardill, Hanlon, & Cronin, 2015b), and light (particularly blue light) can cause chromatophore expansion in a very specific skin patch on the funnel of Octopus bimaculoides (Ramirez & Oakley, 2015). These observations suggest that cephalopod skin can be intrinsically light sensitive, though the evidence is weak and more detailed research is required to show dermal light sensitivity and its possible functions. Nevertheless, this eye-independent light sensing potential may contribute to their unique and novel patterning abilities for camouflage.
Motion tends to give away camouflage, so cephalopods have evolved some behavioral and body patterning tactics to reduce the chance of detection or recognition while they move. Motion camouflage is defined as “movement in a fashion that decreases the probability of movement detection” (Stevens & Merilaita, 2009). Hanlon, Forsythe, and Joneschild (1999) showed how Octopus cyanea on a Tahitian coral reef could move with stealth across open areas; they tended to match their crawling speed to the speed of sun-dappled wave shadows so that their motion roughly equaled that of the surrounding light flicker. Figure 7 illustrates the same tactic observed in Octopus vulgaris on Caribbean coral reefs (Hanlon & Messenger, 2018). This involves a rather sophisticated combination of deploying a specific body pattern and posture and combining it with the appropriate locomotor behavior. Visual perception is a key component of this maneuver because an octopus will view the surrounding background, assess the shape and size and patterning of objects that are present in the vicinity, and choose its own body shape, pattern, and posture to generally resemble nearby objects, thus achieving the camouflage tactic of masquerade (i.e., looking like an object that is not of interest to a predator). Slow stealth movement across open areas are key to this behavior, and overall this represents a defense tactic that requires substantial cognitive capability.
Laboratory experiments to decipher visual mechanisms that guide motion camouflage have been performed only on cuttlefish, and no clear solutions have been determined. Shohet, Baddeley, Anderson, Kelman, and Osorio (2006) found that Sepia officinalis in the laboratory oriented their body orthogonally to benthic stripes and speculated that this may be a physical response to water flow rather than a visual effect to implement motion camouflage, but no obvious function was elucidated. Zylinski et al. (2009b) also tried to sort out some correlates of body patterning behavior and motion in lab trials, but again no clear picture emerged to explain how predators might be deceived visually when the cuttlefish is moving. Interestingly, Josef et al. (2017) found that substrate patch size is an important factor to affect cuttlefish camouflage during movement. Specifically, they showed that the minimal size of an object for eliciting intensity matching response while moving in cuttlefish is about the animal length. However, there is no functional study to verify the effect of changing body pattern on motion camouflage. Clearly much is yet to be learned about the visual perception mechanisms of octopus and cuttlefish that enable them to forage daily and still remain somewhat less detectable or recognizable even when moving.
Challenges and Future Directions
While rapid neural polyphenism in cephalopods probably did not evolve first for camouflage, the speed of skin color change does give animals tremendous flexibility and adapting power to camouflage on almost any background. The dynamic body pattern, such as the wave-like patterning (or “passing clouds”) shown on some cuttlefish species, adds another layer of complexity for motion camouflage (Hanlon & Messenger, 2018). The neural mechanism of generating the dynamic passing cloud skin pattern is largely unknown. One study suggests that these dynamic pigmentation patterns result from the coordinated activation of large chromatophore arrays, with the centrally controlled wave propagation mechanism (Laan et al., 2014). Future experiments with electrophysiology should directly examine the neural control of rapid neural polyphenism by recording the target neurons in the brain and figure out the neural connection underlying dynamic body pattern generation.
Unfortunately, electrophysiological recording from the intact brain of cephalopods is notoriously difficult. Bullock (1984) was the first to record ongoing compound field potentials from octopus brain, and found that they are labile and vertebrate-like. Later, Bullock and Budelmann (1991) developed a preparation to record sensory evoked potentials in unanesthetized and unrestrained cuttlefish Sepia officinalis, and showed that event-related neural activity is evident in several brain regions. Despite these early attempts, single unit recording in the central brain from these soft-bodied animals has not been accomplished, and this technical obstacle prevents us from systematically characterizing neural responses at specific brain areas and examining the functional connections responsible for camouflage body patterning. An alternative approach by tracking the states of tens of thousands of chromatophores at 60 frames per second and at single-cell resolution in cuttlefish Sepia officinalis has recently been developed to allow scientists to infer brain activity and perceptual behavior in freely moving animals (Reiter et al., 2018). This unprecedented high-resolution imaging of individual chromatophores could potentially reveal the underlying neural control of camouflage body pattern dynamic in cephalopods. In addition, optogenetic and neural imaging tools that have revolutionized neuroscience in past decades may also be applied in studying the neural basis of camouflage behavior in cephalopods in the future.
Color blind camouflage is perhaps the most perplexing question in cephalopod behavior, or indeed sensory biology in general. Although the theoretical study of Stubbs and Stubbs (2016) suggests that an off-axis pupil and the principle of chromatic aberration can potentially provide color blind cephalopods with a way to distinguish colors, all behavioral evidence suggests otherwise (Marshall & Messenger, 1996; Mäthger et al., 2006). However, most studies focus on only a few cephalopod species (e.g., cuttlefish Sepia officinalis and octopus Octopus vulgaris), but there are many other shallow-water and coral-dwelling species (e.g., cuttlefish Sepia latimanus and octopus Octopus rubescens) that have been documented in video footage showing extraordinarily fast body color change depending on the surrounding environment. Thus, future research should examine more cephalopod species, especially those living in colorful and complex environments, with a more naturalistic setting and experimental design, to systematically probe their color perception and body coloration. More importantly, it will be critical to elucidate the role of extraocular light sensing capability found in octopus (Ramirez & Oakley, 2015) and the expression of visual pigment found in squid and cuttlefish (Kingston et al., 2015a; Mäthger et al., 2010) in aiding camouflage body patterning. Using genomics approach, future studies may examine whether there are multiple opsin genes in the genome of a given cephalopod species (a prerequisite for color vision) and whether they are expressed in ocular or extraocular locations (visual or peripheral sensing). If cephalopods are indeed visually color blind, how can the light sensitivity on their skin contribute to the apparent body coloration change in color blind camouflage?
Although cephalopod camouflage is one of the most fascinating topics in biology and has been studied extensively by us and others in the past two decades, the neural mechanism underlying extremely diverse and dynamic body patterns shown on various species and in different habitats still remains largely unknown, particularly in the central brain where the visual information is integrated and motor control is executed. On the other hand, even though our image analysis and pattern classification tend to group cephalopod body patterns into three categories, namely Uniform, Mottle, and Disruptive (Hanlon, 2007; Hanlon et al., 2009), how these body colorations are viewed by predators and whether these body patterns defeat the predator visual system equally have not been functionally tested and behaviorally validated against their natural predators. Using hyperspectral imaging systems with higher spatiotemporal and chromatic resolutions, future research may start to look into camouflaged cephalopods in the eyes of the beholder and reveal the functionality of camouflage body patterns through the interaction between prey and predator.
This introduces a key point: field studies of naturally behaving cephalopods are essential in understanding the sensory ecology of rapid adaptive camouflage. Only in those situations can researchers be confident that the cephalopod is receiving the full range of natural light and animal stimulation. Moreover, in an ecosystem replete with predators and prey as well as a wide range of visual microhabitats, the full range of sensory stimuli can be experienced in a single forage. It is a marvel to observe an octopus foraging for several hours throughout multiple habitats on an Indo-Pacific coral reef and making dozens of decisions about which patterns and behaviors to execute to remain undetectable or unrecognizable to visual predators (Forsythe & Hanlon, 1997; Hanlon et al., 1999). Documenting these behaviors with video and light measuring devices enables quantification of rapid polyphenism and how it relates to visual microhabitats in the eye of the beholder (mainly teleost fishes, many of which have highly capable vision). In parallel, specifically designed laboratory behavioral experiments with either live animals or animated ones should be carried out to test the efficacy of various body patterns against different predators. With the newly developed display technology and behavioral paradigm, some of these important issues could be addressed properly in the future.
We thank many colleagues for discussion and research on these subjects but especially Charlie Chubb, Paloma Gonzalez-Bellido, and Trevor Wardill. We are very grateful for funding from AFOSR grant FA9550-14-1-0134, ARO grant # W911NF-16-1-0542, ONR grant N000141712480, and MOST grant 106-2311-B-007-010-MY3, as well as the Sholley Foundation. We acknowledge Olivia Cattau for assistance with Figure 3; Trevor Wardill and Paloma Gonzalez-Bellido for Figures 4C, G, and H; Steve Senft for Figure 4F; and Basia Goschynscka for the drawings in Figure 7.
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